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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Molecular and Translational Classifications of DAMPs in Immunogenic Cell Death</title><author><name sortKey="Garg, Abhishek D" sort="Garg, Abhishek D" uniqKey="Garg A" first="Abhishek D." last="Garg">Abhishek D. Garg</name><affiliation><nlm:aff id="aff1"><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Galluzzi, Lorenzo" sort="Galluzzi, Lorenzo" uniqKey="Galluzzi L" first="Lorenzo" last="Galluzzi">Lorenzo Galluzzi</name><affiliation><nlm:aff id="aff2"><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff6"><institution>Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Apetoh, Lionel" sort="Apetoh, Lionel" uniqKey="Apetoh L" first="Lionel" last="Apetoh">Lionel Apetoh</name><affiliation><nlm:aff id="aff7"><institution>U866, INSERM</institution>,<addr-line>Dijon</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff8"><institution>Faculté de Médecine, Université de Bourgogne</institution>,<addr-line>Dijon</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff9"><institution>Centre Georges François Leclerc</institution>,<addr-line>Dijon</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Baert, Thais" sort="Baert, Thais" uniqKey="Baert T" first="Thais" last="Baert">Thais Baert</name><affiliation><nlm:aff id="aff10"><institution>Department of Gynaecology and Obstetrics, UZ Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff11"><institution>Laboratory of Gynaecologic Oncology, Department of Oncology, Leuven Cancer Institute, KU Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Birge, Raymond B" sort="Birge, Raymond B" uniqKey="Birge R" first="Raymond B." last="Birge">Raymond B. Birge</name><affiliation><nlm:aff id="aff12"><institution>Department of Microbiology, Biochemistry, and Molecular Genetics, University Hospital Cancer Center, Rutgers Cancer Institute of New Jersey, New Jersey Medical School</institution>,<addr-line>Newark, NJ</addr-line>,<country>USA</country></nlm:aff></affiliation></author><author><name sortKey="Bravo San Pedro, Jose Manuel" sort="Bravo San Pedro, Jose Manuel" uniqKey="Bravo San Pedro J" first="José Manuel" last="Bravo-San Pedro">José Manuel Bravo-San Pedro</name><affiliation><nlm:aff id="aff2"><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff6"><institution>Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Breckpot, Karine" sort="Breckpot, Karine" uniqKey="Breckpot K" first="Karine" last="Breckpot">Karine Breckpot</name><affiliation><nlm:aff id="aff13"><institution>Laboratory of Molecular and Cellular Therapy, Vrije Universiteit Brussel</institution>,<addr-line>Jette</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Brough, David" sort="Brough, David" uniqKey="Brough D" first="David" last="Brough">David Brough</name><affiliation><nlm:aff id="aff14"><institution>Faculty of Life Sciences, University of Manchester</institution>,<addr-line>Manchester</addr-line>,<country>UK</country></nlm:aff></affiliation></author><author><name sortKey="Chaurio, Ricardo" sort="Chaurio, Ricardo" uniqKey="Chaurio R" first="Ricardo" last="Chaurio">Ricardo Chaurio</name><affiliation><nlm:aff id="aff15"><institution>Department of Internal Medicine 3 – Rheumatology and Immunology, Friedrich-Alexander-University Erlangen-Nurnberg</institution>,<addr-line>Erlangen</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Cirone, Mara" sort="Cirone, Mara" uniqKey="Cirone M" first="Mara" last="Cirone">Mara Cirone</name><affiliation><nlm:aff id="aff16"><institution>Department of Experimental Medicine, Sapienza University of Rome</institution>,<addr-line>Rome</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Coosemans, An" sort="Coosemans, An" uniqKey="Coosemans A" first="An" last="Coosemans">An Coosemans</name><affiliation><nlm:aff id="aff10"><institution>Department of Gynaecology and Obstetrics, UZ Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff11"><institution>Laboratory of Gynaecologic Oncology, Department of Oncology, Leuven Cancer Institute, KU Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Coulie, Pierre G" sort="Coulie, Pierre G" uniqKey="Coulie P" first="Pierre G." last="Coulie">Pierre G. Coulie</name><affiliation><nlm:aff id="aff17"><institution>de Duve Institute, Université Catholique de Louvain</institution>,<addr-line>Brussels</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="De Ruysscher, Dirk" sort="De Ruysscher, Dirk" uniqKey="De Ruysscher D" first="Dirk" last="De Ruysscher">Dirk De Ruysscher</name><affiliation><nlm:aff id="aff18"><institution>Department of Radiation Oncology, University Hospitals Leuven, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Dini, Luciana" sort="Dini, Luciana" uniqKey="Dini L" first="Luciana" last="Dini">Luciana Dini</name><affiliation><nlm:aff id="aff19"><institution>Department of Biological and Environmental Science and Technology, University of Salento</institution>,<addr-line>Salento</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="De Witte, Peter" sort="De Witte, Peter" uniqKey="De Witte P" first="Peter" last="De Witte">Peter De Witte</name><affiliation><nlm:aff id="aff20"><institution>Laboratory for Molecular Biodiscovery, Department of Pharmaceutical and Pharmacological Sciences, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Dudek Peric, Aleksandra M" sort="Dudek Peric, Aleksandra M" uniqKey="Dudek Peric A" first="Aleksandra M." last="Dudek-Peric">Aleksandra M. Dudek-Peric</name><affiliation><nlm:aff id="aff1"><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Faggioni, Alberto" sort="Faggioni, Alberto" uniqKey="Faggioni A" first="Alberto" last="Faggioni">Alberto Faggioni</name><affiliation><nlm:aff id="aff21"><institution>Sapienza University of Rome</institution>,<addr-line>Rome</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Fucikova, Jitka" sort="Fucikova, Jitka" uniqKey="Fucikova J" first="Jitka" last="Fucikova">Jitka Fucikova</name><affiliation><nlm:aff id="aff22"><institution>SOTIO</institution>,<addr-line>Prague</addr-line>,<country>Czech Republic</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff23"><institution>Department of Immunology, 2nd Faculty of Medicine, University Hospital Motol, Charles University</institution>,<addr-line>Prague</addr-line>,<country>Czech Republic</country></nlm:aff></affiliation></author><author><name sortKey="Gaipl, Udo S" sort="Gaipl, Udo S" uniqKey="Gaipl U" first="Udo S." last="Gaipl">Udo S. Gaipl</name><affiliation><nlm:aff id="aff24"><institution>Department of Radiation Oncology, Universitätsklinikum Erlangen</institution>,<addr-line>Erlangen</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Golab, Jakub" sort="Golab, Jakub" uniqKey="Golab J" first="Jakub" last="Golab">Jakub Golab</name><affiliation><nlm:aff id="aff25"><institution>Department of Immunology, Medical University of Warsaw</institution>,<addr-line>Warsaw</addr-line>,<country>Poland</country></nlm:aff></affiliation></author><author><name sortKey="Gougeon, Marie Lise" sort="Gougeon, Marie Lise" uniqKey="Gougeon M" first="Marie-Lise" last="Gougeon">Marie-Lise Gougeon</name><affiliation><nlm:aff id="aff26"><institution>Biotherapy and Vaccine Unit, Institut Pasteur</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Hamblin, Michael R" sort="Hamblin, Michael R" uniqKey="Hamblin M" first="Michael R." last="Hamblin">Michael R. Hamblin</name><affiliation><nlm:aff id="aff27"><institution>Wellman Center for Photomedicine, Massachusetts General Hospital</institution>,<addr-line>Boston, MA</addr-line>,<country>USA</country></nlm:aff></affiliation></author><author><name sortKey="Hemminki, Akseli" sort="Hemminki, Akseli" uniqKey="Hemminki A" first="Akseli" last="Hemminki">Akseli Hemminki</name><affiliation><nlm:aff id="aff28"><institution>Cancer Gene Therapy Group, Transplantation Laboratory, Haartman Institute, University of Helsinki</institution>,<addr-line>Helsinki</addr-line>,<country>Finland</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff29"><institution>Helsinki University Hospital Comprehensive Cancer Center</institution>,<addr-line>Helsinki</addr-line>,<country>Finland</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff30"><institution>TILT Biotherapeutics Ltd.</institution>,<addr-line>Helsinki</addr-line>,<country>Finland</country></nlm:aff></affiliation></author><author><name sortKey="Herrmann, Martin" sort="Herrmann, Martin" uniqKey="Herrmann M" first="Martin" last="Herrmann">Martin Herrmann</name><affiliation><nlm:aff id="aff15"><institution>Department of Internal Medicine 3 – Rheumatology and Immunology, Friedrich-Alexander-University Erlangen-Nurnberg</institution>,<addr-line>Erlangen</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Hodge, James W" sort="Hodge, James W" uniqKey="Hodge J" first="James W." last="Hodge">James W. Hodge</name><affiliation><nlm:aff id="aff31"><institution>Recombinant Vaccine Group, Laboratory of Tumor Immunology and Biology, National Cancer Institute, National Institutes of Health</institution>,<addr-line>Bethesda, MD</addr-line>,<country>USA</country></nlm:aff></affiliation></author><author><name sortKey="Kepp, Oliver" sort="Kepp, Oliver" uniqKey="Kepp O" first="Oliver" last="Kepp">Oliver Kepp</name><affiliation><nlm:aff id="aff2"><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff32"><institution>Metabolomics and Cell Biology Platforms, Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Kroemer, Guido" sort="Kroemer, Guido" uniqKey="Kroemer G" first="Guido" last="Kroemer">Guido Kroemer</name><affiliation><nlm:aff id="aff2"><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff32"><institution>Metabolomics and Cell Biology Platforms, Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff33"><institution>Pôle de Biologie, Hôpital Européen Georges Pompidou, AP-HP</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff34"><institution>Department of Women’s and Children’s Health, Karolinska University Hospital</institution>,<addr-line>Stockholm</addr-line>,<country>Sweden</country></nlm:aff></affiliation></author><author><name sortKey="Krysko, Dmitri V" sort="Krysko, Dmitri V" uniqKey="Krysko D" first="Dmitri V." last="Krysko">Dmitri V. Krysko</name><affiliation><nlm:aff id="aff35"><institution>Molecular Signaling and Cell Death Unit, Inflammation Research Center, VIB</institution>,<addr-line>Ghent</addr-line>,<country>Belgium</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff36"><institution>Department of Biomedical Molecular Biology, Ghent University</institution>,<addr-line>Ghent</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Land, Walter G" sort="Land, Walter G" uniqKey="Land W" first="Walter G." last="Land">Walter G. Land</name><affiliation><nlm:aff id="aff37"><institution>Molecular ImmunoRheumatology, INSERM UMRS1109, Laboratory of Excellence Transplantex, University of Strasbourg</institution>,<addr-line>Strasbourg</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Madeo, Frank" sort="Madeo, Frank" uniqKey="Madeo F" first="Frank" last="Madeo">Frank Madeo</name><affiliation><nlm:aff id="aff38"><institution>Institute of Molecular Biosciences, NAWI Graz, University of Graz</institution>,<addr-line>Graz</addr-line>,<country>Austria</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff39"><institution>BioTechMed Graz</institution>,<addr-line>Graz</addr-line>,<country>Austria</country></nlm:aff></affiliation></author><author><name sortKey="Manfredi, Angelo A" sort="Manfredi, Angelo A" uniqKey="Manfredi A" first="Angelo A." last="Manfredi">Angelo A. Manfredi</name><affiliation><nlm:aff id="aff40"><institution>IRRCS Istituto Scientifico San Raffaele, Università Vita-Salute San Raffaele</institution>,<addr-line>Milan</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Mattarollo, Stephen R" sort="Mattarollo, Stephen R" uniqKey="Mattarollo S" first="Stephen R." last="Mattarollo">Stephen R. Mattarollo</name><affiliation><nlm:aff id="aff41"><institution>Translational Research Institute, University of Queensland Diamantina Institute, University of Queensland</institution>,<addr-line>Wooloongabba, QLD</addr-line>,<country>Australia</country></nlm:aff></affiliation></author><author><name sortKey="Maueroder, Christian" sort="Maueroder, Christian" uniqKey="Maueroder C" first="Christian" last="Maueroder">Christian Maueroder</name><affiliation><nlm:aff id="aff15"><institution>Department of Internal Medicine 3 – Rheumatology and Immunology, Friedrich-Alexander-University Erlangen-Nurnberg</institution>,<addr-line>Erlangen</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Merendino, Nicol" sort="Merendino, Nicol" uniqKey="Merendino N" first="Nicol" last="Merendino">Nicol Merendino</name><affiliation><nlm:aff id="aff42"><institution>Laboratory of Cellular and Molecular Nutrition, Department of Ecological and Biological Sciences, Tuscia University</institution>,<addr-line>Viterbo</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Multhoff, Gabriele" sort="Multhoff, Gabriele" uniqKey="Multhoff G" first="Gabriele" last="Multhoff">Gabriele Multhoff</name><affiliation><nlm:aff id="aff43"><institution>Department of Radiation Oncology, Klinikum rechts der Isar, Technische Universität München</institution>,<addr-line>Munich</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Pabst, Thomas" sort="Pabst, Thomas" uniqKey="Pabst T" first="Thomas" last="Pabst">Thomas Pabst</name><affiliation><nlm:aff id="aff44"><institution>Department of Medical Oncology, University Hospital</institution>,<addr-line>Bern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Ricci, Jean Ehrland" sort="Ricci, Jean Ehrland" uniqKey="Ricci J" first="Jean-Ehrland" last="Ricci">Jean-Ehrland Ricci</name><affiliation><nlm:aff id="aff45"><institution>INSERM, U1065, Université de Nice-Sophia-Antipolis, Centre Méditerranéen de Médecine Moléculaire (C3M), Équipe “Contrôle Métabolique des Morts Cellulaires”</institution>,<addr-line>Nice</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Riganti, Chiara" sort="Riganti, Chiara" uniqKey="Riganti C" first="Chiara" last="Riganti">Chiara Riganti</name><affiliation><nlm:aff id="aff46"><institution>Department of Oncology, University of Turin</institution>,<addr-line>Turin</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Romano, Erminia" sort="Romano, Erminia" uniqKey="Romano E" first="Erminia" last="Romano">Erminia Romano</name><affiliation><nlm:aff id="aff1"><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Rufo, Nicole" sort="Rufo, Nicole" uniqKey="Rufo N" first="Nicole" last="Rufo">Nicole Rufo</name><affiliation><nlm:aff id="aff1"><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Smyth, Mark J" sort="Smyth, Mark J" uniqKey="Smyth M" first="Mark J." last="Smyth">Mark J. Smyth</name><affiliation><nlm:aff id="aff47"><institution>Immunology in Cancer and Infection Laboratory, QIMR Berghofer Medical Research Insitute</institution>,<addr-line>Herston, QLD</addr-line>,<country>Australia</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff48"><institution>School of Medicine, University of Queensland</institution>,<addr-line>Herston, QLD</addr-line>,<country>Australia</country></nlm:aff></affiliation></author><author><name sortKey="Sonnemann, Jurgen" sort="Sonnemann, Jurgen" uniqKey="Sonnemann J" first="Jürgen" last="Sonnemann">Jürgen Sonnemann</name><affiliation><nlm:aff id="aff49"><institution>Department of Paediatric Haematology and Oncology, Children’s Clinic, Jena University Hospital</institution>,<addr-line>Jena</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Spisek, Radek" sort="Spisek, Radek" uniqKey="Spisek R" first="Radek" last="Spisek">Radek Spisek</name><affiliation><nlm:aff id="aff22"><institution>SOTIO</institution>,<addr-line>Prague</addr-line>,<country>Czech Republic</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff23"><institution>Department of Immunology, 2nd Faculty of Medicine, University Hospital Motol, Charles University</institution>,<addr-line>Prague</addr-line>,<country>Czech Republic</country></nlm:aff></affiliation></author><author><name sortKey="Stagg, John" sort="Stagg, John" uniqKey="Stagg J" first="John" last="Stagg">John Stagg</name><affiliation><nlm:aff id="aff50"><institution>Centre de Recherche du Centre Hospitalier de l’Université de Montréal, Institut du Cancer de Montréal, Faculté de Pharmacie, Université de Montréal</institution>,<addr-line>Montreal, QC</addr-line>,<country>Canada</country></nlm:aff></affiliation></author><author><name sortKey="Vacchelli, Erika" sort="Vacchelli, Erika" uniqKey="Vacchelli E" first="Erika" last="Vacchelli">Erika Vacchelli</name><affiliation><nlm:aff id="aff2"><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff6"><institution>Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Vandenabeele, Peter" sort="Vandenabeele, Peter" uniqKey="Vandenabeele P" first="Peter" last="Vandenabeele">Peter Vandenabeele</name><affiliation><nlm:aff id="aff35"><institution>Molecular Signaling and Cell Death Unit, Inflammation Research Center, VIB</institution>,<addr-line>Ghent</addr-line>,<country>Belgium</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff36"><institution>Department of Biomedical Molecular Biology, Ghent University</institution>,<addr-line>Ghent</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Vandenberk, Lien" sort="Vandenberk, Lien" uniqKey="Vandenberk L" first="Lien" last="Vandenberk">Lien Vandenberk</name><affiliation><nlm:aff id="aff51"><institution>Laboratory of Pediatric Immunology, Department of Microbiology and Immunology, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Van Den Eynde, Benoit J" sort="Van Den Eynde, Benoit J" uniqKey="Van Den Eynde B" first="Benoit J." last="Van Den Eynde">Benoit J. Van Den Eynde</name><affiliation><nlm:aff id="aff52"><institution>Ludwig Institute for Cancer Research, de Duve Institute, Université Catholique de Louvain</institution>,<addr-line>Brussels</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Van Gool, Stefaan" sort="Van Gool, Stefaan" uniqKey="Van Gool S" first="Stefaan" last="Van Gool">Stefaan Van Gool</name><affiliation><nlm:aff id="aff51"><institution>Laboratory of Pediatric Immunology, Department of Microbiology and Immunology, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Velotti, Francesca" sort="Velotti, Francesca" uniqKey="Velotti F" first="Francesca" last="Velotti">Francesca Velotti</name><affiliation><nlm:aff id="aff53"><institution>Department of Ecological and Biological Sciences, Tuscia University</institution>,<addr-line>Viterbo</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Zitvogel, Laurence" sort="Zitvogel, Laurence" uniqKey="Zitvogel L" first="Laurence" last="Zitvogel">Laurence Zitvogel</name><affiliation><nlm:aff id="aff6"><institution>Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff54"><institution>University of Paris Sud</institution>,<addr-line>Le Kremlin-Bicêtre</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff55"><institution>U1015, INSERM</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff56"><institution>Center of Clinical Investigations in Biotherapies of Cancer (CICBT) 507</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Agostinis, Patrizia" sort="Agostinis, Patrizia" uniqKey="Agostinis P" first="Patrizia" last="Agostinis">Patrizia Agostinis</name><affiliation><nlm:aff id="aff1"><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26635802</idno><idno type="pmc">4653610</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4653610</idno><idno type="RBID">PMC:4653610</idno><idno type="doi">10.3389/fimmu.2015.00588</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000265</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000265</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Molecular and Translational Classifications of DAMPs in Immunogenic Cell Death</title><author><name sortKey="Garg, Abhishek D" sort="Garg, Abhishek D" uniqKey="Garg A" first="Abhishek D." last="Garg">Abhishek D. Garg</name><affiliation><nlm:aff id="aff1"><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Galluzzi, Lorenzo" sort="Galluzzi, Lorenzo" uniqKey="Galluzzi L" first="Lorenzo" last="Galluzzi">Lorenzo Galluzzi</name><affiliation><nlm:aff id="aff2"><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff6"><institution>Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Apetoh, Lionel" sort="Apetoh, Lionel" uniqKey="Apetoh L" first="Lionel" last="Apetoh">Lionel Apetoh</name><affiliation><nlm:aff id="aff7"><institution>U866, INSERM</institution>,<addr-line>Dijon</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff8"><institution>Faculté de Médecine, Université de Bourgogne</institution>,<addr-line>Dijon</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff9"><institution>Centre Georges François Leclerc</institution>,<addr-line>Dijon</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Baert, Thais" sort="Baert, Thais" uniqKey="Baert T" first="Thais" last="Baert">Thais Baert</name><affiliation><nlm:aff id="aff10"><institution>Department of Gynaecology and Obstetrics, UZ Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff11"><institution>Laboratory of Gynaecologic Oncology, Department of Oncology, Leuven Cancer Institute, KU Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Birge, Raymond B" sort="Birge, Raymond B" uniqKey="Birge R" first="Raymond B." last="Birge">Raymond B. Birge</name><affiliation><nlm:aff id="aff12"><institution>Department of Microbiology, Biochemistry, and Molecular Genetics, University Hospital Cancer Center, Rutgers Cancer Institute of New Jersey, New Jersey Medical School</institution>,<addr-line>Newark, NJ</addr-line>,<country>USA</country></nlm:aff></affiliation></author><author><name sortKey="Bravo San Pedro, Jose Manuel" sort="Bravo San Pedro, Jose Manuel" uniqKey="Bravo San Pedro J" first="José Manuel" last="Bravo-San Pedro">José Manuel Bravo-San Pedro</name><affiliation><nlm:aff id="aff2"><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff6"><institution>Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Breckpot, Karine" sort="Breckpot, Karine" uniqKey="Breckpot K" first="Karine" last="Breckpot">Karine Breckpot</name><affiliation><nlm:aff id="aff13"><institution>Laboratory of Molecular and Cellular Therapy, Vrije Universiteit Brussel</institution>,<addr-line>Jette</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Brough, David" sort="Brough, David" uniqKey="Brough