AS03-adjuvanted, very-low-dose influenza vaccines induce distinctive immune responses compared to unadjuvanted high-dose vaccines in BALB/c mice

Frontiers in Immunology

Volumn 6, Issue APR, 2015, Pages

  Yam, Karen K ^a   Gupta, Jyotsana ^a   Winter, Kaitlin ^a   Allen, Elizabeth ^a   Brewer, Angela ^a   Beaulieu, Edith ^b   Mallett, Corey P ^b   Burt, David S ^b   Ward, Brian J ^a  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b GLAXOSMITHKLINE   (Canada)

Author keywords

Adjuvant; AS03; Dose sparing; Influenza; Vaccine

Indexed keywords

GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN G ANTIBODY; IMMUNOLOGICAL ADJUVANT; IMMUNOLOGICAL ADJUVANT AS03; INFLUENZA VACCINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 3; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION ASSAY; CELL STIMULATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG MEGADOSE; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; HEMAGGLUTINATION INHIBITION; IMMUNE RESPONSE; INFLUENZA A (H3N2); INFLUENZA MICRONEUTRALIZATION; INFLUENZA VACCINATION; LOW DRUG DOSE; MOUSE; NONHUMAN; SERODIAGNOSIS; SPLEEN CELL; T LYMPHOCYTE ACTIVATION; VACCINATION;

EID: 84934268601     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2015.00207     Document Type: Article

References (36)

