Cross-protective immunity to influenza A viruses

Expert Review of Vaccines

Volumn 9, Issue 11, 2010, Pages 1325-1341

  Epstein, Suzanne L ^a   Price, Graeme E ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

animal models; conserved antigens; cross protection; heterosubtypic immunity; human; influenza; pandemic; subtypes; universal vaccine; vaccine

Indexed keywords

DNA VACCINE; HYBRID PROTEIN; INFLUENZA VACCINE; LIVE VACCINE; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY C179; PEPTIDE VACCINE; RECOMBINANT VACCINE; UNCLASSIFIED DRUG; VAX 102; VIRUS VECTOR;

ADAPTIVE IMMUNITY; ANTIBODY RESPONSE; ANTIGEN SPECIFICITY; ANTIVIRAL ACTIVITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CROSS PROTECTIVE IMMUNITY; CYTOKINE RELEASE; DRUG DESIGN; DRUG EFFICACY; HUMAN; INFECTION PREVENTION; INFECTION SENSITIVITY; INFLUENZA; INFLUENZA VACCINATION; INFLUENZA VIRUS A; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H2N2; INFLUENZA VIRUS A H3N2; INFLUENZA VIRUS A H5N1; MEMORY T LYMPHOCYTE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SINGLE DRUG DOSE; VACCINE PRODUCTION; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS SHEDDING; VIRUS TRANSMISSION;

ANIMALS; CROSS PROTECTION; DISEASE MODELS, ANIMAL; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN;

EID: 78649344230     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.10.123     Document Type: Review

References (166)

1. Cox NJ, Kawaoka Y. Orthomyxoviruses: infuenza. In: Topley and Wilson's Microbiology and Microbial Infections. Collier L, Balows A, Sussman M (Eds). Arnold, London, UK, 385-433 (1998).
2. Lamb RA, Krug RM. Orthomyxoviradae; the viruses and their replication. In: Virology. Knipe DM, Howley PM, Griffn DE et al. (Eds). Lippincott Williams & Wilkins, PA, USA, 1487-1503 (2001).
3. Matrosovich MN, Klenk HD, Kawaoka Y. Receptor specifcity, host-range, and pathogenicity of infuenza viruses. In: Infuenza Virology: Current Topics. Kawaoka Y (Eds). Caister Academic Press, Wymondham, UK, 95-137 (2006).
4. Chen WS, Calvo PA, Malide D et al. A novel infuenza A virus mitochondrial protein that induces cell death. Nat. Med. 7(12), 1306-1312 (2001).
5. Kilbourne ED, Smith C, Brett I, Pokorny BA, Johansson B, Cox N. The total infuenza 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. USA 99(16), 10748-10752 (2002).
6. Hancock K, Veguilla V, Lu X et al. Cross-reactive antibody responses to the 2009 pandemic H1N1 infuenza virus. N. Engl. J. Med. 361(20), 1945-1952 (2009).
7. Treanor JJ, Wilkinson BE, Masseoud F et al. Safety and immunogenicity of a recombinant hemagglutinin vaccine for H5 infuenza in humans. Vaccine 19(13-14), 1732-1737 (2001).
8. Epstein SL. Control of infuenza virus infection by immunity to conserved viral features. Expert Rev. Anti Infect. Ther. 1(4), 627-638 (2003).
9. Tamura S, Tanimoto T, Kurata T. Mechanisms of broad cross-protection provided by infuenza virus infection and their application to vaccines. Jpn J. Infect. Dis. 58(4), 195-207 (2005).
10. Carrat F, Flahault A. Infuenza vaccine: the challenge of antigenic drift. Vaccine 25(39-40), 6852-6862 (2007).
11. Rimmelzwaan GF, Fouchier RA, Osterhaus AD. Infuenza virus-specifc cytotoxic T lymphocytes: a correlate of protection and a basis for vaccine development. Curr. Opin. Biotechnol. 18(6), 529-536 (2007).
12. Grebe KM, Yewdell JW, Bennink JR. Heterosubtypic immunity to infuenza A virus: where do we stand? Microb. Infect. 10(9), 1024-1029 (2008).
