Identification of Amino Acid Substitutions Supporting Antigenic Change of Influenza A(H1N1)pdm09 Viruses
Identifieur interne : 000372 ( Pmc/Checkpoint ); précédent : 000371; suivant : 000373Identification of Amino Acid Substitutions Supporting Antigenic Change of Influenza A(H1N1)pdm09 Viruses
Auteurs : Björn F. Koel [Pays-Bas] ; Ramona Mögling [Pays-Bas, Royaume-Uni] ; Salin Chutinimitkul [Pays-Bas] ; Pieter L. Fraaij [Pays-Bas] ; David F. Burke [Royaume-Uni] ; Stefan Van Der Vliet [Pays-Bas] ; Emmie De Wit [Pays-Bas] ; Theo M. Bestebroer [Pays-Bas] ; Guus F. Rimmelzwaan [Pays-Bas] ; Albert D. M. E. Osterhaus [Pays-Bas] ; Derek J. Smith [Royaume-Uni, Pays-Bas] ; Ron A. M. Fouchier [Pays-Bas] ; Miranda De Graaf [Pays-Bas, Royaume-Uni]Source :
- Journal of Virology [ 0022-538X ] ; 2015.
Abstract
The majority of currently circulating influenza A(H1N1) viruses are antigenically similar to the virus that caused the 2009 influenza pandemic. However, antigenic variants are expected to emerge as population immunity increases. Amino acid substitutions in the hemagglutinin protein can result in escape from neutralizing antibodies, affect viral fitness, and change receptor preference. In this study, we constructed mutants with substitutions in the hemagglutinin of A/Netherlands/602/09 in an attenuated backbone to explore amino acid changes that may contribute to emergence of antigenic variants in the human population. Our analysis revealed that single substitutions affecting the loop that consists of amino acid positions 151 to 159 located adjacent to the receptor binding site caused escape from ferret and human antibodies elicited after primary A(H1N1)pdm09 virus infection. The majority of these substitutions resulted in similar or increased replication efficiency
Url:
DOI: 10.1128/JVI.02962-14
PubMed: 25609810
PubMed Central: 4403388
Affiliations:
- Pays-Bas, Royaume-Uni
- Angleterre, Angleterre de l'Est, Hollande-Méridionale
- Cambridge, Rotterdam
- Université de Cambridge
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PMC:4403388Le document en format XML
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Identification of Amino Acid Substitutions Supporting Antigenic Change of Influenza A(H1N1)pdm09 Viruses</title>
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<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 wicri:level="3"><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Department of Viroscience, Erasmus MC, Rotterdam</wicri:regionArea>
<placeName><settlement type="city">Rotterdam</settlement>
<region nuts="2" type="province">Hollande-Méridionale</region>
</placeName>
</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 wicri:level="3"><nlm:aff id="aff1">Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</nlm:aff>
<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Department of Viroscience, Erasmus MC, Rotterdam</wicri:regionArea>
<placeName><settlement type="city">Rotterdam</settlement>
<region nuts="2" type="province">Hollande-Méridionale</region>
</placeName>
</affiliation>
<affiliation wicri:level="4"><nlm:aff id="aff2">Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge, United Kingdom</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea>Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge</wicri:regionArea>
<orgName type="university">Université de Cambridge</orgName>
<placeName><settlement type="city">Cambridge</settlement>
<region type="country">Angleterre</region>
<region type="région" nuts="1">Angleterre de l'Est</region>
</placeName>
</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="2015">2015</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<p>The majority of currently circulating influenza A(H1N1) viruses are antigenically similar to the virus that caused the 2009 influenza pandemic. However, antigenic variants are expected to emerge as population immunity increases. Amino acid substitutions in the hemagglutinin protein can result in escape from neutralizing antibodies, affect viral fitness, and change receptor preference. In this study, we constructed mutants with substitutions in the hemagglutinin of A/Netherlands/602/09 in an attenuated backbone to explore amino acid changes that may contribute to emergence of antigenic variants in the human population. Our analysis revealed that single substitutions affecting the loop that consists of amino acid positions 151 to 159 located adjacent to the receptor binding site caused escape from ferret and human antibodies elicited after primary A(H1N1)pdm09 virus infection. The majority of these substitutions resulted in similar or increased replication efficiency <italic>in vitro</italic>
compared to that of the virus carrying the wild-type hemagglutinin and did not result in a change of receptor preference. However, none of the substitutions was sufficient for escape from the antibodies in sera from individuals that experienced both seasonal and pandemic A(H1N1) virus infections. These results suggest that antibodies directed against epitopes on seasonal A(H1N1) viruses contribute to neutralization of A(H1N1)pdm09 antigenic variants, thereby limiting the number of possible substitutions that could lead to escape from population immunity.
