1887

Abstract

Virus-specific CD8 T-cells contribute to protective immunity against influenza A virus (IAV) infections. As the majority of these cells are directed to conserved viral proteins, they may afford protection against IAVs of various subtypes. The present study assessed the cross-reactivity of human CD8 T-lymphocytes, induced by infection with seasonal A (H1N1) or A (H3N2) influenza virus, with 2009 pandemic influenza A (H1N1) virus [A(H1N1)pdm09] and swine-origin triple-reassortant A (H3N2) [A(H3N2)v] viruses that are currently causing an increasing number of human cases in the USA. It was demonstrated that CD8 T-cells induced after seasonal IAV infections exerted lytic activity and produced gamma interferon upon restimulation with A(H1N1)pdm09 and A(H3N2)v influenza A viruses. Furthermore, CD8 T-cells directed to A(H1N1)pdm09 virus displayed a high degree of cross-reactivity with A(H3N2)v viruses. It was concluded that cross-reacting T-cells had the potential to afford protective immunity against A(H1N1)pdm09 viruses during the pandemic and offer some degree of protection against infection with A(H3N2)v viruses.

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2013-03-01
2020-10-21
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References

  1. 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 Immunol 18:469–476 [CrossRef][PubMed]
    [Google Scholar]
  2. Boon A. C., de Mutsert G., Graus Y. M., Fouchier R. A., Sintnicolaas K., Osterhaus A. D., Rimmelzwaan G. F. 2002; The magnitude and specificity of influenza A virus-specific cytotoxic T-lymphocyte responses in humans is related to HLA-A and -B phenotype. J Virol 76:582–590 [CrossRef][PubMed]
    [Google Scholar]
  3. Boon A. C., De Mutsert G., Fouchier R. A., Sintnicolaas K., Osterhaus A. D., Rimmelzwaan G. F. 2004a; Preferential HLA usage in the influenza virus-specific CTL response. J Immunol 172:4435–4443[PubMed] [CrossRef]
    [Google Scholar]
  4. Boon A. C., de Mutsert G., van Baarle D., Smith D. J., Lapedes A. S., Fouchier R. A., Sintnicolaas K., Osterhaus A. D., Rimmelzwaan G. F. 2004b; Recognition of homo- and heterosubtypic variants of influenza A viruses by human CD8+ T lymphocytes. J Immunol 172:2453–2460[PubMed] [CrossRef]
    [Google Scholar]
  5. Bui H. H., Sidney J., Li W., Fusseder N., Sette A. 2007; Development of an epitope conservancy analysis tool to facilitate the design of epitope-based diagnostics and vaccines. BMC Bioinformatics 8:361 [CrossRef][PubMed]
    [Google Scholar]
  6. CDC 2011a; CDC Confirms Two Human Infections with Novel Influenza Viruses. Centers for Disease Control and Prevention. http://www.cdc.gov/media/haveyouheard/stories/novel_influenza.html
  7. CDC 2011b; Limited Human-to-human Transmission of Novel Influenza A (H3N2) Virus – Iowa, November 2011. MMWR Morb Mortal Wkly Rep 60:1615–1617[PubMed]
    [Google Scholar]
  8. CDC 2012a; Evaluation of Rapid Influenza Diagnostic Tests for Influenza A (H3N2)v Virus and Updated Case Count United States, 2012. Centers for Disease Control and Prevention. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6132a4.htm
  9. CDC 2012b; First H3N2 variant virus infection reported for 2012. Centers for Disease Control and Prevention. http://www.cdc.gov/flu/spotlights/h3n2v-variant-utah.htm
