Heterologous prime-boost vaccination with MF59-adjuvanted H5 vaccines promotes antibody affinity maturation towards the hemagglutinin HA1 domain and broad H5N1 cross-clade neutralization

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Khurana, Surender ^a   Coyle, Elizabeth M ^a   Dimitrova, Milena ^a   Castellino, Flora ^b   Nicholson, Karl ^c   Del Giudice, Giuseppe ^b   Golding, Hana ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; INFLUENZA VIRUS HEMAGGLUTININ; MIFAMURTIDE; NEUTRALIZING ANTIBODY; POLYCLONAL ANTIBODY; VIRUS ANTIBODY; HEMAGGLUTININ; IMMUNOLOGICAL ADJUVANT; MF59 OIL EMULSION; POLYSORBATE; SQUALENE; SUBUNIT VACCINE;

ANTIBODY AFFINITY; ANTIBODY TITER; ANTIGEN ANTIBODY COMPLEX; ANTIGEN BINDING; ARTICLE; CLADISTICS; CONTROLLED STUDY; HUMAN; HUMORAL IMMUNITY; IN VITRO STUDY; INFLUENZA A (H5N1); INFLUENZA VACCINATION; INFLUENZA VIRUS A; INFLUENZA VIRUS A H5N3; MAJOR CLINICAL STUDY; NONHUMAN; PROTEIN DOMAIN; VIRUS NEUTRALIZATION; BLOOD; CHEMISTRY; CLINICAL TRIAL; CROSS PRESENTATION; CROSS REACTION; IMMUNIZATION; IMMUNOLOGY; INFLUENZA; INFLUENZA VIRUS A H5N1; PROTEIN TERTIARY STRUCTURE; SERODIAGNOSIS; VACCINATION; VIROLOGY;

ADJUVANTS, IMMUNOLOGIC; ANTIBODIES, VIRAL; ANTIBODY AFFINITY; CROSS REACTIONS; CROSS-PRIMING; HEMAGGLUTININS; HUMANS; IMMUNIZATION, SECONDARY; INFLUENZA A VIRUS, H5N1 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; NEUTRALIZATION TESTS; POLYSORBATES; PROTEIN STRUCTURE, TERTIARY; SQUALENE; VACCINATION; VACCINES, SUBUNIT;

EID: 84899698087     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095496     Document Type: Article

References (25)

