Prospects for Broadly Protective Influenza Vaccines

American Journal of Preventive Medicine

Volumn 49, Issue 6, 2015, Pages S355-S363

  Treanor, John Jay ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEMAGGLUTININ; IMMUNOLOGICAL ADJUVANT; INACTIVATED VACCINE; INFLUENZA VACCINE; SIALIDASE; VIRUS HEMAGGLUTININ; CD4 ANTIGEN; CD8 ANTIGEN; PHARMACEUTICAL VEHICLES AND ADDITIVES; VIRUS ENVELOPE PROTEIN; VIRUS VACCINE;

ANTIBODY BLOOD LEVEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY RESPONSE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; DEVELOPING COUNTRY; HUMAN; IMMUNE RESPONSE; IMMUNOGLOBULIN GENE; IMMUNOSUPPRESSIVE TREATMENT; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H5N1); INFLUENZA VIRUS; NONHUMAN; REVIEW; VACCINATION; VIRION; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS NEUTRALIZATION; HEMAGGLUTINATION; IMMUNOLOGY; INTRANASAL DRUG ADMINISTRATION;

ADJUVANTS, PHARMACEUTIC; ADMINISTRATION, INTRANASAL; ANTIGENS, CD4; ANTIGENS, CD8; HEMAGGLUTINATION; HEMAGGLUTININS; HUMANS; NEURAMINIDASE; VIRAL ENVELOPE PROTEINS; VIRAL VACCINES;

EID: 84951567527     PISSN: 07493797     EISSN: 18732607     Source Type: Journal    
DOI: 10.1016/j.amepre.2015.09.012     Document Type: Review

References (86)

1. C. Andrewes, W. Smith Influenza: experiments on the active immunisation of mice Br J Exp Path 18 1937 43
2. T. Francis Jr., J.E. Salk, H.E. Pearson, P.N. Brown Protective effect of vaccination against influenza Proc Soc Exp Biol Med 55 1944 104 105
3. E.D. Kilbourne, C. Smith, I. Brett, B.A. Pokorny, B. Johansson, N. Cox 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 USA 99 2002 10748 10752
4. [Erratum appears in Proc Natl Acad Sci USA. 2003 Jan 21;100(2):764]
5. E.D. Kilbourne, J.P. Loge Influenza A prime: a clinical study of an epidemic caused by a new strain of virus Ann Intern Med 33 1950 371 382
6. A. Reber, J. Katz Immunologic assessment of influenza vaccines and immune correlates of protection Expert Rev Vaccines 12 2013 519 536
7. I. Stephenson, R.G. Das, J.M. Wood, J.M. Katz Comparison of neutralising antibody assays for detection of antibody to influenza A/H3N2 viruses: an international collaborative study Vaccine 25 2007 4056 4063
8. S. Black, U. Nicolay, T. Mesikari, M. Knuf, G. DelGuidice, G. Cioppa et al. Hemagglutination inhibition antibody titers as a correlate of protection for inactivated influenza vaccines in children Pediatr Infect Dis J 30 2011 1081 1085
9. I.A. Wilson, N.J. Cox Structural basis of immune recognition of influenza virus hemagglutinin Annu Rev Immunol 8 1990 737 771
10. J.W. Yewdell To dream the impossible dream: universal influenza vaccination Curr Opin Virol 3 2013 316 321
11. A.K. Kashyap, J. Steel, A.F. Oner, M.A. Dillon, R.E. Swale, K.M. Wall et al. Combinatorial antibody libraries from survivors of the Turkish H5N1 avian influenza outbreak reveal virus neutralization strategies Proc Natl Acad Sci USA 105 2008 5986 5991
12. J. Wrammert, D. Koutsnanos, G.-M. Li, S. Edupuganti, J. Sui, M. Morrissey et al. Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection J Exp Med 208 2011 191
13. D.C. Ekiert, G. Bhabha, M.-A. Elsliger, R.H.E. Friesen, M. Johngeneelen, M. Throsby et al. Antibody recognition of a highly conserved influenza virus epitope Science 324 2009 246 251
14. D.C. Ekiert, R.H.E. Friesen, G. Bhabha, T. Kwaks, M. Jongeneelen, W. Yu et al. A highly conserved neutralizing epitope on group 2 influenza A Viruses Sci 333 2011 843 850
15. M.S. Miller, T. Tsibane, F. Krammer, R. Hai, S. Rahmat, C.F. Basler et al. 1976 and 2009 H1N1 influenza virus vaccines boost anti-hemagglutinin stalk antibodies in humans J Infect Dis 207 2013 98 105