13. Tripp RA, Tompkins SM. Recombinant vaccines for infuenza virus. Curr. Opin Invest. Drugs 9(8), 836-845 (2008).
14. Brown LE, Kelso A. Prospects for an infuenza vaccine that induces cross-protective cytotoxic T lymphocytes. Immunol. Cell Biol. 87(4), 300-308 (2009)
15. Schulman JL, Kilbourne ED. Induction of partial specifc heterotypic immunity in mice by a single infection with infuenza A virus. J. Bacteriol. 89, 170-174 (1965).
16. Yetter RA, Lehrer S, Ramphal R, Small PA Jr. Outcome of infuenza infection: effect of site of initial infection and heterotypic immunity. Infect. Immun. 29, 654-662 (1980).
17. Kreijtz JHCM, Bodewes R, van den Brand JMA et al. Infection of mice with a human infuenza A/H3N2 virus induces protective immunity against lethal infection with infuenza A/H5N1 virus. Vaccine 27(36), 4983-4989 (2009).
18. + T cells in primary and secondary infuenza pneumonia. Immunity 8, 683-691 (1998).
19. Sweet C, Fenton RJ, Price GE. The ferret as an animal model of infuenza 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).
20. Smith H, Sweet C. Lessons for human infuenza from pathogenicity studies with ferrets. Rev. Infect. Dis. 10(1), 56-75 (1988).
21. Yetter RA, Barber WH, Small PA Jr. Heterotypic immunity to infuenza in ferrets. Infect. Immun. 29, 650-653 (1980).
22. McLaren C, Potter CW Immunity to infuenza in ferrets. VII. Effect of previous infection with heterotypic and heterologous infuenza viruses on the response of ferrets to inactivated infuenza virus vaccines. J. Hyg (Lond.) 72(1), 91-100 (1974).
23. Steel J, Staeheli P, Mubareka S, Garcia-Sastre A, Palese P, Lowen AC. Transmission of pandemic H1N1 infuenza virus and impact of prior exposure to seasonal strains or interferon treatment. J. Virol. 84(1), 21-26 (2010).
24. Straight TM, Ottolini MG, Prince GA, Eichelberger MC. Evidence of a cross-protective immune response to infuenza A in the cotton rat model. Vaccine 24(37-39), 6264-6271 (2006).
25. Heinen PP, de Boer-Luijtze EA, Bianchi ATJ. Respiratory and systemic humoral and cellular immune responses of pigs to a heterosubtypic infuenza A virus infection. J. Gen. Virol. 82, 2697-2707 (2001).
26. Seo SH, Webster RG. Cross-reactive, cell-mediated immunity and protection of chickens from lethal H5N1 infuenza virus infection in Hong Kong poultry markets. J. Virol. 75(6), 2516-2525 (2001).
27. Fereidouni SR, Starick E, Beer M et al Highly pathogenic avian infuenza virus infection of mallards with homo-and heterosubtypic immunity induced by low pathogenic avian infuenza viruses. PLoS ONE 4(8), e6706 (2009).
28. Liang S, Mozdzanowska K, Palladino G, Gerhard W Heterosubtypic immunity to infuenza type A virus in mice: effector mechanisms and their longevity J. Immunol. 152, 1653-1661 (1994).
29. + T cells clear infuenza virus by perforin or Fas dependent processes. J. Immunol. 159, 5197-5200 (1997).
30. Trapani JA, Smyth MJ. Functional signifcance of the perforin/granzyme cell death pathway. Nat. Rev. Immunol. 2(10), 735-747 (2002).
31. Furuya Y, Chan J, Regner M et al Cytotoxic T cells are the predominant players providing cross-protective immunity induced by y-irradiated infuenza A viruses. J. Virol. 84(9), 4212-4221 (2010).
32. Bot A, Bot S, Bona CA. Protective role of y interferon during the recall response to infuenza virus. J. Virol. 72(8), 6637-6645 (1998).
33. Nguyen HH, van Ginkel FW, Vu HL, Novak MJ, McGhee JR, Mestecky J. y interferon is not required for mucosal cytotoxic T-lymphocyte responses or heterosubtypic immunity to infuenza A virus infection in mice. J. Virol. 74(12), 5495-5501 (2000).
34. + cytotoxic T lymphocytes. J. Infect. Dis. 183(3), 368-376 (2001).
35. Epstein SL, Lo C-Y, Misplon JA, Bennink JR. Mechanism of protective immunity against infuenza virus infection in mice without antibodies. J. Immunol. 160(1), 322-327 (1998).
