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Review

Cross-protective immunity to influenza A viruses

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Pages 1325-1341 | Published online: 09 Jan 2014

References

  • Cox NJ, Kawaoka Y. Orthomyxoviruses: influenza. In: Topley and Wilson’s Microbiology and Microbial Infections. Collier L, Balows A, Sussman M (Eds). Arnold, London, UK, 385–433 (1998).
  • Lamb RA, Krug RM. Orthomyxoviradae; the viruses and their replication. In: Virology. Knipe DM, Howley PM, Griffin DE et al. (Eds). Lippincott Williams & Wilkins, PA, USA, 1487–1503 (2001).
  • Matrosovich MN, Klenk HD, Kawaoka Y. Receptor specificity, host-range, and pathogenicity of influenza viruses. In: Influenza Virology: Current Topics. Kawaoka Y (Eds). Caister Academic Press, Wymondham, UK, 95–137 (2006).
  • Chen WS, Calvo PA, Malide D et al. A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med.7(12), 1306–1312 (2001).
  • Kilbourne ED, Smith C, Brett I, Pokorny BA, Johansson B, Cox N. The total influenza vaccine failure of 1947 revisited: major intrasubtypic antigenic change can explain failure of vaccine in a post-World War II epidemic. Proc. Natl Acad. Sci. USA99(16), 10748–10752 (2002).
  • Hancock K, Veguilla V, Lu X et al. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N. Engl. J. Med.361(20), 1945–1952 (2009).
  • Treanor JJ, Wilkinson BE, Masseoud F et al. Safety and immunogenicity of a recombinant hemagglutinin vaccine for H5 influenza in humans. Vaccine19(13–14), 1732–1737 (2001).
  • Epstein SL. Control of influenza virus infection by immunity to conserved viral features. Expert Rev. Anti Infect. Ther.1(4), 627–638 (2003).
  • Tamura S, Tanimoto T, Kurata T. Mechanisms of broad cross-protection provided by influenza virus infection and their application to vaccines. Jpn J. Infect. Dis.58(4), 195–207 (2005).
  • Carrat F, Flahault A. Influenza vaccine: the challenge of antigenic drift. Vaccine25(39–40), 6852–6862 (2007).
  • Rimmelzwaan GF, Fouchier RA, Osterhaus AD. Influenza virus-specific cytotoxic T lymphocytes: a correlate of protection and a basis for vaccine development. Curr. Opin. Biotechnol.18(6), 529–536 (2007).
  • Grebe KM, Yewdell JW, Bennink JR. Heterosubtypic immunity to influenza A virus: where do we stand? Microb. Infect.10(9), 1024–1029 (2008).
  • Tripp RA, Tompkins SM. Recombinant vaccines for influenza virus. Curr. Opin Invest. Drugs9(8), 836–845 (2008).
  • Brown LE, Kelso A. Prospects for an influenza vaccine that induces cross-protective cytotoxic T lymphocytes. Immunol. Cell Biol.87(4), 300–308 (2009).
  • Schulman JL, Kilbourne ED. Induction of partial specific heterotypic immunity in mice by a single infection with influenza A virus. J. Bacteriol.89, 170–174 (1965).
  • Yetter RA, Lehrer S, Ramphal R, Small PA Jr. Outcome of influenza infection: effect of site of initial infection and heterotypic immunity. Infect. Immun.29, 654–662 (1980).
  • Kreijtz JHCM, Bodewes R, van den Brand JMA et al. Infection of mice with a human influenza A/H3N2 virus induces protective immunity against lethal infection with influenza A/H5N1 virus. Vaccine27(36), 4983–4989 (2009).
  • Flynn KJ, Belz GT, Altman JD, Ahmed R, Woodland DL, Doherty PC. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity8, 683–691 (1998).
  • Sweet C, Fenton RJ, Price GE. The ferret as an animal model of influenza virus infection. In: Handbook of Animal Models of Infection: Experimental Models in Antimicrobial Chemotherapy. Zak O, Sande M (Eds). Academic Press, London, UK, 989–998 (1999).
  • Smith H, Sweet C. Lessons for human influenza from pathogenicity studies with ferrets. Rev. Infect. Dis.10(1), 56–75 (1988).
