Real-Time Whole-Body Visualization of Chikungunya Virus Infection and Host Interferon Response in Zebrafish
Identifieur interne : 001465 ( Ncbi/Merge ); précédent : 001464; suivant : 001466Real-Time Whole-Body Visualization of Chikungunya Virus Infection and Host Interferon Response in Zebrafish
Auteurs : Nuno Palha [France] ; Florence Guivel-Benhassine [France] ; Valérie Briolat [France] ; Georges Lutfalla [France] ; Marion Sourisseau [France] ; Felix Ellett [Australie] ; Chieh-Huei Wang [Australie] ; Graham J. Lieschke [Australie] ; Philippe Herbomel [France] ; Olivier Schwartz [France] ; Jean-Pierre Levraud [France]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2013.
Abstract
Chikungunya Virus (CHIKV), a re-emerging arbovirus that may cause severe disease, constitutes an important public health problem. Herein we describe a novel CHIKV infection model in zebrafish, where viral spread was live-imaged in the whole body up to cellular resolution. Infected cells emerged in various organs in one principal wave with a median appearance time of ∼14 hours post infection. Timing of infected cell death was organ dependent, leading to a shift of CHIKV localization towards the brain. As in mammals, CHIKV infection triggered a strong type-I interferon (IFN) response, critical for survival. IFN was mainly expressed by neutrophils and hepatocytes. Cell type specific ablation experiments further demonstrated that neutrophils play a crucial, unexpected role in CHIKV containment. Altogether, our results show that the zebrafish represents a novel valuable model to dynamically visualize replication, pathogenesis and host responses to a human virus.
Url:
DOI: 10.1371/journal.ppat.1003619
PubMed: 24039582
PubMed Central: 3764224
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France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Macrophages et Développement de l'Immunité, Department of Developmental and Stem Cells Biology, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>CNRS URA2578, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS URA2578, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff3"><addr-line>Université Pierre et Marie Curie, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Pierre et Marie Curie, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement><settlement type="city">Paris</settlement></placeName><orgName type="university">Université Pierre-et-Marie-Curie</orgName></affiliation></author><author><name sortKey="Guivel Benhassine, Florence" sort="Guivel Benhassine, Florence" uniqKey="Guivel Benhassine F" first="Florence" last="Guivel-Benhassine">Florence Guivel-Benhassine</name><affiliation wicri:level="3"><nlm:aff id="aff4"><addr-line>Institut Pasteur, Virus et Immunité, Department of Virology, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Virus et Immunité, Department of Virology, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff5"><addr-line>CNRS URA3015, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS URA3015, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Briolat, Valerie" sort="Briolat, Valerie" uniqKey="Briolat V" first="Valérie" last="Briolat">Valérie Briolat</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut Pasteur, Macrophages et Développement de l'Immunité, Department of Developmental and Stem Cells Biology, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Macrophages et Développement de l'Immunité, Department of Developmental and Stem Cells Biology, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>CNRS URA2578, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS URA2578, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Lutfalla, Georges" sort="Lutfalla, Georges" uniqKey="Lutfalla G" first="Georges" last="Lutfalla">Georges Lutfalla</name><affiliation wicri:level="3"><nlm:aff id="aff6"><addr-line>CNRS UMR5235, Dynamiques des Interactions Membranaires et Pathologiques, Montpellier, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS UMR5235, Dynamiques des Interactions Membranaires et Pathologiques, Montpellier</wicri:regionArea><placeName><region type="region">Occitanie (région administrative)</region><region type="old region">Languedoc-Roussillon</region><settlement type="city">Montpellier</settlement></placeName></affiliation><affiliation wicri:level="4"><nlm:aff id="aff7"><addr-line>Université Montpellier II, Montpellier, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Université Montpellier II, Montpellier</wicri:regionArea><placeName><region type="region">Occitanie (région administrative)</region><region type="old region">Languedoc-Roussillon</region><settlement type="city">Montpellier</settlement><settlement type="city">Montpellier</settlement></placeName><orgName type="university">Université Montpellier 2</orgName></affiliation></author><author><name sortKey="Sourisseau, Marion" sort="Sourisseau, Marion" uniqKey="Sourisseau M" first="Marion" last="Sourisseau">Marion Sourisseau</name><affiliation wicri:level="3"><nlm:aff id="aff4"><addr-line>Institut Pasteur, Virus et Immunité, Department of Virology, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Virus et Immunité, Department of Virology, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff5"><addr-line>CNRS