1887

Journal of General Virology header logo

Volume 95, Issue 12

Infection of influenza virus neuraminidase-vaccinated mice with homologous influenza virus leads to strong protection against heterologous influenza viruses Free

Abstract

Vaccination is the best measure to prevent influenza pandemics. Here, we studied the protective effect against heterologous influenza viruses, including A/reassortant/NYMC X-179A (pH1N1), A/Chicken/Henan/12/2004 (H5N1), A/Chicken/Jiangsu/7/2002 (H9N2) and A/Guizhou/54/89×A/PR/8/34 (A/Guizhou-X) (H3N2), in mice first vaccinated with a DNA vaccine of haemagglutinin (HA) or neuraminidase (NA) of A/PR/8/34 (PR8) and then infected with the homologous virus. We showed that PR8 HA or NA vaccination both protected mice against a lethal dose of the homologous virus; PR8 HA or NA DNA vaccination and then PR8 infection in mice offered poor or excellent protection, respectively, against a second, heterologous influenza virus challenge. In addition, before the second heterologous influenza infection, the highest antibody level against nucleoprotein (NP) and matrix (M1 and M2) proteins was found in the PR8 NA-vaccinated and PR8-infected group. The level of induced cellular immunity against NP and M1 showed a trend consistent with that seen in antibody levels. However, PR8 HA+NA vaccination and then PR8 infection resulted in limited protection against heterologous influenza virus challenge. Results of the present study demonstrated that infection of the homologous influenza virus in mice already immunized with a NA vaccine could provide excellent protection against subsequent infection of a heterologous influenza virus. These findings suggested that NA, a major antigen of influenza virus, could be an important candidate antigen for universal influenza vaccines.

  • Received:
  • Accepted:
  • Published Online:
© 2014 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.067736-0
2014-12-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/12/2627.html?itemId=/content/journal/jgv/10.1099/vir.0.067736-0&mimeType=html&fmt=ahah

