Antibody and T-cell responses to a virosomal adjuvanted H9N2 avian influenza vaccine: Impact of distinct additional adjuvants

Vaccine

Volumn 26, Issue 29-30, 2008, Pages 3640-3646

  Radošević, Katarina ^a   Rodriguez, Ariane ^a   Mintardjo, Ratna ^a   Tax, Dennis ^a   Bengtsson, Karin Lövgren ^b   Thompson, Catherine ^c   Zambon, Maria ^c   Weverling, Gerrit Jan ^a   UytdeHaag, Fons ^a   Goudsmit, Jaap ^a,d  

^a CRUCELL HOLLAND BV   (Netherlands)

^b Isconova AB   (Sweden)

^c PUBLIC HEALTH ENGLAND   (United Kingdom)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Adjuvant; Influenza; Virosome

Indexed keywords

ALUMINUM HYDROXIDE; ALUMINUM PHOSPHATE; ANTIVIRUS AGENT; AVIAN INFLUENZA VACCINE; IMMUNOGLOBULIN G2A; MATRIX M; N ACETYLMURAMYLALANYL DEXTRO ISOGLUTAMINYLALANYL DIPALMITOYLPHOSPHATIDYLETHANOLAMINE; VIROSOMAL ADJUVANTED H9N2 AVIAN INFLUENZA VACCINE; VIRUS ANTIBODY;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; AVIAN INFLUENZA; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG MEGADOSE; DRUG POTENTIATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HEMAGGLUTINATION INHIBITION TEST; IMMUNE RESPONSE; INFLUENZA VIRUS A H9N2; MONOTHERAPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL;

ADJUVANTS, IMMUNOLOGIC; ALUMINUM COMPOUNDS; ALUMINUM HYDROXIDE; ANIMALS; ANTIBODIES, VIRAL; BIRDS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; INFLUENZA A VIRUS, H9N2 SUBTYPE; INFLUENZA IN BIRDS; INFLUENZA VACCINES; LYMPHOCYTE SUBSETS; MICE; MICE, INBRED BALB C; PHOSPHATES; POLYSORBATES; SQUALENE; T-LYMPHOCYTES; VACCINES, VIROSOME;

EID: 45049086937     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2008.04.071     Document Type: Article

References (63)

