Cross-protective immune responses elicited by live attenuated influenza vaccines

Yonsei Medical Journal

Volumn 54, Issue 2, 2013, Pages 271-282

  Jang, Yo Han ^a   Seong, Baik Lin ^a,b  

^a Department of Biotechnology   (South Korea)

^b Yonsei University   (South Korea)

Author keywords

Cold adaptation; Cross protection; Influenza live attenuated vaccine; Universal vaccine

Indexed keywords

EPITOPE; HEMAGGLUTININ; IMMUNOGLOBULIN A ANTIBODY; INFLUENZA VACCINE; NEUTRALIZING ANTIBODY; SIALIDASE;

2009 H1N1 INFLUENZA; CROSS PROTECTION; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; NONHUMAN; REVIEW; VIRUS NEUTRALIZATION;

ADAPTIVE IMMUNITY; ANTIGENS, VIRAL; CROSS PROTECTION; GENOME, VIRAL; HUMANS; IMMUNITY, INNATE; INFLUENZA VACCINES; INFLUENZA, HUMAN; ORTHOMYXOVIRIDAE; VACCINES, ATTENUATED;

EID: 84873254941     PISSN: 05135796     EISSN: None     Source Type: Journal    
DOI: 10.3349/ymj.2013.54.2.271     Document Type: Review

References (94)

