Productive replication of avian influenza viruses in chicken endothelial cells is determined by hemagglutinin cleavability and is related to innate immune escape.
Identifieur interne : 000549 ( Main/Exploration ); précédent : 000548; suivant : 000550Productive replication of avian influenza viruses in chicken endothelial cells is determined by hemagglutinin cleavability and is related to innate immune escape.
Auteurs : Adrien Lion [France] ; Mathilde Richard [Pays-Bas] ; Evelyne Esnault [France] ; Emmanuel Kut [France] ; Denis Soubieux [France] ; Vanaïque Guillory [France] ; Mélody Germond [France] ; Caroline Blondeau [France] ; Rodrigo Guabiraba [France] ; Kirsty R. Short [Australie] ; Daniel Marc [France] ; Pascale Quéré [France] ; Sascha Trapp [France]Source :
- Virology [ 1096-0341 ] ; 2017.
Abstract
Endotheliotropism is a hallmark of gallinaceous poultry infections with highly pathogenic avian influenza (HPAI) viruses and a feature that distinguishes HPAI from low pathogenic avian influenza (LPAI) viruses. Here, we used chicken aortic endothelial cells (chAEC) as a novel in vitro infection model to assess the susceptibility, permissiveness, and host response of chicken endothelial cells (EC) to infections with avian influenza (AI) viruses. Our data show that productive replication of AI viruses in chAEC is critically determined by hemagglutinin cleavability, and is thus an exclusive trait of HPAI viruses. However, we provide evidence for a link between limited (i.e. trypsin-dependent) replication of certain LPAI viruses, and the viruses' ability to dampen the antiviral innate immune response in infected chAEC. Strikingly, this cell response pattern was also detected in HPAI virus-infected chAEC, suggesting that viral innate immune escape might be a prerequisite for robust AI virus replication in chicken EC.
DOI: 10.1016/j.virol.2017.10.007
PubMed: 29031164
Affiliations:
- Australie, France, Pays-Bas
- Centre-Val de Loire, Hollande-Méridionale, Région Centre
- Rotterdam, Tours
- Université François-Rabelais de Tours
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France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author><author><name sortKey="Richard, Mathilde" sort="Richard, Mathilde" uniqKey="Richard M" first="Mathilde" last="Richard">Mathilde Richard</name><affiliation wicri:level="3"><nlm:affiliation>Erasmus Medical Center, Department of Viroscience, Rotterdam, The Netherlands.</nlm:affiliation><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Erasmus Medical Center, Department of Viroscience, Rotterdam</wicri:regionArea><placeName><settlement type="city">Rotterdam</settlement><region nuts="2" type="province">Hollande-Méridionale</region></placeName></affiliation></author><author><name sortKey="Esnault, Evelyne" sort="Esnault, Evelyne" uniqKey="Esnault E" first="Evelyne" last="Esnault">Evelyne Esnault</name><affiliation wicri:level="4"><nlm:affiliation>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author><author><name sortKey="Kut, Emmanuel" sort="Kut, Emmanuel" uniqKey="Kut E" first="Emmanuel" last="Kut">Emmanuel Kut</name><affiliation wicri:level="4"><nlm:affiliation>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author><author><name sortKey="Soubieux, Denis" sort="Soubieux, Denis" uniqKey="Soubieux D" first="Denis" last="Soubieux">Denis Soubieux</name><affiliation wicri:level="4"><nlm:affiliation>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author><author><name sortKey="Guillory, Vanaique" sort="Guillory, Vanaique" uniqKey="Guillory V" first="Vanaïque" last="Guillory">Vanaïque Guillory</name><affiliation wicri:level="4"><nlm:affiliation>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author><author><name sortKey="Germond, Melody" sort="Germond, Melody" uniqKey="Germond M" first="Mélody" last="Germond">Mélody Germond</name><affiliation wicri:level="4"><nlm:affiliation>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author><author><name sortKey="Blondeau, Caroline" sort="Blondeau, Caroline" uniqKey="Blondeau C" first="Caroline" last="Blondeau">Caroline Blondeau</name><affiliation wicri:level="4"><nlm:affiliation>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author><author><name sortKey="Guabiraba, Rodrigo" sort="Guabiraba, Rodrigo" uniqKey="Guabiraba R" first="Rodrigo" last="Guabiraba">Rodrigo Guabiraba</name><affiliation wicri:level="4"><nlm:affiliation>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author><author><name sortKey="Short, Kirsty R" sort="Short, Kirsty R" uniqKey="Short K" first="Kirsty R" last="Short">Kirsty R. Short</name><affiliation wicri:level="1"><nlm:affiliation>Erasmus Medical Center, Department of Viroscience, Rotterdam, The Netherlands; University of Queensland, School of Biomedical Sciences, Brisbane, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Erasmus