Genomewide Analysis of Reassortment and Evolution of Human Influenza A(H3N2) Viruses Circulating between 1968 and 2011
Identifieur interne : 000679 ( Pmc/Corpus ); précédent : 000678; suivant : 000680Genomewide Analysis of Reassortment and Evolution of Human Influenza A(H3N2) Viruses Circulating between 1968 and 2011
Auteurs : Kim B. Westgeest ; Colin A. Russell ; Xudong Lin ; Monique I. J. Spronken ; Theo M. Bestebroer ; Justin Bahl ; Ruud Van Beek ; Eugene Skepner ; Rebecca A. Halpin ; Jan C. De Jong ; Guus F. Rimmelzwaan ; Albert D. M. E. Osterhaus ; Derek J. Smith ; David E. Wentworth ; Ron A. M. Fouchier ; Miranda De GraafSource :
- Journal of Virology [ 0022-538X ] ; 2014.
Abstract
Influenza A(H3N2) viruses became widespread in humans during the 1968 H3N2 virus pandemic and have been a major cause of influenza epidemics ever since. These viruses evolve continuously by reassortment and genomic evolution. Antigenic drift is the cause for the need to update influenza vaccines frequently. Using two data sets that span the entire period of circulation of human influenza A(H3N2) viruses, it was shown that influenza A(H3N2) virus evolution can be mapped to 13 antigenic clusters. Here we analyzed the full genomes of 286 influenza A(H3N2) viruses from these two data sets to investigate the genomic evolution and reassortment patterns. Numerous reassortment events were found, scattered over the entire period of virus circulation, but most prominently in viruses circulating between 1991 and 1998. Some of these reassortment events persisted over time, and one of these coincided with an antigenic cluster transition. Furthermore, selection pressures and nucleotide and amino acid substitution rates of all proteins were studied, including those of the recently discovered PB1-N40, PA-X, PA-N155, and PA-N182 proteins. Rates of nucleotide and amino acid substitutions were most pronounced for the hemagglutinin, neuraminidase, and PB1-F2 proteins. Selection pressures were highest in hemagglutinin, neuraminidase, matrix 1, and nonstructural protein 1. This study of genotype in relation to antigenic phenotype throughout the period of circulation of human influenza A(H3N2) viruses leads to a better understanding of the evolution of these viruses.
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DOI: 10.1128/JVI.02163-13
PubMed: 24371052
PubMed Central: 3958060
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Russell</name><affiliation><nlm:aff id="aff2">Department of Zoology, University of Cambridge, Cambridge, United Kingdom</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Fogarty International Center, National Institutes of Health, Bethesda, Maryland, USA</nlm:aff></affiliation></author><author><name sortKey="Lin, Xudong" sort="Lin, Xudong" uniqKey="Lin X" first="Xudong" last="Lin">Xudong Lin</name><affiliation><nlm:aff id="aff4">School of Public Health, State University of New York, Albany, New York, USA</nlm:aff></affiliation><affiliation><nlm:aff id="aff5">J. Craig Venter Institute, Rockville, Maryland, USA</nlm:aff></affiliation></author><author><name sortKey="Spronken, Monique I J" sort="Spronken, Monique I J" uniqKey="Spronken M" first="Monique I. J." last="Spronken">Monique I. J. Spronken</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Bestebroer, Theo M" sort="Bestebroer, Theo M" uniqKey="Bestebroer T" first="Theo M." last="Bestebroer">Theo M. 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Halpin</name><affiliation><nlm:aff id="aff5">J. Craig Venter Institute, Rockville, Maryland, USA</nlm:aff></affiliation></author><author><name sortKey="De Jong, Jan C" sort="De Jong, Jan C" uniqKey="De Jong J" first="Jan C." last="De Jong">Jan C. De Jong</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Rimmelzwaan, Guus F" sort="Rimmelzwaan, Guus F" uniqKey="Rimmelzwaan G" first="Guus F." last="Rimmelzwaan">Guus F. Rimmelzwaan</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Osterhaus, Albert D M E" sort="Osterhaus, Albert D M E" uniqKey="Osterhaus A" first="Albert D. M. E." last="Osterhaus">Albert D. M. E. Osterhaus</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Smith, Derek J" sort="Smith, Derek J" uniqKey="Smith D" first="Derek J." last="Smith">Derek J. Smith</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">Department of Zoology, University of Cambridge, Cambridge, United Kingdom</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Fogarty International Center, National Institutes of Health, Bethesda, Maryland, USA</nlm:aff></affiliation></author><author><name sortKey="Wentworth, David E" sort="Wentworth, David E" uniqKey="Wentworth D" first="David E." last="Wentworth">David E. Wentworth</name><affiliation><nlm:aff id="aff4">School of Public Health, State University of New York, Albany, New York, USA</nlm:aff></affiliation><affiliation><nlm:aff id="aff5">J. Craig