</p>
<p><bold>IMPORTANCE</bold>
Influenza A viruses can cause significant morbidity and mortality in humans. Amino acid substitutions in the hemagglutinin protein can result in escape from antibody-mediated neutralization. This allows the virus to reinfect individuals that have acquired immunity to previously circulating strains through infection or vaccination. To date, the vast majority of A(H1N1)pdm09 strains remain antigenically similar to the virus that caused the 2009 influenza pandemic. However, antigenic variants are expected to emerge as a result of increasing population immunity. We show that single amino acid substitutions near the receptor binding site were sufficient to escape from antibodies specific for A(H1N1)pdm09 viruses but not from antibodies elicited in response to infections with seasonal A(H1N1) and A(H1N1)pdm09 viruses. This study identified substitutions in A(H1N1)pdm09 viruses that support escape from population immunity but also suggested that the number of potential escape variants is limited by previous exposure to seasonal A(H1N1) 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">25609810</article-id>
<article-id pub-id-type="pmc">4403388</article-id>
<article-id pub-id-type="publisher-id">02962-14</article-id>
<article-id pub-id-type="doi">10.1128/JVI.02962-14</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Genetic Diversity and Evolution</subject>
</subj-group>
</article-categories>
<title-group><article-title>Identification of Amino Acid Substitutions Supporting Antigenic Change of Influenza A(H1N1)pdm09 Viruses</article-title>
<alt-title alt-title-type="running-head">A(H1N1)pdm09 Viruses: Possibilities for Antigenic Change</alt-title>
<alt-title alt-title-type="short-authors">Koel et al.</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Koel</surname>
<given-names>Björn F.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mögling</surname>
<given-names>Ramona</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chutinimitkul</surname>
<given-names>Salin</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Fraaij</surname>
<given-names>Pieter L.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Burke</surname>
<given-names>David F.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>van der Vliet</surname>
<given-names>Stefan</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>de Wit</surname>
<given-names>Emmie</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">*</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>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="aff2"><sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
<xref ref-type="aff" rid="aff1"><sup>a</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>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<aff id="aff1"><label>a</label>
Department of Viroscience, Erasmus MC, Rotterdam, The Netherlands</aff>
<aff id="aff2"><label>b</label>
Center for Pathogen Evolution, Department of Zoology, University of Cambridge, Cambridge, United Kingdom</aff>
<aff id="aff3"><label>c</label>
Department of Pediatrics, Erasmus MC-Sophia, Rotterdam, The Netherlands</aff>
<aff id="aff4"><label>d</label>
WHO Collaborating Centre for Modeling Evolution and Control of Emerging Infectious Diseases, University of Cambridge, Cambridge, United Kingdom</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>
<fn id="fn1" fn-type="present-address"><label>*</label>
<p>Present address: Emmie de Wit, Laboratory of Virology, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Hamilton, Montana, USA.</p>
</fn>
<fn fn-type="other"><p><bold>Citation</bold>
Koel BF, Mögling R, Chutinimitkul S, Fraaij PL, Burke DF, van der Vliet S, de Wit E, Bestebroer TM, Rimmelzwaan GF, Osterhaus ADME, Smith DJ, Fouchier RAM, de Graaf M. 2015. Identification of amino acid substitutions supporting antigenic change of influenza A(H1N1)pdm09 viruses. J Virol 89:3763–3775. doi:<ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.1128/JVI.02962-14">10.1128/JVI.02962-14</ext-link>
.</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>21</day>
<month>1</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection"><day>1</day>
<month>4</month>
<year>2015</year>
</pub-date>
<volume>89</volume>
<issue>7</issue>
<fpage>3763</fpage>
<lpage>3775</lpage>
<history><date date-type="received"><day>9</day>
<month>10</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>9</day>
<month>1</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2015, American Society for Microbiology. All Rights Reserved.</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>American Society for Microbiology</copyright-holder>
</permissions>
<self-uri content-type="pdf" xlink:href="zjv00715003763.pdf"></self-uri>
<abstract><title>ABSTRACT</title>
<p>The majority of currently circulating influenza A(H1N1) viruses are antigenically similar to the virus that caused the 2009 influenza pandemic. However, antigenic variants are expected to emerge as population immunity increases. Amino acid substitutions in the hemagglutinin protein can result in escape from neutralizing antibodies, affect viral fitness, and change receptor preference. In this study, we constructed mutants with substitutions in the hemagglutinin of A/Netherlands/602/09 in an attenuated backbone to explore amino acid changes that may contribute to emergence of antigenic variants in the human population. Our analysis revealed that single substitutions affecting the loop that consists of amino acid positions 151 to 159 located adjacent to the receptor binding site caused escape from ferret and human antibodies elicited after primary A(H1N1)pdm09 virus infection. The majority of these substitutions resulted in similar or increased replication efficiency <italic>in vitro</italic>
compared to that of the virus carrying the wild-type hemagglutinin and did not result in a change of receptor preference. However, none of the substitutions was sufficient for escape from the antibodies in sera from individuals that experienced both seasonal and pandemic A(H1N1) virus infections. These results suggest that antibodies directed against epitopes on seasonal A(H1N1) viruses contribute to neutralization of A(H1N1)pdm09 antigenic variants, thereby limiting the number of possible substitutions that could lead to escape from population immunity.
