Three mutations switch H7N9 influenza to human-type receptor specificity
Identifieur interne : 000B89 ( Pmc/Curation ); précédent : 000B88; suivant : 000B90Three mutations switch H7N9 influenza to human-type receptor specificity
Auteurs : Robert P. De Vries [États-Unis, Pays-Bas] ; Wenjie Peng [États-Unis] ; Oliver C. Grant [États-Unis] ; Andrew J. Thompson [États-Unis] ; Xueyong Zhu [États-Unis] ; Kim M. Bouwman [Pays-Bas] ; Alba T. Torrents De La Pena [Pays-Bas] ; Marielle J. Van Breemen [Pays-Bas] ; Iresha N. Ambepitiya Wickramasinghe [Pays-Bas] ; Cornelis A. M. De Haan [Pays-Bas] ; Wenli Yu [États-Unis] ; Ryan Mcbride [États-Unis] ; Rogier W. Sanders [Pays-Bas, États-Unis] ; Robert J. Woods [États-Unis] ; Monique H. Verheije [Pays-Bas] ; Ian A. Wilson [États-Unis] ; James C. Paulson [États-Unis]Source :
- PLoS Pathogens [ 1553-7366 ] ; 2017.
Abstract
The avian H7N9 influenza outbreak in 2013 resulted from an unprecedented incidence of influenza transmission to humans from infected poultry. The majority of human H7N9 isolates contained a hemagglutinin (HA) mutation (Q226L) that has previously been associated with a switch in receptor specificity from avian-type (NeuAcα2-3Gal) to human-type (NeuAcα2-6Gal), as documented for the avian progenitors of the 1957 (H2N2) and 1968 (H3N2) human influenza pandemic viruses. While this raised concern that the H7N9 virus was adapting to humans, the mutation was not sufficient to switch the receptor specificity of H7N9, and has not resulted in sustained transmission in humans. To determine if the H7 HA was capable of acquiring human-type receptor specificity, we conducted mutation analyses. Remarkably, three amino acid mutations conferred a switch in specificity for human-type receptors that resembled the specificity of the 2009 human H1 pandemic virus, and promoted binding to human trachea epithelial cells.
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DOI: 10.1371/journal.ppat.1006390
PubMed: 28617868
PubMed Central: 5472306
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De Vries</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Department of Chemical Biology and Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht University, CG Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Department of Chemical Biology and Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht University, CG Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Peng, Wenjie" sort="Peng, Wenjie" uniqKey="Peng W" first="Wenjie" last="Peng">Wenjie Peng</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation></author><author><name sortKey="Grant, Oliver C" sort="Grant, Oliver C" uniqKey="Grant O" first="Oliver C." last="Grant">Oliver C. 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Paulson</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28617868</idno><idno type="pmc">5472306</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5472306</idno><idno type="RBID">PMC:5472306</idno><idno type="doi">10.1371/journal.ppat.1006390</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">000B89</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000B89</idno><idno type="wicri:Area/Pmc/Curation">000B89</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000B89</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Three mutations switch H7N9 influenza to human-type receptor specificity</title><author><name sortKey="De Vries, Robert P" sort="De Vries, Robert P" uniqKey="De Vries R" first="Robert P." last="De Vries">Robert P. De Vries</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Department of Chemical Biology and Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht University, CG Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Department of Chemical Biology and Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht University, CG Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Peng, Wenjie" sort="Peng, Wenjie" uniqKey="Peng W" first="Wenjie" last="Peng">Wenjie Peng</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation></author><author><name sortKey="Grant, Oliver C" sort="Grant, Oliver C" uniqKey="Grant O" first="Oliver C." last="Grant">Oliver C. Grant</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Complex Carbohydrate Research Center, University of Georgia, Athens, GA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Complex Carbohydrate Research Center, University of Georgia, Athens, GA</wicri:regionArea></affiliation></author><author><name sortKey="Thompson, Andrew J" sort="Thompson, Andrew J" uniqKey="Thompson A" first="Andrew J." last="Thompson">Andrew J. Thompson</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation></author><author><name sortKey="Zhu, Xueyong" sort="Zhu, Xueyong" uniqKey="Zhu X" first="Xueyong" last="Zhu">Xueyong Zhu</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation></author><author><name