Venter Institute, Rockville, Maryland, USA</nlm:aff></affiliation></author><author><name sortKey="Fouchier, Ron A M" sort="Fouchier, Ron A M" uniqKey="Fouchier R" first="Ron A. M." last="Fouchier">Ron A. M. Fouchier</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="De Graaf, Miranda" sort="De Graaf, Miranda" uniqKey="De Graaf M" first="Miranda" last="De Graaf">Miranda De Graaf</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24371052</idno><idno type="pmc">3958060</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3958060</idno><idno type="RBID">PMC:3958060</idno><idno type="doi">10.1128/JVI.02163-13</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000679</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000679</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Genomewide Analysis of Reassortment and Evolution of Human Influenza A(H3N2) Viruses Circulating between 1968 and 2011</title><author><name sortKey="Westgeest, Kim B" sort="Westgeest, Kim B" uniqKey="Westgeest K" first="Kim B." last="Westgeest">Kim B. Westgeest</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Russell, Colin A" sort="Russell, Colin A" uniqKey="Russell C" first="Colin A." last="Russell">Colin A. Russell</name><affiliation><nlm:aff id="aff2">Department of Zoology, University of Cambridge, Cambridge, United Kingdom</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Fogarty International Center, National Institutes of Health, Bethesda, Maryland, USA</nlm:aff></affiliation></author><author><name sortKey="Lin, Xudong" sort="Lin, Xudong" uniqKey="Lin X" first="Xudong" last="Lin">Xudong Lin</name><affiliation><nlm:aff id="aff4">School of Public Health, State University of New York, Albany, New York, USA</nlm:aff></affiliation><affiliation><nlm:aff id="aff5">J. Craig Venter Institute, Rockville, Maryland, USA</nlm:aff></affiliation></author><author><name sortKey="Spronken, Monique I J" sort="Spronken, Monique I J" uniqKey="Spronken M" first="Monique I. J." last="Spronken">Monique I. J. Spronken</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Bestebroer, Theo M" sort="Bestebroer, Theo M" uniqKey="Bestebroer T" first="Theo M." last="Bestebroer">Theo M. Bestebroer</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Bahl, Justin" sort="Bahl, Justin" uniqKey="Bahl J" first="Justin" last="Bahl">Justin Bahl</name><affiliation><nlm:aff id="aff6">Center for Infectious Diseases, The University of Texas School of Public Health, Houston, Texas, USA</nlm:aff></affiliation></author><author><name sortKey="Van Beek, Ruud" sort="Van Beek, Ruud" uniqKey="Van Beek R" first="Ruud" last="Van Beek">Ruud Van Beek</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Skepner, Eugene" sort="Skepner, Eugene" uniqKey="Skepner E" first="Eugene" last="Skepner">Eugene Skepner</name><affiliation><nlm:aff id="aff2">Department of Zoology, University of Cambridge, Cambridge, United Kingdom</nlm:aff></affiliation></author><author><name sortKey="Halpin, Rebecca A" sort="Halpin, Rebecca A" uniqKey="Halpin R" first="Rebecca A." last="Halpin">Rebecca A. Halpin</name><affiliation><nlm:aff id="aff5">J. Craig Venter Institute, Rockville, Maryland, USA</nlm:aff></affiliation></author><author><name sortKey="De Jong, Jan C" sort="De Jong, Jan C" uniqKey="De Jong J" first="Jan C." last="De Jong">Jan C. De Jong</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Rimmelzwaan, Guus F" sort="Rimmelzwaan, Guus F" uniqKey="Rimmelzwaan G" first="Guus F." last="Rimmelzwaan">Guus F. Rimmelzwaan</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Osterhaus, Albert D M E" sort="Osterhaus, Albert D M E" uniqKey="Osterhaus A" first="Albert D. M. E." last="Osterhaus">Albert D. M. E. Osterhaus</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="Smith, Derek J" sort="Smith, Derek J" uniqKey="Smith D" first="Derek J." last="Smith">Derek J. Smith</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">Department of Zoology, University of Cambridge, Cambridge, United Kingdom</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Fogarty International Center, National Institutes of Health, Bethesda, Maryland, USA</nlm:aff></affiliation></author><author><name sortKey="Wentworth, David E" sort="Wentworth, David E" uniqKey="Wentworth D" first="David E." last="Wentworth">David E. Wentworth</name><affiliation><nlm:aff id="aff4">School of Public Health, State University of New York, Albany, New York, USA</nlm:aff></affiliation><affiliation><nlm:aff id="aff5">J. Craig Venter Institute, Rockville, Maryland, USA</nlm:aff></affiliation></author><author><name sortKey="Fouchier, Ron A M" sort="Fouchier, Ron A M" uniqKey="Fouchier R" first="Ron A. M." last="Fouchier">Ron A. M. Fouchier</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author><author><name sortKey="De Graaf, Miranda" sort="De Graaf, Miranda" uniqKey="De Graaf M" first="Miranda" last="De