Influenza vaccines: T-cell responses deserve more attention

Expert Review of Vaccines

Volumn 11, Issue 8, 2012, Pages 949-962

  Schotsaert, Michael ^a,b   Saelens, Xavier ^a,b   Leroux Roels, Geert ^c  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c GHENT UNIVERSITY HOSPITAL   (Belgium)

Author keywords

cellular immunity; correlates of protection; cross protection; infection permissive; influenza; T lymphocyte

Indexed keywords

EPITOPE; INFLUENZA VACCINE; ISCOM; LIVE VACCINE; VIRUS ANTIBODY; VIRUS NUCLEOPROTEIN;

ADJUVANT THERAPY; ANTIBODY RESPONSE; ANTIGEN PRESENTATION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CROSS REACTION; CYTOTOXIC T LYMPHOCYTE; DISEASE MODEL; HUMAN; INFLUENZA; INFLUENZA VACCINATION; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H2N2; INFLUENZA VIRUS A H3N2; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; VIRUS IMMUNITY;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CROSS PROTECTION; CROSS REACTIONS; HEMAGGLUTINATION INHIBITION TESTS; HUMANS; IMMUNITY, CELLULAR; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS; INFLUENZA VACCINES; INFLUENZA, HUMAN; TIME FACTORS; VACCINES, ATTENUATED;

EID: 84866661827     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1586/erv.12.71     Document Type: Review

References (96)