D" first="David" last="Brough">David Brough</name><affiliation><nlm:aff id="aff14"><institution>Faculty of Life Sciences, University of Manchester</institution>,<addr-line>Manchester</addr-line>,<country>UK</country></nlm:aff></affiliation></author><author><name sortKey="Chaurio, Ricardo" sort="Chaurio, Ricardo" uniqKey="Chaurio R" first="Ricardo" last="Chaurio">Ricardo Chaurio</name><affiliation><nlm:aff id="aff15"><institution>Department of Internal Medicine 3 – Rheumatology and Immunology, Friedrich-Alexander-University Erlangen-Nurnberg</institution>,<addr-line>Erlangen</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Cirone, Mara" sort="Cirone, Mara" uniqKey="Cirone M" first="Mara" last="Cirone">Mara Cirone</name><affiliation><nlm:aff id="aff16"><institution>Department of Experimental Medicine, Sapienza University of Rome</institution>,<addr-line>Rome</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Coosemans, An" sort="Coosemans, An" uniqKey="Coosemans A" first="An" last="Coosemans">An Coosemans</name><affiliation><nlm:aff id="aff10"><institution>Department of Gynaecology and Obstetrics, UZ Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff11"><institution>Laboratory of Gynaecologic Oncology, Department of Oncology, Leuven Cancer Institute, KU Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Coulie, Pierre G" sort="Coulie, Pierre G" uniqKey="Coulie P" first="Pierre G." last="Coulie">Pierre G. Coulie</name><affiliation><nlm:aff id="aff17"><institution>de Duve Institute, Université Catholique de Louvain</institution>,<addr-line>Brussels</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="De Ruysscher, Dirk" sort="De Ruysscher, Dirk" uniqKey="De Ruysscher D" first="Dirk" last="De Ruysscher">Dirk De Ruysscher</name><affiliation><nlm:aff id="aff18"><institution>Department of Radiation Oncology, University Hospitals Leuven, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Dini, Luciana" sort="Dini, Luciana" uniqKey="Dini L" first="Luciana" last="Dini">Luciana Dini</name><affiliation><nlm:aff id="aff19"><institution>Department of Biological and Environmental Science and Technology, University of Salento</institution>,<addr-line>Salento</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="De Witte, Peter" sort="De Witte, Peter" uniqKey="De Witte P" first="Peter" last="De Witte">Peter De Witte</name><affiliation><nlm:aff id="aff20"><institution>Laboratory for Molecular Biodiscovery, Department of Pharmaceutical and Pharmacological Sciences, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Dudek Peric, Aleksandra M" sort="Dudek Peric, Aleksandra M" uniqKey="Dudek Peric A" first="Aleksandra M." last="Dudek-Peric">Aleksandra M. Dudek-Peric</name><affiliation><nlm:aff id="aff1"><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Faggioni, Alberto" sort="Faggioni, Alberto" uniqKey="Faggioni A" first="Alberto" last="Faggioni">Alberto Faggioni</name><affiliation><nlm:aff id="aff21"><institution>Sapienza University of Rome</institution>,<addr-line>Rome</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Fucikova, Jitka" sort="Fucikova, Jitka" uniqKey="Fucikova J" first="Jitka" last="Fucikova">Jitka Fucikova</name><affiliation><nlm:aff id="aff22"><institution>SOTIO</institution>,<addr-line>Prague</addr-line>,<country>Czech Republic</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff23"><institution>Department of Immunology, 2nd Faculty of Medicine, University Hospital Motol, Charles University</institution>,<addr-line>Prague</addr-line>,<country>Czech Republic</country></nlm:aff></affiliation></author><author><name sortKey="Gaipl, Udo S" sort="Gaipl, Udo S" uniqKey="Gaipl U" first="Udo S." last="Gaipl">Udo S. Gaipl</name><affiliation><nlm:aff id="aff24"><institution>Department of Radiation Oncology, Universitätsklinikum Erlangen</institution>,<addr-line>Erlangen</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Golab, Jakub" sort="Golab, Jakub" uniqKey="Golab J" first="Jakub" last="Golab">Jakub Golab</name><affiliation><nlm:aff id="aff25"><institution>Department of Immunology, Medical University of Warsaw</institution>,<addr-line>Warsaw</addr-line>,<country>Poland</country></nlm:aff></affiliation></author><author><name sortKey="Gougeon, Marie Lise" sort="Gougeon, Marie Lise" uniqKey="Gougeon M" first="Marie-Lise" last="Gougeon">Marie-Lise Gougeon</name><affiliation><nlm:aff id="aff26"><institution>Biotherapy and Vaccine Unit, Institut Pasteur</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Hamblin, Michael R" sort="Hamblin, Michael R" uniqKey="Hamblin M" first="Michael R." last="Hamblin">Michael R. Hamblin</name><affiliation><nlm:aff id="aff27"><institution>Wellman Center for Photomedicine, Massachusetts General Hospital</institution>,<addr-line>Boston, MA</addr-line>,<country>USA</country></nlm:aff></affiliation></author><author><name sortKey="Hemminki, Akseli" sort="Hemminki, Akseli" uniqKey="Hemminki A" first="Akseli" last="Hemminki">Akseli Hemminki</name><affiliation><nlm:aff id="aff28"><institution>Cancer Gene Therapy Group, Transplantation Laboratory, Haartman Institute, University of Helsinki</institution>,<addr-line>Helsinki</addr-line>,<country>Finland</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff29"><institution>Helsinki University Hospital Comprehensive Cancer Center</institution>,<addr-line>Helsinki</addr-line>,<country>Finland</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff30"><institution>TILT Biotherapeutics Ltd.</institution>,<addr-line>Helsinki</addr-line>,<country>Finland</country></nlm:aff></affiliation></author><author><name sortKey="Herrmann, Martin" sort="Herrmann, Martin" uniqKey="Herrmann M" first="Martin" last="Herrmann">Martin Herrmann</name><affiliation><nlm:aff id="aff15"><institution>Department of Internal Medicine 3 – Rheumatology and Immunology, Friedrich-Alexander-University Erlangen-Nurnberg</institution>,<addr-line>Erlangen</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Hodge, James W" sort="Hodge, James W" uniqKey="Hodge J" first="James W." last="Hodge">James W. Hodge</name><affiliation><nlm:aff id="aff31"><institution>Recombinant Vaccine Group, Laboratory of Tumor Immunology and Biology, National Cancer Institute, National Institutes of Health</institution>,<addr-line>Bethesda, MD</addr-line>,<country>USA</country></nlm:aff></affiliation></author><author><name sortKey="Kepp, Oliver" sort="Kepp, Oliver" uniqKey="Kepp O" first="Oliver" last="Kepp">Oliver Kepp</name><affiliation><nlm:aff id="aff2"><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff32"><institution>Metabolomics and Cell Biology Platforms, Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Kroemer, Guido" sort="Kroemer, Guido" uniqKey="Kroemer G" first="Guido" last="Kroemer">Guido Kroemer</name><affiliation><nlm:aff id="aff2"><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff32"><institution>Metabolomics and Cell Biology Platforms, Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff33"><institution>Pôle de Biologie, Hôpital Européen Georges Pompidou, AP-HP</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff34"><institution>Department of Women’s and Children’s Health, Karolinska University Hospital</institution>,<addr-line>Stockholm</addr-line>,<country>Sweden</country></nlm:aff></affiliation></author><author><name sortKey="Krysko, Dmitri V" sort="Krysko, Dmitri V" uniqKey="Krysko D" first="Dmitri V." last="Krysko">Dmitri V. Krysko</name><affiliation><nlm:aff id="aff35"><institution>Molecular Signaling and Cell Death Unit, Inflammation Research Center, VIB</institution>,<addr-line>Ghent</addr-line>,<country>Belgium</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff36"><institution>Department of Biomedical Molecular Biology, Ghent University</institution>,<addr-line>Ghent</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Land, Walter G" sort="Land, Walter G" uniqKey="Land W" first="Walter G." last="Land">Walter G. Land</name><affiliation><nlm:aff id="aff37"><institution>Molecular ImmunoRheumatology, INSERM UMRS1109, Laboratory of Excellence Transplantex, University of Strasbourg</institution>,<addr-line>Strasbourg</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Madeo, Frank" sort="Madeo, Frank" uniqKey="Madeo F" first="Frank" last="Madeo">Frank Madeo</name><affiliation><nlm:aff id="aff38"><institution>Institute of Molecular Biosciences, NAWI Graz, University of Graz</institution>,<addr-line>Graz</addr-line>,<country>Austria</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff39"><institution>BioTechMed Graz</institution>,<addr-line>Graz</addr-line>,<country>Austria</country></nlm:aff></affiliation></author><author><name sortKey="Manfredi, Angelo A" sort="Manfredi, Angelo A" uniqKey="Manfredi A" first="Angelo A." last="Manfredi">Angelo A. Manfredi</name><affiliation><nlm:aff id="aff40"><institution>IRRCS Istituto Scientifico San Raffaele, Università Vita-Salute San Raffaele</institution>,<addr-line>Milan</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Mattarollo, Stephen R" sort="Mattarollo, Stephen R" uniqKey="Mattarollo S" first="Stephen R." last="Mattarollo">Stephen R. Mattarollo</name><affiliation><nlm:aff id="aff41"><institution>Translational Research Institute, University of Queensland Diamantina Institute, University of Queensland</institution>,<addr-line>Wooloongabba, QLD</addr-line>,<country>Australia</country></nlm:aff></affiliation></author><author><name sortKey="Maueroder, Christian" sort="Maueroder, Christian" uniqKey="Maueroder C" first="Christian" last="Maueroder">Christian Maueroder</name><affiliation><nlm:aff id="aff15"><institution>Department of Internal Medicine 3 – Rheumatology and Immunology, Friedrich-Alexander-University Erlangen-Nurnberg</institution>,<addr-line>Erlangen</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Merendino, Nicol" sort="Merendino, Nicol" uniqKey="Merendino N" first="Nicol" last="Merendino">Nicol Merendino</name><affiliation><nlm:aff id="aff42"><institution>Laboratory of Cellular and Molecular Nutrition, Department of Ecological and Biological Sciences, Tuscia University</institution>,<addr-line>Viterbo</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Multhoff, Gabriele" sort="Multhoff, Gabriele" uniqKey="Multhoff G" first="Gabriele" last="Multhoff">Gabriele Multhoff</name><affiliation><nlm:aff id="aff43"><institution>Department of Radiation Oncology, Klinikum rechts der Isar, Technische Universität München</institution>,<addr-line>Munich</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Pabst, Thomas" sort="Pabst, Thomas" uniqKey="Pabst T" first="Thomas" last="Pabst">Thomas Pabst</name><affiliation><nlm:aff id="aff44"><institution>Department of Medical Oncology, University Hospital</institution>,<addr-line>Bern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Ricci, Jean Ehrland" sort="Ricci, Jean Ehrland" uniqKey="Ricci J" first="Jean-Ehrland" last="Ricci">Jean-Ehrland Ricci</name><affiliation><nlm:aff id="aff45"><institution>INSERM, U1065, Université de Nice-Sophia-Antipolis, Centre Méditerranéen de Médecine Moléculaire (C3M), Équipe “Contrôle Métabolique des Morts Cellulaires”</institution>,<addr-line>Nice</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Riganti, Chiara" sort="Riganti, Chiara" uniqKey="Riganti C" first="Chiara" last="Riganti">Chiara Riganti</name><affiliation><nlm:aff id="aff46"><institution>Department of Oncology, University of Turin</institution>,<addr-line>Turin</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Romano, Erminia" sort="Romano, Erminia" uniqKey="Romano E" first="Erminia" last="Romano">Erminia Romano</name><affiliation><nlm:aff id="aff1"><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Rufo, Nicole" sort="Rufo, Nicole" uniqKey="Rufo N" first="Nicole" last="Rufo">Nicole Rufo</name><affiliation><nlm:aff id="aff1"><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Smyth, Mark J" sort="Smyth, Mark J" uniqKey="Smyth M" first="Mark J." last="Smyth">Mark J. Smyth</name><affiliation><nlm:aff id="aff47"><institution>Immunology in Cancer and Infection Laboratory, QIMR Berghofer Medical Research Insitute</institution>,<addr-line>Herston, QLD</addr-line>,<country>Australia</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff48"><institution>School of Medicine, University of Queensland</institution>,<addr-line>Herston, QLD</addr-line>,<country>Australia</country></nlm:aff></affiliation></author><author><name sortKey="Sonnemann, Jurgen" sort="Sonnemann, Jurgen" uniqKey="Sonnemann J" first="Jürgen" last="Sonnemann">Jürgen Sonnemann</name><affiliation><nlm:aff id="aff49"><institution>Department of Paediatric Haematology and Oncology, Children’s Clinic, Jena University Hospital</institution>,<addr-line>Jena</addr-line>,<country>Germany</country></nlm:aff></affiliation></author><author><name sortKey="Spisek, Radek" sort="Spisek, Radek" uniqKey="Spisek R" first="Radek" last="Spisek">Radek Spisek</name><affiliation><nlm:aff id="aff22"><institution>SOTIO</institution>,<addr-line>Prague</addr-line>,<country>Czech Republic</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff23"><institution>Department of Immunology, 2nd Faculty of Medicine, University Hospital Motol, Charles University</institution>,<addr-line>Prague</addr-line>,<country>Czech Republic</country></nlm:aff></affiliation></author><author><name sortKey="Stagg, John" sort="Stagg, John" uniqKey="Stagg J" first="John" last="Stagg">John Stagg</name><affiliation><nlm:aff id="aff50"><institution>Centre de Recherche du Centre Hospitalier de l’Université de Montréal, Institut du Cancer de Montréal, Faculté de Pharmacie, Université de Montréal</institution>,<addr-line>Montreal, QC</addr-line>,<country>Canada</country></nlm:aff></affiliation></author><author><name sortKey="Vacchelli, Erika" sort="Vacchelli, Erika" uniqKey="Vacchelli E" first="Erika" last="Vacchelli">Erika Vacchelli</name><affiliation><nlm:aff id="aff2"><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff4"><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff5"><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff6"><institution>Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Vandenabeele, Peter" sort="Vandenabeele, Peter" uniqKey="Vandenabeele P" first="Peter" last="Vandenabeele">Peter Vandenabeele</name><affiliation><nlm:aff id="aff35"><institution>Molecular Signaling and Cell Death Unit, Inflammation Research Center, VIB</institution>,<addr-line>Ghent</addr-line>,<country>Belgium</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff36"><institution>Department of Biomedical Molecular Biology, Ghent University</institution>,<addr-line>Ghent</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Vandenberk, Lien" sort="Vandenberk, Lien" uniqKey="Vandenberk L" first="Lien" last="Vandenberk">Lien Vandenberk</name><affiliation><nlm:aff id="aff51"><institution>Laboratory of Pediatric Immunology, Department of Microbiology and Immunology, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Van Den Eynde, Benoit J" sort="Van Den Eynde, Benoit J" uniqKey="Van Den Eynde B" first="Benoit J." last="Van Den Eynde">Benoit J. Van Den Eynde</name><affiliation><nlm:aff id="aff52"><institution>Ludwig Institute for Cancer Research, de Duve Institute, Université Catholique de Louvain</institution>,<addr-line>Brussels</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Van Gool, Stefaan" sort="Van Gool, Stefaan" uniqKey="Van Gool S" first="Stefaan" last="Van Gool">Stefaan Van Gool</name><affiliation><nlm:aff id="aff51"><institution>Laboratory of Pediatric Immunology, Department of Microbiology and Immunology, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author><author><name sortKey="Velotti, Francesca" sort="Velotti, Francesca" uniqKey="Velotti F" first="Francesca" last="Velotti">Francesca Velotti</name><affiliation><nlm:aff id="aff53"><institution>Department of Ecological and Biological Sciences, Tuscia University</institution>,<addr-line>Viterbo</addr-line>,<country>Italy</country></nlm:aff></affiliation></author><author><name sortKey="Zitvogel, Laurence" sort="Zitvogel, Laurence" uniqKey="Zitvogel L" first="Laurence" last="Zitvogel">Laurence Zitvogel</name><affiliation><nlm:aff id="aff6"><institution>Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff54"><institution>University of Paris Sud</institution>,<addr-line>Le Kremlin-Bicêtre</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff55"><institution>U1015, INSERM</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff56"><institution>Center of Clinical Investigations in Biotherapies of Cancer (CICBT) 507</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></nlm:aff></affiliation></author><author><name sortKey="Agostinis, Patrizia" sort="Agostinis, Patrizia" uniqKey="Agostinis P" first="Patrizia" last="Agostinis">Patrizia Agostinis</name><affiliation><nlm:aff id="aff1"><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></nlm:aff></affiliation></author></analytic><series><title level="j">Frontiers in Immunology</title><idno type="eISSN">1664-3224</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The immunogenicity of malignant cells has recently been acknowledged as a critical determinant of efficacy in cancer therapy. Thus, besides developing direct immunostimulatory regimens, including dendritic cell-based vaccines, checkpoint-blocking therapies, and adoptive T-cell transfer, researchers have started to focus on the overall immunobiology of neoplastic cells. It is now clear that cancer cells can succumb to some anticancer therapies by undergoing a peculiar form of cell death that is characterized by an increased immunogenic potential, owing to the emission of the so-called “damage-associated molecular patterns” (DAMPs). The emission of DAMPs and other immunostimulatory factors by cells succumbing to immunogenic cell death (ICD) favors the establishment of a productive interface with the immune system. This results in the elicitation of tumor-targeting immune responses associated with the elimination of residual, treatment-resistant cancer cells, as well as with the establishment of immunological memory. Although ICD has been characterized with increased precision since its discovery, several questions remain to be addressed. Here, we summarize and tabulate the main molecular, immunological, preclinical, and clinical aspects of ICD, in an attempt to capture the essence of this phenomenon, and identify future challenges for this rapidly expanding field of investigation.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Galluzzi, L" uniqKey="Galluzzi L">L Galluzzi</name></author><author><name sortKey="Vacchelli, E" uniqKey="Vacchelli E">E Vacchelli</name></author><author><name sortKey="Bravo San Pedro, Jm" uniqKey="Bravo San Pedro J">JM Bravo-San Pedro</name></author><author><name sortKey="Buque, A" uniqKey="Buque A">A Buque</name></author><author><name sortKey="Senovilla, L" uniqKey="Senovilla L">L Senovilla</name></author><author><name sortKey="Baracco, Ee" uniqKey="Baracco E">EE Baracco</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Kepp, O" uniqKey="Kepp O">O Kepp</name></author><author><name sortKey="Tesniere, A" 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ref-type="aff" rid="aff32"><sup>32</sup></xref><xref ref-type="aff" rid="aff33"><sup>33</sup></xref><xref ref-type="aff" rid="aff34"><sup>34</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/21898"></uri></contrib><contrib contrib-type="author"><name><surname>Krysko</surname><given-names>Dmitri V.</given-names></name><xref ref-type="aff" rid="aff35"><sup>35</sup></xref><xref ref-type="aff" rid="aff36"><sup>36</sup></xref></contrib><contrib contrib-type="author"><name><surname>Land</surname><given-names>Walter G.</given-names></name><xref ref-type="aff" rid="aff37"><sup>37</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/41045"></uri></contrib><contrib contrib-type="author"><name><surname>Madeo</surname><given-names>Frank</given-names></name><xref ref-type="aff" rid="aff38"><sup>38</sup></xref><xref ref-type="aff" rid="aff39"><sup>39</sup></xref><uri xlink:type="simple" 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xlink:href="http://frontiersin.org/people/u/212023"></uri></contrib><contrib contrib-type="author"><name><surname>Multhoff</surname><given-names>Gabriele</given-names></name><xref ref-type="aff" rid="aff43"><sup>43</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/30408"></uri></contrib><contrib contrib-type="author"><name><surname>Pabst</surname><given-names>Thomas</given-names></name><xref ref-type="aff" rid="aff44"><sup>44</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/291391"></uri></contrib><contrib contrib-type="author"><name><surname>Ricci</surname><given-names>Jean-Ehrland</given-names></name><xref ref-type="aff" rid="aff45"><sup>45</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/291377"></uri></contrib><contrib contrib-type="author"><name><surname>Riganti</surname><given-names>Chiara</given-names></name><xref ref-type="aff" rid="aff46"><sup>46</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/75554"></uri></contrib><contrib contrib-type="author"><name><surname>Romano</surname><given-names>Erminia</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Rufo</surname><given-names>Nicole</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Smyth</surname><given-names>Mark J.</given-names></name><xref ref-type="aff" rid="aff47"><sup>47</sup></xref><xref ref-type="aff" rid="aff48"><sup>48</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sonnemann</surname><given-names>Jürgen</given-names></name><xref ref-type="aff" rid="aff49"><sup>49</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/288672"></uri></contrib><contrib contrib-type="author"><name><surname>Spisek</surname><given-names>Radek</given-names></name><xref ref-type="aff" rid="aff22"><sup>22</sup></xref><xref ref-type="aff" rid="aff23"><sup>23</sup></xref></contrib><contrib contrib-type="author"><name><surname>Stagg</surname><given-names>John</given-names></name><xref ref-type="aff" rid="aff50"><sup>50</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/119949"></uri></contrib><contrib contrib-type="author"><name><surname>Vacchelli</surname><given-names>Erika</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref><xref ref-type="aff" rid="aff6"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>Vandenabeele</surname><given-names>Peter</given-names></name><xref ref-type="aff" rid="aff35"><sup>35</sup></xref><xref ref-type="aff" rid="aff36"><sup>36</sup></xref></contrib><contrib contrib-type="author"><name><surname>Vandenberk</surname><given-names>Lien</given-names></name><xref ref-type="aff" rid="aff51"><sup>51</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/278291"></uri></contrib><contrib contrib-type="author"><name><surname>Van den Eynde</surname><given-names>Benoit J.