36. Benton KA, Misplon JA, Lo C-Y, Brutkiewicz RR, Prasad SA, Epstein SL. Heterosubtypic immunity to infuenza A virus in mice lacking either IgA, all Ig, NKT cells or g/d T cells. J. Immunol. 166, 7437-7445 (2001).
37. Graham MB, Braciale TJ. Resistance to and recovery from lethal infuenza virus infection in B lymphocyte-defcient mice. J. Exp. Med. 186(12), 2063-2068 (1997).
38. + T cells is ineffcient in the absence of B cells. J. Virol. 72(1), 882-885 (1998).
39. + CTL against infuenza-sensitized autologous splenocytes. Immunol. Lett. 46, 67-73 (1995).
40. -/- respiratory epithelium. J. Virol. 70, 1288-1291 (1996).
41. Brown DM, Dilzer AM, Meents DL, Swain SL. CD4 T cell-mediated protection from lethal infuenza: perforin and antibody-mediated mechanisms a one-two punch. J. Immunol. 177(5), 2888-2898 (2006).
42. + T helper type 2 T lymphocytes do not promote recovery from experimental virus infection. J. Exp. Med. 180, 1273-1282 (1994).
43. Scherle PA, Gerhard W. Functional analysis of infuenza-specifc helper T cell clones in vivo. T cells specifc for internal viral proteins provide cognate help for B cell responses to hemagglutinin. J. Exp. Med. 164, 1114-1128 (1986).
44. Russell SM, Liew FY. T cells primed by infuenza virion internal components can cooperate in the antibody response to haemagglutinin. Nature 280(5718), 147-148 (1979).
45. Mbawuike IN, Six HR, Cate TR, Couch RB. Vaccination with inactivated infuenza A virus during pregnancy protects neonatal mice against lethal challenge by infuenza A viruses representing three subtypes. J. Virol. 64, 1370-1374 (1990).
46. Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W. A universal infuenza A vaccine based on the extracellular domain of the M2 protein. Nat. Med. 5(10), 1157-1163 (1999).
47. Fan J, Liang X, Horton MS et al. Preclinical study of infuenza virus A M2 peptide conjugate vaccines in mice, ferrets, and rhesus monkeys. Vaccine 22(23-24), 2993-3003 (2004).
48. Tompkins SM, Zhao ZS, Lo C-Y et al. Matrix protein 2 vaccination and protection against infuenza viruses, including subtype H5N1. Emerg. Infect. Dis. 13(3), 426-435 (2007).
49. Epstein SL, Lo C-Y, Misplon JA et al. Mechanisms of heterosubtypic immunity to lethal infuenza A virus infection in immunocompetent, T cell-depleted, b2-microglobulin-defcient, and J chain-defcient mice. J. Immunol. 158, 1222-1230 (1997).
50. Tumpey TM, Renshaw M, Clements JD, Katz JM. Mucosal delivery of inactivated infuenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal infuenza A H5N1 virus infection. J. Virol. 75(11), 5141-5150 (2001).
51. Fazekas de St Groth S, Donnelley M. Studies in experimental immunology of infuenza. I V. The protective value of active immunization. Aust. J. Exp. Biol. Med. Sci. 28, 61-75 (1950).
52. Takada A, Kuboki N, Okazaki K et al. Avirulent avian infuenza virus as a vaccine strain against a potential human pandemic. J. Virol. 73(10), 8303-8307 (1999).
53. 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 infuenza A virus infection in mice. Vaccine 21(23), 3212-3218 (2003).
54. Quan FS, Compans RW, Nguyen HH, Kang SM. Induction of heterosubtypic immunity to infuenza virus by intranasal immunization. J. Virol. 82(3), 1350-1359 (2008).
55. Baumgarth N, Kelso A. Functionally distinct T cells in three compartments of the respiratory tract after infuenza virus infection. Eur. J. Immunol. 26(9), 2189-2197 (1996).
56. + cytotoxic T lymphocyte responses induced in mucosa-associated tissues. Virology 254, 50-60 (1999).
57. + T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 166(3), 1813-1822 (2001).
58. Price GE, Soboleski MR, Lo CY et al Vaccination focusing immunity on conserved antigens protects mice and ferrets against virulent H1N1 and H5N1 infuenza A viruses. Vaccine 27(47), 6512-6521 (2009).