1. Fiore AE, Uyeki TM, Broder K et al.; Centers for Disease Control and Prevention (CDC). Prevention and control of influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. MMWR. Recomm. Rep. 59(RR-8), 1-62 (2010).
2. Cox NJ, Subbarao K. Influenza. Lancet 354(9186), 1277-1282 (1999).
3. Belshe R, Lee MS, Walker RE, Stoddard J, Mendelman PM. Safety, immunogenicity and efficacy of intranasal, live attenuated influenza vaccine. Expert Rev. Vaccines 3(6), 643-654 (2004).
4. Belshe RB. The need for quadrivalent vaccine against seasonal influenza. Vaccine 28(Suppl. 4), D45-D53 (2010).
5. Doherty PC, Turner SJ, Webby RG, Thomas PG. Influenza and the challenge for immunology. Nat. Immunol. 7(5), 449-455 (2006).
6. Hobson D, Curry RL, Beare AS, Ward-Gardner A. The role of serum haemagglutination-inhibiting antibody in protection against challenge infection with influenza A2 and B viruses. J. Hyg. (Lond.) 70(4), 767-777 (1972).
7. Black S, Nicolay U, Vesikari T et al. Hemagglutination inhibition antibody titers as a correlate of protection for inactivated influenza vaccines in children. Pediatr. Infect. Dis. J. 30(12), 1081-1085 (2011).
8. Gravenstein S, Drinka P, Duthie EH et al. Efficacy of an influenza hemagglutinindiphtheria toxoid conjugate vaccine in elderly nursing home subjects during an influenza outbreak. J. Am. Geriatr. Soc. 42(3), 245-251 (1994).
9. Ohmit SE, Petrie JG, Cross RT, Johnson E, Monto AS. Influenza hemagglutinationinhibition antibody titer as a correlate of vaccine-induced protection. J. Infect. Dis. 204(12), 1879-1885 (2011).
10. McElhaney JE, Dutz JP. Better influenza vaccines for older people: what will it take? J. Infect. Dis. 198(5), 632-634 (2008).
11. Jordan WS Jr, Badger GF, Dingle JH. A study of illness in a group of Cleveland families. XVI. The epidemiology of influenza, 1948-1953. Am. J. Hygiene 68(2), 169-189 (1958).
12. 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).
13. 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(1), 81-88 (1985).
14. McMichael AJ, Gotch FM, Noble GR, Beare PA. Cytotoxic T-cell immunity to influenza. N. Engl. J. Med. 309(1), 13-17 (1983).
15. Wilkinson TM, Li CK, Chui CS et al. Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans. Nat. Med. 18(2), 274-280 (2012).
16. Hensley SE, Das SR, Gibbs JS et al. Influenza A virus hemagglutinin antibody escape promotes neuraminidase antigenic variation and drug resistance. PLoS ONE 6(2), e15190 (2011).
17. Boon AC, de Mutsert G, Graus YM 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).
18. Rimmelzwaan GF, Boon AC, Voeten JT, Berkhoff EG, Fouchier RA, Osterhaus AD. Sequence variation in the influenza A virus nucleoprotein associated with escape from cytotoxic T lymphocytes. Virus Res. 103(1-2), 97-100 (2004).
19. Gras S, Kedzierski L, Valkenburg SA et al. Cross-reactive CD8+ T-cell immunity between the pandemic H1N1-2009 and H1N1-1918 influenza A viruses. Proc. Natl Acad. Sci. USA 107(28), 12599-12604 (2010).
20. Smed-Sörensen A, Chalouni C, Chatterjee B et al. Influenza A virus infection of human primary dendritic cells impairs their ability to cross-present antigen to CD8 T cells. PLoS Pathog. 8(3), e1002572 (2012).
21. Gianfrani C, Oseroff C, Sidney J, Chesnut RW, Sette A. Human memory CTL response specific for influenza A virus is broad and multispecific. Hum. Immunol. 61(5), 438-452 (2000).
22. Gotch F, McMichael A, Smith G, Moss B. Identification of viral molecules recognized by influenza-specific human cytotoxic T lymphocytes. J. Exp. Med. 165(2), 408-416 (1987).
23. Jameson J, Cruz J, Ennis FA. Human cytotoxic T-lymphocyte repertoire to influenza A viruses. J. Virol. 72(11), 8682-8689 (1998).
24. 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).
25. Kreijtz JH, de Mutsert G, van Baalen CA, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Cross-recognition of avian H5N1 influenza virus by human cytotoxic T-lymphocyte populations directed to human influenza A virus. J. Virol. 82(11), 5161-5166 (2008).