sortKey="Bouwman, Kim M" sort="Bouwman, Kim M" uniqKey="Bouwman K" first="Kim M." last="Bouwman">Kim M. Bouwman</name><affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Pathology Division, Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, CL Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Pathology Division, Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, CL Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="De La Pena, Alba T Torrents" sort="De La Pena, Alba T Torrents" uniqKey="De La Pena A" first="Alba T. Torrents" last="De La Pena">Alba T. Torrents De La Pena</name><affiliation wicri:level="1"><nlm:aff id="aff006"><addr-line>Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, AZ Amsterdam, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, AZ Amsterdam</wicri:regionArea></affiliation></author><author><name sortKey="Van Breemen, Marielle J" sort="Van Breemen, Marielle J" uniqKey="Van Breemen M" first="Marielle J." last="Van Breemen">Marielle J. Van Breemen</name><affiliation wicri:level="1"><nlm:aff id="aff006"><addr-line>Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, AZ Amsterdam, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, AZ Amsterdam</wicri:regionArea></affiliation></author><author><name sortKey="Ambepitiya Wickramasinghe, Iresha N" sort="Ambepitiya Wickramasinghe, Iresha N" uniqKey="Ambepitiya Wickramasinghe I" first="Iresha N." last="Ambepitiya Wickramasinghe">Iresha N. Ambepitiya Wickramasinghe</name><affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Pathology Division, Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, CL Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Pathology Division, Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, CL Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="De Haan, Cornelis A M" sort="De Haan, Cornelis A M" uniqKey="De Haan C" first="Cornelis A. M." last="De Haan">Cornelis A. M. De Haan</name><affiliation wicri:level="1"><nlm:aff id="aff007"><addr-line>Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1,CL Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1,CL Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Yu, Wenli" sort="Yu, Wenli" uniqKey="Yu W" first="Wenli" last="Yu">Wenli Yu</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation></author><author><name sortKey="Mcbride, Ryan" sort="Mcbride, Ryan" uniqKey="Mcbride R" first="Ryan" last="Mcbride">Ryan Mcbride</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation></author><author><name sortKey="Sanders, Rogier W" sort="Sanders, Rogier W" uniqKey="Sanders R" first="Rogier W." last="Sanders">Rogier W. Sanders</name><affiliation wicri:level="1"><nlm:aff id="aff006"><addr-line>Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, AZ Amsterdam, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, AZ Amsterdam</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff008"><addr-line>Department of Microbiology and Immunology, Weil Medical College of Cornell University, New York, NY, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Immunology, Weil Medical College of Cornell University, New York, NY</wicri:regionArea></affiliation></author><author><name sortKey="Woods, Robert J" sort="Woods, Robert J" uniqKey="Woods R" first="Robert J." last="Woods">Robert J. Woods</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Complex Carbohydrate Research Center, University of Georgia, Athens, GA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Complex Carbohydrate Research Center, University of Georgia, Athens, GA</wicri:regionArea></affiliation></author><author><name sortKey="Verheije, Monique H" sort="Verheije, Monique H" uniqKey="Verheije M" first="Monique H." last="Verheije">Monique H. Verheije</name><affiliation wicri:level="1"><nlm:aff id="aff005"><addr-line>Pathology Division, Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, CL Utrecht, The Netherlands</addr-line></nlm:aff><country xml:lang="fr">Pays-Bas</country><wicri:regionArea>Pathology Division, Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, CL Utrecht</wicri:regionArea></affiliation></author><author><name sortKey="Wilson, Ian A" sort="Wilson, Ian A" uniqKey="Wilson I" first="Ian A." last="Wilson">Ian A. Wilson</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff009"><addr-line>Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></affiliation></author><author><name sortKey="Paulson, James C" sort="Paulson, James C" uniqKey="Paulson J" first="James C." last="Paulson">James C. Paulson</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA</wicri:regionArea></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="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The avian H7N9 influenza outbreak in 2013 resulted from an unprecedented incidence of influenza transmission to humans