Cross-clade protective immune responses to influenza viruses with H5N1 HA and NA elicited by an influenza virus-like particle

PLoS ONE

Volumn 3, Issue 1, 2008, Pages

  Bright, Rick A ^a   Carter, Donald M ^b   Crevar, Corey J ^b   Toapanta, Franklin R ^b   Steckbeck, Jonathan D ^b   Cole, Kelly S ^b   Kumar, Niranjan M ^a   Pushko, Peter ^a   Smith, Gale ^a   Tumpey, Terrence M ^c   Ross, Ted M ^b  

^a NOVAVAX INC   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HN PROTEIN; INFLUENZA VACCINE; RECOMBINANT VACCINE; VIROTHERAPY AGENT; VIRUS ANTIGEN; VIRUS HEMAGGLUTININ; HEMAGGLUTININ, HUMAN INFLUENZA A VIRUS; INFLUENZA VIRUS HEMAGGLUTININ; SIALIDASE; VIRUS ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY DETECTION; ANTIBODY TITER; ANTIGEN BINDING; ARTICLE; AVIAN INFLUENZA; BACULOVIRUS EXPRESSION SYSTEM; CELLULAR IMMUNITY; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG DOSE REGIMEN; DRUG EFFICACY; FEMALE; HUMORAL IMMUNITY; IMMUNE RESPONSE; INFECTION PREVENTION; INFLUENZA VACCINATION; INFLUENZA VIRUS A H5N1; INSECT CELL; MOUSE; NONHUMAN; PANDEMIC; SINGLE DRUG DOSE; VIROTHERAPY; VIRUS ISOLATION; VIRUS LIKE AGENT; VIRUS RECOMBINATION; WEIGHT REDUCTION; ANIMAL; ARMYWORM; BACULOVIRUS; BIOSYNTHESIS; CROSS REACTION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYMOLOGY; IMMUNOLOGY; ISOLATION AND PURIFICATION; SURFACE PLASMON RESONANCE; VIRION;

HEXAPODA; MAMMALIA; MUS; ORTHOMYXOVIRIDAE;

ANIMALS; ANTIBODIES, VIRAL; BACULOVIRIDAE; CROSS REACTIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; IMMUNITY, CELLULAR; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; MICE; NEURAMINIDASE; SPODOPTERA; SURFACE PLASMON RESONANCE; VIRION;

EID: 42949157327     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0001501     Document Type: Article

References (79)