1. Galli G, Hancock K, Hoschler K, DeVos J, Praus M, 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 U S A 106: 7962-7967.
2. Stephenson I, Nicholson KG, Hoschler K, Zambon MC, Hancock K, et al. (2008) Antigenically distinct MF59-adjuvanted vaccine to boost immunity to H5N1. N Engl J Med 359: 1631-1633.
3. Khurana S, Chearwae W, Castellino F, Manischewitz J, King LR, et al. (2010) Vaccines with MF59 Adjuvant Expand the Antibody Repertoire to Target Protective Sites of Pandemic Avian H5N1 Influenza Virus. Science Translational Medicine 2: 15ra15-15ra15.
4. Dormitzer PR, Galli G, Castellino F, Golding H, Khurana S, et al. (2011) Influenza vaccine immunology. Immunol Rev 239: 167-177.
5. Nicholson KG, Colegate AE, Podda A, Stephenson I, Wood J, et al. (2001) 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: 1937-1943. (Pubitemid 32568336)
6. Stephenson I, Nicholson KG, Colegate A, Podda A, Wood J, et al. (2003) Boosting immunity to influenza H5N1 with MF59-adjuvanted H5N3 A/Duck/ Singapore/97 vaccine in a primed human population. Vaccine 21: 1687-1693. (Pubitemid 36287599)
7. Khurana S, Verma N, Yewdell JW, Hilbert AK, Castellino F, et al. (2011) MF59 adjuvant enhances diversity and affinity of antibody-mediated immune response to pandemic influenza vaccines. Sci Transl Med 3: 85ra48.
8. Verma S, Dimitrova M, Munjal A, Fontana J, Crevar CJ, et al. (2012) Oligomeric recombinant H5 HA1 vaccine produced in bacteria protects ferrets from homologous and heterologous wild-type H5N1 influenza challenge and controls viral loads better than subunit H5N1 vaccine by eliciting high-affinity antibodies. J Virol 86: 12283-12293.
9. Khurana S, Suguitan AL Jr, Rivera Y, Simmons CP, Lanzavecchia A, et al. (2009) Antigenic fingerprinting of H5N1 avian influenza using convalescent sera and monoclonal antibodies reveals potential vaccine and diagnostic targets. PLoS Med 6: e1000049.
10. Khurana S, Verma N, Talaat KR, Karron RA, Golding H (2011) Immune response following H1N1pdm09 vaccination: differences in antibody repertoire and avidity in young adults and elderly populations stratified by age and gender. J Infect Dis 205: 610-620.
11. Khurana S, Frasca D, Blomberg B, Golding H (2012) AID activity in B cells strongly correlates with polyclonal antibody affinity maturation in-vivo following pandemic 2009-H1N1 vaccination in humans. PLoS Pathog 8: e1002920.
12. Khurana S, Wu J, Dimitrova M, King LR, Manischewitz J, et al. (2013) DNA priming prior to inactivated influenza A(H5N1) vaccination expands the antibody epitope repertoire and increases affinity maturation in a boost-interval- dependent manner in adults. J Infect Dis 208: 413-417.
13. Jones PD, Ada GL (1987) Persistence of influenza virus-specific antibody-secreting cells and B-cell memory after primary murine influenza virus infection. Cell Immunol 109: 53-64. (Pubitemid 17155708)
14. Jones PD, Ada GL (1987) Influenza-specific antibody-secreting cells and B cell memory in the murine lung after immunization with wild-type, cold-adapted variant and inactivated influenza viruses. Vaccine 5: 244-248. (Pubitemid 17134676)
15. Hyland L, Sangster M, Sealy R, Coleclough C (1994) Respiratory virus infection of mice provokes a permanent humoral immune response. J Virol 68: 6083-6086. (Pubitemid 24258630)
16. Tarlinton D, Good-Jacobson K (2013) Diversity among memory B cells: origin, consequences, and utility. Science 341: 1205-1211.
17. Purtha WE, Tedder TF, Johnson S, Bhattacharya D, Diamond MS (2011) Memory B cells, but not long-lived plasma cells, possess antigen specificities for viral escape mutants. J Exp Med 208: 2599-2606.
18. Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, et al. (2011) Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208: 181-193.
19. Ekiert DC, Bhabha G, Elsliger MA, Friesen RH, Jongeneelen M, et al. (2009) Antibody recognition of a highly conserved influenza virus epitope. Science 324: 246-251.
20. Dilillo DJ, Tan GS, Palese P, Ravetch JV (2014) Broadly neutralizing hemagglutinin stalk-specific antibodies require FcgammaR interactions for protection against influenza virus in vivo. Nat Med 20: 143-151.
21. Banzhoff A, Gasparini R, Laghi-Pasini F, Staniscia T, Durando P, et al. (2009) MF59-adjuvanted H5N1 vaccine induces immunologic memory and heterotypic antibody responses in non-elderly and elderly adults. PLoS ONE 4: e4384.
22. Garcon N, Vaughn DW, Didierlaurent AM (2012) Development and evaluation of AS03, an Adjuvant System containing alpha-tocopherol and squalene in an oil-in-water emulsion. Expert Rev Vaccines 11: 349-366.
23. Moris P, van der Most R, Leroux-Roels I, Clement F, Drame M, et al. (2010) H5N1 influenza vaccine formulated with AS03 A induces strong cross-reactive and polyfunctional CD4 T-cell responses. J Clin Immunol 31: 443-454.
24. Galli G, Medini D, Borgogni E, Zedda L, Bardelli M, 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 U S A 106: 3877-3882.
25. Spensieri F, Borgogni E, Zedda L, Bardelli M, Buricchi F, et al. (2013) Human circulating influenza-CD4+ ICOS1+IL-21+ T cells expand after vaccination, exert helper function, and predict antibody responses. Proc Natl Acad Sci U S A 110: 14330-14335.