1887

Abstract

It was recently shown that the use of an experimental subunit vaccine protected mice against infection with a human A/H3N2 influenza virus, but consequently affected the induction of heterosubtypic immunity to a highly pathogenic A/H5N1 influenza virus, which was otherwise induced by the A/H3N2 infection. As whole inactivated virus (WIV) vaccines are widely used to protect against seasonal influenza and also contain inner viral proteins such as the nucleoprotein (NP), the potential of a WIV vaccine to induce protective immunity against infection was tested with a homologous A/H3N2 (A/Hong Kong/2/68) and a heterosubtypic A/H5N1 influenza virus (A/Indonesia/5/05). As expected, the vaccine afforded protection against infection with the A/H3N2 virus only. In addition, it was demonstrated that the use of WIV vaccine for protection against A/H3N2 infection affected the induction of heterosubtypic immunity that was otherwise afforded by A/H3N2 influenza virus infection. The reduction in protective immunity correlated with changes in the immunodominance patterns of the CD8 T-cell responses directed to the epitopes located in the acid polymerase subunit of the viral RNA polymerase (PA) and the NP (NP). In unvaccinated mice that experienced infection with the A/H3N2 influenza virus, the magnitude of the CD8 T-cell response to both peptides was similar on secondary infection with A/H5N1 influenza virus. In contrast, prior vaccination with WIV affected the immunodominance pattern and skewed the response after infection with influenza virus A/Indonesia/5/05 towards a dominant NP-specific response. These findings may have implications for vaccination strategies aimed at the induction of protective immunity to seasonal and/or pandemic influenza.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.020784-0
2010-07-01
2019-11-15
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/7/1743.html?itemId=/content/journal/jgv/10.1099/vir.0.020784-0&mimeType=html&fmt=ahah

References

  1. Altman, J. D., Moss, P. A., Goulder, P. J., Barouch, D. H., McHeyzer-Williams, M. G., Bell, J. I., McMichael, A. J. & Davis, M. M. ( 1996; ). Phenotypic analysis of antigen-specific T lymphocytes. Science 274, 94–96.[CrossRef]
    [Google Scholar]
  2. Bachmann, M. F., Wolint, P., Schwarz, K., Jäger, P. & Oxenius, A. ( 2005; ). Functional properties and lineage relationship of CD8+ T cell subsets identified by expression of IL-7 receptor α and CD62L. J Immunol 175, 4686–4696.[CrossRef]
    [Google Scholar]
  3. Belz, G. T., Xie, W., Altman, J. D. & Doherty, P. C. ( 2000; ). A previously unrecognized H-2Db-restricted peptide prominent in the primary influenza A virus-specific CD8+ T-cell response is much less apparent following secondary challenge. J Virol 74, 3486–3493.[CrossRef]
    [Google Scholar]
  4. Benton, K. A., Misplon, J. A., Lo, C. Y., Brutkiewicz, R. R., Prasad, S. A. & Epstein, S. L. ( 2001; ). Heterosubtypic immunity to influenza A virus in mice lacking IgA, all Ig, NKT cells, or γδ T cells. J Immunol 166, 7437–7445.[CrossRef]
    [Google Scholar]
  5. Bevan, M. J. ( 2006; ). Cross-priming. Nat Immunol 7, 363–365.[CrossRef]
    [Google Scholar]
  6. Bodewes, R., Kreijtz, J. H. & Rimmelzwaan, G. F. ( 2009a; ). Yearly influenza vaccinations: a double-edged sword? Lancet Infect Dis 9, 784–788.[CrossRef]
    [Google Scholar]
  7. Bodewes, R., Kreijtz, J. H., Baas, C., Geelhoed-Mieras, M. M., de Mutsert, G., van Amerongen, G., van den Brand, J. M., Fouchier, R. A., Osterhaus, A. D. & other authors ( 2009b; ). Vaccination against human influenza A/H3N2 virus prevents the induction of heterosubtypic immunity against lethal infection with avian influenza A/H5N1 virus. PLoS One 4, e5538 [CrossRef]
    [Google Scholar]
  8. Carragher, D. M., Kaminski, D. A., Moquin, A., Hartson, L. & Randall, T. D. ( 2008; ). A novel role for non-neutralizing antibodies against nucleoprotein in facilitating resistance to influenza virus. J Immunol 181, 4168–4176.[CrossRef]
    [Google Scholar]
  9. Cassetti, M. C., Couch, R., Wood, J. & Pervikov, Y. ( 2005; ). Report of meeting on the development of influenza vaccines with broad spectrum and long-lasting immune responses, World Health Organization, Geneva, Switzerland, 26–27 February 2004. Vaccine 23, 1529–1533.[CrossRef]
    [Google Scholar]
  10. Centers for Disease Control and Prevention ( 2009; ). Update: infections with a swine-origin influenza A (H1N1) virus – United States and other countries, April 28, 2009. MMWR Morb Mortal Wkly Rep 58, 431–433.
