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Special Topic: Progress and Challenges in Vaccinology

Development of a Vaccine Against Pandemic Influenza Viruses: Current Status and Perspectives

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Pages 392-426 | Published online: 03 Aug 2009

REFERENCES

  • Treanor J. J., King J. C., Zangwill K. M. New approaches to influenza vaccine. New Generation Vaccines, M. Levine, J. B. Kaper, R. Rappuoli, M. A. Liu, M. F. Good. Marcel Dekker, New York, Basel 2004; 537–558
  • Claas E. C. J., Osterhaus A. D. M. E., van Beek R., De Jong J. C., Rimmelzwaan G. F., Senne D. A., Krauss S., Shortridge K. F., Webster R. G. Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 1998; 351: 472–477
  • Katz J. M., Bridges C. B., Rowe T., Hu-Primmer J., Lu X., Abernathy R. A., Clarke M., Conn L., Kwong H., Lee M., Au G., Ho Y. Y., Mak K. H., Cox N. J., Fukuda K. Antibody response in individuals infected with avian influenza A (H5N1) viruses and detection of anti-H5 antibody among household and social contacts. J Infect Dis 1999; 180: 1763–1770
  • Fukuda K., Levandowski R. A., Bridges C. B., Cox N. J. Inactivated Influenza Vaccines. Vaccines, S. A. Plotkin, W. A. Orenstein. Elsevier, Philadelphia 2004; 339–370
  • Smith G. J., Fan X. H., Wang J., Li K. S., Qin K., Zhang J. X., Vijaykrishna D., Cheung C. L., Huang K., Rayner J. M., Peiris J. S., Chen H., Webster R. G., Guan Y. Emergence and predominance of an H5N1 influenza variant in China. Proc. Natl. Acad. Sci. USA 2006; 103: 16936–16941
  • Palese P. Making better influenza virus vaccines?. Emerg Infect Dis 2006; 12: 61–65
  • Johansson B. E., Brett I. C. Changing perspective on immunization against influenza. Vaccine 2007; 25: 3062–3065
  • Hoskins T. W., Davies J. R., Smith A. J., Miller C. L., Allchin A. Assessment of inactivated influenza A vaccine after three outbreaks of influenza at Christ's Hospital. Lancet 1979; 1: 33–35
  • Treanor J. J., Wilkinson B. E., Masseoud F., Hu-Primmer J., Battaglia R., O'Brien D., Wolff M., Rabinovich G., Blackwelder W., Katz J. M. Safety and immunogenicity of a recombinant hemagglutinin vaccine for H5 influenza in humans. Vaccine 2001; 19: 1732–1737
  • Nicholson K. G., Colegate A. E., Podda A., Stephenson I., Wood J., Ypma E., Zambon M. C. 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
  • The World Health Organization Global Influenza Program Surveillance Network. Evolution of H5N1 avian influenza viruses in Asia. Emerg Infect Dis 2005; 11: 1515–1521
  • Senne D. A., Panigrahy B., Kawaoka Y., Pearson J. E., Süss J., Lipkind M., Kida H., Webster R. G. Survey of the hemagglutinin (HA) cleavage site sequence of H5 and H7 avian influenza viruses: amino acid sequence at the HA cleavage site as a marker of pathogenicity potential. Avian Dis 1996; 40: 425–437
  • Treanor J. J., Campbell J. D., Zangwill K. M., Rowe T., Wolff M. Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine. N Engl J Med 2006; 354: 1343–1351
  • 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. Safety and immunogenicity of an inactivated adjuvanted whole-virion influenza A (H5N1) vaccine: a phase I randomised controlled trial. Lancet 2006; 368: 991–997
  • Zangwill K. M., Treanor J. J., Campbell J. D., Noah D. L., Ryea J. Evaluation of the safety and immunogenicity of a booster (third) dose of inactivated subvirion H5N1 influenza vaccine in humans. J Infect Dis 2008; 197: 580–583
  • Poland G. A., Jacobson R. M., Targonski P. V. Avian and pandemic influenza: an overview. Vaccine 2007; 25: 3057–3061
  • Stephenson I., Gust I., Pervikov Y., Kieny M. P. Development of vaccines against influenza H5. Lancet Infect Dis 2006; 6: 458–460
  • Leroux-Roels I., Borkowski A., Vanwolleghem T., Dramé M., Clement F., Hons E., Devaster J. M., Leroux-Roels G. Antigen sparing and cross-reactive immunity with an adjuvanted rH5N1 prototype pandemic influenza vaccine: a randomised controlled trial. Lancet 2007; 370: 580–589
  • Luke C. J., Subbarao K. Vaccines for pandemic influenza. Emerg Infect Dis 2006; 12: 66–72
  • Nichol K. L., Treanor J. J. Vaccines for seasonal and pandemic influenza. J Infect Dis 2006; 194: S111–S118
