The Interplay of Autophagy and Tumor Microenvironment in Colorectal Cancer—Ways of Enhancing Immunotherapy Action
Identifieur interne : 000885 ( Pmc/Curation ); précédent : 000884; suivant : 000886The Interplay of Autophagy and Tumor Microenvironment in Colorectal Cancer—Ways of Enhancing Immunotherapy Action
Auteurs : Evangelos Koustas ; Panagiotis Sarantis ; Georgia Kyriakopoulou ; Athanasios G. Papavassiliou ; Michalis V. Karamouzis [Grèce]Source :
- Cancers [ 2072-6694 ] ; 2019.
Abstract
Autophagy as a primary homeostatic and catabolic process is responsible for the degradation and recycling of proteins and cellular components. The mechanism of autophagy has a crucial role in several cellular functions and its dysregulation is associated with tumorigenesis, tumor–stroma interactions, and resistance to cancer therapy. A growing body of evidence suggests that autophagy is also a key regulator of the tumor microenvironment and cellular immune response in different types of cancer, including colorectal cancer (CRC). Furthermore, autophagy is responsible for initiating the immune response especially when it precedes cell death. However, the role of autophagy in CRC and the tumor microenvironment remains controversial. In this review, we identify the role of autophagy in tumor microenvironment regulation and the specific mechanism by which autophagy is implicated in immune responses during CRC tumorigenesis and the context of anticancer therapy.
Url:
DOI: 10.3390/cancers11040533
PubMed: 31013961
PubMed Central: 6520891
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">The Interplay of Autophagy and Tumor Microenvironment in Colorectal Cancer—Ways of Enhancing Immunotherapy Action</title><author><name sortKey="Koustas, Evangelos" sort="Koustas, Evangelos" uniqKey="Koustas E" first="Evangelos" last="Koustas">Evangelos Koustas</name><affiliation><nlm:aff id="af1-cancers-11-00533">Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</nlm:aff></affiliation></author><author><name sortKey="Sarantis, Panagiotis" sort="Sarantis, Panagiotis" uniqKey="Sarantis P" first="Panagiotis" last="Sarantis">Panagiotis Sarantis</name><affiliation><nlm:aff id="af1-cancers-11-00533">Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</nlm:aff></affiliation></author><author><name sortKey="Kyriakopoulou, Georgia" sort="Kyriakopoulou, Georgia" uniqKey="Kyriakopoulou G" first="Georgia" last="Kyriakopoulou">Georgia Kyriakopoulou</name><affiliation><nlm:aff id="af1-cancers-11-00533">Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</nlm:aff></affiliation></author><author><name sortKey="Papavassiliou, Athanasios G" sort="Papavassiliou, Athanasios G" uniqKey="Papavassiliou A" first="Athanasios G." last="Papavassiliou">Athanasios G. Papavassiliou</name><affiliation><nlm:aff id="af1-cancers-11-00533">Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</nlm:aff></affiliation></author><author><name sortKey="Karamouzis, Michalis V" sort="Karamouzis, Michalis V" uniqKey="Karamouzis M" first="Michalis V." last="Karamouzis">Michalis V. Karamouzis</name><affiliation><nlm:aff id="af1-cancers-11-00533">Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-cancers-11-00533">First Department of Internal Medicine, ‘Laiko’ General Hospital, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece</nlm:aff><country xml:lang="fr">Grèce</country><wicri:regionArea>First Department of Internal Medicine, ‘Laiko’ General Hospital, Medical School, National and Kapodistrian University of Athens, 11527 Athens</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31013961</idno><idno type="pmc">6520891</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6520891</idno><idno type="RBID">PMC:6520891</idno><idno type="doi">10.3390/cancers11040533</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000885</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000885</idno><idno type="wicri:Area/Pmc/Curation">000885</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000885</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">The Interplay of Autophagy and Tumor Microenvironment in Colorectal Cancer—Ways of Enhancing Immunotherapy Action</title><author><name sortKey="Koustas, Evangelos" sort="Koustas, Evangelos" uniqKey="Koustas E" first="Evangelos" last="Koustas">Evangelos Koustas</name><affiliation><nlm:aff id="af1-cancers-11-00533">Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</nlm:aff></affiliation></author><author><name sortKey="Sarantis, Panagiotis" sort="Sarantis, Panagiotis" uniqKey="Sarantis P" first="Panagiotis" last="Sarantis">Panagiotis Sarantis</name><affiliation><nlm:aff id="af1-cancers-11-00533">Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</nlm:aff></affiliation></author><author><name sortKey="Kyriakopoulou, Georgia" sort="Kyriakopoulou, Georgia" uniqKey="Kyriakopoulou G" first="Georgia" last="Kyriakopoulou">Georgia Kyriakopoulou</name><affiliation><nlm:aff id="af1-cancers-11-00533">Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</nlm:aff></affiliation></author><author><name sortKey="Papavassiliou, Athanasios G" sort="Papavassiliou, Athanasios G" uniqKey="Papavassiliou A" first="Athanasios G." last="Papavassiliou">Athanasios G. Papavassiliou</name><affiliation><nlm:aff id="af1-cancers-11-00533">Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</nlm:aff></affiliation></author><author><name sortKey="Karamouzis, Michalis V" sort="Karamouzis, Michalis V" uniqKey="Karamouzis M" first="Michalis V." last="Karamouzis">Michalis V. Karamouzis</name><affiliation><nlm:aff id="af1-cancers-11-00533">Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-cancers-11-00533">First Department of Internal