1. Englund JA, Champlin RE, Wyde PR, Kantarjian H, Atmar RL, Tarrand J, et al. Common emergence of amantadine-and rimantadine-resistant influenza A viruses in symptomatic immunocompromised adults. Clin Infect Dis 1998;26:1418-24.
2. de Jong MD, Tran TT, Truong HK, Vo MH, Smith GJ, Nguyen VC, et al. Oseltamivir resistance during treatment of influenza A (H5N1) infection. N Engl J Med 2005;353:2667-72.
3. Wiley DC, Wilson IA, Skehel JJ. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature 1981;289:373-8.
4. de Jong JC, Claas EC, Osterhaus AD, Webster RG, Lim WL. A pandemic warning? Nature 1997;389:554.
5. Claas EC, Osterhaus AD, van Beek R, De Jong JC, Rimmelzwaan GF, Senne DA, et al. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 1998;351:472-7.
6. Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, et al. Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 1998;279:393-6.
7. Herfst S, Schrauwen EJ, Linster M, Chutinimitkul S, de Wit E, Munster VJ, et al. Airborne transmission of influenza A/H5N1 virus between ferrets. Science 2012;336:1534-41.
8. Russell CA, Fonville JM, Brown AE, Burke DF, Smith DL, James SL, et al. The potential for respiratory droplet-transmissible A/H5N1 influenza virus to evolve in a mammalian host. Science 2012;336:1541-7.
9. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature 2012;486:420-8.
10. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009; 325:197-201.
11. Shinde V, Bridges CB, Uyeki TM, Shu B, Balish A, Xu X, et al. Triple-reassortant swine influenza A (H1) in humans in the United States, 2005-2009. N Engl J Med 2009;360:2616-25.
12. Octaviani CP, Ozawa M, Yamada S, Goto H, Kawaoka Y. High level of genetic compatibility between swine-origin H1N1 and highly pathogenic avian H5N1 influenza viruses. J Virol 2010;84: 10918-22.
13. Cline TD, Karlsson EA, Freiden P, Seufzer BJ, Rehg JE, Webby RJ, et al. Increased pathogenicity of a reassortant 2009 pandemic H1N1 influenza virus containing an H5N1 hemagglutinin. J Virol 2011;85:12262-70.
14. Welsh RM, Che JW, Brehm MA, Selin LK. Heterologous immunity between viruses. Immunol Rev 2010;235:244-66.
15. Bender BS, Croghan T, Zhang L, Small PA Jr. Transgenic mice lacking class I major histocompatibility complex-restricted T cells have delayed viral clearance and increased mortality after influenza virus challenge. J Exp Med 1992;175:1143-5.
16. Doherty PC. Cytotoxic T cell effector and memory function in viral immunity. Curr Top Microbiol Immunol 1996;206:1-14.
17. 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 2000;191:1853-67.
18. McMichael AJ, Gotch FM, Noble GR, Beare PA. Cytotoxic T-cell immunity to influenza. N Engl J Med 1983;309:13-7.
19. Selin LK, Vergilis K, Welsh RM, Nahill SR. Reduction of otherwise remarkably stable virus-specific cytotoxic T lymphocyte memory by heterologous viral infections. J Exp Med 1996;183: 2489-99.
20. Selin LK, Lin MY, Kraemer KA, Pardoll DM, Schneck JP, Varga SM, et al. Attrition of T cell memory: selective loss of LCMV epitope-specific memory CD8 T cells following infections with heterologous viruses. Immunity 1999;11:733-42.
21. Brehm MA, Pinto AK, Daniels KA, Schneck JP, Welsh RM, Selin LK. T cell immunodominance and maintenance of memory regulated by unexpectedly cross-reactive pathogens. Nat Immunol 2002;3:627-34.
22. Treanor JJ, Wilkinson BE, Masseoud F, Hu-Primmer J, Battaglia R, O'Brien D, et al. Safety and immunogenicity of a recombinant hemagglutinin vaccine for H5 influenza in humans. Vaccine 2001;19:1732-7.
23. Nicholson KG, Colegate AE, Podda A, Stephenson I, Wood J, Ypma E, et al. Safety and antigenicity of non-adjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a randomised trial of two potential vaccines against H5N1 influenza. Lancet 2001;357:1937-43.
24. Aymard M, Valette M, Lina B, Thouvenot D. Surveillance and impact of influenza in Europe. Groupe Regional d'Observation de la Grippe and European Influenza Surveillance Scheme. Vaccine 1999;17 Suppl 1:S30-41.
25. Klimov A, Simonsen L, Fukuda K, Cox N. Surveillance and impact of influenza in the United States. Vaccine 1999;17 Suppl 1:S42-6.
26. Steel J, Lowen AC, Wang TT, Yondola M, Gao Q, Haye K, et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain. MBio 2010;1. pii: e00018-10.
