A Neutralizing Monoclonal Antibody Targeting the Acid-Sensitive Region in Chikungunya Virus E2 Protects from Disease
Identifieur interne : 004872 ( Main/Exploration ); précédent : 004871; suivant : 004873A Neutralizing Monoclonal Antibody Targeting the Acid-Sensitive Region in Chikungunya Virus E2 Protects from Disease
Auteurs : Suganya Selvarajah [États-Unis] ; Nicole R. Sexton [États-Unis] ; Kristen M. Kahle [États-Unis] ; Rachel H. Fong [États-Unis] ; Kimberly-Anne Mattia [États-Unis] ; Joy Gardner [Australie] ; Kai Lu [États-Unis] ; Nathan M. Liss [États-Unis] ; Beatriz Salvador [États-Unis] ; David F. Tucker [États-Unis] ; Trevor Barnes [États-Unis] ; Manu Mabila [États-Unis] ; Xiangdong Zhou [États-Unis] ; Giada Rossini [Italie] ; Joseph B. Rucker [États-Unis] ; David Avram Sanders [États-Unis] ; Andreas Suhrbier [Australie] ; Vittorio Sambri [Italie] ; Alain Michault [France] ; Marcus O. Muench [États-Unis] ; Benjamin J. Doranz [États-Unis] ; Graham Simmons [États-Unis]Source :
- PLoS Neglected Tropical Diseases [ 1935-2727 ] ; 2013.
Abstract
The mosquito-borne alphavirus, chikungunya virus (CHIKV), has recently reemerged, producing the largest epidemic ever recorded for this virus, with up to 6.5 million cases of acute and chronic rheumatic disease. There are currently no licensed vaccines for CHIKV and current anti-inflammatory drug treatment is often inadequate. Here we describe the isolation and characterization of two human monoclonal antibodies, C9 and E8, from CHIKV infected and recovered individuals. C9 was determined to be a potent virus neutralizing antibody and a biosensor antibody binding study demonstrated it recognized residues on intact CHIKV VLPs. Shotgun mutagenesis alanine scanning of 98 percent of the residues in the E1 and E2 glycoproteins of CHIKV envelope showed that the epitope bound by C9 included amino-acid 162 in the acid-sensitive region (ASR) of the CHIKV E2 glycoprotein. The ASR is critical for the rearrangement of CHIKV E2 during fusion and viral entry into host cells, and we predict that C9 prevents these events from occurring. When used prophylactically in a CHIKV mouse model, C9 completely protected against CHIKV viremia and arthritis. We also observed that when administered therapeutically at 8 or 18 hours post-CHIKV challenge, C9 gave 100% protection in a pathogenic mouse model. Given that targeting this novel neutralizing epitope in E2 can potently protect both in vitro and in vivo, it is likely to be an important region both for future antibody and vaccine-based interventions against CHIKV.
Url:
DOI: 10.1371/journal.pntd.0002423
PubMed: 24069479
PubMed Central: 3772074
Affiliations:
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Sexton</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Blood Systems Research Institute, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Blood Systems Research Institute, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Kahle, Kristen M" sort="Kahle, Kristen M" uniqKey="Kahle K" first="Kristen M." last="Kahle">Kristen M. Kahle</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Integral Molecular, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integral Molecular, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Fong, Rachel H" sort="Fong, Rachel H" uniqKey="Fong R" first="Rachel H." last="Fong">Rachel H. Fong</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Integral Molecular, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integral Molecular, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Mattia, Kimberly Anne" sort="Mattia, Kimberly Anne" uniqKey="Mattia K" first="Kimberly-Anne" last="Mattia">Kimberly-Anne Mattia</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Integral Molecular, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integral Molecular, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Gardner, Joy" sort="Gardner, Joy" uniqKey="Gardner J" first="Joy" last="Gardner">Joy Gardner</name><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Queensland Institute of Medical