Evaluation of mucosal adjuvants and immunization routes for the induction of systemic and mucosal humoral immune responses in macaques

Human Vaccines and Immunotherapeutics

Volumn 11, Issue 12, 2015, Pages 2913-2922

  Veazey, Ronald S ^a   Siddiqui, Asna ^b   Klein, Katja ^b,c   Buffa, Viviana ^b   Fischetti, Lucia ^b   Doyle Meyers, Lara ^a   King, Deborah F ^b   Tregoning, John S ^b   Shattock, Robin J ^b  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Adjuvant; Inflammation; Intranasal; Macaque; Mucosal; TLR ligand

Indexed keywords

BETA GALACTOSIDASE; CHITOSAN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; KEYHOLE LIMPET HEMOCYANIN; MONOCYTE CHEMOTACTIC PROTEIN 1; OVALBUMIN; PAM3CSK4; PHOSPHORYL LIPID A; POLYINOSINIC POLYCYTIDYLIC ACID; RANTES; RESIQUIMOD; THYMIC STROMAL LYMPHOPOIETIN; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ANTIBODY; CYTOKINE; HEMOCYANIN; IMIDAZOLE DERIVATIVE; KEYHOLE-LIMPET HEMOCYANIN; LIPOPEPTIDE; PAM(3)CSK(4) PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CD3+ T LYMPHOCYTE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HUMORAL IMMUNITY; INFLAMMATION; MUCOSAL IMMUNITY; NONHUMAN; RHESUS MONKEY; ANIMAL; ANTIBODY PRODUCTION; BLOOD; EVALUATION STUDY; IMMUNIZATION; IMMUNOLOGY; INTRAMUSCULAR DRUG ADMINISTRATION; INTRANASAL DRUG ADMINISTRATION; MUCOSA; PROCEDURES;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; ANTIBODIES; ANTIBODY FORMATION; BETA-GALACTOSIDASE; CHITOSAN; CYTOKINES; FEMALE; HEMOCYANIN; IMIDAZOLES; IMMUNITY, MUCOSAL; IMMUNIZATION; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INFLAMMATION; INJECTIONS, INTRAMUSCULAR; LIPOPEPTIDES; MACACA MULATTA; MUCOUS MEMBRANE; OVALBUMIN; POLY I-C;

EID: 84961768899     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.1080/21645515.2015.1070998     Document Type: Article

References (36)