27. Ulmer JB, Fu TM, Deck RR, Friedman A, Guan L, DeWitt C, et al. Protective CD4+ and CD8+ T cells against influenza virus induced by vaccination with nucleoprotein DNA. J Virol 1998;72: 5648-53.
28. Fu TM, Guan L, Friedman A, Schofield TL, Ulmer JB, Liu MA, et al. Dose dependence of CTL precursor frequency induced by a DNA vaccine and correlation with protective immunity against influenza virus challenge. J Immunol 1999;162:4163-70.
29. Ulmer JB, Deck RR, Dewitt CM, Donnhly JI, Liu MA. Generation of MHC class I-restricted cytotoxic T lymphocytes by expression of a viral protein in muscle cells: antigen presentation by non-muscle cells. Immunology 1996;89:59-67.
30. Klinman DM, Takeno M, Ichino M, Gu M, Yamshchikov G, Mor G, et al. DNA vaccines: safety and efficacy issues. Springer Semin Immunopathol 1997;19:245-56.
31. + T cell immunity in children. J Virol 2011;85:11995-2000.
32. Bodewes R, Kreijtz JH, Baas C, Geelhoed-Mieras MM, de Mutsert G, van Amerongen G, 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 2009;4:e5538.
33. Bodewes R, Kreijtz JH, Geelhoed-Mieras MM, van Amerongen G, Verburgh RJ, van Trierum SE, 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 2011;85:2695-702.
34. Bodewes R, Kreijtz JH, Hillaire ML, Geelhoed-Mieras MM, Fouchier RA, Osterhaus AD, et al. Vaccination with whole inactivated virus vaccine affects the induction of heterosubtypic immunity against influenza virus A/H5N1 and immunodominance of virus-specific CD8+ T-cell responses in mice. J Gen Virol 2010;91(Pt 7):1743-53.
35. Suguitan AL Jr, McAuliffe J, Mills KL, Jin H, Duke G, Lu B, et al. Live, attenuated influenza A H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS Med 2006;3: e360.
36. Fan S, Gao Y, Shinya K, Li CK, Li Y, Shi J, et al. Immunogenicity and protective efficacy of a live attenuated H5N1 vaccine in nonhuman primates. PLoS Pathog 2009;5:e1000409.
37. Desheva JA, Lu XH, Rekstin AR, Rudenko LG, Swayne DE, Cox NJ, et al. Characterization of an influenza A H5N2 reassortant as a candidate for live-attenuated and inactivated vaccines against highly pathogenic H5N1 viruses with pandemic potential. Vaccine 2006;24:6859-66.
38. Chen GL, Min JY, Lamirande EW, Santos C, Jin H, Kemble G, et al. Comparison of a live attenuated 2009 H1N1 vaccine with seasonal influenza vaccines against 2009 pandemic H1N1 virus infection in mice and ferrets. J Infect Dis 2011;203:930-6.
39. Yang P, Duan Y, Wang C, Xing L, Gao X, Tang C, et al. Immunogenicity and protective efficacy of a live attenuated vaccine against the 2009 pandemic A H1N1 in mice and ferrets. Vaccine 2011;29:698-705.
40. Jang YH, Byun YH, Lee YJ, Lee YH, Lee KH, Seong BL. Cold-adapted pandemic 2009 H1N1 influenza virus live vaccine elicits cross-reactive immune responses against seasonal and H5 influenza A viruses. J Virol 2012;86:5953-8.
41. Murphy BR, Clements ML. The systemic and mucosal immune response of humans to influenza A virus. Curr Top Microbiol Immunol 1989;146:107-16.
42. 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 2001;75:5141-50.
43. Beyer WE, Palache AM, de Jong JC, Osterhaus AD. Cold-adapted live influenza vaccine versus inactivated vaccine: systemic vaccine reactions, local and systemic antibody response, and vaccine efficacy. A meta-analysis. Vaccine 2002;20:1340-53.
44. Powers DC, Fries LF, Murphy BR, Thumar B, Clements ML. In elderly persons live attenuated influenza A virus vaccines do not offer an advantage over inactivated virus vaccine in inducing serum or secretory antibodies or local immunologic memory. J Clin Microbiol 1991;29:498-505.
45. Hillaire ML, Osterhaus AD, Rimmelzwaan GF. Induction of virus-specific cytotoxic T lymphocytes as a basis for the development of broadly protective influenza vaccines. J Biomed Biotechnol 2011; 2011:939860.
46. Belshe RB, Gruber WC, Mendelman PM, Cho I, Reisinger K, Block SL, et al. Efficacy of vaccination with live attenuated, cold-adapted, trivalent, intranasal influenza virus vaccine against a variant (A/Sydney) not contained in the vaccine. J Pediatr 2000;136: 168-75.
47. Nichol KL, Mendelman PM, Mallon KP, Jackson LA, Gorse GJ, Belshe RB, et al. Effectiveness of live, attenuated intranasal influenza virus vaccine in healthy, working adults: a randomized controlled trial. JAMA 1999;282:137-44.