  • Bresson J. L. P. C., Launay O., Gerdil C., Saville M., Wood J., Höschler K., Zambon M. C. Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet 2006; 367: 1657–1664
  • Ninomiya A., Imai M., Tashiro M., Odagiri T. 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 2007; 25: 3554–3560
  • Bungener L., Geeraedts F., Ter W., Veer Medema J., Wilschut J., Huckriede A. Alum boosts TH2-type antibody responses to whole-inactivated virus influenza vaccine in mice but does not confer superior protection. Vaccine 2008; 26: 2350–2359
  • O'Hagan D. T., Wack A., Podda A. MF59 is a safe and potent vaccine adjuvant for flu vaccines in humans: what did we learn during its development?. Clin. Pharmacol Ther 2007; 82: 740–744
  • Huckriede A., Bungener L., Stegmann T., Daemen T., Medema J., Palache A. M., Wilschut J. The virosome concept for influenza vaccines. Vaccine 2005; 23: S26–S38
  • Glück R., Burri K. G., Metcalfe I. Adjuvant and antigen delivery properties of virosomes. Curr Drug Deliv 2005; 2: 395–400
  • De Donato S., Granoff D., Minutello M., Lecchi G., Faccini M., Agnello M., Senatore F., Verweij P., Fritzell B., Podda A. Safety and immunogenicity of MF59-adjuvanted influenza vaccine in the elderly. Vaccine 1999; 17: 3094–3101
  • Del Giudice G., Hilbert A. K., Bugarini R., Minutello A., Popova O., Toneatto D., Schoendorf I., Borkowski A., Rappuoli R., Podda A. An MF59-adjuvanted inactivated influenza vaccine containing A/Panama/1999 (H3N2) induced broader serological protection against heterovariant influenza virus strain A/Fujian/2002 than a subunit and a split influenza vaccine. Vaccine 2006; 24: 3063–3065
  • Stephenson I., Bugarini R., Nicholson K. G., Podda A., Wood J. M., Zambon M. C., Katz J. M. 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 2005; 191: 1210–1215
  • Ansaldi F., Bacilieri S., Durando P., Sticchi L., Valle L., Montomoli E., Icardi G., Gasparini R., Crovari P. Cross-protection by MF59-adjuvanted influenza vaccine: neutralizing and haemagglutination-inhibiting antibody activity against A(H3N2) drifted influenza viruses. Vaccine 2008; 26: 1525–1529
  • Wack A., Baudner B. C., Hilbert A. K., Manini I., Nuti S., Tavarini S., Scheffczik H., Ugozzoli M., Singh M., Kazzaz J., Montomoli E., Del Giudice G., Rappuoli R., O'Hagan D. T. Combination adjuvants for the induction of potent, long-lasting antibody and T-cell responses to influenza vaccine in mice. Vaccine 2008; 26: 552–561
  • de Bruijn I., Meyer I., Gerez L., Nauta J., Giezeman K., Palache B. Antibody induction by virosomal, MF59-adjuvanted, or conventional influenza vaccines in the elderly. Vaccine 2007; 26: 119–127
  • de Bruijn I. A., Nauta J., Gerez L., Palache A. M. The virosomal influenza vaccine Invivac: immunogenicity and tolerability compared to an adjuvanted influenza vaccine (Fluad) in elderly subjects. Vaccine 2006; 24: 6629–6631
  • Garçon N., Chomez P., Van Mechelen M. GlaxoSmithKline Adjuvant Systems in vaccines: concepts, achievements and perspectives. Expert Rev. Vaccines 2007; 6: 723–739
  • Leroux-Roels I., Bernhard R., Gérard P., Dramé M., Hanon E., Leroux-Roels G. Broad Clade 2 cross-reactive immunity induced by an adjuvanted clade 1 rH5N1 pandemic influenza vaccine. PLoS ONE. 2008; 3: e1665
  • Vandepapelière P., Horsmans Y., Moris P., Van Mechelen M., Janssens M., Koutsoukos M., Van P., Belle Clement F., Hanon E., Wettendorff M., Garçon N., Leroux-Roels G. Vaccine adjuvant systems containing monophosphoryl lipid A and QS21 induce strong and persistent humoral and T cell responses against hepatitis B surface antigen in healthy adult volunteers. Vaccine 2008; 26: 1375–1386
  • Stephenson I., Zambon M. C., Rudin A., Colegate A., Podda A., Bugarini R., Del G., Giudice Minutello A., Bonnington S., Holmgren J., Mills K. H., Nicholson K. G. Phase I evaluation of intranasal trivalent inactivated influenza vaccine with nontoxigenic Escherichia coli enterotoxin and novel biovector as mucosal adjuvants, using adult volunteers. J Virol 2006; 80: 4962–4970
  • Treanor J., Nolan C., O'Brien D., Burt D., Lowell G., Linden J., Fries L. Intranasal administration of a proteosome-influenza vaccine is well-tolerated and induces serum and nasal secretion influenza antibodies in healthy human subjects. Vaccine 2006; 24: 254–262
