1887

Abstract

Pre-existing immunity played a significant role in protection during the latest influenza A virus H1N1 pandemic, especially in older age groups. Structural similarities were found between A(H1N1)2009 and older H1N1 virus strains to which humans had already been exposed. Broadly cross-reactive antibodies capable of neutralizing the A(H1N1)2009 virus have been implicated in this immune protection in adults. We investigated the serological profile of a group of young children aged 9 years (=55), from whom paired blood samples were available, just prior to the pandemic wave (March 2009) and shortly thereafter (March 2010). On the basis of A(H1N1)2009 seroconversion, 27 of the 55 children (49 %) were confirmed to be infected between these two time points. Within the non-infected group of 28 children (51 %), high levels of seasonal antibodies to H1 and H3 HA1 antigens were detected prior to pandemic exposure, reflecting past infection with H1N1 and H3N2, both of which had circulated in The Netherlands prior to the pandemic. In some children, this reactivity coincided with specific antibody reactivity against A(H1N1)2009. While these antibodies were not able to neutralize the A(H1N1)2009 virus, they were able to mediate antibody-dependent cellular cytotoxicity (ADCC) upon interaction with the A(H1N1)2009 virus. This finding suggests that cross-reactive antibodies could contribute to immune protection in children via ADCC.

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2016-09-01
2019-12-14
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References

  1. Ahmed M. S., Jacques L. C., Mahallawi W., Ferrara F., Temperton N., Upile N., Vaughan C., Sharma R., Beer H. et al. 2015; Cross-reactive immunity against influenza viruses in children and adults following 2009 pandemic H1N1 infection. Antiviral Res114:106–112 [CrossRef][PubMed]
    [Google Scholar]
  2. Baas D. C., Koopmans M. P., de Bruin E., ten Hulscher H. I., Buisman A. M., Hendrikx L. H., van Beek J., Godeke G. J., Reimerink J., van Binnendijk R. S.. 2013; Detection of influenza A virus homo- and heterosubtype-specific memory B-cells using a novel protein microarray-based analysis tool. J Med Virol85:899–909 [CrossRef][PubMed]
    [Google Scholar]
  3. Black S., Nicolay U., Vesikari T., Knuf M., Del Giudice G., Della Cioppa G., Tsai T., Clemens R., Rappuoli R.. 2011; Hemagglutination inhibition antibody titers as a correlate of protection for inactivated influenza vaccines in children. Pediatr Infect Dis J30:1081–1085 [CrossRef][PubMed]
    [Google Scholar]
  4. Bodewes R., de Mutsert G., van der Klis F. R., Ventresca M., Wilks S., Smith D. J., Koopmans M., Fouchier R. A., Osterhaus A. D., Rimmelzwaan G. F.. 2011; Prevalence of antibodies against seasonal influenza A and B viruses in children in Netherlands. Clin Vaccine Immunol18:469–476 [CrossRef][PubMed]
    [Google Scholar]
  5. Co M. D., Terajima M., Thomas S. J., Jarman R. G., Rungrojcharoenkit K., Fernandez S., Yoon I. K., Buddhari D., Cruz J., Ennis F. A.. 2014; Relationship of preexisting influenza hemagglutination inhibition, complement-dependent lytic, and antibody-dependent cellular cytotoxicity antibodies to the development of clinical illness in a prospective study of A(H1N1)pdm09 Influenza in children. Viral Immunol27:375–382 [CrossRef][PubMed]
    [Google Scholar]
  6. Corti D., Suguitan A. L., Pinna D., Silacci C., Fernandez-Rodriguez B. M., Vanzetta F., Santos C., Luke C. J., Torres-Velez F. J. et al. 2010; Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J Clin Invest120:1663–1673 [CrossRef][PubMed]
    [Google Scholar]
  7. Corti D., Voss J., Gamblin S. J., Codoni G., Macagno A., Jarrossay D., Vachieri S. G., Pinna D., Minola A. et al. 2011; A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science333:850–856 [CrossRef][PubMed]
    [Google Scholar]
  8. de Bruin E., Loeber J. G., Meijer A., Castillo G. M., Cepeda M. L., Torres-Sepúlveda M. R., Borrajo G. J., Caggana M., Giguere Y. et al. 2014; Evolution of an influenza pandemic in 13 countries from 5 continents monitored by protein microarray from neonatal screening bloodspots. J Clin Virol61:74–80 [CrossRef][PubMed]