Research, Brisbane, Queensland, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Queensland Institute of Medical Research, Brisbane, Queensland</wicri:regionArea><wicri:noRegion>Queensland</wicri:noRegion></affiliation></author><author><name sortKey="Lu, Kai" sort="Lu, Kai" uniqKey="Lu K" first="Kai" last="Lu">Kai Lu</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Blood Systems Research Institute, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Blood Systems Research Institute, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Liss, Nathan M" sort="Liss, Nathan M" uniqKey="Liss N" first="Nathan M." last="Liss">Nathan M. Liss</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Blood Systems Research Institute, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Blood Systems Research Institute, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Salvador, Beatriz" sort="Salvador, Beatriz" uniqKey="Salvador B" first="Beatriz" last="Salvador">Beatriz Salvador</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Blood Systems Research Institute, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Blood Systems Research Institute, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Tucker, David F" sort="Tucker, David F" uniqKey="Tucker D" first="David F." last="Tucker">David F. Tucker</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Integral Molecular, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integral Molecular, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Barnes, Trevor" sort="Barnes, Trevor" uniqKey="Barnes T" first="Trevor" last="Barnes">Trevor Barnes</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Integral Molecular, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integral Molecular, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Mabila, Manu" sort="Mabila, Manu" uniqKey="Mabila M" first="Manu" last="Mabila">Manu Mabila</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Integral Molecular, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integral Molecular, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Zhou, Xiangdong" sort="Zhou, Xiangdong" uniqKey="Zhou X" first="Xiangdong" last="Zhou">Xiangdong Zhou</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Integral Molecular, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integral Molecular, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Rossini, Giada" sort="Rossini, Giada" uniqKey="Rossini G" first="Giada" last="Rossini">Giada Rossini</name><affiliation wicri:level="1"><nlm:aff id="aff5"><addr-line>DIMES, Microbiology, University of Bologna, Bologna, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>DIMES, Microbiology, University of Bologna, Bologna</wicri:regionArea><wicri:noRegion>Bologna</wicri:noRegion></affiliation></author><author><name sortKey="Rucker, Joseph B" sort="Rucker, Joseph B" uniqKey="Rucker J" first="Joseph B." last="Rucker">Joseph B. Rucker</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Integral Molecular, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integral Molecular, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Sanders, David Avram" sort="Sanders, David Avram" uniqKey="Sanders D" first="David Avram" last="Sanders">David Avram Sanders</name><affiliation wicri:level="2"><nlm:aff id="aff6"><addr-line>Purdue University, West Lafayette, Indiana, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Purdue University, West Lafayette, Indiana</wicri:regionArea><placeName><region type="state">Indiana</region></placeName></affiliation></author><author><name sortKey="Suhrbier, Andreas" sort="Suhrbier, Andreas" uniqKey="Suhrbier A" first="Andreas" last="Suhrbier">Andreas Suhrbier</name><affiliation wicri:level="1"><nlm:aff id="aff4"><addr-line>Queensland Institute of Medical Research, Brisbane, Queensland, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Queensland Institute of Medical Research, Brisbane, Queensland</wicri:regionArea><wicri:noRegion>Queensland</wicri:noRegion></affiliation></author><author><name sortKey="Sambri, Vittorio" sort="Sambri, Vittorio" uniqKey="Sambri