</given-names></name><xref ref-type="aff" rid="aff52"><sup>52</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/32052"></uri></contrib><contrib contrib-type="author"><name><surname>Van Gool</surname><given-names>Stefaan</given-names></name><xref ref-type="aff" rid="aff51"><sup>51</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/187468"></uri></contrib><contrib contrib-type="author"><name><surname>Velotti</surname><given-names>Francesca</given-names></name><xref ref-type="aff" rid="aff53"><sup>53</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/288691"></uri></contrib><contrib contrib-type="author"><name><surname>Zitvogel</surname><given-names>Laurence</given-names></name><xref ref-type="aff" rid="aff6"><sup>6</sup></xref><xref ref-type="aff" rid="aff54"><sup>54</sup></xref><xref ref-type="aff" rid="aff55"><sup>55</sup></xref><xref ref-type="aff" rid="aff56"><sup>56</sup></xref></contrib><contrib contrib-type="author"><name><surname>Agostinis</surname><given-names>Patrizia</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1">*</xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/120137"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Cell Death Research and Therapy Laboratory, Department of Cellular Molecular Medicine, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></aff><aff id="aff2"><sup>2</sup><institution>Equipe 11 Labellisée Ligue Contre le Cancer, Centre de Recherche des Cordeliers</institution>,<addr-line>Paris</addr-line>,<country>France</country></aff><aff id="aff3"><sup>3</sup><institution>U1138, INSERM</institution>,<addr-line>Paris</addr-line>,<country>France</country></aff><aff id="aff4"><sup>4</sup><institution>Université Paris Descartes, Sorbonne Paris Cité</institution>,<addr-line>Paris</addr-line>,<country>France</country></aff><aff id="aff5"><sup>5</sup><institution>Université Pierre et Marie Curie</institution>,<addr-line>Paris</addr-line>,<country>France</country></aff><aff id="aff6"><sup>6</sup><institution>Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></aff><aff id="aff7"><sup>7</sup><institution>U866, INSERM</institution>,<addr-line>Dijon</addr-line>,<country>France</country></aff><aff id="aff8"><sup>8</sup><institution>Faculté de Médecine, Université de Bourgogne</institution>,<addr-line>Dijon</addr-line>,<country>France</country></aff><aff id="aff9"><sup>9</sup><institution>Centre Georges François Leclerc</institution>,<addr-line>Dijon</addr-line>,<country>France</country></aff><aff id="aff10"><sup>10</sup><institution>Department of Gynaecology and Obstetrics, UZ Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></aff><aff id="aff11"><sup>11</sup><institution>Laboratory of Gynaecologic Oncology, Department of Oncology, Leuven Cancer Institute, KU Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></aff><aff id="aff12"><sup>12</sup><institution>Department of Microbiology, Biochemistry, and Molecular Genetics, University Hospital Cancer Center, Rutgers Cancer Institute of New Jersey, New Jersey Medical School</institution>,<addr-line>Newark, NJ</addr-line>,<country>USA</country></aff><aff id="aff13"><sup>13</sup><institution>Laboratory of Molecular and Cellular Therapy, Vrije Universiteit Brussel</institution>,<addr-line>Jette</addr-line>,<country>Belgium</country></aff><aff id="aff14"><sup>14</sup><institution>Faculty of Life Sciences, University of Manchester</institution>,<addr-line>Manchester</addr-line>,<country>UK</country></aff><aff id="aff15"><sup>15</sup><institution>Department of Internal Medicine 3 – Rheumatology and Immunology, Friedrich-Alexander-University Erlangen-Nurnberg</institution>,<addr-line>Erlangen</addr-line>,<country>Germany</country></aff><aff id="aff16"><sup>16</sup><institution>Department of Experimental Medicine, Sapienza University of Rome</institution>,<addr-line>Rome</addr-line>,<country>Italy</country></aff><aff id="aff17"><sup>17</sup><institution>de Duve Institute, Université Catholique de Louvain</institution>,<addr-line>Brussels</addr-line>,<country>Belgium</country></aff><aff id="aff18"><sup>18</sup><institution>Department of Radiation Oncology, University Hospitals Leuven, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></aff><aff id="aff19"><sup>19</sup><institution>Department of Biological and Environmental Science and Technology, University of Salento</institution>,<addr-line>Salento</addr-line>,<country>Italy</country></aff><aff id="aff20"><sup>20</sup><institution>Laboratory for Molecular Biodiscovery, Department of Pharmaceutical and Pharmacological Sciences, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></aff><aff id="aff21"><sup>21</sup><institution>Sapienza University of Rome</institution>,<addr-line>Rome</addr-line>,<country>Italy</country></aff><aff id="aff22"><sup>22</sup><institution>SOTIO</institution>,<addr-line>Prague</addr-line>,<country>Czech Republic</country></aff><aff id="aff23"><sup>23</sup><institution>Department of Immunology, 2nd Faculty of Medicine, University Hospital Motol, Charles University</institution>,<addr-line>Prague</addr-line>,<country>Czech Republic</country></aff><aff id="aff24"><sup>24</sup><institution>Department of Radiation Oncology, Universitätsklinikum Erlangen</institution>,<addr-line>Erlangen</addr-line>,<country>Germany</country></aff><aff id="aff25"><sup>25</sup><institution>Department of Immunology, Medical University of Warsaw</institution>,<addr-line>Warsaw</addr-line>,<country>Poland</country></aff><aff id="aff26"><sup>26</sup><institution>Biotherapy and Vaccine Unit, Institut Pasteur</institution>,<addr-line>Paris</addr-line>,<country>France</country></aff><aff id="aff27"><sup>27</sup><institution>Wellman Center for Photomedicine, Massachusetts General Hospital</institution>,<addr-line>Boston, MA</addr-line>,<country>USA</country></aff><aff id="aff28"><sup>28</sup><institution>Cancer Gene Therapy Group, Transplantation Laboratory, Haartman Institute, University of Helsinki</institution>,<addr-line>Helsinki</addr-line>,<country>Finland</country></aff><aff id="aff29"><sup>29</sup><institution>Helsinki University Hospital Comprehensive Cancer Center</institution>,<addr-line>Helsinki</addr-line>,<country>Finland</country></aff><aff id="aff30"><sup>30</sup><institution>TILT Biotherapeutics Ltd.</institution>,<addr-line>Helsinki</addr-line>,<country>Finland</country></aff><aff id="aff31"><sup>31</sup><institution>Recombinant Vaccine Group, Laboratory of Tumor Immunology and Biology, National Cancer Institute, National Institutes of Health</institution>,<addr-line>Bethesda, MD</addr-line>,<country>USA</country></aff><aff id="aff32"><sup>32</sup><institution>Metabolomics and Cell Biology Platforms, Gustave Roussy Comprehensive Cancer Institute</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></aff><aff id="aff33"><sup>33</sup><institution>Pôle de Biologie, Hôpital Européen Georges Pompidou, AP-HP</institution>,<addr-line>Paris</addr-line>,<country>France</country></aff><aff id="aff34"><sup>34</sup><institution>Department of Women’s and Children’s Health, Karolinska University Hospital</institution>,<addr-line>Stockholm</addr-line>,<country>Sweden</country></aff><aff id="aff35"><sup>35</sup><institution>Molecular Signaling and Cell Death Unit, Inflammation Research Center, VIB</institution>,<addr-line>Ghent</addr-line>,<country>Belgium</country></aff><aff id="aff36"><sup>36</sup><institution>Department of Biomedical Molecular Biology, Ghent University</institution>,<addr-line>Ghent</addr-line>,<country>Belgium</country></aff><aff id="aff37"><sup>37</sup><institution>Molecular ImmunoRheumatology, INSERM UMRS1109, Laboratory of Excellence Transplantex, University of Strasbourg</institution>,<addr-line>Strasbourg</addr-line>,<country>France</country></aff><aff id="aff38"><sup>38</sup><institution>Institute of Molecular Biosciences, NAWI Graz, University of Graz</institution>,<addr-line>Graz</addr-line>,<country>Austria</country></aff><aff id="aff39"><sup>39</sup><institution>BioTechMed Graz</institution>,<addr-line>Graz</addr-line>,<country>Austria</country></aff><aff id="aff40"><sup>40</sup><institution>IRRCS Istituto Scientifico San Raffaele, Università Vita-Salute San Raffaele</institution>,<addr-line>Milan</addr-line>,<country>Italy</country></aff><aff id="aff41"><sup>41</sup><institution>Translational Research Institute, University of Queensland Diamantina Institute, University of Queensland</institution>,<addr-line>Wooloongabba, QLD</addr-line>,<country>Australia</country></aff><aff id="aff42"><sup>42</sup><institution>Laboratory of Cellular and Molecular Nutrition, Department of Ecological and Biological Sciences, Tuscia University</institution>,<addr-line>Viterbo</addr-line>,<country>Italy</country></aff><aff id="aff43"><sup>43</sup><institution>Department of Radiation Oncology, Klinikum rechts der Isar, Technische Universität München</institution>,<addr-line>Munich</addr-line>,<country>Germany</country></aff><aff id="aff44"><sup>44</sup><institution>Department of Medical Oncology, University Hospital</institution>,<addr-line>Bern</addr-line>,<country>Switzerland</country></aff><aff id="aff45"><sup>45</sup><institution>INSERM, U1065, Université de Nice-Sophia-Antipolis, Centre Méditerranéen de Médecine Moléculaire (C3M), Équipe “Contrôle Métabolique des Morts Cellulaires”</institution>,<addr-line>Nice</addr-line>,<country>France</country></aff><aff id="aff46"><sup>46</sup><institution>Department of Oncology, University of Turin</institution>,<addr-line>Turin</addr-line>,<country>Italy</country></aff><aff id="aff47"><sup>47</sup><institution>Immunology in Cancer and Infection Laboratory, QIMR Berghofer Medical Research Insitute</institution>,<addr-line>Herston, QLD</addr-line>,<country>Australia</country></aff><aff id="aff48"><sup>48</sup><institution>School of Medicine, University of Queensland</institution>,<addr-line>Herston, QLD</addr-line>,<country>Australia</country></aff><aff id="aff49"><sup>49</sup><institution>Department of Paediatric Haematology and Oncology, Children’s Clinic, Jena University Hospital</institution>,<addr-line>Jena</addr-line>,<country>Germany</country></aff><aff id="aff50"><sup>50</sup><institution>Centre de Recherche du Centre Hospitalier de l’Université de Montréal, Institut du Cancer de Montréal, Faculté de Pharmacie, Université de Montréal</institution>,<addr-line>Montreal, QC</addr-line>,<country>Canada</country></aff><aff id="aff51"><sup>51</sup><institution>Laboratory of Pediatric Immunology, Department of Microbiology and Immunology, KU Leuven – University of Leuven</institution>,<addr-line>Leuven</addr-line>,<country>Belgium</country></aff><aff id="aff52"><sup>52</sup><institution>Ludwig Institute for Cancer Research, de Duve Institute, Université Catholique de Louvain</institution>,<addr-line>Brussels</addr-line>,<country>Belgium</country></aff><aff id="aff53"><sup>53</sup><institution>Department of Ecological and Biological Sciences, Tuscia University</institution>,<addr-line>Viterbo</addr-line>,<country>Italy</country></aff><aff id="aff54"><sup>54</sup><institution>University of Paris Sud</institution>,<addr-line>Le Kremlin-Bicêtre</addr-line>,<country>France</country></aff><aff id="aff55"><sup>55</sup><institution>U1015, INSERM</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></aff><aff id="aff56"><sup>56</sup><institution>Center of Clinical Investigations in Biotherapies of Cancer (CICBT) 507</institution>,<addr-line>Villejuif</addr-line>,<country>France</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Fabrizio Mattei, Istituto Superiore di Sanità, Italy</p></fn><fn fn-type="edited-by"><p>Reviewed by: Luis De La Cruz-Merino, Hospital Universitario Virgen Macarena, Spain; Carlos Alfaro, Clínica Universidad de Navarra, Spain</p></fn><corresp content-type="corresp" id="cor1">*Correspondence: Abhishek D. Garg, <email>abhishek.garg@med.kuleuven.be</email>, <email>abhishekdgarg@gmail.com</email>; Patrizia Agostinis, <email>patrizia.agostinis@med.kuleuven.be</email></corresp><fn fn-type="other" id="fn001"><p>Specialty section: This article was submitted to Tumor Immunity, a section of the journal Frontiers in Immunology</p></fn></author-notes><pub-date pub-type="epub"><day>20</day><month>11</month><year>2015</year></pub-date><pub-date pub-type="collection"><year>2015</year></pub-date><volume>6</volume><elocation-id>588</elocation-id><history><date date-type="received"><day>17</day><month>9</month><year>2015</year></date><date date-type="accepted"><day>02</day><month>11</month><year>2015</year></date></history><permissions><copyright-statement>Copyright © 2015 Garg, Galluzzi, Apetoh, Baert, Birge, Bravo-San Pedro, Breckpot, Brough, Chaurio, Cirone, Coosemans, Coulie, De Ruysscher, Dini, de Witte, Dudek-Peric, Faggioni, Fucikova, Gaipl, Golab, Gougeon, Hamblin, Hemminki, Herrmann, Hodge, Kepp, Kroemer, Krysko, Land, Madeo, Manfredi, Mattarollo, Maueroder, Merendino, Multhoff, Pabst, Ricci, Riganti, Romano, Rufo, Smyth, Sonnemann, Spisek, Stagg, Vacchelli, Vandenabeele, Vandenberk, Van den Eynde, Van Gool, Velotti, Zitvogel and Agostinis.</copyright-statement><copyright-year>2015</copyright-year><copyright-holder>Garg, Galluzzi, Apetoh, Baert, Birge, Bravo-San Pedro, Breckpot, Brough, Chaurio, Cirone, Coosemans, Coulie, De Ruysscher, Dini, de Witte, Dudek-Peric, Faggioni, Fucikova, Gaipl, Golab, Gougeon, Hamblin, Hemminki, Herrmann, Hodge, Kepp, Kroemer, Krysko, Land, Madeo, Manfredi, Mattarollo, Maueroder, Merendino, Multhoff, Pabst, Ricci, Riganti, Romano, Rufo, Smyth, Sonnemann, Spisek, Stagg, Vacchelli, Vandenabeele, Vandenberk, Van den Eynde, Van Gool, Velotti, Zitvogel and Agostinis</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>The immunogenicity of malignant cells has recently been acknowledged as a critical determinant of efficacy in cancer therapy. Thus, besides developing direct immunostimulatory regimens, including dendritic cell-based vaccines, checkpoint-blocking therapies, and adoptive T-cell transfer, researchers have started to focus on the overall immunobiology of neoplastic cells. It is now clear that cancer cells can succumb to some anticancer therapies by undergoing a peculiar form of cell death that is characterized by an increased immunogenic potential, owing to the emission of the so-called “damage-associated molecular patterns” (DAMPs). The emission of DAMPs and other immunostimulatory factors by cells succumbing to immunogenic cell death (ICD) favors the establishment of a productive interface with the immune system. This results in the elicitation of tumor-targeting immune responses associated with the elimination of residual, treatment-resistant cancer cells, as well as with the establishment of immunological memory. Although ICD has been characterized with increased precision since its discovery, several questions remain to be addressed. Here, we summarize and tabulate the main molecular, immunological, preclinical, and clinical aspects of ICD, in an attempt to capture the essence of this phenomenon, and identify future challenges for this rapidly expanding field of investigation.</p></abstract><kwd-group><kwd>anti-tumor immunity</kwd><kwd>immunogenicity</kwd><kwd>immunotherapy</kwd><kwd>molecular medicine</kwd><kwd>oncoimmunology</kwd><kwd>patient prognosis</kwd><kwd>translational medicine</kwd></kwd-group><counts><fig-count count="2"></fig-count><table-count count="8"></table-count><equation-count count="0"></equation-count><ref-count count="246"></ref-count><page-count count="24"></page-count><word-count count="17338"></word-count></counts></article-meta></front><body><sec id="S1"><title>Introduction and Historical Background</title><p>Augmenting the immunogenicity of cancer cells to improve the efficacy of cancer therapy is a paradigm that has gained significant momentum over the past 5 years (<xref rid="B1" ref-type="bibr">1</xref>–<xref rid="B5" ref-type="bibr">5</xref>). Researchers have realized that besides therapeutically exploiting innate or adaptive immune cells directly (e.g., through dendritic cell (DC)-based vaccines or adoptive T-cell transfer) and/or improving the effector functions of T cells (through checkpoint-blocking therapies), cancer cells also need to be made immunogenic (<xref rid="B1" ref-type="bibr">1</xref>, <xref rid="B4" ref-type="bibr">4</xref>, <xref rid="B6" ref-type="bibr">6</xref>, <xref rid="B7" ref-type="bibr">7</xref>). This has diverted attention toward studying the interface between stressed or dying cancer cells and the immune system, in the hope of efficiently exploiting it for therapeutic purposes (<xref rid="B1" ref-type="bibr">1</xref>).</p><p>Early indications regarding immune system-driven tumor control emerged in the eighteenth century, when feverish infections in cancer patients were circumstantially associated with tumor remission (<xref rid="B8" ref-type="bibr">8</xref>). The first evidence that immunotherapy can be applied to achieve tumor regression emerged from the work of William Coley, who in the 1890s achieved tumor regression in some sarcoma/lymphoma patients upon the intra-tumoral injection of streptococcal cultures (provided by Robert Koch) (<xref rid="B8" ref-type="bibr">8</xref>, <xref rid="B9" ref-type="bibr">9</xref>). In the following 43 years, Coley injected nearly 900 (mostly sarcoma) patients with his bacterial preparation (achieving a cure rate >10%), which later became known as “Coley’s toxin” (<xref rid="B8" ref-type="bibr">8</xref>, <xref rid="B10" ref-type="bibr">10</xref>). However, the Coley’s toxin came under intense scrutiny owing to an elevated toxicity and some difficulties in reproducing remission rates (<xref rid="B8" ref-type="bibr">8</xref>). Eventually, the first experimental evidence that virus-unrelated tumors can indeed be recognized by the host immune system emerged in the 1940s, and by the 1960s, coupled with the discovery of T cells, it was proposed that the human immune system may also react against tumors (<xref rid="B11" ref-type="bibr">11</xref>). The ability of anticancer therapies to enhance the immunogenic potential of malignant cells gained some appreciation by the 1970s (<xref rid="B12" ref-type="bibr">12</xref>–<xref rid="B14" ref-type="bibr">14</xref>). It was recognized that if specific treatments are applied (e.g., radiotherapy, the bacillus Calmette–Guerin, or some chemotherapeutics), the immunogenicity of malignant cells increases enough to induce durable anti-tumor immunity (<xref rid="B12" ref-type="bibr">12</xref>–<xref rid="B14" ref-type="bibr">14</xref>). By the 1980s, researchers started to report more specific observations regarding the therapeutic impact of cancer cell immunogenicity, e.g., the ability of curative hyperthermia to cause the (heat-shock based) generation of circumstantial anti-tumor immunity (<xref rid="B15" ref-type="bibr">15</xref>), the fact that the immunogenicity of cancer cells influences patient prognosis after radiotherapy (<xref rid="B16" ref-type="bibr">16</xref>), and the increase in tumor immunogenicity due to hydrostatic pressure (<xref rid="B17" ref-type="bibr">17</xref>). However, these early studies (especially those published before the 1980s) had several issues linked to a lack in consensus. For instance, due to early controversies on the existence of tumor-associated antigens (TAAs) (<xref rid="B11" ref-type="bibr">11</xref>), the target of tumor-specific immune responses was unclear, and the mechanism of action of some therapies came under scrutiny. Moreover, such therapies could operate by directly modulating immune effector cells rather than improving the immunogenic potential of tumors (<xref rid="B18" ref-type="bibr">18</xref>). In particular, the death of cancer cells exposed to therapy was never suspected to drive anti-tumor immunity, since it was considered to be a relatively “silent” process in terms of immunogenicity (<xref rid="B19" ref-type="bibr">19</xref>). Moreover, the classical “self/non-self” theory was unable to explain the possibility that dying cancer cells could elicit an immune response (<xref rid="B20" ref-type="bibr">20</xref>).</p><p>By the early 1990s, the molecular characterization of mice and human TAAs clarified the entities targeted by anti-tumor immune responses (<xref rid="B11" ref-type="bibr">11</xref>). Similarly, the so-called “danger theory” started to emerge, challenging the classical model of “self/non-self” immune recognition, especially in a diseased or damaged tissue (<xref rid="B20" ref-type="bibr">20</xref>, <xref rid="B21" ref-type="bibr">21</xref>). This model proposed that the immune recognition is not restricted to “non-self” entities, but rather discriminates between “dangerous” and “safe” entities, irrespective of source (<xref rid="B20" ref-type="bibr">20</xref>–<xref rid="B22" ref-type="bibr">22</xref>). Indeed, “dangerous” entities include pathogens as well as injured, infected, diseased and necrotic tissues, or cells undergoing non-physiological cell death which emit danger signals (or alarmins) with pro-inflammatory activity (<xref rid="B21" ref-type="bibr">21</xref>, <xref rid="B22" ref-type="bibr">22</xref>). These danger signals are now collectively referred to as “damage-associated molecular patterns” (DAMPs) (<xref rid="B23" ref-type="bibr">23</xref>). DAMPs are endogenous molecules that are concealed intracellularly in normal conditions, but are exposed or released upon stress, injury, cell death, thereby becoming able to bind cognate receptors on immune cells (<xref rid="B3" ref-type="bibr">3</xref>, <xref rid="B24" ref-type="bibr">24</xref>–<xref rid="B27" ref-type="bibr">27</xref>). Table <xref ref-type="table" rid="T1">1</xref> summarizes the most prominent DAMPs characterized to date and their mode of emission, the cell death pathway they are associated with, and their known cognate receptors. It is important to consider that not all DAMPs may act as immunogenic danger signals. Several DAMPs exist that are crucial for the maintenance of tissue homeostasis, and the avoidance of auto-immune responses, as they exert immunosuppressive effects, including phosphatidylserine (PS), annexin A1 (ANXA1), death domain 1α (DD1α), B-cell CLL/lymphoma 2 (BCL2) and some extracellular matrix-derived molecules (Table <xref ref-type="table" rid="T1">1</xref>). Accordingly, the blockade of these anti-inflammatory DAMPs accentuates the immunogenic potential of dying cells, or renders immunogenic otherwise tolerogenic forms of cell death (<xref rid="B28" ref-type="bibr">28</xref>, <xref rid="B29" ref-type="bibr">29</xref>). Moreover, some danger signals are not always involved in the immunogenicity of cell death, but act as “bystanders.” This is the case for heat shock protein 90 kDa alpha (cytosolic), class A member 1 (HSP90AA1, best known as HSP90) exposed on the cell surface after melphalan treatment (<xref rid="B30" ref-type="bibr">30</xref>). Last (but not least), several DAMPs may be subjected to post-translational modifications (e.g., oxidation, reduction, citrullination) that may potentially neutralize, increase, or change their immunogenic properties (<xref rid="B31" ref-type="bibr">31</xref>, <xref rid="B32" ref-type="bibr">32</xref>) – a process that is still incompletely understood.