  • Yetter RA, Barber WH, Small PA Jr. Heterotypic immunity to influenza in ferrets. Infect. Immun.29, 650–653 (1980).
  • McLaren C, Potter CW. Immunity to influenza in ferrets. VII. Effect of previous infection with heterotypic and heterologous influenza viruses on the response of ferrets to inactivated influenza virus vaccines. J. Hyg. (Lond.)72(1), 91–100 (1974).
  • Steel J, Staeheli P, Mubareka S, Garcia-Sastre A, Palese P, Lowen AC. Transmission of pandemic H1N1 influenza virus and impact of prior exposure to seasonal strains or interferon treatment. J. Virol.84(1), 21–26 (2010).
  • Straight TM, Ottolini MG, Prince GA, Eichelberger MC. Evidence of a cross-protective immune response to influenza A in the cotton rat model. Vaccine24(37–39), 6264–6271 (2006).
  • Heinen PP, de Boer-Luijtze EA, Bianchi ATJ. Respiratory and systemic humoral and cellular immune responses of pigs to a heterosubtypic influenza A virus infection. J. Gen. Virol.82, 2697–2707 (2001).
  • Seo SH, Webster RG. Cross-reactive, cell-mediated immunity and protection of chickens from lethal H5N1 influenza virus infection in Hong Kong poultry markets. J. Virol.75(6), 2516–2525 (2001).
  • Fereidouni SR, Starick E, Beer M et al. Highly pathogenic avian influenza virus infection of mallards with homo- and heterosubtypic immunity induced by low pathogenic avian influenza viruses. PLoS ONE4(8), e6706 (2009).
  • Liang S, Mozdzanowska K, Palladino G, Gerhard W. Heterosubtypic immunity to influenza type A virus in mice: effector mechanisms and their longevity. J. Immunol.152, 1653–1661 (1994).
  • Topham DJ, Tripp RA, Doherty PC. CD8+ T cells clear influenza virus by perforin or Fas dependent processes. J. Immunol.159, 5197–5200 (1997).
  • Trapani JA, Smyth MJ. Functional significance of the perforin/granzyme cell death pathway. Nat. Rev. Immunol.2(10), 735–747 (2002).
  • Furuya Y, Chan J, Regner M et al. Cytotoxic T cells are the predominant players providing cross-protective immunity induced by γ-irradiated influenza A viruses. J. Virol.84(9), 4212–4221 (2010).
  • Bot A, Bot S, Bona CA. Protective role of g interferon during the recall response to influenza virus. J. Virol.72(8), 6637–6645 (1998).
  • Nguyen HH, van Ginkel FW, Vu HL, Novak MJ, McGhee JR, Mestecky J. γ interferon is not required for mucosal cytotoxic T-lymphocyte responses or heterosubtypic immunity to influenza A virus infection in mice. J. Virol.74(12), 5495–5501 (2000).
  • Nguyen HH, van Ginkel FW, Vu HL, McGhee JR, Mestecky J. Heterosubtypic immunity to influenza A virus infection requires B cells but not CD8+ cytotoxic T lymphocytes. J. Infect. Dis.183(3), 368–376 (2001).
  • Epstein SL, Lo C-Y, Misplon JA, Bennink JR. Mechanism of protective immunity against influenza virus infection in mice without antibodies. J. Immunol.160(1), 322–327 (1998).
  • Benton KA, Misplon JA, Lo C-Y, Brutkiewicz RR, Prasad SA, Epstein SL. Heterosubtypic immunity to influenza A virus in mice lacking either IgA, all Ig, NKT cells or γ/δ T cells. J. Immunol.166, 7437–7445 (2001).
  • Graham MB, Braciale TJ. Resistance to and recovery from lethal influenza virus infection in B lymphocyte-deficient mice. J. Exp. Med.186(12), 2063–2068 (1997).
  • Topham DJ, Doherty PC. Clearance of an influenza A virus by CD4+ T cells is inefficient in the absence of B cells. J. Virol.72(1), 882–885 (1998).
  • Taylor SF, Bender BS. β2-microglobulin-deficient mice demonstrate class II MHC restricted anti-viral CD4+ but not CD8+ CTL against influenza-sensitized autologous splenocytes. Immunol. Lett.46, 67–73 (1995).
