Universal M2 ectodomain-based influenza A vaccines: preclinical and clinical developments

References

• Jefferson TO, Rivetti D, Di Pietrantonj C, Rivetti A, Demicheli V. Vaccines for preventing influenza in healthy adults. Cochrane Database Syst. Rev.2, CD001269 (2007).
   Google Scholar
• Nichol KL, Nordin JD, Nelson DB, Mullooly JP, Hak E. Effectiveness of influenza vaccine in the community-dwelling elderly. N. Engl. J. Med.357(14), 1373–1381 (2007).
   PubMed Web of Science ®Google Scholar
• de Jong JC, Palache AM, Beyer WE et al. Haemagglutination-inhibiting antibody to influenza virus. Dev. Biol. (Basel)115, 63–73 (2003).
   PubMedGoogle Scholar
• al-Mazrou A, Scheifele DW, Soong T, Bjornson G. Comparison of adverse reactions to whole-virion and split-virion influenza vaccines in hospital personnel. CMAJ145(3), 213–218 (1991).
   PubMed Web of Science ®Google Scholar
• Belshe R, Lee MS, Walker RE, Stoddard J, Mendelman PM. Safety, immunogenicity and efficacy of intranasal, live attenuated influenza vaccine. Expert Rev. Vaccines3(6), 643–654 (2004).
   PubMedGoogle Scholar
• Rudenko LG, Lonskaya NI, Klimov AI, Vasilieva RI, Ramirez A. Clinical and epidemiological evaluation of a live, cold-adapted influenza vaccine for 3–14-year-olds. Bull. WHO74(1), 77–84 (1996).
   PubMed Web of Science ®Google Scholar
• Mendelman PM, Rappaport R, Cho I et al. Live attenuated influenza vaccine induces cross-reactive antibody responses in children against an A/Fujian/411/2002-like H3N2 antigenic variant strain. Pediatr. Infect. Dis. J.23(11), 1053–1055 (2004).
   PubMed Web of Science ®Google Scholar
• The MIV Study Group. The macro-epidemiology of influenza vaccination in 56 countries, 1997–2003. Vaccine23(44), 5133–5143 (2005).
   PubMed Web of Science ®Google Scholar
• Plotkin JB, Dushoff J. Codon bias and frequency-dependent selection on the hemagglutinin epitopes of influenza A virus. Proc. Natl Acad. Sci. USA100(12), 7152–7157 (2003).
   PubMedGoogle Scholar
• Kilbourne ED, Johansson BE, Grajower B. Independent and disparate evolution in nature of influenza A virus hemagglutinin and neuraminidase glycoproteins. Proc. Natl Acad. Sci. USA87(2), 786–790 (1990).
   PubMed Web of Science ®Google Scholar
• Skowronski DM, Masaro C, Kwindt TL et al. Estimating vaccine effectiveness against laboratory-confirmed influenza using a sentinel physician network: results from the 2005–2006 season of dual A and B vaccine mismatch in Canada. Vaccine25(15), 2842–2851 (2007).
   PubMed Web of Science ®Google Scholar
• Abdel-Ghafar AN, Chotpitayasunondh T, Gao Z et al. Update on avian influenza A (H5N1) virus infection in humans. N. Engl. J. Med.358(3), 261–273 (2008).
   PubMed Web of Science ®Google Scholar
• Claas EC, Osterhaus AD, van Beek R et al. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet351(9101), 472–477 (1998).
   PubMed Web of Science ®Google Scholar
• Chen R, Holmes EC. Avian influenza virus exhibits rapid evolutionary dynamics. Mol. Biol. Evol.23(12), 2336–2341 (2006).
   PubMed Web of Science ®Google Scholar
• Leroux-Roels I, Bernhard R, Gerard P et al. Broad clade 2 cross-reactive immunity induced by an adjuvanted clade 1 rH5N1 pandemic influenza vaccine. PLoS ONE3(2), e1665 (2008).
   PubMed Web of Science ®Google Scholar
• Tompkins SM, Zhao ZS, Lo CY et al. Matrix protein 2 vaccination and protection against influenza viruses, including subtype H5N1. Emerg. Infect. Dis.13(3), 426–435 (2007).
   PubMed Web of Science ®Google Scholar
• Black RA, Rota PA, Gorodkova N, Klenk HD, Kendal AP. Antibody response to the M2 protein of influenza A virus expressed in insect cells. J. Gen. Virol.74(Pt 1), 143–146 (1993).
   PubMed Web of Science ®Google Scholar
• Drummond JE, Shaw EE, Antonello JM et al. Design and optimization of a multiplex anti-influenza peptide immunoassay. J. Immunol. Methods334(1–2), 11–20 (2008).