    [Google Scholar]
  9. DiLillo D. J., Tan G. S., Palese P., Ravetch J.. 2014; Broadly neutralizing hemagglutinin stalk–specific antibodies require FcγR interactions for protection against influenza virus in vivo. Nat Med20:143–151 [CrossRef]
    [Google Scholar]
  10. Ekiert D. C., Bhabha G., Elsliger M. A., Friesen R. H., Jongeneelen M., Throsby M., Goudsmit J., Wilson I. A.. 2009; Antibody recognition of a highly conserved influenza virus epitope. Science324:246–251 [CrossRef][PubMed]
    [Google Scholar]
  11. Freidl G. S., Binger T., Müller M. A., de Bruin E., van Beek J., Corman V. M., Rasche A., Drexler J. F., Sylverken A. et al. 2015; Serological evidence of influenza A viruses in frugivorous bats from Africa. PLoS One10:e0127035 [CrossRef][PubMed]
    [Google Scholar]
  12. Garten R. J., Davis C. T., Russell C. A., Shu B., Lindstrom S., Balish A., Sessions W. M., Xu X., Skepner E. et al. 2009; Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science325:197–201 [CrossRef][PubMed]
    [Google Scholar]
  13. Greenbaum J. A., Kotturi M. F., Kim Y., Oseroff C., Vaughan K., Salimi N., Vita R., Ponomarenko J., Scheuermann R. H. et al. 2009; Pre-existing immunity against swine-origin H1N1 influenza viruses in the general human population. Proc Natl Acad Sci U S A106:20365–20370 [CrossRef]
    [Google Scholar]
  14. Hancock K., Veguilla V., Lu X., Zhong W., Butler E. N., Sun H., Liu F., Dong L., DeVos J. R. et al. 2009; Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med361:1945–1952 [CrossRef][PubMed]
    [Google Scholar]
  15. Haran J. P., Hoaglin D. C., Chen H., Boyer E. W., Lu S.. 2014; Antigen-specific H1N1 influenza antibody responses in acute respiratory tract infections and their relation to influenza infection and disease course. J Clin Virol60:367–373 [CrossRef][PubMed]
    [Google Scholar]
  16. Hashimoto G., Wright P. F., Karzon D. T.. 1983; Antibody-dependent cell-mediated cytotoxicity against influenza virus-infected cells. J Infect Dis148:785–794 [CrossRef][PubMed]
    [Google Scholar]
  17. Hendrikx L. H., Felderhof M. K., Oztürk K., de Rond L. G., van Houten M. A., Sanders E. A., Berbers G. A., Buisman A. M.. 2011; Enhanced memory B-cell immune responses after a second acellular pertussis booster vaccination in children 9 years of age. Vaccine30:51–58 [CrossRef][PubMed]
    [Google Scholar]
  18. Jegaskanda S., Job E. R., Kramski M., Laurie K., Isitman G., de Rose R., Winnall W. R., Stratov I., Brooks A. G. et al. 2013a; Cross-reactive influenza-specific antibody-dependent cellular cytotoxicity antibodies in the absence of neutralizing antibodies. J Immunol190:1837–1848 [CrossRef][PubMed]
    [Google Scholar]
  19. Jegaskanda S., Laurie K. L., Amarasena T. H., Winnall W. R., Kramski M., De Rose R., Barr I. G., Brooks A. G., Reading P. C., Kent S. J.. 2013b; Age-associated cross-reactive antibody-dependent cellular cytotoxicity toward 2009 pandemic influenza A virus subtype H1N1. J Infect Dis208:1051–1061 [CrossRef]
    [Google Scholar]
  20. Jegaskanda S., Reading P. C., Kent S. J.. 2014a; Influenza-specific antibody-dependent cellular cytotoxicity: toward a universal influenza vaccine. J Immunol193:469–475 [CrossRef][PubMed]
    [Google Scholar]
  21. Jegaskanda S., Vandenberg K., Laurie K. L., Loh L., Kramski M., Winnall W. R., Kedzierska K., Rockman S., Kent S. J.. 2014b; Cross-reactive influenza-specific antibody-dependent cellular cytotoxicity in intravenous immunoglobulin as a potential therapeutic against emerging influenza viruses. J Infect Dis210:1811–1822 [CrossRef][PubMed]
    [Google Scholar]
  22. Jegerlehner A., Schmitz N., Storni T., Bachmann M. F.. 2004; Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J Immunol172:5598–5605 [CrossRef][PubMed]
    [Google Scholar]
  23. Koopmans M., de Bruin E., Godeke G. J., Friesema I., van Gageldonk R., Schipper M., Meijer A., van Binnendijk R., Rimmelzwaan G. F. et al. 2012; Profiling of humoral immune responses to influenza viruses by using protein microarray. Clin Microbiol Infect18:797–807 [CrossRef][PubMed]
