Top

Published in:

01-12-2007 | Review

The threat of avian influenza A (H5N1). Part IV: development of vaccines

Authors: Jindrich Cinatl jr, Martin Michaelis, Hans W. Doerr

Published in: Medical Microbiology and Immunology | Issue 4/2007

Abstract

Among emerging and re-emerging infectious diseases, influenza constitutes one of the major threats to mankind. In this review series epidemiologic, virologic and pathologic concerns raised by infections of humans with avian influenza virus A/H5N1 are discussed. This fourth part focuses on vaccine development. Several phase I clinical studies with vaccines against H5 viruses have demonstrated limited efficacy compared to seasonal influenza vaccines. To induce protective immunity two immunisations with increased amounts of H5N1 vaccine were required. Novel vaccination strategies that are egg- and adjuvant-independent, broadly cross-reactive and long-lasting are highly desirable.

Webster RG, Govorkova EA (2006) H5N1 influenza—continuing evolution and spread. N Engl J Med 335:2174–2177

Cinatl J Jr, Michaelis M, Doerr HW (2007) The threat of avian influenza a (H5N1). Part I: epidemiologic concerns and virulence determinants. Med Microbiol Immunol. 2007 [Epub ahead of print]

Cinatl J Jr, Michaelis M, Doerr HW (2007) The threat of avian influenza a (H5N1). Part II: clues to pathogenicity and pathology. Med Microbiol Immunol. 2007 [Epub ahead of print]

The Writing Committee of the World Health Organization (WHO) Consultation on Human Influenza A/H5 (2005) Avian influenza A (H5N1) infection in humans. N Engl J Med 353:1374–1385

Schunemann HJ, Hill SR, Kakad M, Bellamy R, Uyeki TM, Hayden FG, Yazdanpanah Y, Beigel J, Chotpitayasunondh T, Del Mar C, Farrar J, Tran TH, Ozbay B, Sugaya N, Fukuda K, Shindo N, Stockman L, Vist GE, Croisier A, Nagjdaliyev A, Roth C, Thomson G, Zucker H, Oxman AD, WHO Rapid Advice Guideline Panel on Avian Influenza (2007) WHO rapid advice guidelines for pharmacological management of sporadic human infection with avian influenza A (H5N1) virus. Lancet Infect Dis 7:21–31PubMed

Cinatl J Jr, Michaelis M, Doerr HW (2007) The threat of avian influenza A (H5N1). Part III: antiviral therapy. Med Microbiol Immunol 2007 [Epub ahead of print]

World Health Organization (2006) Antigenic and genetic characteristics of H5N1 viruses and H5N1 vaccine viruses developed for potential use as pre-pandemic vaccine. Wkly Epidemiol Rec 81(34/35):328–330

Subbarao K, Murphy BR, Fauci AS (2006) Development of effective vaccines against pandemic influenza. Immunity 24:5–9PubMed

Stephenson I, Gust I, Pervikov Y, Kieny MP (2006) Development of vaccines against influenza H5. Lancet Infect Dis 6:458–460PubMed

10.

Subbarao K, Luke C (2007) H5N1 viruses and vaccines. PLoS Pathog 3:e40PubMed

11.

Johansson BE, Bucher DJ, Kilbourne ED (1989) Purified influenza virus hemagglutinin and neuraminidase are equivalent in stimulation of antibody response but induce contrasting types of immunity to infection. J Virol 63:1239–1246PubMed

12.

Tamura S, Tanimoto T, Kurata T (2005) Mechanisms of broad cross-protection provided by influenza virus infection and their application to vaccines. Jpn J Infect Dis 58:195–207PubMed

13.

Powers DC, Kilbourne ED, Johansson BE (1996) Neuraminidase-specific antibody responses to inactivated influenza virus vaccine in young and elderly adults. Clin Diagn Lab Immunol 3:511–516PubMed

14.

Black RA, Rota PA, Gorodkova N, Klenk HD, Kendal AP (1993) Antibody response to the M2 protein of influenza A virus expressed in insect cells. J Gen Virol 74:143–146PubMed

15.

Murphy BR, Clements ML (1989) The systemic and mucosal immune response of humans to influenza A virus. Curr Top Microbiol Immunol 146:107–116PubMed

16.