from infected poultry. The majority of human H7N9 isolates contained a hemagglutinin (HA) mutation (Q226L) that has previously been associated with a switch in receptor specificity from avian-type (NeuAcα2-3Gal) to human-type (NeuAcα2-6Gal), as documented for the avian progenitors of the 1957 (H2N2) and 1968 (H3N2) human influenza pandemic viruses. While this raised concern that the H7N9 virus was adapting to humans, the mutation was not sufficient to switch the receptor specificity of H7N9, and has not resulted in sustained transmission in humans. To determine if the H7 HA was capable of acquiring human-type receptor specificity, we conducted mutation analyses. Remarkably, three amino acid mutations conferred a switch in specificity for human-type receptors that resembled the specificity of the 2009 human H1 pandemic virus, and promoted binding to human trachea epithelial cells.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Chen, Y" uniqKey="Chen Y">Y Chen</name></author><author><name sortKey="Liang, W" uniqKey="Liang W">W Liang</name></author><author><name sortKey="Yang, S" uniqKey="Yang S">S Yang</name></author><author><name sortKey="Wu, N" uniqKey="Wu N">N Wu</name></author><author><name sortKey="Gao, H" uniqKey="Gao H">H Gao</name></author><author><name sortKey="Sheng, J" uniqKey="Sheng J">J Sheng</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Hu, J" uniqKey="Hu J">J Hu</name></author><author><name sortKey="Zhu, Y" uniqKey="Zhu Y">Y Zhu</name></author><author><name sortKey="Zhao, B" uniqKey="Zhao B">B 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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, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28617868</article-id><article-id pub-id-type="pmc">5472306</article-id><article-id pub-id-type="doi">10.1371/journal.ppat.1006390</article-id><article-id pub-id-type="publisher-id">PPATHOGENS-D-16-02788</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Chemical Characterization</subject><subj-group><subject>Binding Analysis</subject><subj-group><subject>Receptor Binding Assays</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H7N9</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical microbiology</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H7N9</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Pathology and laboratory medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H7N9</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H7N9</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Microbial Mutation</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Respiratory System</subject><subj-group><subject>Trachea</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Anatomy</subject><subj-group><subject>Respiratory System</subject><subj-group><subject>Trachea</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H1N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical microbiology</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H1N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Pathology and laboratory medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H1N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H1N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Animals</subject><subj-group><subject>Vertebrates</subject><subj-group><subject>Amniotes</subject><subj-group><subject>Birds</subject><subj-group><subject>Fowl</subject><subj-group><subject>Gamefowl</subject><subj-group><subject>Chickens</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Animals</subject><subj-group><subject>Vertebrates</subject><subj-group><subject>Amniotes</subject><subj-group><subject>Birds</subject><subj-group><subject>Poultry</subject><subj-group><subject>Chickens</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H5N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical microbiology</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H5N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Pathology and laboratory medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H5N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject><subj-group><subject>H5N1</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Infectious Diseases</subject><subj-group><subject>Zoonoses</subject><subj-group><subject>H5N1</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>RNA viruses</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Microbiology</subject><subj-group><subject>Medical microbiology</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and health sciences</subject><subj-group><subject>Pathology and laboratory medicine</subject><subj-group><subject>Pathogens</subject><subj-group><subject>Microbial pathogens</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and life sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Viruses</subject><subj-group><subject>Viral pathogens</subject><subj-group><subject>Orthomyxoviruses</subject><subj-group><subject>Influenza viruses</subject><subj-group><subject>Influenza A virus</subject></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Three mutations switch H7N9 influenza to human-type receptor specificity</article-title><alt-title alt-title-type="running-head">H7N9 human-type receptor binding</alt-title></title-group><contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>de Vries</surname><given-names>Robert P.