    [Google Scholar]
  24. Krause J. C., Tumpey T. M., Huffman C. J., McGraw P. A., Pearce M. B., Tsibane T., Hai R., Basler C. F., Crowe J. E.. 2010; Naturally occurring human monoclonal antibodies neutralize both 1918 and 2009 pandemic influenza A (H1N1) viruses. J Virol84:3127–3130 [CrossRef][PubMed]
    [Google Scholar]
  25. Lamb R. A., Zebedee S. L., Richardson C. D.. 1985; Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell40:627–633 [CrossRef][PubMed]
    [Google Scholar]
  26. Lemaitre M., Leruez-Ville M., De Lamballerie X. N., Salez N., Garrone P., Fluckiger A. C., Klatzmann D., Carrat F.. 2011; Seasonal H1N1 2007 influenza virus infection is associated with elevated pre-exposure antibody titers to the 2009 pandemic influenza A (H1N1) virus. Clin Microbiol Infect17:732–737 [CrossRef][PubMed]
    [Google Scholar]
  27. Li G. M., Chiu C., Wrammert J., McCausland M., Andrews S. F., Zheng N. Y., Lee J. H., Huang M., Qu X. et al. 2012; Pandemic H1N1 influenza vaccine induces a recall response in humans that favors broadly cross-reactive memory B cells. Proc Natl Acad Sci U S A109:9047–9052 [CrossRef][PubMed]
    [Google Scholar]
  28. Olivier J., Johnson W. D., Marshall G. D.. 2008; The logarithmic transformation and the geometric mean in reporting experimental IgE results: what are they and when and why to use them?. Ann Allergy Asthma Immunol100:333–337 [CrossRef][PubMed]
    [Google Scholar]
  29. Schmitz N., Beerli R. R., Bauer M., Jegerlehner A., Dietmeier K., Maudrich M., Pumpens P., Saudan P., Bachmann M. F.. 2012; Universal vaccine against influenza virus: linking TLR signaling to anti-viral protection. Eur J Immunol42:863–869 [CrossRef][PubMed]
    [Google Scholar]
  30. Skehel J. J., Wiley D. C.. 2000; Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem69:531–569 [CrossRef][PubMed]
    [Google Scholar]
  31. Srivastava V., Yang Z., Hung I. F., Xu J., Zheng B., Zhang M. Y.. 2013; Identification of dominant antibody-dependent cell-mediated cytotoxicity epitopes on the hemagglutinin antigen of pandemic H1N1 influenza virus. J Virol87:5831–5840 [CrossRef][PubMed]
    [Google Scholar]
  32. Tamura M., Webster R. G., Ennis F. A.. 1993; Neutralization and infection-enhancement epitopes of influenza A virus hemagglutinin. J Immunol151:1731–1738
    [Google Scholar]
  33. te Beest D., de Bruin E., Imholz S., Wallinga J., Teunis P., Koopmans M., van Boven M.. 2014; Discrimination of influenza infection (A/2009 H1N1) from prior exposure by antibody protein microarray analysis. PLoS One9:e113021 [CrossRef][PubMed]
    [Google Scholar]
  34. Terajima M., Co M. D., Cruz J., Ennis F. A.. 2015; High antibody-dependent cellular cytotoxicity antibody titers to H5N1 and H7N9 avian influenza A viruses in healthy US adults and older children. J Infect Dis212:1052–1060 [CrossRef][PubMed]
    [Google Scholar]
  35. Throsby M., van den Brink E., Jongeneelen M., Poon L. L., Alard P., Cornelissen L., Bakker A., Cox F., van Deventer E. et al. 2008; Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS One3:e3942 [CrossRef][PubMed]
    [Google Scholar]
  36. Voskoboinik I., Whisstock J. C., Trapani J. A.. 2015; Perforin and granzymes: function, dysfunction and human pathology. Nat Rev Immunol15:388–400 [CrossRef][PubMed]
    [Google Scholar]
  37. Watanabe T., Zhong G., Russell C. A., Nakajima N., Hatta M., Hanson A., McBride R., Burke D. F., Takahashi K. et al. 2014; Circulating avian influenza viruses closely related to the 1918 virus have pandemic potential. Cell Host Microbe15:692–705 [CrossRef][PubMed]
    [Google Scholar]
  38. Wrammert J., Koutsonanos D., Li G. M., Edupuganti S., Sui J., Morrissey M., McCausland M., Skountzou I., Hornig M. et al. 2011; Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med208:181–193 [CrossRef][PubMed]
    [Google Scholar]
  39. Xu R., Ekiert D. C., Krause J. C., Hai R., Crowe J. E., Wilson I. A.. 2010; Structural basis of preexisting immunity to the 2009 H1N1 pandemic influenza virus. Science328:357–360 [CrossRef][PubMed]
    [Google Scholar]
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