1. WHO. Influenza fact sheets; 2007.
2. Atmar R.L., Keitel W.A., Patel S.M., Katz J.M., She D., El Sahly H., et al. Safety and immunogenicity of nonadjuvanted and MF59-adjuvanted influenza A/H9N2 vaccine preparations. Clin Infect Dis 43 9 (2006) 1135-1142
3. Nicholson K.G., Colegate A.E., Podda A., Stephenson I., Wood J., Ypma E., et al. Safety and antigenicity of non-adjuvanted and MF59-adjuvanted influenza A/Duck/Singapore/97 (H5N3) vaccine: a randomised trial of two potential vaccines against H5N1 influenza. Lancet 357 9272 (2001) 1937-1943
4. Treanor J.J., Campbell J.D., Zangwill K.M., Rowe T., and Wolff M. Safety and immunogenicity of an inactivated subvirion influenza A (H5N1) vaccine. N Engl J Med 354 13 (2006) 1343-1351
5. Bresson J.L., Perronne C., Launay O., Gerdil C., Saville M., Wood J., et al. Safety and immunogenicity of an inactivated split-virion influenza A/Vietnam/1194/2004 (H5N1) vaccine: phase I randomised trial. Lancet 367 9523 (2006) 1657-1664
6. Stephenson I., Nicholson K.G., Gluck R., Mischler R., Newman R.W., Palache A.M., et al. Safety and antigenicity of whole virus and subunit influenza A/Hong Kong/1073/99 (H9N2) vaccine in healthy adults: phase I randomised trial. Lancet 362 9400 (2003) 1959-1966
7. Moss P. Cellular immune responses to influenza. In: Brown F., Haaheim L.R., and Schild G.C. (Eds). Laboratory correlates of immunity to influenza-a reassessment. Vol. 115: Dev Biol (2003), Basel, Karger 31-37
8. Swain S.L., Agrewala J.N., Brown D.M., Jelley-Gibbs D.M., Golech S., Huston G., et al. CD4+ T-cell memory: generation and multi-faceted roles for CD4+ T cells in protective immunity to influenza. Immunol Rev 211 (2006) 8-22
9. Thomas P.G., Keating R., Hulse-Post D.J., and Doherty P.C. Cell-mediated protection in influenza infection. Emerg Infect Dis 12 1 (2006) 48-54
10. Gerhard W. The role of the antibody response in influenza virus infection. Curr Top Microbiol Immunol 260 (2001) 171-190
11. Subbarao K., and Joseph T. Scientific barriers to developing vaccines against avian influenza viruses. Nat Rev Immunol 7 4 (2007) 267-278
12. Gluck R., Mischler R., Finkel B., Que J.U., Scarpa B., and Cryz Jr. S.J. Immunogenicity of new virosome influenza vaccine in elderly people. Lancet 344 8916 (1994) 160-163
13. Almeida J.D., Edwards D.C., Brand C.M., and Heath T.D. Formation of virosomes from influenza subunits and liposomes. Lancet 2 7941 (1975) 899-901
14. Conne P., Gauthey L., Vernet P., Althaus B., Que J.U., Finkel B., et al. Immunogenicity of trivalent subunit versus virosome-formulated influenza vaccines in geriatric patients. Vaccine 15 15 (1997) 1675-1679
15. Mischler R., and Metcalfe I.C. Inflexal V a trivalent virosome subunit influenza vaccine: production. Vaccine 20 Suppl. 5 (2002) B17-B23
16. Stegmann T., Morselt H.W., Booy F.P., van Breemen J.F., Scherphof G., and Wilschut J. Functional reconstitution of influenza virus envelopes. EMBO J 6 9 (1987) 2651-2659
17. Gluck R., and Metcalfe I.C. New technology platforms in the development of vaccines for the future. Vaccine 20 Suppl. 5 (2002) B10-B16
18. Moser C., Metcalfe I.C., and Viret J.F. Virosomal adjuvanted antigen delivery systems. Expert Rev Vaccines 2 2 (2003) 189-196
19. Huckriede A., Bungener L., ter Veer W., Holtrop M., Daemen T., Palache A.M., et al. Influenza virosomes: combining optimal presentation of hemagglutinin with immunopotentiating activity. Vaccine 21 9-10 (2003) 925-931
20. Huckriede A., Bungener L., Stegmann T., Daemen T., Medema J., Palache A.M., et al. The virosome concept for influenza vaccines. Vaccine 23 Suppl. 1 (2005) S26-S38
21. Glenny A.T., Buttle G.A.H., and Stevens M.F. Rate of disappearance of diphteria toxoid injected into rabbits and guinea-pigs: toxoid precipitation with alum. J Pathol 34 (1931) 267-275
22. Glenny A.T., Pope C.G., Waddington H., and Wallace U. Immunological notes XVII to XXIV. J Pathol 29 (1926) 31-40
23. Gabutti G., Guido M., Durando P., De Donno A., Quattrocchi M., Bacilieri S., et al. Safety and immunogenicity of conventional subunit and MF59-adjuvanted influenza vaccines in human immunodeficiency virus-1-seropositive patients. J Int Med Res 33 4 (2005) 406-416