URA3015, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS URA3015, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Ellett, Felix" sort="Ellett, Felix" uniqKey="Ellett F" first="Felix" last="Ellett">Felix Ellett</name><affiliation wicri:level="1"><nlm:aff id="aff8"><addr-line>Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Wang, Chieh Huei" sort="Wang, Chieh Huei" uniqKey="Wang C" first="Chieh-Huei" last="Wang">Chieh-Huei Wang</name><affiliation wicri:level="1"><nlm:aff id="aff8"><addr-line>Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Lieschke, Graham J" sort="Lieschke, Graham J" uniqKey="Lieschke G" first="Graham J." last="Lieschke">Graham J. Lieschke</name><affiliation wicri:level="1"><nlm:aff id="aff8"><addr-line>Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria</wicri:regionArea><wicri:noRegion>Victoria</wicri:noRegion></affiliation></author><author><name sortKey="Herbomel, Philippe" sort="Herbomel, Philippe" uniqKey="Herbomel P" first="Philippe" last="Herbomel">Philippe Herbomel</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut Pasteur, Macrophages et Développement de l'Immunité, Department of Developmental and Stem Cells Biology, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Macrophages et Développement de l'Immunité, Department of Developmental and Stem Cells Biology, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>CNRS URA2578, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS URA2578, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Schwartz, Olivier" sort="Schwartz, Olivier" uniqKey="Schwartz O" first="Olivier" last="Schwartz">Olivier Schwartz</name><affiliation wicri:level="3"><nlm:aff id="aff4"><addr-line>Institut Pasteur, Virus et Immunité, Department of Virology, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Virus et Immunité, Department of Virology, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff5"><addr-line>CNRS URA3015, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS URA3015, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Levraud, Jean Pierre" sort="Levraud, Jean Pierre" uniqKey="Levraud J" first="Jean-Pierre" last="Levraud">Jean-Pierre Levraud</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>Institut Pasteur, Macrophages et Développement de l'Immunité, Department of Developmental and Stem Cells Biology, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Institut Pasteur, Macrophages et Développement de l'Immunité, Department of Developmental and Stem Cells Biology, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>CNRS URA2578, Paris, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>CNRS URA2578, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author></analytic><series><title level="j">PLoS Pathogens</title><idno type="ISSN">1553-7366</idno><idno type="eISSN">1553-7374</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>Chikungunya Virus (CHIKV), a re-emerging arbovirus that may cause severe disease, constitutes an important public health problem. Herein we describe a novel CHIKV infection model in zebrafish, where viral spread was live-imaged in the whole body up to cellular resolution. Infected cells emerged in various organs in one principal wave with a median appearance time of ∼14 hours post infection. Timing of infected cell death was organ dependent, leading to a shift of CHIKV localization towards the brain. As in mammals, CHIKV infection triggered a strong type-I interferon (IFN) response, critical for survival. IFN was mainly expressed by neutrophils and hepatocytes. Cell type specific ablation experiments further demonstrated that neutrophils play a crucial, unexpected role in CHIKV containment. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS Pathog</journal-id><journal-id journal-id-type="iso-abbrev">PLoS Pathog</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plospath</journal-id><journal-title-group><journal-title>PLoS Pathogens</journal-title></journal-title-group><issn pub-type="ppub">1553-7366</issn><issn pub-type="epub">1553-7374</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24039582</article-id><article-id pub-id-type="pmc">3764224</article-id><article-id pub-id-type="publisher-id">PPATHOGENS-D-13-00510</article-id><article-id pub-id-type="doi">10.1371/journal.ppat.1003619</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v2"><subject>Biology</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immunity</subject><subj-group><subject>Immunity to Infections</subject><subject>Innate Immunity</subject></subj-group></subj-group><subj-group><subject>Immune Response</subject></subj-group></subj-group><subj-group><subject>Microbiology</subject><subj-group><subject>Virology</subject><subj-group><subject>Viral Transmission and Infection</subject><subj-group><subject>Host Cells</subject><subject>Neuroinvasiveness</subject><subject>Viral Clearance</subject></subj-group></subj-group><subj-group><subject>Animal Models of Infection</subject></subj-group></subj-group><subj-group><subject>Host-Pathogen Interaction</subject></subj-group></subj-group><subj-group><subject>Model Organisms</subject><subj-group><subject>Animal Models</subject><subj-group><subject>Zebrafish</subject></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Real-Time