Graaf">Miranda De Graaf</name><affiliation><nlm:aff id="aff1">Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</nlm:aff></affiliation></author></analytic><series><title level="j">Journal of Virology</title><idno type="ISSN">0022-538X</idno><idno type="eISSN">1098-5514</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>ABSTRACT</title><p>Influenza A(H3N2) viruses became widespread in humans during the 1968 H3N2 virus pandemic and have been a major cause of influenza epidemics ever since. These viruses evolve continuously by reassortment and genomic evolution. Antigenic drift is the cause for the need to update influenza vaccines frequently. Using two data sets that span the entire period of circulation of human influenza A(H3N2) viruses, it was shown that influenza A(H3N2) virus evolution can be mapped to 13 antigenic clusters. Here we analyzed the full genomes of 286 influenza A(H3N2) viruses from these two data sets to investigate the genomic evolution and reassortment patterns. Numerous reassortment events were found, scattered over the entire period of virus circulation, but most prominently in viruses circulating between 1991 and 1998. Some of these reassortment events persisted over time, and one of these coincided with an antigenic cluster transition. Furthermore, selection pressures and nucleotide and amino acid substitution rates of all proteins were studied, including those of the recently discovered PB1-N40, PA-X, PA-N155, and PA-N182 proteins. Rates of nucleotide and amino acid substitutions were most pronounced for the hemagglutinin, neuraminidase, and PB1-F2 proteins. Selection pressures were highest in hemagglutinin, neuraminidase, matrix 1, and nonstructural protein 1. This study of genotype in relation to antigenic phenotype throughout the period of circulation of human influenza A(H3N2) viruses leads to a better understanding of the evolution of these viruses.</p><p><bold>IMPORTANCE</bold> Each winter, influenza virus infects approximately 5 to 15% of the world's population, resulting in significant morbidity and mortality. Influenza A(H3N2) viruses evolve continuously by reassortment and genomic evolution. This leads to changes in antigenic recognition (antigenic drift) which make it necessary to update vaccines against influenza A(H3N2) viruses frequently. In this study, the relationship of genetic evolution to antigenic change spanning the entire period of A(H3N2) virus circulation was studied for the first time. The results presented in this study contribute to a better understanding of genetic evolution in correlation with antigenic evolution of influenza A(H3N2) viruses.</p></div></front></TEI><pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Virol</journal-id><journal-id journal-id-type="iso-abbrev">J. Virol</journal-id><journal-id journal-id-type="hwp">jvi</journal-id><journal-id journal-id-type="pmc">jvi</journal-id><journal-id journal-id-type="publisher-id">JVI</journal-id><journal-title-group><journal-title>Journal of Virology</journal-title></journal-title-group><issn pub-type="ppub">0022-538X</issn><issn pub-type="epub">1098-5514</issn><publisher><publisher-name>American Society for Microbiology</publisher-name><publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24371052</article-id><article-id pub-id-type="pmc">3958060</article-id><article-id pub-id-type="publisher-id">02163-13</article-id><article-id pub-id-type="doi">10.1128/JVI.02163-13</article-id><article-categories><subj-group subj-group-type="heading"><subject>Genetic Diversity and Evolution</subject></subj-group></article-categories><title-group><article-title>Genomewide Analysis of Reassortment and Evolution of Human Influenza A(H3N2) Viruses Circulating between 1968 and 2011</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Westgeest</surname><given-names>Kim B.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Russell</surname><given-names>Colin A.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Lin</surname><given-names>Xudong</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref><xref ref-type="aff" rid="aff5"><sup>e</sup></xref></contrib><contrib contrib-type="author"><name><surname>Spronken</surname><given-names>Monique I. J.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bestebroer</surname><given-names>Theo M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bahl</surname><given-names>Justin</given-names></name><xref ref-type="aff" rid="aff6"><sup>f</sup></xref></contrib><contrib contrib-type="author"><name><surname>van Beek</surname><given-names>Ruud</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Skepner</surname><given-names>Eugene</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Halpin</surname><given-names>Rebecca A.</given-names></name><xref ref-type="aff" rid="aff5"><sup>e</sup></xref></contrib><contrib contrib-type="author"><name><surname>de Jong</surname><given-names>Jan C.