59. + memory T cells. J. Exp. Med. 186(6), 859-865 (1997).
60. 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. USA 101(43), 15440-15445 (2004).
61. + T cells for long-term pulmonary protection against infuenza. Eur. J. Immunol. 36(3), 770-778 (2006).
62. Tamura S, Hasegawa H, Kurata T. Estimation of the effective doses of nasal-inactivated infuenza vaccine in humans from mouse-model experiments. Jpn J. Infect. Dis. 63(1), 8-15 (2010).
63. Yoshikawa T, Suzuki Y, Nomoto A, Sata T, Kurata T, Tamura S. Antibody responses and protection against infuenza virus infection in different congenic strains of mice immunized intranasally with adjuvant-combined A/Beijing/262/95 (H1N1) virus hemagglutinin or neuraminidase. Vaccine 21(1-2), 60-66 (2002).
64. Misplon JA, Lo CY, Gabbard JD, Tompkins SM, Epstein SL. Genetic control of immune responses to infuenza A matrix 2 protein (M2). Vaccine 28(36), 5817-5827 (2010).
65. Hennessy AV, Davenport FM, Horton RJM, Napier JA, Francis T Jr. Asian infuenza: occurrence and recurrence, a community and family study. Mil. Med. 129, 38-50 (1964).
66. Slepushkin AN. The effect of a previous attack of A1 infuenza on susceptibility to A2 virus during the 1957 outbreak. Bull. World Health Organ. 20, 297-301 (1959).
67. Epstein SL. Prior H1N1 infuenza 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).
68. Steinhoff MC, Fries LF, Karron RA, Clements ML, Murphy BR. Effect of heterosubtypic immunity on infection with attenuated infuenza-A virus vaccines in young children. J. Clin. Microbiol. 31(4), 836-838 (1993).
69. Frank AL, Taber LH, Wells JM. Individuals infected with two subtypes of infuenza A virus in the same season. J. Infect. Dis. 147, 120-124 (1983).
70. 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 infuenza viruses. J. Infect. Dis. 151, 81-88 (1985).
71. Carrat F, Vergu E, Ferguson NM et al. Time lines of infection and disease in human infuenza: a review of volunteer challenge studies. Am. J. Epidemiol. 167(7), 775-785 (2008).
72. McMichael AJ, Gotch FM, Noble GR, Beare PA. Cytotoxic T-cell immunity to infuenza. N. Engl. J. Med. 309, 13-17 (1983).
73. 2) virus in man. J. Infect. Dis. 128(4), 479-487 (1973).
74. McMichael AJ, Dongworth DW, Gotch FM, Clark A, Potter CW. Declining T-cell immunity to infuenza, 1977-1982. Lancet 2(8353), 762-764 (1983).
75. Lee LY, Ha DLA, Simmons C et al. Memory T cells established by seasonal human infuenza A infection cross-react with avian infuenza A (H5N1) in healthy individuals. J. Clin. Invest. 118(10), 3478-3490 (2008).
76. + T cells directed against H5N1 infuenza virus. J. Immunol. 180(3), 1758-1768 (2008).
77. Greenbaum JA, Kotturi MF, Kim Y et al. Pre-existing immunity against swine-origin H1N1 infuenza viruses in the general human population. Proc. Natl Acad. Sci. USA 106(48), 20365-20370 (2009).
78. Ge X, Tan V, Bollyky PL, Standifer NE, James EA, Kwok WW. Assessment of seasonal infuenza A virus-specifc CD4 T-cell responses to 2009 pandemic H1N1 swine-origin infuenza A virus. J. Virol 84(7), 3312-3319 (2010).
79. Alexander J, Bilsel P, del Guercio MF et al. Identifcation of broad binding class I HLA supertype epitopes to provide universal coverage of infuenza A virus. Hum. Immunol. 71, 468-474 (2010).
80. Rao SS, Kong WP, Wei CJ et al. Comparative effcacy of hemagglutinin, nucleoprotein, and matrix 2 protein gene-based vaccination against H5N1 infuenza in mouse and ferret. PLoS ONE 5(3), e9812 (2010).
81. Price GE, Soboleski MR, Lo C-Y et al. Single-dose mucosal immunization with a candidate universal infuenza vaccine provides rapid protection from virulent H5N1, H3N2 and H1N1 viruses. PLoS ONE 5(10), e13162 (2010).