1. Lycke N. Recent progress in mucosal vaccine development: potential and limitations. Nat Rev Immunol 2012; 12:592-605 PMID22828912; http://dx.doi.org/10.1038/nri3251
2. Neutra MR, Kozlowski PA. Mucosal vaccines: the promise and the challenge. Nat Rev Immunol 2006; 6:148-58 PMID16491139; http://dx.doi.org/10.1038/nri1777
3. Mestecky J, McGhee JR, Michalek SM, Arnold RR, Crago SS, Babb JL. Concept of the local and common mucosal immune response. Adv Exp Med Biol 1978; 107:185-92
4. Holmgren J, Czerkinsky C. Mucosal immunity and vaccines. Nat Med 2005; 11:S45-S53 PMID15812489; http://dx.doi.org/10.1038/nm1213
5. Newsted D, Fallahi F, Golshani A, Azizi A. Advances and challenges in mucosal adjuvant technology. Vaccine 2015; 33:2399-405 PMID25865473; http://dx.doi.org/10.1016/j.vaccine.2015.03.096
6. Riese P, Sakthivel P, Trittel S, Guzman CA. Intranasal formulations: promising strategy to deliver vaccines. Expert opin Drug Deliv 2014; 11:1619-34 PMID24962722; http://dx.doi.org/10.1517/17425247.2014.931936
7. Lewis DJ, Huo Z, Barnett S, Kromann I, Giemza R, Galiza E, Woodrow M, Thierry-Carstensen B, Andersen P, Novicki D, et al. Transient facial nerve paralysis (Bell’s palsy) following intranasal delivery of a genetically detoxified mutant of Escherichia coli heat labile toxin. PloS one 2009; 4:e6999 PMID19756141; http://dx.doi.org/10.1371/journal.pone.0006999
8. Buffa V, Klein K, Fischetti L, Shattock RJ. Evaluation of TLR Agonists as Potential Mucosal Adjuvants for HIV gp140 and Tetanus Toxoid in Mice. PloS one 2012; 7:e50529 PMID23272062; http://dx.doi.org/10.1371/journal.pone.0050529
9. Van Roey GA, Arias MA, Tregoning JS, Rowe G, Shat-tock RJ. Thymic stromal lymphopoietin (TSLP) acts as a potent mucosal adjuvant for HIV-1 gp140 vaccination in mice. Eur J Immunol 2012; 42:353-63 PMID22057556; http://dx.doi.org/10.1002/eji.201141787
10. Fouda GG, Amos JD, Wilks AB, Pollara J, Ray CA, Chand A, Kunz EL, Liebl BE, Whitaker K, Carville A, et al. Mucosal immunization of lactating female rhesus monkeys with a transmitted/founder HIV-1 envelope induces strong Env-specific IgA antibody responses in JVI.00528-13 breast milk. J Virol 2013; 87:6986-99; PMID23596289; http://dx.doi.org/10.1128/JVI.00528-13
11. Li Y, To J, Verdia-Baguena C, Dossena S, Surya W, Huang M, Paulmichl M, Liu DX, Aguilella VM, Torres J. Inhibition of the human respiratory syncytial virus small hydrophobic protein and structural variations in a bicelle environment. J Virol 2014; 88:11899-914 PMID25100835; http://dx.doi.org/10.1128/ JVI.00839-14
12. Kobayashi T, Fukushima K, Sannan T, Saito N, Takiguchi Y, Sato Y, Hasegawa H, Ishikawa K. Evaluation of the effectiveness and safety of chitosan derivatives as adjuvants for intranasal vaccines. Viral Immunol 2013; 26:133-42 PMID23509985; http://dx.doi.org/10.1089/vim.2012.0057
13. Vasiliev YM. Chitosan-based vaccine adjuvants: incomplete characterization complicates preclinical and clinical evaluation. Expert Rev Vaccines 2015; 14:37-53 PMID25262982; http://dx.doi.org/10.1586/14760584.2015.956729
14. McNeela EA, Jabbal-Gill I, Illum L, Pizza M, Rappuoli R, Podda A, Lewis DJ, Mills KH. Intranasal immunization with genetically detoxified diphtheria toxin induces T cell responses in humans: enhancement of Th2 responses and toxin-neutralizing antibodies by formulation with chitosan. Vaccine 2004; 22:909-14 PMID15161067; http://dx.doi.org/10.1016/j.vaccine.2003.09.012
15. Huo Z, Sinha R, McNeela EA, Borrow R, Giemza R, Cosgrove C, Heath PT, Mills KH, Rappuoli R, Griffin GE, et al. Induction of protective serum meningococcal bactericidal and diphtheria-neutralizing antibodies and mucosal immunoglobulin A in volunteers by nasal insufflations of the Neisseria meningitidis serogroup C polysaccharide-CRM197 conjugate vaccine mixed with chitosan. Infect Immun 2005; 73:8256-65 PMID16299322; http://dx.doi.org/10.1128/IAI.73.12.8256-8265.2005
16. Robinson M, Strickland I, Coyle A, Sleeman M, Anderson I, May RM. Thymic Stromal Lympho-poeitin (TSLP) Activates Human And Cynomolgus Macaque Dendritic Cells And Induces Th1 As Well As Th2 Responses In Human Total T Helper Cells. ATS: American Thoracic Society, 2010:A3794-A.
17. Epaulard O, Adam L, Poux C, Zurawski G, Salabert N, Rosenbaum P, Dereuddre-Bosquet N, Zurawski S, Fla- mar AL, Oh S, et al. Macrophage-and neutrophil-193:2416-26 http://dx.doi.org/10.4049/jimmunol.1303339
18. Morse MA, Chapman R, Powderly J, Blackwell K, Keler T, Green J, Riggs R, He LZ, Ramakrishna V, Vitale L, et al. Phase I study utilizing a novel antigen-presenting cell-targeted vaccine with Toll-like receptor stimulation to induce immunity to self-antigens in cancer patients. Clin Cancer Res 2011; 17:4844-53 PMID21632857; http://dx.doi.org/10.1158/1078-0432.CCR-11-0891
19. Clejan S, Mandrea E, Pandrea IV, Dufour J, Japa S, Veazey RS. Immune responses induced by intranasal imiquimod and implications for therapeutics in rhinovirus infections. J Cell Mol Med 2005; 9:457-61 PMID15963264; http://dx.doi.org/10.1111/j.1582-4934.2005.tb00370.x
