MF59 and Pam3CSK4 boost adaptive responses to influenza subunit vaccine through an IFN type I-independent mechanism of action

Journal of Immunology

Volumn 188, Issue 7, 2012, Pages 3088-3098

  Caproni, Elena ^a   Tritto, Elaine ^b   Cortese, Mario ^a   Muzzi, Alessandro ^a   Mosca, Flaviana ^a   Monaci, Elisabetta ^a   Baudner, Barbara ^a   Seubert, Anja ^a   De Gregorio, Ennio ^a  

^a NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^b NOVARTIS PHARMA AG   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; HEMAGGLUTININ ANTIBODY; IMMUNOLOGICAL ADJUVANT; INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; INTERFERON; INTERFERON 1 RECEPTOR; INTERFERON RECEPTOR; MIFAMURTIDE; MONOCLONAL ANTIBODY; PAM3CSK4; PROTEIN ANTIBODY; RESIQUIMOD; TETANUS TOXOID; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BLOOD CELL; CONTROLLED STUDY; DNA MICROARRAY; FEMALE; GENE CONTROL; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LEUKOCYTE MIGRATION; LYMPH NODE; MOUSE; MUSCLE; NONHUMAN; PRIORITY JOURNAL; SEASONAL INFLUENZA; SPLEEN CELL; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; UPREGULATION;

ADAPTIVE IMMUNITY; ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, MONOCLONAL; CHEMOTAXIS; FEMALE; GENE EXPRESSION REGULATION; IMMUNITY, INNATE; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; INFLUENZA B VIRUS; INFLUENZA VACCINES; INTERFERON-ALPHA; LIPOPEPTIDES; LYMPH NODES; LYMPHOCYTE SUBSETS; MICE; MICE, INBRED BALB C; MUSCLES; POLYSORBATES; SPECIFIC PATHOGEN-FREE ORGANISMS; SPLEEN; SQUALENE; TETANUS TOXOID; VACCINES, SUBUNIT;

EID: 84859412452     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101764     Document Type: Article

References (33)