82. Lo C-Y, Wu Z, Misplon JA et al. Comparison of vaccines for induction of heterosubtypic immunity to infuenza A virus: cold-adapted vaccine versus DNA prime-adenovirus boost strategies. Vaccine 26(17), 2062-2072 (2008).
83. Barefoot B, Thornburg NJ, Barouch DH et al. Comparison of multiple vaccine vectors in a single heterologous prime-boost trial. Vaccine 26(48), 6108-6118 (2008).
84. Belshe RB, Edwards KM, Vesikari T et al. Live attenuated versus inactivated infuenza vaccine in infants and young children. N. Engl. J. Med. 356(7), 685-696 (2007).
85. Monto AS, Ohmit SE, Petrie JG et al. Comparative effcacy of inactivated and live attenuated infuenza vaccines. N. Engl. J. Med. 361(13), 1260-1267 (2009).
86. 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).
87. Taylor PM, Davey J, Howland K, Rothbard JB, Askonas BA. Class I MHC molecules rather than other mouse genes dictate infuenza epitope recognition by cytotoxic T cells. Immunogenetics 26, 267-272 (1987).
88. Brett SJ, Blau J, Hughes-Jenkins CM, Rhodes J, Liew FY, Tite JP. Human T cell recognition of infuenza A nucleoprotein-specifcity and genetic restriction of immunodominant T helper cell epitopes. J. Immunol. 147(3), 984-991 (1991).
89. Ulmer JB, Donnelly JJ, Parker SE et al. Heterologous protection against infuenza by injection of DNA encoding a viral protein. Science 259, 1745-1749 (1993).
90. Robinson HL, Boyle CA, Feltquate DM, Morin MJ, Santoro JC, Webster RG. DNA immunization for infuenza virus: studies using hemagglutinin-and nucleoprotein-expressing DNAs. J. Infect. Dis. S50-S55 (1997).
91. Cox RJ, Mykkeltvedt E, Robertson J, Haaheim LR. Non-lethal viral challenge of infuenza haemagglutinin and nucleoprotein DNA vaccinated mice results in reduced viral replication. Scand. J. Immunol. 55(1), 14-23 (2002).
92. Epstein SL, Kong W P, Misplon JA et al. Protection against multiple infuenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine 23(46-47), 5404-5410 (2005).
93. Yewdell JW, Hackett CJ. Specifcity and function of T lymphocytes induced by infuenza A viruses. In: The Infuenza Viruses. Krug RM (Eds). Plenum Publishing Corp., NY, USA, 361-429 (1989).
94. Crowe SR, Miller SC, Shenyo RM, Woodland DL. Vaccination with an acidic polymerase, epitope of infuenza virus elicits a potent antiviral T cell response but delayed clearance of an infuenza virus challenge. J. Immunol. 174(2), 696-701 (2005).
95. Matsui M, Kohyama S, Suda T et al. A CTL-based liposomal vaccine capable of inducing protection against heterosubtypic infuenza viruses in HLA-A*0201 transgenic mice. Biochem. Biophys. Res. Commun. 391(3), 1494-1499 (2010).
96. Draper SJ, Heeney JL. Viruses as vaccine vectors for infectious diseases and cancer. Nat. Rev. Micro. 8(1), 62-73 (2010).
97. Jameson J, Cruz J, Ennis FA. Human cytotoxic T-lymphocyte repertoire to infuenza A viruses. J. Virol. 72(11), 8682-8689 (1998).
98. Gianfrani C, Oseroff C, Sidney J, Chesnut RW, Sette A. Human memory CTL response specifc for infuenza A virus is broad and multispecifc. Human Immunol. 61, 438-452 (2000).
99. Liu WL, Zou P, Chen YH. Monoclonal antibodies recognizing EVETPIRN epitope of infuenza A virus M2 protein could protect mice from lethal infuenza A virus challenge. Immunol. Lett. 93(2-3), 131-136 (2004).
100. Zou P, Liu WL, Chen YH. The epitope recognized by a monoclonal antibody in infuenza A virus M2 protein is immunogenic and confers immune protection. Int. Immunopharmacol. 5(4), 631-635 (2005).
101. Smirnov YA, Lipatov AS, Gitelman AK et al. An epitope shared by the hemagglutinins of H1, H2, H5, and H6 subtypes of infuenza A virus. Acta Virologica 43(4), 237-244 (1999).
