A comparison of non-toxin vaccine adjuvants for their ability to enhance the immunogenicity of nasally-administered anthrax recombinant protective antigen

Vaccine

Volumn 31, Issue 11, 2013, Pages 1480-1489

  Gwinn, William M ^a   Johnson, Brandi T ^a   Kirwan, Shaun M ^a   Sobel, Ashley E ^a   Abraham, Soman N ^a   Gunn, Michael D ^a   Staats, Herman F ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Compound 48 80; Nasal immunization; Non toxin adjuvants; Toll like receptor ligands

Indexed keywords

3M 019; ADJUVANT; ANTHRAX VACCINE; CHOLERA TOXIN; CPG OLIGODEOXYNUCLEOTIDE; GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN A; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 5; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTRALIZING ANTIBODY; PAM3CSK4 ADJUVANT; RANTES; RESIQUIMOD; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTHRAX; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOGENICITY; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOSTIMULATION; IN VIVO STUDY; INNATE IMMUNITY; LETHAL GENE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; TREATMENT DURATION;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ANIMALS; ANTHRAX VACCINES; ANTIBODIES, BACTERIAL; ANTIBODIES, NEUTRALIZING; ANTIGENS, BACTERIAL; ANTITOXINS; BACTERIAL TOXINS; CYTOKINES; FEMALE; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN G; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; SERUM; VACCINES, SYNTHETIC;

EID: 84874409728     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2013.01.012     Document Type: Article

References (48)