  • Topham DJ, Tripp RA, Sarawar SR, Sangster MY, Doherty PC. Immune CD4+ T cells promote the clearance of influenza virus from major histocompatibility complex class II-/- respiratory epithelium. J. Virol.70, 1288–1291 (1996).
  • Brown DM, Dilzer AM, Meents DL, Swain SL. CD4 T cell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms a one–two punch. J. Immunol.177(5), 2888–2898 (2006).
  • Graham MB, Braciale VL, Braciale TJ. Influenza virus-specific CD4+ T helper type 2 T lymphocytes do not promote recovery from experimental virus infection. J. Exp. Med.180, 1273–1282 (1994).
  • Scherle PA, Gerhard W. Functional analysis of influenza-specific helper T cell clones in vivo. T cells specific for internal viral proteins provide cognate help for B cell responses to hemagglutinin. J. Exp. Med.164, 1114–1128 (1986).
  • Russell SM, Liew FY. T cells primed by influenza virion internal components can cooperate in the antibody response to haemagglutinin. Nature280(5718), 147–148 (1979).
  • Mbawuike IN, Six HR, Cate TR, Couch RB. Vaccination with inactivated influenza A virus during pregnancy protects neonatal mice against lethal challenge by influenza A viruses representing three subtypes. J. Virol.64, 1370–1374 (1990).
  • Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat. Med.5(10), 1157–1163 (1999).
  • 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).
  • Tompkins SM, Zhao ZS, Lo C-Y et al. Matrix protein 2 vaccination and protection against influenza viruses, including subtype H5N1. Emerg. Infect. Dis.13(3), 426–435 (2007).
  • Epstein SL, Lo C-Y, Misplon JA et al. Mechanisms of heterosubtypic immunity to lethal influenza A virus infection in immunocompetent, T cell-depleted, β2-microglobulin-deficient, and J chain-deficient mice. J. Immunol.158, 1222–1230 (1997).
  • Tumpey TM, Renshaw M, Clements JD, Katz JM. Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection. J. Virol.75(11), 5141–5150 (2001).
  • Fazekas de St Groth S, Donnelley M. Studies in experimental immunology of influenza. IV. The protective value of active immunization. Aust. J. Exp. Biol. Med. Sci.28, 61–75 (1950).
  • Takada A, Kuboki N, Okazaki K et al. Avirulent avian influenza virus as a vaccine strain against a potential human pandemic. J. Virol.73(10), 8303–8307 (1999).
  • Takada A, Matsushita S, Ninomiya A, Kawaoka Y, Kida H. Intranasal immunization with formalin-inactivated virus vaccine induces a broad spectrum of heterosubtypic immunity against influenza A virus infection in mice. Vaccine21(23), 3212–3218 (2003).
  • Quan FS, Compans RW, Nguyen HH, Kang SM. Induction of heterosubtypic immunity to influenza virus by intranasal immunization. J. Virol.82(3), 1350–1359 (2008).
  • Baumgarth N, Kelso A. Functionally distinct T cells in three compartments of the respiratory tract after influenza virus infection. Eur. J. Immunol.26(9), 2189–2197 (1996).
  • Nguyen HH, Moldoveanu Z, Novak MJ et al. Heterosubtypic immunity to lethal influenza A virus infection is associated with virus-specific CD8+ cytotoxic T lymphocyte responses induced in mucosa-associated tissues. Virology254, 50–60 (1999).
  • Hogan RJ, Usherwood EJ, Zhong WM et al. Activated antigen-specific CD8+ T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol.166(3), 1813–1822 (2001).
  • Price GE, Soboleski MR, Lo CY et al. Vaccination focusing immunity on conserved antigens protects mice and ferrets against virulent H1N1 and H5N1 influenza A viruses. Vaccine27(47), 6512–6521 (2009).
  • Lalvani A, Brookes R, Hambleton S, Britton WJ, Hill AVS, McMichael AJ. Rapid effector function in CD8+ memory T cells. J. Exp. Med.186(6), 859–865 (1997).
  • Jackson DC, Lau YF, Le T et al. A totally synthetic vaccine of generic structure that targets Toll-like receptor 2 on dendritic cells and promotes antibody or cytotoxic T cell responses. Proc. Natl Acad. Sci. USA101(43), 15440–15445 (2004).