  • Lowell G. H. B. D., White G. Proteosome technology for vaccines and adjuvants. New Generation Vaccines, M. M. Levine, J. B. Kaper, R. Rappuoli, M. A. Liu, M. F. Good. Marcel Dekker, New York - Basel 2004; 271–283
  • Morein B., Sundquist B., Höglund S., Dalsgaard K., Osterhaus A. Iscom, a novel structure for antigenic presentation of membrane proteins from enveloped viruses. Nature 1984; 308: 457–460
  • Rimmelzwaan G. F., Baars M., van Beek R., van G., Amerongen Lövgren-Bengtsson K., Claas E. C., Osterhaus A. D. Induction of protective immunity against influenza virus in a macaque model: comparison of conventional and iscom vaccines. J Gen Virol 1997; 78: 757–765
  • Rimmelzwaan G. F., Claas E. C., van Amerongen G., de Jong J. C., Osterhaus A. D. ISCOM vaccine induced protection against a lethal challenge with a human H5N1 influenza virus. Vaccine 1999; 17: 1355–1358
  • Rimmelzwaan G. F., Baars M., van Amerongen G., van Beek R., Osterhaus A. D. A single dose of an ISCOM influenza vaccine induces long-lasting protective immunity against homologous challenge infection but fails to protect Cynomolgus macaques against distant drift variants of influenza A (H3N2) viruses. Vaccine 2001; 20: 158–163
  • Webster R. G., Govorkova E. A. H5N1 influenza—continuing evolution and spread. N Engl J Med 2006; 335: 2174–2177
  • Sugaya N., Nerome K., Ishida M., Matsumoto M., Mitamura K., Nirasawa M. Efficacy of inactivated vaccine in preventing antigenically drifted influenza Type A and well-matched Type B. JAMA 1994; 272: 1122–1126
  • Brett I. C., Johansson B. E. Immunization against influenza A virus: comparison of conventional inactivated, live-attenuated and recombinant baculovirus produced purified hemagglutinin and neuraminidase vaccines in a murine model system. Virology 2005; 339: 273–280
  • Besselaar T. G., Botha L., McAnerney J. V., Schoub B. D. Antigenic and molecular analysis of influenza A (H3N2) virus strains isolated from a localised influenza outbreak in South Africa in 2003. J Med Virol 2004; 73: 71–78
  • CDC. Update: Influenza Activity—United States, 2003–2004 season. Morb Mortal Wkly Rep 2004; 53: 284–287
  • Govorkova E. A., Webby R. J., Humberd J., Seiler J. P., Webster R. G. Immunization with reverse-genetics-produced H5N1 influenza vaccine protects ferrets against homologous and heterologous challenge. J Infect Dis 2006; 194: 159–167
  • Lipatov A. S., Hoffmann E., Salomon R., Yen H. L., Webster R. G. 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 2006; 194: 1040–1043
  • Onishchenko G. G., Zverev V. V., Katlinskii A. V., Semchenko A. V., Korovkin S. A., Mel'nikov S. Ia., Mironov A. N. Tetravaccine–new fundamental approach to prevention of influenza pandemic. Zh Mikrobiol Epidemiol Immunobiol 2007; 4: 15–19
  • Webby R., Perez D. R., Coleman J. S., Guan Y., Knight J. H., Govorkova E. A., McClain-Moss L. R., Peiris J. S., Rehg J. E., Tuomanen E. I., Webster R. G. Responsiveness to a pandemic alert: use of reverse genetics for rapid development of influenza vaccines. Lancet 2004; 363: 1099–1103
  • Hoffmann E., Lipatov A. S., Webby R. J., Govorkova E. A., Webster R. G. Role of specific hemagglutinin amino acids in the immunogenicity and protection of H5N1 influenza virus vaccines. Proc Natl Acad Sci USA 2005; 102: 12915–12920
  • Lipatov A. S., Webby R. J., Govorkova E. A., Krauss S., Webster R. G. Efficacy of H5 influenza vaccines produced by reverse genetics in a lethal mouse model. J Infect Dis 2005; 191: 1216–1220
  • Tian G., Zhang S., Li Y., Bu Z., Liu P., Zhou J., Li C., Shi J., Yu K., Chen H. Protective efficacy in chickens, geese and ducks of an H5N1-inactivated vaccine developed by reverse genetics. Virology 2005; 341: 153–162
  • Girard M., Cherian T, Pervikov Y., Kieny M. P. A review of vaccine research and development: human acute respiratory infections. Vaccine 2005; 23: 5708–5724
  • Fauci A. S. Pandemic influenza threat and preparedness. Emerg Infect Dis 2006; 12: 73–77
  • Shi H., Liu X. F., Zhang X., Chen S., Sun L., Lu J. Generation of an attenuated H5N1 avian influenza virus vaccine with all eight genes from avian viruses. Vaccine 2007; 25: 7379–7384