1. Xiao B.G., Link H. Mucosal tolerance: a two-edged sword to prevent and treat autoimmune diseases. Clin Immunol Immunopathol 1997, 85(2):119-128.
2. Pizza M., Giuliani M.M., Fontana M.R., Monaci E., Douce G., Dougan G., et al. Mucosal vaccines: non toxic derivatives of LT and CT as mucosal adjuvants. Vaccine 2001, 19(17/19):2534-2541.
3. Snider D.P., Marshall J.S., Perdue M.H., Liang H. Production of IgE antibody and allergic sensitization of intestinal and peripheral tissues after oral immunization with protein Ag and cholera toxin. J Immunol 1994, 153(2):647-657.
4. van Ginkel F.W., Jackson R.J., Yuki Y., McGhee J.R. Cutting edge: the mucosal adjuvant cholera toxin redirects vaccine proteins into olfactory tissues. J Immunol 2000, 165:4778-4782.
5. Couch R.B. Nasal vaccination, Escherichia coli enterotoxin, and Bell's palsy. N Engl J Med 2004, 350(February (9)):860-861.
6. Hodge L.M., Marinaro M., Jones H.P., McGhee J.R., Kiyono H., Simecka J.W., et al. (IgA) responses and IgE-associated inflammation along the respiratory tract after mucosal but not systemic immunization. Infect Immun 2001, 69(April (4)):2328-2338.
7. Staats H.F., Ennis F.A. IL-1 is an effective adjuvant for mucosal and systemic immune responses when coadministered with protein immunogens. J Immunol 1999, 162(May (10)):6141-6147.
8. Bradney C.P., Sempowski G.D., Liao H.X., Haynes B.F., Staats H.F. Cytokines as adjuvants for the induction of anti-human immunodeficiency virus peptide immunoglobulin G (IgG) and IgA antibodies in serum and mucosal secretions after nasal immunization. J Virol 2002, 76(January (2)):517-524.
9. Przetak M., Chow J., Cheng H., Rose J., Hawkins L.D., Ishizaka S.T. Novel synthetic LPS receptor agonists boost systemic and mucosal antibody responses in mice. Vaccine 2003, 21(February (9/10)):961-970.
10. Chisholm D., Libet L., Hayashi T., Horner A.A. Airway peptidoglycan and immunostimulatory DNA exposures have divergent effects on the development of airway allergen hypersensitivities. J Allergy Clin Immunol 2004, 113(March (3)):448-454.
11. Lahiri A., Das P., Chakravortty D. Engagement of TLR signaling as adjuvant: towards smarter vaccine and beyond. Vaccine 2008, 26(December (52)):6777-6783.
12. Caproni E., Tritto E., Cortese M., Muzzi A., Mosca F., Monaci E., et al. MF59 and Pam3CSK4 boost adaptive responses to influenza subunit vaccine through an IFN Type I-independent mechanism of action. J Immunol 2012, 188(April (1)):3088-3098.
13. El-Kamary S.S., Pasetti M.F., Mendelman P.M., Frey S.E., Bernstein D.I., Treanor J.J., et al. Adjuvanted intranasal Norwalk virus-like particle vaccine elicits antibodies and antibody-secreting cells that express homing receptors for mucosal and peripheral lymphoid tissues. J Infect Dis 2010 Dec 1, 202(11):1649-1658.
14. McLachlan J.B., Shelburne C.P., Hart J.P., Pizzo S.V., Goyal R., Brooking-Dixon R., et al. Mast cell activators: a new class of highly effective vaccine adjuvants. Nat Med 2008, 14(May (5)):536-541.
15. Meng S., Liu Z., Xu L., Li L., Mei S., Bao L., et al. Intranasal immunization with recombinant HA and mast cell activator C48/80 elicits protective immunity against 2009 pandemic H1N1 influenza in mice. PLoS ONE 2008, 6(5):e19863.
16. Staats H.F., Fielhauer J.R., Thompson A.L., Tripp A.A., Sobel A.E., Maddaloni M., et al. Mucosal targeting of a BoNT/A subunit vaccine adjuvanted with a mast cell activator enhances induction of BoNT/A neutralizing antibodies in rabbits. PLoS ONE 2011, 6(1):e16532.
17. Wang S.H., Kirwan S.M., Abraham S.N., Staats H.F., Hickey A.J. Stable dry powder formulation for nasal delivery of anthrax vaccine. J Pharm Sci 2012, 101(January (1)):31-47.
18. Gwinn W.M., Kirwan S.M., Wang S.H., Ashcraft K.A., Sparks N.L., Doil C.R., et al. Effective induction of protective systemic immunity with nasally administered vaccines adjuvanted with IL-1. Vaccine 2010, 28(October (42)):6901-6914.
19. Rosset M.B., Ballerini C., Gregoire S., Metharom P., Carnaud C., Aucouturier P. Breaking immune tolerance to the prion protein using prion protein peptides plus oligodeoxynucleotide-CpG in mice. J Immunol 2004, 172(May (9)):5168-5174.
20. Redecke V., Hacker H., Datta R.A., Fermin A., Pitha P.M., Broide D.H., et al. Cutting edge: activation of toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma. J Immunol 2004, 172(March (5)):2739-2743.
21. Quarcoo D., Weixler S., Joachim R.A., Stock P., Kallinich T., Ahrens B., et al. Resiquimod, a new immune response modifier from the family of imidazoquinolinamines, inhibits allergen-induced Th2 responses, airway inflammation and airway hyper-reactivity in mice. Clin Exp Aller 2004, 34(August (8)):1314-1320.
22. Otero M., Calarota S.A., Felber B., Laddy D., Pavlakis G., Boyer J.D., et al. Resiquimod is a modest adjuvant for HIV-1 gag-based genetic immunization in a mouse model. Vaccine 2004, 22(April (13/14)):1782-1790.
23. McGowen A.L., Hale L.P., Shelburne C.P., Abraham S.N., Staats H.F. The mast cell activator compound 48/80 is safe and effective when used as an adjuvant for intradermal immunization with Bacillus anthracis protective antigen. Vaccine 2009, 27(June (27)):3544-3552.
24. de Jonge M.I., Hamstra H.J., Jiskoot W., Roholl P., Williams N.A., Dankert J., et al. Intranasal immunisation of mice with liposomes containing recombinant meningococcal OpaB and OpaJ proteins. Vaccine 2004, September (22)(29/30):4021-4028.