  • Deliyannis G, Kedzierska K, Lau YF et al. Intranasal lipopeptide primes lung-resident memory CD8+ T cells for long-term pulmonary protection against influenza. Eur. J. Immunol.36(3), 770–778 (2006).
  • Tamura S, Hasegawa H, Kurata T. Estimation of the effective doses of nasal-inactivated influenza vaccine in humans from mouse-model experiments. Jpn J. Infect. Dis.63(1), 8–15 (2010).
  • Yoshikawa T, Suzuki Y, Nomoto A, Sata T, Kurata T, Tamura S. Antibody responses and protection against influenza virus infection in different congenic strains of mice immunized intranasally with adjuvant-combined A/Beijing/262/95 (H1N1) virus hemagglutinin or neuraminidase. Vaccine21(1–2), 60–66 (2002).
  • Misplon JA, Lo CY, Gabbard JD, Tompkins SM, Epstein SL. Genetic control of immune responses to influenza A matrix 2 protein (M2). Vaccine28(36), 5817–5827 (2010).
  • Hennessy AV, Davenport FM, Horton RJM, Napier JA, Francis T Jr. Asian influenza: occurrence and recurrence, a community and family study. Mil. Med.129, 38–50 (1964).
  • Slepushkin AN. The effect of a previous attack of A1 influenza on susceptibility to A2 virus during the 1957 outbreak. Bull. World Health Organ.20, 297–301 (1959).
  • Epstein SL. 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(1), 49–53 (2006).
  • Steinhoff MC, Fries LF, Karron RA, Clements ML, Murphy BR. Effect of heterosubtypic immunity on infection with attenuated influenza-A virus vaccines in young children. J. Clin. Microbiol.31(4), 836–838 (1993).
  • Frank AL, Taber LH, Wells JM. Individuals infected with two subtypes of influenza A virus in the same season. J. Infect. Dis.147, 120–124 (1983).
  • Sonoguchi T, Naito H, Hara M, Takeuchi Y, Fukumi H. 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 (1985).
  • Carrat F, Vergu E, Ferguson NM et al. Time lines of infection and disease in human influenza: a review of volunteer challenge studies. Am. J. Epidemiol.167(7), 775–785 (2008).
  • McMichael AJ, Gotch FM, Noble GR, Beare PA. Cytotoxic T-cell immunity to influenza. N. Engl. J. Med.309, 13–17 (1983).
  • Murphy BR, Chalhub EG, Nusinoff SR, Kasel J, Chanock RM. Temperature-sensitive mutants of influenza virus. III. Further characterization of the ts-1[E] influenza A recombinant (H3N2) virus in man. J. Infect. Dis.128(4), 479–487 (1973).
  • McMichael AJ, Dongworth DW, Gotch FM, Clark A, Potter CW. Declining T-cell immunity to influenza, 1977–1982. Lancet2(8353), 762–764 (1983).
  • Lee LY, Ha DLA, Simmons C et al. Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J. Clin. Invest.118(10), 3478–3490 (2008).
  • Roti M, Yang J, Berger D, Huston L, James EA, Kwok WW. Healthy human subjects have CD4+ T cells directed against H5N1 influenza virus. J. Immunol.180(3), 1758–1768 (2008).
  • Greenbaum JA, Kotturi MF, Kim Y et al. Pre-existing immunity against swine-origin H1N1 influenza viruses in the general human population. Proc. Natl Acad. Sci. USA106(48), 20365–20370 (2009).
  • Ge X, Tan V, Bollyky PL, Standifer NE, James EA, Kwok WW. Assessment of seasonal influenza A virus-specific CD4 T-cell responses to 2009 pandemic H1N1 swine-origin influenza A virus. J. Virol.84(7), 3312–3319 (2010).
  • Alexander J, Bilsel P, del Guercio MF et al. Identification of broad binding class I HLA supertype epitopes to provide universal coverage of influenza A virus. Hum. Immunol.71, 468–474 (2010).
  • Rao SS, Kong WP, Wei CJ et al. Comparative efficacy of hemagglutinin, nucleoprotein, and matrix 2 protein gene-based vaccination against H5N1 influenza in mouse and ferret. PLoS ONE5(3), e9812 (2010).
  • Price GE, Soboleski MR, Lo C-Y et al. Single-dose mucosal immunization with a candidate universal influenza vaccine provides rapid protection from virulent H5N1, H3N2 and H1N1 viruses. PLoS ONE5(10), e13162 (2010).