16. R. Nachbagauer, T.J. Wohlbold, A. Hirsh, R. Hai, H. Sjursen, P. Palese et al. Induction of broadly reactive anti-hemagglutinin stalk antibodies by an H5N1 vaccine in humans J Virol 88 2014 13260 13268
17. P. Palese, T.T. Wang Why do influenza subtypes die out? A hypothesis mBio 2 2011 e00150 e211
18. F. Krammer, P. Palese Influenza virus hemagglutinin stalk-based antibodies and vaccines Curr Opin Virol 3 2013 521 530
19. J. Sui, J. Sheehan, W.C. Hwang, L.A. Bankston, S.K. Burchett, C.Y. Huang et al. Wide prevalence of heterosubtypic broadly neutralizing human anti-influenza A antibodies Clin Infect Dis 52 2011 1003 1009
20. I. Margine, R. Hai, R.A. Albrecht, G. Obermoser, A. Harrod, J. Banchereau et al. H3N2 influenza virus infection induces broadly reactive hemagglutinin stalk antibodies in humans and mice J Virol 87 2013 4728 4737
21. N. Pica, P. Palese Towards a universal influenza virus vaccine: prospects and challenges Annu Rev Med 64 2013 189 202
22. F. Krammer, N. Pica, R. Hai, I. Margine, P. Palese Chimeric hemagglutinin influenza virus vaccine constructs elicit broadly protective stalk-specific antibodies J Virol 87 2013 6542 6550
23. F. Krammer, I. Margine, R. Hai, A. Flood, A. Hirsh, V. Tsvetnitsky et al. H3 stalk-based chimeric hemagglutinin influenza virus constructs protect mice from H7N9 challenge J Virol 88 2014 2340 2343
24. J. Steel, A.C. Lowen, T.T. Wang, M. Yondola, Q. Gao, K. Hay et al. Influenza virus vaccine based on the conserved hemagglutinin stalk domain mBio 1 2010 e00018-10
25. T.T. Wang, G.S. Tan, R. Hai, P. Natalie, L. Ngai, D.C. Ekiert et al. Vacccination with a synthetic peptide from the influenza virus hemagglutinin provides protection against distinct viral subtypes Proc Natl Acad Sci USA 107 2010 18979 18984
26. Y. Lu, J.P. Welsh, J.R. Swartz Production and stabilization of the trimeric influenza hemagglutinin stem domain for potentially broadly protective influenza vaccines Proc Natl Acad Sci USA 111 2014 125 130
27. E.A. Weaver, A.M. Rubrum, R.J. Webby, M.A. Barry Protection against divergent influenza H1N1 virus by a centralized influenza hemagglutinin PLoS ONE 6 2011 e18314 [Electronic Resource]
28. B.M. Giles, T.M. Ross A computationally optimized broadly reactive antigen (COBRA) based H5N1 VLP vaccine elicits broadly reactive antibodies in mice and ferrets Vaccine 29 2011 3043 3054
29. B.M. Giles, S.J. Bissel, D.R. DeAlmeida, C.A. Wiley, T.M. Ross Antibody breadth and protective efficacy are increased by vaccination with computationally optimized hemagglutinin but not with polyvalent hemagglutinin-based H5N1 virus-like particle vaccines Clin Vaccine Immunol 19 2012 128 139
30. B.M. Giles, C.J. Crevar, D.M. Carter, S.J. Bissel, S. Schultz-Cherry, C.A. Wiley et al. A computationally optimized hemagglutinin virus-like particle vaccine elicits broadly reactive antibodies that protect nonhuman primates from H5N1 infection J Infect Dis 205 2012 1562 15710
31. R.G. Webster, P.A. Reay, W.G. Laver Protection against lethal influenza with neuraminidase Virology 164 1988 230 237
32. Y. Kawaoka, S. Krauss, R.G. Webster Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics J Virol 63 1989 4603 4608
33. B.R. Murphy, J.A. Kasel, R.M. Chanock Association of serum antineuraminidase antibody with resistance to influenza in man N Engl J Med 286 1972 1329 1332
34. A.S. Monto, A.P. Kendal Effect of neuraminidase antibody on Hong Kong influenza Lancet 7804 1973 623 625
35. M.L. Clements, R.F. Betts, E.L. Tierney, B.R. Murphy Serum and nasal wash antibodies associated with resistance to experimental challenge with influenza A wild-type virus J Clin Microbiol 24 1986 157 160