V" first="Vittorio" last="Sambri">Vittorio Sambri</name><affiliation wicri:level="1"><nlm:aff id="aff5"><addr-line>DIMES, Microbiology, University of Bologna, Bologna, Italy</addr-line></nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>DIMES, Microbiology, University of Bologna, Bologna</wicri:regionArea><wicri:noRegion>Bologna</wicri:noRegion></affiliation></author><author><name sortKey="Michault, Alain" sort="Michault, Alain" uniqKey="Michault A" first="Alain" last="Michault">Alain Michault</name><affiliation wicri:level="1"><nlm:aff id="aff7"><addr-line>Centre Hospitalier Universitaire, Groupe Hospitalier Sud-Réunion, La Reunion, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Centre Hospitalier Universitaire, Groupe Hospitalier Sud-Réunion, La Reunion</wicri:regionArea><wicri:noRegion>La Reunion</wicri:noRegion><wicri:noRegion>La Reunion</wicri:noRegion></affiliation></author><author><name sortKey="Muench, Marcus O" sort="Muench, Marcus O" uniqKey="Muench M" first="Marcus O." last="Muench">Marcus O. Muench</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Blood Systems Research Institute, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Blood Systems Research Institute, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Doranz, Benjamin J" sort="Doranz, Benjamin J" uniqKey="Doranz B" first="Benjamin J." last="Doranz">Benjamin J. Doranz</name><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Integral Molecular, Philadelphia, Pennsylvania, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Integral Molecular, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Simmons, Graham" sort="Simmons, Graham" uniqKey="Simmons G" first="Graham" last="Simmons">Graham Simmons</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Blood Systems Research Institute, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Blood Systems Research Institute, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Laboratory Medicine, University of California, San Francisco, San Francisco, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author></analytic><series><title level="j">PLoS Neglected Tropical Diseases</title><idno type="ISSN">1935-2727</idno><idno type="eISSN">1935-2735</idno><imprint><date when="2013">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The mosquito-borne alphavirus, chikungunya virus (CHIKV), has recently reemerged, producing the largest epidemic ever recorded for this virus, with up to 6.5 million cases of acute and chronic rheumatic disease. There are currently no licensed vaccines for CHIKV and current anti-inflammatory drug treatment is often inadequate. Here we describe the isolation and characterization of two human monoclonal antibodies, C9 and E8, from CHIKV infected and recovered individuals. C9 was determined to be a potent virus neutralizing antibody and a biosensor antibody binding study demonstrated it recognized residues on intact CHIKV VLPs. Shotgun mutagenesis alanine scanning of 98 percent of the residues in the E1 and E2 glycoproteins of CHIKV envelope showed that the epitope bound by C9 included amino-acid 162 in the acid-sensitive region (ASR) of the CHIKV E2 glycoprotein. The ASR is critical for the rearrangement of CHIKV E2 during fusion and viral entry into host cells, and we predict that C9 prevents these events from occurring. When used prophylactically in a CHIKV mouse model, C9 completely protected against CHIKV viremia and arthritis. We also observed that when administered therapeutically at 8 or 18 hours post-CHIKV challenge, C9 gave 100% protection in a pathogenic mouse model. Given that targeting this novel neutralizing epitope in E2 can potently protect both in vitro and in vivo, it is likely to be an important region both for future antibody and vaccine-based interventions against CHIKV.