  • Cinatl J. J., Michaelis M., Doerr H. W. The threat of avian influenza A (H5N1). Part IV: Development of vaccines. Med Microbiol Immunol 2007; 196: 213–225
  • Treanor J. J., Schiff G. M., Couch R. B., Cate T. R., Brady R. C., Hay C. M., Wolff M., She D., Cox M. M. Dose-related safety and immunogenicity of a trivalent baculovirus-expressed influenza-virus hemagglutinin vaccine in elderly adults. J Infect Dis 2006; 193: 1223–1228
  • Wang K., Holtz K. M., Anderson K., Chubet R., Mahmoud W., Cox M. M. Expression and purification of an influenza hemagglutinin—one step closer to a recombinant protein-based influenza vaccine. Vaccine 2006; 24: 2176–2185
  • Galarza J. M., Latham T., Cupo A. Virus-like particle (VLP) vaccine conferred complete protection against a lethal influenza virus challenge. Viral Immunol. 2005; 18: 244–251
  • Bright R. A., Carter D. M., Daniluk S., Toapanta F. R., Ahmad A., Gavrilov V., Massare M., Pushko P., Mytle N., Rowe T., Smith G., Ross T. M. Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine 2007; 25: 3871–3878
  • Galarza J. M., Latham T., Cupo A. Virus-like particle vaccine conferred complete protection against a lethal influenza virus challenge. Viral Immunol 2005; 18: 365–372
  • Matassov D., Cupo A., Galarza J. M. A novel intranasal virus-like particle (VLP) vaccine designed to protect against the pandemic 1918 influenza A virus (H1N1). Viral Immunol 2007; 20: 441–452
  • Pushko P. T. T. M., Bu F., Knell J., Robinson R., Smith G. Influenza virus-like particles comprised of the HA, NA, and M1 proteins of H9N2 influenza virus induce protective immune responses in BALB/c mice. Vaccine 2005; 23: 5751–5759
  • Treanor J. J., Schiff G. M., Hayden F. G., Brady R. C., Hay C. M., Meyer A. L., Holden-Wiltse J., Liang H., Gilbert A., Cox M. Safety and immunogenicity of a baculovirus-expressed hemagglutinin influenza vaccine: a randomized controlled trial. JAMA 2007; 297: 1577–1582
  • Carrat F., Flahault A. Influenza vaccine: the challenge of antigenic drift. Vaccine 2007; 25: 6852–6862
  • Kendal A. P. 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 1997; 13: 591–609
  • Belshe R. B., Edwards K. M., Vesikari T., Black S. V., Walker R. E., Hultquist M., Kemble G., Connor E. M. CAIV-T Comparative Efficacy Study Group. Live attenuated versus inactivated influenza vaccine in infants and young children. N Engl J Med 2007; 356: 685–696
  • Belshe R. B., Maassab H. F., Mendelman P. M. Influenza Vaccine- Live. Orenstein, S. A. Vaccines, W. A. Plotkin. Elsevier, Philadelphia 2004; 371–388
  • Ohmit S. E., Victor J. C., Rotthoff J. R., Teich E. R., Truscon R. K., Baum L. L., Rangarajan B., Newton D. W., Boulton M. L., Monto A. S. Prevention of antigenically drifted influenza by inactivated and live attenuated vaccines. N Engl J Med 2006; 355: 2513–2522
  • Jameson J., Cruz J., Ennis F. A. Human cytotoxic T-lymphocyte repertoire to influenza A viruses. J Virol 1998; 72: 8682–8689
  • Boon A. C., de Mutsert G., van Baarle D., Smith D. J., Lapedes A. S., Fouchier R. A., Sintnicolaas K., Osterhaus A. D., Rimmelzwaan G. F. Recognition of homo- and heterosubtypic variants of influenza A viruses by human CD8+ T lymphocytes. J Immunol 2004; 172: 2453–2460
  • Jameson J., Cruz J., Terajima M., Ennis F. A. Human CD8+ and CD4+ T lymphocyte memory to influenza A viruses of swine and avian species. J Immunol 1999; 162: 7578–7583
  • Seo S. H., Webster R. G. Cross-reactive, cell-mediated immunity and protection of chickens from lethal H5N1 influenza virus infection in Hong Kong poultry markets. J Virol 2001; 75: 2516–2525
  • Li S., Liu C., Klimov A., Subbarao K., Perdue M. L., Mo D., Ji Y., Woods L., Hietala S., Bryant M. Recombinant influenza A virus vaccines for the pathogenic human A/Hong Kong/97 (H5N1) viruses. J Infect Dis 1999; 179: 1132–1138
  • Suguitan A. L., McAuliffe J. J., Mills K. L., Jin H., Duke G., Lu B., Luke C. J., Murphy B., Swayne D. E., Kemble G., Subbarao K. Live, attenuated influenza A H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS ONE. 2006; 3: e360
  • Lu X., Edwards L. E., Desheva J. A., Nguyen D. C., Rekstin A., Stephenson I., Szretter K., Cox N. J., Rudenko L. G., Klimov A., Katz J. M. Cross-protective immunity in mice induced by live-attenuated or inactivated vaccines against highly pathogenic influenza A (H5N1) viruses. Vaccine 2006; 24: 6588–6593
