Incorporation of LpxL1, a detoxified lipopolysaccharide adjuvant, in influenza H5N1 virosomes increases vaccine immunogenicity

Vaccine

Volumn 27, Issue 6, 2009, Pages 947-955

  de Vries, J J C ^a   Bungener, L ^a   ter Veer, W ^a   van Alphen, L ^b   van der Ley, P ^b   Wilschut, J ^a   Huckriede, A ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b NETHERLANDS VACCINE INSTITUTE   (Netherlands)

Author keywords

Adjuvant; H5N1; Influenza; LPS; Vaccine; Virosomes

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; GAMMA INTERFERON; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; INFLUENZA VACCINE; INTERLEUKIN 4; NEISSERIA MENINGITIDIS LIPOPOLYSACCHARIDE DERIVATIVE LPXL1; UNCLASSIFIED DRUG; VIROSOME;

ADJUVANT THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; CONTROLLED STUDY; DRUG DISTRIBUTION; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; HEMAGGLUTINATION INHIBITION TEST; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; INFLUENZA; INFLUENZA VIRUS A H5N1; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TH1 CELL; VIRUS ENVELOPE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, VIRAL; FEMALE; HEMAGGLUTINATION INHIBITION TESTS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; IMMUNIZATION, SECONDARY; IMMUNOGLOBULIN G; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; INTERFERON-GAMMA; INTERLEUKIN-4; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED BALB C; NEISSERIA MENINGITIDIS; T-LYMPHOCYTES; VACCINES, VIROSOME;

EID: 58249120884     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2008.11.046     Document Type: Article

References (42)