  • Lo C-Y, 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).
  • Barefoot B, Thornburg NJ, Barouch DH et al. Comparison of multiple vaccine vectors in a single heterologous prime–boost trial. Vaccine26(48), 6108–6118 (2008).
  • Belshe RB, Edwards KM, Vesikari T et al. Live attenuated versus inactivated influenza vaccine in infants and young children. N. Engl. J. Med.356(7), 685–696 (2007).
  • Monto AS, Ohmit SE, Petrie JG et al. Comparative efficacy of inactivated and live attenuated influenza vaccines. N. Engl. J. Med.361(13), 1260–1267 (2009).
  • Asmuth DM, Brown EL, DiNubile MJ et al. Comparative cell-mediated immunogenicity of DNA/DNA, DNA/adenovirus type 5 (Ad5), or Ad5/Ad5 HIV-1 clade B gag vaccine prime–boost regimens. J. Infect. Dis.201(1), 132–141 (2010).
  • Taylor PM, Davey J, Howland K, Rothbard JB, Askonas BA. Class I MHC molecules rather than other mouse genes dictate influenza epitope recognition by cytotoxic T cells. Immunogenetics26, 267–272 (1987).
  • Brett SJ, Blau J, Hughes-Jenkins CM, Rhodes J, Liew FY, Tite JP. Human T cell recognition of influenza A nucleoprotein – specificity and genetic restriction of immunodominant T helper cell epitopes. J. Immunol.147(3), 984–991 (1991).
  • Ulmer JB, Donnelly JJ, Parker SE et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science259, 1745–1749 (1993).
  • Robinson HL, Boyle CA, Feltquate DM, Morin MJ, Santoro JC, Webster RG. DNA immunization for influenza virus: studies using hemagglutinin- and nucleoprotein-expressing DNAs. J. Infect. Dis.S50–S55 (1997).
  • Cox RJ, Mykkeltvedt E, Robertson J, Haaheim LR. Non-lethal viral challenge of influenza haemagglutinin and nucleoprotein DNA vaccinated mice results in reduced viral replication. Scand. J. Immunol.55(1), 14–23 (2002).
  • Epstein SL, Kong WP, Misplon JA et al. Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine23(46–47), 5404–5410 (2005).
  • Yewdell JW, Hackett CJ. Specificity and function of T lymphocytes induced by influenza A viruses. In: The Influenza Viruses. Krug RM (Eds). Plenum Publishing Corp., NY, USA, 36–429 (1989).
  • Crowe SR, Miller SC, Shenyo RM, Woodland DL. Vaccination with an acidic polymerase, epitope of influenza virus elicits a potent antiviral T cell response but delayed clearance of an influenza virus challenge. J. Immunol.174(2), 696–701 (2005).
  • Matsui M, Kohyama S, Suda T et al. A CTL-based liposomal vaccine capable of inducing protection against heterosubtypic influenza viruses in HLA-A*0201 transgenic mice. Biochem. Biophys. Res. Commun.391(3), 1494–1499 (2010).
  • Draper SJ, Heeney JL. Viruses as vaccine vectors for infectious diseases and cancer. Nat. Rev. Micro.8(1), 62–73 (2010).
  • Jameson J, Cruz J, Ennis FA. Human cytotoxic T-lymphocyte repertoire to influenza A viruses. J. Virol.72(11), 8682–8689 (1998).
  • Gianfrani C, Oseroff C, Sidney J, Chesnut RW, Sette A. Human memory CTL response specific for influenza A virus is broad and multispecific. Human Immunol.61, 438–452 (2000).
  • Liu WL, Zou P, Chen YH. Monoclonal antibodies recognizing EVETPIRN epitope of influenza A virus M2 protein could protect mice from lethal influenza A virus challenge. Immunol. Lett.93(2–3), 131–136 (2004).
  • Zou P, Liu WL, Chen YH. The epitope recognized by a monoclonal antibody in influenza A virus M2 protein is immunogenic and confers immune protection. Int. Immunopharmacol.5(4), 631–635 (2005).
  • Smirnov YA, Lipatov AS, Gitelman AK et al. An epitope shared by the hemagglutinins of H1, H2, H5, and H6 subtypes of influenza A virus. Acta Virologica43(4), 237–244 (1999).