</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p><bold>A list of prominent damage-associated molecular patterns (DAMPs) associated with cell death pathways or extracellular matrix</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">DAMPs</th><th valign="top" align="left" rowspan="1" colspan="1">Localization and mode-of-emission</th><th valign="top" align="left" rowspan="1" colspan="1">Relevant cell death pathway</th><th valign="top" align="left" rowspan="1" colspan="1">Receptors</th><th valign="top" align="center" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Annexin A1</td><td valign="top" align="left" rowspan="1" colspan="1">Surface exposed or actively/passively released?</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">FPR-1 receptor</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B33" ref-type="bibr">33</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Adenosine triphosphate</td><td valign="top" align="left" rowspan="1" colspan="1">Actively or passively released</td><td valign="top" align="left" rowspan="1" colspan="1">ICD, apoptosis/secondary necrosis and necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">P<sub>2</sub>Y<sub>2</sub> and P<sub>2</sub>×<sub>7</sub></td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B34" ref-type="bibr">34</xref>–<xref rid="B37" ref-type="bibr">37</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">B-cell CLL/lymphoma 2</td><td valign="top" align="left" rowspan="1" colspan="1">Passive release</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">TLR2</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B38" ref-type="bibr">38</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Biglycan</td><td valign="top" align="left" rowspan="1" colspan="1">Extracellular matrix</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">TLR2, TLR4, P<sub>2</sub>×<sub>4</sub>, and P<sub>2</sub>×<sub>7</sub></td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B39" ref-type="bibr">39</xref>, <xref rid="B40" ref-type="bibr">40</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Calreticulin</td><td valign="top" align="left" rowspan="1" colspan="1">Mostly surface exposed; sometimes passively released</td><td valign="top" align="left" rowspan="1" colspan="1">ICD</td><td valign="top" align="left" rowspan="1" colspan="1">CD91</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B41" ref-type="bibr">41</xref>–<xref rid="B44" ref-type="bibr">44</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Cardiolipin</td><td valign="top" align="left" rowspan="1" colspan="1">Surface exposed?</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B45" ref-type="bibr">45</xref>, <xref rid="B46" ref-type="bibr">46</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Ceramide and sphingosine-1-phosphate</td><td valign="top" align="left" rowspan="1" colspan="1">Surface exposed</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B47" ref-type="bibr">47</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Covalent/cross-linked dimer of ribosomal protein S19</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released?</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">CD88</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B48" ref-type="bibr">48</xref>–<xref rid="B51" ref-type="bibr">51</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Carbamoyl-phosphate synthase 1</td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B52" ref-type="bibr">52</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Cyclophilin A</td><td valign="top" align="left" rowspan="1" colspan="1">Passive release</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">CD147</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B53" ref-type="bibr">53</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Cytochrome <italic>c</italic></td><td valign="top" align="left" rowspan="1" colspan="1">Passively released?</td><td valign="top" align="left" rowspan="1" colspan="1">Secondary necrosis and necrosis?</td><td valign="top" align="left" rowspan="1" colspan="1">LPG?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B54" ref-type="bibr">54</xref>, <xref rid="B55" ref-type="bibr">55</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Death domain 1α</td><td valign="top" align="left" rowspan="1" colspan="1">Surface exposed</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">DD1α</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B56" ref-type="bibr">56</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Endothelial monocyte-activating polypeptide II</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released?</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">CXCR3?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B50" ref-type="bibr">50</xref>, <xref rid="B57" ref-type="bibr">57</xref>, <xref rid="B58" ref-type="bibr">58</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">F-actin</td><td valign="top" align="left" rowspan="1" colspan="1">Passive release</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">DNGR-1/Clec9a</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B59" ref-type="bibr">59</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Fibrinogen</td><td valign="top" align="left" rowspan="1" colspan="1">Extracellular matrix</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">TLR4</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B40" ref-type="bibr">40</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Fibronectin extra domain A</td><td valign="top" align="left" rowspan="1" colspan="1">Extracellular matrix</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">TLR4?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B40" ref-type="bibr">40</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Fragments of human tyrosyl tRNA synthetase</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released?</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B50" ref-type="bibr">50</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Genomic DNA, mRNA, snRNPs</td><td valign="top" align="left" rowspan="1" colspan="1">Passive release</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">TLR3</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B3" ref-type="bibr">3</xref>, <xref rid="B60" ref-type="bibr">60</xref>, <xref rid="B61" ref-type="bibr">61</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">GRP78/BiP</td><td valign="top" align="left" rowspan="1" colspan="1">Passive release</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis, apoptosis?</td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B31" ref-type="bibr">31</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">H<sub>2</sub>0<sub>2</sub></td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B62" ref-type="bibr">62</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Heat shock proteins (HSP70, HSP90, HSP60, HSP72, and GP96)</td><td valign="top" align="left" rowspan="1" colspan="1">Surface exposure, active secretion, or passive release</td><td valign="top" align="left" rowspan="1" colspan="1">ICD, apoptosis/secondary necrosis, necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">CD91, TLR2, TLR4, SREC-1 and FEEL-1</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B63" ref-type="bibr">63</xref>–<xref rid="B67" ref-type="bibr">67</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Heparan sulfate fragments</td><td valign="top" align="left" rowspan="1" colspan="1">Extracellular matrix</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">TLR4</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B40" ref-type="bibr">40</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Hepatoma-derived growth factor</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B68" ref-type="bibr">68</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Histones</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">TLR-9</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B69" ref-type="bibr">69</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">High-mobility group box 1</td><td valign="top" align="left" rowspan="1" colspan="1">Mostly passively released; sometimes actively released</td><td valign="top" align="left" rowspan="1" colspan="1">ICD, secondary necrosis and necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">TLR2, TLR4, RAGE and TIM3</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B70" ref-type="bibr">70</xref>–<xref rid="B73" ref-type="bibr">73</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">High-mobility group nucleosome binding domain 1</td><td valign="top" align="left" rowspan="1" colspan="1">Passive release</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">TLR4</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B74" ref-type="bibr">74</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Hyaluronan</td><td valign="top" align="left" rowspan="1" colspan="1">Extracellular matrix</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">TLR2 and TLR4</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B40" ref-type="bibr">40</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">IL-1α</td><td valign="top" align="left" rowspan="1" colspan="1">Passive release</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">IL-1R</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B75" ref-type="bibr">75</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">IL-33</td><td valign="top" align="left" rowspan="1" colspan="1">Passive release</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">ST2</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B3" ref-type="bibr">3</xref>, <xref rid="B61" ref-type="bibr">61</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">IL-6</td><td valign="top" align="left" rowspan="1" colspan="1">Passive release</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">IL-6R and GP130</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B76" ref-type="bibr">76</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Lysophosphatidylcholine</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released?</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">G2A</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B50" ref-type="bibr">50</xref>, <xref rid="B77" ref-type="bibr">77</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Mit DNA</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">TLR-9</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B78" ref-type="bibr">78</xref>–<xref rid="B80" ref-type="bibr">80</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Monosodium urate or uric acid</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">Purinergic receptors</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B50" ref-type="bibr">50</xref>, <xref rid="B81" ref-type="bibr">81</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>N</italic>-formylated peptides</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">FPR-1</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B78" ref-type="bibr">78</xref>, <xref rid="B82" ref-type="bibr">82</xref>–<xref rid="B84" ref-type="bibr">84</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Oxidation-associated molecular patterns (reactive protein carbonyls, per-oxidized phospholipids, oxidized low-density lipoprotein)</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis, Secondary necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">CD36, SR-A, TLR-2/4, CD14</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B85" ref-type="bibr">85</xref>–<xref rid="B87" ref-type="bibr">87</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Peroxiredoxin 1</td><td valign="top" align="left" rowspan="1" colspan="1">Actively secreted or passively released</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis, necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">TLR4</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B88" ref-type="bibr">88</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Phosphatidylserine</td><td valign="top" align="left" rowspan="1" colspan="1">Actively externalized on the surface</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">TIM-1/-3/-4, BAI1, Stabilin-2, MFG-E8, C1q</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B56" ref-type="bibr">56</xref>, <xref rid="B89" ref-type="bibr">89</xref>–<xref rid="B93" ref-type="bibr">93</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">S100/calgranulin protein family members (S100A8, S100A9, S100A12/EN-RAGE)</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released</td><td valign="top" align="left" rowspan="1" colspan="1">Necrosis</td><td valign="top" align="left" rowspan="1" colspan="1">RAGE</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B50" ref-type="bibr">50</xref>, <xref rid="B94" ref-type="bibr">94</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Tenascin-C</td><td valign="top" align="left" rowspan="1" colspan="1">Extracellular matrix</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">TLR4?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B95" ref-type="bibr">95</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Thrombospondin 1 and its heparin-binding domain</td><td valign="top" align="left" rowspan="1" colspan="1">Passively released or surface associated</td><td valign="top" align="left" rowspan="1" colspan="1">Apoptosis</td><td valign="top" align="left" rowspan="1" colspan="1">α<sub>v</sub>β<sub>3</sub> integrin</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B50" ref-type="bibr">50</xref>, <xref rid="B96" ref-type="bibr">96</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Versican</td><td valign="top" align="left" rowspan="1" colspan="1">Extracellular matrix</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">TLR2, TLR6, and CD14</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B40" ref-type="bibr">40</xref>)</td></tr></tbody></table><table-wrap-foot><p><italic>CD, cluster of differentiation; CLEC9A, C-type lectin domain family 9, member A; CPS-1, carbamoyl-phosphate synthase 1, mitochondrial; CXCR3, C-X-C motif receptor 3; FEEL-1/CLEVER-1, fasciclin EGF-like/common lymphatic endothelial and vascular endothelial receptor-1; FPR-1, formyl peptides receptor-1; G2A, G2 accumulation; HMGB1, high-mobility group box 1; HSP, heat shock proteins; ICD, immunogenic cell death; IL, interleukin; LPG, leucine-rich alpha-2-glycoprotein-1; MFG-E8, milk fat globule-egf factor 8 protein; Mit DNA, mitochondrial DNA; P2XR, P2X receptor; P2YR, P2Y receptor; RAGE, receptor for advanced glycation endproducts; SREC-1, scavenger receptor class f member 1; TFAM, mitochondrial transcription factor A; TIM, transmembrane immunoglobulin and mucin domain; TLR, toll-like receptor(s)</italic>.</p><p><italic>Glossary (<xref rid="B5" ref-type="bibr">5</xref>, <xref rid="B19" ref-type="bibr">19</xref>, <xref rid="B97" ref-type="bibr">97</xref>): (1) <italic>Necrosis</italic>: primary necrosis is a form of cell death that can occur in a regulated or accidental manner, characterized by cellular swelling and rapid breakdown of the plasma membrane; (2) <italic>Necroptosis</italic>: necroptosis is a form of regulated cell death (RCD) manifesting with necrotic morphology and controlled by a signaling cascade involving (among other proteins) RIPK1, RIPK3, and MLKL; (3) <italic>Apoptosis</italic>: apoptosis is a form of RCD largely dependent on caspases activity and morphologically characterized by cell shrinkage, membrane blebbing, formation of apoptotic bodies, chromatin condensation, and systematic DNA fragmentation; (4) <italic>Secondary Necrosis</italic>: Secondary necrosis is a terminal process experienced by late-apoptotic cells if they are not cleared by phagocytes in time, and is characterized by general spill-over of apoptotic cellular contents</italic>.</p><p><italic>“?” Unclear or not determined yet</italic>.</p></table-wrap-foot></table-wrap><p>Despite these advances, the overall role of regulated cell death (RCD) (<xref rid="B97" ref-type="bibr">97</xref>) in augmenting cancer immunogenicity remained obscure. Initial observations involving the immunogenicity of cell death in the efficacy of cancer therapy were published between 1998 and 2004, when it was proposed that the non-apoptotic demise of malignant cells (within the context of the so-called “immunogenic death”) could be associated with the emission of the danger signal heat shock 70 kDa protein 1A (HSPA1A, best known as HSP70) (Table <xref ref-type="table" rid="T1">1</xref>), enhancing the immunogenic potential of dying cancer cells <italic>in vivo</italic> (<xref rid="B98" ref-type="bibr">98</xref>, <xref rid="B99" ref-type="bibr">99</xref>). The dogmatic view that only necrotic or non-apoptotic (as postulated by the “immunogenic death” concept) cancer cells are characterized by an elevated immunogenic potential started to be questioned by a series of studies published between 2005 and 2007 (<xref rid="B41" ref-type="bibr">41</xref>, <xref rid="B70" ref-type="bibr">70</xref>, <xref rid="B100" ref-type="bibr">100</xref>, <xref rid="B101" ref-type="bibr">101</xref>). These publications outlined that cancer cells undergoing apoptosis in response to specific anticancer therapies are immunogenic [a subroutine termed immunogenic cell death (ICD)], as long as they emit precise DAMPs in a spatiotemporally defined fashion (<xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B103" ref-type="bibr">103</xref>). Cells succumbing to ICD are sufficient for the elicitation of durable anti-tumor immune responses (<xref rid="B1" ref-type="bibr">1</xref>, <xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B53" ref-type="bibr">53</xref>, <xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B104" ref-type="bibr">104</xref>). ICD is indeed paralleled by the redirection and emission of DAMPs, owing to the stimulation of distinct danger signaling pathways occurring in synchrony with cell death signaling (<xref rid="B103" ref-type="bibr">103</xref>). Table <xref ref-type="table" rid="T2">2</xref> summarizes the main signaling pathways that play a role in the trafficking and emission of DAMPs. ICD-associated DAMPs and other immunostimulatory factors released by cells destined to undergo ICD favor the establishment of a productive interface between dying cancer cells and innate immune cells (like DCs or macrophages), thereby leading to the initiation of a therapeutically relevant adaptive immune response (Figure <xref ref-type="fig" rid="F1">1</xref>) (<xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B105" ref-type="bibr">105</xref>). In some contexts, DAMPs may regulate the function of specific innate immune cell subsets, e.g., following anthracycline treatment, extracellular adenosine triphosphate (ATP) assists in recruitment and differentiation of CD11c<sup>+</sup>Cd11b<sup>+</sup>Ly6C<sup>high</sup> cells into CD11c<sup>+</sup>CD86<sup>+</sup>MHCII<sup>+</sup> DCs (<xref rid="B106" ref-type="bibr">106</xref>); similarly, necrosis associated F-actin exposure activates an immune response by directing the dead cell debris to specifically CD8α<sup>+</sup> DCs (<xref rid="B59" ref-type="bibr">59</xref>, <xref rid="B107" ref-type="bibr">107</xref>). Indeed, DCs and other antigen-presenting cells exposed to cancer cells succumbing to ICD can then prime CD4<sup>+</sup> T cells (and polarize them into T<sub>H</sub>1, T<sub>H</sub>17, or T<sub>H</sub>1/T<sub>H</sub>17-like phenotype), CD8<sup>+</sup> cytotoxic T lymphocytes (CTLs) and γδ T lymphocytes against one or several TAAs (Figure <xref ref-type="fig" rid="F1">1</xref>) (<xref rid="B102" ref-type="bibr">102</xref>). Of note, residual cancer cells that survive ICD inducers can also show some enduring immunogenic characteristics that make them susceptible to immunological control by CTLs (<xref rid="B108" ref-type="bibr">108</xref>–<xref rid="B110" ref-type="bibr">110</xref>).</p><table-wrap id="T2" position="float"><label>Table 2</label><caption><p><bold>Danger signaling pathways characterized as traffickers of DAMPs</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">DAMPs</th><th valign="top" align="center" rowspan="1" colspan="1">Role of ROS</th><th valign="top" align="center" rowspan="1" colspan="1">Role of ER stress</th><th valign="top" align="center" rowspan="1" colspan="1">Role of autophagy</th><th valign="top" align="center" rowspan="1" colspan="1">Role of chaperone-mediated autophagy</th><th valign="top" align="center" rowspan="1" colspan="1">Role of secretory pathway</th><th valign="top" align="center" rowspan="1" colspan="1">Caspase activity</th><th valign="top" align="center" rowspan="1" colspan="1">Role of lysosomes</th><th valign="top" align="left" rowspan="1" colspan="1">Comments</th><th valign="top" align="center" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Secreted ATP</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">+/0</td><td valign="top" align="center" rowspan="1" colspan="1">+/0</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">+/0</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">+/0</td><td valign="top" align="left" rowspan="1" colspan="1">Underlying pathway is highly inducer dependent</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B34" ref-type="bibr">34</xref>, <xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B111" ref-type="bibr">111</xref>–<xref rid="B113" ref-type="bibr">113</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">?