</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-5093-7115</contrib-id><name><surname>Peng</surname><given-names>Wenjie</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Grant</surname><given-names>Oliver C.</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Thompson</surname><given-names>Andrew J.</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zhu</surname><given-names>Xueyong</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bouwman</surname><given-names>Kim M.</given-names></name><xref ref-type="aff" rid="aff005"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>de la Pena</surname><given-names>Alba T. Torrents</given-names></name><xref ref-type="aff" rid="aff006"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>van Breemen</surname><given-names>Marielle J.</given-names></name><xref ref-type="aff" rid="aff006"><sup>6</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ambepitiya Wickramasinghe</surname><given-names>Iresha N.</given-names></name><xref ref-type="aff" rid="aff005"><sup>5</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0002-4459-9874</contrib-id><name><surname>de Haan</surname><given-names>Cornelis A. M.</given-names></name><xref ref-type="aff" rid="aff007"><sup>7</sup></xref></contrib><contrib contrib-type="author"><name><surname>Yu</surname><given-names>Wenli</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0001-8616-1910</contrib-id><name><surname>McBride</surname><given-names>Ryan</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Sanders</surname><given-names>Rogier W.</given-names></name><xref ref-type="aff" rid="aff006"><sup>6</sup></xref><xref ref-type="aff" rid="aff008"><sup>8</sup></xref></contrib><contrib contrib-type="author"><name><surname>Woods</surname><given-names>Robert J.</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-1274-2987</contrib-id><name><surname>Verheije</surname><given-names>Monique H.</given-names></name><xref ref-type="aff" rid="aff005"><sup>5</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wilson</surname><given-names>Ian A.</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref><xref ref-type="aff" rid="aff009"><sup>9</sup></xref></contrib><contrib contrib-type="author"><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-4589-5322</contrib-id><name><surname>Paulson</surname><given-names>James C.</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Departments of Molecular Medicine, & Immunology and Microbiology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Department of Chemical Biology and Drug Discovery, Utrecht Institute for Pharmaceutical Sciences, Utrecht University, CG Utrecht, The Netherlands</addr-line></aff><aff id="aff003"><label>3</label><addr-line>Complex Carbohydrate Research Center, University of Georgia, Athens, GA, United States of America</addr-line></aff><aff id="aff004"><label>4</label><addr-line>Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></aff><aff id="aff005"><label>5</label><addr-line>Pathology Division, Department of Pathobiology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, CL Utrecht, The Netherlands</addr-line></aff><aff id="aff006"><label>6</label><addr-line>Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, AZ Amsterdam, The Netherlands</addr-line></aff><aff id="aff007"><label>7</label><addr-line>Virology Division, Department of Infectious Diseases & Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1,CL Utrecht, The Netherlands</addr-line></aff><aff id="aff008"><label>8</label><addr-line>Department of Microbiology and Immunology, Weil Medical College of Cornell University, New York, NY, United States of America</addr-line></aff><aff id="aff009"><label>9</label><addr-line>Skaggs Institute for Chemical Biology, The Scripps Research Institute, La Jolla, CA, United States of America</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Fernandez-Sesma</surname><given-names>Ana</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Icahn School of Medicine at Mount Sinai, UNITED STATES</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p><list list-type="simple"><list-item><p><bold>Conceptualization:</bold> RPdV WP XZ IAW JCP.</p></list-item><list-item><p><bold>Data curation:</bold> RPdV AJT XZ KMB ATTdlP INAW RM RWS IAW JCP.</p></list-item><list-item><p><bold>Formal analysis:</bold> RPdV AJT XZ KMB ATTdlP OCG RWS RJW.