  • Desheva J. A., Lu X. H., Rekstin A. R., Rudenko L. G., Swayne D. E., Cox N. J., Katz J. M., Klimov A. I. 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: 6859–6866
  • Song H., Nieto G. R., Perez D. R. A new generation of modified live-attenuated avian influenza viruses using a two-strategy combination as potential vaccine candidates. J Virol 2007; 81: 9238–9248
  • Wang X., Li M., Zheng H., Muster T., Palese P., Beg A. A., García-Sastre A. Influenza A virus NS1 protein prevents activation of NF-kappaB and induction of alpha/beta interferon. J Virol 2000; 74: 11566–11573
  • Donelan N., Basler C. F., García-Sastre A. A recombinant influenza A virus expressing an RNA-binding-defective NS1 protein induces high levels of beta interferon and is attenuated in mice. J Virol. 2003; 77: 13257–13266
  • Egorov A., Brandt S., Sereinig S., Romanova J., Ferko B., Katinger D., Grassauer A., Alexandrova G., Katinger H., Muster T. Transfectant influenza A viruses with long deletions in the NS1 protein grow efficiently in Vero cells. J Virol. 1998; 72: 6437–6441
  • Talon J., Salvatore M., O'Neill R. E., Nakaya Y., Zheng H., Muster T., Garcia-Sastre A., Palese P. Influenza A and B viruses expressing altered NS1 proteins: A vaccine approach. Proc. Natl. Acad. Sci. USA 2000; 97: 4309–4314
  • Garcia-Sastre A., Egorov A., Matassov D., Brandt S., Levy D. E., Durbin J. E., Palese P., Muster T. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology. 1998; 252: 324–330
  • Quinlivan M., Zamarin D., García-Sastre A., Cullinane A., Chambers T., Palese P. Attenuation of equine influenza viruses through truncations of the NS1 protein. J Virol. 2005; 79: 8431–8439
  • Ferko B., Stasakova J., Romanova J., Kittel C., Sereinig S., Katinger H., Egorov A. Immunogenicity and protection efficacy of replication-deficient influenza A viruses with altered NS1 genes. J Virol. 2004; 78: 13037–13045
  • 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. Type I IFN as a natural adjuvant for a protective immune response: lessons from the influenza vaccine model. J Immunol. 2002; 169: 375–383
  • Richt J. A., Lekcharoensuk P., Lager K. M., Vincent A. L., Loiacono C. M., Janke B. H., Wu W. H., Yoon K. J., Webby R. J., Solórzano A., García-Sastre A. Vaccination of pigs against swine influenza viruses by using an NS1-truncated modified live-virus vaccine. J Virol 2006; 80: 11009–11018
  • Vincent A. L., Ma W., Lager K. M., Janke B. H., Webby R. J., García-Sastre A., Richt J. A. Efficacy of intranasal administration of a truncated NS1 modified live influenza virus vaccine in swine. Vaccine 2007; 25: 7999–8009
  • Watanabe T., Watanabe S., Ito H., Kida H., Kawaoka Y. Influenza A virus can undergo multiple cycles of replication without M2 ion channel activity. J Virol 2001; 75: 5656–5662
  • Takeda M., Pekosz A., Shuck K., Pinto L. H., Lamb R. A. Influenza a virus M2 ion channel activity is essential for efficient replication in tissue culture. J Virol 2002; 76: 1391–1399
  • Iwatsuki-Horimoto K., Horimoto T., Noda T., Kiso M., Maeda J., Watanabe S., Muramoto Y., Fujii K., Kawaoka Y. The cytoplasmic tail of the influenza A virus M2 protein plays a role in viral assembly. J Virol 2006; 80: 5233–5240
  • McCown M. F., Pekosz A. The influenza A virus M2 cytoplasmic tail is required for infectious virus production and efficient genome packaging. J Virol 2005; 79: 3595–3605
  • McCown M. F., Pekosz A. Distinct domains of the influenza a virus M2 protein cytoplasmic tail mediate binding to the M1 protein and facilitate infectious virus production. J Virol 2006; 80: 3595–3605
  • Watanabe T., Watanabe S., Kida H., Kawaoka Y. Influenza A virus with defective M2 ion channel activity as a live vaccine. Virology 2002; 299: 266–270
  • Watanabe T., Watanabe S., Kim J. H., Hatta M., Kawaoka Y. Novel approach to the development of effective H5N1 influenza A virus vaccines: use of M2 cytoplasmic tail mutants. J Virol 2008; 82: 2486–2492
  • Wolff J. A., Malone R. W., Williams P., Chong W., Acsadi G., Jani A., Felgner P. L. Direct gene transfer into mouse muscle in vivo. Science. 1990; 247: 1465–1468
