Human Influenza A Virus Hemagglutinin Glycan Evolution Follows a Temporal Pattern to a Glycan Limit
Identifieur interne : 000F73 ( Ncbi/Merge ); précédent : 000F72; suivant : 000F74Human Influenza A Virus Hemagglutinin Glycan Evolution Follows a Temporal Pattern to a Glycan Limit
Auteurs : Meghan O. Altman [États-Unis] ; Matthew Angel [États-Unis] ; Ivan Košík [États-Unis] ; Nídia S. Trovão [États-Unis] ; Seth J. Zost [États-Unis] ; James S. Gibbs [États-Unis] ; Lorenzo Casalino [États-Unis] ; Rommie E. Amaro [États-Unis] ; Scott E. Hensley [États-Unis] ; Martha I. Nelson [États-Unis] ; Jonathan W. Yewdell [États-Unis]Source :
- mBio [ 2150-7511 ] ; 2019.
Abstract
Frequent mutation of its major antibody target, the glycoprotein hemagglutinin, ensures that the influenza virus is perennially both a rapidly emerging virus and a major threat to public health. One type of mutation escapes immunity by adding a glycan onto an area of hemagglutinin that many antibodies recognize. This study revealed that these glycan changes follow a simple temporal pattern. Every 5 to 7 years, hemagglutinin adds a new glycan, up to a limit. After this limit is reached, no net additions of glycans occur. Instead, glycans are swapped or lost at longer intervals. Eventually, a pandemic replaces the terminally glycosylated hemagglutinin with a minimally glycosylated one from the animal reservoir, restarting the cycle. This pattern suggests the following: (i) some hemagglutinins are evolved for this decades-long process, which is both defined by and limited by successive glycan addition; and (ii) hemagglutinin's antibody dominance and its capacity for mutations are highly adapted features that allow influenza to outpace our antibody-based immunity.
Url:
DOI: 10.1128/mBio.00204-19
PubMed: 30940704
PubMed Central: 6445938
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Trovão</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Division of International Epidemiology and Population Studies, Fogarty International Center, NIH, Bethesda, Maryland, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of International Epidemiology and Population Studies, Fogarty International Center, NIH, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation><affiliation wicri:level="2"><nlm:aff id="aff3"><addr-line>Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York City, New York, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York City, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Zost, Seth J" sort="Zost, Seth J" uniqKey="Zost S" first="Seth J." last="Zost">Seth J. Zost</name><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Gibbs, James S" sort="Gibbs, James S" uniqKey="Gibbs J" first="James S." last="Gibbs">James S. Gibbs</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Cellular Biology Section, Laboratory of Viral Diseases NIAID, NIH, Bethesda, Maryland, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Cellular Biology Section, Laboratory of Viral Diseases NIAID, NIH, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Casalino, Lorenzo" sort="Casalino, Lorenzo" uniqKey="Casalino L" first="Lorenzo" last="Casalino">Lorenzo Casalino</name><affiliation wicri:level="2"><nlm:aff id="aff5"><addr-line>Department of Chemistry and Biochemistry and the National Biomedical Computation Resource, University of California, San Diego, La Jolla, California, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry and Biochemistry and the National Biomedical Computation Resource, University of California, San Diego, La Jolla, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Amaro, Rommie E" sort="Amaro, Rommie E" uniqKey="Amaro R" first="Rommie E." last="Amaro">Rommie E. 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Hensley</name><affiliation wicri:level="2"><nlm:aff id="aff4"><addr-line>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania</wicri:regionArea><placeName><region type="state">Pennsylvanie</region></placeName></affiliation></author><author><name sortKey="Nelson, Martha I" sort="Nelson, Martha I" uniqKey="Nelson M" first="Martha I." last="Nelson">Martha I. Nelson</name><affiliation wicri:level="2"><nlm:aff id="aff2"><addr-line>Division of International Epidemiology and Population Studies, Fogarty International Center, NIH, Bethesda, Maryland, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of International Epidemiology and Population Studies, Fogarty International Center, NIH, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Yewdell, Jonathan W" sort="Yewdell, Jonathan W" uniqKey="Yewdell J" first="Jonathan W." last="Yewdell">Jonathan W. Yewdell</name><affiliation wicri:level="2"><nlm:aff id="aff1"><addr-line>Cellular Biology Section, Laboratory of Viral Diseases NIAID, NIH, Bethesda, Maryland, USA</addr-line></nlm:aff><country xml:lang="fr">États-Unis</country><wicri:regionArea>Cellular Biology Section, Laboratory of Viral Diseases NIAID, NIH, Bethesda, Maryland</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Frequent mutation of its major antibody target, the glycoprotein hemagglutinin, ensures that the influenza virus is perennially both a rapidly emerging virus and a major threat to public health. One type of mutation escapes immunity by adding a glycan onto an area of hemagglutinin that many antibodies recognize. This study revealed that these glycan changes follow a simple temporal pattern. Every 5 to 7 years, hemagglutinin adds a new glycan, up to a limit. After this limit is reached, no net additions of glycans occur. Instead, glycans are swapped or lost at longer intervals. Eventually, a pandemic replaces the terminally glycosylated hemagglutinin with a minimally glycosylated one from the animal reservoir, restarting the cycle. This pattern suggests the following: (i) some hemagglutinins are evolved for this decades-long process, which is both defined by and limited by successive glycan addition; and (ii) hemagglutinin's antibody dominance and its capacity for mutations are highly adapted features that allow influenza to outpace our antibody-based immunity.