McMichael AJ, Gotch FM, Noble GR, Beare PA (1983) Cytotoxic T-cell immunity to influenza. N Engl J Med 309:13–17PubMedCrossRef

17.

Bender BS, Croghan T, Zhang L, Small PA Jr (1992) 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 175:1143–1145PubMed

18.

Yewdell JW, Bennink JR, Smith GL, Moss B (1985) Influenza A virus nucleoprotein is a major target antigen for cross-reactive anti-influenza A virus cytotoxic T lymphocytes. Proc Natl Acad Sci USA 82:1785–1789PubMed

19.

Wang M, Lamberth K, Harndahl M, Roder G, Stryhn A, Larsen MV, Nielsen M, Lundegaard C, Tang ST, Dziegiel MH, Rosenkvist J, Pedersen AE, Buus S, Claesson MH, Lund O (2007) CTL epitopes for influenza A including the H5N1 bird flu; genome-, pathogen-, and HLA-wide screening. Vaccine 25(15):2823–2831PubMed

20.

Jameson J, Cruz J, Ennis FA (1998) Human cytotoxic T-lymphocyte repertoire to influenza A viruses. J Virol 72:8682–8689PubMed

21.

Nakajima K, Desselberger U, Palese P (1978) Recent human influenza A (H1N1) viruses are closely related genetically to strains isolated in 1950. Nature 274:334–339PubMed

22.

Horimoto T, Kawaoka Y (2006) Strategies for developing vaccines against H5N1 influenza A viruses. Trends Mol Med 12:506–514PubMed

23.

Couch RB, Kasel JA (1983) Immunity to influenza in man. Annu Rev Microbiol 37:529–549PubMed

24.

Epstein SL (2006) Prior H1N1 influenza infection and susceptibility of Cleveland Family Study participants during the H2N2 pandemic of 1957: an experiment of nature. J Infect Dis 193:49–53PubMed

25.

Murphy BR, Kasel JA, Chanock RM (1972) Association of serum anti-neuraminidase antibody with resistance to influenza in man. N Engl J Med 286:1329–1332PubMedCrossRef

26.

Gillim-Ross L, Subbarao K (2007) Can immunity induced by the human influenza virus N1 neuraminidase provide some protection from Avian Influenza H5N1 Viruses? PLoS Med 4:e91PubMed

27.

Sandbulte MR, Jimenez GS, Boon AC, Smith LR, Treanor JJ, Webby RJ (2007) Cross-reactive neuraminidase antibodies afford partial protection against H5N1 in mice and are present in unexposed humans. PLoS Med 4:e59PubMed

28.

Ulmer JB, Valley U, Rappuoli R (2006) Vaccine manufacturing: challenges and solutions. Nat Biotechnol 24:1377–1383PubMed

29.

Hehme N, Engelmann H, Kunzel W, Neumeier E, Sanger R (2002) Pandemic preparedness: lessons learnt from H2N2 and H9N2 candidate vaccines. Med Microbiol Immunol 191:203–208PubMed

30.

Hehme N, Engelmann H, Kuenzel W, Neumeier E, Saenger R (2004) Immunogenicity of a monovalent, aluminum-adjuvanted influenza whole virus vaccine for pandemic use. Virus Res 103:163–171PubMed

31.

Nonacs R, Humborg C, Tam JP, Steinman RM (1992) Mechanisms of mouse spleen dendritic cell function in the generation of influenza-specific, cytolytic T lymphocytes. J Exp Med 176:519–529PubMed

32.

Bhardwaj N, Bender A, Gonzalez N, Bui LK, Garrett MC, Steinman RM (1994) Influenza virus-infected dendritic cells stimulate strong proliferative and cytolytic responses from human CD8+ T cells. J Clin Invest 94:797–807PubMedCrossRef

33.

Heath WR, Carbone FR (2001) Cross-presentation in viral immunity and self-tolerance. Nat Rev Immunol 1:126–134PubMed

34.

Takada A, Kuboki N, Okazaki K, Ninomiya A, Tanaka H, Ozaki H, Itamura S, Nishimura H, Enami M, Tashiro M, Shortridge KF, Kida H (1999) Avirulent Avian influenza virus as a vaccine strain against a potential human pandemic. J Virol 73:8303–8307PubMed

35.