20. Pockros PJ, Guyader D, Patton H, Tong MJ, Wright T, McHutchison JG, Meng TC. Oral resiquimod in chronic HCV infection: Safety and efficacy in 2 placebo-controlled, double-blind phase IIa studies. J Hepatol 2007; 47:174-82 PMID17532523; http://dx.doi.org/10.1016/j.jhep.2007.02.025
21. McCluskie MJ, Brazolot Millan CL, Gramzinski RA, Robinson HL, Santoro JC, Fuller JT, Widera G, Haynes JR, Purcell RH, Davis HL, et al. Route and method of delivery of DNA vaccine influence immune responses in mice and non-human primates. Mol Med 1999; 5:287-300 PMID10390545; http://dx.doi.org/10.1007/s0089490050287
22. Xiao P, Patterson LJ, Kuate S, Brocca-Cofano E, Thomas MA, Venzon D, Zhao J, DiPasquale J, Fenizia C, Lee EM, et al. Replicating adenovirus-simian immunodeficiency virus (SIV) recombinant priming and envelope protein boosting elicits localized, mucosal IgA immunity in rhesus macaques correlated with delayed acquisition following a repeated low-dose rectal SIV(mac251) challenge. J Virol 2012; 86:4644-57 PMID22345466; http://dx.doi.org/10.1128/JVI.06812-11
23. Kraan H, Vrieling H, Czerkinsky C, Jiskoot W, Kersten G, Amorij JP. Buccal and sublingual vaccine delivery. J Control Release 2014; 190:580-92 PMID24911355; http://dx.doi.org/10.1016/j.jconrel.2014.05.060
24. Larche M. Immune mechanisms of sublingual immunotherapy: are oral Langerhans cells the masters of tolerance? J Allergy Clin Immunol 2010; 126:646-7 PMID20816196; http://dx.doi.org/10.1016/j.jaci.2010.07.027
25. Huo Z, Bissett SL, Giemza R, Beddows S, Oeser C, Lewis DJ. Systemic and mucosal immune responses to sublingual or intramuscular human papilloma virus antigens in healthy female volunteers. PloS One 2012; 7:e33736 PMID22438987; http://dx.doi.org/10.1371/journal.pone.0033736
26. Belyakov IM, Isakov D, Zhu Q, Dzutsev A, Berzofsky JA. A novel functional CTL avidity/activity compart-mentalization to the site of mucosal immunization con- tributes to protection of macaques against simian/ human immunodeficiency viral depletion of mucosal CD4C T cells. J Immunol 2007; 178:7211-21 http://dx.doi.org/10.4049/jimmunol.178.11.7211
27. Belyakov IM, Hel Z, Kelsall B, Kuznetsov VA, Ahlers JD, Nacsa J, Watkins DI, Allen TM, Sette A, Altman J, et al. Mucosal AIDS vaccine reduces disease and viral load in gut reservoir and blood after mucosal infection of macaques. Nat Med 2001; 7:1320-6 PMID11726972; http://dx.doi.org/10.1038/nm1201-1320
28. Sharpe S, Hanke T, Tinsley-Bown A, Dennis M, Dow- all S, McMichael A, Cranage M. Mucosal immunization with PLGA-microencapsulated DNA primes a SIV-specific CTL response revealed by boosting with cognate recombinant modified vaccinia virus Ankara. Virology 2003; 313:13-21; PMID12951017; http://x.doi.org/10.1016/S0042-6822(03)00282-4
29. Wright PF, Mestecky J, McElrath MJ, Keefer MC, Gorse GJ, Goepfert PA, Moldoveanu Z, Schwartz D, Spearman PW, El Habib R, et al. Comparison of systemic and mucosal delivery of 2 canarypox virus vaccines expressing either HIV-1 genes or the gene for rabies virus G protein. J Infect Dis 2004; 189:1221-31; PMID15031791; http://dx.doi.org/10.1086/382088
30. Spasova DS, Surh CD. Blowing on embers: commensal microbiota and our immune system. Front Immunol 2014; 5:318; PMID25120539; http://dx.doi.org/10.3389/fimmu.2014.00318
31. Arias MA, Van Roey GA, Tregoning JS, Moutaftsi M, Coler RN, Windish HP, Reed SG, Carter D, Shattock RJ. Glucopyranosyl Lipid Adjuvant (GLA), a Synthetic TLR4 Agonist, Promotes Potent Systemic and Mucosal Responses to Intranasal Immunization with HIVgp140. PloS one 2012; 7:e41144; PMID22829921; http://dx.doi.org/10.1371/journal.pone.0041144
32. Gwinn WM, Johnson BT, Kirwan SM, Sobel AE, Abraham SN, Gunn MD, Staats HF. A comparison of non-toxin vaccine adjuvants for their ability to enhance the immunogenicity of nasally-administered anthrax recombinant protective antigen. Vaccine 2013; 31:1480-9; PMID23352329; http://dx.doi.org/10.1016/j.vaccine.2013.01.012
33. Ketloy C, Engering A, Srichairatanakul U, Limsalakpetch A, Yongvanitchit K, Pichyangkul S, Ruxrungtham K. Expression and function of Toll-like receptors on dendritic cells and other antigen presenting cells from non-human primates. Vet Immunol Immunopathol 2008; 125:18-30; PMID18571243; http://dx.doi.org/10.1016/j.vetimm.2008.05.001
34. Klein K, Mann JF, Rogers P, Shattock RJ. Polymericpenetration enhancers promote humoral immune responses to mucosal vaccines. J Control Release 2014;183:43-50; PMID24657807; http://dx.doi.org/10.1016/j.jconrel.2014.03.018
35. Tregoning JS, Buffa V, Oszmiana A, Klein K, Walters AA, Shattock RJ. A “prime-pull” vaccine strategy has a modest effect on local and systemic antibody responses to HIV gp140 in mice. PloS one 2013; 8:e80559; PMID24260419; http://dx.doi.org/10.1371/journal.pone.0080559
36. Lewis DJ, Fraser CA, Mahmoud AN, Wiggins RC, Woodrow M, Cope A, Cai C, Giemza R, Jeffs SA, Manoussaka M, et al. Phase I Randomised Clinical Trial of an HIV-1 CN54, Clade C, Trimeric Envelope Vaccine Candidate Delivered Vaginally. PloS one 2011; 6:e25165; PMID21984924; http://dx.doi.org/10.1371/journal.pone.0025165