48. Clover RD, Crawford S, Glezen WP, Taber LH, Matson CC, Couch RB. Comparison of heterotypic protection against influenza A/Taiwan/86 (H1N1) by attenuated and inactivated vaccines to A/Chile/83-like viruses. J Infect Dis 1991;163:300-4.
49. Edwards KM, Dupont WD, Westrich MK, Plummer WD Jr, Palmer PS, Wright PF. A randomized controlled trial of cold-adapted and inactivated vaccines for the prevention of influenza A disease. J Infect Dis 1994;169:68-76.
50. Ohmit SE, Victor JC, Rotthoff JR, Teich ER, Truscon RK, Baum LL, et al. Prevention of antigenically drifted influenza by inactivated and live attenuated vaccines. N Engl J Med 2006;355:2513-22.
51. Belshe RB, Edwards KM, Vesikari T, Black SV, Walker RE, Hultquist M, et al. Live attenuated versus inactivated influenza vaccine in infants and young children. N Engl J Med 2007;356: 685-96.
52. Powell TJ, Strutt T, Reome J, Hollenbaugh JA, Roberts AD, Woodland DL, 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 2007; 178:1030-8.
53. Ding H, Tsai C, Zhou F, Buchy P, Deubel V, Zhou P. Heterosubtypic antibody response elicited with seasonal influenza vaccine correlates partial protection against highly pathogenic H5N1 virus. PLoS One 2011;6:e17821.
54. Sandbulte MR, Jimenez GS, Boon AC, Smith LR, Treanor JJ, Webby RJ. Cross-reactive neuraminidase antibodies afford partial protection against H5N1 in mice and are present in unexposed humans. PLoS Med 2007;4:e59.
55. van Maurik A, Sabarth N, Dacho HS, Brühl P, Schwendinger M, Crowe BA, et al. Seasonal influenza vaccine elicits heterosubtypic immunity against H5N1 that can be further boosted by H5N1 vaccination. Vaccine 2010;28:1778-85.
56. Shi J, Wen Z, Guo J, Zhang Y, Deng G, Shu Y, et al. Protective efficacy of an H1N1 cold-adapted live vaccine against the 2009 pandemic H1N1, seasonal H1N1, and H5N1 influenza viruses in mice. Antiviral Res 2012;93:346-53.
57. WHO/OIE/FAO H5N1 Evolution Working Group. Continued evolution of highly pathogenic avian influenza A (H5N1): updated nomenclature. Influenza Other Respi Viruses 2012;6:1-5.
58. WHO/OIE/FAO H5N1 Evolution Working Group. Continuing progress towards a unified nomenclature for the highly pathogenic H5N1 avian influenza viruses: divergence of clade 2.2 viruses. Influenza Other Respi Viruses 2009;3:59-62.
59. Gustin KM, Maines TR, Belser JA, van Hoeven N, Lu X, Dong L, et al. Comparative immunogenicity and cross-clade protective efficacy of mammalian cell-grown inactivated and live attenuated H5N1 reassortant vaccines in ferrets. J Infect Dis 2011;204:1491-9.
60. Chen Z, Wang W, Zhou H, Suguitan AL Jr, Shambaugh C, Kim L, et al. Generation of live attenuated novel influenza virus A/California/7/09 (H1N1) vaccines with high yield in embryonated chicken eggs. J Virol 2010;84:44-51.
61. Girard MP, Katz JM, Pervikov Y, Hombach J, Tam JS. Report of the 7th meeting on Evaluation of Pandemic Influenza Vaccines in Clinical Trials, World Health Organization, Geneva, 17-18 February 2011. Vaccine 2011;29:7579-86.
62. Chen GL, Lau YF, Lamirande EW, McCall AW, Subbarao K. Seasonal influenza infection and live vaccine prime for a response to the 2009 pandemic H1N1 vaccine. Proc Natl Acad Sci U S A 2011;108:1140-5.
63. Sun K, Ye J, Perez DR, Metzger DW. Seasonal FluMist vaccination induces cross-reactive T cell immunity against H1N1 (2009) influenza and secondary bacterial infections. J Immunol 2011; 186:987-93.
64. Qiu C, Huang Y, Wang Q, Tian D, Zhang W, Hu Y, et al. Boosting heterosubtypic neutralization antibodies in recipients of 2009 pandemic H1N1 influenza vaccine. Clin Infect Dis 2012;54:17-24.
65. Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, Morrissey M, et al. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 2011;208:181-93.
66. Jang YH, Seong BL. Principles underlying rational design of live attenuated influenza vaccines. Clin Exp Vaccin Res 2012;1:35-49.
67. Murphy KM, Travers P, Walport M, Janeway C. Janeway's Immunobiology. 7th ed. Garland Science; 2008.
68. Yewdell JW, Bennink JR, Smith GL, Moss B. Influenza A virus nucleoprotein is a major target antigen for cross-reactive anti-influenza A virus cytotoxic T lymphocytes. Proc Natl Acad Sci U S A 1985;82:1785-9.
69. Gotch F, McMichael A, Smith G, Moss B. Identification of viral molecules recognized by influenza-specific human cytotoxic T lymphocytes. J Exp Med 1987;165:408-16.
