Effect of viral membrane fusion activity on antibody induction by influenza H5N1 whole inactivated virus vaccine

Vaccine

Volumn 30, Issue 45, 2012, Pages 6501-6507

  Geeraedts, Felix ^a   ter Veer, Wouter ^a   Wilschut, Jan ^a   Huckriede, Anke ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Fusion; IFNalpha; Influenza; Th1; Whole inactivated virus vaccine

Indexed keywords

ALPHA INTERFERON; HEMAGGLUTINATION INHIBITING ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; INACTIVATED VIRUS VACCINE; INFLUENZA VACCINE; TOLL LIKE RECEPTOR 7;

ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG RESPONSE; FEMALE; IMMUNOGENICITY; MEMBRANE FUSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; VIRUS CELL INTERACTION; VIRUS ENVELOPE;

ANIMALS; ANTIBODIES, VIRAL; DENDRITIC CELLS; FEMALE; FORMALDEHYDE; HEMAGGLUTINATION INHIBITION TESTS; IMMUNOGLOBULIN G; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; INTERFERON-ALPHA; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE INFECTIONS; TOLL-LIKE RECEPTOR 7; VACCINES, INACTIVATED; VIRUS INTERNALIZATION;

EID: 84866510206     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2012.07.036     Document Type: Article

References (53)