  • Ulmer J. B., Donnelly J. J., Parker S. E., Rhodes G. H., Felgner P. L., Dwarki V. J., Gromkowski S. H., Deck R. R., DeWitt C. M., Friedman A., Hawe L. A., Leander K. R., Martinez D., Perry H. C., Shiver J. W., Montgomery D. L., Liu M. A. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science. 1993; 259: 1745–1749
  • Ulmer J. B., Fu T. M., Deck R. R., Friedman A., Guan L., DeWitt C., Liu X., Wang S., Liu M. A., Donnelly J. J., Caulfield M. J. Protective CD4+ and CD8+ T cells against influenza virus induced by vaccination with nucleoprotein DNA. J Virol 1998; 72: 5648–5653
  • Robinson H. L., Hunt L. A., Webster R. G. Protection against a lethal influenza virus challenge by immunization with a haemagglutinin-expressing plasmid DNA. Vaccine 1993; 11: 957–960
  • Donnelly J. J., Friedman A., Martinez D., Montgomery D. L., Shiver J. W., Motzel S. L., Ulmer J. B., Liu M. A. Preclinical efficacy of a prototype DNA vaccine: enhanced protection against antigenic drift in influenza virus. Nat. Med. 1995; 1: 583–587
  • Epstein S., Stack A., Misplon J. A., Lo C. Y., Mostowski H., Bennink J., Subbarao K. Vaccination with DNA encoding internal proteins of influenza virus does not require CD8(+) cytotoxic T lymphocytes: either CD4(+) or CD8(+) T cells can promote survival and recovery after challenge. Int. Immunol. 2000; 12: 91–101
  • Fu T. M., Guan L., Friedman A., Schofield T. L., Ulmer J. B., Liu M. A., Donnelly J. J. Dose dependence of CTL precursor frequency induced by a DNA vaccine and correlation with protective immunity against influenza virus challenge. J Immunol. 1999; 162: 4163–4170
  • Ljungberg K., Wahren B., Almqvist J., Hinkula J., Linde A., Winberg G. Effective construction of DNA vaccines against variable influenza genes by homologous recombination. Virology 2000; 268: 244–250
  • Epstein S., Kong W. P., Misplon J. A., Lo C. Y., Tumpey T. M., Xu L., Nabel G. J. Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine. 2005; 23: 5404–5410
  • Liu M. A., McClements W., Ulmer J. B., Shiver J., Donnelly J. Immunization of non-human primates with DNA vaccines. Vaccine. 1997; 15: 909–912
  • Robinson H. L., Boyle C. A., Feltquate D. M., Morin M. J., Santoro J. C., Webster R. G. DNA immunization for influenza virus: studies using hemagglutinin- and nucleoprotein-expressing DNAs. J Infect Dis 1997; 176: S50–S55
  • Kodihalli S., Goto H., Kobasa D. L., Krauss S., Kawaoka Y., Webster R. G. DNA vaccine encoding hemagglutinin provides protective immunity against H5N1 influenza virus infection in mice. J. Virol. 1999; 73: 2094–2098
  • Chen Z., Yoshikawa T., Kadowaki S., Hagiwara Y., Matsuo K., Asanuma H., Aizawa C., Kurata T., Tamura S. Protection and antibody responses in different strains of mouse immunized with plasmid DNAs encoding influenza virus haemagglutinin, neuraminidase and nucleoprotein. J. Gen. Virol. 1999; 80: 2559–2564
  • Chen Z., Matsuo K., Asanuma H., Takahashi H., Iwasaki T., Suzuki Y., Aizawa C., Kurata T., Tamura S. Enhanced protection against a lethal influenza virus challenge by immunization with both hemagglutinin- and neuraminidase-expressing DNAs. Vaccine. 1999; 17: 653–659
  • Epstein S., Tumpey T. M., Misplon J. A., Lo C. Y., Cooper L. A., Subbarao K., Renshaw M., Sambhara S., Katz J. M. DNA vaccine expressing conserved influenza virus proteins protective against H5N1 challenge infection in mice. Emerg. Infect. Dis. 2002; 8: 796–801
  • Wang S., Taaffe J., Parker C., Solorzano A., Cao H., Garcia-Sastre A., Lu S. Hemagglutinin (HA) proteins from H1 and H3 serotypes of influenza A viruses require different antigen designs for the induction of optimal protective antibody responses as studied by codon-optimized HA DNA vaccines. J Virol 2006; 80: 11628–11637
  • Jiang Y., Yu K., Zhang H., Zhang P., Li C., Tian G., Li Y., Wang X., Ge J., Bu Z., Chen H. Enhanced protective efficacy of H5 subtype avian influenza DNA vaccine with codon optimized HA gene in a pCAGGS plasmid vector. Antviral Res. 2007; 75: 234–241
  • Jimenez G. S., Planchon R., Wei Q., Rusalov D., Geall A., Enas J., Lalor P., Leamy V., Vahle R., Luke C. J., Rolland A., Kaslow D. C., Smith L. R. Vaxfectin-formulated influenza DNA vaccines encoding NP and M2 viral proteins protect mice against lethal viral challenge. Hum. Vaccin. 2007; 3: 157–164
