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BioMed Research International
Volume 2013 (2013), Article ID 686549, 12 pages
http://dx.doi.org/10.1155/2013/686549
Research Article

Virus-Like Particles Containing the Tetrameric Ectodomain of Influenza Matrix Protein 2 and Flagellin Induce Heterosubtypic Protection in Mice

Department of Microbiology and Immunology and Emory Vaccine Center, Emory University School of Medicine, Atlanta, GA, USA

Received 15 April 2013; Accepted 28 June 2013

Academic Editor: Phillip E. Klebba

Copyright © 2013 Li Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. E. de Wit and R. A. M. Fouchier, “Emerging influenza,” Journal of Clinical Virology, vol. 41, no. 1, pp. 1–6, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. G. J. D. Smith, D. Vijaykrishna, J. Bahl et al., “Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza a epidemic,” Nature, vol. 459, no. 7250, pp. 1122–1125, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. J. P. Tite, C. Hughes-Jenkins, D. O'Callaghan et al., “Anti-viral immunity induced by recombinant nucleoprotein of influenza A virus. II. Protection from influenza infection and mechanism of protection,” Immunology, vol. 71, no. 2, pp. 202–207, 1990. View at Scopus
  4. S. L. Epstein, W.-P. Kong, J. A. Misplon et al., “Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein,” Vaccine, vol. 23, no. 46-47, pp. 5404–5410, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Schotsaert, M. De Filette, W. Fiers, and X. Saelens, “Universal M2 ectodomain-based influenza A vaccines: preclinical and clinical developments,” Expert Review of Vaccines, vol. 8, no. 4, pp. 499–508, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. M. De Filette, W. Fiers, W. Martens et al., “Improved design and intranasal delivery of an M2e-based human influenza A vaccine,” Vaccine, vol. 24, no. 44-46, pp. 6597–6601, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. A. I. Wolf, K. Mozdzanowska, K. L. Williams et al., “Vaccination with M2e-based multiple antigenic peptides: characterization of the B cell response and protection efficacy in inbred and outbred mice,” PLoS ONE, vol. 6, no. 12, Article ID e28445, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. J. Feng, M. Zhang, K. Mozdzanowska et al., “Influenza A virus infection engenders a poor antibody response against the ectodomain of matrix protein 2,” Virology Journal, vol. 3, article 102, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. F. Steinhagen, T. Kinjo, C. Bode, and D. M. Klinman, “TLR-based immune adjuvants,” Vaccine, vol. 29, no. 17, pp. 3341–3355, 2011. View at Publisher · View at Google Scholar · View at Scopus
  10. B. Z. Wang, H. S. Gill, S. M. Kang, et al., “Enhanced influenza virus-like particle vaccines containing the extracellular domain of matrix protein 2 and a Toll-like receptor ligand,” Clinical and Vaccine Immunology, vol. 19, pp. 1119–1125, 2012.
  11. B.-Z. Wang, R. Xu, F.-S. Quan, S.-M. Kang, L. Wang, and R. W. Compans, “Intranasal immunization with influenza VLPs incorporating membrane-anchored flagellin induces strong heterosubtypic protection,” PLoS ONE, vol. 5, no. 11, Article ID e13972, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. B.-Z. Wang, F.-S. Quan, S.-M. Kang, J. Bozja, I. Skountzou, and R. W. Compans, “Incorporation of membrane-anchored flagellin into influenza virus-like particles enhances the breadth of immune responses,” Journal of Virology, vol. 82, no. 23, pp. 11813–11823, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Yoshioka, S.-I. Aizawa, and S. Yamaguchi, “Flagellar filament structure and cell motility of Salmonella typhimurium mutants lacking part of the outer domain of flagellin,” Journal of Bacteriology, vol. 177, no. 4, pp. 1090–1093, 1995. View at Scopus
  14. E. Andersen-Nissen, K. D. Smith, K. L. Strobe et al., “Evasion of Toll-like receptor 5 by flagellated bacteria,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 26, pp. 9247–9252, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. M. F. Smith Jr., A. Mitchell, G. Li et al., “Toll-like receptor (TLR) 2 and TLR5, but not TLR4, are required for Helicobacter pylori-induced NF-κB activation and chemokine expression by epithelial cells,” Journal of Biological Chemistry, vol. 278, no. 35, pp. 32552–32560, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Nempont, D. Cayet, M. Rumbo, C. Bompard, V. Villeret, and J.-C. Sirard, “Deletion of Flagellin's hypervariable region abrogates antibody-mediated neutralization and systemic activation of TLR5-dependent immunity,” Journal of Immunology, vol. 181, no. 3, pp. 2036–2043, 2008. View at Scopus