Medicine, ‘Laiko’ General Hospital, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece</nlm:aff><country xml:lang="fr">Grèce</country><wicri:regionArea>First Department of Internal Medicine, ‘Laiko’ General Hospital, Medical School, National and Kapodistrian University of Athens, 11527 Athens</wicri:regionArea></affiliation></author></analytic><series><title level="j">Cancers</title><idno type="eISSN">2072-6694</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Autophagy as a primary homeostatic and catabolic process is responsible for the degradation and recycling of proteins and cellular components. The mechanism of autophagy has a crucial role in several cellular functions and its dysregulation is associated with tumorigenesis, tumor–stroma interactions, and resistance to cancer therapy. A growing body of evidence suggests that autophagy is also a key regulator of the tumor microenvironment and cellular immune response in different types of cancer, including colorectal cancer (CRC). Furthermore, autophagy is responsible for initiating the immune response especially when it precedes cell death. However, the role of autophagy in CRC and the tumor microenvironment remains controversial. In this review, we identify the role of autophagy in tumor microenvironment regulation and the specific mechanism by which autophagy is implicated in immune responses during CRC tumorigenesis and the context of anticancer therapy.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Siegel, R L" uniqKey="Siegel R">R.L. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Cancers (Basel)</journal-id><journal-id journal-id-type="iso-abbrev">Cancers (Basel)</journal-id><journal-id journal-id-type="publisher-id">cancers</journal-id><journal-title-group><journal-title>Cancers</journal-title></journal-title-group><issn pub-type="epub">2072-6694</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31013961</article-id><article-id pub-id-type="pmc">6520891</article-id><article-id pub-id-type="doi">10.3390/cancers11040533</article-id><article-id pub-id-type="publisher-id">cancers-11-00533</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>The Interplay of Autophagy and Tumor Microenvironment in Colorectal Cancer—Ways of Enhancing Immunotherapy Action</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Koustas</surname><given-names>Evangelos</given-names></name><xref ref-type="aff" rid="af1-cancers-11-00533">1</xref></contrib><contrib contrib-type="author"><name><surname>Sarantis</surname><given-names>Panagiotis</given-names></name><xref ref-type="aff" rid="af1-cancers-11-00533">1</xref></contrib><contrib contrib-type="author"><name><surname>Kyriakopoulou</surname><given-names>Georgia</given-names></name><xref ref-type="aff" rid="af1-cancers-11-00533">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-5803-4527</contrib-id><name><surname>Papavassiliou</surname><given-names>Athanasios G.</given-names></name><xref ref-type="aff" rid="af1-cancers-11-00533">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-1369-8201</contrib-id><name><surname>Karamouzis</surname><given-names>Michalis V.</given-names></name><xref ref-type="aff" rid="af1-cancers-11-00533">1</xref><xref ref-type="aff" rid="af2-cancers-11-00533">2</xref><xref rid="c1-cancers-11-00533" ref-type="corresp">*</xref></contrib></contrib-group><aff id="af1-cancers-11-00533"><label>1</label>Molecular Oncology Unit, Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece;<email>vang.koustas@gmail.com</email> (E.K.);<email>psarantis@bioacademy.gr</email> (P.S.);<email>gpkyriakopoulou@yahoo.com</email> (G.K.);<email>papavas@med.uoa.gr</email> (A.G.P.)</aff><aff id="af2-cancers-11-00533"><label>2</label>First Department of Internal Medicine, ‘Laiko’ General Hospital, Medical School, National and Kapodistrian University of Athens, 11527 Athens, Greece</aff><author-notes><corresp id="c1-cancers-11-00533"><label>*</label>Correspondence: <email>mkaramouz@med.uoa.gr</email>; Tel.: +30-210-746-2508 or +30-210-746-2509; Fax: +30-210-746-2703</corresp></author-notes><pub-date pub-type="epub"><day>14</day><month>4</month><year>2019</year></pub-date><pub-date pub-type="collection"><month>4</month><year>2019</year></pub-date><volume>11</volume><issue>4</issue><elocation-id>533</elocation-id><history><date date-type="received"><day>25</day><month>3</month><year>2019</year></date><date date-type="accepted"><day>11</day><month>4</month><year>2019</year></date></history><permissions><copyright-statement>© 2019 by the authors.</copyright-statement><copyright-year>2019</copyright-year><license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>).</license-p></license></permissions><abstract><p>Autophagy as a primary homeostatic and catabolic process is responsible for the degradation and recycling of proteins and cellular components. The mechanism of autophagy has a crucial role in several cellular functions and its dysregulation is associated with tumorigenesis, tumor–stroma interactions, and resistance to cancer therapy. A growing body of evidence suggests that autophagy is also a key regulator of the tumor microenvironment and cellular immune response in different types of cancer, including colorectal cancer (CRC). Furthermore, autophagy is responsible for initiating the immune response especially when it precedes cell death. However, the role of autophagy in CRC and the tumor microenvironment remains controversial. In this review, we identify the role of autophagy in tumor microenvironment regulation and the specific mechanism by which autophagy is implicated in immune responses during CRC tumorigenesis and the context of anticancer therapy.