1. Taubenberger J.K., Reid A.H., Lourens R.M., Wang R., Jin G., Fanning T.G. Characterization of the 1918 influenza virus polymerase genes. Nature 2005, 437(7060):889-893.
2. Kawaoka Y., Krauss S., Webster R.G. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol 1989, 63(11):4603-4608.
3. Webster R.G., Laver W.G. The origin of pandemic influenza. Bull World Health Organ 1972, 47(4):449-452.
4. Garten R.J., Davis C.T., Russell C.A., Shu B., Lindstrom S., Balish A., et al. Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 2009, 325(5937):197-201.
5. Guan Y., Vijaykrishna D., Bahl J., Zhu H., Wang J., Smith G.J. The emergence of pandemic influenza viruses. Protein Cell 2010, 1(1):9-13.
6. http://www.who.int/csr/disease/avian_influenza/country/cases_table_2011_01_20/en/index.html.
7. De Wit E., Fouchier R.A. Emerging influenza. J Clin Virol 2008, 41(1):1-6.
8. Peiris M., Yuen K.Y., Leung C.W., Chan K.H., Ip P.L., Lai R.W., et al. Human infection with influenza H9N2. Lancet 1999, 354(9182):916-917.
9. Fedson D.S. Vaccine development for an imminent pandemic: why we should worry, what we must do. Hum Vaccine 2006, 2(1):38-42.
10. Wright P.F. Vaccine preparedness-are we ready for the next influenza pandemic?. N Engl J Med 2008, 358(24):2540-2543.
11. Nicholson K.G., Tyrrell D.A., Harrison P., Potter C.W., Jennings R., Clark A., et al. Clinical studies of monovalent inactivated whole virus and subunit A/USSR/77 (H1N1) vaccine: serological responses and clinical reactions. J Biol Stand 1979, 7(2):123-136.
12. Beyer W.E., Palache A.M., Osterhaus A.D. Comparison of serology and reactogenicity between influenza subunit vaccines and whole virus or split vaccines: a review and meta-analysis of the literature. Clin Drug Investig 1998, 15:1-12.
13. Stephenson I., Nicholson K.G., Glück 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 2003, 362(9400):1959-1966.
14. Ehrlich H.J., Müller M., Oh H.M., Tambyah P.A., Joukhadar C., Montomoli E., et al. A clinical trial of a whole-virus H5N1 vaccine derived from cell culture. N Engl J Med 2008, 358(24):2573-2584.
15. 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 2006, 368:991-997.
16. Bungener L., Geeraedts F., Ter Veer W., 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(19):2350-2359.
17. Huber V.C., McKeon R.M., Brackin M.N., Miller L.A., Keating R., Brown S.A., et al. Distinct contributions of vaccine-induced immunoglobulin G1 (IgG1) and IgG2a antibodies to protective immunity against influenza. Clin Vaccine Immunol 2006, 13(9):981-990.
18. Hovden A.O., Cox R.J., 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 2005, 62:36-44.
19. Geeraedts F., Bungener L., Pool J., Ter Veer W., Wilschut J., Huckriede A. Whole inactivated virus influenza vaccine is superior to subunit vaccine in inducing immune responses and secretion of proinflammatory cytokines by DCs. Influenza Other Respir Viruses 2008, 2:41-51.
20. http://www.emea.europa.eu/docs/enGB/document_library/EPAR-Public_assessment%20report/human/000982/WC500022673.pdf.
21. http://www.baxter.com/press_room/press_releases/2009/10_07_09-celvapan.html.
22. Koyama S., Ishii K.J., Kumar H., Tanimoto T., Coban C., Uematsu S., et al. Differential role of TLR- and RLR-signaling in the immune responses to influenza A virus infection and vaccination. J Immunol 2007, 179:4711-4720.
23. Geeraedts F., Goutagny N., Hornung V., Severa M., de Haan A., Pool J., et al. Superior immunogenicity of inactivated whole virus H5N1 influenza vaccine is primarily controlled by toll-like receptor signalling. PLoS Pathog 2008, 4(8):e1000138.
24. Kasturi S.P., Skountzou I., Albrecht R.A., Koutsonanos D., Hua T., Nakaya H.I., et al. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 2011, 470(7335):543-547.
25. Heer A.K., Shamshiev A., Donda A., Uematsu S., Akira S., Kopf M., et al. TLR signaling fine-tunes anti-influenza B cell responses without regulating effector T cell responses. J Immunol 2007, 178(4):2182-2191.
26. Koyama S., Aoshi T., Tanimoto T., Kumagai Y., Kobiyama K., Tougan T., et al. Plasmacytoid dendritic cells delineate immunogenicity of influenza vaccine subtypes. Sci Transl Med 2010, 2(25):25ra24.
27. Lund J.M., Alexopoulou L., Sato A., Karow M., Adams N.C., Gale N.W., et al. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci U S A 2004, 101(15):5598-5603.
28. Diebold S.S., Kaisho T., Hemmi H., Akira S., Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 2004, 303:1529-1531.
29. Mitchison N.A. T-cell-B-cell cooperation. Nat Rev Immunol 2004, 4(April (4)):308-312.