1. Gillim-Ross L, Subbarao K (2006) Emerging respiratory viruses: challenges and vaccine strategies. Clin Microbiol Rev 19: 614-636.
2. Luke CJ, Subbarao K (2006) Vaccines for pandemic influenza. Emerg Infect Dis 12: 66-72.
3. Subbarao, K, Murphy BR, Fauci AS (2006) Development of effective vaccines against pandemic influenza. Immunity 24: 5-9.
4. Suguitan AL Jr, McAuliffe J, Mills KL, Jin H, Duke G, et al. (2006) Live, attenuated influenza A H5N1 candidate vaccines provide broad cross-protection in mice and ferrets. PLoS Med 3: c360.
5. Leroux-Roels I, Borkowski A, Vanwolleghem T, Drame M, Clement F, et al. (2007) Antigen sparing and cross-reactive immunity with an adjuvanted rH5NI prototype pandemic influenza vaccine: a randomised controlled trial. Lancet 370: 580-589.
6. Subbarao K, Klimox A, Katz J, Regnery H, Lim W, et al. (1998) Characterization of an avian influenza A (H5N1) virus isolated from a chiid with a fatal respiratory illness. Science 279: 393-396.
7. Cheung CL, Rayner JM, Smith GJ, Wang P, Naipospos TS, et al. (2006) Distribution of amantadine-resistant H5N1 avian influenza variants in Asia. J Infect Dis 193: 1626-1629.
8. de Jong MD, Tran TT, Truong HK, Vo MH, Smith GJ, et al. (2005) Oseltamivir resistance during treatment of influenza A (H5N1) infection. N Engl J Med 353: 2667-2672.
9. Hurt AC, Selleck P, Komadina N, Shaw R, Brown L, et al. (2006) Susceptibility of highly pathogenic A(H5N1) avian influenza viruses to the neuraminidase inhibitors and adamantanes. Antiviral Res.
10. Le QM, Kiso M, Someya K, Sakai YT, Nguyen TH, et al. (2005) Avian flu: isolation of drug-resistant H5N1 virus. Nature 437: 1108.
11. Stohr K (2005) Avian Influenza and Pandemics - Research Needs and Opportunities. N Fngl J Med 352: 333-340.
12. Organization WH (2006) Recommendation of Pandemic Vaccine Selection. http://www.who.int/csr/disease/influenza/mission/en/ accessed Jan 2008.
13. Organization WH. (2006) Avian influenza - situation in Indonesia - update 35. http://www.who.int/csr/don/2006_10_03/en/index.html accessed Jan 2008.
14. Pushko P, Tumpey TM, Bu F, Knell J, Robinson R, et al. (2005) Influenza virus-like particles comprised of the HA, NA, and MI proteins of H9N2 influenza virus induce protective immune responses in BALB/c mice. Vaccine 23: 5751-5759.
15. Bright RA, Carter DM, Daniluk S, Ahmad A, Massare M, et al. (2007) Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine 25: 3871-3878.
16. Reed L, Muench H (1938) A simple method of estimating fifty percent endpoints. Am J Hyg 27: 493-497.
17. Organization WH (2005) Emerging Infectious Diseases. Emerg Infect Dis II: 1515-1521.
18. Wood J, Schild G, Newman R, Seagroatt V (1997) Application of an improved single-radial-immunodiffusion technique for the assay of haemagglutinin antigen content of whole virus and subunit influenza vaccines. Dev Biol Stand 39: 193-200.
19. Bower JF, Green TD, Ross TM (2004) DNA vaccines expressing soluble CD4-envelope proteins fused to C3d elicit cross-reactive neutralizing antibodies to HIV-1. Virology 328: 292-300.
20. Bower JF, Sanders KL, Ross TM (2005) C3d enhances immune responses using low doses of DNA expressing the HIV-1 envelope from codon-optimized gene sequences. Curr HIV Res 3: 191-198.
21. Bright RA, Ross TM, Subbarao K, Robinson HL, Katz JM (2003) Impact of glycosylation on the immunogenicity of a DNA-based influenza H5 HA vaccine. Virology 308: 270-278.
22. Mitchell JA, Green TD, Bright RA, Ross TM (2003) Induction of heterosubtypic immunity to influenza A virus using a DNA vaccine expressing hemagglutinin-C3d fusion proteins. Vaccine 21: 902-914.
23. Ross TM, Xu Y, Bright RA, Robinson HL (2000) C3d enhancement of antibodies to hemagglutinin accelerates protection against influenza virus challenge. Nat Immumol 1: 127-131.
24. Toapanta FR, Ross TM (2004) Mouse strain-dependent differences in enhancement of immune responses by C3d. Vaccine 22: 1773-1781.
25. Bright RA, Medina MJ, Xu X, Perez-Oronoz G, Wallis TR, et al. (2005) Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 366: 1175-1181.
26. Bright RA, Shay DK, Shu B, Cox NJ, Klimov AI (2006) Adamantane resistance among influenza A viruses isolated early during the 2005-2006 influenza season in the United States. JAMA 295: 891-894.
27. Askonas B, McMichael A, Webster R (1982) The immune response to influenza viruses and the problem of protection against infection, in Bascin and applied influenza research. e. Beare AS, ed. CRC Press. pp 159-188.
28. Szucs TD, Ruef C, Muller D, Sokolovic E, Beeler I, et al. (2001) The economic impact of influenza in a university hospital setting. Infect Control Hosp Epidemiol 22: 472-474.
29. Tobita K (1975) Permanent canine kidney (MDCK) cells for isolation and plaque assay of influenza B viruses. Med Microbiol Immunol 162: 23-27.