70. Tan PT, Khan AM, August JT. Highly conserved influenza A sequences as T cell epitopes-based vaccine targets to address the viral variability. Hum Vaccin 2011;7:402-9.
71. Gras S, Kedzierski L, Valkenburg SA, Laurie K, Liu YC, Denholm JT, et al. Cross-reactive CD8+ T-cell immunity between the pandemic H1N1-2009 and H1N1-1918 influenza A viruses. Proc Natl Acad Sci U S A 2010;107:12599-604.
72. Grandea AG 3rd, Olsen OA, Cox TC, Renshaw M, Hammond PW, Chan-Hui PY, et al. Human antibodies reveal a protective epitope that is highly conserved among human and nonhuman influenza A viruses. Proc Natl Acad Sci U S A 2010;107:12658-63.
73. Hendrickson BA, Conner DA, Ladd DJ, Kendall D, Casanova JE, Corthesy B, et al. Altered hepatic transport of immunoglobulin A in mice lacking the J chain. J Exp Med 1995;182:1905-11.
74. Niles MJ, Matsuuchi L, Koshland ME. Polymer IgM assembly and secretion in lymphoid and nonlymphoid cell lines: evidence that J chain is required for pentamer IgM synthesis. Proc Natl Acad Sci U S A 1995;92:2884-8.
75. Renegar KB, Jackson GD, Mestecky J. In vitro comparison of the biologic activities of monoclonal monomeric IgA, polymeric IgA, and secretory IgA. J Immunol 1998;160:1219-23.
76. 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 2008;181: 4168-76.
77. Rangel-Moreno J, Carragher DM, Misra RS, Kusser K, Hartson L, Moquin A, et al. B cells promote resistance to heterosubtypic strains of influenza via multiple mechanisms. J Immunol 2008; 180:454-63.
78. 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 2001;166:7381-8.
79. 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 2004;172:5598-605.
80. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M, Throsby M, et al. Antibody recognition of a highly conserved influenza virus epitope. Science 2009;324:246-51.
81. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science 2011;333:850-6.
82. Prabhu N, Prabakaran M, Ho HT, Velumani S, Qiang J, Goutama M, et al. Monoclonal antibodies against the fusion peptide of hemagglutinin protect mice from lethal influenza A virus H5N1 infection. J Virol 2009;83:2553-62.
83. Krause JC, Tsibane T, Tumpey TM, Huffman CJ, Basler CF, Crowe JE Jr. A broadly neutralizing human monoclonal antibody that recognizes a conserved, novel epitope on the globular head of the influenza H1N1 virus hemagglutinin. J Virol 2011;85:10905-8.
84. Whittle JR, Zhang R, Khurana S, King LR, Manischewitz J, Golding H, et al. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc Natl Acad Sci U S A 2011;108:14216-21.
85. Lingwood D, McTamney PM, Yassine HM, Whittle JR, Guo X, Boyington JC, et al. Structural and genetic basis for development of broadly neutralizing influenza antibodies. Nature 2012;489: 566-70.
86. Seo SU, Lee KH, Byun YH, Kweon MN, Seong BL. Immediate and broad-spectrum protection against heterologous and heterotypic lethal challenge in mice by live influenza vaccine. Vaccine 2007;25:8067-76.
87. Bodewes R, Kreijtz JH, Rimmelzwaan GF. Yearly influenza vaccinations: a double-edged sword? Lancet Infect Dis 2009;9:784-8.
88. Heikkinen T, Peltola V. Influenza vaccination of children. Lancet Infect Dis 2009;9:720-1.
89. Skowronski DM, De Serres G, Crowcroft NS, Janjua NZ, Boulianne N, Hottes TS, et al. Association between the 2008-09 seasonal influenza vaccine and pandemic H1N1 illness during Spring-Summer 2009: four observational studies from Canada. PLoS Med 2010;7:e1000258.
90. Yewdell JW, Bennink JR. Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses. Annu Rev Immunol 1999;17:51-88.
91. Haanen JB, Wolkers MC, Kruisbeek AM, Schumacher TN. Selective expansion of cross-reactive CD8(+) memory T cells by viral variants. J Exp Med 1999;190:1319-28.
92. Zhao ZS, Granucci F, Yeh L, Schaffer PA, Cantor H. Molecular mimicry by herpes simplex virus-type 1: autoimmune disease after viral infection. Science 1998;279:1344-7.
93. Tsunoda I, Kuang LQ, Kobayashi-Warren M, Fujinami RS. Central nervous system pathology caused by autoreactive CD8+ T-cell clones following virus infection. J Virol 2005;79:14640-6.
94. Chen AT, Cornberg M, Gras S, Guillonneau C, Rossjohn J, Trees A, et al. Loss of anti-viral immunity by infection with a virus encoding a cross-reactive pathogenic epitope. PLoS Pathog 2012;8: e1002633.