26. 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).
27. Manicassamy B, Manicassamy S, Belicha-Villanueva A, Pisanelli G, Pulendran B, García-Sastre A. Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc. Natl Acad. Sci. USA 107(25), 11531-11536 (2010).
28. Dolan BP, Li L, Takeda K, Bennink JR, Yewdell JW. Defective ribosomal products are the major source of antigenic peptides endogenously generated from influenza A virus neuraminidase. J. Immunol. 184(3), 1419-1424 (2010).
29. Hillaire ML, van Trierum SE, Kreijtz JH et al. Cross-protective immunity against influenza pH1N1 2009 viruses induced by seasonal influenza A (H3N2) virus is mediated by virus-specific T-cells. J. Gen. Virol. 92(Pt 10), 2339-2349 (2011).
30. Kreijtz JH, Bodewes R, van Amerongen G et al. Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine 25(4), 612-620 (2007).
31. 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).
32. Yap KL, Ada GL, McKenzie IF. Transfer of specific cytotoxic T lymphocytes protects mice inoculated with influenza virus. Nature 273(5659), 238-239 (1978).
33. Christensen JP, Doherty PC, Branum KC, Riberdy JM. Profound protection against respiratory challenge with a lethal H7N7 influenza A virus by increasing the magnitude of CD8(+) T-cell memory. J. Virol. 74(24), 11690-11696 (2000).
34. Yetter RA, Barber WH, Small PA Jr. Heterotypic immunity to influenza in ferrets. Infect. Immun. 29(2), 650-653 (1980).
35. Bodewes R, Kreijtz JH, Geelhoed-Mieras MM et al. Vaccination against seasonal influenza A/H3N2 virus reduces the induction of heterosubtypic immunity against influenza A/H5N1 virus infection in ferrets. J. Virol. 85(6), 2695-2702 (2011).
36. Heinen PP, de Boer-Luijtze EA, Bianchi AT. Respiratory and systemic humoral and cellular immune responses of pigs to a heterosubtypic influenza A virus infection. J. Gen. Virol. 82(Pt 11), 2697-2707 (2001).
37. De Vleeschauwer A, Van Reeth K. Prior infection of pigs with swine influenza viruses is a barrier to infection with avian influenza viruses. Vet. Microbiol. 146(3-4), 340-345 (2010).
38. Van Reeth K, Braeckmans D, Cox E et al. Prior infection with an H1N1 swine influenza virus partially protects pigs against a low pathogenic H5N1 avian influenza virus. Vaccine 27(45), 6330-6339 (2009).
39. 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).
40. Saslaw S, Wilson HE. Reactions of monkeys to experimentally induced influenza virus A infection; an analysis of the relative rôles of humoral and cellular immunity under conditions of optimal or deficient nutrition. J. Exp. Med. 84, 113-125 (1946).
41. Weinfurter JT, Brunner K, Capuano SV 3rd et al. Cross-reactive T cells are involved in rapid clearance of 2009 pandemic H1N1 influenza virus in nonhuman primates. PLoS Pathog. 7(11), e1002381 (2011).
42. 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. USA 106(48), 20365-20370 (2009).
43. Khandaker G, Dierig A, Rashid H, King C, Heron L, Booy R. Systematic review of clinical and epidemiological features of the pandemic influenza A (H1N1) 2009. Influenza Other Respi. Viruses 5(3), 148-156 (2011).
44. 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).
45. de Bree GJ, van Leeuwen EM, Out TA, Jansen HM, Jonkers RE, van Lier RA. Selective accumulation of differentiated CD8+ T cells specific for respiratory viruses in the human lung. J. Exp. Med. 202(10), 1433-1442 (2005).
46. Brown DM, Dilzer AM, Meents DL, Swain SL. CD4 T cell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-two punch. J. Immunol. 177(5), 2888-2898 (2006).
47. 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(4), 1273-1282 (1994).
48. Belz GT, Wodarz D, Diaz G, Nowak MA, Doherty PC. Compromised influenza virus-specific CD8(+)-T-cell memory in CD4(+)-T-cell-deficient mice. J. Virol. 76(23), 12388-12393 (2002).
49. 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(4), 1114-1128 (1986).
50. Brincks EL, Katewa A, Kucaba TA, Griffith TS, Legge KL. CD8 T cells utilize TRAIL to control influenza virus infection. J. Immunol. 181(7), 4918-4925 (2008).