1. Fiore, A. E., D. K. Shay, K. Broder, J. K. Iskander, T. M. Uyeki, G. Mootrey, J. S. Bresee, and N. S. Cox; Centers for Disease Control and Prevention (CDC); Advisory Committee on Immunization Practices (ACIP). 2008. Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP), 2008. MMWR Recomm. Rep. 57(RR-7): 1-60.
2. Gross, P. A., F. A. Ennis, P. F. Gaerlan, L. J. Denson, C. R. Denning, and D. Schiffman. 1977. A controlled double-blind comparison of reactogenicity, immunogenicity, and protective efficacy of whole-virus and split-product influenza vaccines in children. J. Infect. Dis. 136: 623-632. (Pubitemid 8223673)
3. Gross, P. A., and F. A. Ennis. 1977. Influenza vaccine: split-product versus whole-virus types: how do they differ. N. Engl. J. Med. 296: 567-568. (Pubitemid 8071482)
4. Rhorer, J., C. S. Ambrose, S. Dickinson, H. Hamilton, N. A. Oleka, F. J. Malinoski, and J. Wittes. 2009. Efficacy of live attenuated influenza vaccine in children: a meta-analysis of nine randomized clinical trials. Vaccine 27: 1101-1110.
5. Koyama, S., T. Aoshi, T. Tanimoto, Y. Kumagai, K. Kobiyama, T. Tougan, K. Sakurai, C. Coban, T. Horii, S. Akira, and K. J. Ishii. 2010. Plasmacytoid dendritic cells delineate immunogenicity of influenza vaccine subtypes. Sci. Transl. Med. 2: 25ra24.
6. Co, M. D., L. Orphin, J. Cruz, P. Pazoles, K. M. Green, J. Potts, A. M. Leporati, J. A. Babon, J. E. Evans, F. A. Ennis, and M. Terajima. 2009. In vitro evidence that commercial influenza vaccines are not similar in their ability to activate human T cell responses. Vaccine 27: 319-327.
7. Proietti, E., L. Bracci, S. Puzelli, T. Di Pucchio, P. Sestili, E. De Vincenzi, M. Venditti, I. Capone, I. Seif, E. De Maeyer, et al. 2002. Type I IFN as a natural adjuvant for a protective immune response: lessons from the influenza vaccine model. J. Immunol. 169: 375-383. (Pubitemid 34686158)
8. O'Hagan, D. T., A. Wack, and A. Podda. 2007. MF59 is a safe and potent vaccine adjuvant for flu vaccines in humans: what did we learn during its development? Clin. Pharmacol. Ther. 82: 740-744. (Pubitemid 350114825)
9. Podda, A. 2001. The adjuvanted influenza vaccines with novel adjuvants: experience with the MF59-adjuvanted vaccine. Vaccine 19: 2673-2680. (Pubitemid 32234288)
10. Dupuis, M., T. J. Murphy, D. Higgins, M. Ugozzoli, G. van Nest, G. Ott, and D. M. McDonald. 1998. Dendritic cells internalize vaccine adjuvant after intramuscular injection. Cell. Immunol. 186: 18-27. (Pubitemid 28285344)
11. Dupuis, M., D. M. McDonald, and G. Ott. 1999. Distribution of adjuvant MF59 and antigen gD2 after intramuscular injection in mice. Vaccine 18: 434-439. (Pubitemid 29462599)
12. Dupuis, M., K. Denis-Mize, A. LaBarbara, W. Peters, I. F. Charo, D. M. McDonald, and G. Ott. 2001. Immunization with the adjuvant MF59 induces macrophage trafficking and apoptosis. Eur. J. Immunol. 31: 2910-2918. (Pubitemid 32994542)
13. Mosca, F., E. Tritto, A. Muzzi, E. Monaci, F. Bagnoli, C. Iavarone, D. O'Hagan, R. Rappuoli, and E. De Gregorio. 2008. Molecular and cellular signatures of human vaccine adjuvants. Proc. Natl. Acad. Sci. USA 105: 10501-10506.
14. Seubert, A., E. Monaci, M. Pizza, D. T. O'Hagan, and A. Wack. 2008. The adjuvants aluminum hydroxide and MF59 induce monocyte and granulocyte chemoattractants and enhance monocyte differentiation toward dendritic cells. J. Immunol. 180: 5402-5412.
15. Calabro, S., M. Tortoli, B. C. Baudner, A. Pacitto, M. Cortese, D. T. O'Hagan, E. De Gregorio, A. Seubert, and A. Wack. 2011. Vaccine adjuvants alum and MF59 induce rapid recruitment of neutrophils and monocytes that participate in antigen transport to draining lymph nodes. Vaccine 29: 1812-1823.
16. Vesikari, T., M. Pellegrini, A. Karvonen, N. Groth, A. Borkowski, D. T. O'Hagan, and A. Podda. 2009. Enhanced immunogenicity of seasonal influenza vaccines in young children using MF59 adjuvant. Pediatr. Infect. Dis. J. 28: 563-571.
17. Galli, G., D. Medini, E. Borgogni, L. Zedda, M. Bardelli, C. Malzone, S. Nuti, S. Tavarini, C. Sammicheli, A. K. Hilbert, et al. 2009. Adjuvanted H5N1 vaccine induces early CD4+ T cell response that predicts long-term persistence of protective antibody levels. Proc. Natl. Acad. Sci. USA 106: 3877-3882.
