Fitness costs limit influenza A virus hemagglutinin glycosylation as an immune evasion strategy
Identifieur interne : 000C62 ( Main/Exploration ); précédent : 000C61; suivant : 000C63Fitness costs limit influenza A virus hemagglutinin glycosylation as an immune evasion strategy
Auteurs : Suman R. Das [États-Unis] ; Scott E. Hensley [États-Unis] ; Alexandre David [États-Unis] ; Loren Schmidt [États-Unis] ; James S. Gibbs [États-Unis] ; Pere Puigb [États-Unis] ; William L. Ince [États-Unis] ; Jack R. Bennink [États-Unis] ; Jonathan W. Yewdell [États-Unis]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2011.
Abstract
Here, we address the question of why the influenza A virus hemagglutinin (HA) does not escape immunity by hyperglycosylation. Uniquely among dozens of monoclonal antibodies specific for A/Puerto Rico/8/34, escape from H28-A2 neutralization requires substitutions introducing N-linked glycosylation at residue 131 or 144 in the globular domain. This escape decreases viral binding to cellular receptors, which must be compensated for by additional substitutions in HA or neuraminidase that enable viral replication. Sequence analysis of circulating H1 influenza viruses confirms the in vivo relevance of our findings: natural occurrence of glycosylation at residue 131 is always accompanied by a compensatory mutation known to increase HA receptor avidity. In vaccinated mice challenged with WT vs. H28-A2 escape mutants, the selective advantage conferred by glycan-mediated global reduction in antigenicity is trumped by the costs of diminished receptor avidity. These findings show that, although N-linked glycosylation can broadly diminish HA antigenicity, fitness costs restrict its deployment in immune evasion.
Url:
DOI: 10.1073/pnas.1108754108
PubMed: 22106257
PubMed Central: 3251056
Affiliations:
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Das</name><affiliation wicri:level="2"><nlm:aff id="aff1">Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases,<institution>National Institutes of Health</institution>, Bethesda, MD 20892;</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>, Bethesda</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff wicri:cut="; and" id="aff2">Emory Vaccine Center,<institution>Emory University</institution>, Atlanta, GA 30322</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Géorgie (États-Unis)</region></placeName><wicri:cityArea>, Atlanta</wicri:cityArea></affiliation></author><author><name sortKey="Hensley, Scott E" sort="Hensley, Scott E" uniqKey="Hensley S" first="Scott E." last="Hensley">Scott E. Hensley</name><affiliation wicri:level="2"><nlm:aff id="aff1">Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases,<institution>National Institutes of Health</institution>, Bethesda, MD 20892;</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>, Bethesda</wicri:cityArea></affiliation></author><author><name sortKey="David, Alexandre" sort="David, Alexandre" uniqKey="David A" first="Alexandre" last="David">Alexandre David</name><affiliation wicri:level="2"><nlm:aff id="aff1">Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases,<institution>National Institutes of Health</institution>, Bethesda, MD 20892;</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>, Bethesda</wicri:cityArea></affiliation></author><author><name sortKey="Schmidt, Loren" sort="Schmidt, Loren" uniqKey="Schmidt L" first="Loren" last="Schmidt">Loren Schmidt</name><affiliation wicri:level="2"><nlm:aff id="aff1">Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases,<institution>National Institutes of Health</institution>, Bethesda, MD 20892;</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>, Bethesda</wicri:cityArea></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">Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases,<institution>National Institutes of Health</institution>, Bethesda, MD 20892;</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>, Bethesda</wicri:cityArea></affiliation></author><author><name sortKey="Puigb, Pere" sort="Puigb, Pere" uniqKey="Puigb P" first="Pere" last="Puigb">Pere Puigb</name><affiliation wicri:level="2"><nlm:aff id="aff3">National Center for Biotechnology Information, National Library of Medicine,<institution>National Institutes of Health</institution>, Bethesda, MD 20894</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>, Bethesda</wicri:cityArea></affiliation></author><author><name sortKey="Ince, William L" sort="Ince, William L" uniqKey="Ince W" first="William L." last="Ince">William L. Ince</name><affiliation wicri:level="2"><nlm:aff id="aff1">Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases,<institution>National Institutes of Health</institution>, Bethesda, MD 20892;</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>, Bethesda</wicri:cityArea></affiliation></author><author><name sortKey="Bennink, Jack R" sort="Bennink, Jack R" uniqKey="Bennink J" first="Jack R." last="Bennink">Jack R. Bennink</name><affiliation wicri:level="2"><nlm:aff id="aff1">Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases,<institution>National Institutes of Health</institution>, Bethesda, MD 20892;</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>, Bethesda</wicri:cityArea></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">Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases,<institution>National Institutes of Health</institution>, Bethesda, MD 20892;</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">Maryland</region></placeName><wicri:cityArea>, Bethesda</wicri:cityArea></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><idno type="eISSN">1091-6490</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Here, we address the question of why the influenza A virus hemagglutinin (HA) does not escape immunity by hyperglycosylation. Uniquely among dozens of monoclonal antibodies specific for A/Puerto Rico/8/34, escape from H28-A2 neutralization requires substitutions introducing N-linked glycosylation at residue 131 or 144 in the globular domain. This escape decreases viral binding to cellular receptors, which must be compensated for by additional substitutions in HA or neuraminidase that enable viral replication. Sequence analysis of circulating H1 influenza viruses confirms the in vivo relevance of our findings: natural occurrence of glycosylation at residue 131 is always accompanied by a compensatory mutation known to increase HA receptor avidity. In vaccinated mice challenged with WT vs. H28-A2 escape mutants, the selective advantage conferred by glycan-mediated global reduction in antigenicity is trumped by the costs of diminished receptor avidity. These findings show that, although N-linked glycosylation can broadly diminish HA antigenicity, fitness costs restrict its deployment in immune evasion.</p></div></front></TEI><affiliations><list><country><li>États-Unis</li></country><region><li>Géorgie (États-Unis)</li><li>Maryland</li></region></list><tree><country name="États-Unis"><region name="Maryland"><name sortKey="Das, Suman R" sort="Das, Suman R" uniqKey="Das S" first="Suman R." last="Das">Suman R. Das</name></region><name sortKey="Bennink, Jack R" sort="Bennink, Jack R" uniqKey="Bennink J" first="Jack R." last="Bennink">Jack R. Bennink</name><name sortKey="Das, Suman R" sort="Das, Suman R" uniqKey="Das S" first="Suman R." last="Das">Suman R. Das</name><name sortKey="David, Alexandre" sort="David, Alexandre" uniqKey="David A" first="Alexandre" last="David">Alexandre David</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="Ince, William L" sort="Ince, William L" uniqKey="Ince W" first="William L." last="Ince">William L. Ince</name><name sortKey="Puigb, Pere" sort="Puigb, Pere" uniqKey="Puigb P" first="Pere" last="Puigb">Pere Puigb</name><name sortKey="Schmidt, Loren" sort="Schmidt, Loren" uniqKey="Schmidt L" first="Loren" last="Schmidt">Loren Schmidt</name><name sortKey="Yewdell, Jonathan W" sort="Yewdell, Jonathan W" uniqKey="Yewdell J" first="Jonathan W." last="Yewdell">Jonathan W. Yewdell</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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