Webby RJ, Perez DR, Coleman JS, Guan Y, Knight JH, Govorkova EA, McClain-Moss LR, Peiris JS, Rehg JE, Tuomanen EI, Webster RG (2004) Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. Lancet 363:1099–1103PubMed

36.

Wood JM, Robertson JS (2004) From lethal virus to life-saving vaccine: developing inactivated vaccines for pandemic influenza. Nat Rev Microbiol 2:842–847PubMed

37.

Horimoto T, Takada A, Fujii K, Goto H, Hatta M, Watanabe S, Iwatsuki-Horimoto K, Ito M, Tagawa-Sakai Y, Yamada S, Ito H, Ito T, Imai M, Itamura S, Odagiri T, Tashiro M, Lim W, Guan Y, Peiris M, Kawaoka Y (2006) The development and characterization of H5 influenza virus vaccines derived from a 2003 human isolate. Vaccine 24:3669–3676PubMed

38.

Nicolson C, Major D, Wood JM, Robertson JS (2005) Generation of influenza vaccine viruses on Vero cells by reverse genetics: an H5N1 candidate vaccine strain produced under a quality system. Vaccine 23:2943–2952PubMed

39.

Horimoto T, Kawaoka Y (2005) Influenza: lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol 3:591–600PubMed

40.

Lin J, Zhang J, Dong X, Fang H, Chen J, Su N, Gao Q, Zhang Z, Liu Y, Wang Z, Yang M, Sun R, Li C, Lin S, Ji M, Liu Y, Wang X, Wood J, Feng Z, Wang Y, Yin W (2006) Safety and immunogenicity of an inactivated adjuvanted whole-virion influenza A (H5N1) vaccine: a phase I randomised controlled trial. Lancet 368:991–997PubMed

41.

Nicholson KG, Tyrrell DA, Harrison P, Potter CW, Jennings R, Clark A, Schild GC, Wood JM, Yetts R, Seagroatt V, Huggins A, Anderson SG (1979) Clinical studies of monovalent inactivated whole virus and subunit A/USSR/77 (H1N1) vaccine: serological responses and clinical reactions. J Biol Stand 7:123–136PubMed

42.

Wright PF, Thompson J, Vaughn WK, Folland DS, Sell SH, Karzon DT (1977) Trials of influenza A/New Jersey/76 virus vaccine in normal children: an overview of age-related antigenicity and reactogenicity. J Infect Dis 136(Suppl):S731–S741PubMed

43.

Ninomiya A, Imai M, Tashiro M, Odagiri T (2007) Inactivated influenza H5N1 whole-virus vaccine with aluminum adjuvant induces homologous and heterologous protective immunities against lethal challenge with highly pathogenic H5N1 avian influenza viruses in a mouse model. Vaccine 25(18):3554–3560PubMed

44.

Govorkova EA, Webby RJ, Humberd J, Seiler JP, Webster RG (2006) Immunization with reverse-genetics-produced H5N1 influenza vaccine protects ferrets against homologous and heterologous challenge. J Infect Dis 194:159–167PubMed

45.

Lipatov AS, Hoffmann E, Salomon R, Yen HL, Webster RG (2006) Cross-protectiveness and immunogenicity of influenza A/Duck/Singapore/3/97(H5) vaccines against infection with A/Vietnam/1203/04(H5N1) virus in ferrets. J Infect Dis 194:1040–1043PubMed

46.

Couch RB, Keitel WA, Cate TR (1997) Improvement of inactivated influenza virus vaccines. J Infect Dis 176(Suppl 1):S38–S44PubMed

47.

Hilleman MR (2002) Realities and enigmas of human viral influenza: pathogenesis, epidemiology and control. Vaccine 20:3068–3087PubMed

48.

Stephenson I, Nicholson KG, Wood JM, Zambon MC, Katz JM (2004) Confronting the avian influenza threat: vaccine development for a potential pandemic. Lancet Infect Dis 4:499–509PubMed

49.

Bresson JL, Perronne C, Launay O, Gerdil C, Saville M, Wood J, Hoschler K, Zambon MC (2006) Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet 367:1657–1664PubMed

50.