   PubMedGoogle Scholar
• Feng J, Zhang M, Mozdzanowska K et al. Influenza A virus infection engenders a poor antibody response against the ectodomain of matrix protein 2. Virol. J.3, 102 (2006).
   PubMedGoogle Scholar
• Kitikoon P, Strait EL, Thacker EL. The antibody responses to swine influenza virus (SIV) recombinant matrix 1 (rM1), matrix 2 (M2), and hemagglutinin (HA) proteins in pigs with different SIV exposure. Vet. Microbiol.126(1–3), 51–62 (2008).
   PubMedGoogle Scholar
• Liu W, Li H, Chen YH. N-terminus of M2 protein could induce antibodies with inhibitory activity against influenza virus replication. FEMS Immunol. Med. Microbiol.35(2), 141–146 (2003).
   PubMedGoogle Scholar
• Mozdzanowska K, Feng J, Eid M et al. 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. Vaccine21(19–20), 2616–2626 (2003).
   PubMed Web of Science ®Google Scholar
• Zharikova D, Mozdzanowska K, Feng J, Zhang M, Gerhard W. Influenza type A virus escape mutants emerge in vivo in the presence of antibodies to the ectodomain of matrix protein 2. J. Virol.79(11), 6644–6654 (2005).
   PubMed Web of Science ®Google Scholar
• Gerhard W, Mozdzanowska K, Zharikova D. Prospects for universal influenza virus vaccine. Emerg. Infect. Dis.12(4), 569–574 (2006).
   PubMed Web of Science ®Google Scholar
• Lamb RA, Choppin PW. Identification of a second protein (M2) encoded by RNA segment 7 of influenza virus. Virology112(2), 729–737 (1981).
   PubMed Web of Science ®Google Scholar
• Lamb RA, Zebedee SL, Richardson CD. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell40(3), 627–633 (1985).
   PubMed Web of Science ®Google Scholar
• Schnell JR, Chou JJ. Structure and mechanism of the M2 proton channel of influenza A virus. Nature451(7178), 591–595 (2008).
   PubMed Web of Science ®Google Scholar
• Stouffer AL, Acharya R, Salom D et al. Structural basis for the function and inhibition of an influenza virus proton channel. Nature451(7178), 596–599 (2008).
   PubMed Web of Science ®Google Scholar
• Ciampor F, Thompson CA, Grambas S, Hay AJ. Regulation of pH by the M2 protein of influenza A viruses. Virus Res.22(3), 247–258 (1992).
   PubMedGoogle Scholar
• Sakaguchi T, Leser GP, Lamb RA. The ion channel activity of the influenza virus M2 protein affects transport through the Golgi apparatus. J. Cell. Biol.133(4), 733–747 (1996).
   PubMedGoogle Scholar
• Takeuchi K, Lamb RA. Influenza virus M2 protein ion channel activity stabilizes the native form of fowl plague virus hemagglutinin during intracellular transport. J. Virol.68(2), 911–919 (1994).
   PubMedGoogle Scholar
• Iwatsuki-Horimoto K, Horimoto T, Noda T et al. The cytoplasmic tail of the influenza A virus M2 protein plays a role in viral assembly. J. Virol.80(11), 5233–5240 (2006).
   PubMedGoogle Scholar
• McCown MF, Pekosz A. The influenza A virus M2 cytoplasmic tail is required for infectious virus production and efficient genome packaging. J. Virol.79(6), 3595–3605 (2005).
   PubMedGoogle Scholar
• Chen BJ, Leser GP, Jackson D, Lamb RA. The influenza virus M2 protein cytoplasmic tail interacts with the M1 protein and influences virus assembly at the site of virus budding. J. Virol.82(20), 10059–10070 (2008).
   PubMed Web of Science ®Google Scholar
• McCown MF, Pekosz A. Distinct domains of the influenza a virus M2 protein cytoplasmic tail mediate binding to the M1 protein and facilitate infectious virus production. J. Virol.80(16), 8178–8189 (2006).
   PubMedGoogle Scholar
• Zebedee SL, Lamb RA. Influenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J. Virol.62(8), 2762–2772 (1988).
   PubMed Web of Science ®Google Scholar
• Treanor JJ, Tierney EL, Zebedee SL, Lamb RA, Murphy BR. Passively transferred monoclonal antibody to the M2 protein inhibits influenza A virus replication in mice. J. Virol.64(3), 1375–1377 (1990).
   PubMed Web of Science ®Google Scholar
• Wang R, Song A, Levin J et al. Therapeutic potential of a fully human monoclonal antibody against influenza A virus M2 protein. Antiviral Res.80(2), 168–177 (2008).