</td><td valign="top" align="left" rowspan="1" colspan="1">Mostly released passively on account of necrosis; only DT-EGF reported to cause active secretion so far</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B73" ref-type="bibr">73</xref>, <xref rid="B114" ref-type="bibr">114</xref>, <xref rid="B115" ref-type="bibr">115</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Secreted or surface HSP70</td><td valign="top" align="center" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="left" rowspan="1" colspan="1">ABC transporters help in endolysosomal-secretion; HSP70 has also been reported to be secreted in an exosome surface-bound format</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B116" ref-type="bibr">116</xref>–<xref rid="B122" ref-type="bibr">122</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">−/0</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">+/0</td><td valign="top" align="center" rowspan="1" colspan="1">?</td><td valign="top" align="left" rowspan="1" colspan="1">LRP1/lipid rafts mediate surface tethering; components that positively regulate surface-CRT in an inducer-dependent fashion: ERp57, PI3K p110α, BAX/BAK, cytosolic ER-Ca<sup>2+</sup>, BAP31; of note, anthracycline-induced pathway of surface CRT induction has been found to be conserved from yeast to mammals</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B34" ref-type="bibr">34</xref>, <xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B111" ref-type="bibr">111</xref>, <xref rid="B112" ref-type="bibr">112</xref>, <xref rid="B116" ref-type="bibr">116</xref>, <xref rid="B123" ref-type="bibr">123</xref>, <xref rid="B124" ref-type="bibr">124</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP90</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">?</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">+</td><td valign="top" align="center" rowspan="1" colspan="1">?</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B30" ref-type="bibr">30</xref>, <xref rid="B125" ref-type="bibr">125</xref>)</td></tr></tbody></table><table-wrap-foot><p><italic>“+” denotes ability to positively regulate trafficking; “−” denotes ability to negatively regulate trafficking; “0” denotes confirmation of no role in regulation of trafficking and “?” denotes that the role in regulating the trafficking is unknown; “+/0” denotes positive or no role in regulation of trafficking in an inducer-dependent fashion; “−/0” denotes negative or no role in regulation of trafficking in an inducer-dependent fashion</italic>.</p><p><italic>ATP, adenosine triphosphate; CRT, calreticulin; DT-EGF, epidermal growth factor receptor-targeted diphtheria toxin; ER, endoplasmic reticulum; HMGB1, high-mobility group box 1 protein; HSP, heat shock protein; LRP1, low-density lipoprotein receptor-related protein 1; ROS, reactive oxygen species</italic>.</p></table-wrap-foot></table-wrap><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold>The molecular complexity of immunogenic cell death in cancer</bold>. Cancer cells undergoing immunogenic cell death (ICD) emit danger signals for establishing a productive interface with components of the host immune system, including dendritic cells (DCs). DCs exposed to cancer cells succumbing to ICD “prime” the adaptive arm of the immune system, consisting of various effector T-cell populations, which in turn targets therapy-resistant cancer cells. Various molecules are critical for the execution of these processes. The molecular network of ICD-relevant proteins was build using the STRING modeling database (<uri xlink:type="simple" xlink:href="http://string-db.org/">http://string-db.org/</uri>) (<xref rid="B126" ref-type="bibr">126</xref>).</p></caption><graphic xlink:href="fimmu-06-00588-g001"></graphic></fig></sec><sec id="S2"><title>Immunogenic Cell Death Inducers</title><p>Over the past few years, a number of single-agent ICD inducers have been discovered, encompassing conventional chemotherapeutics, targeted anticancer agents and various other biological and physicochemical therapies (<xref rid="B18" ref-type="bibr">18</xref>, <xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B104" ref-type="bibr">104</xref>, <xref rid="B127" ref-type="bibr">127</xref>). Table <xref ref-type="table" rid="T3">3</xref> summarizes single-agent ICD inducers characterized so far, as per consensus guidelines (<xref rid="B104" ref-type="bibr">104</xref>), and the spectra of DAMPs and other immunostimulatory signals associated with them. For combinatorial therapeutic strategies capable of achieving ICD, readers may want to refer to other recent publications (<xref rid="B18" ref-type="bibr">18</xref>, <xref rid="B128" ref-type="bibr">128</xref>, <xref rid="B129" ref-type="bibr">129</xref>). It is clear that a general structure–function relationship capable of clustering all existing ICD inducers and predicting new ones does not exist (<xref rid="B130" ref-type="bibr">130</xref>), an issue that makes discovering new ICD-inducing therapies based on cheminformatic analyses challenging, if not impossible. A peculiar characteristic of most, if not all, ICD inducers is their ability to induce reactive oxygen species (ROS)-based/associated endoplasmic reticulum (ER) stress, as first delineated for anthracyclines (<xref rid="B30" ref-type="bibr">30</xref>, <xref rid="B34" ref-type="bibr">34</xref>, <xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B42" ref-type="bibr">42</xref>, <xref rid="B123" ref-type="bibr">123</xref>, <xref rid="B131" ref-type="bibr">131</xref>–<xref rid="B133" ref-type="bibr">133</xref>). This peculiarity was exploited for the targeted discovery of hypericin-based photodynamic therapy (Hyp-PDT) – a therapeutic modality that can trigger ICD through the induction of ROS that target the ER (<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B116" ref-type="bibr">116</xref>, <xref rid="B134" ref-type="bibr">134</xref>). Along with an ever more precise characterization of the links between ROS, ER stress, and ICD induction (<xref rid="B135" ref-type="bibr">135</xref>, <xref rid="B136" ref-type="bibr">136</xref>), it became clear that the more “focused” ER stress is, the higher the probability of inducing ICD (<xref rid="B3" ref-type="bibr">3</xref>, <xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B53" ref-type="bibr">53</xref>, <xref rid="B137" ref-type="bibr">137</xref>). These observations paved way for a classification system based on how ICD inducers engage ER stress for cell death and danger signaling (<xref rid="B3" ref-type="bibr">3</xref>, <xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B53" ref-type="bibr">53</xref>, <xref rid="B138" ref-type="bibr">138</xref>). Based on this classification, Type I ICD inducers are defined as anticancer agents that act on non-ER proteins for the induction of cell death, but promote collateral ER stress for danger signaling, thereby operating on multiple targets (<xref rid="B3" ref-type="bibr">3</xref>, <xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B53" ref-type="bibr">53</xref>), while Type II ICD inducers are anticancer agents that target the ER for both cell death induction and danger signaling (<xref rid="B3" ref-type="bibr">3</xref>, <xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B53" ref-type="bibr">53</xref>). Table <xref ref-type="table" rid="T4">4</xref> summarizes the classification of current ICD inducers into Type I and Type II, and their cell death/danger signaling targets. Such a classification suggest that while Type I ICD inducers can be discovered through various approaches (e.g., DAMP-based drug screening platforms) (<xref rid="B130" ref-type="bibr">130</xref>, <xref rid="B139" ref-type="bibr">139</xref>), putative Type II ICD inducers can be characterized rapidly on the basis of their ability to selectively or predominantly target the ER. Recent findings comforted the purpose and usefulness of this classification system, as two novel Type II ICD inducers [i.e., Pt<sup>II</sup> N-heterocyclic carbene complex (<xref rid="B140" ref-type="bibr">140</xref>) and Newcastle disease virotherapy (NDV) (<xref rid="B43" ref-type="bibr">43</xref>)] were identified based on the notion that they induce predominant ROS-based ER stress (<xref rid="B138" ref-type="bibr">138</xref>). Nevertheless, as more ICD inducers and features are discovered, this classification system is expected to evolve or be substituted by a more refined one.</p><table-wrap id="T3" position="float"><label>Table 3</label><caption><p><bold>A list of prominent single-agent immunogenic cell death (ICD) inducers in cancer and their specific associations with danger signaling and other immunostimulatory signaling</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">ICD inducers</th><th valign="top" align="center" colspan="2" rowspan="1">Associated ICD-relevant DAMPs<hr></hr></th><th valign="top" align="left" rowspan="1" colspan="1">Other immunostimulatory activities or danger signals and other comments on immunomodulatory activity</th><th valign="top" align="center" rowspan="1" colspan="1">Reference</th></tr><tr><th valign="top" align="left" rowspan="1" colspan="1"></th><th valign="top" align="left" rowspan="1" colspan="1">DAMP</th><th valign="top" align="left" rowspan="1" colspan="1">Stage of cell death</th><th valign="top" align="left" rowspan="1" colspan="1"></th><th valign="top" align="left" rowspan="1" colspan="1"></th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines (epirubicin, doxorubicin, idarubicin, mitoxantrone), oxaliplatin, UVC radiation and radiotherapy</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT<break></break>Surface HSP70<break></break>Secreted ATP<break></break>Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Pre-apoptotic<break></break>Mid-apoptotic<break></break>Early/mid-apoptotic<break></break>Post-apoptotic</td><td valign="top" align="left" rowspan="1" colspan="1">Activation of Type I IFN response comprising MX-1 centered signature, consisting of IFN-α/β and CXCL10; surface exposure of mannose-6-phopshate receptor, which enables better interface with CTLs and facilitates GZMB-mediated cell death; radiotherapy is known to increase expression levels of various antigens in number of cancer models as well as induce “abscopal effect” in both preclinical and clinical models; overall <italic>CALR</italic> levels were predictive of prolonged OS in radiotherapy-treated lung cancer patients</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B42" ref-type="bibr">42</xref>, <xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B127" ref-type="bibr">127</xref>, <xref rid="B141" ref-type="bibr">141</xref>–<xref rid="B144" ref-type="bibr">144</xref>)</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">Anti-EGFR antibody – 7A7</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Pre-apoptotic</td><td valign="top" align="left" rowspan="3" colspan="1">–</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B145" ref-type="bibr">145</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP70</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP90</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">Bleomycin</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Mid/post-apoptotic</td><td valign="top" align="left" rowspan="3" colspan="1">Induces ambivalent immune response, i.e., all valid ICD markers but also increased Treg differentiation and, thus, a good candidate for anti-Treg combinatorial therapy</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B146" ref-type="bibr">146</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Secreted ATP</td><td valign="top" align="left" rowspan="1" colspan="1">Mid/post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">Bortezomib</td><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP90</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td><td valign="top" align="left" rowspan="3" colspan="1">–</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B66" ref-type="bibr">66</xref>, <xref rid="B100" ref-type="bibr">100</xref>, <xref rid="B127" ref-type="bibr">127</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP70</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">Oncolytic Adenovirus</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="3" colspan="1">?</td><td valign="top" align="left" rowspan="3" colspan="1">Immunogenicity of these viruses can be further increased by producing transgenic versions producing CD40L or GM-CSF</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B147" ref-type="bibr">147</xref>, <xref rid="B148" ref-type="bibr">148</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released ATP</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td></tr><tr><td valign="top" align="left" rowspan="4" colspan="1"><italic>Clostridium difficile</italic> toxin B</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td><td valign="top" align="left" rowspan="4" colspan="1">–</td><td valign="top" align="center" rowspan="4" colspan="1">(<xref rid="B149" ref-type="bibr">149</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released ATP</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HSP70/90</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">Coxsackievirus B3 (CVB3)<sup>#</sup></td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early-apoptotic</td><td valign="top" align="left" rowspan="3" colspan="1">–</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B150" ref-type="bibr">150</xref>, <xref rid="B151" ref-type="bibr">151</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Secreted ATP</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="2" colspan="1">Cyclophosphamide</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Pre-apoptotic</td><td valign="top" align="left" rowspan="2" colspan="1">Facilitates an interface between gut microbiota (leaked due to gut perforation) and host immune system thereby allowing Th17 cells-dependent anti-tumor immune responses; cyclophosphamide’s effects on anti-tumor immunity are strongly dose dependent. High doses of this chemotherapeutic can be immunosuppressive yet low or metronomic doses facilitate anti-tumor immunity through targeted depletion of Tregs/MDSCs. In ICD set-up, a low dose (100 mg/kg in mice) of cyclophosphamide was shown to exert anti-tumor immunity</td><td valign="top" align="center" rowspan="2" colspan="1">(<xref rid="B18" ref-type="bibr">18</xref>, <xref rid="B152" ref-type="bibr">152</xref>, <xref rid="B153" ref-type="bibr">153</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="5" colspan="1">High hydrostatic pressure</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td><td valign="top" align="left" rowspan="5" colspan="1">–</td><td valign="top" align="center" rowspan="5" colspan="1">(<xref rid="B154" ref-type="bibr">154</xref>–<xref rid="B156" ref-type="bibr">156</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP70</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP90</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Secreted ATP</td><td valign="top" align="left" rowspan="1" colspan="1">Mid/post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Mid/post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="7" colspan="1">Hypericin-based PDT</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Pre-apoptotic</td><td valign="top" align="left" rowspan="7" colspan="1">High accumulation of OAMPs like protein carbonyls; down-regulates CD47; induces up-regulation of various molecules associated with Type I IFN response (<italic>IRF7</italic>, <italic>IRF1</italic>, <italic>OASL, IL18, CXCL2, IL15, IL8</italic>) but not IFN-α secretion</td><td valign="top" align="center" rowspan="7" colspan="1">(<xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B30" ref-type="bibr">30</xref>, <xref rid="B34" ref-type="bibr">34</xref>, <xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B112" ref-type="bibr">112</xref>, <xref rid="B116" ref-type="bibr">116</xref>, <xref rid="B157" ref-type="bibr">157</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP70</td><td valign="top" align="left" rowspan="1" colspan="1">Pre-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP90</td><td valign="top" align="left" rowspan="1" colspan="1">Pre-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Secreted ATP</td><td valign="top" align="left" rowspan="1" colspan="1">Pre-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HSP70/90</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">Microwave thermal ablation</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="3" colspan="1">?</td><td valign="top" align="left" rowspan="3" colspan="1">–</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B158" ref-type="bibr">158</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Secreted ATP</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td></tr><tr><td valign="top" align="left" rowspan="2" colspan="1">Newcastle disease virus (NDV)</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-necroptotic</td><td valign="top" align="left" rowspan="2" colspan="1">Increases expression levels of PMEL17 antigen in glioma cells; NDV treatment has also been shown to induce “abscopal effect” in a murine melanoma model</td><td valign="top" align="center" rowspan="2" colspan="1">(<xref rid="B43" ref-type="bibr">43</xref>, <xref rid="B159" ref-type="bibr">159</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-necroptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Paclitaxel</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT<break></break>Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic<break></break>Post-apoptotic</td><td valign="top" align="left" rowspan="1" colspan="1">Overall <italic>CALR</italic> levels were predictive of prolonged OS or PFS in paclitaxel-treated ovarian cancer patients thereby establishing clinical validity of ICD in paclitaxel treatment set-up; paclitaxel has also been reported to enhance overall antigen levels</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B42" ref-type="bibr">42</xref>, <xref rid="B144" ref-type="bibr">144</xref>, <xref rid="B160" ref-type="bibr">160</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Patupilone</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B128" ref-type="bibr">128</xref>)</td></tr><tr><td valign="top" align="left" rowspan="5" colspan="1">Photofrin-based PDT</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td><td valign="top" align="left" rowspan="5" colspan="1">The only anticancer modality for which a comparison between DAMPs induced by <italic>in vitro</italic> versus <italic>in vivo</italic> treatment was carried out – however, none of ICD-related DAMPs were tested</td><td valign="top" align="center" rowspan="5" colspan="1">(<xref rid="B47" ref-type="bibr">47</xref>, <xref rid="B161" ref-type="bibr">161</xref>–<xref rid="B164" ref-type="bibr">164</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP70/60</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface ceramide</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface S1P</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">Pt<sup>II</sup> N-heterocyclic carbene complex</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Pre-apoptotic</td><td valign="top" align="left" rowspan="3" colspan="1">–</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B140" ref-type="bibr">140</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released ATP</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">RIG-I-like helicases (RLH) ligand</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early-apoptotic</td><td valign="top" align="left" rowspan="3" colspan="1">Induces Type I IFN response</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B165" ref-type="bibr">165</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HSP70</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">Septacidin</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Pre-apoptotic</td><td valign="top" align="left" rowspan="3" colspan="1">–</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B139" ref-type="bibr">139</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Secreted ATP</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="2" colspan="1">Shikonin</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td><td valign="top" align="left" rowspan="2" colspan="1">Also, causes surface exposure of GRP78 a prominent inducer of pro-tumorigenic effects; enhances overall cancer antigen levels</td><td valign="top" align="center" rowspan="2" colspan="1">(<xref rid="B160" ref-type="bibr">160</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Surface HSP70</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">Vorinostat</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early/mid-apoptotic</td><td valign="top" align="left" rowspan="3" colspan="1">–</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B166" ref-type="bibr">166</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Secreted ATP</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="3" colspan="1">Wogonin</td><td valign="top" align="left" rowspan="1" colspan="1">Surface CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Early-apoptotic</td><td valign="top" align="left" rowspan="3" colspan="1">Surface-Annexin A1 is also induced by wogonin. In an ICD set-up, the role of Annexin A1 is not clear since it is a noted anti-inflammatory factor</td><td valign="top" align="center" rowspan="3" colspan="1">(<xref rid="B167" ref-type="bibr">167</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released ATP</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Released HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Post-apoptotic</td></tr></tbody></table><table-wrap-foot><p><italic>CRT or <italic>CALR</italic>, calreticulin; CTLs, cytotoxic T lymphocytes; DAMPs, damage-associated molecular patterns; EGFR, epidermal growth factor receptor; GZMB, granzyme B; HMGB1, high-mobility group box-1 protein; HSP, heat shock protein; ICD, immunogenic cell death; IFN, interferon; MDSC, myeloid-derived suppressor cells; OAMPs, oxidation-associated molecular patterns; OS, overall survival; PFS, progression-free survival</italic>.