Nicholson KG, Colegate AE, Podda A, Stephenson I, Wood J, Ypma E, Zambon MC (2001) 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 357:1937–1943PubMed

51.

Stephenson I, Bugarini R, Nicholson KG, Podda A, Wood JM, Zambon MC, Katz JM (2005) Cross-reactivity to highly pathogenic avian influenza H5N1 viruses after vaccination with nonadjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a potential priming strategy. J Infect Dis 191:1210–1215PubMed

52.

Treanor JJ, Campbell JD, Zangwill KM, Rowe T, Wolff M (2006) Safety and immunogenicity of an inactivated subvirion influenza A (H5N1)vaccine. N Engl J Med 2354:1343–1351

53.

Stephenson I (2006) H5N1 vaccines: how prepared are we for a pandemic? Lancet 368:965–966PubMed

54.

Treanor JJ, Schiff GM, Couch RB, Cate TR, Brady RC, Hay CM, Wolff M, She D, Cox MM (2006) Dose-related safety and immunogenicity of a trivalent baculovirus-expressed influenza-virus hemagglutinin vaccine in elderly adults. J Infect Dis 193:1223–1228PubMed

55.

Wang K, Holtz KM, Anderson K, Chubet R, Mahmoud W, Cox MM (2006) Expression and purification of an influenza hemagglutinin—one step closer to a recombinant protein-based influenza vaccine. Vaccine 24:2176–2185PubMed

56.

Treanor JJ, Wilkinson BE, Masseoud F, Hu-Primmer J, Battaglia R, O’Brien D, Wolff M, Rabinovich G, Blackwelder W, Katz JM (2001) Safety and immunogenicity of a recombinant hemagglutinin vaccine for H5 influenza in humans. Vaccine 19:1732–1737PubMed

57.

Kendal AP (1997) Cold-adapted live attenuated influenza vaccines developed in Russia: can they contribute to meeting the needs for influenza control in other countries? Eur J Epidemiol 13:591–609PubMed

58.

Jin H, Lu B, Zhou H, Ma C, Zhao J, Yang CF, Kemble G, Greenberg H (2003) Multiple amino acid residues confer temperature sensitivity to human influenza virus vaccine strains (FluMist) derived from cold-adapted A/Ann Arbor/6/60. Virology 306:18–24PubMed

59.

Hoffmann E, Mahmood K, Chen Z, Yang CF, Spaete J, Greenberg HB, Herlocher ML, Jin H, Kemble G (2005) Multiple gene segments control the temperature sensitivity and attenuation phenotypes of ca B/Ann Arbor/1/66. J Virol 79:11014–11021PubMed

60.

Belshe RB, Nichol KL, Black SB, Shinefield H, Cordova J, Walker R, Hessel C, Cho I, Mendelman PM (2004) Safety, efficacy, and effectiveness of live, attenuated, cold-adapted influenza vaccine in an indicated population aged 5–49 years. Clin Infect Dis 39:920–927PubMed

61.

Belshe RB, Edwards KM, Vesikari T, Black SV, Walker RE, Hultquist M, Kemble G, Connor EM; CAIV-T Comparative Efficacy Study Group (2007) Live attenuated versus inactivated influenza vaccine in infants and young children. N Engl J Med 356:685–696PubMed

62.

Youngner JS, Treanor JJ, Betts RF, Whitaker-Dowling P (1994) Effect of simultaneous administration of cold-adapted and wild-type influenza A viruses on experimental wild-type influenza infection in humans. J Clin Microbiol 32:750–754PubMed

63.

Buonagurio DA, Bechert TM, Yang CF, Shutyak L, D’Arco GA, Kazachkov Y, Wang HP, Rojas EA, O’Neill RE, Spaete RR, Coelingh KL, Zamb TJ, Sidhu MS, Udem SA (2006) Genetic stability of live, cold-adapted influenza virus components of the FluMist/CAIV-T vaccine throughout the manufacturing process. Vaccine 24:2151–2160PubMed

64.