102. Okuno Y, Isegawa Y, Sasao F, Ueda S. A common neutralizing epitope conserved between the hemagglutinins of infuenza A virus H1 and H2 strains. J. Virol. 67, 2552-2558 (1993).
103. + memory B cells. PLoS ONE 3(12), e3942 (2008).
104. Zebedee SL, Lamb RA. Infuenza A virus M2 protein: monoclonal antibody restriction of virus growth and detection of M2 in virions. J. Virol. 62(8), 2762-2772 (1988).
105. Liu WL, Zou P, Ding J, Lu Y, Chen YH. Sequence comparison between the extracellular domain of M2 protein human and avian infuenza A virus provides new information for bivalent infuenza vaccine design. Microb. Infect. 7(2), 171-177 (2005).
106. Sui JH, Hwang WC, Perez S et al. Structural and functional bases for broad-spectrum neutralization of avian and human infuenza A viruses. Nat. Struct. Mol. Biol. 16(3), 265-273 (2009).
107. Corti D, Suguitan AL Jr, Pinna D et al. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal infuenza vaccine. J. Clin. Invest. 120(5), 1663-1673 (2010).
108. Steel J, Lowen AC, Wang TT et al. Infuenza virus vaccine based on the conserved hemagglutinin stalk domain. mBio 1(1), e00018-10 (2010).
109. Bommakanti G, Citron MP, Hepler RW et al. Design of an HA2-based Escherichia coli expressed infuenza immunogen that protects mice from pathogenic challenge. Proc. Natl Acad. Sci. USA 107(31), 13701-13706 (2010).
110. Ekiert DC, Bhabha G, Elsliger MA et al. Antibody recognition of a highly conserved infuenza virus epitope. Science 324(5924), 246-251 (2009).
111. Heiny AT, Miotto O, Srinivasan KN et al. Evolutionarily conserved protein sequences of infuenza A viruses, avian and human, as vaccine targets. PLoS ONE 2(11), e1190 (2007).
112. Assarsson E, Bui HH, Sidney J et al. Immunomic analysis of the repertoire of T-cell specifcities for infuenza A virus in humans. J. Virol. 82(24), 12241-12251 (2008).
113. + T cell epitopes protects against lethal viral challenge in HLA-DR transgenic mice. Vaccine 28(3), 664-672 (2010).
114. + T-cell responses to internal proteins, hemagglutinins, and neuraminidases. Human Immunol. 70(9), 711-721 (2009).
115. Stoloff GA, Caparros-Wanderley W. Synthetic multi-epitope peptides identifed in silico induce protective immunity against multiple infuenza serotypes. Eur. J. Immunol. 37(9), 2441-2449 (2007).
116. Bui HH, Peters B, Assarsson E, Mbawuike I, Sette A. Ab and T cell epitopes of infuenza A virus, knowledge and opportunities. Proc. Natl Acad. Sci. USA 104(1), 246-251 (2007).
117. + IFN-y and Th lymphocyte responses: evaluation of multiepitope polypeptides as a mode for vaccine delivery. J. Immunol. 168(12), 6189-6198 (2002).
118. Fomsgaard A, Nielsen HV, Kirkby N et al. Induction of cytotoxic T-cell responses by gene gun DNA vaccination with minigenes encoding infuenza A virus HA and NP CTL-epitopes. Vaccine 18(7-8), 681-691 (1999).
119. Levi R, Arnon R. Synthetic recombinant infuenza vaccine induces effcient long-term immunity and cross-strain protection. Vaccine 14, 85-92 (1996).
120. Adar Y, Singer Y, Levi R et al. A universal epitope-based infuenza vaccine and its effcacy against H5N1. Vaccine 27(15), 2099-2107 (2009).
121. Boon ACM, de Mutsert G, Graus YMF et al. Sequence variation in a newly identifed HLA-B35-restricted epitope in the infuenza a virus nucleoprotein associated with escape from cytotoxic T lymphocytes. J. Virol. 76(5), 2567-2572 (2002).
122. Voeten JT, Bestebroer TM, Nieuwkoop NJ, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Antigenic drift in the infuenza A virus (H3N2) nucleoprotein and escape from recognition by cytotoxic T lymphocytes. J. Virol. 74(15), 6800-6807 (2000).
