In contrast to conventional inactivated influenza vaccines, 4xM2e.HSP70c fusion protein fully protected mice against lethal dose of H1, H3 and H9 influenza A isolates circulating in Iran

Virology

Volumn 430, Issue 1, 2012, Pages 63-72

  Ebrahimi, Seyyed Mahmoud ^a   Dabaghian, Mehran ^b   Tebianian, Majid ^c   Zabeh Jazi, Mohammad Hossein ^b  

^a BAQIYATALLAH UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b UNIVERSITY OF TEHRAN   (Iran)

^c RAZI VACCINE AND SERUM RESEARCH INSTITUTE   (Iran)

Author keywords

Fusion protein; HSP70c; Influenza A; M2e; Universal vaccine

Indexed keywords

INFLUENZA VACCINE; MATRIX PROTEIN 2 HEAT SHOCK PROTEIN 70 FUSION PROTEIN; UNCLASSIFIED DRUG; VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HISTOPATHOLOGY; IMMUNOGENICITY; INFECTION PREVENTION; INFLUENZA A; INFLUENZA A (H1N1); INFLUENZA A (H3N2); INFLUENZA VACCINATION; INFLUENZA VIRUS A H9N2; IRAN; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; VIRAL CLEARANCE; VIRUS ISOLATION; VIRUS LOAD; WEIGHT REDUCTION;

ANIMALS; BACTERIAL PROTEINS; BODY WEIGHT; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION; HSP70 HEAT-SHOCK PROTEINS; HUMANS; INFLUENZA A VIRUS; INFLUENZA VACCINES; INFLUENZA, HUMAN; INJECTIONS, INTRAMUSCULAR; IRAN; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE INFECTIONS; RECOMBINANT FUSION PROTEINS; REPETITIVE SEQUENCES, AMINO ACID; SURVIVAL ANALYSIS; VACCINATION; VACCINES, SYNTHETIC; VIRAL MATRIX PROTEINS;

ESCHERICHIA COLI; INFLUENZA A VIRUS; MUS; MYCOBACTERIUM TUBERCULOSIS; ORTHOMYXOVIRIDAE;

EID: 84861823634     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.04.015     Document Type: Article

References (57)