  • Okuno Y, Isegawa Y, Sasao F, Ueda S. A common neutralizing epitope conserved between the hemagglutinins of influenza A virus H1 and H2 strains. J. Virol.67, 2552–2558 (1993).
  • Throsby M, van den Brink E, Jongeneelen M et al. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS ONE3(12), e3942 (2008).
  • 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).
  • Liu WL, Zou P, Ding J, Lu Y, Chen YH. Sequence comparison between the extracellular domain of M2 protein human and avian influenza A virus provides new information for bivalent influenza vaccine design. Microb. Infect.7(2), 171–177 (2005).
  • Sui JH, Hwang WC, Perez S et al. Structural and functional bases for broad-spectrum neutralization of avian and human influenza A viruses. Nat. Struct. Mol. Biol.16(3), 265–273 (2009).
  • Corti D, Suguitan AL Jr, Pinna D et al. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J. Clin. Invest.120(5), 1663–1673 (2010).
  • Steel J, Lowen AC, Wang TT et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. mBio1(1), e00018-10 (2010).
  • Bommakanti G, Citron MP, Hepler RW et al. Design of an HA2-based Escherichia coli expressed influenza immunogen that protects mice from pathogenic challenge. Proc. Natl Acad. Sci. USA107(31), 13701–13706 (2010).
  • Ekiert DC, Bhabha G, Elsliger MA et al. Antibody recognition of a highly conserved influenza virus epitope. Science324(5924), 246–251 (2009).
  • Heiny AT, Miotto O, Srinivasan KN et al. Evolutionarily conserved protein sequences of influenza A viruses, avian and human, as vaccine targets. PLoS ONE2(11), e1190 (2007).
  • Assarsson E, Bui HH, Sidney J et al. Immunomic analysis of the repertoire of T-cell specificities for influenza A virus in humans. J. Virol.82(24), 12241–12251 (2008).
  • Alexander J, Bilsel P, del Guercio MF et al. Universal influenza DNA vaccine encoding conserved CD4+ T cell epitopes protects against lethal viral challenge in HLA-DR transgenic mice. Vaccine28(3), 664–672 (2010).
  • Babon JA, Cruz J, Orphin L et al. Genome-wide screening of human T-cell epitopes in influenza A virus reveals a broad spectrum of CD4+ T-cell responses to internal proteins, hemagglutinins, and neuraminidases. Human Immunol.70(9), 711–721 (2009).
  • Stoloff GA, Caparros-Wanderley W. Synthetic multi-epitope peptides identified in silico induce protective immunity against multiple influenza serotypes. Eur. J. Immunol.37(9), 2441–2449 (2007).
  • Bui HH, Peters B, Assarsson E, Mbawuike I, Sette A. Ab and T cell epitopes of influenza A virus, knowledge and opportunities. Proc. Natl Acad. Sci. USA104(1), 246–251 (2007).
  • Alexander J, Oseroff C, Dahlberg C et al. A decaepitope polypeptide primes for multiple CD8+ IFN-γ and Th lymphocyte responses: evaluation of multiepitope polypeptides as a mode for vaccine delivery. J. Immunol.168(12), 6189–6198 (2002).
  • Fomsgaard A, Nielsen HV, Kirkby N et al. Induction of cytotoxic T-cell responses by gene gun DNA vaccination with minigenes encoding influenza A virus HA and NP CTL-epitopes. Vaccine18(7–8), 681–691 (1999).
  • Levi R, Arnon R. Synthetic recombinant influenza vaccine induces efficient long-term immunity and cross-strain protection. Vaccine14, 85–92 (1996).
  • Adar Y, Singer Y, Levi R et al. A universal epitope-based influenza vaccine and its efficacy against H5N1. Vaccine27(15), 2099–2107 (2009).
  • Boon ACM, de Mutsert G, Graus YMF et al. Sequence variation in a newly identified HLA-B35-restricted epitope in the influenza a virus nucleoprotein associated with escape from cytotoxic T lymphocytes. J. Virol.76(5), 2567–2572 (2002).
  • Voeten JT, Bestebroer TM, Nieuwkoop NJ, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Antigenic drift in the influenza A virus (H3N2) nucleoprotein and escape from recognition by cytotoxic T lymphocytes. J. Virol.74(15), 6800–6807 (2000).