  10. CDC 2012c; Influenza A (H3N2) variant virus. Centers for Disease Control and Prevention. http://www.cdc.gov/flu/swineflu/h3n2v-outbreak.htm
  11. CDC 2012d). Notes from the field: outbreak of influenza A (H3N2) virus among persons and swine at a county fair – Indiana, July 2012. MMWR Morb Mortal Wkly Rep 61:561[PubMed]
    [Google Scholar]
  12. Claas E. C., Kawaoka Y., de Jong J. C., Masurel N., Webster R. G. 1994; Infection of children with avian–human reassortant influenza virus from pigs in Europe. Virology 204:453–457 [CrossRef][PubMed]
    [Google Scholar]
  13. Dawood F. S., Iuliano A. D., Reed C., Meltzer M. I., Shay D. K., Cheng P.-Y., Bandaranayake D., Breiman R. F., Brooks W. A. other authors 2012; Estimated global mortality associated with the first 12 months of 2009 pandemic influenza A H1N1 virus circulation: a modelling study. Lancet Infect Dis 12:687–695 [CrossRef][PubMed]
    [Google Scholar]
  14. de Jong J. C., de Ronde-Verloop J. M., Bangma P. J., van Kregten E., Kerckhaert J., Paccaud M. F., Wicki F., Wunderli W. 1986; Isolation of swine-influenza-like A(H1N1) viruses from man in Europe, 1986. Lancet 328:1329–1330 [CrossRef][PubMed]
    [Google Scholar]
  15. de Jong J. C., Claas E. C., Osterhaus A. D., Webster R. G., Lim W. L. 1997; A pandemic warning?. Nature 389:554 [CrossRef][PubMed]
    [Google Scholar]
  16. Ducatez M. F., Hause B., Stigger-Rosser E., Darnell D., Corzo C., Juleen K., Simonson R., Brockwell-Staats C., Rubrum A. other authors 2011; Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States. Emerg Infect Dis 17:1624–1629 [CrossRef][PubMed]
    [Google Scholar]
  17. Fan X., Zhu H., Zhou B., Smith D. K., Chen X., Lam T. T., Poon L. L., Peiris M., Guan Y. 2012; Emergence and dissemination of a swine H3N2 reassortant influenza virus with 2009 pandemic H1N1 genes in pigs in China. J Virol 86:2375–2378 [CrossRef][PubMed]
    [Google Scholar]
  18. Fouchier R. A., Schneeberger P. M., Rozendaal F. W., Broekman J. M., Kemink S. A., Munster V., Kuiken T., Rimmelzwaan G. F., Schutten M. other authors 2004; Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc Natl Acad Sci U S A 101:1356–1361 [CrossRef][PubMed]
    [Google Scholar]
  19. Garten R. J., Davis C. T., Russell C. A., Shu B., Lindstrom S., Balish A., Sessions W. M., Xu X., Skepner E. other authors 2009; Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197–201 [CrossRef][PubMed]
    [Google Scholar]
  20. Gaydos J. C., Hodder R. A., Top F. H. Jr, Soden V. J., Allen R. G., Bartley J. D., Zabkar J. H., Nowosiwsky T., Russell P. K. 1977; Swine influenza A at Fort Dix, New Jersey (January–February 1976). I. Case finding and clinical study of cases. J Infect Dis 136:Suppl.S356–S362 [CrossRef][PubMed]
    [Google Scholar]
  21. Girard M. P., Tam J. S., Assossou O. M., Kieny M. P. 2010; The 2009 A (H1N1) influenza virus pandemic: a review. Vaccine 28:4895–4902 [CrossRef][PubMed]
    [Google Scholar]
  22. Gras S., Kedzierski L., Valkenburg S. A., Laurie K., Liu Y. C., Denholm J. T., Richards M. J., Rimmelzwaan G. F., Kelso A. other authors 2010; Cross-reactive CD8+ T-cell immunity between the pandemic H1N1-2009 and H1N1-1918 influenza A viruses. Proc Natl Acad Sci U S A 107:12599–12604 [CrossRef][PubMed]