1. Aida Y., Pabst M.J. Removal of endotoxin from protein solutions by phase separation using Triton X-114. J. Immunol. Methods 1990, 132:191-195.
2. Arnold D., Raath S., Rammensee H.G., Schild H. Cross-priming of minor histocompatibility antigen-specific cytotoxic T cells upon immunization with the heat shock protein gp96. J. Exp. Med. 1995, 182:885.
3. Bakkouri K.E., Descamps F., De Filette M., Smet A., Festjens E.L., et al. Universal vaccine based on ectodomain of matrix Protein 2 of Influenza A: Fc receptors and alveolar macrophages mediate protection. J. Immunol. 2011, 186:1022-1031.
4. Baumgarth N., Brown L., Jackson D., Kelso A. Novel features of the respiratory tract T-cell response to influenza virus infection: lung T cells increase expression of gamma interferon mRNA in vivo and maintain high levels of mRNA expression for interleukin-5 (IL-5) and IL-10. J. Virol. 1994, 68:7575-7581.
5. Blachere N.E., Li Z., Chandawarkar R.Y., Suto R., Jaikaria N.S., Basu S., Udono H., Srivastava P.K. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. J. Exp. Med. 1997, 186:1315.
6. Brett I.C., Johansson B.E. Immunization against influenza A virus: comparison of conventional inactivated, live-attenuated and recombinant baculovirus produced purified hemagglutinin and neuraminidase vaccines in a murine model system. Virology 2005, 339:273-280.
7. Castellino F., Boucher P.E., Eichelberg K., Mayhew M., Rothman J.E., Houghton A.N., Germain R.N. Receptor-mediated uptake of antigen/ heat shock protein complexes results in major histocompatibility complex class I antigen presentation via two distinct processing pathways. J. Exp. Med. 2000, 191:1957.
8. Castellino F., Boucher P.E., Eichelberg K., Mayhew M., Rothman J.E., Houghton A.N., Germain R.N. Receptor-mediated uptake of antigen/heat shock protein complexes results in major histocompatibility complex class I antigen presentation via two distinct processing pathways. J. Exp. Med. 2000, 191:1957-1964.
9. Chen S.H., Wang T.L., Hung C.F. Enhancement of DNA vaccine potency by linkage of antigen gene to an HSP70 gene. Cancer Res. 2000, 15:1035-1042.
10. Cho B.K., Palliser D., Guillen E., Wisniewski J., Young R.A., Chen J., Eisen H.N. A proposed mechanism for the induction of cytotoxic T lymphocyte production by heat shock fusion proteins. Immunity 2000, 12:263-272.
11. Chunxia S., Duan X., Wang X., Wang C., Cao R., Zhou B., Chen P. Heterologous expression of FMDV immunodominant epitopes and HSP70 in P. pastoris and the subsequent immune response in mice. Vet. Microbiol. 2006, 124:256-263.
12. Ciampor F., Thompson C.A., Grambas S., Hay A.J. Regulation of pH by the M2 protein of influenza A viruses. Virus Res. 1992, 22:247-258.
13. Cox R.J., Brokstad K.A., Ograz P. Influenza virus: immunity and vaccination strategies. Comparison of the immune response to inactivated and live, attenuated influenza vaccines. Scand. J. Immunol. 2004, 59:1-15.
14. De Filette M., Martens W., Smet A., Schotsaert M., Birkett A., Londoño-Arcila P., Fiers W., Saelens X. Universal influenza A M2e-HBc vaccine protects against disease even in the presence of pre-existing anti-HBc antibodies. Vaccine 2008, 26:6503-6507.
15. Doherty P.C., Topham D.J., Tripp R.A., Cardin R.O., Brooks J.W., Stevenson P.G. Effector CD4+ and CD8+ T-cell mechanisms in the control of respiratory virus infections. Immunol. Rev. 1997, 159:105-117.
16. 0359-610 in prokaryotic system as a fusion protein. Mol. Biol. Rep. 2010, 37:2877-2883.
17. Ebrahimi S.M., Tebianian M. Influenza A viruses: why focusing on M2e-based universal vaccines. Virus Genes 2011, 42:1-8.
18. Ebrahimi S.M., Ziapour S., Tebianian M., Dabaghian M., Mohammadi M. Study of infection with an Iranian field-isolated H9N2 avian influenza virus in vaccinated and unvaccinated Japanese quail. Avian Dis. 2011, 55:195-200.