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Robinson, Mc" uniqKey="Robinson M">MC Robinson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rezza, G" uniqKey="Rezza G">G Rezza</name></author><author><name sortKey="Nicoletti, L" uniqKey="Nicoletti L">L Nicoletti</name></author><author><name sortKey="Angelini, R" uniqKey="Angelini R">R Angelini</name></author><author><name sortKey="Romi, R" uniqKey="Romi R">R Romi</name></author><author><name sortKey="Finarelli, Ac" uniqKey="Finarelli A">AC Finarelli</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Grandadam, M" uniqKey="Grandadam M">M Grandadam</name></author><author><name sortKey="Caro, V" 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C">CL North</name></author><author><name sortKey="Kuhn, Rj" uniqKey="Kuhn R">RJ Kuhn</name></author><author><name sortKey="Sanders, Da" uniqKey="Sanders D">DA Sanders</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pinna, D" uniqKey="Pinna D">D Pinna</name></author><author><name sortKey="Corti, D" uniqKey="Corti D">D Corti</name></author><author><name sortKey="Jarrossay, D" uniqKey="Jarrossay D">D Jarrossay</name></author><author><name sortKey="Sallusto, F" uniqKey="Sallusto F">F Sallusto</name></author><author><name sortKey="Lanzavecchia, A" uniqKey="Lanzavecchia A">A Lanzavecchia</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Paes, C" uniqKey="Paes C">C Paes</name></author><author><name sortKey="Ingalls, J" uniqKey="Ingalls J">J Ingalls</name></author><author><name sortKey="Kampani, K" uniqKey="Kampani K">K Kampani</name></author><author><name sortKey="Sulli, C" uniqKey="Sulli C">C Sulli</name></author><author><name sortKey="Kakkar, E" uniqKey="Kakkar E">E Kakkar</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gardner, J" uniqKey="Gardner J">J Gardner</name></author><author><name sortKey="Anraku, I" uniqKey="Anraku I">I Anraku</name></author><author><name sortKey="Le, Tt" uniqKey="Le T">TT Le</name></author><author><name sortKey="Larcher, T" uniqKey="Larcher T">T Larcher</name></author><author><name sortKey="Major, L" uniqKey="Major L">L Major</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sambri, V" uniqKey="Sambri V">V Sambri</name></author><author><name sortKey="Cavrini, F" uniqKey="Cavrini F">F Cavrini</name></author><author><name sortKey="Rossini, G" uniqKey="Rossini G">G Rossini</name></author><author><name sortKey="Pierro, A" uniqKey="Pierro A">A Pierro</name></author><author><name sortKey="Landini, Mp" uniqKey="Landini M">MP 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Li</name></author><author><name sortKey="Jose, J" uniqKey="Jose J">J Jose</name></author><author><name sortKey="Xiang, Y" uniqKey="Xiang Y">Y Xiang</name></author><author><name sortKey="Kuhn, Rj" uniqKey="Kuhn R">RJ Kuhn</name></author><author><name sortKey="Rossmann, Mg" uniqKey="Rossmann M">MG Rossmann</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tsetsarkin, Ka" uniqKey="Tsetsarkin K">KA Tsetsarkin</name></author><author><name sortKey="Mcgee, Ce" uniqKey="Mcgee C">CE McGee</name></author><author><name sortKey="Volk, Sm" uniqKey="Volk S">SM Volk</name></author><author><name sortKey="Vanlandingham, Dl" uniqKey="Vanlandingham D">DL Vanlandingham</name></author><author><name sortKey="Weaver, Sc" uniqKey="Weaver S">SC Weaver</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Parren, Pw" uniqKey="Parren P">PW Parren</name></author><author><name sortKey="Burton, Dr" uniqKey="Burton D">DR Burton</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Parren, Pw" uniqKey="Parren P">PW Parren</name></author><author><name sortKey="Geisbert, Tw" uniqKey="Geisbert T">TW Geisbert</name></author><author><name sortKey="Maruyama, T" uniqKey="Maruyama T">T Maruyama</name></author><author><name sortKey="Jahrling, Pb" uniqKey="Jahrling P">PB Jahrling</name></author><author><name sortKey="Burton, Dr" uniqKey="Burton D">DR Burton</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Akahata, W" uniqKey="Akahata W">W Akahata</name></author><author><name sortKey="Nabel, Gj" uniqKey="Nabel G">GJ Nabel</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pence, Df" uniqKey="Pence D">DF Pence</name></author><author><name sortKey="Davis, Nl" uniqKey="Davis N">NL Davis</name></author><author><name sortKey="Johnston, Re" uniqKey="Johnston R">RE