1. Luke C.J., and Subbarao K. Vaccines for pandemic influenza. Emerg Infect Dis 12 1 (2006) 66-72
2. Subbarao K., and Joseph T. Scientific barriers to developing vaccines against avian influenza viruses. Nat Rev Immunol 7 4 (2007) 267-278
3. Leroux-Roels I., Borkowski A., Vanwolleghem T., Dramé M., Clement F., and Hons E. Antigen sparing and cross-reactive immunity with an adjuvanted rH5N1 prototype pandemic influenza vaccine: a randomised controlled trial. Lancet 370 9587 (2007) 580-589
4. Huckriede A., Bungener L., Stegmann T., Daemen T., Medema J., and Palache A.M. The virosome concept for influenza vaccines. Vaccine 23 Suppl. 1 (2005) S26-S38
5. Conne P., Gauthey L., Vernet P., Althaus B., Que J.U., and Finkel B. Immunogenicity of trivalent subunit versus virosome-formulated influenza vaccines in geriatric patients. Vaccine 15 15 (1997) 1675-1679
6. de Bruijn I.A., Nauta J., Cramer W.C., Gerez L., and Palache A.M. Clinical experience with inactivated, virosomal influenza vaccine. Vaccine 23 Suppl. 1 (2005) S39-S49
7. de B.I., Meyer I., Gerez L., Nauta J., Giezeman K., and Palache B. Antibody induction by virosomal, MF59-adjuvanted, or conventional influenza vaccines in the elderly. Vaccine 26 1 (2007) 119-127
8. 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
9. Guy B. The perfect mix: recent progress in adjuvant research. Nat Rev Microbiol 5 7 (2007) 505-517
10. Mata-Haro V., Cekic C., Martin M., Chilton P.M., Casella C.R., and Mitchell T.C. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 316 5831 (2007) 1628-1632
11. Mbawuike I.N., Acuna C., Caballero D., Pham-Nguyen K., Gilbert B., and Petribon P. Reversal of age-related deficient influenza virus-specific CTL responses and IFN-gamma production by monophosphoryl lipid A. Cell Immunol 173 1 (1996) 64-78
12. Przetak M., Chow J., Cheng H., Rose J., Hawkins L.D., and Ishizaka S.T. Novel synthetic LPS receptor agonists boost systemic and mucosal antibody responses in mice. Vaccine 21 9-10 (2003) 961-970
13. Thompson H.S., Davies M.L., Watts M.J., Mann A.E., Holding F.P., and O'Neill T. Enhanced immunogenicity of a recombinant genital warts vaccine adjuvanted with monophosphoryl lipid A. Vaccine 16 20 (1998) 1993-1999
14. Baldridge J.R., Yorgensen Y., Ward J.R., and Ulrich J.T. Monophosphoryl lipid A enhances mucosal and systemic immunity to vaccine antigens following intranasal administration. Vaccine 18 22 (2000) 2416-2425
15. Beutler B., and Rietschel E.T. Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol 3 2 (2003) 169-176
16. Geurtsen J., Steeghs L., Hamstra H.J., Ten Hove J., De Haan A., and Kuipers B. Expression of the lipopolysaccharide-modifying enzymes PagP and PagL modulates the endotoxic activity of Bordetella pertussis. Infect Immun 74 10 (2006) 5574-5585
17. van der Ley P., Steeghs L., Hamstra H.J., ten Hove J., Zomer B., and van Alphen L. Modification of lipid A biosynthesis in Neisseria meningitidis lpxL mutants: influence on lipopolysaccharide structure, toxicity, and adjuvant activity. Infect Immun 69 10 (2001) 5981-5990
18. Fransen F., Boog C.J., van Putten J.P., and van der L.P. Agonists of Toll-like receptors 3, 4, 7, and 9 are candidates for use as adjuvants in an outer membrane vaccine against Neisseria meningitidis serogroup B. Infect Immun 75 12 (2007) 5939-5946
19. Dijkstra J., Bron R., Wilschut J., de Haan A., and Ryan J.L. Activation of murine lymphocytes by lipopolysaccharide incorporated in fusogenic, reconstituted influenza virus envelopes (virosomes). J Immunol 157 3 (1996) 1028-1036
20. Karkhanis Y.D., Zeltner J.Y., Jackson J.J., and Carlo D.J. A new and improved microassay to determine 2-keto-3-deoxyoctonate in lipopolysaccharide of Gram-negative bacteria. Anal Biochem 85 2 (1978) 595-601
21. Subbarao K., Chen H., Swayne D., Mingay L., Fodor E., and Brownlee G. Evaluation of a genetically modified reassortant H5N1 influenza A virus vaccine candidate generated by plasmid-based reverse genetics. Virology 305 1 (2003) 192-200
22. de Jonge J., Schoen P., ter Veer W., Stegmann T., Wilschut J., and Huckriede A. Use of a dialyzable short-chain phospholipid for efficient solubilization and reconstitution of influenza virus envelopes. Biochim Biophys Acta 1758 4 (2006) 527-536
23. Peterson G.L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83 2 (1977) 346-356
24. Böttcher C.J., Van Gent C.M., and Fries C. A rapid and sensitive submicro phosphorous determination. Anal Chim Acta 24 (1961) 203-204
25. Blum H., Beier H., and Gross H.J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 9 (1987) 93-99
26. Lesse A.J., Campagnari A.A., Bittner W.E., and Apicella M.A. Increased resolution of lipopolysaccharides and lipooligosaccharides utilizing tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis. J Immunol Methods 126 1 (1990) 109-117
27. Stegmann T., Schoen P., Bron R., Wey J., Bartoldus I., and Ortiz A. Evaluation of viral membrane fusion assays. Comparison of the octadecylrhodamine dequenching assay with the pyrene excimer assay. Biochemistry 32 42 (1993) 11330-11337
28. Bungener L., Serre K., Bijl L., Leserman L., Wilschut J., and Daemen T. Virosome-mediated delivery of protein antigens to dendritic cells. Vaccine 20 17-18 (2002) 2287-2295
29. http://www.who.int/csr/resources/publications/influenza/en/whocdscsrncs20025rev.pdf
30. European Medicines Agency (EMEA). Note for guidance on harmonisation of requirements for influenza vaccines CPMP/BWP/214/97.
31. Miyahira Y., Murata K., Rodriguez D., Rodriguez J.R., Esteban M., and Rodrigues M.M. Quantification of antigen specific CD8+ T cells using an ELISPOT assay. J Immunol Methods 181 1 (1995) 45-54
32. http://www.who.int/vaccine_research/diseases/influenza/flu_trials_tables/en/print.html
33. Huber V.C., McKeon R.M., Brackin M.N., Miller L.A., Keating R., and Brown S.A. Distinct contribution of vaccine-induced immunoglobulin G1 (IgG1) and IgG2a antibodies to protective immunity against influenza. Clin Vaccine Immunol 13 (2006) 981-990
34. Bungener L., Geeraedts F., ter Veer W., Medema J., Wilschut J., and Huckriede A. Alum boosts TH2-type antibody responses to whole-inactivated virus influenza vaccine in mice but does not confer superior protection. Vaccine 26 (2008) 2350-2359
35. Moran T.M., Isobe H., Fernandez-Sesma A., and Schulman J.L. Interleukin-4 causes delayed virus clearance in influenza virus-infected mice. J Virol 70 (1996) 5230-5235
36. Thoelen S., Van Damme P., Mathei C., Leroux-Roels G., Desombere I., and Safary A. Safety and immunogenicity of a hepatitis B vaccine formulated with a novel adjuvant system. Vaccine 16 7 (1998) 708-LA
37. McCormack S., Tilzey A., Carmichael A., Gotch F., Kepple J., Newberry A., et al. A phase I trial in HIV negative healthy volunteers evaluating the effect of potent adjuvants on immunogenicity of a recombinant gp120W61D derived from dual tropic R5X4 HIV-1ACH320. Vaccine 18 13 (2000) 1166-1177
38. De Becker G., Moulin V., Pajak B., Bruck C., Francotte M., and Thiriart C. The adjuvant monophosphoryl lipid A increases the function of antigen-presenting cells. Int Immunol 12 6 (2000) 807-815
39. Husebye H., Halaas O., Stenmark H., Tunheim G., Sandanger O., and Bogen B. Endocytic pathways regulate Toll-like receptor 4 signaling and link innate and adaptive immunity. EMBO J 25 4 (2006) 683-692
40. Blander J.M., and Medzithov R. Toll-dependent selection of microbial antigens for presentation by dendritic cells. Nature 440 (2006) 808-812
41. van Berkel M.E., Schrijver E.H., van Mourik A., Tesselaar K., van der Ley P., and Steeghs L. A critical contribution of both CD28 and ICOS in the adjuvant activity of Neisseria meningitidis H44/76 LPS and lpxL1 LPS. Vaccine 25 24 (2007) 4681-4688
42. Guo J., Stolina M., Bready J.V., Yin S., Horan T., and Yoshinaga S.K. Stimulatory effects of B7-related protein-1 on cellular and humoral immune responses in mice. J Immunol 166 9 (2001) 5578-5584