19. Fabrice C., Vergu E., Ferguson N.M., Lemaitre M., Cauchemez S., Leach S., Valleron A.J. Time lines of infection and disease in human influenza: A review of volunteer challenge studies. Am. J. Epidemiol. 2008, 167:775-785.
20. Fan J., Liang X., Horton M.S., Perry H.C., Citron M.P., et al. Preclinical study of influenza virus A M2 peptide conjugates vaccines in mice, ferrets, and rhesus monkeys. Vaccine 2004, 22:2993-3003.
21. Fan W., Huang J.H., Yuan X.Y., Huang W.H., Chen Y.H. Characterization of immunity induced by M2e of influenza virus. Vaccine 2007, 25:8868-8873.
22. Fei-fei G., Qiu Y., Gao X., Yang Y., Chen P. Fusion expression of major antigenic segment of JEV E protein-hsp70 and the identification of domain acting as adjuvant in hsp70. Vet. Immunol. Immunopathol. 2006, 113:288-296.
23. Fiers W., De Filette M., Birkett A., Neirynck S., Min Jou W. A "universal" human influenza A vaccine. Virus Res. 2004, 103:173-176.
24. Fischer W.B., Sansom M.S. Viral ion channels: structure and function. Biochim. Biophys. Acta 2002, 1561:27-45.
25. Frace A.M., Klimov A.I., Rowe T., Black R.A., Katz J.M. Modified M2 proteins produce heterotypic immunity against influenza A virus. Vaccine 1999, 17:2237-2244.
26. Garten R.J., Davis C.T., Russell C.A., Shu B., Lindstrom S., Balish A., Sessions W.M., Xu X., Skepner E., Deyde V., et al. Antigenic and genetic characteristics of swine origin 2009 A (H1N1) influenza viruses circulating in humans. Science 2009, 325:197-201.
27. Haga T., Horimoto T. Animal models to study influenza virus pathogenesis and control. Antimicrob. Agents J. 2010, 2:15-21.
28. Huleatt J.W., Valerian N., Priyanka D., Yan H., Duane H., Andrea J., et al. Potent immunogenicity and efficacy of a universal influenza vaccine candidate comprising a recombinant fusion protein linking influenza M2e to the TLR5 ligand flagellin. Vaccine 2008, 26:201-214.
29. Jegerlehner A., Schmitz N., Storni T., Bachmann.M.F. Influenza A vaccine based on the xtracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J. Immunol. 2004, 172:5598-5605.
30. Jegerlehner A., Tissot A., Lechner F., Sebbel P., Erdmann I., Kundig T., et al. A molecular assembly system that renders antigens of choice highly repetitive for induction of protective B cell responses. Vaccine 2002, 20:3104-3112.
31. Johansson B., Bucher D., Kilbourne E. Purified influenza virus hemagglutinin and neuraminidase are equivalent in stimulation of antibody response but induce contrasting types of immunity to infection. J. Virol. 1989, 63:1239.
32. Lamb R.A., Zebedee S.L., Richardson C.D. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell 1985, 40:627-633.
33. Li X., Yang X., Li L., Liu H., Liu J. A truncated C-terminal fragment of Mycobacterium tuberculosis HSP70 gene enhanced potency of HBV DNA vaccine. Vaccine 2006, 24:3321-3331.
34. Lincoln L.H.L., Benjamin J.C., Vicky J.F., Chan K.H., Eric H.Y.L., et al. Viral shedding and clinical illness in naturally acquired influenza virus infections. J. Infect. Dis. 2010, 201:1509-1516.
35. Liu W., Chen Y.H. High epitope density in a single protein molecule significantly enhances antigenicity as well as immunogenicity: a novel strategy for modern vaccine development and a preliminary investigation about B cell discrimination of monomeric proteins. Eur. J. Immunol. 2005, 35:505-514.
36. Liu W., Li H., Chen Y.H. N-terminus of M2 protein could induce antibodies with inhibitory activity against influenza virus replication. FEMS Immunol. Med. Microbiol. 2003, 35:141-146.
37. Liu W., Zou P., Ding J., Lu Y., Chen Y.H. Sequence comparison between the extracellular domain of M2 protein human and avian influenza A virus provides new information for bivalent influenza vaccine design. Microbes Infect. 2005, 7:171-177.
38. Lu X., Tumpey T.M., Morken T., Zaki S.R., Cox N.J., Katz J.M. A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans. J. Virol. 1999, 73:5903-5911.