51. Topham DJ, Tripp RA, Doherty PC. CD8+ T cells clear influenza virus by perforin or Fas-dependent processes. J. Immunol. 159(11), 5197-5200 (1997).
52. Sun J, Madan R, Karp CL, Braciale TJ. Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat. Med. 15(3), 277-284 (2009).
53. Kohlmeier JE, Miller SC, Smith J et al. The chemokine receptor CCR5 plays a key role in the early memory CD8+ T-cell response to respiratory virus infections. Immunity 29(1), 101-113 (2008).
54. Takamura S, Roberts AD, Jelley-Gibbs DM, Wittmer ST, Kohlmeier JE, Woodland DL. The route of priming influences the ability of respiratory virus-specific memory CD8+ T cells to be activated by residual antigen. J. Exp. Med. 207(6), 1153-1160 (2010).
55. Williams MA, Bevan MJ. Effector and memory CTL differentiation. Annu. Rev. Immunol. 25, 171-192 (2007).
56. Kohlmeier JE, Reiley WW, Perona-Wright G et al. Inflammatory chemokine receptors regulate CD8(+) T-cell contraction and memory generation following infection. J. Exp. Med. 208(8), 1621-1634 (2011).
57. Gooskens J, Jonges M, Claas EC, Meijer A, Kroes AC. Prolonged influenza virus infection during lymphocytopenia and frequent detection of drug-resistant viruses. J. Infect. Dis. 199(10), 1435-1441 (2009).
58. Lee LY, Ha do LA, 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).
59. Yamada T. Poverty, wealth, and access to pandemic influenza vaccines. N. Engl. J. Med. 361(12), 1129-1131 (2009).
60. McMichael AJ, Gotch FM, Dongworth DW, Clark A, Potter CW. Declining T-cell immunity to influenza, 1977-82. Lancet 2(8353), 762-764 (1983).
61. Zinkernagel RM. On natural and artificial vaccinations. Annu. Rev. Immunol. 21, 515-546 (2003).
62. Olive C. Pattern recognition receptors: sentinels in innate immunity and targets of new vaccine adjuvants. Expert Rev. Vaccines 11(2), 237-256 (2012).
63. Leroux-Roels I, Leroux-Roels G. Current status and progress of prepandemic and pandemic influenza vaccine development. Expert Rev. Vaccines 8(4), 401-423 (2009).
64. Galli G, Medini D, Borgogni E et al. Adjuvanted H5N1 vaccine induces early CD4+ T-cell response that predicts long-term persistence of protective antibody levels. Proc. Natl Acad. Sci. USA 106(10), 3877-3882 (2009).
65. Moris P, van der Most R, Leroux-Roels I et al. H5N1 influenza vaccine formulated with AS03 A induces strong cross-reactive and polyfunctional CD4 T-cell responses. J. Clin. Immunol. 31(3), 443-454 (2011).
66. Roman F, Clément F, Dewé W et al. Effect on cellular and humoral immune responses of the AS03 adjuvant system in an A/H1N1/2009 influenza virus vaccine administered to adults during two randomized controlled trials. Clin. Vaccine Immunol. 18(5), 835-843 (2011).
67. Howard MK, Kistner O, Barrett PN. Pre-clinical development of cell culture (Vero)-derived H5N1 pandemic vaccines. Biol. Chem. 389(5), 569-577 (2008).
68. Ehrlich HJ, Müller M, Oh HM et al.; Baxter H5N1 Pandemic Influenza Vaccine Clinical Study Team. A clinical trial of a whole-virus H5N1 vaccine derived from cell culture. N. Engl. J. Med. 358(24), 2573-2584 (2008).
69. Crowe BA, Brühl P, Gerencer M et al. Evaluation of the cellular immune responses induced by a non-adjuvanted inactivated whole virus A/H5N1/VN/1203 pandemic influenza vaccine in humans. Vaccine 29(2), 166-173 (2010).
70. Kistner O, Howard MK, Spruth M et al. Cell culture (Vero) derived whole virus (H5N1) vaccine based on wild-type virus strain induces cross-protective immune responses. Vaccine 25(32), 6028-6036 (2007).
71. Tambyah PA, Wilder-Smith A, Pavlova BG et al. Safety and immunogenicity of two different doses of a Vero cell-derived, whole virus clade 2 H5N1 (A/Indonesia/05/2005) influenza vaccine. Vaccine 30(2), 329-335 (2012).
72. Brühl P, Kerschbaum A, Kistner O, Barrett N, Dorner F, Gerencer M. Humoral and cell-mediated immunity to vero cellderived influenza vaccine. Vaccine 19(9-10), 1149-1158 (2000).
73. Kistner O, Crowe BA, Wodal W et al. A whole virus pandemic influenza H1N1 vaccine is highly immunogenic and protective in active immunization and passive protection mouse models. PLoS ONE 5(2), e9349 (2010).