  • Ohba K., Yoshida S., Zahidunnabi D. M., Shimura H., Sakamaki N., Takeshita F., Yamamoto N., Okuda K. Mutant influenza A virus nucleoprotein is preferentially localized in the cytoplasm and its immunization in mice shows higher immunogenicity and cross-reactivity. Vaccine 2007; 25: 4291–4300
  • Tompkins S., Zhao Z. S., Lo C. Y., Misplon J. A., Liu T., Ye Z., Hogan R. J., Wu Z., Benton K. A., Tumpey T. M., Epstein S. L. Matrix protein 2 vaccination and protection against influenza viruses, including subtype H5N1. Emerg. Infect. Dis. 2007; 13: 426–435
  • Draghia-Akli R., Khan A. S., Brown P. A., Pope M. A., Wu L., Hirao L., Weiner D. B. Parameters for DNA vaccination using adaptive constant-current electroporation in mouse and pig models. Vaccine 2008; 26
  • Khan A. S., Pope M. A., Draghia-Akli R. Highly efficient constant-current electroporation increases in vivo plasmid expression. DNA Cell Biol. 2005; 24: 810–818
  • Tjelle T. E., Rabussay D., Ottensmeier C., Mathiesen I., Kjeken R. Taking electroporation-based delivery of DNA vaccination into humans: a generic clinical protocol. Methods Mol. Biol. 2008; 423: 497–507
  • Jean Patterson L., Peng B., Nan X., Robert-Guroff M. Live adenovirus recombinants as vaccine vectors. New Generation Vaccines, M. Levine, J. B. Kaper, R. Rappuoli, M. A. Liu, M. F. Good. Marcel Dekker, New York, Basel 2004; 325–336
  • Lo C. Y., Wu Z., Misplon J. A., Price G. E., Pappas C., Kong W. P., Tumpey T. M., Epstein S. L. Comparison of vaccines for induction of heterosubtypic immunity to influenza A virus: cold-adapted vaccine versus DNA prime-adenovirus boost strategies. Vaccine. 2008; 26: 2062–2072
  • Hoelscher M., Garg S., Bangari D. S., Belser J. A., Lu X., Stephenson I., Bright R. A., Katz J. M., Mittal S. K., Sambhara S. Development of adenoviral-vector-based pandemic influenza vaccine against antigenically distinct human H5N1 strains in mice. Lancet. 2006; 367: 475–481
  • Gao W., Soloff A. C., Lu X., Montecalvo A., Nguyen D. C., Matsuoka Y., Robbins P. D., Swayne D. E., Donis R. O., Katz J. M., Barratt-Boyes S. M., Gambotto A. Protection of mice and poultry from lethal H5N1 avian influenza virus through adenovirus-based immunization. J Virol 2006; 80: 1959–1964
  • Wesley R., Tang M., Lager K. M. Protection of weaned pigs by vaccination with human adenovirus 5 recombinant viruses expressing the hemagglutinin and the nucleoprotein of H3N2 swine influenza virus. Vaccine. 2004; 22: 3427–3434
  • Roy S., Kobinger G. P., Lin J., Figueredo J., Calcedo R., Kobasa D., Wilson J. M. Partial protection against H5N1 influenza in mice with a single dose of a chimpanzee adenovirus vector expressing nucleoprotein. Vaccine. 2007; 25: 6845–6851
  • HIV vaccine failure prompts Merck to halt trial. Nature. 2007; 449: 390
  • Failed HIV vaccine may have increased vulnerability to infection. Clin Infect Dis 2008; 46: iii
  • Sekaly R. P. The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development?. J. Exp. Med. 2008; 205: 7–12
  • Karaca K., Swayne D. E., Grosenbaugh D., Bublot M., Robles A., Spackman E., Nordgren R. Immunogenicity of fowlpox virus expressing the avian influenza virus H5 gene (TROVAC AIV-H5) in cats. Clin Diagn Lab Immunol 2005; 12: 1340–1342
  • Veits J., Wiesner D., Fuchs W., Hoffmann B., Granzow H., Starick E., Mundt E., Schirrmeier H., Mebatsion T., Mettenleiter T. C., Romer-Oberdorfer A. Newcastle disease virus expressing H5 hemagglutinin gene protects chickens against Newcastle disease and avian influenza. Proc Natl Acad Sci USA 2006; 103: 8197–8202
  • Sylte M. J., Hubby B., Suarez D. L. Influenza neuraminidase antibodies provide partial protection for chickens against high pathogenic avian influenza infection. Vaccine 2007; 25: 3763–3772
  • Hubby B., Talarico T., Maughan M., Reap E. A., Berglund P., Kamrud K. I., Copp L., Lewis W., Cecil C., Norberg P., Wagner J., Watson A., Negri S., Burnett B. K., Graham A., Smith J. F., Chulay J. D. Development and preclinical evaluation of an alphavirus replicon vaccine for influenza. Vaccine 2007; 25: 8180–8189