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Rimmelzwaan</surname><given-names>Guus F.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Osterhaus</surname><given-names>Albert D. M. E.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Smith</surname><given-names>Derek J.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wentworth</surname><given-names>David E.</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref><xref ref-type="aff" rid="aff5"><sup>e</sup></xref></contrib><contrib contrib-type="author"><name><surname>Fouchier</surname><given-names>Ron A. M.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>de Graaf</surname><given-names>Miranda</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><aff id="aff1"><label>a</label>Department of Viroscience, Erasmus Medical Center, Rotterdam, Netherlands</aff><aff id="aff2"><label>b</label>Department of Zoology, University of Cambridge, Cambridge, United Kingdom</aff><aff id="aff3"><label>c</label>Fogarty International Center, National Institutes of Health, Bethesda, Maryland, USA</aff><aff id="aff4"><label>d</label>School of Public Health, State University of New York, Albany, New York, USA</aff><aff id="aff5"><label>e</label>J. Craig Venter Institute, Rockville, Maryland, USA</aff><aff id="aff6"><label>f</label>Center for Infectious Diseases, The University of Texas School of Public Health, Houston, Texas, USA</aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>García-Sastre</surname><given-names>A.</given-names></name><role>Editor</role></contrib></contrib-group><author-notes><corresp id="cor1">Address correspondence to Miranda de Graaf, <email>m.degraaf@erasmusmc.nl</email>.</corresp></author-notes><pub-date pub-type="ppub"><month>3</month><year>2014</year></pub-date><volume>88</volume><issue>5</issue><fpage>2844</fpage><lpage>2857</lpage><history><date date-type="received"><day>5</day><month>8</month><year>2013</year></date><date date-type="accepted"><day>5</day><month>12</month><year>2013</year></date></history><permissions><copyright-statement>Copyright © 2014, American Society for Microbiology. All Rights Reserved.</copyright-statement><copyright-year>2014</copyright-year><copyright-holder>American Society for Microbiology</copyright-holder></permissions><self-uri xlink:title="pdf" xlink:type="simple" xlink:href="zjv00514002844.pdf"></self-uri><abstract><title>ABSTRACT</title><p>Influenza A(H3N2) viruses became widespread in humans during the 1968 H3N2 virus pandemic and have been a major cause of influenza epidemics ever since. These viruses evolve continuously by reassortment and genomic evolution. Antigenic drift is the cause for the need to update influenza vaccines frequently. Using two data sets that span the entire period of circulation of human influenza A(H3N2) viruses, it was shown that influenza A(H3N2) virus evolution can be mapped to 13 antigenic clusters. Here we analyzed the full genomes of 286 influenza A(H3N2) viruses from these two data sets to investigate the genomic evolution and reassortment patterns. Numerous reassortment events were found, scattered over the entire period of virus circulation, but most prominently in viruses circulating between 1991 and 1998. Some of these reassortment events persisted over time, and one of these coincided with an antigenic cluster transition. Furthermore, selection pressures and nucleotide and amino acid substitution rates of all proteins were studied, including those of the recently discovered PB1-N40, PA-X, PA-N155, and PA-N182 proteins. Rates of nucleotide and amino acid substitutions were most pronounced for the hemagglutinin, neuraminidase, and PB1-F2 proteins. Selection pressures were highest in hemagglutinin, neuraminidase, matrix 1, and nonstructural protein 1. This study of genotype in relation to antigenic phenotype throughout the period of circulation of human influenza A(H3N2) viruses leads to a better understanding of the evolution of these viruses.</p><p><bold>IMPORTANCE</bold> Each winter, influenza virus infects approximately 5 to 15% of the world's population, resulting in significant morbidity and mortality. Influenza A(H3N2) viruses evolve continuously by reassortment and genomic evolution. This leads to changes in antigenic recognition (antigenic drift) which make it necessary to update vaccines against influenza A(H3N2) viruses frequently. In this study, the relationship of genetic evolution to antigenic change spanning the entire period of A(H3N2) virus circulation was studied for the first time. The results presented in this study contribute to a better understanding of genetic evolution in correlation with antigenic evolution of influenza A(H3N2) viruses.</p></abstract></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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