18. Leroux-Roels, I., F. Roman, S. Forgus, C. Maes, F. De Boever, M. Dramé, P. Gillard, R. van der Most, M. Van Mechelen, E. Hanon, and G. Leroux-Roels. 2010. Priming with AS03 A-adjuvanted H5N1 influenza vaccine improves the kinetics, magnitude and durability of the immune response after a heterologous booster vaccination: an open non-randomised extension of a double-blind randomised primary study. Vaccine 28: 849-857.
19. Galli, G., K. Hancock, K. Hoschler, J. DeVos, M. Praus, M. Bardelli, C. Malzone, F. Castellino, C. Gentile, T. McNally, et al. 2009. Fast rise of broadly cross-reactive antibodies after boosting long-lived human memory B cells primed by an MF59 adjuvanted prepandemic vaccine. Proc. Natl. Acad. Sci. USA 106: 7962-7967.
20. Clark, T. W., M. Pareek, K. Hoschler, H. Dillon, K. G. Nicholson, N. Groth, and I. Stephenson. 2009. Trial of 2009 influenza A (H1N1) monovalent MF59-adjuvanted vaccine. N. Engl. J. Med. 361: 2424-2435.
21. Bernstein, D. I., K. M. Edwards, C. L. Dekker, R. Belshe, H. K. Talbot, I. L. Graham, D. L. Noah, F. He, and H. Hill. 2008. Effects of adjuvants on the safety and immunogenicity of an avian influenza H5N1 vaccine in adults. J. Infect. Dis. 197: 667-675. (Pubitemid 351364465)
22. Wack, A., B. C. Baudner, A. K. Hilbert, I. Manini, S. Nuti, S. Tavarini, H. Scheffczik, M. Ugozzoli, M. Singh, J. Kazzaz, et al. 2008. Combination adjuvants for the induction of potent, long-lasting antibody and T-cell responses to influenza vaccine in mice. Vaccine 26: 552-561.
23. Storey, J. D., and R. Tibshirani. 2003. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 100: 9440-9445. (Pubitemid 37033947)
24. Guiducci, C., R. L. Coffman, and F. J. Barrat. 2009. Signalling pathways leading to IFN-alpha production in human plasmacytoid dendritic cell and the possible use of agonists or antagonists of TLR7 and TLR9 in clinical indications. J. Intern. Med. 265: 43-57.
25. Kadowaki, N., and Y. J. Liu. 2002. Natural type I interferon-producing cells as a link between innate and adaptive immunity. Hum. Immunol. 63: 1126-1132. (Pubitemid 36025987)
26. Wille-Reece, U., B. J. Flynn, K. Loré, R. A. Koup, R. M. Kedl, J. J. Mattapallil, W. R. Weiss, M. Roederer, and R. A. Seder. 2005. HIV Gag protein conjugated to a Toll-like receptor 7/8 agonist improves the magnitude and quality of Th1 and CD8+ T cell responses in nonhuman primates. Proc. Natl. Acad. Sci. USA 102: 15190-15194. (Pubitemid 41513357)
27. Valensi, J. P., J. R. Carlson, and G. A. Van Nest. 1994. Systemic cytokine profiles in BALB/c mice immunized with trivalent influenza vaccine containing MF59 oil emulsion and other advanced adjuvants. J. Immunol. 153: 4029-4039.
28. Adkins, B., and R. Q. Du. 1998. Newborn mice develop balanced Th1/Th2 primary effector responses in vivo but are biased to Th2 secondary responses. J. Immunol. 160: 4217-4224. (Pubitemid 28217275)
29. Khan, S., M. S. Bijker, J. J. Weterings, H. J. Tanke, G. J. Adema, T. van Hall, J. W. Drijfhout, C. J. Melief, H. S. Overkleeft, G. A. van der Marel, et al. 2007. Distinct uptake mechanisms but similar intracellular processing of two different Toll-like receptor ligand-peptide conjugates in dendritic cells. J. Biol. Chem. 282: 21145-21159. (Pubitemid 47099911)
30. Tighe, H., K. Takabayashi, D. Schwartz, R. Marsden, L. Beck, J. Corbeil, D. D. Richman, J. J. Eiden, Jr., H. L. Spiegelberg, and E. Raz. 2000. Conjugation of protein to immunostimulatory DNA results in a rapid, long-lasting and potent induction of cell-mediated and humoral immunity. Eur. J. Immunol. 30: 1939-1947. (Pubitemid 30456190)
31. Hood, J. D., H. J. Warshakoon, M. R. Kimbrell, N. M. Shukla, S. S. Malladi, X. Wang, and S. A. David. 2010. Immunoprofiling Toll-like receptor ligands: comparison of immunostimulatory and proinflammatory profiles in ex vivo human blood models. Hum. Vaccin. 6: 322-335.
32. Kool, M., V. Pétrilli, T. De Smedt, A. Rolaz, H. Hammad, M. van Nimwegen, I. M. Bergen, R. Castillo, B. N. Lambrecht, and J. Tschopp. 2008. Cutting edge: alum adjuvant stimulates inflammatory dendritic cells through activation of the NALP3 inflammasome. J. Immunol. 181: 3755-3759.
33. Kastenmüller, K., U. Wille-Reece, R. W. Lindsay, L. R. Trager, P. A. Darrah, B. J. Flynn, M. R. Becker, M. C. Udey, B. E. Clausen, B. Z. Igyarto, et al. 2011. Protective T cell immunity in mice following protein-TLR7/8 agonist-conjugate immunization requires aggregation, type I IFN, and multiple DC subsets. J. Clin. Invest. 121: 1782-1796.