25. Thompson A.L., Johnson B.T., Sempowski G.D., Gunn M.D., Hou B., DeFranco A.L., et al. Maximal adjuvant activity of nasally delivered IL-1alpha requires adjuvant-responsive CD11c(+) cells and does not correlate with adjuvant-induced in vivo cytokine production. J Immunol 2012, 188(March (6)):2834-2846.
26. Staats H.F., Alam S.M., Scearce R.M., Kirwan S.M., Zhang J.X., Gwinn W.M., et al. In vitro and in vivo characterization of anthrax anti-protective antigen and anti-lethal factor monoclonal antibodies after passive transfer in a mouse lethal toxin challenge model to define correlates of immunity. Infect Immun 2007, 75(November (11)):5443-5452.
27. Valensi J.P., Carlson J.R., Van Nest G.A. Systemic cytokine profiles in BALB/c mice immunized with trivalent influenza vaccine containing MF59 oil emulsion and other advanced adjuvants. J Immunol 1994, 153(November (9)):4029-4039.
28. Seubert A., Monaci E., Pizza M., O'Hagan D.T., Wack A. The adjuvants aluminum hydroxide and MF59 induce monocyte and granulocyte chemoattractants and enhance monocyte differentiation toward dendritic cells. J Immunol 2008, 180(April (8)):5402-5412.
29. Korsholm K.S., Petersen R.V., Agger E.M., Andersen P. T-helper 1 and T-helper 2 adjuvants induce distinct differences in the magnitude, quality and kinetics of the early inflammatory response at the site of injection. Immunology 2010, (January (1)):75-86.
30. Danuser B., Rebsamen H., Weber C., Krueger H. Lipopolysaccharide-induced nasal cytokine response: a dose-response evaluation. Eur Arch Otorhinolaryngol 2000, 257(December (10)):527-532.
31. Boyaka P.N., Tafaro A., Fischer R., Leppla S.H., Fujihashi K., McGhee J.R. Effective mucosal immunity to anthrax: neutralizing antibodies and Th cell responses following nasal immunization with protective antigen. J Immunol 2003, 170(June (11)):5636-5643.
32. Weeratna R.D., Makinen S.R., McCluskie M.J., Davis H.L. TLR agonists as vaccine adjuvants: comparison of CpG ODN and Resiquimod (R-848). Vaccine 2005, 23(November (45)):5263-5270.
33. Ghosh T.K., Mickelson D.J., Fink J., Solberg J.C., Inglefield J.R., Hook D., et al. Toll-like receptor (TLR) 2-9 agonists-induced cytokines and chemokines: I. Comparison with T cell receptor-induced responses. Cell Immunol 2006, 243(September (1)):48-57.
34. Wang S.H., Thompson A.L., Hickey A.J., Staats H.F. Dry powder vaccines for mucosal administration: critical factors in manufacture and delivery. Curr Top Microbiol Immunol 2012, 354(August):121-156.
35. Huang J., Mikszta J.A., Ferriter M.S., Jiang G., Harvey N.G., Dyas B., et al. Intranasal administration of dry powder anthrax vaccine provides protection against lethal aerosol spore challenge. Hum Vaccines 2007, 3(May-June (3)):90-93.
36. Elson C.O. Cholera toxin as a mucosal adjuvant: effects of H-2 major histocompatibility complex and lps genes. Infect Immun 1992, 60(7):2874-2879.
37. Durand V., Wong S.Y., Tough D.F., Le Bon A. Shaping of adaptive immune responses to soluble proteins by TLR agonists: a role for IFN-alpha/beta. Immunol Cell Biol 2004, 82(December (6)):596-602.
38. Johnston D., Zaidi B., Bystryn J.C. TLR7 imidazoquinoline ligand 3M-019 is a potent adjuvant for pure protein prototype vaccines. Cancer Immunol Immunother 2007, 56(August (8)):1133-1141.
39. Little S.F., Ivins B.E., Fellows P.F., Pitt M.L., Norris S.L., Andrews G.P. Defining a serological correlate of protection in rabbits for a recombinant anthrax vaccine. Vaccine 2004, 22(January (3/4)):422-430.
40. Marinaro M., Staats H.F., Hiroi T., Jackson R.J., Coste M., Boyaka P.N., et al. Mucosal adjuvant effect of cholera toxin in mice results from induction of T helper 2 (Th2) cells and IL-4. J Immunol 1995, 155(November (10)):4621-4629.
41. Yamamoto S., Kiyono H., Yamamoto M., Imaoka K., Yamamoto M., Fujihashi K., et al. A nontoxic mutant of cholera toxin elicits Th2-type responses for enhanced mucosal immunity. Proc Natl Acad Sci USA 1997, 94(10):5267-5272.
42. Fischer R., McGhee J.R., Vu H.L., Atkinson T.P., Jackson R.J., Tome D., et al. Oral and nasal sensitization promote distinct immune responses and lung reactivity in a mouse model of peanut allergy. Am J Pathol 2005, 167(Dec (6)):1621-1630.
43. Rynkiewicz D., Rathkopf M., Sim I., Waytes A.T., Hopkins R.J., Giri L., et al. Marked enhancement of the immune response to BioThrax(R) (anthrax vaccine adsorbed) by the TLR9 agonist CPG 7909 in healthy volunteers. Vaccine 2011, 29(August (37)):6313-6320.
44. Goldsmith P., Bunker C., Leslie T., Foreman J., Dowd P.M. The effect of topical steroid on the actions of vasoconstrictor and vasodilator peptides in human skin. Skin Pharmacol 1996, 9(5):289-297.
45. Couch R.B., Atmar R.L., Cate T.R., Quarles J.M., Keitel W.A., Arden N.H., et al. Contrasting effects of type I interferon as a mucosal adjuvant for influenza vaccine in mice and humans. Vaccine 2009, 27(August (39)):5344-5348.
46. Mansson A., Bachar O., Adner M., Cardell L.O. Nasal CpG oligodeoxynucleotide administration induces a local inflammatory response in nonallergic individuals. Allergy 2009, 64(September (9)):1292-1300.
47. Virtala R., Ekman A.K., Jansson L., Westin U., Cardell L.O. Airway inflammation evaluated in a human nasal lipopolysaccharide challenge model by investigating the effect of a CXCR2 inhibitor. Clin Exp Allergy Apr;42(4): 2012, 590-596.
48. Morse M.A., Chapman R., Powderly J., Blackwell K., Keler T., Green J., 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 Jul 15;17(14): 2011, 4844-4853.