24. Baldo V., Baldovin T., Floreani A., Carraro A.M., and Trivello R. MF59-adjuvanted influenza vaccine confers superior immunogenicity in adult subjects (18-60 years of age) with chronic diseases who are at risk of post-influenza complications. Vaccine 25 20 (2007) 3955-3961
25. Ott G., Barchfeld G.L., Chernoff D., Radhakrishnan R., van Hoogevest P., and Van Nest G. MF59. Design and evaluation of a safe and potent adjuvant for human vaccines. Pharm Biotechnol 6 (1995) 277-296
26. Cataldo D.M., and Van Nest G. The adjuvant MF59 increases the immunogenicity and protective efficacy of subunit influenza vaccine in mice. Vaccine 15 16 (1997) 1710-1715
27. Morein B., Sundquist B., Hoglund S., Dalsgaard K., and Osterhaus A. Iscom, a novel structure for antigenic presentation of membrane proteins from enveloped viruses. Nature 308 5958 (1984) 457-460
28. Pearse M.J., and Drane D. ISCOMATRIX adjuvant: a potent inducer of humoral and cellular immune responses. Vaccine 22 19 (2004) 2391-2395
29. Sjolander A., Drane D., Maraskovsky E., Scheerlinck J.P., Suhrbier A., Tennent J., et al. Immune responses to ISCOM formulations in animal and primate models. Vaccine 19 17-19 (2001) 2661-2665
30. Rimmelzwaan G.F., Baars M., van Beek R., van Amerongen G., Lovgren-Bengtsson K., Claas E.C., et al. Induction of protective immunity against influenza virus in a macaque model: comparison of conventional and iscom vaccines. J Gen Virol 78 Pt 4 (1997) 757-765
31. Coulter A., Harris R., Davis R., Drane D., Cox J., Ryan D., et al. Intranasal vaccination with ISCOMATRIX adjuvanted influenza vaccine. Vaccine 21 9-10 (2003) 946-949
32. Rimmelzwaan G.F., Nieuwkoop N., Brandenburg A., Sutter G., Beyer W.E., Maher D., et al. A randomized, double blind study in young healthy adults comparing cell mediated and humoral immune responses induced by influenza ISCOM vaccines and conventional vaccines. Vaccine 19 9-10 (2000) 1180-1187
33. Davis I.D., Chen W., Jackson H., Parente P., Shackleton M., Hopkins W., et al. Recombinant NY-ESO-1 protein with ISCOMATRIX adjuvant induces broad integrated antibody and CD4(+) and CD8(+) T cell responses in humans. Proc Natl Acad Sci USA 101 29 (2004) 10697-10702
34. Ennis F.A., Cruz J., Jameson J., Klein M., Burt D., and Thipphawong J. Augmentation of human influenza A virus-specific cytotoxic T lymphocyte memory by influenza vaccine and adjuvanted carriers (ISCOMS). Virology 259 2 (1999) 256-261
35. Frazer I.H., Quinn M., Nicklin J.L., Tan J., Perrin L.C., Ng P., et al. Phase 1 study of HPV16-specific immunotherapy with E6E7 fusion protein and ISCOMATRIX adjuvant in women with cervical intraepithelial neoplasia. Vaccine 23 2 (2004) 172-181
36. Stewart T.J., Drane D., Malliaros J., Elmer H., Malcolm K.M., Cox J.C., et al. ISCOMATRIX adjuvant: an adjuvant suitable for use in anticancer vaccines. Vaccine 22 27-28 (2004) 3738-3743
37. Lindblad E.B. Mineral adjuvants (2006), Elsevier Academic Press p. 217-234
38. Stephenson I., Wood J.M., Nicholson K.G., Charlett A., and Zambon M.C. Detection of anti-H5 responses in human sera by HI using horse erythrocytes following MF59-adjuvanted influenza A/Duck/Singapore/97 vaccine. Virus Res 103 1-2 (2004) 91-95
39. Radosevic K., Wieland C.W., Rodriguez A., Weverling G.J., Mintardjo R., Gillissen G., et al. Protective immune responses to a recombinant adenovirus type 35 tuberculosis vaccine in two mouse strains: CD4 and CD8 T-cell epitope mapping and role of gamma interferon. Infect Immun 75 8 (2007) 4105-4115
40. Braciale T.J., Braciale V.L., Winkler M., Stroynowski I., Hood L., Sambrook J., et al. On the role of the transmembrane anchor sequence of influenza hemagglutinin in target cell recognition by class I MHC-restricted, hemagglutinin-specific cytolytic T lymphocytes. J Exp Med 166 3 (1987) 678-692
41. www.ifpma.org/. /Documents/NR5877/Table_Avian_Pandemic_Influenza_RnD_17Oct06.pdf; 2006.