    [Google Scholar]
  11. Chan, M. ( 2009; ). World Now at the Start of 2009 Influenza Pandemic. Statement to the press by the World Health Organization director-general. Available at http://www.who.int/mediacentre/news/statements/2009/h1n1_pandemic_phase6_20090611/en/index.html.
  12. Chen, W., Pang, K., Masterman, K. A., Kennedy, G., Basta, S., Dimopoulos, N., Hornung, F., Smyth, M., Bennink, J. R. & other authors ( 2004; ). Reversal in the immunodominance hierarchy in secondary CD8+ T cell responses to influenza A virus: roles for cross-presentation and lysis-independent immunodomination. J Immunol 173, 5021–5027.[CrossRef]
    [Google Scholar]
  13. Crowe, S. R., Turner, S. J., Miller, S. C., Roberts, A. D., Rappolo, R. A., Doherty, P. C., Ely, K. H. & Woodland, D. L. ( 2003; ). Differential antigen presentation regulates the changing patterns of CD8+ T cell immunodominance in primary and secondary influenza virus infections. J Exp Med 198, 399–410.[CrossRef]
    [Google Scholar]
  14. Doherty, P. C., Biddison, W. E., Bennink, J. R. & Knowles, B. B. ( 1978; ). Cytotoxic T-cell responses in mice infected with influenza and vaccinia viruses vary in magnitude with H-2 genotype. J Exp Med 148, 534–543.[CrossRef]
    [Google Scholar]
  15. Epstein, S. L. ( 2006; ). Prior H1N1 influenza infection and susceptibility of Cleveland Family Study participants during the H2N2 pandemic of 1957: an experiment of nature. J Infect Dis 193, 49–53.[CrossRef]
    [Google Scholar]
  16. Epstein, S. L., Lo, C. Y., Misplon, J. A., Lawson, C. M., Hendrickson, B. A., Max, E. E. & Subbarao, K. ( 1997; ). Mechanisms of heterosubtypic immunity to lethal influenza A virus infection in fully immunocompetent, T cell-depleted, β2-microglobulin-deficient, and J chain-deficient mice. J Immunol 158, 1222–1230.
    [Google Scholar]
  17. Fiore, A. E., Shay, D. K., Broder, K., Iskander, J. K., Uyeki, T. M., Mootrey, G., Bresee, J. S., Cox, N. S. & other authors ( 2008; ). Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2008. MMWR Recomm Rep 57, 1–60.
    [Google Scholar]
  18. Flynn, K. J., Belz, G. T., Altman, J. D., Ahmed, R., Woodland, D. L. & Doherty, P. C. ( 1998; ). Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 8, 683–691.[CrossRef]
    [Google Scholar]
  19. Frank, A. L., Puck, J., Hughes, B. J. & Cate, T. R. ( 1980; ). Microneutralization test for influenza A and B and parainfluenza 1 and 2 viruses that uses continuous cell lines and fresh serum enhancement. J Clin Microbiol 12, 426–432.