Whole-Body Visualization of Chikungunya Virus Infection and Host Interferon Response in Zebrafish</article-title><alt-title alt-title-type="running-head">Whole-Body Visualization of CHIKV Infection</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Palha</surname><given-names>Nuno</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="aff" rid="aff3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Guivel-Benhassine</surname><given-names>Florence</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Briolat</surname><given-names>Valérie</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lutfalla</surname><given-names>Georges</given-names></name><xref ref-type="aff" rid="aff6"><sup>6</sup></xref><xref ref-type="aff" rid="aff7"><sup>7</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sourisseau</surname><given-names>Marion</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>¤a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ellett</surname><given-names>Felix</given-names></name><xref ref-type="aff" rid="aff8"><sup>8</sup></xref><xref ref-type="author-notes" rid="fn2"><sup>¤b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Chieh-Huei</given-names></name><xref ref-type="aff" rid="aff8"><sup>8</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lieschke</surname><given-names>Graham J.</given-names></name><xref ref-type="aff" rid="aff8"><sup>8</sup></xref></contrib><contrib contrib-type="author"><name><surname>Herbomel</surname><given-names>Philippe</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Schwartz</surname><given-names>Olivier</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref><xref ref-type="aff" rid="aff5"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Levraud</surname><given-names>Jean-Pierre</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib></contrib-group><aff id="aff1"><label>1</label><addr-line>Institut Pasteur, Macrophages et Développement de l'Immunité, Department of Developmental and Stem Cells Biology, Paris, France</addr-line></aff><aff id="aff2"><label>2</label><addr-line>CNRS URA2578, Paris, France</addr-line></aff><aff id="aff3"><label>3</label><addr-line>Université Pierre et Marie Curie, Paris, France</addr-line></aff><aff id="aff4"><label>4</label><addr-line>Institut Pasteur, Virus et Immunité, Department of Virology, Paris, France</addr-line></aff><aff id="aff5"><label>5</label><addr-line>CNRS URA3015, Paris, France</addr-line></aff><aff id="aff6"><label>6</label><addr-line>CNRS UMR5235, Dynamiques des Interactions Membranaires et Pathologiques, Montpellier, France</addr-line></aff><aff id="aff7"><label>7</label><addr-line>Université Montpellier II, Montpellier, France</addr-line></aff><aff id="aff8"><label>8</label><addr-line>Australian Regenerative Medicine Institute, Monash University, Clayton, Victoria, Australia</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Heise</surname><given-names>Mark T.</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>University of North Carolina at Chapel Hill, United States of America</addr-line></aff><author-notes><corresp id="cor1">* E-mail: <email>jean-pierre.levraud@pasteur.fr</email></corresp><fn fn-type="COI-statement"><p>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p>Conceived and designed the experiments: JPL OS NP. Performed the experiments: NP JPL FGB MS GL VB CHW. Analyzed the data: NP JPL OS PH. Contributed reagents/materials/analysis tools: FE GJL. Wrote the paper: NP JPL OS.</p></fn><fn id="fn1" fn-type="current-aff"><label>¤a</label><p>Current address: Mount Sinai School of Medicine, New York, New York, United States of America.</p></fn><fn id="fn2" fn-type="current-aff"><label>¤b</label><p>Current address: MRC Centre for Developmental and Biomedical Genetics, Sheffield, United Kingdom.</p></fn></author-notes><pub-date pub-type="collection"><month>9</month><year>2013</year></pub-date><pub-date pub-type="epub"><day>5</day><month>9</month><year>2013</year></pub-date><volume>9</volume><issue>9</issue><elocation-id>e1003619</elocation-id><history><date date-type="received"><day>22</day><month>2</month><year>2013</year></date><date date-type="accepted"><day>29</day><month>7</month><year>2013</year></date></history><permissions><copyright-statement>© 2013 Palha et al</copyright-statement><copyright-year>2013</copyright-year><copyright-holder>Palha et al</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, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.</license-p></license></permissions><abstract><p>Chikungunya Virus (CHIKV), a re-emerging arbovirus that may cause severe disease, constitutes an important public health problem. Herein we describe a novel CHIKV infection model in zebrafish, where viral spread was live-imaged in the whole body up to cellular resolution. Infected cells emerged in various organs in one principal wave with a median appearance time of ∼14 hours post infection. Timing of infected cell death was organ dependent, leading to a shift of CHIKV localization towards the brain. As in mammals, CHIKV infection triggered a strong type-I interferon (IFN) response, critical for survival. IFN was mainly expressed by neutrophils and hepatocytes. Cell type specific ablation experiments further demonstrated that neutrophils play a crucial, unexpected role in CHIKV containment. Altogether, our results show that the zebrafish represents a novel valuable model to dynamically visualize replication, pathogenesis and host responses to a human virus.