    [Google Scholar]
  23. Grebe K. M., Yewdell J. W., Bennink J. R. 2008; Heterosubtypic immunity to influenza A virus: where do we stand?. Microbes Infect 10:1024–1029 [CrossRef][PubMed]
    [Google Scholar]
  24. Hancock K., Veguilla V., Lu X., Zhong W., Butler E. N., Sun H., Liu F., Dong L., DeVos J. R. other authors 2009; Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med 361:1945–1952 [CrossRef][PubMed]
    [Google Scholar]
  25. Herfst S., Schrauwen E. J., Linster M., Chutinimitkul S., de Wit E., Munster V. J., Sorrell E. M., Bestebroer T. M., Burke D. F. other authors 2012; Airborne transmission of influenza A/H5N1 virus between ferrets. Science 336:1534–1541 [CrossRef][PubMed]
    [Google Scholar]
  26. Hillaire M. L., Osterhaus A. D., Rimmelzwaan G. F. 2011a; Induction of virus-specific cytotoxic T lymphocytes as a basis for the development of broadly protective influenza vaccines. J Biomed Biotechnol 2011:939860 [CrossRef][PubMed]
    [Google Scholar]
  27. Hillaire M. L., van Trierum S. E., Kreijtz J. H., Bodewes R., Geelhoed-Mieras M. M., Nieuwkoop N. J., Fouchier R. A., Kuiken T., Osterhaus A. D., Rimmelzwaan G. F. 2011b; Cross-protective immunity against influenza pH1N1 2009 viruses induced by seasonal influenza A (H3N2) virus is mediated by virus-specific T-cells. J Gen Virol 92:2339–2349 [CrossRef][PubMed]
    [Google Scholar]
  28. Imai M., Watanabe T., Hatta M., Das S. C., Ozawa M., Shinya K., Zhong G., Hanson A., Katsura H. other authors 2012; Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 486:420–428[PubMed]
    [Google Scholar]
  29. Ito T., Couceiro J. N., Kelm S., Baum L. G., Krauss S., Castrucci M. R., Donatelli I., Kida H., Paulson J. C. other authors 1998; Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 72:7367–7373[PubMed]
    [Google Scholar]
  30. Jameson J., Cruz J., Terajima M., Ennis F. A. 1999; Human CD8+ and CD4+ T lymphocyte memory to influenza A viruses of swine and avian species. J Immunol 162:7578–7583[PubMed]
    [Google Scholar]
  31. Kreijtz J. H., de Mutsert G., van Baalen C. A., Fouchier R. A., Osterhaus A. D., Rimmelzwaan G. F. 2008; Cross-recognition of avian H5N1 influenza virus by human cytotoxic T-lymphocyte populations directed to human influenza A virus. J Virol 82:5161–5166 [CrossRef][PubMed]
    [Google Scholar]
  32. Lee L. Y., Ha L. A., Simmons C., de Jong M. D., Chau N. V., Schumacher R., Peng Y. C., McMichael A. J., Farrar J. J. other authors 2008; Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J Clin Invest 118:3478–3490[PubMed]
    [Google Scholar]
  33. Lin Y. P., Shaw M., Gregory V., Cameron K., Lim W., Klimov A., Subbarao K., Guan Y., Krauss S. other authors 2000; Avian-to-human transmission of H9N2 subtype influenza A viruses: relationship between H9N2 and H5N1 human isolates. Proc Natl Acad Sci U S A 97:9654–9658 [CrossRef][PubMed]
    [Google Scholar]
  34. Lukacher A. E., Braciale V. L., Braciale T. J. 1984; In vivo effector function of influenza virus-specific cytotoxic T lymphocyte clones is highly specific. J Exp Med 160:814–826 [CrossRef][PubMed]
    [Google Scholar]