    [Google Scholar]
  20. 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]
    [Google Scholar]
  21. Greenbaum, J. A., Kotturi, M. F., Kim, Y., Oseroff, C., Vaughan, K., Salimi, N., Vita, R., Ponomarenko, J., Scheuermann, R. H. & other authors ( 2009; ). Pre-existing immunity against swine-origin H1N1 influenza viruses in the general human population. Proc Natl Acad Sci U S A 106, 20365–20370.[CrossRef]
    [Google Scholar]
  22. Haanen, J. B., Wolkers, M. C., Kruisbeek, A. M. & Schumacher, T. N. ( 1999; ). Selective expansion of cross-reactive CD8+ memory T cells by viral variants. J Exp Med 190, 1319–1328.[CrossRef]
    [Google Scholar]
  23. Heikkinen, T. & Peltola, V. ( 2009; ). Influenza vaccination of children. Lancet Infect Dis 9, 720–721.[CrossRef]
    [Google Scholar]
  24. Heikkinen, T., Booy, R., Campins, M., Finn, A., Olcen, P., Peltola, H., Rodrigo, C., Schmitt, H. J., Schumacher, F. & other authors ( 2006; ). Should healthy children be vaccinated against influenza? A consensus report of the Summits of Independent European Vaccination Experts. Eur J Pediatr 165, 223–228.[CrossRef]
    [Google Scholar]
  25. 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.
    [Google Scholar]
  26. 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 Immunol 172, 5598–5605.[CrossRef]
    [Google Scholar]
  27. Kaiser, J. ( 2006; ). A one-size-fits-all flu vaccine? Science 312, 380–382.[CrossRef]
    [Google Scholar]
  28. Karber, G. ( 1931; ). Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Naunyn Schmiedebergs Arch Pharmacol 162, 480–483.[CrossRef]
    [Google Scholar]
  29. Kreijtz, J. H., Bodewes, R., van Amerongen, G., Kuiken, T., Fouchier, R. A., Osterhaus, A. D. & Rimmelzwaan, G. F. ( 2007; ). Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine 25, 612–620.[CrossRef]
    [Google Scholar]
  30. 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]
    [Google Scholar]
  31. Kreijtz, J. H., Bodewes, R., van den Brand, J. M., de Mutsert, G., Baas, C., van Amerongen, G., Fouchier, R. A., Osterhaus, A. D. & Rimmelzwaan, G. F. ( 2009; ). Infection of mice with a human influenza A/H3N2 virus induces protective immunity against lethal infection with influenza A/H5N1 virus. Vaccine 27, 4983–4989.[CrossRef]
    [Google Scholar]
  32. Lee, L. Y., Ha, D. L., 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.
    [Google Scholar]
  33. Liang, S., Mozdzanowska, K., Palladino, G. & Gerhard, W. ( 1994; ). Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J Immunol 152, 1653–1661.
    [Google Scholar]
  34. 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]
    [Google Scholar]
  35. Moyron-Quiroz, J. E., Rangel-Moreno, J., Kusser, K., Hartson, L., Sprague, F., Goodrich, S., Woodland, D. L., Lund, F. E. & Randall, T. D. ( 2004; ). Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat Med 10, 927–934.[CrossRef]
    [Google Scholar]
  36. Neirynck, S., Deroo, T., Saelens, X., Vanlandschoot, P., Jou, W. M. & Fiers, W. ( 1999; ). A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med 5, 1157–1163.[CrossRef]
    [Google Scholar]
  37. Nguyen, H. H., Moldoveanu, Z., Novak, M. J., van Ginkel, F. W., Ban, E., Kiyono, H., McGhee, J. R. & Mestecky, J. ( 1999; ). Heterosubtypic immunity to lethal influenza A virus infection is associated with virus-specific CD8+ cytotoxic T lymphocyte responses induced in mucosa-associated tissues. Virology 254, 50–60.[CrossRef]
    [Google Scholar]
  38. Nguyen, H. H., van Ginkel, F. W., Vu, H. L., Novak, M. J., McGhee, J. R. & Mestecky, J. ( 2000; ). Gamma interferon is not required for mucosal cytotoxic T-lymphocyte responses or heterosubtypic immunity to influenza A virus infection in mice. J Virol 74, 5495–5501.[CrossRef]
    [Google Scholar]
  39. Nguyen, H. H., van Ginkel, F. W., Vu, H. L., McGhee, J. R. & Mestecky, J. ( 2001; ). Heterosubtypic immunity to influenza A virus infection requires B cells but not CD8+ cytotoxic T lymphocytes. J Infect Dis 183, 368–376.[CrossRef]
    [Google Scholar]
  40. Nguyen, H. H., Zemlin, M., Ivanov, I. I., Andrasi, J., Zemlin, C., Vu, H. L., Schelonka, R., Schroeder, H. W., Jr & Mestecky, J. ( 2007; ). Heterosubtypic immunity to influenza A virus infection requires a properly diversified antibody repertoire. J Virol 81, 9331–9338.[CrossRef]
    [Google Scholar]
  41. O’Neill, E., Krauss, S. L., Riberdy, J. M., Webster, R. G. & Woodland, D. L. ( 2000; ). Heterologous protection against lethal A/HongKong/156/97 (H5N1) influenza virus infection in C57BL/6 mice. J Gen Virol 81, 2689–2696.