Medical Center, Department of Viroscience, Rotterdam, The Netherlands; University of Queensland, School of Biomedical Sciences, Brisbane</wicri:regionArea><wicri:noRegion>Brisbane</wicri:noRegion></affiliation></author><author><name sortKey="Marc, Daniel" sort="Marc, Daniel" uniqKey="Marc D" first="Daniel" last="Marc">Daniel Marc</name><affiliation wicri:level="4"><nlm:affiliation>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author><author><name sortKey="Quere, Pascale" sort="Quere, Pascale" uniqKey="Quere P" first="Pascale" last="Quéré">Pascale Quéré</name><affiliation wicri:level="4"><nlm:affiliation>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author><author><name sortKey="Trapp, Sascha" sort="Trapp, Sascha" uniqKey="Trapp S" first="Sascha" last="Trapp">Sascha Trapp</name><affiliation wicri:level="4"><nlm:affiliation>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly, France. Electronic address: sascha.trapp@inra.fr.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>INRA ISP, Université François Rabelais de Tours, UMR 1282, Nouzilly</wicri:regionArea><wicri:noRegion>Nouzilly</wicri:noRegion><orgName type="university">Université François-Rabelais de Tours</orgName><placeName><settlement type="city">Tours</settlement><region type="old region" nuts="2">Région Centre</region><region type="region" nuts="2">Centre-Val de Loire</region></placeName></affiliation></author></analytic><series><title level="j">Virology</title><idno type="eISSN">1096-0341</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Endotheliotropism is a hallmark of gallinaceous poultry infections with highly pathogenic avian influenza (HPAI) viruses and a feature that distinguishes HPAI from low pathogenic avian influenza (LPAI) viruses. Here, we used chicken aortic endothelial cells (chAEC) as a novel in vitro infection model to assess the susceptibility, permissiveness, and host response of chicken endothelial cells (EC) to infections with avian influenza (AI) viruses. Our data show that productive replication of AI viruses in chAEC is critically determined by hemagglutinin cleavability, and is thus an exclusive trait of HPAI viruses. However, we provide evidence for a link between limited (i.e. trypsin-dependent) replication of certain LPAI viruses, and the viruses' ability to dampen the antiviral innate immune response in infected chAEC. Strikingly, this cell response pattern was also detected in HPAI virus-infected chAEC, suggesting that viral innate immune escape might be a prerequisite for robust AI virus replication in chicken EC.</div></front></TEI><affiliations><list><country><li>Australie</li><li>France</li><li>Pays-Bas</li></country><region><li>Centre-Val de Loire</li><li>Hollande-Méridionale</li><li>Région Centre</li></region><settlement><li>Rotterdam</li><li>Tours</li></settlement><orgName><li>Université François-Rabelais de Tours</li></orgName></list><tree><country name="France"><region name="Région Centre"><name sortKey="Lion, Adrien" sort="Lion, Adrien" uniqKey="Lion A" first="Adrien" last="Lion">Adrien Lion</name></region><name sortKey="Blondeau, Caroline" sort="Blondeau, Caroline" uniqKey="Blondeau C" first="Caroline" last="Blondeau">Caroline Blondeau</name><name sortKey="Esnault, Evelyne" sort="Esnault, Evelyne" uniqKey="Esnault E" first="Evelyne" last="Esnault">Evelyne Esnault</name><name sortKey="Germond, Melody" sort="Germond, Melody" uniqKey="Germond M" first="Mélody" last="Germond">Mélody Germond</name><name sortKey="Guabiraba, Rodrigo" sort="Guabiraba, Rodrigo" uniqKey="Guabiraba R" first="Rodrigo" last="Guabiraba">Rodrigo Guabiraba</name><name sortKey="Guillory, Vanaique" sort="Guillory, Vanaique" uniqKey="Guillory V" first="Vanaïque" last="Guillory">Vanaïque Guillory</name><name sortKey="Kut, Emmanuel" sort="Kut, Emmanuel" uniqKey="Kut E" first="Emmanuel" last="Kut">Emmanuel Kut</name><name sortKey="Marc, Daniel" sort="Marc, Daniel" uniqKey="Marc D" first="Daniel" last="Marc">Daniel Marc</name><name sortKey="Quere, Pascale" sort="Quere, Pascale" uniqKey="Quere P" first="Pascale" last="Quéré">Pascale Quéré</name><name sortKey="Soubieux, Denis" sort="Soubieux, Denis" uniqKey="Soubieux D" first="Denis" last="Soubieux">Denis Soubieux</name><name sortKey="Trapp, Sascha" sort="Trapp, Sascha" uniqKey="Trapp S" first="Sascha" last="Trapp">Sascha Trapp</name></country><country name="Pays-Bas"><region name="Hollande-Méridionale"><name sortKey="Richard, Mathilde" sort="Richard, Mathilde" uniqKey="Richard M" first="Mathilde" last="Richard">Mathilde Richard</name></region></country><country name="Australie"><noRegion><name sortKey="Short, Kirsty R" sort="Short, Kirsty R" uniqKey="Short K" first="Kirsty R" last="Short">Kirsty R. 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