  • Price GE, Ou R, Jiang H, Huang L, Moskophidis D. Viral escape by selection of cytotoxic T cell-resistant variants in influenza A virus pneumonia. J. Exp. Med.191(11), 1853–1867 (2000).
  • Epstein SL, Tumpey TM, Misplon JA et al. DNA vaccine expressing conserved influenza virus proteins protective against H5N1 challenge infection in mice. Emerg. Infect. Dis.8(8), 796–801 (2002).
  • 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).
  • Eichelberger M, Golding H, Hess M et al. FDA/NIH/WHO public workshop on immune correlates of protection against influenza A viruses in support of pandemic vaccine development, Bethesda, Maryland, US, December 10–11, 2007. Vaccine26(34), 4299–4303 (2008).
  • Murphy BR, Kasel JA, Chanock RM. Association of serum anti-neuraminidase antibody with resistance to influenza in man. N. Engl. J. Med.286, 1329–1332 (1972).
  • Murphy BR. Mucosal immunity to viruses. In: Mucosal Immunology. Elsevier Academic Press, MA, USA (1992).
  • Belshe RB, Gruber WC, Mendelman PM et al. Correlates of immune protection induced by live, attenuated, cold-adapted, trivalent, intranasal influenza virus vaccine. J. Infect. Dis.181(3), 1133–1137 (2000).
  • McElhaney JE, Xie DX, Hager WD et al. T cell responses are better correlates of vaccine protection in the elderly. J. Immunol.176(10), 6333–6339 (2006).
  • Forrest BD, Pride MW, Dunning AJ et al. Correlation of cellular immune responses with protection against culture-confirmed influenza virus in young children. Clin.Vaccine Immunol.15(7), 1042–1053 (2008).
  • Fiers W, De FM, El BK et al. M2e-based universal influenza A vaccine. Vaccine27(45), 6280–6283 (2009).
  • Smith LR, Wloch MK, Ye M et al. Phase 1 clinical trials of the safety and immunogenicity of adjuvanted plasmid DNA vaccines encoding influenza A virus H5 hemagglutinin. Vaccine28(13), 2565–2572 (2010).
  • Carrat F, Lavenu A, Cauchemez S, Deleger S. Repeated influenza vaccination of healthy children and adults: borrow now, pay later? Epidemiol. Infect.134(1), 63–70 (2006).
  • Bodewes R, Kreijtz JHCM, Baas C et al. Vaccination against human influenza A/H3N2 virus prevents the induction of heterosubtypic immunity against lethal infection with avian influenza A/H5N1 virus. PLoS ONE4(5), e5538 (2009).
  • Bodewes R, Kreijtz JH, Rimmelzwaan GF. Yearly influenza vaccinations: a double-edged sword? Lancet Infect. Dis.9(12), 784–788 (2009).
  • Settembre EC, Dormitzer PR, Rappuoli R. H1N1: can a pandemic cycle be broken? Sci. Transl. Med.2(24), 24ps14 (2010).
  • Alsharifi M, Furuya Y, Bowden TR et al. Intranasal flu vaccine protective against seasonal and H5N1 avian influenza infections. PLoS ONE4(4), e5336 (2009).
  • Tannock GA, Paul JA, Barry RD. Relative immunogenicity of the cold-adapted influenza virus A/Ann Arbor/6/60 (A/AA/6/60-ca), recombinants of A/AA/6/60-ca, and parental strains with similar surface antigens. Infect. Immun.43(2), 457–462 (1984).
  • Tannock GA, Paul JA. Homotypic and heterotypic immunity of influenza A viruses induced by recombinants of the cold-adapted master strain A/Ann Arbor/6/60-ca. Arch. Virol.92(1–2), 121–133 (1987).
  • Powell TJ, Strutt T, Reome J et al. Priming with cold-adapted influenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J. Immunol.178(2), 1030–1038 (2007).
  • Talon J, Salvatore M, O’Neill RE et al. Influenza A and B viruses expressing altered NS1 proteins: a vaccine approach. Proc. Natl Acad. Sci. USA97(8), 4309–4314 (2000).
