Evaluation of Mucosal and Systemic Immune Responses Elicited by GPI-0100- Adjuvanted Influenza Vaccine Delivered by Different Immunization Strategies

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Liu, Heng ^a   Patil, Harshad P ^a   de Vries Idema, Jacqueline ^a   Wilschut, Jan ^a   Huckriede, Anke ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GPI 0100; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; INFLUENZA VACCINE; PR8 INFLUENZA SUBUNIT VACCINE; SAPONIN; UNCLASSIFIED DRUG;

ADMINISTRATION OF DRUGS, FOOD AND CHEMICALS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BAGG ALBINO MOUSE; CELLULAR IMMUNITY; DRUG DELIVERY SYSTEM; DRUG FORMULATION; FEMALE; IMMUNE RESPONSE; INFLUENZA VACCINATION; INTRAPULMONARY ADMINISTRATION; MOUSE; MUCOSAL ADMINISTRATION; MUCOSAL IMMUNITY; NONHUMAN; PARENTERAL DRUG ADMINISTRATION; RESPIRATORY TRACT INFECTION; SYSTEMIC IMMUNE RESPONSE;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODIES, VIRAL; CELL LINE; DRUG ADMINISTRATION ROUTES; DRUG EVALUATION, PRECLINICAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNITY; IMMUNITY, MUCOSAL; IMMUNIZATION; IMMUNIZATION, SECONDARY; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; LUNG; MICE; MICE, INBRED BALB C; SAPONINS; T-LYMPHOCYTES; VACCINES, SUBUNIT;

EID: 84881163364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069649     Document Type: Article

References (40)