Johnston</name></author></analytic></biblStruct></listBibl></div1></back></TEI><affiliations><list><country><li>Australie</li><li>France</li><li>Italie</li><li>États-Unis</li></country><region><li>Californie</li><li>Indiana</li><li>Pennsylvanie</li></region></list><tree><country name="États-Unis"><region name="Californie"><name sortKey="Selvarajah, Suganya" sort="Selvarajah, Suganya" uniqKey="Selvarajah S" first="Suganya" last="Selvarajah">Suganya Selvarajah</name></region><name sortKey="Barnes, Trevor" sort="Barnes, Trevor" uniqKey="Barnes T" first="Trevor" last="Barnes">Trevor Barnes</name><name sortKey="Doranz, Benjamin J" sort="Doranz, Benjamin J" uniqKey="Doranz B" first="Benjamin J." last="Doranz">Benjamin J. Doranz</name><name sortKey="Fong, Rachel H" sort="Fong, Rachel H" uniqKey="Fong R" first="Rachel H." last="Fong">Rachel H. Fong</name><name sortKey="Kahle, Kristen M" sort="Kahle, Kristen M" uniqKey="Kahle K" first="Kristen M." last="Kahle">Kristen M. Kahle</name><name sortKey="Liss, Nathan M" sort="Liss, Nathan M" uniqKey="Liss N" first="Nathan M." last="Liss">Nathan M. Liss</name><name sortKey="Liss, Nathan M" sort="Liss, Nathan M" uniqKey="Liss N" first="Nathan M." last="Liss">Nathan M. Liss</name><name sortKey="Lu, Kai" sort="Lu, Kai" uniqKey="Lu K" first="Kai" last="Lu">Kai Lu</name><name sortKey="Lu, Kai" sort="Lu, Kai" uniqKey="Lu K" first="Kai" last="Lu">Kai Lu</name><name sortKey="Mabila, Manu" sort="Mabila, Manu" uniqKey="Mabila M" first="Manu" last="Mabila">Manu Mabila</name><name sortKey="Mattia, Kimberly Anne" sort="Mattia, Kimberly Anne" uniqKey="Mattia K" first="Kimberly-Anne" last="Mattia">Kimberly-Anne Mattia</name><name sortKey="Muench, Marcus O" sort="Muench, Marcus O" uniqKey="Muench M" first="Marcus O." last="Muench">Marcus O. Muench</name><name sortKey="Muench, Marcus O" sort="Muench, Marcus O" uniqKey="Muench M" first="Marcus O." last="Muench">Marcus O. Muench</name><name sortKey="Rucker, Joseph B" sort="Rucker, Joseph B" uniqKey="Rucker J" first="Joseph B." last="Rucker">Joseph B. Rucker</name><name sortKey="Salvador, Beatriz" sort="Salvador, Beatriz" uniqKey="Salvador B" first="Beatriz" last="Salvador">Beatriz Salvador</name><name sortKey="Salvador, Beatriz" sort="Salvador, Beatriz" uniqKey="Salvador B" first="Beatriz" last="Salvador">Beatriz Salvador</name><name sortKey="Sanders, David Avram" sort="Sanders, David Avram" uniqKey="Sanders D" first="David Avram" last="Sanders">David Avram Sanders</name><name sortKey="Selvarajah, Suganya" sort="Selvarajah, Suganya" uniqKey="Selvarajah S" first="Suganya" last="Selvarajah">Suganya Selvarajah</name><name sortKey="Sexton, Nicole R" sort="Sexton, Nicole R" uniqKey="Sexton N" first="Nicole R." last="Sexton">Nicole R. Sexton</name><name sortKey="Simmons, Graham" sort="Simmons, Graham" uniqKey="Simmons G" first="Graham" last="Simmons">Graham Simmons</name><name sortKey="Simmons, Graham" sort="Simmons, Graham" uniqKey="Simmons G" first="Graham" last="Simmons">Graham Simmons</name><name sortKey="Tucker, David F" sort="Tucker, David F" uniqKey="Tucker D" first="David F." last="Tucker">David F. Tucker</name><name sortKey="Zhou, Xiangdong" sort="Zhou, Xiangdong" uniqKey="Zhou X" first="Xiangdong" last="Zhou">Xiangdong Zhou</name></country><country name="Australie"><noRegion><name sortKey="Gardner, Joy" sort="Gardner, Joy" uniqKey="Gardner J" first="Joy" last="Gardner">Joy Gardner</name></noRegion><name sortKey="Suhrbier, Andreas" sort="Suhrbier, Andreas" uniqKey="Suhrbier A" first="Andreas" last="Suhrbier">Andreas Suhrbier</name></country><country name="Italie"><noRegion><name sortKey="Rossini, Giada" sort="Rossini, Giada" uniqKey="Rossini G" first="Giada" last="Rossini">Giada Rossini</name></noRegion><name sortKey="Sambri, Vittorio" sort="Sambri, Vittorio" uniqKey="Sambri V" first="Vittorio" last="Sambri">Vittorio Sambri</name></country><country name="France"><noRegion><name sortKey="Michault, Alain" sort="Michault, Alain" uniqKey="Michault A" first="Alain" last="Michault">Alain Michault</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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