30. Wang J.P., Liu P., Latz E., Golenbock D.T., Finberg R.W., Libraty D.H. Flavivirus activation of plasmacytoid dendritic cells delineates key elements of TLR7 signaling beyond endosomal recognition. J Immunol 2006, 177(10):7114-7121.
31. Bridges C.B., Katz J., Levandowski R., Cox N.J. Inactivated influenza vaccines. Vaccines 2008, 259-290. Saunders Elsevier. 5th ed. S.A. Plotkin, W.A. Orenstein, P.A. Offit (Eds.).
32. Peterson G.L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 1977 Dec, 83(2):346-356.
33. Hemmi H., Kaisho T., Takeuchi O., Sato S., Sanjo H., Hoshino K., et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002, 3(2):196-200.
34. Gilliet M., Boonstra A., Paturel C., Antonenko S., Xu X.L., Trinchieri G., et al. The development of murine plasmacytoid dendritic cell precursors is differentially regulated by FLT3-ligand and granulocyte/macrophage colony-stimulating factor. J Exp Med 2002, 195(7):953-958.
35. Böttcher C.S.F., van Gent C.M., Fries C. A rapid and sensitive sub-micro phosphorus determination. Anal Chim Acta 1961, 24:203-204.
36. Stegmann T., Schoen P., Bron R., Wey J., Bartoldus I., Ortiz A., et al. Evaluation of viral membrane fusion assays. Comparison of the octadecylrhodamine dequenching assay with the pyrene excimer assay. Biochemistry 1993, 32(42):11330-11337.
37. Stegmann T., Morselt H.W., Booy F.P., van Breemen J.F., Scherphof G., Wilschut J. Functional reconstitution of influenza virus envelopes. EMBO J 1987, 6:2651-2659.
38. Yoshimura A., Ohnishi S. Uncoating of influenza virus in endosomes. J Virol 1984, 51(2):497-504.
39. Macdonald R.A., Hosking C.S., Jones C.L. The measurement of relative antibody affinity by ELISA using thiocyanate elution. J Immunol Methods 1988, 106(2):191-194.
40. Wuorimaa T., Dagan R., Merja Väkeväinen M., Bailleux F., Haikala R., Yaich M., et al. Avidity and subclasses of IgG after immunization of infants with an 11-valent pneumococcal conjugate vaccine with or without aluminum adjuvant. J Infect Dis 2001, 184(9):1211-1215.
41. Wang J.P., Asher D.R., Chan M., Kurt-Jones E.A., Finberg R.W. Cutting edge: antibody-mediated TLR7-dependent recognition of viral RNA. J Immunol 2007, 178(6):3363-3367.
42. Lee H.K., Lund J.M., Ramanathan B., Mizushima N., Iwasaki A. Autophagy-dependent viral recognition by plasmacytoid dendritic cells. Science 2007, 315(5817):1398-1401.
43. Reis e Sousa C. Eating in to avoid infection. Science 2007, 315(5817):1376-1377.
44. di Tommaso A., de Magistris M.T., Bugnoli M., Marsili I., Rappuoli R., Abrignani S. Formaldehyde treatment of proteins can constrain presentation to T cells by limiting antigen processing. Infect Immun 1994, 62(5):1830-1834.
45. Gilbert C., Svejstrup J.Q. RNA immunoprecipitation for determining RNA-protein associations in vivo. Curr Protoc Mol Biol 2006, 75. 27.4.1-27.4.11.
46. Nishiya T., Kajita E., Miwa S., Defranco A.L. TLR3 and TLR7 are targeted to the same intracellular compartments by distinct regulatory elements. J Biol Chem 2005, 280(44):37107-37117.
47. Heil F., Ahmad-Nejad P., Hemmi H., Hochrein H., Ampenberger F., Gellert T., et al. The Toll-like receptor 7 (TLR7)-specific stimulus loxoribine uncovers a strong relationship within the TLR7, 8 and 9 subfamily. Eur J Immunol 2003, 33(11):2987-2997.
48. Delgado M.F., Coviello S., Monsalvo A.C., Melendi G.A., Hernandez J.Z., Batalle J.P., et al. Lack of antibody affinity maturation due to poor Toll-like receptor stimulation leads to enhanced respiratory syncytial virus disease. Nat Med 2009, 15(1):34-41.
49. Murphy B.R., Prince G.A., Walsh E.E., Kim H.W., Parrott R.H., Hemming V.G., et al. Dissociation between serum neutralizing and glycoprotein antibody responses of infants and children who received inactivated respiratory syncytial virus vaccine. J Clin Microbiol 1986, 24:197-202.
50. Goldstein M.A., Tauraso N.M. Effect of formalin, beta-propiolactone, merthiolate, and ultraviolet light upon influenza virus infectivity chicken cell agglutination, hemagglutination, and antigenicity. Appl Microbiol 1970, 19(2):290-294.
51. Budimir N., Meijerhof T., Wilschut J., Huckriede A., De Haan A. The role of membrane fusion activity of a whole inactivated influenza virus vaccine in (re)activation of influenza-specific cytotoxic T lymphocytes. Vaccine 2010, 28(52):8280-8287.
52. Budimir N., Huckriede A., Meijerhof T., Boon L., Gostick E., Price D.A., et al. Induction of heterosubtypic cross-protection against influenza by a whole inactivated virus vaccine: the role of viral membrane fusion activity. PLoS One 2012, 7(1):e30898.
53. Rimmelzwaan G.F., Fouchier R.A., Osterhaus A.D. Influenza virus-specific cytotoxic T lymphocytes: a correlate of protection and a basis for vaccine development. Curr Opin Biotechnol 2007, 18(6):529-536.