Li S, Liu C, Klimov A, Subbarao K, Perdue ML, Mo D, Ji Y, Woods L, Hietala S, Bryant M (1999) Recombinant influenza A virus vaccines for the pathogenic human A/Hong Kong/97 (H5N1) viruses. J Infect Dis 179:1132–1138PubMed

65.

Suguitan AL Jr, McAuliffe J, Mills KL, Jin H, Duke G, Lu B, Luke CJ, Murphy B, Swayne DE, Kemble G, Subbarao K (2006) Live, attenuated influenza A H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS Med 3:e360PubMed

66.

Lu X, Edwards LE, Desheva JA, Nguyen DC, Rekstin A, Stephenson I, Szretter K, Cox NJ, Rudenko LG, Klimov A, Katz JM (2006) Cross-protective immunity in mice induced by live-attenuated or inactivated vaccines against highly pathogenic influenza A (H5N1) viruses. Vaccine 24:6588–6593PubMed

67.

Desheva JA, Lu XH, Rekstin AR, Rudenko LG, Swayne DE, Cox NJ, Katz JM, Klimov AI (2006) 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 24:6859–6866PubMed

68.

Ada G, Ramshaw I (2003) DNA vaccination. Expert Opin Emerg Drugs 8:27–35PubMed

69.

Ulmer JB (2002) Influenza DNA vaccines. Vaccine 20(Suppl 2):S74–S76PubMed

70.

Hoare M, Levy MS, Bracewell DG, Doig SD, Kong S, Titchener-Hooker N, Ward JM, Dunnill P (2005) Biprocess engineering issues that would be faced in producing a DNA vaccine at up to 100m³ fermentation scale for an influenza pandemic. Biotechnol Prog 21:1577–1592PubMed

71.

Liu MA, McClements W, Ulmer JB, Shiver J, Donnelly J (1997) Immunization of non-human primates with DNA vaccines. Vaccine 15:909–912PubMed

72.

Pertmer TM, Eisenbraun MD, McCabe D, Prayaga SK, Fuller DH, Haynes JR (1995) Gene gun-based nucleic acid immunization: elicitation of humoral and cytotoxic T lymphocyte responses following epidermal delivery of nanogram quantities of DNA. Vaccine 13:1427–1430PubMed

73.

Robinson HL, Hunt LA, Webster RG (1993) Protection against a lethal influenza virus challenge by immunization with a haemagglutinin-expressing plasmid DNA. Vaccine 11:957–960PubMed

74.

Ulmer JB, Fu TM, Deck RR, Friedman A, Guan L, DeWitt C, Liu X, Wang S, Liu MA, Donnelly JJ, Caulfield MJ (1998) Protective CD4+ and CD8+ T cells against influenza virus induced by vaccination with nucleoprotein DNA. J Virol 72:5648–5653PubMed

75.

Ulmer JB, Donnelly JJ, Parker SE, Rhodes GH, Felgner PL, Dwarki VJ, Gromkowski SH, Deck RR, DeWitt CM, Friedman A et al (1993) Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 259:1745–1749PubMed

76.

Kodihalli S, Kobasa DL, Webster RG (2000) Strategies for inducing protection against avian influenza A virus subtypes with DNA vaccines. Vaccine 18:2592–2599PubMed

77.

Epstein SL, Tumpey TM, Misplon JA, Lo CY, Cooper LA, Subbarao K, Renshaw M, Sambhara S, Katz JM (2002) DNA vaccine expressing conserved influenza virus proteins protective against H5N1 challenge infection in mice. Emerg Infect Dis 8:796–801PubMed

78.

Kodihalli S, Goto H, Kobasa DL, Krauss S, Kawaoka Y, Webster RG (1999) DNA vaccine encoding hemagglutinin provides protective immunity against H5N1 influenza virus infection in mice. J Virol 73:2094–2098PubMed

79.

Laddy DJ, Yan J, Corbitt N, Kobasa D, Kobinger GP, Weiner DB (2007) Immunogenicity of novel consensus-based DNA vaccines against avian influenza. Vaccine 25(16):2984–2989PubMed

80.

Gao W, Soloff AC, Lu X, Montecalvo A, Nguyen DC, Matsuoka Y, Robbins PD, Swayne DE, Donis RO, Katz JM, Barratt-Boyes SM, Gambotto A (2006) Protection of mice and poultry from lethal H5N1 avian influenza virus through adenovirus-based immunization. J Virol 80:1959–1964PubMed

81.

