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Research Article

Hemagglutinin stalk antibodies elicited by the 2009 pandemic influenza virus as a mechanism for the extinction of seasonal H1N1 viruses

Natalie Pica, Rong Hai, Florian Krammer, Taia T. Wang, Jad Maamary, Dirk Eggink, Gene S. Tan, Jens C. Krause, Thomas Moran, Cheryl R. Stein, David Banach, Jens Wrammert, Robert B. Belshe, Adolfo García-Sastre, and Peter Palese
PNAS first published January 30, 2012; https://doi.org/10.1073/pnas.1200039109
Natalie Pica
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Rong Hai
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Florian Krammer
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Taia T. Wang
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Jad Maamary
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Dirk Eggink
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Gene S. Tan
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Jens C. Krause
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Thomas Moran
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Cheryl R. Stein
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David Banach
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Jens Wrammert
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Robert B. Belshe
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Adolfo García-Sastre
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Peter Palese
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  • For correspondence: peter.palese@mssm.edu
  1. Contributed by Peter Palese, January 3, 2012 (sent for review December 28, 2011)

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Abstract

After the emergence of pandemic influenza viruses in 1957, 1968, and 2009, existing seasonal viruses were observed to be replaced in the human population by the novel pandemic strains. We have previously hypothesized that the replacement of seasonal strains was mediated, in part, by a population-scale boost in antibodies specific for conserved regions of the hemagglutinin stalk and the viral neuraminidase. Numerous recent studies have shown the role of stalk-specific antibodies in neutralization of influenza viruses; the finding that stalk antibodies can effectively neutralize virus alters the existing dogma that influenza virus neutralization is mediated solely by antibodies that react with the globular head of the viral hemagglutinin. The present study explores the possibility that stalk-specific antibodies were boosted by infection with the 2009 H1N1 pandemic virus and that those antibodies could have contributed to the disappearance of existing seasonal H1N1 influenza virus strains. To study stalk-specific antibodies, we have developed chimeric hemagglutinin constructs that enable the measurement of antibodies that bind the hemagglutinin protein and neutralize virus but do not have hemagglutination inhibition activity. Using these chimeric hemagglutinin reagents, we show that infection with the 2009 pandemic H1N1 virus elicited a boost in titer of virus-neutralizing antibodies directed against the hemagglutinin stalk. In addition, we describe assays that can be used to measure influenza virus-neutralizing antibodies that are not detected in the traditional hemagglutination inhibition assay.

  • cross-reactivity
  • cross-protection
  • subtype

Footnotes

  • ↵1N.P. and R.H. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. E-mail: peter.palese{at}mssm.edu.
  • Author contributions: N.P., R.H., F.K., T.T.W. and P.P. designed research; N.P., R.H., F.K., T.T.W., J.M., D.E., G.S.T., and J.C.K. performed research; T.M., C.R.S., D.B., J.W., and R.B.B. contributed new reagents/analytic tools; N.P., R.H., F.K., T.T.W., J.M., D.E., G.S.T., J.C.K., T.M., J.W., A.G.-S., and P.P. analyzed data; and N.P., T.T.W., and P.P. wrote the paper.

  • The authors declare no conflict of interest.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1200039109/-/DCSupplemental.

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Hemagglutinin stalk antibodies elicited by the 2009 pandemic influenza virus as a mechanism for the extinction of seasonal H1N1 viruses
Natalie Pica, Rong Hai, Florian Krammer, Taia T. Wang, Jad Maamary, Dirk Eggink, Gene S. Tan, Jens C. Krause, Thomas Moran, Cheryl R. Stein, David Banach, Jens Wrammert, Robert B. Belshe, Adolfo García-Sastre, Peter Palese
Proceedings of the National Academy of Sciences Jan 2012, 201200039; DOI: 10.1073/pnas.1200039109

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Hemagglutinin stalk antibodies elicited by the 2009 pandemic influenza virus as a mechanism for the extinction of seasonal H1N1 viruses
Natalie Pica, Rong Hai, Florian Krammer, Taia T. Wang, Jad Maamary, Dirk Eggink, Gene S. Tan, Jens C. Krause, Thomas Moran, Cheryl R. Stein, David Banach, Jens Wrammert, Robert B. Belshe, Adolfo García-Sastre, Peter Palese
Proceedings of the National Academy of Sciences Jan 2012, 201200039; DOI: 10.1073/pnas.1200039109
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