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Couch, Rb" uniqKey="Couch R">RB Couch</name></author><author><name sortKey="Kasel, Ja" uniqKey="Kasel J">JA Kasel</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Keil, W" uniqKey="Keil W">W Keil</name></author><author><name sortKey="Geyer, R" uniqKey="Geyer R">R Geyer</name></author><author><name sortKey="Dabrowski, J" uniqKey="Dabrowski J">J Dabrowski</name></author><author><name sortKey="Dabrowski, U" uniqKey="Dabrowski U">U Dabrowski</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">mBio</journal-id><journal-id journal-id-type="iso-abbrev">MBio</journal-id><journal-id journal-id-type="hwp">mbio</journal-id><journal-id journal-id-type="pmc">mbio</journal-id><journal-id journal-id-type="publisher-id">mBio</journal-id><journal-title-group><journal-title>mBio</journal-title></journal-title-group><issn pub-type="epub">2150-7511</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">30940704</article-id><article-id pub-id-type="pmc">6445938</article-id><article-id pub-id-type="publisher-id">mBio00204-19</article-id><article-id pub-id-type="doi">10.1128/mBio.00204-19</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="overline"><subject>Host-Microbe Biology</subject></subj-group></article-categories><title-group><article-title>Human Influenza A Virus Hemagglutinin Glycan Evolution Follows a Temporal Pattern to a Glycan Limit</article-title><alt-title alt-title-type="running-head">HA Glycan Evolution</alt-title><alt-title alt-title-type="short-authors">Altman et al.</alt-title></title-group><contrib-group><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-8910-9074</contrib-id><name><surname>Altman</surname><given-names>Meghan O.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Angel</surname><given-names>Matthew</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-5756-5182</contrib-id><name><surname>Košík</surname><given-names>Ivan</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Trovão</surname><given-names>Nídia S.</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"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-6712-5076</contrib-id><name><surname>Zost</surname><given-names>Seth J.</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gibbs</surname><given-names>James S.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-3581-1148</contrib-id><name><surname>Casalino</surname><given-names>Lorenzo</given-names></name><xref ref-type="aff" rid="aff5"><sup>e</sup></xref></contrib><contrib contrib-type="author"><name><surname>Amaro</surname><given-names>Rommie E.</given-names></name><xref ref-type="aff" rid="aff5"><sup>e</sup></xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-2928-7506</contrib-id><name><surname>Hensley</surname><given-names>Scott E.</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-4814-0179</contrib-id><name><surname>Nelson</surname><given-names>Martha I.</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-3826-1906</contrib-id><name><surname>Yewdell</surname><given-names>Jonathan W.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><aff id="aff1"><label>a</label><addr-line>Cellular Biology Section, Laboratory of Viral Diseases NIAID, NIH, Bethesda, Maryland, USA</addr-line></aff><aff id="aff2"><label>b</label><addr-line>Division of International Epidemiology and Population Studies, Fogarty International Center, NIH, Bethesda, Maryland, USA</addr-line></aff><aff id="aff3"><label>c</label><addr-line>Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York City, New York, USA</addr-line></aff><aff id="aff4"><label>d</label><addr-line>Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA</addr-line></aff><aff id="aff5"><label>e</label><addr-line>Department of Chemistry and Biochemistry and the National Biomedical Computation Resource, University of California, San Diego, La Jolla, California, USA</addr-line></aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Griffin</surname><given-names>Diane E.</given-names></name><role>Editor</role><aff>Johns Hopkins Bloomberg School of Public Health</aff></contrib></contrib-group><contrib-group><contrib contrib-type="reviewer"><name><surname>Wilson</surname><given-names>Ian</given-names></name><role>Solicited external reviewer</role><aff>The Scripps Research Institute</aff></contrib><contrib contrib-type="reviewer"><name><surname>de Haan</surname><given-names>Cornelis</given-names></name><role>Solicited external reviewer</role><aff>Utrecht University</aff></contrib></contrib-group><author-notes><corresp id="cor1">Address correspondence to Meghan O. Altman, <email>meghan@altmans.org</email>, or Jonathan W. Yewdell, <email>jyewdell@niaid.nih.gov</email>.