30. Tobita K, Sugiura A, Enomote C, Furuyama M (1975) Plaque assay and primary isolation of influenza A viruses in an established line of canine kidney cells (MDCK) in the presence of trypsin. Med Microbiol Immunol 162: 9-14.
31. Steckbeck JD, Grieser HJ, Sturgeon T, Taber R, Chow A, et al. (2006) Dynamic evolution of antibody populations in a rhesus macaque infected with attenuated simian immunodeficiency virus identified by surface plasmon resonance. J Med Primatol 35: 248-260.
32. Steckbeck JD, Orlov I, Chow A, Grieser H, Miller K, et al. (2005) Kinetic rates of antibody binding correlate with neutralization sensitivity of variant simian immunodeficiency virus strains. J Virol 79: 12311-12320.
33. Braciale TJ, Yap KL (1978) Role of viral infectivity in the induction of influenza virus-specific cytotoxic T cells. J Exp Med 147: 1236-1252.
34. Hoelscher MA, Garg S, Bangari DS, Belser JA, Lu X, et al. (2006) Development of adenoviral-vector-based pandemic influenza vaccine against antigenically distinct human H5N1 strains in mice. Lancet 367: 475-481.
35. Lalvani A, Dong T, Ogg G, Patham AA, Newell H, et al. (1997) Optimization of a peptide-based protocol employing IL-7. for in vitro restimulation of human cytotoxic T lymphocyte precursors. J Immunol Methods 210: 65-77.
36. Sambhara S, Kurichh A, Miranda R, James O, Underdown B, et al. (2001) Severe impairment of primary but not memory responses to influenza viral antigens in aged mice: costimulation in vivo partially reverses impaired primary immune responses. Cell Immunol 210: 1-4.
37. Sambhara S, Kurichh A, Miranda R, Tumpey T, Rowe T, et al. (2001) Heterosubtypic immunity against human influenza A viruses, including recently emerged avian H5 and H9 viruses, induced by FLU-ISCOM vaccine in mice requires both cytotoxic T-lymphocyte and macrophage function. Cell Immunol 211: 143-153.
38. Yap KL, Ada GL, McKenzie IF (1978) Transfer of specific cytotoxic T lymphocytes protects mice inoculated with influenza virus. Nature 273: 238-239.
39. Sandbulte MR, Jimenez GS, Boon AC, Smith LR, Treanor JJ, et al. (2007) Cross-Reactive Neuraminidase Antibodies Afford Partial Protection against H5N1 in Mice and Are Present in Unexposed Humans. PLoS Med 4: e59.
40. Haffar OK, Smithgall MD, Moran PA, Travis BM, Zarling JM, et al. (1991) HIV-specific humoral and cellular immunity in rabbits vaccinated with recombinant human immunodeficiency virus-like gag-env particles. Virology 183: 487-495.
41. McBurney SP, Young KR, Nwaigwe CI, Soloff AC, Cole KS, et al. (2006), Lentivirus-like particles without reverse transcriptase elicit efficient immune responses. Curr HIV Res 4: 475-484.
42. McBurney SP, Young KR, Ross TM (2006) Membrane embedded HIV-1 envelope on the surface of a virus-like particle elicits broader immune responses than soluble envelopes. Virology.
43. Young YR, Ross TM (2006) Elicitation of immunity to HIV type 1 Gag is determined by Gag structure. AIDS Res Hum Retroviruses 22: 99-108.
44. Despres P, Combredet C, Frenkiel MP, Lorin C, Brahic M, et al. (2005) Live measles vaccine expressing the secreted form of the West Nile virus envelope glycoprotein protects against West Nile virus encephalitis. J Infect Dis 191: 207-214.
45. Lorin C, Mollet L, Delebecque F, Combredet C, Hurtrel B, et al. (2004) A single injection of recombinant measle's virus vaccines expressing human immunodeficiency virus (HIV) type 1 clade B envelope glycoproteins induces neutralizing antibodies and cellular immune responses to HIV. J Virol 78: 146-157.
46. Evans TG, Bonnez W, Rose RC, Koenig S, Demeter L, et al. (2001) A Phase 1 study of a recombinant viruslike particle vaccine against human papillomavirus type 11 in healthy adult volunteers. J Infect Dis 183: 1485-1493.
47. Koutsky LA, Ault KA, Wheeler CM, Brown DR, Barr E, et al. (2002) A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 347: 1645-1651.
48. Asahi-Ozaki Y, Yoshikawa T, Iwakura Y, Suzuki Y, Tamura, S, et al. (2004) Secretory IgA antibodies provide cross-protection against infection with different strains of influenza B virus. J Med Virol 74: 328-335.
49. Liew FY, Russell SM, Appleyard G, Brand CM, Beale J (1984) Cross-protection in mice infected with influenza A virus by the respiratory route is correlated with local IgA antibody rather than serum antibody or cytotoxic T cell reactivity. Eur J Immunol 14: 350-356.
50. Yoshikawa T, Matsuo K, Matsuo K, Suzuki Y, Nommo A, et al. (2004) Total viral genome copies and virus-Ig complexes after infection with influenza virus in the nasal secretions of immunized mice. J Gen Virol 85: 2339-2346.