</p></list-item><list-item><p><bold>Funding acquisition:</bold> RPdV AJT MHV CAMdH RJW IAW JCP.</p></list-item><list-item><p><bold>Investigation:</bold> RPdV AJT XZ KMB INAW RM OCG.</p></list-item><list-item><p><bold>Methodology:</bold> RPdV WP AJT XZ OCG RM MHV IAW JCP.</p></list-item><list-item><p><bold>Project administration:</bold> RPdV MHV IAW JCP.</p></list-item><list-item><p><bold>Resources:</bold> RPdV WP RM WY RJW MHV CAMdH IAW JCP.</p></list-item><list-item><p><bold>Software:</bold> RM OCG.</p></list-item><list-item><p><bold>Supervision:</bold> RPdV RJW MHV IAW JCP.</p></list-item><list-item><p><bold>Validation:</bold> RPdV MHV IAW JCP.</p></list-item><list-item><p><bold>Visualization:</bold> RPdV OCG AJT XZ ATTdlP RWS JCP.</p></list-item><list-item><p><bold>Writing – original draft:</bold> RPdV JCP.</p></list-item><list-item><p><bold>Writing – review & editing:</bold> RPdV WP OCG AJT XZ KMB ATTdlP MJvB INAW CAMdH WY RM RJW MHV IAW JCP.</p></list-item></list></p></fn><corresp id="cor001">* E-mail: <email>jpaulson@scripps.edu</email></corresp></author-notes><pub-date pub-type="epub"><day>15</day><month>6</month><year>2017</year></pub-date><pub-date pub-type="collection"><month>6</month><year>2017</year></pub-date><volume>13</volume><issue>6</issue><elocation-id>e1006390</elocation-id><history><date date-type="received"><day>21</day><month>12</month><year>2016</year></date><date date-type="accepted"><day>28</day><month>4</month><year>2017</year></date></history><permissions><copyright-statement>© 2017 de Vries et al</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>de Vries 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 <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="ppat.1006390.pdf"></self-uri><abstract><p>The avian H7N9 influenza outbreak in 2013 resulted from an unprecedented incidence of influenza transmission to humans from infected poultry. The majority of human H7N9 isolates contained a hemagglutinin (HA) mutation (Q226L) that has previously been associated with a switch in receptor specificity from avian-type (NeuAcα2-3Gal) to human-type (NeuAcα2-6Gal), as documented for the avian progenitors of the 1957 (H2N2) and 1968 (H3N2) human influenza pandemic viruses. While this raised concern that the H7N9 virus was adapting to humans, the mutation was not sufficient to switch the receptor specificity of H7N9, and has not resulted in sustained transmission in humans. To determine if the H7 HA was capable of acquiring human-type receptor specificity, we conducted mutation analyses. Remarkably, three amino acid mutations conferred a switch in specificity for human-type receptors that resembled the specificity of the 2009 human H1 pandemic virus, and promoted binding to human trachea epithelial cells.</p></abstract><abstract abstract-type="summary"><title>Author summary</title><p>Influenza A virus of the H7N9 subtype continues to cross the species barrier from poultry to humans. This zoonotic ability is remarkable as the virus retains specificity to avian-type receptors. To effectively transmit between humans, the virus needs to acquire human-type receptor specificity. In this study, we show that recombinant H7 proteins need three amino acid mutations to change specificity to human-type receptors. Although we are not allowed to assess if these mutations would lead to efficient transmission in the ferret model, this knowledge will aid in surveillance. If these amino acid mutations are observed to arise during natural selection in humans, timely actions could be taken.</p></abstract><funding-group><award-group id="award001"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000002</institution-id><institution>National Institutes of Health</institution></institution-wrap></funding-source><award-id>AI114730</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-4589-5322</contrib-id><name><surname>Paulson</surname><given-names>James C.</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000002</institution-id><institution>National Institutes of Health</institution></institution-wrap></funding-source><award-id>AI117675</award-id><principal-award-recipient><name><surname>Wilson</surname><given-names>Ian A.</given-names></name></principal-award-recipient></award-group><award-group id="award003"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000002</institution-id><institution>National Institutes of Health</institution></institution-wrap></funding-source><award-id>GM103390</award-id><principal-award-recipient><name><surname>Woods</surname><given-names>Robert J.</given-names></name></principal-award-recipient></award-group><award-group id="award004"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000002</institution-id><institution>National Institutes of Health</institution></institution-wrap></funding-source><award-id>GM100058</award-id><principal-award-recipient><name><surname>Woods</surname><given-names>Robert J.