</p></abstract><kwd-group><kwd>Autophagy</kwd><kwd>colorectal cancer</kwd><kwd>immunotherapy</kwd><kwd>tumor stroma</kwd><kwd>tumor microenvironment</kwd></kwd-group></article-meta></front><floats-group><fig id="cancers-11-00533-f001" orientation="portrait" position="float"><label>Figure 1</label><caption><p>The role of autophagy in the presentation of immunogenic peptides in antigen-presenting cells (APCs). Autophagy has a vital role in the degradation of proteins in order for APCs to use them as antigenic peptides on Major Histocompatibility Complex (MHC)-I and II. Three distinct pathways of antigen processing by the APC have been identified: Exogenous (1A), cross-presentation (1B), and endogenous (1C) pathway. In the exogenous pathway, different antigens and peptides are produced outside the APC and placed on the MHC class II for recognition by CD4+ T cells. The exogenous pathway occurs in macrophages, dendritic cells, and B cells. The endogenous pathway loads cell-produced antigenic peptides onto MHC class I for recognition by CD8+ T cells. The endogenous pathway is responsible for immune recognition of peptides from the virus or self-digested peptides. The endogenous pathway characterizes many cell types, not just APCs, allowing for sensing of viral infection in all cell types. In the cross-presentation pathway, different peptides, from endocytosis and the autophagy degradation pathway, are loaded on MHC class I for recognition by CD8+ T cells. The peptides originate from the surrounding cell environment of tumor apoptotic bodies. This pathway targets virus-infected cells other than APCs and the tumor. The cross-presentation pathway is identified as the most efficient in dendritic cells.</p></caption><graphic xlink:href="cancers-11-00533-g001"></graphic></fig><table-wrap id="cancers-11-00533-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-11-00533-t001_Table 1</object-id><label>Table 1</label><caption><p>Clinical studies with immunotherapy for patients with Please define this term if appropriate.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Number of Study</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Immune Target</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Agent/Compound</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Phase of Study</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT01876511</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02981524</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Cyclophosphamide followed by Pembrolizumab</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03657641</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab + Vicriviroc</td><td align="center" valign="middle" rowspan="1" colspan="1">I/II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03631407</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab + Regorafenib</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03475004</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab, Bevacizumab, and Binimetinib</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03658772</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab + grapiprant</td><td align="center" valign="middle" rowspan="1" colspan="1">I</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03519412</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab + temozolomide</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02713373</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab + cetuximab</td><td align="center" valign="middle" rowspan="1" colspan="1">I/II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02375672</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab + FOLFOX</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03332498</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab + Ibrutinib</td><td align="center" valign="middle" rowspan="1" colspan="1">I/II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02851004</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab + SBRT</td><td align="center" valign="middle" rowspan="1" colspan="1">I/II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02837263</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Pembrolizumab + BBI609</td><td align="center" valign="middle" rowspan="1" colspan="1">I</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02992912</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Atezolizumab + stereotactic ablative radiotherapy</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03712943</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Nivolumab + Regorafenib</td><td align="center" valign="middle" rowspan="1" colspan="1">I</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03711058</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Nivolumab + Copanlisib</td><td align="center" valign="middle" rowspan="1" colspan="1">I/II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03414983</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Nivolumab, Oxaliplatin, Leucovorin, Fluorouracil, Bevacizumab</td><td align="center" valign="middle" rowspan="1" colspan="1">II/III</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02860546</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Nivolumab + TAS-102</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03026140</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1 and CTLA-4</td><td align="center" valign="middle" rowspan="1" colspan="1">Nivolumab + Ipilimumab +/− celecoxib</td><td align="center" valign="middle" rowspan="1" colspan="1">I/III</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03693846</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1 and CTLA-4</td><td