42. www.who.int/vaccine_research/diseases/influenza/flu_trials_tables/en/print.html
43. Ninomiya A., Imai M., Tashiro M., and 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 25 18 (2007) 3554-3560
44. Lin J., Zhang J., Dong X., Fang H., Chen J., Su N., et al. Safety and immunogenicity of an inactivated adjuvanted whole-virion influenza A (H5N1) vaccine: a phase I randomised controlled trial. Lancet 368 9540 (2006) 991-997
45. Hehme N., Engelmann H., Kuenzel W., Neumeier E., and Saenger R. Immunogenicity of a monovalent, aluminum-adjuvanted influenza whole virus vaccine for pandemic use. Virus Res 103 1-2 (2004) 163-171
46. Ott G., Barchfeld G.L., and Van Nest G. Enhancement of humoral response against human influenza vaccine with the simple submicron oil/water emulsion adjuvant MF59. Vaccine 13 16 (1995) 1557-1562
47. Lindblad E.B., Elhay M.J., Silva R., Appelberg R., and Andersen P. Adjuvant modulation of immune responses to tuberculosis subunit vaccines. Infect Immun 65 2 (1997) 623-629
48. Sambhara S., Woods S., Arpino R., Kurichh A., Tamane A., Bengtsson K.L., et al. Influenza (H1N1)-ISCOMs enhance immune responses and protection in aged mice. Mech Ageing Dev 96 1-3 (1997) 157-169
49. Martin J.T. Development of an adjuvant to enhance the immune response to influenza vaccine in the elderly. Biologicals 25 2 (1997) 209-213
50. Podda A., Del Guidice G., and O'Hagan D. MF59: a safe and potent adjuvant for human use (2006), Elsevier Academic Press p. 149-160
51. Sjolander A., van't Land B., and Lovgren Bengtsson K. Iscoms containing purified Quillaja saponins upregulate both Th1-like and Th2-like immune responses. Cell Immunol 177 1 (1997) 69-76
52. Huber V.C., Lynch J.M., Bucher D.J., Le J., and Metzger D.W. Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J Immunol 166 12 (2001) 7381-7388
53. Fazekas G., Rosenwirth B., Dukor P., Gergely J., and Rajnavolgyi E. IgG isotype distribution of local and systemic immune responses induced by influenza virus infection. Eur J Immunol 24 12 (1994) 3063-3067
54. Stevens T.L., Bossie A., Sanders V.M., Fernandez-Botran R., Coffman R.L., Mosmann T.R., et al. Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature 334 6179 (1988) 255-258
55. Hovden A.O., Cox R.J., and Haaheim L.R. Whole influenza virus vaccine is more immunogenic than split influenza virus vaccine and induces primarily an IgG2a response in BALB/c mice. Scand J Immunol 62 1 (2005) 36-44
56. Moran T.M., Park H., Fernandez-Sesma A., and Schulman J.L. Th2 responses to inactivated influenza virus can Be converted to Th1 responses and facilitate recovery from heterosubtypic virus infection. J Infect Dis 180 3 (1999) 579-585
57. Liang S., Mozdzanowska K., Palladino G., and Gerhard W. Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J Immunol 152 4 (1994) 1653-1661
58. O'Neill E., Krauss S.L., Riberdy J.M., Webster R.G., and Woodland D.L. Heterologous protection against lethal A/HongKong/156/97 (H5N1) influenza virus infection in C57BL/6 mice. J Gen Virol 81 Pt 11 (2000) 2689-2696
59. Sambhara S., Kurichh A., Miranda R., Tumpey T., Rowe T., Renshaw M., et al. 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 2 (2001) 143-153
60. Christensen J.P., Doherty P.C., Branum K.C., and Riberdy J.M. Profound protection against respiratory challenge with a lethal H7N7 influenza A virus by increasing the magnitude of CD8(+) T-cell memory. J Virol 74 24 (2000) 11690-11696
61. Andrew M.E., and Coupar B.E. Efficacy of influenza haemagglutinin and nucleoprotein as protective antigens against influenza virus infection in mice. Scand J Immunol 28 1 (1988) 81-85
62. McElhaney J.E., Xie D., Hager W.D., Barry M.B., Wang Y., Kleppinger A., et al. T cell responses are better correlates of vaccine protection in the elderly. J Immunol 176 10 (2006) 6333-6339
63. Sambhara S., Woods S., Arpino R., Kurichh A., Tamane A., Underdown B., et al. Heterotypic protection against influenza by immunostimulating complexes is associated with the induction of cross-reactive cytotoxic T lymphocytes. J Infect Dis 177 5 (1998) 1266-1274