1. Tosh PK, Jacobson RM, Poland GA. Influenza vaccines: from surveillance through production to protection. Mayo Clin Proc (2010) 85:257-73. doi: 10.4065/mcp.2009.0615
2. Technical Advisory Group on Vaccine-Preventable Diseases. Final Recommendations of Pandemic Influenza. Pan American Health Organization, Regional Office of the World Health Organization (2009). Available from: http://www.paho.org/english/ad/fch/im/PandemicFlu_TAGReco_Aug2009_e.pdf
3. GlaxoSmithKline Inc. Arepanrix H1N1 [Package Insert]. Mississauga, ON (2009). Available from: http://www.hc-sc.gc.ca/dhp-mps/prodpharma/legislation/interimorders-arretesurgence/prodinfo-vaccin-eng.php
4. Leroux-Roels G. Prepandemic H5N1 influenza vaccine adjuvanted with AS03: a review of the pre-clinical and clinical data. Expert Opin Biol Ther (2009) 9:1057-71. doi:10.1517/14712590903066695
5. Langley JM, Frenette L, Ferguson L, Riff D, Sheldon E, Risi G, et al. Safety and cross-reactive immunogenicity of candidate AS03-adjuvanted prepandemic H5N1 influenza vaccines: a randomized controlled phase 1/2 trial in adults. J Infect Dis (2010) 201:1644-53. doi:10.1086/652701
6. Ferguson M, Risi G, Davis M, Sheldon E, Baron M, Li P, et al. Safety and long-term humoral immune response in adults after vaccination with an H1N1 2009 pandemic influenza vaccine with or without AS03 adjuvant. J Infect Dis (2012) 205:733-44. doi:10.1093/infdis/jir641
7. Moris P, van der Most R, Leroux-Roels I, Clement F, Drame M, Hanon E, et al. H5N1 influenza vaccine formulated with AS03A induces strong cross-reactive and polyfunctional CD4 T-cell responses. J Clin Immunol (2011) 31:443-54. doi:10.1007/s10875-010-9490-6
8. Garcon N, Vaughn DW, Didierlaurent AM. Development and evaluation of AS03, an adjuvant system containing alpha-tocopherol and squalene in an oil-in-water emulsion. Expert Rev Vaccines (2012) 11:349-66. doi:10.1586/erv.11.192
9. Leroux-Roels I, Bernhard R, Gerard P, Drame M, Hanon E, Leroux-Roels G. Broad Clade 2 cross-reactive immunity induced by an adjuvanted clade 1 rH5N1 pandemic influenza vaccine. PLoS One (2008) 3:e1665. doi:10.1371/journal.pone.0001665
10. Morel S, Didierlaurent A, Bourguignon P, Delhaye S, Baras B, Jacob V, et al. Adjuvant system AS03 containing alpha-tocopherol modulates innate immune response and leads to improved adaptive immunity. Vaccine (2011) 29:2461-73. doi:10.1016/j.vaccine.2011.01.011
11. Yam KK, Gupta J, Brewer A, Scheifele DW, Halperin S, Ward BJ. Unusual patterns of IgG avidity in some young children following two doses of the adjuvanted pandemic H1N1 (2009) influenza virus vaccine. Clin Vaccine Immunol (2013) 20:459-67. doi:10.1128/CVI.00619-12
12. Yam KK, Gipson E, Klein M, Walmsley S, Haase D, Halperin S, et al. High level antibody avidity is achieved in HIV-seropositive recipients of an inactivated split adjuvanted (AS03A) influenza vaccine. J Clin Immunol (2014) 34:655-62. doi:10.1007/s10875-014-0054-z
13. Scheifele DW, Ward BJ, Dionne M, Vanderkooi O, Langley JM, Dobson S, et al. Evaluation of adjuvanted pandemic H1N1(2009) influenza vaccine after one and two doses in young children. Pediatr Infect Dis J (2011) 30:402-7. doi:10.1097/INF.0b013e3182068f33
14. Moon JJ, Suh H, Li AV, Ockenhouse CF, Yadava A, Irvine DJ. Enhancing humoral responses to a malaria antigen with nanoparticle vaccines that expand Tfh cells and promote germinal center induction. Proc Natl Acad Sci U S A (2012) 109:1080-5. doi:10.1073/pnas.1112648109
15. Khurana S, Verma N, Talaat KR, Karron RA, Golding H. 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 (2012) 205:610-20. doi:10.1093/infdis/jir791
16. Morel S, Denoel P, Godfroid F, Cortvrindt C, Vanderheyde N, Poolman J. Induction of Bordetella pertussis-specific immune memory by DTPa vaccines. Vaccine (2011) 29:3449-55. doi:10.1016/j.vaccine.2011.02.062
17. Giannini SL, Hanon E, Moris P, Van MM, Morel S, Dessy F, et al. Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only. Vaccine (2006) 24:5937-49. doi:10.1016/j.vaccine.2006.06.005