36. B.E. Johansson, B. Grajower, E.D. Kilbourne Infection-permissive immunization with influenza virus neuraminidase prevents weight loss in infected mice Vaccine 11 1993 1037 1039
37. M.R. Sandbulte, K.B. Westgeest, J. Gao, X. Xu, A.I. Klimov, C.A. Russell et al. Discordant antigenic drift of neuraminidase and hemagglutinin in H1N1 and H3N2 influenza viruses Proc Natl Acad Sci USA 108 2011 20748 20753
38. C.R. Lambre, H. Terzidis, A. Greffard, R.G. Webster Measurement of anti-influenza neuraminidase antibody using a peroxidase-linked lectin and microtitre plates coated with natural substrates J Immunol Methods 135 1990 49 57
39. T.R. Cate, Y. Rayford, D. Nino, P.L. Winokur, R.C. Brady, R. Belshe et al. A high dosage influenza vaccine induced significantly more neuraminidase antibody than standard vaccine amont elderly subjects Vaccine 28 2010 2076 2078
40. M.R. Laguio-Vila, M.G. Thompson, S. Reynolds, S.M. Spencer, M. Gaglani, A. Naleway et al. Comparison of serum hemagglutinin and neuraminidase inhibition antiboides after 2010-2011 trivalent inactivated vaccination in healthcare personnel Open Forum Infect Dis 2015 ofu115
41. A.S. Monto, J.G. Petrie, R.T. Cross, E. Johnson, M. Liu, W. Zhong et al. Antibody to influenza virus neuraminidase: an independent correlate of protection J Infect Dis 2015 [in press]
42. B.E. Johansson, E.D. Kilbourne Dissociation of influenza virus hemagglutinin and neuraminidase eliminates their intravirionic antigenic competion J Virol 67 1993 5721 5723
43. B.E. Johansson Immunization with influenza A virus hemagglutinin and neuraminidase produced in recombinant baculovirus results in a balanced and broadened immune response superior to conventional vaccine Vaccine 17 1999 2073 2080
44. E.D. Kilbourne, R.B. Couch, J.A. Kasel, W.A. Keitel, T.R. Cate, J.H. Quarles et al. Purified influenza A virus N2 neuraminidase vaccine is immunogenic and non-toxic in humans Vaccine 13 1995 1799 1803
45. R. Fritz, N. Sabarth, S. Kiermayr, C. Hohenadl, M.K. Howard, R. Ilk et al. A vero cell-derived whole-virus H5N1 vaccine effectively induces neuraminidase-inhibiting antibodies J Infect Dis 205 2012 28 34
46. M.R. Sandbulte, G.S. Jimenez, A.C.M. Boon, Larry R. Smith, J.J. Treanor, R.J. Webby Cross-reactive neuraminidase antibodies afford partial protection against H5N1 in mice and are present in unexposed humans PLOS Med 4 2007 e59
47. G. Schiff, E. Kilbourne, G. Smith, C. Hackett, S. Manoff Phase 2 clinical evaluation of an influenza A virus recombinant N2 neuraminidase. In: options for the control of influenza IV Crete 2000
48. J.J. Treanor, E.L. Tierney, S.L. Zebedee, R.A. Lamb, B.R. Murphy Passively transferred monoclonal antibody to the M2 protein inhibits influenza A virus replication in mice J Virol 64 1990 1375 1377
49. R.A. Black, P.A. Rota, N. Gorodkova, H.-D. Klenk, A.P. Kendal Antibody response to the M2 protein of influenza A virus expressed in insect cells J Gen Virol 74 1993 143 146
50. W. Zhong, C. Reed, P.J. Blair, J.M. Katz, K. Hancock Serum antibody response to matrix 2 protein following natural infection with 2009 pandemic influenza A (H1N1) virus in humans J Infect Dis 209 2014 986 994
51. A. Jegerlehner, N. Schmitz, T. Storni, M.F. Bachmann, A. Influenza vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity J Immunol 172 2004 5598 5605
52. N. Schmitz, R.R. Beerli, M. Bauer, A. Jegerlehner, K. Dietmeier, M. Maudrich et al. Universal vaccine against influenza virus: linking TLR signaling to anti-viral protection Eur J Immunol 42 2012 863 869
53. J.W. Huleatt, V. Nakaar, P. Desai, Y. Huang, D. Hewitt, A. Jacobs et al. Potent immunogenicity and efficacy of a universal influenza vaccine candidate comprising a recombinant fusion protein linking influenza M2e to the TLR5 ligand flagellin Vaccine 26 2008 201 214