  17. M. De Filette, W. Martens, K. Roose et al., “An influenza A vaccine based on tetrameric ectodomain of matrix protein 2,” Journal of Biological Chemistry, vol. 283, no. 17, pp. 11382–11387, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. E. V. Vassilieva, B.-Z. Wang, A. N. Vzorov et al., “Enhanced mucosal immune responses to HIV virus-like particles containing a membrane-anchored adjuvant,” MBio, vol. 2, no. 1, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. J.-M. Song, B.-Z. Wang, K.-M. Park et al., “Influenza virus-like particles containing M2 induce broadly cross protective immunity,” PLoS ONE, vol. 6, no. 1, Article ID e14538, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. R. Ito, Y. A. Ozaki, T. Yoshikawa et al., “Roles of anti-hemagglutinin IgA and IgG antibodies in different sites of the respiratory tract of vaccinated mice in preventing lethal influenza pneumonia,” Vaccine, vol. 21, no. 19-20, pp. 2362–2371, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. J. H. C. M. Kreijtz, R. Bodewes, G. van Amerongen et al., “Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice,” Vaccine, vol. 25, no. 4, pp. 612–620, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. S. H. S. Sang Heui Seo and R. G. Webster, “Cross-reactive, cell-mediated immunity and protection of chickens from lethal H5N1 influenza virus infection in Hong Kong poultry markets,” Journal of Virology, vol. 75, no. 6, pp. 2516–2525, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. X. Lu, T. M. Tumpey, T. Morken, S. R. Zaki, N. J. Cox, and J. M. Katz, “A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans,” Journal of Virology, vol. 73, no. 7, pp. 5903–5911, 1999. View at Scopus
  24. A. N. Honko, N. Sriranganathan, C. J. Lees, and S. B. Mizel, “Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis,” Infection and Immunity, vol. 74, no. 2, pp. 1113–1120, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Vijay-Kumar, F. A. Carvalho, J. D. Aitken, N. H. Fifadara, and A. T. Gewirtz, “TLR5 or NLRC4 is necessary and sufficient for promotion of humoral immunity by flagellin,” European Journal of Immunology, vol. 40, no. 12, pp. 3528–3534, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. A. F. Cunningham, M. Khan, J. Ball et al., “Responses to the soluble flagellar protein FliC are Th2, while those to FliC on Salmonella are Th1,” European Journal of Immunology, vol. 34, no. 11, pp. 2986–2995, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Gianfrani, C. Oseroff, J. Sidney, R. W. Chesnut, and A. Sette, “Human memory CTL response specific for influenza a virus is broad and multispecific,” Human Immunology, vol. 61, no. 5, pp. 438–452, 2000. View at Publisher · View at Google Scholar · View at Scopus
  28. A. Jegerlehner, N. Schmitz, T. Storni, and M. F. Bachmann, “Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity,” Journal of Immunology, vol. 172, no. 9, pp. 5598–5605, 2004. View at Scopus
  29. J. Mestecky and J. R. McGhee, “Immunoglobulin A (IgA): molecular and cellular interactions involved in IgA biosynthesis and immune response,” Advances in Immunology, vol. 40, pp. 153–245, 1987. View at Scopus
  30. G.-G. Zhang, D.-X. Li, H.-H. Zhang, Y.-M. Zeng, and L. Chen, “Enhancement of mucosal immune response against the M2eHBc+ antigen in mice with the fusion expression products of LTB and M2eHBc+ through mucosal immunization route,” Veterinary Research Communications, vol. 33, no. 7, pp. 735–747, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Mozdzanowska, D. Zharikova, M. Cudic, L. Otvos, and W. Gerhard, “Roles of adjuvant and route of vaccination in antibody response and protection engendered by a synthetic matrix protein 2-based influenza A virus vaccine in the mouse,” Virology Journal, vol. 4, article 118, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. M. De Filette, A. Ramne, A. Birkett et al., “The universal influenza vaccine M2e-HBc administered intranasally in combination with the adjuvant CTA1-DD provides complete protection,” Vaccine, vol. 24, no. 5, pp. 544–551, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. Y. Asahi, T. Yoshikawa, I. Watanabe et al., “Protection against influenza virus infection in polymeric Ig receptor knockout mice immunized intranasally with adjuvant-combined vaccines,” Journal of Immunology, vol. 168, no. 6, pp. 2930–2938, 2002. View at Scopus
  34. K. B. Renegar, C. D. Johnson, R. C. Dewitt et al., “Impairment of mucosal immunity by total parenteral nutrition: requirement for IgA in marine nasotracheal anti-influenza immunity,” Journal of Immunology, vol. 166, no. 2, pp. 819–825, 2001. View at Scopus
  35. C. Patry, Y. Sibille, A. Lehuen, and R. C. Monteiro, “Identification of Fcα receptor (CD89) isoforms generated by alternative splicing that are differentially expressed between blood monocytes and alveolar macrophages,” Journal of Immunology, vol. 156, no. 11, pp. 4442–4448, 1996. View at Scopus
  36. I. Abusugra and B. Morein, “Iscom is an efficient mucosal delivery system for Mycoplasma mycoides subsp. mycoides (MmmSC) antigens inducing high mucosal and systemic antibody responses,” FEMS Immunology and Medical Microbiology, vol. 23, no. 1, pp. 5–12, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. E. L. Parr and M. B. Parr, “Immunoglobulin G, plasma cells, and lymphocytes in the murine vagina after vaginal or parenteral immunization with attenuated herpes simplex virus type 2,” Journal of Virology, vol. 72, no. 6, pp. 5137–5145, 1998. View at Scopus