</p></abstract><abstract abstract-type="summary"><title>Author Summary</title><p>Chikungunya, a re-emerging disease caused by a mosquito-transmitted virus, is an important public health problem. We developed a zebrafish model for chikungunya virus infection. For the first time, rise and death of virus-infected cells could be live imaged in the entire body of a vertebrate. We observed a widespread wave of apparition of newly infected cells during the first day after inoculation of the virus. We then found that infected cells died at a strongly organ-dependent rate, accounting for the progressive shift of virus localization. Notably, the virus persisted in the brain despite apparent recovery of infected zebrafish. We found this recovery to be critically dependent on the host type I interferon response. Surprisingly, we identified neutrophils as a major cell population expressing interferon and controlling chikungunya virus.</p></abstract><funding-group><funding-statement>This work was financed by the Agence Nationale de la Recherche (Zebraflam grant ANR-10-MIDI-009, and CHIK-HOST-PATH2 grant), Region Ile-de-France (DIM-Malinf), and institutional grants from the Institut Pasteur and CNRS. NP is endowed with a fellowship from Fundação para a Ciência e a Tecnologia (SFRH/BD/60678/2009). GJL is supported by the National Health and Medical Research Council (grants 461208 and 637394). The Australian Regenerative Medicine Institute is supported by grants from the State Government of Victoria and the Australian Government. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><page-count count="15"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>Australie</li><li>France</li></country><region><li>Languedoc-Roussillon</li><li>Occitanie (région administrative)</li><li>Île-de-France</li></region><settlement><li>Montpellier</li><li>Paris</li></settlement><orgName><li>Université Montpellier 2</li><li>Université Pierre-et-Marie-Curie</li></orgName></list><tree><country name="France"><region name="Île-de-France"><name sortKey="Palha, Nuno" sort="Palha, Nuno" uniqKey="Palha N" first="Nuno" last="Palha">Nuno Palha</name></region><name sortKey="Briolat, Valerie" sort="Briolat, Valerie" uniqKey="Briolat V" first="Valérie" last="Briolat">Valérie Briolat</name><name sortKey="Briolat, Valerie" sort="Briolat, Valerie" uniqKey="Briolat V" first="Valérie" last="Briolat">Valérie Briolat</name><name sortKey="Guivel Benhassine, Florence" sort="Guivel Benhassine, Florence" uniqKey="Guivel Benhassine F" first="Florence" last="Guivel-Benhassine">Florence Guivel-Benhassine</name><name sortKey="Guivel Benhassine, Florence" sort="Guivel Benhassine, Florence" uniqKey="Guivel Benhassine F" first="Florence" last="Guivel-Benhassine">Florence Guivel-Benhassine</name><name sortKey="Herbomel, Philippe" sort="Herbomel, Philippe" uniqKey="Herbomel P" first="Philippe" last="Herbomel">Philippe Herbomel</name><name sortKey="Herbomel, Philippe" sort="Herbomel, Philippe" uniqKey="Herbomel P" first="Philippe" last="Herbomel">Philippe Herbomel</name><name sortKey="Levraud, Jean Pierre" sort="Levraud, Jean Pierre" uniqKey="Levraud J" first="Jean-Pierre" last="Levraud">Jean-Pierre Levraud</name><name sortKey="Levraud, Jean Pierre" sort="Levraud, Jean Pierre" uniqKey="Levraud J" first="Jean-Pierre" last="Levraud">Jean-Pierre Levraud</name><name sortKey="Lutfalla, Georges" sort="Lutfalla, Georges" uniqKey="Lutfalla G" first="Georges" last="Lutfalla">Georges Lutfalla</name><name sortKey="Lutfalla, Georges" sort="Lutfalla, Georges" uniqKey="Lutfalla G" first="Georges" last="Lutfalla">Georges Lutfalla</name><name sortKey="Palha, Nuno" sort="Palha, Nuno" uniqKey="Palha N" first="Nuno" last="Palha">Nuno Palha</name><name sortKey="Palha, Nuno" sort="Palha, Nuno" uniqKey="Palha N" first="Nuno" last="Palha">Nuno Palha</name><name sortKey="Schwartz, Olivier" sort="Schwartz, Olivier" uniqKey="Schwartz O" first="Olivier" last="Schwartz">Olivier Schwartz</name><name sortKey="Schwartz, Olivier" sort="Schwartz, Olivier" uniqKey="Schwartz O" first="Olivier" last="Schwartz">Olivier Schwartz</name><name sortKey="Sourisseau, Marion" sort="Sourisseau, Marion" uniqKey="Sourisseau M" first="Marion" last="Sourisseau">Marion Sourisseau</name><name sortKey="Sourisseau, Marion" sort="Sourisseau, Marion" uniqKey="Sourisseau M" first="Marion" last="Sourisseau">Marion Sourisseau</name></country><country name="Australie"><noRegion><name sortKey="Ellett, Felix" sort="Ellett, Felix" uniqKey="Ellett F" first="Felix" last="Ellett">Felix Ellett</name></noRegion><name sortKey="Lieschke, Graham J" sort="Lieschke, Graham J" uniqKey="Lieschke G" first="Graham J." last="Lieschke">Graham J. Lieschke</name><name sortKey="Wang, Chieh Huei" sort="Wang, Chieh Huei" uniqKey="Wang C" first="Chieh-Huei" last="Wang">Chieh-Huei Wang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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