</p><p><italic>Important note: It is worth noting that recently various promising candidate therapies have emerged that induce <italic>in vitro</italic> DAMPs relevant for ICD, e.g., Rose Bengal-based PDT (<xref rid="B168" ref-type="bibr">168</xref>), Docosahexaenoic acid (<xref rid="B169" ref-type="bibr">169</xref>), and Capsaicin (<xref rid="B170" ref-type="bibr">170</xref>, <xref rid="B171" ref-type="bibr">171</xref>). Such agents may emerge as potent inducers of ICD in future, however, in order to establish them as inducers of ICD-like immunogenicity, it is imperative to confirm their (i.e., cancer cells treated with these agents) ability to stimulate T cells (<italic>in vitro</italic> or <italic>in vivo</italic>) and/or induce anti-cancer vaccination effect, <italic>in vivo</italic>, as per the consensus guidelines (<xref rid="B104" ref-type="bibr">104</xref>)</italic>.</p><p><italic>Glossary: In the current setting, it is crucial to differentiate between the meanings of the words, “immunogenic” and “immunogenicity” as they are not supposed to have inter-changeable meanings. <italic>Immunogenic</italic>, derives from the word <italic>immunogen</italic>, which refers to any substance that can elicit an immune response; this includes, whole cells or organisms (eukaryotic or prokaryotic), specific cellular entities or specific proteins (e.g., antigens) (<xref rid="B172" ref-type="bibr">172</xref>). On the other hand, <italic>immunogenicity</italic> is a much more specific terms that is closer to <italic>antigenicity</italic> in operational sense, since it refers to the ability of a specific entity (e.g., an antigen or an epitope) to be recognized by the immune system through binding interactions with T or B cells, which may or may not result in an overt immunological response (<xref rid="B4" ref-type="bibr">4</xref>, <xref rid="B11" ref-type="bibr">11</xref>)</italic>.</p><p><italic>“?” Unclear or not determined yet</italic>.</p><p><italic>“#” Unconfirmed anti-tumour immune responses in adaptive immune system-competent</italic>.</p></table-wrap-foot></table-wrap><table-wrap id="T4" position="float"><label>Table 4</label><caption><p><bold>Classification of ICD inducers into Type I and Type II based on their ER or non-ER-targeting <italic>modus operandi</italic></bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">ICD inducer</th><th valign="top" align="left" rowspan="1" colspan="1">Site of Cell-death inducing effects</th><th valign="top" align="left" rowspan="1" colspan="1">Site of danger signaling induction</th><th valign="top" align="center" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td valign="top" align="left" colspan="4" rowspan="1"><bold>Type I inducers – agents that induce icd through a “collateral” er stress effect</bold></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines (epirubicin, doxorubicin, idarubicin, mitoxantrone), oxaliplatin, UVC radiation and radiotherapy</td><td valign="top" align="left" rowspan="1" colspan="1">Nucleus (DNA or the DNA replication machinery proteins)</td><td valign="top" align="left" rowspan="1" colspan="1">ER, autophagy, pannexin channels, lysosomes</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B36" ref-type="bibr">36</xref>, <xref rid="B41" ref-type="bibr">41</xref>, <xref rid="B70" ref-type="bibr">70</xref>, <xref rid="B111" ref-type="bibr">111</xref>, <xref rid="B130" ref-type="bibr">130</xref>, <xref rid="B173" ref-type="bibr">173</xref>, <xref rid="B174" ref-type="bibr">174</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Anti-EGFR antibody – 7A7</td><td valign="top" align="left" rowspan="1" colspan="1">Cell surface (epidermal growth factor receptor or EGFR)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B145" ref-type="bibr">145</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Bleomycin</td><td valign="top" align="left" rowspan="1" colspan="1">Nucleus (causes DNA strand-breaks)</td><td valign="top" align="left" rowspan="1" colspan="1">ER?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B146" ref-type="bibr">146</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Bortezomib</td><td valign="top" align="left" rowspan="1" colspan="1">Cytosol (26S proteasome or ERAD machinery; CIP2A/cancerous inhibitor of protein phosphatase 2A)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B100" ref-type="bibr">100</xref>, <xref rid="B175" ref-type="bibr">175</xref>, <xref rid="B176" ref-type="bibr">176</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Clostridium difficile</italic> toxin B</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoskeleton (causes cytoskeletal disruption by targeting RhoA, CDC42 and Rac1)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B149" ref-type="bibr">149</xref>, <xref rid="B177" ref-type="bibr">177</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Cyclophosphamide</td><td valign="top" align="left" rowspan="1" colspan="1">Nucleus (DNA)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B152" ref-type="bibr">152</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">High hydrostatic pressure</td><td valign="top" align="left" rowspan="1" colspan="1">Broad disrupting/denaturing effects on membranes, and proteins</td><td valign="top" align="left" rowspan="1" colspan="1">ER (mitochondria?)</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B154" ref-type="bibr">154</xref>, <xref rid="B178" ref-type="bibr">178</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Microwave thermal ablation</td><td valign="top" align="left" rowspan="1" colspan="1">Hyperthermic ablation of cellular components</td><td valign="top" align="left" rowspan="1" colspan="1">ER?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B158" ref-type="bibr">158</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Paclitaxel, patupilone</td><td valign="top" align="left" rowspan="1" colspan="1">Cytoskeleton (target microtubules thereby disrupting cytoskeletal functions)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B42" ref-type="bibr">42</xref>, <xref rid="B104" ref-type="bibr">104</xref>, <xref rid="B179" ref-type="bibr">179</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Photofrin-based PDT</td><td valign="top" align="left" rowspan="1" colspan="1">Cellular membranes (ROS-based damage of membranes)</td><td valign="top" align="left" rowspan="1" colspan="1">ER?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B180" ref-type="bibr">180</xref>, <xref rid="B181" ref-type="bibr">181</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">RIG-I-like helicases (RLH) ligand</td><td valign="top" align="left" rowspan="1" colspan="1">Cytosol (targets RIG-I-like helicases)</td><td valign="top" align="left" rowspan="1" colspan="1">ER?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B165" ref-type="bibr">165</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Septacidin</td><td valign="top" align="left" rowspan="1" colspan="1">?</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B139" ref-type="bibr">139</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Shikonin</td><td valign="top" align="left" rowspan="1" colspan="1">Cytosol (tumor-specific pyruvate kinase-M2 protein)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B160" ref-type="bibr">160</xref>, <xref rid="B182" ref-type="bibr">182</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Vorinostat</td><td valign="top" align="left" rowspan="1" colspan="1">Nucleus/Cytosol (targets histone deacetylase)</td><td valign="top" align="left" rowspan="1" colspan="1">ER?</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B166" ref-type="bibr">166</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Wogonin</td><td valign="top" align="left" rowspan="1" colspan="1">Mitochondria (generates mitochondria-derived ROS)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B167" ref-type="bibr">167</xref>, <xref rid="B183" ref-type="bibr">183</xref>)</td></tr><tr><td valign="top" align="left" colspan="4" rowspan="1"><bold>Type II inducers – agents that induce icd through a “focused” er stress effect</bold></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Hypericin-based PDT</td><td valign="top" align="left" rowspan="1" colspan="1">ER (ROS-based damage at the ER membrane)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B63" ref-type="bibr">63</xref>, <xref rid="B116" ref-type="bibr">116</xref>, <xref rid="B181" ref-type="bibr">181</xref>, <xref rid="B184" ref-type="bibr">184</xref>, <xref rid="B185" ref-type="bibr">185</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Oncolytic adenovirus</td><td valign="top" align="left" rowspan="1" colspan="1">ER (ER membranes and lumen)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B104" ref-type="bibr">104</xref>, <xref rid="B147" ref-type="bibr">147</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Oncolytic coxsackievirus B3 (CVB3)</td><td valign="top" align="left" rowspan="1" colspan="1">ER (ER membranes and lumen)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B150" ref-type="bibr">150</xref>, <xref rid="B186" ref-type="bibr">186</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Oncolytic Newcastle disease virus (NDV)</td><td valign="top" align="left" rowspan="1" colspan="1">ER (ER membranes and lumen)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B43" ref-type="bibr">43</xref>, <xref rid="B159" ref-type="bibr">159</xref>, <xref rid="B187" ref-type="bibr">187</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Pt<sup>II</sup> N-heterocyclic carbene complex</td><td valign="top" align="left" rowspan="1" colspan="1">Predominantly targets ER (generates ER-directed ROS)</td><td valign="top" align="left" rowspan="1" colspan="1">ER</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B140" ref-type="bibr">140</xref>)</td></tr></tbody></table><table-wrap-foot><p><italic>EGFR, epidermal growth factor receptor; ER, endoplasmic reticulum; ICD, immunogenic cell death; PDT, photodynamic therapy; ROS, reactive oxygen species</italic>.</p><p><italic>“?” Unclear or not determined yet</italic>.</p></table-wrap-foot></table-wrap><p>Since its discovery, a plethora of molecular and immunological components responsible for ICD have been discovered (Figure <xref ref-type="fig" rid="F1">1</xref>) (<xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B188" ref-type="bibr">188</xref>). Table <xref ref-type="table" rid="T5">5</xref> summarizes the molecular and immunological determinants of ICD characterized so far, as well as the models of ICD in which they operate (in a positive, negative or dispensable manner). Anthracyclines and oxaliplatin are the most common ICD inducers employed in experimental settings, followed by Hyp-PDT. According to current understanding, cancer cell-associated determinants of ICD can be subdivided into those that are common to all ICD inducers (i.e., “core” signaling components), and those that operate in an ICD inducer-dependent manner (i.e., “private” signaling components) (<xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B189" ref-type="bibr">189</xref>). Thus, eukaryotic translation initiation factor 2-alpha kinase 3 (EIF2AK3, best known as PERK) and the ER-to-Golgi secretory machinery are considered “core” signaling components on the cancer cell side (<xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B102" ref-type="bibr">102</xref>). Similarly, from the immune system side, a general role for (IFNγ-producing) CD4<sup>+</sup> and CD8<sup>+</sup> T cells has been confirmed for most, if not all, ICD inducers (Table <xref ref-type="table" rid="T5">5</xref>). Interestingly, some components that are required for ICD induction by some agents (like autophagy for anthracyclines and oxaliplatin) (<xref rid="B190" ref-type="bibr">190</xref>) might be either dispensable for ICD induction by other agents, e.g., autophagy for NDV (<xref rid="B43" ref-type="bibr">43</xref>) and phosphorylation of eukaryotic translation initiation factor 2α (eIF2α), caspase-8 (CASP8) activation or cytosolic Ca<sup>2+</sup> levels for Hyp-PDT (<xref rid="B35" ref-type="bibr">35</xref>); or even negatively regulate ICD in some settings, e.g., autophagy in case of Hyp-PDT (<xref rid="B34" ref-type="bibr">34</xref>) (Table <xref ref-type="table" rid="T5">5</xref>). Thus, it will be important to expand our molecular knowledge of ICD to as many experimental settings as possible.</p><table-wrap id="T5" position="float"><label>Table 5</label><caption><p><bold>A list of molecular and immunological components crucial for regulation of ICD</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">Molecular or immunological components</th><th valign="top" align="left" rowspan="1" colspan="1">Acting on the level of?</th><th valign="top" align="center" colspan="3" rowspan="1">Role in regulating ICD or ICD-related determinants for various therapies/inducers<hr></hr></th><th valign="top" align="left" rowspan="1" colspan="1">Confirmed by which experimental intervention?</th><th valign="top" align="left" rowspan="1" colspan="1">Reference</th></tr><tr><th valign="top" align="left" rowspan="1" colspan="1"></th><th valign="top" align="left" rowspan="1" colspan="1"></th><th valign="top" align="left" rowspan="1" colspan="1">Positive regulation</th><th valign="top" align="left" rowspan="1" colspan="1">Negative regulation</th><th valign="top" align="left" rowspan="1" colspan="1">No role in regulation</th><th valign="top" align="left" rowspan="1" colspan="1"></th><th valign="top" align="left" rowspan="1" colspan="1"></th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Actin cytoskeleton</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines, hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Pharmacological inhibitors of actin polymerization</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B123" ref-type="bibr">123</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">ATG5, ATG7, or BECN1</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines, oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">Hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">Newcastle disease virotherapy</td><td valign="top" align="left" rowspan="1" colspan="1">ATG5, ATG7 or BECN1 si/shRNA, ATG5 KO MEFs, or transgenic mice model of spontaneous melanoma with <italic>Atg7</italic><sup>−/−</sup> phenotype or pharmacological inhibitors of macroautophagy</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B34" ref-type="bibr">34</xref>, <xref rid="B43" ref-type="bibr">43</xref>, <xref rid="B112" ref-type="bibr">112</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">BAX/BAK</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines, hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">BAX/BAK KO MEFs or Bax/Bak si/shRNA</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B123" ref-type="bibr">123</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Calreticulin</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines, radiotherapy, oxaliplatin, hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">CRT si/shRNA</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B41" ref-type="bibr">41</xref>, <xref rid="B116" ref-type="bibr">116</xref>, <xref rid="B123" ref-type="bibr">123</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Caspase 1</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Casp1</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B36" ref-type="bibr">36</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Caspase-8</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">Caspase-8 si/shRNA or HeLa cancer cells expressing CrmA (a caspase-8 inhibitory protein)</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B123" ref-type="bibr">123</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">CD4<sup>+</sup>/CD8<sup>+</sup> T cells</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin, hypericin-PDT, high hydrostatic pressure, bortezomib, vorinostat, photofrin-PDT, Newcastle disease virotherapy, cyclophosphamide</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Antibody-based depletion; <italic>Ex vivo</italic> co-culture experiments</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B34" ref-type="bibr">34</xref>, <xref rid="B43" ref-type="bibr">43</xref>, <xref rid="B100" ref-type="bibr">100</xref>, <xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B152" ref-type="bibr">152</xref>, <xref rid="B161" ref-type="bibr">161</xref>, <xref rid="B162" ref-type="bibr">162</xref>, <xref rid="B166" ref-type="bibr">166</xref>, <xref rid="B191" ref-type="bibr">191</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">CXCL10</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Recombinant protein</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B141" ref-type="bibr">141</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">CXCR3</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Cxcr3</italic><sup>−/−</sup> mice or antibody-based blockade</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B141" ref-type="bibr">141</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">eIF2α-P</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">MEFs expressing non-phosphorylable version of eIF2α-P, salubrinal or pharmacological inhibitors of GADD34</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B123" ref-type="bibr">123</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">ER-Ca<sup>2+</sup></td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">BAPTA, a Ca<sup>2+</sup> chelator or Reticulon-1C overexpression;</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">ERp57</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">ERp57 si/shRNA or ERp57 KO MEFs</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B116" ref-type="bibr">116</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">ER-to-Golgi transport</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines, hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Brefeldin A, a secretory pathway inhibitor</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B123" ref-type="bibr">123</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">HMGB1</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">HMGB1 si/shRNA</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B70" ref-type="bibr">70</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">HSP90</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Bortezomib</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Pharmacological HSP90 inhibitors</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B66" ref-type="bibr">66</xref>, <xref rid="B67" ref-type="bibr">67</xref>, <xref rid="B100" ref-type="bibr">100</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">HSP70</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Shikonin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Antibody-mediated protein depletion</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B192" ref-type="bibr">192</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">IFN-α/β or IFN-α-receptor</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines, cyclophosphamide, and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Antibody-based blockade or recombinant proteins (wherever applicable)</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B141" ref-type="bibr">141</xref>, <xref rid="B152" ref-type="bibr">152</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">IFN-γ and IFN-γ-receptor</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Ifng</italic><sup>−/−</sup> or <italic>Ifngr1</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B70" ref-type="bibr">70</xref>, <xref rid="B102" ref-type="bibr">102</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">IL17A or IL17A-receptor</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Il17a</italic><sup>−/−</sup> or <italic>Il17ra</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B36" ref-type="bibr">36</xref>, <xref rid="B193" ref-type="bibr">193</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">IL1-receptor</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Il1r1</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B36" ref-type="bibr">36</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">IL-1β</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Antibody-based blockade</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B36" ref-type="bibr">36</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Lipid rafts</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Mitoxantrone</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">Hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">MBC, a cholesterol-chelator that disrupts lipid rafts</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">LRP1</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Mitoxantrone, hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">LRP1 shRNA, LRP1 KO MEFs, LRP1 KO CHO cells and LRP1 overexpression in CHO cells</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">LY96 and MyD88 (TLR-adaptors)</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Ly96</italic><sup>−/−</sup> or <italic>Myd88</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B102" ref-type="bibr">102</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">NLRP3</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Nlrp3</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B36" ref-type="bibr">36</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">P2 × 7 receptor</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>P2rx7</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B36" ref-type="bibr">36</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Perforin</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Prf1</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B36" ref-type="bibr">36</xref>, <xref rid="B70" ref-type="bibr">70</xref>, <xref rid="B102" ref-type="bibr">102</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">PERK</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines, hypericin-PDT, wogonin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">PERK si/shRNA, PERK KO MEFs</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B123" ref-type="bibr">123</xref>, <xref rid="B167" ref-type="bibr">167</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">PI3K p110α</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines, hypericin-PDT, wogonin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">PI3K p110α shRNA or wortmannin, a pharmacological inhibitor</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B35" ref-type="bibr">35</xref>, <xref rid="B167" ref-type="bibr">167</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Rag2</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin, vorinostat, cyclophosphamide, photofrin-PDT, Newcastle disease virotherapy</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Rag2</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B43" ref-type="bibr">43</xref>, <xref rid="B70" ref-type="bibr">70</xref>, <xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B152" ref-type="bibr">152</xref>, <xref rid="B161" ref-type="bibr">161</xref>, <xref rid="B162" ref-type="bibr">162</xref>, <xref rid="B166" ref-type="bibr">166</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">STAT3</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Stat3</italic><sup>−/−</sup> cancer cells</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B194" ref-type="bibr">194</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">TLR3</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">TLR3 si/shRNA or <italic>Tlr3</italic><sup>−/−</sup> cancer cells</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B141" ref-type="bibr">141</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">TLR4</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Tlr4</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B70" ref-type="bibr">70</xref>, <xref rid="B102" ref-type="bibr">102</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">TNF or TNF-receptor</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines and/or oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>Tnf</italic><sup>−/−</sup> or <italic>Tnfr1</italic><sup>−/−</sup> mice</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B102" ref-type="bibr">102</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">LAMP2A</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cells?