Hoelscher MA, Garg S, Bangari DS, Belser JA, Lu X, Stephenson I, Bright RA, Katz JM, Mittal SK, Sambhara S (2006) Development of adenoviral-vector-based pandemic influenza vaccine against antigenically distinct human H5N1 strains in mice. Lancet 367:475–481PubMed

82.

Karaca K, Swayne DE, Grosenbaugh D, Bublot M, Robles A, Spackman E, Nordgren R (2005) Immunogenicity of fowlpox virus expressing the avian influenza virus H5 gene (TROVAC AIV-H5) in cats. Clin Diagn Lab Immunol 12:1340–1342PubMed

83.

Veits J, Wiesner D, Fuchs W, Hoffmann B, Granzow H, Starick E, Mundt E, Schirrmeier H, Mebatsion T, Mettenleiter TC, Romer-Oberdorfer A (2006) Newcastle disease virus expressing H5 hemagglutinin gene protects chickens against Newcastle disease and avian influenza. Proc Natl Acad Sci USA 103:8197–8202PubMed

84.

Ge J, Deng G, Wen Z, Tian G, Wang Y, Shi J, Wang X, Li Y, Hu S, Jiang Y, Yang C, Yu K, Bu Z, Chen H (2007) Newcastle disease virus-based live attenuated vaccine completely protects chickens and mice from lethal challenge of homologous and heterologous H5N1 avian influenza viruses. J Virol 81:150–158PubMed

85.

Bukreyev A, Huang Z, Yang L, Elankumaran S, St Claire M, Murphy BR, Samal SK, Collins PL (2005) Recombinant newcastle disease virus expressing a foreign viral antigen is attenuated and highly immunogenic in primates. J Virol 79:13275–13284PubMed

86.

Egorov A, Brandt S, Sereinig S, Romanova J, Ferko B, Katinger D, Grassauer A, Alexandrova G, Katinger H, Muster T (1998) Transfectant influenza A viruses with long deletions in the NS1 protein grow efficiently in Vero cells. J Virol 72:6437–6441PubMed

87.

Garcia-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE, Durbin JE, Palese P, Muster T (1998) Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252:324–330PubMed

88.

Talon J, Salvatore M, O’Neill RE, Nakaya Y, Zheng H, Muster T, Garcia-Sastre A, Palese P (2000) Influenza A and B viruses expressing altered NS1 proteins: A vaccine approach. Proc Natl Acad Sci USA 97:4309–4314PubMed

89.

Ferko B, Stasakova J, Romanova J, Kittel C, Sereinig S, Katinger H, Egorov A (2004) Immunogenicity and protection efficacy of replication-deficient influenza A viruses with altered NS1 genes. J Virol 78:13037–13045PubMed

90.

Proietti E, Bracci L, Puzelli S, Di Pucchio T, Sestili P, De Vincenzi E, Venditti M, Capone I, Seif I, De Maeyer E, Tough D, Donatelli I, Belardelli F (2002) Type I IFN as a natural adjuvant for a protective immune response: lessons from the influenza vaccine model. J Immunol 169:375–383PubMed

91.

Bracci L, Canini I, Puzelli S, Sestili P, Venditti M, Spada M, Donatelli I, Belardelli F, Proietti E (2005) Type I IFN is a powerful mucosal adjuvant for a selective intranasal vaccination against influenza virus in mice and affects antigen capture at mucosal level. Vaccine 23:2994–3004PubMed

92.

Neirynck S, Deroo T, Saelens X, Vanlandschoot P, Jou WM, Fiers W (1999) A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat Med 5:1157–1163PubMed

93.

Ernst WA, Kim HJ, Tumpey TM, Jansen AD, Tai W, Cramer DV, Adler-Moore JP, Fujii G (2006) Protection against H1, H5, H6 and H9 influenza A infection with liposomal matrix 2 epitope vaccines. Vaccine 24:5158–5168PubMed

94.

Gerhard W (2006) Influenza A virus infection engenders a poor antibody response against the ectodomain of matrix protein 2. Virol J 3:102PubMed

95.