References

  1. Carrat F., Flahault A. 2007; Influenza vaccine: the challenge of antigenic drift. Vaccine 25:6852–6862 [View Article][PubMed]
     [Google Scholar]
  2. Carter D. M., Bloom C. E., Nascimento E. J., Marques E. T., Craigo J. K., Cherry J. L., Lipman D. J., Ross T. M. 2013; Sequential seasonal H1N1 influenza virus infections protect ferrets against novel 2009 H1N1 influenza virus. J Virol 87:1400–1410 [View Article][PubMed]
     [Google Scholar]
  3. Chang H., Huang C., Wu J., Fang F., Zhang W., Wang F., Chen Z. 2010; A single dose of DNA vaccine based on conserved H5N1 subtype proteins provides protection against lethal H5N1 challenge in mice pre-exposed to H1N1 influenza virus. Virol J 7:197 [View Article][PubMed]
     [Google Scholar]
  4. Chen Z., Sahashi Y., Matsuo K., Asanuma H., Takahashi H., Iwasaki T., Suzuki Y., Aizawa C., Kurata T., Tamura S. 1998; Comparison of the ability of viral protein-expressing plasmid DNAs to protect against influenza. Vaccine 16:1544–1549 [View Article][PubMed]
     [Google Scholar]
  5. Chen Z., Kadowaki S., Hagiwara Y., Yoshikawa T., Matsuo K., Kurata T., Tamura S. 2000; Cross-protection against a lethal influenza virus infection by DNA vaccine to neuraminidase. Vaccine 18:3214–3222 [View Article][PubMed]
     [Google Scholar]
  6. Chen J., Fang F., Li X., Chang H., Chen Z. 2005; Protection against influenza virus infection in BALB/c mice immunized with a single dose of neuraminidase-expressing DNAs by electroporation. Vaccine 23:4322–4328 [View Article][PubMed]
     [Google Scholar]
  7. Chen Q., Kuang H., Wang H., Fang F., Yang Z., Zhang Z., Zhang X., Chen Z. 2009; Comparing the ability of a series of viral protein-expressing plasmid DNAs to protect against H5N1 influenza virus. Virus Genes 38:30–38 [View Article][PubMed]
     [Google Scholar]
  8. Colman P. M., Ward C. W. 1985; Structure and diversity of influenza virus neuraminidase. Curr Top Microbiol Immunol 114:177–255[PubMed]
     [Google Scholar]
  9. Couceiro J. N., Paulson J. C., Baum L. G. 1993; Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res 29:155–165 [View Article][PubMed]
     [Google Scholar]
  10. Effros R. B., Doherty P. C., Gerhard W., Bennink J. 1977; Generation of both cross-reactive and virus-specific T-cell populations after immunization with serologically distinct influenza A viruses. J Exp Med 145:557–568 [View Article][PubMed]
     [Google Scholar]
  11. 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 [View Article][PubMed]
     [Google Scholar]
  12. Epstein S. L., Kong W. P., Misplon J. A., Lo C. Y., Tumpey T. M., Xu L., Nabel G. J. 2005; Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine 23:5404–5410 [View Article][PubMed]
     [Google Scholar]
  13. Fan J., Liang X., Horton M. S., Perry H. C., Citron M. P., Heidecker G. J., Fu T. M., Joyce J., Przysiecki C. T.other authors 2004; Preclinical study of influenza virus A M2 peptide conjugate vaccines in mice, ferrets, and rhesus monkeys. Vaccine 22:2993–3003 [View Article][PubMed]
     [Google Scholar]
  14. Fang F., Cai X. Q., Chang H. Y., Wang H. D., Yang Z. D., Chen Z. 2008; Protection abilities of influenza B virus DNA vaccines expressing hemagglutinin, neuraminidase, or both in mice. Acta Virol 52:107–112[PubMed]
     [Google Scholar]
  15. Fereidouni S. R., Starick E., Beer M., Wilking H., Kalthoff D., Grund C., Häuslaigner R., Breithaupt A., Lange E., Harder T. C. 2009; Highly pathogenic avian influenza virus infection of mallards with homo- and heterosubtypic immunity induced by low pathogenic avian influenza viruses. PLoS ONE 4:e6706 [View Article][PubMed]
     [Google Scholar]
  16. Furuya Y., Chan J., Regner M., Lobigs M., Koskinen A., Kok T., Manavis J., Li P., Müllbacher A., Alsharifi M. 2010; Cytotoxic T cells are the predominant players providing cross-protective immunity induced by gamma-irradiated influenza A viruses. J Virol 84:4212–4221 [View Article][PubMed]
     [Google Scholar]
  17. Gambaryan A. S., Piskarev V. E., Yamskov I. A., Sakharov A. M., Tuzikov A. B., Bovin N. V., Nifant’ev N. E., Matrosovich M. N. 1995; Human influenza virus recognition of sialyloligosaccharides. FEBS Lett 366:57–60 [View Article][PubMed]
     [Google Scholar]
  18. Gao R., Cao B., Hu Y., Feng Z., Wang D., Hu W., Chen J., Jie Z., Qiu H.other authors 2013; Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med 368:1888–1897 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  20. Guo L., Zheng M., Ding Y., Li D., Yang Z., Wang H., Chen Q., Sui Z., Fang F., Chen Z. 2010; Protection against multiple influenza A virus subtypes by intranasal administration of recombinant nucleoprotein. Arch Virol 155:1765–1775 [View Article][PubMed]
     [Google Scholar]
  21. Guo H., Santiago F., Lambert K., Takimoto T., Topham D. J. 2011; T cell-mediated protection against lethal 2009 pandemic H1N1 influenza virus infection in a mouse model. J Virol 85:448–455 [View Article][PubMed]
     [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 [View Article][PubMed]
     [Google Scholar]
  23. Harley V. R., Ward C. W., Hudson P. J. 1989; Molecular cloning and analysis of the N5 neuraminidase subtype from an avian influenza virus. Virology 169:239–243 [View Article][PubMed]
     [Google Scholar]