</td><td valign="top" align="left" rowspan="1" colspan="1">Mitoxantrone and hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">LAMP2A KO MEFs</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B112" ref-type="bibr">112</xref>)</td></tr></tbody></table><table-wrap-foot><p><italic>ATG, autophagy-related protein; BECN1, beclin-1; CD, cluster of differentiation; CRT, calreticulin; CXCL, C-X-C ligand; CXCR, C-X-C motif receptor; eIF2, eukaryotic initiation factor 2; ER, endoplasmic reticulum; ERp57, endoplasmic reticulum protein 57; HMGB1, high-mobility group box 1; HSP, heat shock protein; Hyp-PDT, hypericin-based photodynamic therapy; ICD, immunogenic cell death; IFN, interferon; IL, interleukin; KO MEFs, knock-out murine embryonic fibroblasts; LAMP, lysosome-associated membrane glycoprotein; LRP1, low-density lipoprotein receptor-related protein 1; MBC, methyl-β-cyclodextrin; NLRP3, NOD-like receptor family, pyrin domain containing 3; PERK, protein kinase RNA-like endoplasmic reticulum kinase; PI3K, phosphoinositide 3-kinase; PRF, perforin; TLR, toll-like receptor; TNF, tumor necrosis factor</italic>.</p></table-wrap-foot></table-wrap></sec><sec id="S3"><title>Immunogenic Cell Death from Bench to Bedside</title><p>The relevance of ICD has been verified in a number of rodent models, with a variety of chemical and physicochemical ICD inducers (<xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B102" ref-type="bibr">102</xref>). Table <xref ref-type="table" rid="T6">6</xref> summarizes the most prominent mouse or rat models used so far for the characterization and study of ICD. For the moment, ICD has been mostly investigated in heterotopic syngeneic subcutaneous models (<xref rid="B195" ref-type="bibr">195</xref>). Within such models, inter-species differences (mouse <italic>versus</italic> rats), inter-strain differences (among BALB/c, C57BL/6, C3H and KMF mice), and inter-cell line differences, as well as differences in therapeutic setups (prophylactic <italic>versus</italic> curative) have been amply accounted for (Table <xref ref-type="table" rid="T6">6</xref>). Nevertheless, there is predominance in the use of cancer cells derived from carcinogen-induced tumors and transplanted subcutaneously (Table <xref ref-type="table" rid="T6">6</xref>). In very few cases, ICD has been characterized in either orthotopic (for NDV) or spontaneous (for anthracyclines) tumor murine models (Table <xref ref-type="table" rid="T6">6</xref>). This has been questioned as a prominent Achilles’ heel of ICD research (<xref rid="B195" ref-type="bibr">195</xref>). While this criticism is valid, it has to be recognized that no rodent model is perfect at all immunological levels (<xref rid="B196" ref-type="bibr">196</xref>).</p><table-wrap id="T6" position="float"><label>Table 6</label><caption><p><bold>A list of prominent preclinical mice or rat models used for analysis of ICD</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">ICD inducer</th><th valign="top" align="center" colspan="4" rowspan="1">Mice tumor models utilized for positive ICD characterization or ICD “restoration/rescue” analysis<hr></hr></th></tr><tr><th valign="top" align="left" rowspan="1" colspan="1"></th><th valign="top" align="left" rowspan="1" colspan="1">Heterotopic subcutaneous mice or rat models</th><th valign="top" align="left" rowspan="1" colspan="1">Orthotopic mice models</th><th valign="top" align="left" rowspan="1" colspan="1">Spontaneous tumor mice models</th><th valign="top" align="left" rowspan="1" colspan="1">Carcinogen-induced tumor models</th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines</td><td valign="top" align="left" rowspan="1" colspan="1">CT26 cells in BALB/c mice – prophylactic immunization model (<xref rid="B41" ref-type="bibr">41</xref>, <xref rid="B70" ref-type="bibr">70</xref>, <xref rid="B111" ref-type="bibr">111</xref>, <xref rid="B123" ref-type="bibr">123</xref>, <xref rid="B197" ref-type="bibr">197</xref>) and curative tumor model (<xref rid="B41" ref-type="bibr">41</xref>, <xref rid="B70" ref-type="bibr">70</xref>, <xref rid="B111" ref-type="bibr">111</xref>, <xref rid="B197" ref-type="bibr">197</xref>); MCA205 cells in C57BL/6 mice – prophylactic immunization and curative tumor model (<xref rid="B36" ref-type="bibr">36</xref>, <xref rid="B70" ref-type="bibr">70</xref>, <xref rid="B111" ref-type="bibr">111</xref>, <xref rid="B130" ref-type="bibr">130</xref>); MCA-2/-4 cells in C57BL/6 mice – curative tumor model (<xref rid="B36" ref-type="bibr">36</xref>); D122 cells in C57BL/6 mice – prophylactic immunization model (<xref rid="B145" ref-type="bibr">145</xref>); AY27 cells in Fischer 344 rats – prophylactic immunization model (<xref rid="B42" ref-type="bibr">42</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">MMTV-<italic>Neu</italic>T breast cancer mice model – curative set-up (<xref rid="B198" ref-type="bibr">198</xref>); <italic>Braf</italic><sup>Ca/+</sup>; <italic>Pten</italic><sup>fl/fl</sup>-melanoma mice model – curative set-up (<xref rid="B199" ref-type="bibr">199</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Anti-EGFR antibody (7A7)</td><td valign="top" align="left" rowspan="1" colspan="1">D122 cells in C57BL/6 mice – curative tumor model and prophylactic immunization model (<xref rid="B145" ref-type="bibr">145</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Bleomycin</td><td valign="top" align="left" rowspan="1" colspan="1">CT26 cells in BALB/c mice – curative tumor model (<xref rid="B146" ref-type="bibr">146</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Bortezomib</td><td valign="top" align="left" rowspan="1" colspan="1">67NR cells in BALB/c mice – prophylactic immunization model with use of stimulated DCs (<xref rid="B200" ref-type="bibr">200</xref>); B16 cells in C57BL/6 mice – curative tumor model, combination treatment with AdVMART1/DC and bortezomib is significantly better than bortezomib alone (<xref rid="B201" ref-type="bibr">201</xref>); HM-1 cells in C57BL/6 x C3/He F<sub>1</sub> origin mice – prophylactic immunization model (<xref rid="B202" ref-type="bibr">202</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">CD40L-encoding Oncolytic Adenovirus</td><td valign="top" align="left" rowspan="1" colspan="1">MB49 cells in C57BL/6 mice – curative tumor model (<xref rid="B147" ref-type="bibr">147</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Clostridium difficile</italic> toxin B</td><td valign="top" align="left" rowspan="1" colspan="1">CT26 cells in BALB/c mice – prophylactic immunization model (<xref rid="B149" ref-type="bibr">149</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Coxsackievirus B3</td><td valign="top" align="left" rowspan="1" colspan="1">A549 and EBC-1 cells in nude BALB/c mice – curative tumor model (<xref rid="B150" ref-type="bibr">150</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Cyclophosphamide</td><td valign="top" align="left" rowspan="1" colspan="1">EG7 cells in C57BL/6 mice (<xref rid="B152" ref-type="bibr">152</xref>); AB1-HA cells in BALB/c mice – curative tumor model followed by resistance to challenge with live cells (<xref rid="B203" ref-type="bibr">203</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Hypericin-based PDT</td><td valign="top" align="left" rowspan="1" colspan="1">CT26 cells in BALB/c mice – prophylactic immunization model (<xref rid="B35" ref-type="bibr">35</xref>); – curative tumor model (<xref rid="B184" ref-type="bibr">184</xref>); AY27 cells in Fischer 344 rats – prophylactic immunization model (<xref rid="B42" ref-type="bibr">42</xref>); B78 cells in C57BL/6 mice – prophylactic immunization model (<xref rid="B30" ref-type="bibr">30</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Microwave thermal ablation</td><td valign="top" align="left" rowspan="1" colspan="1">K7M2 cells in BALB/c mice or UMR106 cells in SD rats – prophylactic immunization model (<xref rid="B158" ref-type="bibr">158</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Newcastle disease virus (NDV)</td><td valign="top" align="left" rowspan="1" colspan="1">B16 cells in C57BL/6 mice – curative tumor model (<xref rid="B159" ref-type="bibr">159</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">GL261 cells in C57BL/6 mice – curative tumor model (<xref rid="B43" ref-type="bibr">43</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">CT26 cells in BALB/c mice – prophylactic immunization model (<xref rid="B123" ref-type="bibr">123</xref>, <xref rid="B197" ref-type="bibr">197</xref>); – curative tumor model (<xref rid="B197" ref-type="bibr">197</xref>); EL4 cells in C57BL/6 mice – curative tumor model (<xref rid="B36" ref-type="bibr">36</xref>); EG7 cells in C57BL/6 mice – curative tumor model (<xref rid="B36" ref-type="bibr">36</xref>); EG7 cells in C3H mice – prophylactic immunization model (<xref rid="B70" ref-type="bibr">70</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Photofrin-based PDT</td><td valign="top" align="left" rowspan="1" colspan="1">EMT6 cells in BALB/c mice – curative tumor model (<xref rid="B161" ref-type="bibr">161</xref>); SCCVII cells in C3H/HeN mice – curative tumor model (<xref rid="B162" ref-type="bibr">162</xref>, <xref rid="B163" ref-type="bibr">163</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Radiotherapy</td><td valign="top" align="left" rowspan="1" colspan="1">CT26 cells in BALB/c – prophylactic immunization model (<xref rid="B204" ref-type="bibr">204</xref>); 410.4 cells in BALB/c mice – prophylactic immunization model (<xref rid="B205" ref-type="bibr">205</xref>); EG7 cells in C57BL/6 mice and SCC VII cells in C3H mice – prophylactic immunization model (<xref rid="B206" ref-type="bibr">206</xref>); B16F10 cells in C57BL/6 mice – prophylactic immunization model with the use of irradiated cancer cells, as well as DCs stimulated with irradiated cancer cells (<xref rid="B207" ref-type="bibr">207</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">RIG-I-like helicases (RLH) ligand</td><td valign="top" align="left" rowspan="1" colspan="1">Panc02 cells in C57BL/6 mice – prophylactic immunization and curative tumor model (<xref rid="B165" ref-type="bibr">165</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Septacidin</td><td valign="top" align="left" rowspan="1" colspan="1">MCA205 cells in BALB/c mice – prophylactic set-up (<xref rid="B139" ref-type="bibr">139</xref>);</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Shikonin</td><td valign="top" align="left" rowspan="1" colspan="1">B16 cells in C57BL/6 mice – prophylactic immunization model (<xref rid="B160" ref-type="bibr">160</xref>); P388 cells in KMF mice – curative tumor model (<xref rid="B208" ref-type="bibr">208</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">4T1 cells in BALB/c mice – curative tumor model (<xref rid="B192" ref-type="bibr">192</xref>);</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">UVC irradiation</td><td valign="top" align="left" rowspan="1" colspan="1">CT26 cells in BALB/c mice – prophylactic immunization model (<xref rid="B204" ref-type="bibr">204</xref>); EG7 cells in C57BL/6 mice – curative tumor model (<xref rid="B152" ref-type="bibr">152</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Vorinostat</td><td valign="top" align="left" rowspan="1" colspan="1">MC38 or Eμ-myc 4242/299 lymphoma in C57BL/6 mice – curative tumor set-up (<xref rid="B166" ref-type="bibr">166</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="left" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">High hydrostatic pressure</td><td valign="top" align="left" rowspan="2" colspan="4">No mice or rat based preclinical data available to support their ICD-functions</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Pt<sup>II</sup> N-heterocyclic carbene complex</td></tr></tbody></table><table-wrap-foot><p><italic>DC, dendritic cell; ICD, immunogenic cell death; PDT, photodynamic therapy</italic>.</p></table-wrap-foot></table-wrap><p>As a recent systematic review summarized (<xref rid="B196" ref-type="bibr">196</xref>), heterotopic murine models suffer from a number of caveats, including the inability to recapitulate the early interaction between transformed cells and the immune system and the incompatibility between the cancer type and the site-of-transplantation (<xref rid="B196" ref-type="bibr">196</xref>). Orthotopic murine models are useful as they overcome the cancer cell-tissue type incompatibility issue (<xref rid="B196" ref-type="bibr">196</xref>). While genetically engineered tumor murine models (GEMMs) overcome most of the issues mentioned above, they come with their own set of shortcomings, including a limited genetic mosaicism, a low tumor heterogeneity, a lack of well-defined immunogenic TAAs, the presence of unintended “passenger” genetic modifications, and a reduced mutational spectrum (<xref rid="B196" ref-type="bibr">196</xref>). Many of these parameters are critical for responses to immunotherapy/ICD. For instance, the lack of well-defined immunogenic TAAs was the reason why preliminary results obtained in spontaneously developing murine tumors disputed the very existence of TAAs (<xref rid="B11" ref-type="bibr">11</xref>). Similarly, a high mutational spectrum (which produces considerable amounts of neo-antigens) has been found to be mandatory for the clinical efficacy of checkpoint blockers (<xref rid="B209" ref-type="bibr">209</xref>). Last (but not least), laboratory rodent models in general are associated with some critical issues, including the fact that a high level of inbreeding (which produces a number of shortcomings e.g., homozygous recessive defects) reduces the general immunological fitness, responsiveness and diversity in these models (<xref rid="B196" ref-type="bibr">196</xref>, <xref rid="B210" ref-type="bibr">210</xref>, <xref rid="B211" ref-type="bibr">211</xref>). Moreover, numerous immunological differences between mouse and humans tend to affect the translational relevance of the findings obtained (<xref rid="B26" ref-type="bibr">26</xref>, <xref rid="B211" ref-type="bibr">211</xref>, <xref rid="B212" ref-type="bibr">212</xref>). Also, the time frames of tumor growth rates between rodent models and humans are relatively divergent (<xref rid="B196" ref-type="bibr">196</xref>, <xref rid="B213" ref-type="bibr">213</xref>, <xref rid="B214" ref-type="bibr">214</xref>). This further complicates clinical translation of immunotherapeutic paradigms since the level of immunosurveillance and immunoediting experienced by human tumors can be much higher than any rodent tumor model.</p><p>In summary, it would be ideal to test ICD across as many different rodent models as possible, in order to determine the features that can be exploited for therapeutic purposes in humans. Moreover, if ICD fails in a specific experimental model, active effort should be made to characterize the mechanisms behind such failure, since resistance phenotypes can have profound clinical implications. This emerges from various studies summarized in Table <xref ref-type="table" rid="T7">7</xref>. Indeed, several ICD resistance mechanisms exist operating at both the cancer cell and the immune system level, which have been characterized in different experimental models. Several of these resistance mechanisms have also been identified in cancer patients, thereby justifying further studies along these lines Table <xref ref-type="table" rid="T7">7</xref>.</p><table-wrap id="T7" position="float"><label>Table 7</label><caption><p><bold>Existence of intrinsic or naturally occurring resistance to ICD in experimental cancer models</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">ICD inducer(s)</th><th valign="top" align="left" rowspan="1" colspan="1">Experimental set-up where resistance was observed</th><th valign="top" align="left" rowspan="1" colspan="1">Reason behind resistance</th><th valign="top" align="left" rowspan="1" colspan="1">Rescued by?</th><th valign="top" align="left" rowspan="1" colspan="1">Clinical applicability verified?</th><th valign="top" align="center" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td valign="top" align="left" colspan="6" rowspan="1"><bold><italic>In vivo</italic> preclinical setting (cancer cell or host immune system-level resistance)</bold></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines or anthracycline plus oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">C3H mice with naturally occurring <italic>tlr4</italic> mutation</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system-level resistance: defective <italic>TLR4</italic> in C3H mice causes failure of HMGB1-mediated immunity thereby leading to resistance to anti-cancer vaccination effect associated with anthracyclines treatment</td><td valign="top" align="left" rowspan="1" colspan="1">Adoptive transfer of TLR4-expressing DCs loaded with dying tumor cells</td><td valign="top" align="left" rowspan="1" colspan="1">Yes; breast cancer, colon cancer, and lung cancer patients carrying TLR4 gene mutation that ablates its ability to bind its ligands is associated with worse prognosis post-treatment</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B215" ref-type="bibr">215</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Doxorubicin</td><td valign="top" align="left" rowspan="1" colspan="1">AT-3 or 4T1.2 breast cancer cells in C57BL/6 or BALB/c mice, respectively</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cell-level resistance: CD73 overexpression confers chemo-resistance to doxorubicin by suppressing anti-tumor immunity through A2A adenosine receptors</td><td valign="top" align="left" rowspan="1" colspan="1">Blockade of CD73</td><td valign="top" align="left" rowspan="1" colspan="1">Yes; in triple-negative breast cancer patients, high CD73 in anthracycline-treatment set-up associated with lower rate of complete responses</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B216" ref-type="bibr">216</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Mitoxantrone and Hypericin-PDT</td><td valign="top" align="left" rowspan="1" colspan="1">AY27 rat bladder cancer cells in Fischer 344 rats</td><td valign="top" align="left" rowspan="1" colspan="1">Cancer cell-level resistance: low endogenous CRT levels, resulted in severely reduced surface-CRT upon treatment with mitoxantrone or Hyp-PDT; this in turn compromised immunogenic phagocytic clearance and anti-cancer vaccination effect</td><td valign="top" align="left" rowspan="1" colspan="1">Exogenous addition of recombinant CRT</td><td valign="top" align="left" rowspan="1" colspan="1">Yes; high tumoral <italic>CALR</italic> levels correlated with high expression of phagocytosis-associated genes and predicted for prolonged survival after RT or PTX treatment of lung or ovarian cancer patients respectively</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B42" ref-type="bibr">42</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">Autochthonous transgenic adenocarcinoma of the mouse prostate (TRAMP) model of metastatic prostate cancer</td><td valign="top" align="left" rowspan="1" colspan="1">Host immune system-level resistance: immunosuppressive B cells expressing IgA, IL10 and PD-L1 cause resistance to anti-tumorigenic effects of oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">Genetic or pharmacological depletion of B cells</td><td valign="top" align="left" rowspan="1" colspan="1">Not directly, but possible validity is supported by human patient data showing that IL-10 expressing IgA+ cells are abundant in therapy-resistant prostate cancer and are negative prognostic indicators</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B217" ref-type="bibr">217</xref>)</td></tr><tr><td valign="top" align="left" colspan="6" rowspan="1"><bold><italic>In vitro</italic> preclinical setting (cancer cell-level resistance)</bold></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Anthracycline</td><td valign="top" align="left" rowspan="1" colspan="1">SH-SY5Y neuroblastoma cell line</td><td valign="top" align="left" rowspan="1" colspan="1">Anthracycline treatment of these cells failed to induce surface-CRT due to reduced capacity to efflux ER-Ca<sup>2+</sup> into cytosol</td><td valign="top" align="left" rowspan="1" colspan="1">Overexpression of reticulon-1C</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B132" ref-type="bibr">132</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Doxorubicin</td><td valign="top" align="left" rowspan="1" colspan="1">HT29-dx and HT29 iNOS-cells (human colon cancer cells)</td><td valign="top" align="left" rowspan="1" colspan="1">Doxorubicin failed to induce NO synthesis, which resulted in reduced toxicity, reduced surface-CRT and subsequently compromised immunogenic phagocytic clearance and DC stimulation</td><td valign="top" align="left" rowspan="1" colspan="1">Addition of sodium nitroprusside or a NO donor</td><td valign="top" align="left" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B218" ref-type="bibr">218</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Doxorubicin</td><td valign="top" align="left" rowspan="1" colspan="1">MDR+ human cancer cells (HT29-dx, A549-dx and MCF-7-dx)</td><td valign="top" align="left" rowspan="1" colspan="1">Increased MDR levels caused increased P-glycoprotein expression which caused resistance to doxorubicin-induced ICD by affecting immunogenic phagocytic removal</td><td valign="top" align="left" rowspan="1" colspan="1">Addition of zoledronic acid</td><td valign="top" align="left" rowspan="1" colspan="1">Not directly</td><td valign="top" align="center" rowspan="1" colspan="1">(<xref rid="B219" ref-type="bibr">219</xref>)</td></tr></tbody></table><table-wrap-foot><p><italic>CD, cluster of differentiation; CRT or <italic>CALR</italic>, calreticulin; DC, dendritic cells; ER, endoplasmic reticulum; HMGB1, high-mobility group box-1 protein; HSP, heat shock protein; Hyp-PDT, hypericin-photodynamic therapy; ICD, immunogenic cell death; IL, interleukin; MDR, multiple drug-resistance; NO, nitric oxide; NOS, nitric oxide synthase; PD-L1, programed cell death protein ligand 1; PTX, paclitaxel; RT, radiotherapy; TLR, toll-like receptor</italic>.