</given-names></name></principal-award-recipient></award-group><award-group id="award005"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100000002</institution-id><institution>National Institutes of Health</institution></institution-wrap></funding-source><award-id>GM62116</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-4589-5322</contrib-id><name><surname>Paulson</surname><given-names>James C.</given-names></name></principal-award-recipient></award-group><award-group id="award006"><funding-source><institution>Rubicon and VENI</institution></funding-source><award-id>Netherlands Organization for Scientific Research (NWO)</award-id><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-1274-2987</contrib-id><name><surname>Verheije</surname><given-names>Monique H.</given-names></name></principal-award-recipient></award-group><award-group id="award007"><funding-source><institution>Kwang Hua Education Foundation</institution></funding-source><principal-award-recipient><contrib-id authenticated="true" contrib-id-type="orcid">http://orcid.org/0000-0003-4589-5322</contrib-id><name><surname>Paulson</surname><given-names>James C.</given-names></name></principal-award-recipient></award-group><award-group id="award008"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/100004410</institution-id><institution>European Molecular Biology Organization</institution></institution-wrap></funding-source><award-id>ALTF 963-2014</award-id><principal-award-recipient><name><surname>Thompson</surname><given-names>Andrew J.</given-names></name></principal-award-recipient></award-group><funding-statement>This work was funded in part by National Institutes of Health Grants R56 AI11765 (to IAW), GM100058, GM103390 and U01-CA207824 (to RJW) and AI099274 and AI114730 (to JCP). This work was supported in part by the Scripps Microarray Core Facility, and a contract from the Centers for Disease Control, and the Kwang Hua Educational Foundation (JCP). RPdV is a recipient of Rubicon and VENI grants from the Netherlands Organization for Scientific Research (NWO). CAMdH is supported by a high potential grant from Utrecht University. MHV is a recipient of a MEERVOUD grant from the NWO. AJT is a recipient of a EMBO Long-term Fellowship (EMBO ALTF 963-2014). Several glycans used for HA binding assays were partially provided by the Consortium for Functional Glycomics (<ext-link ext-link-type="uri" xlink:href="http://www.functionalglycomics.org/">http://www.functionalglycomics.org/</ext-link>) funded by NIGMS grant GM62116 (JCP). The Advanced Photon Source beamline 23ID-B (GM/CA CAT) is funded in whole or in part with federal funds from the National Cancer Institute (Y1-CO-1020) and NIGMS (Y1-GM-1104). Use of the Advanced Photon Source was supported by the U.S. Department of Energy (DOE), Basic Energy Sciences, Office of Science, under contract no. DE-AC02-06CH11357. The SSRL Structural Molecular Biology Program is supported by the DOE Office of Biological and Environmental Research and by the NIH, NIGMS (including P41GM103393) and the National Center for Research Resources (NCRR, P41RR001209). 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><fig-count count="6"></fig-count><table-count count="0"></table-count><page-count count="16"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>All relevant data are within the paper and its Supporting Information files and the following links: <<ext-link ext-link-type="uri" xlink:href="http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJK">http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJK</ext-link>> <<ext-link ext-link-type="uri" xlink:href="http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJL">http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJL</ext-link>> <<ext-link ext-link-type="uri" xlink:href="http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJM">http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJM</ext-link>>.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>All relevant data are within the paper and its Supporting Information files and the following links: <<ext-link ext-link-type="uri" xlink:href="http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJK">http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJK</ext-link>> <<ext-link ext-link-type="uri" xlink:href="http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJL">http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJL</ext-link>> <<ext-link ext-link-type="uri" xlink:href="http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJM">http://www.rcsb.org/pdb/explore/explore.do?structureId=5VJM</ext-link>>.</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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