51. Chotpitayasunondh T, Ungchusak K, Hanshaoworakul W, Chunsuthiwat S, Sawanpanyalert P, et al. (2005) Human disease from influenza A (H5N1), Thailand, 2004. Emerg Infect Dis 11: 201-209.
52. Tran TH, Nguyen TL, Nguyen TD, Luong TS, Pham PM, et al. (2004) Avian influenza A (H5N1) in 10 patients in Vietnam. N Engl J Med 350: 1179-1188.
53. Yuen KY, Chan PK, Peiris M, Tsang DN, Que TL, et al. (1998) Clinical features and rapid viral diagnosis of human disease associated with avian influenza A H5N1 virus. Lancet 351: 467-471.
54. de Jong MD, Simmons CP, Thanh TT, Hien VM, Smith GJ, et al. (2006) Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat Med 12: 1203-1207.
55. Kozak W, Poli V, Soszynski D, Conn CA, Leon LR, et al. (1997) Sickness behavior in mice deficient in interleukin-6 during turpentine abscess and influenza pneumonitis. Am J Physiol 272: R621-630.
56. To KF, Chan PK, Chan KF, Lee WK, Lam WY, et al. (2001) Pathology of fatal human infection associated with avian influenza A H5N1 virus. J Med Virol 63: 242-246.
57. Cheung CY, Poon LL, Lau AS, Luk W, Lau YL, et al. (2002) Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet 360: 1831-1837.
58. Epstein SL, Lo CY, Misplon JA, Bennink JR (1998) Mechanism of protective immunity against influenza virus infection in mice without antibodies. J Immunol 160: 322-327.
59. Flynn KJ, Belz GT, Altman JD, Ahmed R, Woodland DL, et al. (1998) Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 8: 683-691.
60. Flynn KJ, Riberdy JM, Christensen JP, Altmam JD, Doherty PC (1999) In vivo proliferation of naive and memory influenza-specific CD8(+) T cells. Proc Natl Acad Sci U S A 96: 8597-8602.
61. Riberdy JM, Flynn KJ, Stech J, Webster RG, Altman JD, et al. (1999) Protection against a lethal avian influenza A virus in a mammalian system. J Viroll 73: 1453-1459.
62. Wiley JA, Cerwenka A, Harkema JR, Dutton RW, Harmsen AG (2001) Production of interferon-gamma by influenza hemagglutinin-specific CD8 effector T cells influences the development of pulmonary immunopathology. Am J Pathol 158: 119-130.
63. Wiley JA, Hogan RJ, Woodland DL, Harmsen AG (2001) Antigen-specific CDB(+) T cells persist in the upper respiratory tract following influenza virus infection. J Immumol 167: 3293-3299.
64. Tochikubo K, Isaka M, Yasuda Y, Kozuka S, Matano K, et al. (1998) Recombinant cholera toxin B subunit acts as an adjuvant for the mucosal and systemic responses ofmice to mucosally co-administered bovine serum albumin. Vaccine 16: 150-155.
65. Wu HY, Nguyen HH, Russell MW (1997) Nasal lymphoid tissue (NALT) as a mucosal immune inductive site. Scand J Immunol 46: 506-513.
66. Sminia T, Draal G (1999) Nasal-associated lymphoid tissue. Mucosal Immunology, Ogra PL, Lamm ME, Bienenstock J, Mestecky J, Stober W, McGhee JR, eds. Vol. 2. London: Academic Press. pp 357-364.
67. Tilney NL (1971) Patterns of lymphatic drainage in the adult laboratory rat. J Anat 109: 369-383.
68. Booy R, Brown LE, Grohmann GS, Macintyre CR (2006) Pandemic vaccines: promises and pitfalls. Med J Aust 185: S62-S65.
69. Bresson JL, Perronne C, Launay O, Gerdil C, Saville M, et al. (2006) Safety and immunogenicity of an inactivated split-virion influenza A/ Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet 367: 1657-1664.
70. Focosi D (2006) An inactivated subvirion influenza A (H5N1) vaccine. N Engl J Med 354: 2724-2725; author reply 2724-2725.
71. Gao W, Soloff AC, Lu X, Montecalvo A, Nguyen DC, et al. (2006) Protection of mice and poultry from lethal H5N1 avian influenza virus through adenovirus-based immunization. J Virol 80: 1959-1964.
72. 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: 159-167.
73. Lin J, Zhang J, Dong X, Fang H, Chen J, et al. (2006) Safety and immunogenicity of an inactivated adjuvanted whole-virion influenza A (H5N1) vaccine: a phase I randomised controlled trial. Lancet 368: 991-997.
74. 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: 2943-2952.
75. Qiao C, Yu K, Jiang Y, Li C, Tian G, et al. (2006) Development of a recombinant fowlpox virus vector-based vaccine of H5N1 subtype avian influenza. Dev Biol (Basel) 124: 127-132.
76. Stephenson I, Bugarini R, Nicholson KG, Podda A, Wood JM, et al. (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: 1210-1215.
77. 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 354: 1343-1351.
78. Webster RG, Webby RJ, Hoffmann E, Rodenberg J, Kumar M, et al. (2006) The immunogenicity and efficacy against H5N1 challenge of reverse genetics-derived H5N3 influenza vaccine in ducks and chickens. Virology 351: 303-311.
79. Subbarao K, Chen H, Swayne D, Mingay L, Fodor E, et al. (2003) Evaluation of a genetically modified reassortant H5N1 influenza A vinis vaccine candidate generated by plasmid-based reverse genetics. Virology 305: 192-200.