  24. Heinen P. P., de Boer-Luijtze E. A., Bianchi A. T. 2001; Respiratory and systemic humoral and cellular immune responses of pigs to a heterosubtypic influenza A virus infection. J Gen Virol 82:2697–2707[PubMed]
     [Google Scholar]
  25. Johansson B. E., Bucher D. J., Kilbourne E. D. 1989; Purified influenza virus hemagglutinin and neuraminidase are equivalent in stimulation of antibody response but induce contrasting types of immunity to infection. J Virol 63:1239–1246[PubMed]
     [Google Scholar]
  26. 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 [View Article][PubMed]
     [Google Scholar]
  27. LaMere M. W., Lam H. T., Moquin A., Haynes L., Lund F. E., Randall T. D., Kaminski D. A. 2011; Contributions of antinucleoprotein IgG to heterosubtypic immunity against influenza virus. J Immunol 186:4331–4339 [View Article][PubMed]
     [Google Scholar]
  28. 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[PubMed]
     [Google Scholar]
  29. Martínez C., del Rio L., Portela A., Domingo E., Ortín J. 1983; Evolution of the influenza virus neuraminidase gene during drift of the N2 subtype. Virology 130:539–545 [View Article][PubMed]
     [Google Scholar]
  30. 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 [View Article][PubMed]
     [Google Scholar]
  31. 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 [View Article][PubMed]
     [Google Scholar]
  32. Neumann G., Noda T., Kawaoka Y. 2009; Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459:931–939 [View Article][PubMed]
     [Google Scholar]
  33. Ozawa T., Jin A., Tajiri K., Takemoto M., Okuda T., Shiraki K., Kishi H., Muraguchi A. 2011; Characterization of a fully human monoclonal antibody against extracellular domain of matrix protein 2 of influenza A virus. Antiviral Res 91:283–287 [View Article][PubMed]
     [Google Scholar]
  34. Qiu M., Fang F., Chen Y., Wang H., Chen Q., Chang H., Wang F., Wang H., Zhang R., Chen Z. 2006; Protection against avian influenza H9N2 virus challenge by immunization with hemagglutinin- or neuraminidase-expressing DNA in BALB/c mice. Biochem Biophys Res Commun 343:1124–1131 [View Article][PubMed]
     [Google Scholar]
  35. Saha S., Yoshida S., Ohba K., Matsui K., Matsuda T., Takeshita F., Umeda K., Tamura Y., Okuda K.other authors 2006; A fused gene of nucleoprotein (NP) and herpes simplex virus genes (VP22) induces highly protective immunity against different subtypes of influenza virus. Virology 354:48–57 [View Article][PubMed]
     [Google Scholar]
  36. Sambhara S., Poland G. A. 2010; H5N1 avian influenza: preventive and therapeutic strategies against a pandemic. Annu Rev Med 61:187–198 [View Article][PubMed]
     [Google Scholar]
  37. Sandbulte M. R., Jimenez G. S., Boon A. C., Smith L. R., Treanor J. J., Webby R. J. 2007; Cross-reactive neuraminidase antibodies afford partial protection against H5N1 in mice and are present in unexposed humans. PLoS Med 4:e59 [View Article][PubMed]
     [Google Scholar]
  38. 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 [View Article][PubMed]
     [Google Scholar]
  39. Sui Z., Chen Q., Fang F., Zheng M., Chen Z. 2010a; Cross-protection against influenza virus infection by intranasal administration of M1-based vaccine with chitosan as an adjuvant. Vaccine 28:7690–7698 [View Article][PubMed]
     [Google Scholar]
  40. Sui Z., Chen Q., Wu R., Zhang H., Zheng M., Wang H., Chen Z. 2010b; Cross-protection against influenza virus infection by intranasal administration of M2-based vaccine with chitosan as an adjuvant. Arch Virol 155:535–544 [View Article][PubMed]
     [Google Scholar]
  41. Watabe S., Xin K. Q., Ihata A., Liu L. J., Honsho A., Aoki I., Hamajima K., Wahren B., Okuda K. 2001; Protection against influenza virus challenge by topical application of influenza DNA vaccine. Vaccine 19:4434–4444 [View Article][PubMed]
     [Google Scholar]
  42. WHO (2002). WHO Manual on Animal Influenza Diagnosis and Surveillance http://www.who.int/csr/resources/publications/influenza/en/whocdscsrncs20025rev.pdf
  43. WHO (2014). Antigenic and genetic characteristics of zoonotic influenza viruses and candidate vaccine viruses developed for potential use in human vaccines http://www.who.int/influenza/vaccines/virus/201402_h5h7h9h10_vaccinevirusupdate.pdf?ua=1
  44. Zhang F., Fang F., Chang H., Peng B., Wu J., Chen J., Wang H., Chen Z. 2013; Comparison of protection against H5N1 influenza virus in mouse offspring provided by maternal vaccination with HA DNA and inactivated vaccine. Arch Virol 158:1253–1265 [View Article][PubMed]
     [Google Scholar]
  45. Zheng L., Wang F., Yang Z., Chen J., Chang H., Chen Z. 2009; A single immunization with HA DNA vaccine by electroporation induces early protection against H5N1 avian influenza virus challenge in mice. BMC Infect Dis 9:17 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.067736-0
Loading
Infection of influenza virus neuraminidase-vaccinated mice with homologous influenza virus leads to strong protection against heterologous influenza viruses
J. Gen. Virol. 95, 2627 (2014); https://doi.org/10.1099/vir.0.067736-0
/content/journal/jgv/10.1099/vir.0.067736-0
/content/journal/jgv/10.1099/vir.0.067736-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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