</p>
<p><bold>IMPORTANCE</bold>
Influenza A viruses can cause significant morbidity and mortality in humans. Amino acid substitutions in the hemagglutinin protein can result in escape from antibody-mediated neutralization. This allows the virus to reinfect individuals that have acquired immunity to previously circulating strains through infection or vaccination. To date, the vast majority of A(H1N1)pdm09 strains remain antigenically similar to the virus that caused the 2009 influenza pandemic. However, antigenic variants are expected to emerge as a result of increasing population immunity. We show that single amino acid substitutions near the receptor binding site were sufficient to escape from antibodies specific for A(H1N1)pdm09 viruses but not from antibodies elicited in response to infections with seasonal A(H1N1) and A(H1N1)pdm09 viruses. This study identified substitutions in A(H1N1)pdm09 viruses that support escape from population immunity but also suggested that the number of potential escape variants is limited by previous exposure to seasonal A(H1N1) viruses.</p>
</abstract>
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</front>
</pmc>
<affiliations><list><country><li>Pays-Bas</li>
<li>Royaume-Uni</li>
</country>
<region><li>Angleterre</li>
<li>Angleterre de l'Est</li>
<li>Hollande-Méridionale</li>
</region>
<settlement><li>Cambridge</li>
<li>Rotterdam</li>
</settlement>
<orgName><li>Université de Cambridge</li>
</orgName>
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<tree><country name="Pays-Bas"><region name="Hollande-Méridionale"><name sortKey="Koel, Bjorn F" sort="Koel, Bjorn F" uniqKey="Koel B" first="Björn F." last="Koel">Björn F. Koel</name>
</region>
<name sortKey="Bestebroer, Theo M" sort="Bestebroer, Theo M" uniqKey="Bestebroer T" first="Theo M." last="Bestebroer">Theo M. Bestebroer</name>
<name sortKey="Chutinimitkul, Salin" sort="Chutinimitkul, Salin" uniqKey="Chutinimitkul S" first="Salin" last="Chutinimitkul">Salin Chutinimitkul</name>
<name sortKey="De Graaf, Miranda" sort="De Graaf, Miranda" uniqKey="De Graaf M" first="Miranda" last="De Graaf">Miranda De Graaf</name>
<name sortKey="De Wit, Emmie" sort="De Wit, Emmie" uniqKey="De Wit E" first="Emmie" last="De Wit">Emmie De Wit</name>
<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>
<name sortKey="Fraaij, Pieter L" sort="Fraaij, Pieter L" uniqKey="Fraaij P" first="Pieter L." last="Fraaij">Pieter L. Fraaij</name>
<name sortKey="Fraaij, Pieter L" sort="Fraaij, Pieter L" uniqKey="Fraaij P" first="Pieter L." last="Fraaij">Pieter L. Fraaij</name>
<name sortKey="Mogling, Ramona" sort="Mogling, Ramona" uniqKey="Mogling R" first="Ramona" last="Mögling">Ramona Mögling</name>
<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>
<name sortKey="Rimmelzwaan, Guus F" sort="Rimmelzwaan, Guus F" uniqKey="Rimmelzwaan G" first="Guus F." last="Rimmelzwaan">Guus F. Rimmelzwaan</name>
<name sortKey="Smith, Derek J" sort="Smith, Derek J" uniqKey="Smith D" first="Derek J." last="Smith">Derek J. Smith</name>
<name sortKey="Van Der Vliet, Stefan" sort="Van Der Vliet, Stefan" uniqKey="Van Der Vliet S" first="Stefan" last="Van Der Vliet">Stefan Van Der Vliet</name>
</country>
<country name="Royaume-Uni"><region name="Angleterre"><name sortKey="Mogling, Ramona" sort="Mogling, Ramona" uniqKey="Mogling R" first="Ramona" last="Mögling">Ramona Mögling</name>
</region>
<name sortKey="Burke, David F" sort="Burke, David F" uniqKey="Burke D" first="David F." last="Burke">David F. Burke</name>
<name sortKey="Burke, David F" sort="Burke, David F" uniqKey="Burke D" first="David F." last="Burke">David F. Burke</name>
<name sortKey="De Graaf, Miranda" sort="De Graaf, Miranda" uniqKey="De Graaf M" first="Miranda" last="De Graaf">Miranda De Graaf</name>
<name sortKey="Smith, Derek J" sort="Smith, Derek J" uniqKey="Smith D" first="Derek J." last="Smith">Derek J. Smith</name>
<name sortKey="Smith, Derek J" sort="Smith, Derek J" uniqKey="Smith D" first="Derek J." last="Smith">Derek J. Smith</name>
</country>
</tree>
</affiliations>
</record>
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