  • Richt JA, Lekcharoensuk P, Lager KM et al. Vaccination of pigs against swine influenza viruses by using an NS1-truncated modified live-virus vaccine. J. Virol.80(22), 11009–11018 (2006).
  • Liu T, Ye Z. Attenuating mutations of the matrix gene of influenza A/WSN/33 virus. J. Virol.79(3), 1918–1923 (2005).
  • Watanabe S, Watanabe T, Kawaoka Y. Influenza A virus lacking M2 protein as a live attenuated vaccine. J. Virol.83(11), 5947–5950 (2009).
  • Mozdzanowska K, Feng JQ, 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).
  • Deres K, Schild H, Wiesmüller KH, Jung G, Rammensee HG. In vivo priming of virus-specific cytotoxic T lymphocytes with synthetic lipopeptide vaccine. Nature342, 561–564 (1989).
  • Carragher DM, Kaminski DA, Moquin A, Hartson L, Randall TD. A novel role for non-neutralizing antibodies against nucleoprotein in facilitating resistance to influenza virus. J. Immunol.181(6), 4168–4176 (2008).
  • Tamura S, Miyata K, Matsuo K et al. Acceleration of influenza virus clearance by Th1 cells in the nasal site of mice immunized intranasally with adjuvant-combined recombinant nucleoprotein. J. Immunol.156(10), 3892–3900 (1996).
  • Slepushkin VA, Katz JM, Black RA, Gamble WC, Rota PA, Cox NJ. Protection of mice against influenza A virus challenge by vaccination with baculovirus-expressed M2 protein. Vaccine13(15), 1399–1402 (1995).
  • Sui Z, Chen Q, Wu R et al. Cross-protection against influenza virus infection by intranasal administration of M2-based vaccine with chitosan as an adjuvant. Arch Virol.155(4), 535–544 (2010).
  • 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).
  • Eliasson DG, Bakkouri KE, Schön K et al. CTA1–M2e-DD: a novel mucosal adjuvant targeted influenza vaccine. Vaccine26(9), 1243–1252 (2008).
  • 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).
  • Liu WL, Zou P, Liu ZQ, Yun L, Jian D, Chen YH. 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).
  • Mbawuike IN, Dillon SB, Demuth SG, Jones CS, Cate TR, Couch RB. Influenza A subtype cross-protection after immunization of outbred mice with a purified chimeric NS1/HA2 influenza virus protein. Vaccine12, 1340–1349 (1994).
  • Okuda K, Ihata A, Watabe S et al. Protective immunity against influenza A virus induced by immunization with DNA plasmid containing influenza M gene. Vaccine19(27), 3681–3691 (2001).
  • 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. Vacc.3(5), 157–164 (2007).
  • Saha S, Yoshida S, Ohba K et al. A fused gene of nucleoprotein (NP) and herpes simplex virus genes (VP22) induces highly protective immunity against different subtypes of influenza virus. Virology354(1), 48–57 (2006).
  • Andrew ME, Coupar BEH, Ada GL, Boyle DB. Cell-mediated immune responses to influenza virus antigens expressed by vaccinia virus recombinants. Microbial. Pathog.1, 443–452 (1986).
  • Epstein SL, Misplon JA, Lawson CM, Subbarao EK, Connors M, Murphy BR. β2-microglobulin-deficient mice can be protected against influenza A infection by vaccination with vaccinia-influenza recombinants expressing hemagglutinin and neuraminidase. J. Immunol.150, 5484–5493 (1993).
  • Hoelscher MA, Singh N, Garg S et al. A broadly protective vaccine against globally dispersed clade 1 and clade 2 H5N1 influenza viruses. J. Infect. Dis.197(8), 1185–1188 (2008).
  • Wesley RD, Tang M, Lager KM. Protection of weaned pigs by vaccination with human adenovirus 5 recombinant viruses expressing the hemagglutinin and the nucleoprotein of H3N2 swine influenza virus. Vaccine22(25–26), 3427–3434 (2004).
  • Roy S, Kobinger GP, Lin J et al. Partial protection against H5N1 influenza in mice with a single dose of a chimpanzee adenovirus vector expressing nucleoprotein. Vaccine25(39–40), 6845–6851 (2007).
  • 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).
  • Ben-Yedidia T, Arnon R. Epitope-based vaccine against influenza. Expert Rev. Vaccines6(6), 939–948 (2007).

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