  35. Matrosovich M. N., Gambaryan A. S., Teneberg S., Piskarev V. E., Yamnikova S. S., Lvov D. K., Robertson J. S., Karlsson K. A. 1997; Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 233:224–234 [CrossRef][PubMed]
    [Google Scholar]
  36. McMichael A. J., Gotch F. M., Noble G. R., Beare P. A. 1983; Cytotoxic T-cell immunity to influenza. N Engl J Med 309:13–17 [CrossRef][PubMed]
    [Google Scholar]
  37. Neumann G., Noda T., Kawaoka Y. 2009; Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459:931–939 [CrossRef][PubMed]
    [Google Scholar]
  38. Olsen C. W., Karasin A. I., Carman S., Li Y., Bastien N., Ojkic D., Alves D., Charbonneau G., Henning B. M. other authors 2006; Triple reassortant H3N2 influenza A viruses, Canada, 2005. Emerg Infect Dis 12:1132–1135 [CrossRef][PubMed]
    [Google Scholar]
  39. Patriarca P. A., Kendal A. P., Zakowski P. C., Cox N. J., Trautman M. S., Cherry J. D., Auerbach D. M., McCusker J., Belliveau R. R., Kappus K. D. 1984; Lack of significant person-to-person spread of swine influenza-like virus following fatal infection in an immunocompromised child. Am J Epidemiol 119:152–158[PubMed]
    [Google Scholar]
  40. Pearce M. B., Jayaraman A., Pappas C., Belser J. A., Zeng H., Gustin K. M., Maines T. R., Sun X., Raman R. other authors 2012; Pathogenesis and transmission of swine origin A(H3N2)v influenza viruses in ferrets. Proc Natl Acad Sci U S A 109:3944–3949 [CrossRef][PubMed]
    [Google Scholar]
  41. Rimmelzwaan G. F., Baars M., Claas E. C., Osterhaus A. D. 1998; Comparison of RNA hybridization, hemagglutination assay, titration of infectious virus and immunofluorescence as methods for monitoring influenza virus replication in vitro. J Virol Methods 74:57–66 [CrossRef][PubMed]
    [Google Scholar]
  42. Rimmelzwaan G. F., de Jong J. C., Bestebroer T. M., van Loon A. M., Claas E. C., Fouchier R. A., Osterhaus A. D. 2001; Antigenic and genetic characterization of swine influenza A (H1N1) viruses isolated from pneumonia patients in The Netherlands. Virology 282:301–306 [CrossRef][PubMed]
    [Google Scholar]
  43. Rogers G. N., D’Souza B. L. 1989; Receptor binding properties of human and animal H1 influenza virus isolates. Virology 173:317–322 [CrossRef][PubMed]
    [Google Scholar]
  44. Seo S. H., Webster R. G. 2001; Cross-reactive, cell-mediated immunity and protection of chickens from lethal H5N1 influenza virus infection in Hong Kong poultry markets. J Virol 75:2516–2525 [CrossRef][PubMed]
    [Google Scholar]
  45. Skowronski D. M., De Serres G., Janjua N. Z., Gardy J. L., Gilca V., Dionne M., Hamelin M. E., Rhéaume C., Boivin G. 2012a; Cross-reactive antibody to swine influenza A(H3N2) subtype virus in children and adults before and after immunisation with 2010/11 trivalent inactivated influenza vaccine in Canada, August to November 2010. Euro Surveill 17:20066[PubMed]
    [Google Scholar]
  46. Skowronski D. M., Janjua N. Z., De Serres G., Purych D., Gilca V., Scheifele D. W., Dionne M., Sabaiduc S., Gardy J. L. other authors 2012b; Cross-reactive and vaccine-induced antibody to an emerging swine-origin variant of influenza A virus subtype H3N2 (H3N2v). J Infect Dis 206:1852–1861 [CrossRef][PubMed]
    [Google Scholar]
  47. Suzuki Y. 2005; Sialobiology of influenza: molecular mechanism of host range variation of influenza viruses. Biol Pharm Bull 28:399–408 [CrossRef][PubMed]