54. B.Z. Wang, H.S. Gill, C. He, C. Ou, L. Wang, Y.C. Wang et al. Microneedle delivery of an M2e-TLR5 ligand fusion protein to skin confers broadly cross-protective influenza immunity J Controlled Release 178 2014 1 7
55. P. Alvarez, V. Zylberman, G. Ghersi, L. Boado, C. Palacios, F. Goldbaum et al. Tandem repeats of the extracellular domain of Matrix 2 influenza protein exposed in Brucella lumazine synthase decameric carrier molecule induce protection in mice Vaccine 31 2013 806 812
56. S. Neirynck, T. Deroo, X. Saelens, P. Vanlandschoot, W.M. Jou, W. Fiers A universal influenza A vaccine based on the extracellular domain of the M2 protein Nat Med 5 1999 1157 1163
57. M.C. Kim, J.S. Lee, Y.M. Kwon, O. Eunju, Y.J. Lee, J.G. Choi et al. Multiple heterologous M2 extracellular domains presented on virus-like particles confer broader and stronger M2 immunity than live influenza A virus infection Antiviral Res 99 2013 328 335
58. Y.N. Lee, M.C. Kim, Y.T. Lee, H.S. Hwang, M.K. Cho, J.S. Lee et al. AS04-adjuvanted virus-like particles containing multiple M2 extracellular domains of influenza virus confer improved protection Vaccine 32 2014 4578 4585
59. L. Wang, A. Hess, T.Z. Chang, Y.C. Wang, J.A. Champion, R.W. Compans et al. Nanoclusters self-assembled from conformation-stabilized influenza M2e as broadly cross-protective influenza vaccines Nanomedicine 10 2014 473 482
60. W. Fiers, M. De Filette, K. El Bakkouri, B. Schepens, K. Roose, M. Schotsaert et al. M2e-based universal influenza A vaccine Vaccine 27 2009 6280 6283
61. E.L. Ramos, J.L. Mitcham, D.T. Koller, A. Bonavia, D.W. Usner, G. Balaratnam et al. Efficacy and safety of treatment with an anti-M2e monoclonal antibody in experimental human influenza J Infect Dis 211 2015 1038 1044
62. D.K. Wagner, M.L. Clements, C.B. Reimer, M. Snydr, D.L. Nelson, B.R. Murphy Analsyis of immunoglobulin G antibody responses after administration of live and inactivated influenza A vaccine indicates that nasal wash immunoglobulin G is a transudate from serum J Clin Microbiol 25 1987 559 562
63. B.R. Murphy, M.L. Clements The systemic and mucosal immune response of humans to influenza Virus Curr Top Microbiol Immunol 146 1989 107 116
64. K.B. Renegar, P.A.J. Small Passive transfer of local immunity to influenza virus by IgA antibody J Immunol 146 1991 1972 1978
65. R.B. Belshe, W.C. Gruber, P.M. Mendelman, I. Cho, K. Reisinger, S.L. Block 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 136 2000 168 175
66. M.B. Mazanec, C.S. Kaetzel, M.E. Lamm, D. Fletcher, J.G. Nedrud Intracellular neutralization of virus by immunoglobulin A antibodies Proc Natl Acad Sci USA 89 1992 6901 6905
67. T.M. Tumpey, M. Renshaw, J.D. Clements, J.M. Katz Mucosal delivery of inactivated influenza vaccine induces B-cell-dependent heterosubtypic cross-protection against lethal influenza A H5N1 virus infection J Virol 75 2001 5141 5150
68. A.J. McMichael, F.M. Gotch, G.R. Noble, P.A.S. Beare Cytotoxic T-cell immunity to influenza N Engl J Med 309 1983 13 17
69. B.D. Forrest, M.W. Pride, A.J. Dunning, M. Rosario, Z. Capeding, T. Chotpitayasunondh et al. Correlation of cellular immune responses with protection against culture-confirmed influenza virus in young children Clin Vaccine Immunol 15 2008 1042 1053
70. T.M. Wilkinson, C.K.F. Li, C.S.C. Chui, A.K.Y. Hu8ang, M. Perkins, J.C. Liebner et al. Preexisting influenza-specific CD4+ T cells correlate with disease protection against influenza challenge in humans Nat Med 18 2012 274 280