123. Price GE, Ou R, Jiang H, Huang L, Moskophidis D. Viral escape by selection of cytotoxic T cell-resistant variants in infuenza A virus pneumonia. J. Exp. Med. 191(11), 1853-1867 (2000).
124. Epstein SL, Tumpey TM, Misplon JA et al. DNA vaccine expressing conserved infuenza virus proteins protective against H5N1 challenge infection in mice. Emerg. Infect. Dis. 8(8), 796-801 (2002).
125. 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) infuenza virus. J. Infect. Dis. 197(12), 1643-1652 (2008).
126. Eichelberger M, Golding H, Hess M et al. FDA/NIH/WHO public workshop on immune correlates of protection against infuenza A viruses in support of pandemic vaccine development, Bethesda, Maryland, US, December 10-11, 2007. Vaccine 26(34), 4299-4303 (2008).
127. Murphy BR, Kasel JA, Chanock RM. Association of serum anti-neuraminidase antibody with resistance to infuenza in man. N. Engl. J. Med. 286, 1329-1332 (1972).
128. Murphy BR. Mucosal immunity to viruses. In: Mucosal Immunology. Elsevier Academic Press, MA, USA (1992).
129. Belshe RB, Gruber WC, Mendelman PM et al. Correlates of immune protection induced by live, attenuated, cold-adapted, trivalent, intranasal infuenza virus vaccine. J. Infect. Dis. 181(3), 1133-1137 (2000).
130. 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).
131. Forrest BD, Pride M W, Dunning AJ et al. Correlation of cellular immune responses with protection against culture-confrmed infuenza virus in young children. Clin. Vaccine Immunol. 15(7), 1042-1053 (2008).
132. Fiers W, De FM, El BK et al. M2e-based universal infuenza A vaccine. Vaccine 27(45), 6280-6283 (2009).
133. Smith LR, Wloch MK, Ye M et al. Phase 1 clinical trials of the safety and immunogenicity of adjuvanted plasmid DNA vaccines encoding infuenza A virus H5 hemagglutinin. Vaccine 28(13), 2565-2572 (2010).
134. Carrat F, Lavenu A, Cauchemez S, Deleger S. Repeated infuenza vaccination of healthy children and adults: borrow now, pay later? Epidemiol. Infect. 134(1), 63-70 (2006).
135. Bodewes R, Kreijtz JHCM, Baas C et al. Vaccination against human infuenza A/H3N2 virus prevents the induction of heterosubtypic immunity against lethal infection with avian infuenza A/H5N1 virus. PLoS ONE 4(5), e5538 (2009).
136. Bodewes R, Kreijtz JH, Rimmelzwaan GF. Yearly infuenza vaccinations: a double-edged sword? Lancet Infect. Dis. 9(12), 784-788 (2009).
137. Settembre EC, Dormitzer PR, Rappuoli R. H1N1: can a pandemic cycle be broken? Sci. Transl. Med. 2(24), 24ps14 (2010).
138. Alsharif M, Furuya Y, Bowden TR et al. Intranasal fu vaccine protective against seasonal and H5N1 avian infuenza infections. PLoS ONE 4(4), e5336 (2009).
139. Tannock GA, Paul JA, Barry RD. Relative immunogenicity of the cold-adapted infuenza 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).
140. Tannock GA, Paul JA. Homotypic and heterotypic immunity of infuenza 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).
141. Powell TJ, Strutt T, Reome J et al. Priming with cold-adapted infuenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J. Immunol. 178(2), 1030-1038 (2007).
142. Talon J, Salvatore M, O'Neill RE et al. Infuenza A and B viruses expressing altered NS1 proteins: a vaccine approach. Proc. Natl Acad. Sci. USA 97(8), 4309-4314 (2000).
143. Richt JA, Lekcharoensuk P, Lager KM et al. Vaccination of pigs against swine infuenza viruses by using an NS1-truncated modifed live-virus vaccine. J. Virol. 80(22), 11009-11018 (2006).
144. Liu T, Ye Z. Attenuating mutations of the matrix gene of infuenza A/WSN/33 virus. J. Virol. 79(3), 1918-1923 (2005).
145. Watanabe S, Watanabe T, Kawaoka Y. Infuenza A virus lacking M2 protein as a live attenuated vaccine. J. Virol. 83(11), 5947-5950 (2009).