1. Brandtzaeg P, (2007) Induction of secretory immunity and memory at mucosal surfaces. Vaccine 25: 5467-5484. doi:10.1016/j.vaccine.2006.12.001. PubMed: 17227687.
2. Brandtzaeg P, (2009) Mucosal immunity: induction, dissemination, and effector functions. Scand J Immunol 70: 505-515. doi:10.1111/j.1365-3083.2009.02319.x. PubMed: 19906191.
3. Brandtzaeg P, Farstad IN, Johansen FE, Morton HC, Norderhaug IN, et al. (1999) The B-cell system of human mucosae and exocrine glands. Immunol Rev 171: 45-87. doi:10.1111/j.1600-065X.1999.tb01342.x. PubMed: 10582165.
4. Brandtzaeg P, Farstad IN, Haraldsen G, (1999) Regional specialization in the mucosal immune system: primed cells do not always home along the same track. Immunol Today 20: 267-277. doi:10.1016/S0167-5699(99)01468-1. PubMed: 10354552.
5. Lycke N, (2012) Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol 12: 592-605. doi:10.1038/nri3251. PubMed: 22828912.
6. van Riet E, Ainai A, Suzuki T, Hasegawa H, (2012) Mucosal IgA responses in influenza virus infections; thoughts for vaccine design. Vaccine 30: 5893-5900. doi:10.1016/j.vaccine.2012.04.109. PubMed: 22835738.
7. Neutra MR, Kozlowski PA, (2006) Mucosal vaccines: the promise and the challenge. Nat Rev Immunol 6: 148-158. doi:10.1038/nri1777. PubMed: 16491139.
8. Belyakov IM, Ahlers JD, (2009) What role does the route of immunization play in the generation of protective immunity against mucosal pathogens? J Immunol 183: 6883-6892. doi:10.4049/jimmunol.0901466. PubMed: 19923474.
9. Haan L, Verweij WR, Holtrop M, Brands R, van Scharrenburg GJ, et al. (2001) Nasal or intramuscular immunization of mice with influenza subunit antigen and the B subunit of Escherichia coli heat-labile toxin induces IgA- or IgG-mediated protective mucosal immunity. Vaccine 19: 2898-2907. doi:10.1016/S0264-410X(00)00556-9. PubMed: 11282201.
10. Defang GN, Martin NJ, Burgess TH, Millar EV, Pecenka LA, et al. (2012) Comparative Analysis of Hemagglutination Inhibition Titers Generated Using Temporally Matched Serum and Plasma Samples. PLOS ONE 7: e48229. doi:10.1371/journal.pone.0048229. PubMed: 23284613.
11. Yamamoto M, Vancott JL, Okahashi N, Marinaro M, Kiyono H, et al. (1996) The role of Th1 and Th2 cells for mucosal IgA responses. Ann N Y Acad Sci 778: 64-71. doi:10.1111/j.1749-6632.1996.tb21115.x. PubMed: 8611017.
12. Stumbles PA, Thomas JA, Pimm CL, Lee PT, Venaille TJ, et al. (1998) Resting respiratory tract dendritic cells preferentially stimulate T helper cell type 2 (Th2) responses and require obligatory cytokine signals for induction of Th1 immunity. J Exp Med 188: 2019-2031. doi:10.1084/jem.188.11.2019. PubMed: 9841916.
13. Huber VC, McKeon RM, Brackin MN, Miller LA, Keating R, et al. (2006) Distinct contributions of vaccine-induced immunoglobulin G1 (IgG1) and IgG2a antibodies to protective immunity against influenza. Clin Vaccine Immunol 13: 981-990. doi:10.1128/CVI.00156-06. PubMed: 16960108.
14. Huber VC, Lynch JM, Bucher DJ, Le J, Metzger DW, (2001) Fc receptor-mediated phagocytosis makes a significant contribution to clearance of influenza virus infections. J Immunol 166: 7381-7388. PubMed: 11390489.
15. Moran TM, Park H, Fernandez-Sesma A, Schulman JL, (1999) Th2 responses to inactivated influenza virus can Be converted to Th1 responses and facilitate recovery from heterosubtypic virus infection. J Infect Dis 180: 579-585. doi:10.1086/314952. PubMed: 10438342.
16. Cristillo AD, Ferrari MG, Hudacik L, Lewis B, Galmin L, et al. (2011) Induction of mucosal and systemic antibody and T-cell responses following prime-boost immunization with novel adjuvanted human immunodeficiency virus-1-vaccine formulations. J Gen Virol 92: 128-140. doi:10.1099/vir.0.023242-0. PubMed: 21169215.
17. Vindurampulle CJ, Cuberos LF, Barry EM, Pasetti MF, Levine MM, (2004) Recombinant Salmonella enterica serovar Typhi in a prime-boost strategy. Vaccine 22: 3744-3750. doi:10.1016/j.vaccine.2004.03.025. PubMed: 15315855.
18. Crouch CF, Daly J, Henley W, Hannant D, Wilkins J, et al. (2005) The use of a systemic prime/mucosal boost strategy with an equine influenza ISCOM vaccine to induce protective immunity in horses. Vet Immunol Immunopathol 108: 345-355. doi:10.1016/j.vetimm.2005.06.009. PubMed: 16098611.
19. Schulte R, Suh YS, Sauermann U, Ochieng W, Sopper S, et al. (2009) Mucosal prior to systemic application of recombinant adenovirus boosting is more immunogenic than systemic application twice but confers similar protection against SIV-challenge in DNA vaccine-primed macaques. Virology 383: 300-309. doi:10.1016/j.virol.2008.10.012. PubMed: 19027133.
20. Ranasinghe C, Eyers F, Stambas J, Boyle DB, Ramshaw IA, et al. (2011) A comparative analysis of HIV-specific mucosal/systemic T cell immunity and avidity following rDNA/rFPV and poxvirus-poxvirus prime boost immunisations. Vaccine 29: 3008-3020. doi:10.1016/j.vaccine.2011.01.106. PubMed: 21352941.