71. S. Sridhar, S. Begom, A. Bermingham, Hoschler i, W. Adamson, W. Carman et al. Cellular immune correlates of protection against symptomatic pandemic influenza Nat Med 19 2013 1305 1312
72. L. Moise, F. Terry, M. Ardito, R. Tassone, H. Latimer, C. Boyle et al. Universal H1N1 influenza vaccine development: identification of consensus class II hemagglutinin and neuraminidase epitopes derived from strains circulating between 1980 and 2011 Hum Vaccines Immunother 9 2013 1598 1607
73. J. Alexander, P. Bilsel, M.F. del Guercio, A. Marinkovic-Petrovic, S. Southwood, S. Stewart et al. Identification of broad binding class I HLA supertype epitopes to provide universal coverage of influenza A virus Hum Immunol 71 2010 468 474
74. J. Alexander, P. Bilsel, M.F. del Guercio, S. Stewart, A. Marinkovic-Petrovic, S. Southwood et al. Universal influenza DNA vaccine encoding conserved CD4+ T cell epitopes protects against lethal viral challenge in HLA-DR transgenic mice Vaccine 28 2010 664 672
75. J. Atsmon, Y. Caraco, S. Ziv-Sefer, D. Shaikevich, E. Abramov, I. Volokhov et al. Priming by a novel universal influenza vaccine (Multimeric-001)-a gateway for improving immune response in the elderly population Vaccine 32 2014 5816 5823
76. J.S. Kwon, J. Yoon, Y.J. Kim, K. Kang, S. Woo, D.I. Jung et al. Vaccinia-based influenza vaccine overcomes previously induced immunodominance hierarchy for heterosubtypic protection Eur J Immunol 44 2014 2360 2369
77. E.A. Hemann, S.M. Kang, K.L. Legge Protective CD8 T cell-mediated immunity against influenza A virus infection following influenza virus-like particle vaccination J Immunol 191 2013 2486 2494
78. Y. Furuya Return of inactivated whole-virus vaccine for superior efficacy Immunol Cell Biol 90 2012 571 578
79. W.A. Keitel, J.D. Campbell, J.J. Treanor, E. Walter, S.M. Patel, F. He et al. Safety and immunogenicity of an inactivated influenza A/H5N1 vaccine given without or with aluminum hydroxide to healthy adults: results of a phase I-II randomized clinical trial J Infect Dis 198 2008 1309 1316
80. R.L. Atmar, W.A. Keitel, S.M. Patel, J.M. Katz, D. She, H. El Sahly et al. Safety and immunogenicity of nonadjuvanted and MF59-adjuvanted influenza A/H9N2 vaccine preparations Clin Infect Dis 43 2006 1135 1142
81. I. Leroux-Roels, A. Borkowski, T. Vanwolleghem, M. Drame, F. Clement, E. Hons et al. Antigen sparing and cross-reactive immunity with an adjuvanted rH5N1 prototype pandemic influenza vaccine: a randomised controlled trial Lancet 370 2007 580 589
82. G. Galli, K. Hancock, K. Hoschler, J. DeVos, M. Praus, M. Bardelli et al. Fast rise of broadly cross-reactive antibodies after boosting long-lived human memory B cells primed by an MF59 adjuvanted prepandemic vaccine Proc Nat Acad Sci U S A 106 2009 7962 7967
83. S. Khurana, N. Verma, J.W. Yewdell, A.K. Hilbert, F. Castellino, M. Lattanzi et al. MF59 adjuvant enhances diversity and affinity of antibody-mediated immune response to pandemic influenza vaccines Sci Transl Med 3 2011 85ra48
84. H. Nohynek, J. Jokinen, M. Partinen, O. Vaarala, T. Kirjavainen, J. Sundman et al. AS03 adjuvanted AH1N1 vaccine associated with an abrupt increase in the incidence of childhood narcolepsy in Finland PLoS ONE 7 2012 e33536
85. P.P. Heinen, F.A. Rijsewijk, E.A. de Boer-Luijtze, A.T. Bianchi Vaccination of pigs with a DNA construct expressing an influenza virus M2-nucleoprotein fusion protein exacerbates disease after challenge with influenza a virus J Gen Virol 83 2002 1851 1859
86. S. Khurana, C.L. Loving, J. Manischewitz, L.R. King, P.C. Gauger, J. Henningson et al. Vaccine-induced anti-HA2 antibodies promote virus fusion and enhance influenza virus respiratory disease Sci Transl Med 5 2013 200ra114