   PubMed Web of Science ®Google Scholar
• Straight TM, Ottolini MG, Prince GA, Eichelberger MC. Antibody contributes to heterosubtypic protection against influenza A-induced tachypnea in cotton rats. Virol. J.5, 44 (2008).
   PubMed Web of Science ®Google Scholar
• Zhou B, Zhong N, Guan Y. Treatment with convalescent plasma for influenza A (H5N1) infection. N. Engl. J. Med.357(14), 1450–1451 (2007).
   PubMed Web of Science ®Google Scholar
• Neirynck S, Deroo T, Saelens X et al. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat. Med.5(10), 1157–1163 (1999).
   PubMed Web of Science ®Google Scholar
• Slepushkin VA, Katz JM, Black RA et al. Protection of mice against influenza A virus challenge by vaccination with baculovirus-expressed M2 protein. Vaccine13(15), 1399–1402 (1995).
   PubMed Web of Science ®Google Scholar
• Lalor PA, Webby RJ, Morrow J et al. Plasmid DNA-based vaccines protect mice and ferrets against lethal challenge with A/Vietnam/1203/04 (H5N1) influenza virus. J. Infect. Dis.197(12), 1643–1652 (2008).
   PubMed Web of Science ®Google Scholar
• Lo CY, Wu Z, Misplon JA et al. Comparison of vaccines for induction of heterosubtypic immunity to influenza A virus: cold-adapted vaccine versus DNA prime–adenovirus boost strategies. Vaccine26(17), 2062–2072 (2008).
   PubMed Web of Science ®Google Scholar
• Jameson J, Cruz J, Ennis FA. Human cytotoxic T-lymphocyte repertoire to influenza A viruses. J. Virol.72(11), 8682–8689 (1998).
   PubMed Web of Science ®Google Scholar
• Rimmelzwaan GF, Boon AC, Voeten JT et al. Sequence variation in the influenza A virus nucleoprotein associated with escape from cytotoxic T lymphocytes. Virus Res.103(1–2), 97–100 (2004).
   PubMed Web of Science ®Google Scholar
• Wu F, Huang JH, Yuan XY, Huang WS, Chen YH. Characterization of immunity induced by M2e of influenza virus. Vaccine25(52), 8868–8873 (2007).
   PubMed Web of Science ®Google Scholar
• Bessa J, Schmitz N, Hinton HJ et al. Efficient induction of mucosal and systemic immune responses by virus-like particles administered intranasally: implications for vaccine design. Eur. J. Immunol.38(1), 114–126 (2008).
   PubMed Web of Science ®Google Scholar
• Denis J, Acosta-Ramirez E, Zhao Y et al. Development of a universal influenza A vaccine based on the M2e peptide fused to the papaya mosaic virus (PapMV) vaccine platform. Vaccine26(27–28), 3395–3403 (2008).
   PubMed Web of Science ®Google Scholar
• Ionescu RM, Przysiecki CT, Liang X et al. Pharmaceutical and immunological evaluation of human papillomavirus viruslike particle as an antigen carrier. J. Pharm. Sci.95(1), 70–79 (2006).
   PubMed Web of Science ®Google Scholar
• Bachmann MF, Rohrer UH, Kundig TM et al. The influence of antigen organization on B cell responsiveness. Science262(5138), 1448–1451 (1993).
   PubMed Web of Science ®Google Scholar
• De Filette M, Min Jou W, Birkett A et al. Universal influenza A vaccine: optimization of M2-based constructs. Virology337(1), 149–161 (2005).
   PubMed Web of Science ®Google Scholar
• Ernst WA, Kim HJ, Tumpey TM et al. Protection against H1, H5, H6 and H9 influenza A infection with liposomal matrix 2 epitope vaccines. Vaccine24(24), 5158–5168 (2006).
   PubMed Web of Science ®Google Scholar
• Fan J, Liang X, Horton MS et al. Preclinical study of influenza virus A M2 peptide conjugate vaccines in mice, ferrets, and rhesus monkeys. Vaccine22(23–24), 2993–3003 (2004).
   PubMed Web of Science ®Google Scholar
• Frace AM, Klimov AI, Rowe T, Black RA, Katz JM. Modified M2 proteins produce heterotypic immunity against influenza A virus. Vaccine17(18), 2237–2244 (1999).
   PubMed Web of Science ®Google Scholar
• Huleatt JW, Nakaar V, Desai P 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. Vaccine26(2), 201–214 (2008).
   PubMed Web of Science ®Google Scholar
• Liu W, Peng Z, Liu Z et al. High epitope density in a single recombinant protein molecule of the extracellular domain of influenza A virus M2 protein significantly enhances protective immunity. Vaccine23(3), 366–371 (2004).