</p></table-wrap-foot></table-wrap><p>A considerable amounts of clinical findings support the relevance of ICD or ICD-related signatures in (at least subsets of) cancer patients. As summarized in Table <xref ref-type="table" rid="T8">8</xref>, various ICD-linked (specific) parameters have been associated with the prognosis of cancer patients treated with clinically relevant ICD inducers (like anthracyclines, oxaliplatin, paclitaxel, or radiotherapy). Moreover, it is becoming clear that ICD-related or ICD-derived (immunological) genetic signatures (e.g., a <italic>MX1</italic>-centered metagene, a <italic>CXCR3</italic>-<italic>PRF1</italic>-<italic>CASP1</italic>-centered metagene, an <italic>ASAH1</italic>-centered metagene) can be positively associated with good prognosis in patients affected by various neoplasms, including breast, lung, and ovarian malignancies (<xref rid="B141" ref-type="bibr">141</xref>, <xref rid="B188" ref-type="bibr">188</xref>, <xref rid="B220" ref-type="bibr">220</xref>). These observations indicate that ICD or ICD-relevant parameters may have prognostic or predictive relevance in at least a subset of cancer patients. It will be important to characterize new and more specific ICD-associated parameters linked to patient prognosis as well as biomarkers that may predict improved disease outcome in cancer patient treated with ICD inducers. Of note, considering the current clinical experience with immunotherapies (<xref rid="B209" ref-type="bibr">209</xref>, <xref rid="B221" ref-type="bibr">221</xref>), the patients with an increased likelihood to benefit from ICD inducers are probably those that display pre-existing (baseline) immune reactivity against cancer cells (<xref rid="B220" ref-type="bibr">220</xref>, <xref rid="B222" ref-type="bibr">222</xref>, <xref rid="B223" ref-type="bibr">223</xref>). This may depend on the ability of ICD to reboot and/or revive pre-existing TAA-directed immunity rather to prime <italic>de novo</italic> immune reactivity (<xref rid="B5" ref-type="bibr">5</xref>, <xref rid="B191" ref-type="bibr">191</xref>, <xref rid="B224" ref-type="bibr">224</xref>). In future, it would be crucial to characterize biomarkers that allow clinicians to delineate patients with reduced baseline immune reactivity against malignant cells so that proper combinatorial therapies involving ICD inducers can be implemented.</p><table-wrap id="T8" position="float"><label>Table 8</label><caption><p><bold>A list of clinical observations supporting the existence of ICD in cancer patients</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1">ICD inducer</th><th valign="top" align="left" rowspan="1" colspan="1">Standard-of-care therapy or regularly applied palliative therapy in clinic?</th><th valign="top" align="left" rowspan="1" colspan="1">ICD-related characteristics regulating clinical patient prognosis or treatment-responsiveness</th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Anthracyclines</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1"><italic>P2RX7</italic> loss-of-function mutation that compromises ICD also negatively affects MFS in breast cancer patients treated with adjuvant anthracyclines (<xref rid="B36" ref-type="bibr">36</xref>); breast cancer patients possessing a wild-type <italic>TLR4</italic> benefited more from the anthracyclines than those who possessed a mutated <italic>TLR4</italic> that compromises ICD (<xref rid="B70" ref-type="bibr">70</xref>); an <italic>MX1</italic>-centered Type I IFN signature in anthracycline-treated breast cancer patients predicts for improved disease outcome (<xref rid="B141" ref-type="bibr">141</xref>); combined positivity for cytoplasmic LC3B+ puncta and nuclear HMGB1 is a positive predictor of improved survival following adjuvant anthracycline-based chemotherapy (<xref rid="B225" ref-type="bibr">225</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">High hydrostatic pressure</td><td valign="top" align="left" rowspan="1" colspan="1">No; but HHP-based anticancer DC vaccines are currently being applied in clinical trials against prostate cancer and ovarian cancer (<xref rid="B155" ref-type="bibr">155</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">No data are available</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Hypericin-based PDT</td><td valign="top" align="left" rowspan="1" colspan="1">No; but few clinical trials have been carried out for non-melanoma skin cancer (<xref rid="B226" ref-type="bibr">226</xref>), cutaneous T-cell lymphoma (<xref rid="B227" ref-type="bibr">227</xref>), mesothelioma (<xref rid="B228" ref-type="bibr">228</xref>), and basal or squamous cell carcinoma (<xref rid="B229" ref-type="bibr">229</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">No data are available</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Oncolytic adenoviruses</td><td valign="top" align="left" rowspan="1" colspan="1">No; but oncolytic adenoviruses are currently being applied in various clinical trials in cancer patients</td><td valign="top" align="left" rowspan="1" colspan="1">Serum HMGB1 levels and the temporal change in their levels during treatment was identified as a prognostic and predictive biomarker in cancer patients (<xref rid="B230" ref-type="bibr">230</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Oxaliplatin</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">Similar to anthracyclines, cancer patients possessing wild-type <italic>TLR4</italic> exhibited prolonged PFS and OS in comparison to patients bearing the loss-of-function allele of <italic>TLR4</italic> (<xref rid="B197" ref-type="bibr">197</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Paclitaxel</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">High tumoral <italic>CALR</italic> levels in paclitaxel-treated ovarian cancer patients associated with prolonged OS/PFS as well as increased expression levels of various phagocytosis-associated genes (<xref rid="B42" ref-type="bibr">42</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Photofrin-based PDT</td><td valign="top" align="left" rowspan="1" colspan="1">Yes; FDA-approved for application in esophageal and lung cancer (<xref rid="B231" ref-type="bibr">231</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">No data available</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Radiotherapy</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">In patients of eosophageal squamous cell carcinoma (ESCC) receiving chemo-radiotherapy significant increase in serum HMGB1-levels and increased intra-tumoral staining of HMGB1 correlated with better patient survival (<xref rid="B232" ref-type="bibr">232</xref>); high tumoral <italic>CALR</italic> levels in radiotherapy-treated lung cancer patients associated with prolonged OS as well as increased expression levels of various phagocytosis-associated genes (<xref rid="B42" ref-type="bibr">42</xref>)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Shikonin</td><td valign="top" align="left" rowspan="1" colspan="1">No; but shikonin is currently being applied in an observational clinical study of breast cancer patients (NCT01287468)</td><td valign="top" align="left" rowspan="1" colspan="1">No data are available</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">UVC irradiation</td><td valign="top" align="left" rowspan="1" colspan="1">No; but UV treatment is sometimes applied for the preparation of clinical cell-based anticancer vaccines (<xref rid="B233" ref-type="bibr">233</xref>)</td><td valign="top" align="left" rowspan="1" colspan="1">No data are available</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Bortezomib, Anti-EGFR antibody (7A7), bleomycin, cyclophosphamide, microwave thermal ablation, vorinostat</td><td valign="top" align="left" rowspan="1" colspan="1">Yes</td><td valign="top" align="left" rowspan="1" colspan="1">No data are available</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Coxsackievirus B3; <italic>Clostridium difficile</italic> toxin B; Microwave thermal ablation; Newcastle disease virus (NDV); RIG-I-like helicases (RLH) ligand; Septacidin; Pt<sup>II</sup> N-heterocyclic carbene complex; Patupilone</td><td valign="top" align="left" rowspan="1" colspan="1">No</td><td valign="top" align="left" rowspan="1" colspan="1">No data are available</td></tr></tbody></table><table-wrap-foot><p><italic>CRT or <italic>CALR</italic>, calreticulin; HMGB1, high-mobility group box-1 protein; Hyp-PDT, hypericin-photodynamic therapy; ICD, immunogenic cell death; IFN, interferon; OS, overall survival; PFS, progression-free survival; TLR, toll-like receptor</italic>.</p></table-wrap-foot></table-wrap></sec><sec id="S4"><title>Confronting the Clinical Realities of Anti-Tumor Immunity</title><p>It is well-established that the response of cancer patients to immunotherapy relies on the activity of effector T cells [that employ their T-cell receptors (TCRs) for recognizing TAAs]. However, these TAA-targeting T cells may also constitute obstacles for effective anti-tumor immunity (<xref rid="B234" ref-type="bibr">234</xref>). As opposed to T lymphocytes recognizing pathogen-associated antigens (PAAs) (Figure <xref ref-type="fig" rid="F2">2</xref>), indeed, T cells directed against some TAAs (derived from non-mutated proteins that are source of self or near-to-self antigens) are developmentally subjected to negative selection in the thymus and peripheral lymphoid organs (<xref rid="B234" ref-type="bibr">234</xref>, <xref rid="B235" ref-type="bibr">235</xref>) (Figure <xref ref-type="fig" rid="F2">2</xref>). As a result, T cells bearing TCRs with high affinity for self antigens (including some TAAs) are clonally deleted to avoid auto-immunity (<xref rid="B234" ref-type="bibr">234</xref>–<xref rid="B237" ref-type="bibr">237</xref>) (Figure <xref ref-type="fig" rid="F2">2</xref>). However, some “leakiness” in this process allows TAA-specific T cells possessing TCRs with low affinity to escape deletion (<xref rid="B234" ref-type="bibr">234</xref>, <xref rid="B236" ref-type="bibr">236</xref>, <xref rid="B237" ref-type="bibr">237</xref>) and persist, although at low precursor frequencies (<xref rid="B238" ref-type="bibr">238</xref>) (Figure <xref ref-type="fig" rid="F2">2</xref>). Unfortunately, as compared to PAA-specific T cells, which bear high-affinity TCRs (Figure <xref ref-type="fig" rid="F2">2</xref>), TAA-specific T cells exhibit limited effector and memory functions (<xref rid="B234" ref-type="bibr">234</xref>, <xref rid="B239" ref-type="bibr">239</xref>). Coupled with the tendency of progressing tumors to generate a highly immunosuppressive microenvironment, this renders the insurgence of lifelong protective immunity nearly impossible (<xref rid="B234" ref-type="bibr">234</xref>). Of note, central and peripheral tolerance may not affect T cells reactive toward neo-tumor-specific antigens (neo-TSAs) e.g., tumor-specific neo-antigens that are generated <italic>de novo</italic> in the course of tumor progression because of mutational events (<xref rid="B240" ref-type="bibr">240</xref>, <xref rid="B241" ref-type="bibr">241</xref>). However, the extent to which such neo-TSAs can elicit consistent “immunodominant” T cell reactivity is still a matter of investigation (<xref rid="B240" ref-type="bibr">240</xref>, <xref rid="B241" ref-type="bibr">241</xref>). Nevertheless, in this context, inefficient T-cell stimulation can be overcome through the ICD-based improvement of effector T-cell functions (<xref rid="B102" ref-type="bibr">102</xref>). ICD can be further combined with checkpoint-blocking therapies, which potently reverse immunosuppression (<xref rid="B209" ref-type="bibr">209</xref>, <xref rid="B242" ref-type="bibr">242</xref>). However, the lifelong maintenance of anti-tumor T cells remains a particularly hard challenge.</p><fig id="F2" position="float"><label>Figure 2</label><caption><p><bold>Population dynamics of antigen-specific T cells during an immune response to infection or cancer</bold>. <bold>(A)</bold> T cells capable of putatively recognizing non-self, pathogen-associated antigens (PAAs) are not exposed to negative selection in the thymus or peripheral organs like lymph nodes. This allows for the constitutive presence of T lymphocytes bearing high-affinity T-cell receptor (TCR) in naïve conditions. Upon infection, these cells undergo robust expansion and acquire potent effector functions, hence driving an immune response that clears the pathogen and PAAs. Finally, PAA-specific T cells undergo contraction along with the establishment of immunological memory. To a limited extent, T cells reacting against PAAs expressed by virus-induced tumors may exhibit similar (although not identical) responses. <bold>(B)</bold> T cells that may recognize self or close-to-self antigens expressed by virus-unrelated malignancies undergo robust negative selection in the thymus and lymph nodes. Thus, all putative T lymphocytes bearing a high-affinity TCR against tumor-associated antigens (TAAs) are eliminated. However, some leakiness in this process allows for the persistence of TAA-specific T lymphocytes with low-affinity TCR, although at very low precursor frequencies. This is one of the reasons why in some individuals immunosurveillance at some stage fails to impede tumor progression. As malignant lesions progress, the amount of TAAs increases, causing a weak rise in TAA-specific T cells. However, tumor progression is generally coupled with the establishment of robust immunosuppressive networks that potently inhibit such TAA-targeting T cells. In this context, the administration of immunogenic cell death (ICD) according to a schedule that does not lead to lymphodepletion can favor the stimulation of TAA-targeting T cells and (re)instate immunosurveillance. Combining ICD inducers with checkpoint-blocking agents may further boost TAA-targeting immune responses. However, these treatments may not ensure the lifelong persistence of TAA-recognizing T cells, some of which are susceptible to elimination through tolerance mechanisms. Anticancer vaccines may counteract, at least to some extent, such loss. The figure was partly inspired from Baitsch et al. (<xref rid="B234" ref-type="bibr">234</xref>).</p></caption><graphic xlink:href="fimmu-06-00588-g002"></graphic></fig><p>In the clinical reality, anticancer agents are administered to patients in a limited number of cycles. Even if these therapeutic regimens may attain optimal efficacy in terms of ICD induction, they are unlikely to ensure the lifelong persistence of TAA-directed T cells with low-affinity TCR (<xref rid="B234" ref-type="bibr">234</xref>, <xref rid="B243" ref-type="bibr">243</xref>). This probably reflects the contraction of TAA-targeting T cells occurring once the immunostimulatory stimulus provided by ICD ceases, owing to peripheral tolerance mechanisms (<xref rid="B234" ref-type="bibr">234</xref>). Clinically, it may not be feasible to administer ICD inducers repeatedly over time, since many of them can cause lymphopenia (which negatively affects disease outcome), or are associated with other side effects (<xref rid="B244" ref-type="bibr">244</xref>). It has been proposed that active immunization with ICD-based anticancer vaccines (which are associated with robust immunogenicity) given in a repetitive manner may achieve this goal (Figure <xref ref-type="fig" rid="F2">2</xref>) (<xref rid="B234" ref-type="bibr">234</xref>, <xref rid="B243" ref-type="bibr">243</xref>, <xref rid="B245" ref-type="bibr">245</xref>). Thus, it will be important to test whether the long-term administration of ICD-based anticancer vaccines can sustain the effector function of TAA-specific T cells bearing low-affinity TCRs, hence, ensuring lifelong disease-free survival. Of note, in the case of hematological malignancies, this issue could be overcome upon the adoptive transfer of CTLs expressing chimeric antigen receptors (CARs) (<xref rid="B1" ref-type="bibr">1</xref>). However, whether CAR-expressing CTLs generate protective immunological memory in the absence of considerable side effects remains to be determined. Moreover, the use of this therapeutic strategy against solid malignancies is relatively challenging owing to lack of well-defined “unique” TAAs (<xref rid="B1" ref-type="bibr">1</xref>, <xref rid="B246" ref-type="bibr">246</xref>).</p></sec><sec id="S5"><title>Conclusion</title><p>The model of ICD has been considerably refined since the initial identification of a cell death modality manifesting apoptotic features but able to induce an adaptive immune response. This model strives to integrate several phenomena observed throughout the second half of the twentieth century in one therapeutically relevant platform. However, as discussed above, several challenges still need to be addressed. First, comprehensive testing should be performed in advanced experimental settings like GEMMs or orthotopic tumor models. Second, ICD resistance mechanisms should be characterized with precision. Third, various issues linked to the successful translation of ICD to cancer therapy will have to be resolved, including (but not limited to) treatment schedules, dosages, and combinatorial strategies. This translational drive also needs to be coupled with effective strategies for the discovery of new and effective ICD inducers. Drug screening programs are often complicated by the possibility of false-positive (due to bystander presence of DAMPs) (<xref rid="B30" ref-type="bibr">30</xref>) or false-negative (due to limited number of biomarkers used for screening) hits. This issue can only be ironed out by discovering new and common regulators of ICD, and integrating them into existing screening platforms. Last, but not least, it will be important to identify new ICD-related/derived biomarkers that can be used to improve current protocols of patient stratification and clinical decision making. We are positive that all these objectives are at reach.</p></sec><sec id="S6"><title>Author Contributions</title><p>ADG did the literature study, data collection, as well as conceived and wrote the manuscript. PA provided senior supervision and guidance, conceived the paper, helped in writing, and critically revised the manuscript. LG improved and edited the manuscript. JMBSP helped with the preparation of figures. All authors participated in the critical reading of the manuscript (wherever applicable), approved content and conclusions, as well as helped in ensuring the accuracy of cited literature.</p></sec><sec id="S7"><title>Conflict of Interest Statement</title><p>Akseli Hemminki is shareholder in Targovax AG and TILT Biotherapeutics Ltd. The remaining authors have no conflict of interest to declare.</p></sec></body><back><ack><p>We would like to explicitly declare that this manuscript does not aim to describe guidelines for the fields of ICD and DAMP research. Rather, it is meant to be a comprehensive classification and review of relevant literature expressing consensus discussions, opinions, and conclusions endorsed and/or supported by a number of researchers and clinicians investigating ICD and DAMPs. We would also like to acknowledge the following colleagues for their support, reading and/or positive appraisal of this manuscript: Wee Han Ang, Vincenzo Barnaba, Marco E. Bianchi, Karin de Visser, Sandra O. Gollnick, Peter Henson, Polly Matzinger, Marek Michalak, Kodi Ravichandran, and Andrew Thorburn. ADG is a recipient of the FWO postdoctoral fellowship 2013. This work was supported by grants from the Fund for Scientific Research Flanders (FWO-Vlaanderen; G.0661.09, G.0728.10 and G.0584.12N) and KU Leuven (GOA/11/009) to PA; This paper presents research results of the IAP7/32, funded by the Interuniversity Attraction Poles Programme, initiated by the Belgian State, Science Policy Office.</p></ack><sec id="S8"><title>Abbreviations</title><p>DAMP, damage-associated molecular pattern; DC, dendritic cell; ER, endoplasmic reticulum; GEMM, genetically engineered murine model; HSP, heat shock protein; Hyp, hypericin; ICD, immunogenic cell death; NDV, Newcastle disease virotherapy; PDT, photodynamic therapy; ROS, reactive oxygen species.</p></sec><ref-list><title>References</title><ref id="B1"><label>1</label><mixed-citation publication-type="journal"><person-group 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