18. Baz M, Samant M, Zekki H, Tribout-Jover P, Plante M, Lanteigne AM, et al. Effects of different adjuvants in the context of intramuscular and intranasal routes on humoral and cellular immune responses induced by detergent-split A/H3N2 influenza vaccines in mice. Clin Vaccine Immunol (2012) 19:209-18. doi:10.1128/CVI.05441-11
19. La Gruta NL, Turner SJ. T cell mediated immunity to influenza: mechanisms of viral control. Trends Immunol (2014) 35:396-402. doi:10.1016/j.it.2014.06.004
20. Dong L, Liu F, Fairman J, Hong DK, Lewis DB, Monath T, et al. Cationic liposome-DNA complexes (CLDC) adjuvant enhances the immunogenicity and cross-protective efficacy of a pre-pandemic influenza A H5N1 vaccine in mice. Vaccine (2012) 30:254-64. doi:10.1016/j.vaccine.2011.10.103
21. Liu H, Bungener L, Ter VW, Coller BA, Wilschut J, Huckriede A. Preclinical evaluation of the saponin derivative GPI-0100 as an immunostimulating and dose-sparing adjuvant for pandemic influenza vaccines. Vaccine (2011) 29:2037-43. doi:10.1016/j.vaccine.2011.01.012
22. McHeyzer-Williams LJ, McHeyzer-Williams MG. Antigen-specific memory B cell development. Annu Rev Immunol (2005) 23:487-513. doi:10.1146/annurev.immunol.23.021704.115732
23. Khurana S, Verma N, Yewdell JW, Hilbert AK, Castellino F, Lattanzi M, et al. MF59 adjuvant enhances diversity and affinity of antibody-mediated immune response to pandemic influenza vaccines. Sci Transl Med (2011) 3:85ra48. doi:10.1126/scitranslmed.3002336
24. Khurana S, Chearwae W, Castellino F, Manischewitz J, King LR, Honorkiewicz A, et al. Vaccines with MF59 adjuvant expand the antibody repertoire to target protective sites of pandemic avian H5N1 influenza virus. Sci Transl Med (2010) 2:15ra5. doi:10.1126/scitranslmed.3000624
25. Amanna IJ, Slifka MK. Mechanisms that determine plasma cell lifespan and the duration of humoral immunity. Immunol Rev (2010) 236:125-38. doi:10.1111/j.1600-065X.2010.00912.x
26. Commins SP, Borish L, Steinke JW. Immunologic messenger molecules: cytokines, interferons, and chemokines. J Allergy Clin Immunol (2010) 125:S53-72. doi:10.1016/j.jaci.2009.07.008
27. Crotty S. Follicular helper CD4 T cells (TFH). Annu Rev Immunol (2011) 29:621-63. doi:10.1146/annurev-immunol-031210-101400
28. Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immunol Cell Biol (2004) 82:488-96. doi:10.1111/j.0818-9641.2004.01272.x
29. Petrovsky N. Vaccine adjuvant safety: the elephant in the room. Expert Rev Vaccines (2013) 12:715-7. doi:10.1586/14760584.2013.811198
30. Della Cioppa G, Nicolay U, Lindert K, Leroux-Roels G, Clement F, Castellino F, et al. Superior immunogenicity of seasonal influenza vaccines containing full dose of MF59 ((R)) adjuvant: results from a dose-finding clinical trial in older adults. Hum Vaccin Immunother (2012) 8:216-27. doi:10.4161/hv.18445
31. Kannanganat S, Ibegbu C, Chennareddi L, Robinson HL, Amara RR. Multiple-cytokine-producing antiviral CD4 T cells are functionally superior to single-cytokine-producing cells. J Virol (2007) 81:8468-76. doi:10.1128/JVI.00228-07
32. Roman F, Clement F, Dewe W, Walravens K, Maes C, Willekens J, et al. Effect on cellular and humoral immune responses of the AS03 adjuvant system in an A/H1N1/2009 influenza virus vaccine administered to adults during two randomized controlled trials. Clin Vaccine Immunol (2011) 18:835-43. doi:10.1128/CVI.00480-10
33. Couch RB, Bayas JM, Caso C, Mbawuike IN, Lopez CN, Claeys C, et al. Superior antigen-specific CD4+ T-cell response with AS03-adjuvantation of a trivalent influenza vaccine in a randomised trial of adults aged 65 and older. BMC Infect Dis (2014) 14:425. doi:10.1186/1471-2334-14-425
34. Ann J, Samant M, Rheaume C, Dumas C, Beaulieu E, Morasse A, et al. Adjuvanted inactivated influenza A(H3N2) vaccines induce stronger immunogenicity in mice and confer higher protection in ferrets than unadjuvanted inactivated vaccines. Vaccine (2014) 32:5730-9. doi:10.1016/j.vaccine.2014.08.029
35. Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci U S A (2013) 110:3507-12. doi:10.1073/pnas.1222878110
36. Magnusson SE, Reimer JM, Karlsson KH, Lilja L, Bengtsson KL, Stertman L. Immune enhancing properties of the novel Matrix-M adjuvant leads to potentiated immune responses to an influenza vaccine in mice. Vaccine (2013) 31:1725-33. doi:10.1016/j.vaccine.2013.01.039