    [Google Scholar]
  48. Taylor P. M., Askonas B. A. 1986; Influenza nucleoprotein-specific cytotoxic T-cell clones are protective in vivo. Immunology 58:417–420[PubMed]
    [Google Scholar]
  49. Thompson C. I., Barclay W. S., Zambon M. C., Pickles R. J. 2006; Infection of human airway epithelium by human and avian strains of influenza A virus. J Virol 80:8060–8068 [CrossRef][PubMed]
    [Google Scholar]
  50. Tu W., Mao H., Zheng J., Liu Y., Chiu S. S., Qin G., Chan P.-L., Lam K.-T., Guan J. other authors 2010; Cytotoxic T lymphocytes established by seasonal human influenza cross-react against 2009 pandemic H1N1 influenza virus. J Virol 84:6527–6535 [CrossRef][PubMed]
    [Google Scholar]
  51. Ungchusak K., Auewarakul P., Dowell S. F., Kitphati R., Auwanit W., Puthavathana P., Uiprasertkul M., Boonnak K., Pittayawonganon C. other authors 2005; Probable person-to-person transmission of avian influenza A (H5N1). N Engl J Med 352:333–340 [CrossRef][PubMed]
    [Google Scholar]
  52. Voeten J. T., Bestebroer T. M., Nieuwkoop N. J., Fouchier R. A., Osterhaus A. D., Rimmelzwaan G. F. 2000; Antigenic drift in the influenza A virus (H3N2) nucleoprotein and escape from recognition by cytotoxic T lymphocytes. J Virol 74:6800–6807 [CrossRef][PubMed]
    [Google Scholar]
  53. Wentworth D. E., Thompson B. L., Xu X., Regnery H. L., Cooley A. J., McGregor M. W., Cox N. J., Hinshaw V. S. 1994; An influenza A (H1N1) virus, closely related to swine influenza virus, responsible for a fatal case of human influenza. J Virol 68:2051–2058[PubMed]
    [Google Scholar]
  54. WHO 2009; Pandemic (H1N1) 2009 – Update 112. Geneva, Switzerland: World Health Organization. Available at. http://www.who.int/csr/don/2010_08_06/en/index.html
  55. WHO 2010; Cumulative Number of Confirmed Human Cases of Avian Influenza A/(H5N1). Geneva, Switzerland: World Health Organization. http://www.who.int/influenza/human_animal_interface/EN_GIP_20120810CumulativeNumberH5N1cases.pdf
  56. WHO 2011; Standardization of Terminology for the Variant A(H3N2) Virus Recently Infecting Humans. Geneva, Switzerland: World Health Organization. http://www.who.int/influenza/gisrs_laboratory/terminology_ah3n2v/en/
  57. Wilkinson T. M., Li C. K., Chui C. S., Huang A. K., Perkins M., Liebner J. C., Lambkin-Williams R., Gilbert A., Oxford J. other authors 2012; Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat Med 18:274–280 [CrossRef][PubMed]
    [Google Scholar]
  58. Yang Z. Y., Huang Y., Ganesh L., Leung K., Kong W. P., Schwartz O., Subbarao K., Nabel G. J. 2004; pH-dependent entry of severe acute respiratory syndrome coronavirus is mediated by the spike glycoprotein and enhanced by dendritic cell transfer through DC-SIGN. J Virol 78:5642–5650 [CrossRef][PubMed]
    [Google Scholar]
  59. Yang Y., Halloran M. E., Sugimoto J. D., Longini I. M. Jr 2007; Detecting human-to-human transmission of avian influenza A (H5N1). Emerg Infect Dis 13:1348–1353 [CrossRef][PubMed]
    [Google Scholar]
  60. Yap K. L., Ada G. L., McKenzie I. F. 1978; Transfer of specific cytotoxic T lymphocytes protects mice inoculated with influenza virus. Nature 273:238–239 [CrossRef][PubMed]
    [Google Scholar]
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