39. Malik Peiris J.S., De Jong M.D., Guan Y. Avian influenza virus (H5N1): a threat to human health. Clin. Microbiol. Rev. 2007, 20:243-267.
40. Mozdzanowska K., Feng J., Eid M., Kragol G., Cudic M., Otvos J.L, Gerhard W. Induction of influenza type A virus-specific resistance by immunization of mice with a synthetic multiple antigenic peptide vaccine that contains ectodomains of matrix protein 2. Vaccine 2003, 21:2616-2626.
41. National Research Council Nutrients Requirements of the Mouse 1995, National Academy Press, Washington, DC, pp. 11-15. 4th rev. ed.
42. Neirynck S., Deroo T., Saelens X., Vanlandschoot P., Min Jou W., Fiers W. A universal influenza A vaccine based on the extracelluar domain of the M2e protein. Nat. Med. 1999, 5:1157-1163.
43. Okuda K., Ihata A., Watabe S., Okada E., Yamakawa T., Hamajima K., Yang J., Ishii N., et al. Protective immunity against influenza A virus induced by immunization with DNA plasmid containing influenza M gene. Vaccine 2001, 19:3681-3691.
44. Qazi K.R., Wikman M., Vasconcelos N.M., Berzins K., Ståhl S., Ferna'ndez C. Enhancement of DNA vaccine potency by linkage of Plasmodiumfalciparum malarial antigen gene fused with a fragment of HSP70 gene. Vaccine 2005, 23:1114-1125.
45. Reed, L.J., Muench, H.A., 1938. Simple method for estimating fifty per cent endpoints. Am. J. Hyg.. 27, 493-497. 1938.
46. Rimmelzwaan G.F., Baars.M., Claas E.C.J., Osterhaus A.D.M.E. Comparison of RNA hybridization, hemagglutination assay, titration of infectious virus and immunofluorescence as methods for monitoring influenza virus replication in vitro. J. Virol. Methods 1998, 74:57.
47. Sealy R., Surman S., Hurwitz J.L., Coleclough C. Antibody response to influenza infection of mice: different patterns for glycoprotein and nucleocapsid antigens. Immunology 2003, 108:431-439.
48. Seo S.H., Hoffmann E., Webster R.G. Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat. Med. 2002, 8:950-954.
49. Slepushkin V.A., Katz J.M., Black R.A., Gamble W.C., Rota P.A., Cox N.J. Protection of mice against influenza A virus challenge by vaccination with baculovirus-expressed M2 protein. Vaccine 1995, 13:1399-1402.
50. Suzue K., Young R.A. Adjuvant-free hsp70 fusion protein system elicits humoral and cellular immune responses to HIV-1 p24. J. Immunol. 1996, 156:873-879.
51. Suzue K., Zhou X., Eisen H.N., Young R.A. Proc. Natl. Acad. Sci. USA. Heat shock fusion proteins as vehicles for antigen delivery into the major histocompatibility complex class I presentation pathway 1997, 94:13146-13151.
52. Takakura Y., Takemoto S., Nishikawa M. Hsp-based tumor vaccines: state-of-the-art and future directions. Curr. Opin. Mol. Ther. 2007, 9:385-391.
53. Takemoto S., Nishikawa M., Takakura Y. Pharmacokinetics and tissue distribution mechanism of mouse recombinant heat shock protein 70 in mice. Pharm. Res. 2005, 22:419-426.
54. Tobian A.A.R., Canaday D.H., Boom W.H., Harding C.V. Bacterial heat shock proteins promote CD91-dependent class I MHC cross-presentation of chaperoned peptide to CD8+T cells by cytosolic mechanisms in dendritic cells versus vacuolar mechanisms in macrophages. J. Immunol. 2004, 172:5277.
55. Turley, C.B., Richard, E.R., Casey, J., David, N.T., Julie, W., et al.. Safety and immunogenicity of a recombinant M2e-flagellin influenza vaccine (STF2.4xM2e) in healthy adults. Vaccine, , in press. http://dx.doi.org/10.1016/j.vaccine.2011.05.041.
56. Udono H., Yamano T., Kawabata Y., Ueda M., Yui K. Generation of cytotoxic T lymphocytes by MHC class I ligands fused to heat shock cognate protein 70. Int. Immunol. 2001, 13:1233-1242.
57. Zhao G., Lin Y., Du L. An M2e-based multiple antigenic peptide vaccine protects mice from lethal challenge with divergent H5N1 influenza viruses. Virol. J. 2010, 7:9.