   PubMed Web of Science ®Google Scholar
• Mozdzanowska K, Furchner M, Zharikova D, Feng J, Gerhard W. Roles of CD4+ T-cell-independent and -dependent antibody responses in the control of influenza virus infection: evidence for noncognate CD4+ T-cell activities that enhance the therapeutic activity of antiviral antibodies. J. Virol.79(10), 5943–5951 (2005).
   PubMed Web of Science ®Google Scholar
• Eriksson AM, Schon KM, Lycke NY. The cholera toxin-derived CTA1-DD vaccine adjuvant administered intranasally does not cause inflammation or accumulate in the nervous tissues. J. Immunol.173(5), 3310–3319 (2004).
   PubMed Web of Science ®Google Scholar
• Eliasson DG, El Bakkouri K, Schon K et al. CTA1-M2e-DD: a novel mucosal adjuvant targeted influenza vaccine. Vaccine26(9), 1243–1252 (2008).
   PubMed Web of Science ®Google Scholar
• Huber VC, Lynch JM, Bucher DJ, Le J, Metzger DW. Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J. Immunol.166(12), 7381–7388 (2001).
   PubMed Web of Science ®Google Scholar
• Jegerlehner A, Schmitz N, Storni T, Bachmann MF. Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J. Immunol.172(9), 5598–5605 (2004).
   PubMed Web of Science ®Google Scholar
• Mozdzanowska K, Zharikova D, Cudic M, Otvos L, Gerhard W. 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. Virol. J.4, 118 (2007).
   PubMed Web of Science ®Google Scholar
• Buckland BC. The process development challenge for a new vaccine. Nature Med.11(4 Suppl.), S16–S19 (2005).
   PubMedGoogle Scholar
• De Filette M, Martens W, Roose K et al. An influenza A vaccine based on tetrameric ectodomain of matrix protein 2. J. Biol. Chem.283(17), 11382–11387 (2008).
   PubMed Web of Science ®Google Scholar
• Govaert TM, Thijs CT, Masurel N et al. The efficacy of influenza vaccination in elderly individuals. A randomized double-blind placebo-controlled trial. JAMA272(21), 1661–1665 (1994).
   PubMed Web of Science ®Google Scholar
• Lin YP, Gregory V, Bennett M, Hay A. Recent changes among human influenza viruses. Virus Res.103(1–2), 47–52 (2004).
   PubMed Web of Science ®Google Scholar
• Bianchi E, Liang X, Ingallinella P et al. Universal influenza B vaccine based on the maturational cleavage site of the hemagglutinin precursor. J. Virol.79(12), 7380–7388 (2005).
   PubMed Web of Science ®Google Scholar
• De Filette M, Ramne A, Birkett A et al. The universal influenza vaccine M2e–HBc administered intranasally in combination with the adjuvant CTA1-DD provides complete protection. Vaccine24(5), 544–551 (2006).
   PubMed Web of Science ®Google Scholar
• Stephenson I, Zambon MC, Rudin A et al. Phase I evaluation of intranasal trivalent inactivated influenza vaccine with nontoxigenic Escherichia coli enterotoxin and novel biovector as mucosal adjuvants, using adult volunteers. J. Virol.80(10), 4962–4970 (2006).
   PubMed Web of Science ®Google Scholar
• Jimenez GS, Planchon R, Wei Q et al. Vaxfectin-formulated influenza DNA vaccines encoding NP and M2 viral proteins protect mice against lethal viral challenge. Hum. Vaccin.3(5), 157–164 (2007).
   PubMed Web of Science ®Google Scholar
• De Filette M, Fiers W, Martens W et al. Improved design and intranasal delivery of an M2e-based human influenza A vaccine. Vaccine24(44–46), 6597–6601 (2006).
   PubMed Web of Science ®Google Scholar
• De Filette M, Martens W, Smet A et al. Universal influenza A M2e-HBc vaccine protects against disease even in the presence of pre-existing anti-HBc antibodies. Vaccine26(51), 6503–6507 (2008)
   PubMed Web of Science ®Google Scholar
• Heinen PP, Rijsewijk FA, de Boer-Luijtze EA, Bianchi AT. Vaccination of pigs with a DNA construct expressing an influenza virus M2–nucleoprotein fusion protein exacerbates disease after challenge with influenza A virus. J. Gen. Virol.83(Pt 8), 1851–1859 (2002).
   PubMed Web of Science ®Google Scholar
• Laddy DJ, Yan J, Kutzler M et al. Heterosubtypic protection against pathogenic human and avian influenza viruses via in vivo electroporation of synthetic consensus DNA antigens. PLoS ONE3(6), e2517 (2008).
   PubMed Web of Science ®Google Scholar
• Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res.32(5), 1792–1797 (2004).
   PubMed Web of Science ®Google Scholar