align="center" valign="middle" rowspan="1" colspan="1">Nivolumab + Ipilimumab</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03104439</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1 and CTLA-4</td><td align="center" valign="middle" rowspan="1" colspan="1">Nivolumab + Ipilimumab + radiotherapy</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03377361</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1 and CTLA-4</td><td align="center" valign="middle" rowspan="1" colspan="1">Nivolumab + Ipilimumab + Trametinib</td><td align="center" valign="middle" rowspan="1" colspan="1">I/II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03832621</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1 and CTLA-4</td><td align="center" valign="middle" rowspan="1" colspan="1">Nivolumab, Ipilimumab, Temozolomide</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02327078</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-1 and IDO</td><td align="center" valign="middle" rowspan="1" colspan="1">Nivolumab + Epacadostat</td><td align="center" valign="middle" rowspan="1" colspan="1">VII</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02983578</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-L1</td><td align="center" valign="middle" rowspan="1" colspan="1">AZD9150 + MEDI4736</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02982694</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-L1</td><td align="center" valign="middle" rowspan="1" colspan="1">Atezolizumab + Bevacizumab</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02777710</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-L1</td><td align="center" valign="middle" rowspan="1" colspan="1">Durvalumab + Pexidartinib</td><td align="center" valign="middle" rowspan="1" colspan="1">I</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT03827044</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-L1</td><td align="center" valign="middle" rowspan="1" colspan="1">Avelumab</td><td align="center" valign="middle" rowspan="1" colspan="1">III</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02669914</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-L1</td><td align="center" valign="middle" rowspan="1" colspan="1">Durvalumab</td><td align="center" valign="middle" rowspan="1" colspan="1">II</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">NCT02754856</td><td align="center" valign="middle" rowspan="1" colspan="1">PD-L1 and CTLA-4</td><td align="center" valign="middle" rowspan="1" colspan="1">MEDI4736 + Tremelimumab</td><td align="center" valign="middle" rowspan="1" colspan="1">I</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NCT03202758</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">PD-L1 and CTLA-4</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Durvalumab, Tremelimumab, and FOLFOX</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">I/II</td></tr></tbody></table><table-wrap-foot><fn><p>NCT, national clinical trial; PD-1, programmed cell death-1; PD-1, programmed cell death-1 ligand; CTLA-4, cytotoxic T-lymphocyte-associated protein 4; IDO, indoleamine-pyrrole 2,3-dioxygenase.</p></fn></table-wrap-foot></table-wrap><table-wrap id="cancers-11-00533-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-11-00533-t002_Table 2</object-id><label>Table 2</label><caption><p>Commonly used molecules inhibiting autophagy. Small molecules that have been identified as inhibitors of autophagy and the main mechanism of action.</p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">Compound</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Autophagy Inhibitors</th></tr><tr><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mechanism of Action</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Bafilomycin A1</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibitor of v-ATPase, inhibition of lysosomal acidification</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Concanamycin A</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibitor of v-ATPase, inhibition of lysosomal acidification</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Azithromycin</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibitor of v-ATPase, inhibition of lysosomal acidification</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">3-Methyladenine (3-MA)</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibitor of class III PI3K</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Chloroquine (CQ)</td><td align="center" valign="middle" rowspan="1" colspan="1">Neutralizes the acidic pH of intracellular vesicles</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Hydroxy-chloroquine (HCQ)</td><td align="center" valign="middle" rowspan="1" colspan="1">CQ derivative-Neutralizes the acidic pH of intracellular vesicles</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Lys05</td><td align="center" valign="middle" rowspan="1" colspan="1">CQ derivative-alter the acidification of the lysosomes</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SAR405</td><td align="center" valign="middle" rowspan="1" colspan="1">Kinase inhibitor of Vps18 and Vps34</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SBI-0206965</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibitor of ULK1</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Verteporfin</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibit acidification of lysosomes</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Clomipramine</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibit acidification of lysosomes</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">desmethylclomipramine (DCMI)</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibit Autophagosome-Lysosome fusion</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Paclitaxel</td><td align="center" valign="middle" rowspan="1" colspan="1">Microtubule stabilizer- inhibits phosphorylation of VPS34 at T159</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SAHA</td><td align="center" valign="middle" rowspan="1" colspan="1">Interact in autophagosome-lysosome fusion</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Monensin</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibit autophagosome-lysosome fusion</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Sputin-1</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibits the activity of ubiquitin-specific peptidases, USP10 and USP13</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SP600125</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibition of JNK—reduction of Beclin-1</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">U0126</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibitor of MEK1 and MEK2</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Wortmannin</td><td align="center" valign="middle" rowspan="1" colspan="1">PI3K inhibitor</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">LY294002</td><td align="center" valign="middle" rowspan="1" colspan="1">PI3K inhibitor</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SB202190</td><td align="center" valign="middle" rowspan="1" colspan="1">Cross-inhibition of the PI3K/mTOR and MAPKs pathway</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">SB203580</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibit autophagy by interfering with the trafficking of Atg9</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">MHY1485</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">mTOR activator</td></tr></tbody></table></table-wrap><table-wrap id="cancers-11-00533-t003" orientation="portrait" position="float"><object-id pub-id-type="pii">cancers-11-00533-t003_Table 3</object-id><label>Table 3</label><caption><p>Commonly used molecules to induce autophagy. Small molecules that have been identified as autophagy inducers and the primary mechanism of action.</p></caption><table frame="hsides" rules="groups"><thead><tr><th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">Compound/Molecule</th><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Autophagy Inducers</th></tr><tr><th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Mechanism of Action</th></tr></thead><tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Rapamycin</td><td align="center" valign="middle" rowspan="1" colspan="1">mTORC1 inhibitor</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Temsirolimus</td><td align="center" valign="middle" rowspan="1" colspan="1">mTORC1 inhibitor</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Deforolimus</td><td align="center" valign="middle" rowspan="1" colspan="1">mTORC1 inhibitor</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Everolimus</td><td align="center" valign="middle" rowspan="1" colspan="1">mTORC1 inhibitor</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Metformin</td><td align="center" valign="middle" rowspan="1" colspan="1">AMPK activator</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Obatoclax</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibitor of Bcl-2 family proteins </td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">isoliensinine</td><td align="center" valign="middle" rowspan="1" colspan="1">Natural alkaloid </td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">cepharanthine</td><td align="center" valign="middle" rowspan="1" colspan="1">Natural alkaloid </td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">liensinine</td><td align="center" valign="middle" rowspan="1" colspan="1">Natural alkaloid </td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Perifosine</td><td align="center" valign="middle" rowspan="1" colspan="1">AKT inhibitor</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Tat–Beclin-1 peptide</td><td align="center" valign="middle" rowspan="1" colspan="1">Releases beclin-1 into cytoplasm-regulate autophagosome formation</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">Lithium</td><td align="center" valign="middle" rowspan="1" colspan="1">Increase the levels of Beclin-1/VPS34 complexes</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">GDC-0980</td><td align="center" valign="middle" rowspan="1" colspan="1">Dual inhibitor of PI3K and mTORC1</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">GDC-0941</td><td align="center" valign="middle" rowspan="1" colspan="1">Inhibitor of class I PI3K </td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">fluspirilene</td><td align="center" valign="middle" rowspan="1" colspan="1">Antagonists of L-type Ca2+ channels</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">verapamil</td><td align="center" valign="middle" rowspan="1" colspan="1">Antagonists of L-type Ca2+ channels</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">loperamide</td><td align="center" valign="middle" rowspan="1" colspan="1">Antagonists of L-type Ca2+ channels</td></tr><tr><td align="center" valign="middle" rowspan="1" colspan="1">nimodipine</td><td align="center" valign="middle" rowspan="1" colspan="1">Antagonists of L-type Ca2+ channels</td></tr><tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">amiodarone</td><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Antagonists of L-type Ca2+ channels</td></tr></tbody></table></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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