</corresp></author-notes><pub-date pub-type="epub"><day>2</day><month>4</month><year>2019</year></pub-date><pub-date pub-type="collection"><season>Mar-Apr</season><year>2019</year></pub-date><volume>10</volume><issue>2</issue><elocation-id>e00204-19</elocation-id><history><date date-type="received"><day>25</day><month>1</month><year>2019</year></date><date date-type="accepted"><day>15</day><month>2</month><year>2019</year></date></history><permissions><license license-type="open-access" xlink:href="https://doi.org/10.1128/AuthorWarrantyLicense.v1"><license-p>This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="mBio.00204-19.pdf"></self-uri><abstract abstract-type="precis"><p>Frequent mutation of its major antibody target, the glycoprotein hemagglutinin, ensures that the influenza virus is perennially both a rapidly emerging virus and a major threat to public health. One type of mutation escapes immunity by adding a glycan onto an area of hemagglutinin that many antibodies recognize. This study revealed that these glycan changes follow a simple temporal pattern. Every 5 to 7 years, hemagglutinin adds a new glycan, up to a limit. After this limit is reached, no net additions of glycans occur. Instead, glycans are swapped or lost at longer intervals. Eventually, a pandemic replaces the terminally glycosylated hemagglutinin with a minimally glycosylated one from the animal reservoir, restarting the cycle. This pattern suggests the following: (i) some hemagglutinins are evolved for this decades-long process, which is both defined by and limited by successive glycan addition; and (ii) hemagglutinin's antibody dominance and its capacity for mutations are highly adapted features that allow influenza to outpace our antibody-based immunity.</p></abstract><abstract><title>ABSTRACT</title><p>Human antibody-based immunity to influenza A virus is limited by antigenic drift resulting from amino acid substitutions in the hemagglutinin (HA) head domain. Glycan addition can cause large antigenic changes but is limited by fitness costs to viral replication. Here, we report that glycans are added to H1 and H3 HAs at discrete 5-to-7-year intervals, until they reach a functional glycan limit, after which glycans are swapped at approximately 2-fold-longer intervals. Consistent with this pattern, 2009 pandemic H1N1 added a glycan at residue N162 over the 2015–2016 season, an addition that required two epistatic HA head mutations for complete glycosylation. These strains rapidly replaced H1N1 strains globally, by 2017 dominating H3N2 and influenza B virus strains for the season. The pattern of glycan modulation that we outline should aid efforts for tracing the epidemic potential of evolving human IAV strains.</p></abstract><kwd-group><title>KEYWORDS</title><kwd>influenza</kwd><kwd>viral evolution</kwd><kwd>hemagglutinin</kwd><kwd>immune evasion</kwd><kwd>glycosylation</kwd></kwd-group><counts><count count="10" count-type="supplementary-material"></count><fig-count count="7"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="57"></ref-count><page-count count="15"></page-count><word-count count="10712"></word-count></counts><custom-meta-group><custom-meta><meta-name>cover-date</meta-name><meta-value>March/April 2019</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list><country><li>États-Unis</li></country><region><li>Californie</li><li>Maryland</li><li>Pennsylvanie</li><li>État de New York</li></region></list><tree><country name="États-Unis"><region name="Maryland"><name sortKey="Altman, Meghan O" sort="Altman, Meghan O" uniqKey="Altman M" first="Meghan O." last="Altman">Meghan O. Altman</name></region><name sortKey="Amaro, Rommie E" sort="Amaro, Rommie E" uniqKey="Amaro R" first="Rommie E." last="Amaro">Rommie E. Amaro</name><name sortKey="Angel, Matthew" sort="Angel, Matthew" uniqKey="Angel M" first="Matthew" last="Angel">Matthew Angel</name><name sortKey="Casalino, Lorenzo" sort="Casalino, Lorenzo" uniqKey="Casalino L" first="Lorenzo" last="Casalino">Lorenzo Casalino</name><name sortKey="Gibbs, James S" sort="Gibbs, James S" uniqKey="Gibbs J" first="James S." last="Gibbs">James S. Gibbs</name><name sortKey="Hensley, Scott E" sort="Hensley, Scott E" uniqKey="Hensley S" first="Scott E." last="Hensley">Scott E. Hensley</name><name sortKey="Kosik, Ivan" sort="Kosik, Ivan" uniqKey="Kosik I" first="Ivan" last="Košík">Ivan Košík</name><name sortKey="Nelson, Martha I" sort="Nelson, Martha I" uniqKey="Nelson M" first="Martha I." last="Nelson">Martha I. Nelson</name><name sortKey="Trovao, Nidia S" sort="Trovao, Nidia S" uniqKey="Trovao N" first="Nídia S." last="Trovão">Nídia S. Trovão</name><name sortKey="Trovao, Nidia S" sort="Trovao, Nidia S" uniqKey="Trovao N" first="Nídia S." last="Trovão">Nídia S. Trovão</name><name sortKey="Yewdell, Jonathan W" sort="Yewdell, Jonathan W" uniqKey="Yewdell J" first="Jonathan W." last="Yewdell">Jonathan W. Yewdell</name><name sortKey="Zost, Seth J" sort="Zost, Seth J" uniqKey="Zost S" first="Seth J." last="Zost">Seth J. Zost</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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