146. Mozdzanowska K, Feng JQ, Eid M et al. Induction of infuenza type A virus-specifc resistance by immunization of mice with a synthetic multiple antigenic peptide vaccine that contains ectodomains of matrix protein 2. Vaccine 21(19-20), 2616-2626 (2003).
147. Deres K, Schild H, Wiesmüller KH, Jung G, Rammensee HG. In vivo priming of virus-specifc cytotoxic T lymphocytes with synthetic lipopeptide vaccine. Nature 342, 561-564 (1989).
148. Carragher DM, Kaminski DA, Moquin A, Hartson L, Randall TD. A novel role for non-neutralizing antibodies against nucleoprotein in facilitating resistance to infuenza virus. J. Immunol. 181(6), 4168-4176 (2008).
149. Tamura S, Miyata K, Matsuo K et al. Acceleration of infuenza 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).
150. Slepushkin VA, Katz JM, Black RA, Gamble WC, Rota PA, Cox NJ. Protection of mice against infuenza A virus challenge by vaccination with baculovirus-expressed M2 protein. Vaccine 13(15), 1399-1402 (1995).
151. Sui Z, Chen Q, Wu R et al. Cross-protection against infuenza virus infection by intranasal administration of M2-based vaccine with chitosan as an adjuvant. Arch Virol. 155(4), 535-544 (2010).
152. Frace AM, Klimov AI, Rowe T, Black RA, Katz JM. Modifed M2 proteins produce heterotypic immunity against infuenza A virus. Vaccine 17(18), 2237-2244 (1999).
153. Eliasson DG, Bakkouri KE, Schön K et al. CTA1-M2e-DD: a novel mucosal adjuvant targeted infuenza vaccine. Vaccine 26(9), 1243-1252 (2008).
154. De Filette M, Martens W, Roose K et al. An infuenza A vaccine based on tetrameric ectodomain of matrix protein 2. J. Biol. Chem. 283(17), 11382-11387 (2008).
155. 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 infuenza A virus M2 protein signifcantly enhances protective immunity. Vaccine 23(3), 366-371 (2004).
156. Mbawuike IN, Dillon SB, Demuth SG, Jones CS, Cate TR, Couch RB. Infuenza A subtype cross-protection after immunization of outbred mice with a purifed chimeric NS1/HA2 infuenza virus protein. Vaccine 12, 1340-1349 (1994).
157. Okuda K, Ihata A, Watabe S et al. Protective immunity against infuenza A virus induced by immunization with DNA plasmid containing infuenza M gene. Vaccine 19(27), 3681-3691 (2001).
158. Jimenez GS, Planchon R, Wei Q et al. Vaxfectin™-formulated infuenza DNA vaccines encoding NP and M2 viral proteins protect mice against lethal viral challenge. Hum. Vacc. 3(5), 157-164 (2007).
159. 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 infuenza virus. Virology 354(1), 48-57 (2006).
160. Andrew ME, Coupar BEH, Ada GL, Boyle DB. Cell-mediated immune responses to infuenza virus antigens expressed by vaccinia virus recombinants. Microbial. Pathog. 1, 443-452 (1986).
161. Epstein SL, Misplon JA, Lawson CM, Subbarao EK, Connors M, Murphy BR. b2-microglobulin-defcient mice can be protected against infuenza A infection by vaccination with vaccinia-infuenza recombinants expressing hemagglutinin and neuraminidase. J. Immunol. 150, 5484-5493 (1993).
162. Hoelscher MA, Singh N, Garg S et al. A broadly protective vaccine against globally dispersed clade 1 and clade 2 H5N1 infuenza viruses. J. Infect. Dis. 197(8), 1185-1188 (2008).
163. 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 infuenza virus. Vaccine 22(25-26), 3427-3434 (2004).
164. Roy S, Kobinger GP, Lin J et al. Partial protection against H5N1 infuenza in mice with a single dose of a chimpanzee adenovirus vector expressing nucleoprotein. Vaccine 25(39-40), 6845-6851 (2007).
165. De Filette M, Fiers W, Martens W et al. Improved design and intranasal delivery of an M2e-based human infuenza A vaccine. Vaccine 24(44-46), 6597-6601 (2006).
166. Ben-Yedidia T, Arnon R. Epitope-based vaccine against infuenza. Expert Rev. Vaccines 6(6), 939-948 (2007).