  • Neirynck S., Deroo T., Saelens X., Vanlandschoot P., Jou W. M., Fiers W. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat. Med. 1999; 5: 1157–1163
  • Fiers W., De Filette M., Birkett A., Neirynck S., Min Jou W. A “universal” human influenza A vaccine. Virus Research 2004; 103: 173–176
  • De Filette M., Min Jou W., Birkett A., Lyons K., Schultz B., Tonkyro A., Resch S., Fiers W. Universal influenza A vaccine: optimization of M2-based constructs. Virology. 2005; 337: 149–161
  • De Filette M., Fiers W., Martens W., Birkett A., Ramne A., Lowenadler B., Lycke N., Jou W. M., Saelens X. Improved design and intranasal delivery of an M2e-based human influenza A vaccine. Vaccine 2006; 24: 6597–6601
  • Zou P., Liu W., Chen Y. H. The epitope recognized by a monoclonal antibody in influenza A virus M2 protein is immunogenic and confers immune protection. Int. Immunopharmacol. 2005; 5: 631–635
  • Fan J., Liang X., Horton M. S., Perry H. C., Citron M. P., Heidecker G. J., Fu T. M., Joyce J., Przysiecki C. T., Keller P. M., Garsky V. M., Ionescu R., Rippeon Y., Shi L., Chastain M. A., Condra J. H., Davies M. E., Liao J., Emini E. A., Shiver J. W. Preclinical study of influenza virus A M2 peptide conjugate vaccines in mice, ferrets, and rhesus monkeys. Vaccine 2004; 22: 2993–3003
  • Jegerlehner A., Schmitz N., Storni T., Bachmann M. F. Influenza A vaccine based on the extracellular domain of M2: weak protection mediated via antibody-dependent NK cell activity. J. Immunol. 2004; 172: 5598–5605
  • Slepushkin V. A., Katz J. M., Black R. A., Gamble W. C., Rota P. A., Cox N. J. Protection of mice against influenza A virus challenge by vaccination with baculovirus-expressed M2 protein. Vaccine 1995; 13: 1399–1402
  • Ernst W. A., Kim H. J., Tumpey T. M., Jansen A. D., Tai W., Cramer D. V., Adler-Moore J. P., Fujii G. Protection against H1, H5, H6 and H9 influenza A infection with liposomal matrix 2 epitope vaccines. Vaccine 2006; 24: 5158–5168
  • Huleatt J. W., Nakaar V., Desai P., Huang Y., Hewitt D., Jacobs A., Tang J., McDonald W., Song L., Evans R. K., Umlauf S., Tussey L., Powell T. J. Potent immunogenicity and efficacy of a universal influenza vaccine candidate comprising a recombinant fusion protein linking influenza M2e to the TLR5 ligand flagellin. Vaccine 2008; 26: 201–214
  • Frace A. M., Klimov A. I., Rowe T., Black R. A., Katz J. M. Modified M2 proteins produce heterotypic immunity against influenza A virus. Vaccine 1999; 17: 2237–2244
  • Ilyinskii P., Gabai V. L., Sunyaev S. R., Thoidis G., Shneider A. M. Toxicity of Influenza A Virus Matrix Protein 2 for Mammalian Cells is Associated with its Intrinsic Proton-Channeling Activity. Cell Cycle. 2007; 6: 2043–2047
  • Saha S., Yoshida S., Ohba K., Matsui K., Matsuda T., Takeshita F., Umeda K., Tamura Y., Okuda K., Klinman D., Xin K. Q., Okuda K. A fused gene of nucleoprotein (NP) and herpes simplex virus genes (VP22) induces highly protective immunity against different subtypes of influenza virus. Virology. 2006; 354: 48–57
  • Wong S. B., Buck C. B. J., Shen X., Siliciano R. F. An evaluation of enforced rapid proteasomal degradation as a means of enhancing vaccine-induced CTL responses. J. Immunol. 2004; 173: 3073–3083
  • Altstein A. D., Gitelman A. K., Smirnov Y. A., Piskareva L. M., Zakharova L. G., Pashvykina G. V., Shmarov M. M., Zhirnov O. P., Varich N. P., Ilyinskii P. O., Shneider A. M. Immunization with influenza A NP-expressing vaccinia virus recombinant protects mice against experimental infection with human and avian influenza viruses. Arch. Virol. 2006; 151: 921–931
  • Ilyinskii P. O., Meriin A. B., Gabai V. L., Zhirnov O. P., Thoidis G., Shneider A. M. Prime-boost vaccination with a combination of proteosome-degradable and wild-type forms of two influenza proteins leads to augmented CTL response. Vaccine 2008; 26: 2177–2185
  • Chen Z., Sahashi Y., Matsuo K., Asanuma H., Takahashi H., Iwasaki T., Suzuki Y., Aizawa C., Kurata T., Tamura S. Comparison of the ability of viral protein-expressing plasmid DNAs to protect against influenza. Vaccine 1998; 16: 1544–1549
  • Doherty P. C., Turner S. J., Webby R. G., Thomas P. G. Influenza and the challenge for immunology. Nat Immunol 2006; 7: 449–455

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