21. Schulze K, Staib C, Schätzl HM, Ebensen T, Erfle V, et al. (2008) A prime-boost vaccination protocol optimizes immune responses against the nucleocapsid protein of the SARS coronavirus. Vaccine 26: 6678-6684. doi:10.1016/j.vaccine.2008.09.006. PubMed: 18805454.
22. Vajdy M, Singh M, Ugozzoli M, Briones M, Soenawan E, et al. (2003) Enhanced mucosal and systemic immune responses to Helicobacter pylori antigens through mucosal priming followed by systemic boosting immunizations. Immunology 110: 86-94. doi:10.1046/j.1365-2567.2003.01711.x. PubMed: 12941145.
23. Huang X, Liu L, Ren L, Qiu C, Wan Y, et al. (2007) Mucosal priming with replicative Tiantan vaccinia and systemic boosting with DNA vaccine raised strong mucosal and systemic HIV-specific immune responses. Vaccine 25: 8874-8884. doi:10.1016/j.vaccine.2007.08.066. PubMed: 18061316.
24. SK Eo, M Gierynska, AA Kamar, BT Rouse,. (2001) Prime-boost immunization with DNA vaccine: mucosal route of administration changes the rules. J Immunol 166: 5473-5479.
25. McCluskie MJ, Weeratna RD, Payette PJ, Davis HL, (2002) Parenteral and mucosal prime-boost immunization strategies in mice with hepatitis B surface antigen and CpG DNA. FEMS Immunol Med Microbiol 32: 179-185. doi:10.1111/j.1574-695X.2002.tb00551.x. PubMed: 11934561.
26. Park KS, Lee J, Ahn SS, Byun YH, Seong BL, et al. (2009) Mucosal immunity induced by adenovirus-based H5N1 HPAI vaccine confers protection against a lethal H5N2 avian influenza virus challenge. Virology 395: 182-189. doi:10.1016/j.virol.2009.09.018. PubMed: 19836045.
27. Liu H, Bungener L, ter Veer W, Coller BA, Wilschut J, et al. (2011) Preclinical evaluation of the saponin derivative GPI-0100 as an immunostimulating and dose-sparing adjuvant for pandemic influenza vaccines. Vaccine 29: 2037-2043. doi:10.1016/j.vaccine.2011.01.012. PubMed: 21251903.
28. Liu H, Patil HP, de Vries-Idema J, Wilschut J, Huckriede A, (2012) Enhancement of the Immunogenicity and Protective Efficacy of a Mucosal Influenza Subunit Vaccine by the Saponin Adjuvant GPI-0100. PLOS ONE 7: e52135. doi:10.1371/journal.pone.0052135. PubMed: 23284901.
29. Peterson GL, (1977) A simplification of the protein assay method of Lowryet al. which is more generally applicable. Anal Biochem 83: 346-356. doi:10.1016/0003-2697(77)90043-4. PubMed: 603028.
30. Bungener L, Geeraedts F, Ter Veer W, Medema J, Wilschut J, et al. (2008) Alum boosts TH2-type antibody responses to whole-inactivated virus influenza vaccine in mice but does not confer superior protection. Vaccine 26: 2350-2359. doi:10.1016/j.vaccine.2008.02.063. PubMed: 18400340.
31. Southam DS, Dolovich M, O'Byrne PM, Inman MD, (2002) Distribution of intranasal instillations in mice: effects of volume, time, body position, and anesthesia. Am J Physiol Lung Cell Mol Physiol 282: L833-L839. PubMed: 11880310.
32. Renegar KB, Small PA Jr, Boykins LG, Wright PF, (2004) Role of IgA versus IgG in the control of influenza viral infection in the murine respiratory tract. J Immunol 173: 1978-1986. PubMed: 15265932.
33. Minne A, Louahed J, Mehauden S, Baras B, Renauld JC, et al. (2007) The delivery site of a monovalent influenza vaccine within the respiratory tract impacts on the immune response. Immunology 122: 316-325. doi:10.1111/j.1365-2567.2007.02641.x. PubMed: 17521369.
34. Geeraedts F, Saluja V, ter Veer W, Amorij JP, Frijlink HW, et al. (2010) Preservation of the immunogenicity of dry-powder influenza H5N1 whole inactivated virus vaccine at elevated storage temperatures. AAPS J 12: 215-222. doi:10.1208/s12248-010-9179-z. PubMed: 20195930.
35. Amorij JP, Hinrichs WLj, Frijlink HW, Wilschut JC, Huckriede A, (2010) Needle-free influenza vaccination. Lancet Infect Dis 10: 699-711. doi:10.1016/S1473-3099(10)70157-2. PubMed: 20883966.
36. Joo HM, He Y, Sundararajan A, Huan L, Sangster MY, (2010) Quantitative analysis of influenza virus-specific B cell memory generated by different routes of inactivated virus vaccination. Vaccine 28: 2186-2194. doi:10.1016/j.vaccine.2009.12.058. PubMed: 20056191.
37. Kohlmeier JE, Woodland DL, (2009) Immunity to respiratory viruses. Annu Rev Immunol 27: 61-82. doi:10.1146/annurev.immunol.021908.132625. PubMed: 18954284.
38. Bice DE, Muggenburg BA, (1996) Pulmonary immune memory: localized production of antibody in the lung after antigen challenge. Immunology 88: 191-197. doi:10.1111/j.1365-2567.1996.tb00004.x. PubMed: 8690450.
39. Mason MJ, Bice DE, Muggenburg BA, (1985) Local pulmonary immune responsiveness after multiple antigenic exposures in the cynomolgus monkey. Am Rev Respir Dis 132: 657-660. PubMed: 4041149.
40. Mason MJ, Gillett NA, Bice DE, (1989) Comparison of systemic and local immune responses after multiple pulmonary antigen exposures. Reg Immunol 2: 149-157. PubMed: 2484300.