Kilbourne ED, Couch RB, Kasel JA, Keitel WA, Cate TR, Quarles JH, Grajower B, Pokorny BA, Johansson BE (1995) Purified influenza A virus N2 neuraminidase vaccine is immunogenic and non-toxic in humans. Vaccine 13:1799–1803PubMed

96.

Johansson BE, Kilbourne ED (1993) Dissociation of influenza virus hemagglutinin and neuraminidase eliminates their intravirionic antigenic competition. J Virol 67:5721–5723PubMed

97.

Feng J, Zhang M, Mozdzanowska K, Zharikova D, Hoff H, Wunner W, Couch RB, Gerdil C (2003) The annual production cycle for influenza vaccine. Vaccine 21:1776–1779

98.

De Filette M, Ramne A, Birkett A, Lycke N, Lowenadler B, Min Jou W, Saelens X, Fiers W (2006) The universal influenza vaccine M2e-HBc administered intranasally in combination with the adjuvant CTA1-DD provides complete protection. Vaccine 24:544–551PubMed

99.

Fan J, Liang X, Horton MS, Perry HC, Citron MP, Heidecker GJ, Fu TM, Joyce J, Przysiecki CT, Keller PM, Garsky VM, Ionescu R, Rippeon Y, Shi L, Chastain MA, Condra JH, Davies ME, Liao J, Emini EA, Shiver JW (2004) Preclinical study of influenza virus A M2 peptide conjugate vaccines in mice, ferrets, and rhesus monkeys. Vaccine 22:2993–3003PubMed

100.

Jegerlehner A, Schmitz N, Storni T, Bachmann MF (2004) Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J Immunol 172:5598–5605PubMed

101.

Gerdil C (2003) The annual production cycle for influenza vaccine. Vaccine 21:1776–1779PubMed

102.

Cinatl J Jr, Cinatl J, Rabenau H, Rapp J, Kornhuber B, Doerr HW (1993) Protein-free culture of Vero cells: a substrate for replication of human pathogenic viruses. Cell Biol Int 17:885–895PubMed

103.

Katz JM, Wang M, Webster RG (1990) Direct sequencing of the HA gene of influenza (H3N2) virus in original clinical samples reveals sequence identity with mammalian cell-grown virus. J Virol 64:1808–1811PubMed

104.

Schild GC, Oxford JS, de Jong JC, Webster RG (1983) Evidence for host-cell selection of influenza virus antigenic variants. Nature 303:706–709PubMed

105.

Alymova IV, Kodihalli S, Govorkova EA, Fanget B, Gerdil C, Webster RG (1998) Immunogenicity and protective efficacy in mice of influenza B virus vaccines grown in mammalian cells or embryonated chicken eggs. J Virol 72:4472–4477PubMed

106.

Pau MG, Ophorst C, Koldijk MH, Schouten G, Mehtali M, Uytdehaag F (2001) The human cell line PER.C6 provides a new manufacturing system for the production of influenza vaccines. Vaccine 19:2716–2721PubMed

Title: The threat of avian influenza A (H5N1). Part IV: development of vaccines
Authors: Jindrich Cinatl jr
Martin Michaelis
Hans W. Doerr
Publication date: 01-12-2007
Publisher: Springer-Verlag
Published in: Medical Microbiology and Immunology / Issue 4/2007
Print ISSN: 0300-8584
Electronic ISSN: 1432-1831
DOI: https://doi.org/10.1007/s00430-007-0052-3

ACC 2024 Congress Coverage

Heart Failure Video

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

The threat of avian influenza A (H5N1). Part IV: development of vaccines

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2007

Immunogenicity and protective efficacy of the E. coli-expressed domain III of Japanese encephalitis virus envelope protein in mice

Hepatitis B virus genotype E surface antigen detection with different immunoassays and diagnostic impact of mutations in the preS/S gene

The threat of avian influenza a (H5N1): part II: Clues to pathogenicity and pathology

The threat of avian influenza A (H5N1). Part III: antiviral therapy

Pathogenesis of leptospirosis: interaction of Leptospira interrogans with in vitro cultured mammalian cells

The threat of avian influenza A (H5N1). Part I: epidemiologic concerns and virulence determinants

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page