74. Nicholson KG, Tyrrell DA, Harrison P et al. Clinical studies of monovalent inactivated whole virus and subunit A/USSR/77 (H1N1) vaccine: serological responses and clinical reactions. J. Biol. Stand. 7(2), 123-136 (1979).
75. Wood JM. Developing vaccines against pandemic influenza. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 356(1416), 1953-1960 (2001).
76. Geeraedts F, Goutagny N, Hornung V et al. Superior immunogenicity of inactivated whole virus H5N1 influenza vaccine is primarily controlled by Toll-like receptor signalling. PLoS Pathog. 4(8), e1000138 (2008).
77. Basta S, Alatery A. The cross-priming pathway: a portrait of an intricate immune system. Scand. J. Immunol. 65(4), 311-319 (2007).
78. Rimmelzwaan GF, Nieuwkoop N, Brandenburg A et al. A randomized, double blind study in young healthy adults comparing cell mediated and humoral immune responses induced by influenza ISCOM vaccines and conventional vaccines. Vaccine 19(9-10), 1180-1187 (2000).
79. 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).
80. Hoft DF, Babusis E, Worku S et al. Live and inactivated influenza vaccines induce similar humoral responses, but only live vaccines induce diverse T-cell responses in young children. J. Infect. Dis. 204(6), 845-853 (2011).
81. Sutter G, Staib C. Vaccinia vectors as candidate vaccines: the development of modified vaccinia virus Ankara for antigen delivery. Curr. Drug Targets. Infect. Disord. 3(3), 263-271 (2003).
82. Kreijtz JH, Suezer Y, de Mutsert G et al. Recombinant modified vaccinia virus Ankara expressing the hemagglutinin gene confers protection against homologous and heterologous H5N1 influenza virus infections in macaques. J. Infect. Dis. 199(3), 405-413 (2009).
83. Kreijtz JH, Süzer Y, Bodewes R et al. Evaluation of a modified vaccinia virus Ankara (MVA)-based candidate pandemic influenza A/H1N1 vaccine in the ferret model. J. Gen. Virol. 91(Pt 11), 2745-2752 (2010).
84. Berthoud TK, Hamill M, Lillie PJ et al. Potent CD8+ T-cell immunogenicity in humans of a novel heterosubtypic influenza A vaccine, MVA-NP+M1. Clin. Infect. Dis. 52(1), 1-7 (2011).
85. 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).
86. Day EB, Zeng W, Doherty PC, Jackson DC, Kedzierska K, Turner SJ. The context of epitope presentation can influence functional quality of recalled influenza A virus-specific memory CD8+ T cells. J. Immunol. 179(4), 2187-2194 (2007).
87. Ledgerwood JE, Wei CJ, Hu Z et al.; VRC 306 Study Team. DNA priming and influenza vaccine immunogenicity: two phase 1 open label randomised clinical trials. Lancet Infect. Dis. 11(12), 916-924 (2011).
88. Kovácová A, Ruttkay-Nedecký G, Haverlík IK, Janecek S. Sequence similarities and evolutionary relationships of influenza virus A hemagglutinins. Virus Genes 24(1), 57-63 (2002).
89. Bodewes R, Kreijtz JH, 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 ONE 4(5), e5538 (2009).
90. Bodewes R, Kreijtz JH, Rimmelzwaan GF. Yearly influenza vaccinations: a doubleedged sword? Lancet Infect. Dis. 9(12), 784-788 (2009).
91. Valkenburg SA, Venturi V, Dang TH et al. Early priming minimizes the age-related immune compromise of CD8+ T-cell diversity and function. PLoS Pathog. 8(2), e1002544 (2012).
92. Deroo T, Jou WM, Fiers W. Recombinant neuraminidase vaccine protects against lethal influenza. Vaccine 14(6), 561-569 (1996).
93. Kilbourne ED, Couch RB, Kasel JA et al. Purified influenza A virus N2 neuraminidase vaccine is immunogenic and non-toxic in humans. Vaccine 13(18), 1799-1803 (1995).
94. 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).
95. Ogra PL, Chow T, Beutner KR et al. Clinical and immunologic evaluation of neuraminidase-specific influenza A virus vaccine in humans. J. Infect. Dis. 135(4), 499-506 (1977).
96. Schotsaert M, De Filette M, Fiers W, Saelens X. Universal M2 ectodomain-based influenza A vaccines: preclinical and clinical developments. Expert Rev. Vaccines 8(4), 499-508 (2009).