    [Google Scholar]
  42. Palmer, D., Dowle, W., Coleman, M. & Schild, G. ( 1975; ). Haemagglutination inhibition test. In Advances in Laboratory Techniques for Influenza Diagnosis: Procedural Guide, pp. 25–62. Atlanta: US Department of Health, Education and Welfare.
  43. Powell, T. J., Strutt, T., Reome, J., Hollenbaugh, J. A., Roberts, A. D., Woodland, D. L., Swain, S. L. & Dutton, R. W. ( 2007; ). Priming with cold-adapted influenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J Immunol 178, 1030–1038.[CrossRef]
    [Google Scholar]
  44. Rangel-Moreno, J., Carragher, D. M., Misra, R. S., Kusser, K., Hartson, L., Moquin, A., Lund, F. E. & Randall, T. D. ( 2008; ). B cells promote resistance to heterosubtypic strains of influenza via multiple mechanisms. J Immunol 180, 454–463.[CrossRef]
    [Google Scholar]
  45. Schulman, J. L. & Kilbourne, E. D. ( 1965; ). Induction of partial specific heterotypic immunity in mice by a single infection with influenza A virus. J Bacteriol 89, 170–174.
    [Google Scholar]
  46. Slepushkin, V. A., Katz, J. M., Black, R. A., Gamble, W. C., Rota, P. A. & Cox, N. J. ( 1995; ). Protection of mice against influenza A virus challenge by vaccination with baculovirus-expressed M2 protein. Vaccine 13, 1399–1402.[CrossRef]
    [Google Scholar]
  47. Sonoguchi, T., Naito, H., Hara, M., Takeuchi, Y. & Fukumi, H. ( 1985; ). Cross-subtype protection in humans during sequential, overlapping, and/or concurrent epidemics caused by H3N2 and H1N1 influenza viruses. J Infect Dis 151, 81–88.[CrossRef]
    [Google Scholar]
  48. Straight, T. M., Ottolini, M. G., Prince, G. A. & Eichelberger, M. C. ( 2008; ). Antibody contributes to heterosubtypic protection against influenza A-induced tachypnea in cotton rats. Virol J 5, 44 [CrossRef]
    [Google Scholar]
  49. Taylor, P. M. & Askonas, B. A. ( 1986; ). Influenza nucleoprotein-specific cytotoxic T-cell clones are protective in vivo. Immunology 58, 417–420.
    [Google Scholar]
  50. Tumpey, T. M., Renshaw, M., Clements, J. D. & Katz, J. M. ( 2001; ). Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection. J Virol 75, 5141–5150.[CrossRef]
    [Google Scholar]
  51. Webster, R. G. & Askonas, B. A. ( 1980; ). Cross-protection and cross-reactive cytotoxic T cells induced by influenza virus vaccines in mice. Eur J Immunol 10, 396–401.[CrossRef]
    [Google Scholar]
  52. Wells, M. A., Ennis, F. A. & Albrecht, P. ( 1981; ). Recovery from a viral respiratory infection. II. Passive transfer of immune spleen cells to mice with influenza pneumonia. J Immunol 126, 1042–1046.
    [Google Scholar]
  53. World Health Organization ( 2009; ). Influenza (Seasonal), Fact Sheet No. 211. Available at http://www.who.int/mediacentre/factsheets/fs211/en/index.html.
  54. World Health Organization ( 2010; ). Cumulative Number of Confirmed Human Cases of Avian Influenza A/(H5N1) Reported to WHO. Available at http://www.who.int/csr/disease/avian_influenza/country/cases_table_2010_03_16/en/index.html. Site accessed March 16, 2010.
  55. 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]
    [Google Scholar]
  56. Yetter, R. A., Barber, W. H. & Small, P. A., Jr ( 1980; ). Heterotypic immunity to influenza in ferrets. Infect Immun 29, 650–653.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.020784-0
Loading
/content/journal/jgv/10.1099/vir.0.020784-0
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error