Mucosal adjuvants based on cholera toxin and E. coli heat-labile enterotoxin

Immunopotentiators in Modern Vaccines

Volumn , Issue , 2006, Pages 235-252

  Holmgren, Jan ^a   Harandi, Ali M ^a   Lebens, Michael ^a   Sun, Jia Bin ^a   Anjuère, Fabienne ^c   Czerkinsky, Cecil ^b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b INSERM   (France)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

EID: 33748183505     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-012088403-2/50015-0     Document Type: Chapter

References (70)

1. Agren L.C., Ekman L., Lowenadler B., Nedrud J.H. Adjuvanticity of the cholera toxin A1-based gene fusion protein, CTA1-DD, is critically dependent on the ADP-ribosyltransferase and Ig-binding activity. J. Immunol. 1999, 162:2432-2440.
2. Anjuère F., Luci C., Lebens M., Rousseau D., Hervouet C., Milon G., Holmgren J., Ardavin C., Czerkinsky C. In vivo adjuvant-induced mobilization and maturation of gut dendritic cells after oral administration of cholera toxin. J Immunol. 2004, 173:5103-5111.
3. Arakawa T., Yu J., Chong D.K., Hough J., Engen P.C., Langridge W.H. A plant-based cholera toxin B subunit-insulin fusion protein protects against the development of autoimmune diabetes. Nature Biotechnol. 1998, 16:934-938.
4. Bäckström M., Shahabi V., Johansson S., Teneberg S., Kjellberg A., Miller-Podraza H., Holmgren J., Lebens M. Structural basis for differential receptor binding of cholera and Escherichia coli heat-labile toxins: influence of heterologous amino acid substitutions in the cholera B-subunit. Mol. Microbiol. 1997, 24:489-497.
5. Bergerot I., Ploix C., Petersen J., Moulin V., Rask C., Fabien N., Lindblad M., Mayer A., Czerkinsky C., Holmgren J., Thivolet C. A cholera toxoidinsulin conjugate as an oral vaccine against spontaneous autoimmune diabetes. Proc. Natl. Acad. Sci. USA 1997, 94:4610-4614.
6. Bergquist C., Johansson E-L., Lagergrd T., Holmgren J., Rudin A. Intranasal vaccination of humans with recombinant cholera toxin B subunit induces systemic and local antibody responses in the upper respiratory tract and the vagina. Infect. Immun. 1997, 65:2676-2684.
7. Boirivant M., Fuss U., Ferroni L., De Pascale M., Strober W. Oral administration of recombinant cholera toxin subunit B inhibits IL-12-mediated murine experimental (trinitrobenzene sulfonic acid) colitis. J. Immunol. 2001, 166:3522-3532.
8. Bregenholt S., Wang M., Wolfe T., Hughes A., Baerentzen L., Dyrberg T., von Herrath M.G., Petersen J.S. The cholera toxin B subunit is a mucosal adjuvant for oral tolerance induction in type 1 diabetes. Scand. J. Immunol. 2003, 57:432-438.
9. Chaillous L., Lefevre H., Thivolet C., Boitard C., Lahlou N., Atlan G., Bouhanick B., Mogenet A., Nicolino M., Carel J.C., Lecomte P., Marecha R., Bougneres P., Charbonnel B., Sai P. Oral insulin administration and residual beta-cell function in recent-onset type 1 diabetes: a multicentre randomised controlled trial. Lancet 2000, 12:545-549.
10. Clemens J., Sack D.A., Harris J.R., Atkinson W., Chakraborty J., Khan M.R., Stanton B.F., Kay B.A., Khan M.U., Yunus M.D., Svennerholm A.-M., Holmgren J. Field trial of oral cholera vaccines in Bangladesh. Lancet 1986, 1:124-127.
11. Clemens J.D., Sack D.A., Harris J.R., Chakraborty J., Khan M.R., Stanton B.F., Ali M., Ahmed F., Yunus M., Kay B.A., Khan M.U., Rao M.R., Svennerholm A.-M., Holmgren J. Impact of B subunit killed whole-cell and killed whole-cell-only oral vaccines against cholera upon treated diarrhoeal illness and mortality in an area endemic for cholera. Lancet 1988, I:1375-1379.
12. Clemens J.D., Sack D.A., Harris J.R., Chakraborty J., Neogy P.K., Stanton B., Huda N., Khan M.U., Kay B.A., Khan M.R., Ansaruzzaman M., Yunus M., Rao M.R., Svennerholm A.-M., Holmgren J. Cross-protection by B subunit-whole cell cholera vaccine against diarrhea associated with heat-labile toxin-producing enterotoxigenic Escherichia coli: results of a large-scale field trial. J. Infect. Dis. 1988, 158:372-377.
13. Clemens J.D., Sack D.A., Harris J.R., Van Loon F., Chakraborty J., Ahmed F., Rao M.R., Khan M.R., Yunus M.D., Huda N., Stanton B.F., Kay B.A., Walter S., Eeckels R., Svennerholm A.-M., Holmgren J. Field trial of oral cholera vaccines in Bangladesh: results from three-year follow-up. Lancet 1990, i:270-273.
14. Couch R.B. Nasal vaccination, Escherichia coli enterotoxin, and Bell's palsy. N. Engl. J. Med. 2004, 350:860-861.
15. De Fijter J.W., Eijgenraam J.W., Braam C.A., Holmgren J., Daha M.R., van Es L.A., van den Wall Blake A.W.L. Deficient IgA1 immune response to nasal cholera toxin subunit B in primary IgA nephropathy. Kidney Int. 1996, 50:952-961.
16. De Haan L., Hirst T.R. Cholera toxin and related enterotoxins: a cell biological and immunological perspective. J. Nat. Toxins 2003, 9:281-297.
17. Di Rienzo V., Marcucci F., Puccinelli P., Parmiani S., Frati F., Sensi L., Canonica G.W., Passalacqua G. Long-lasting effect of sublingual immunotherapy in children with asthma due to house dust mite: a 10-year prospective study. Clin. Exp. Allergy 2003, 33:206-210.
18. Di Tommaso A., Saletti G., Pizza M., Rappuoli R., Dougan G., Abrignani S., Douce G., de Magistris M.T. Induction of antigen specific antibodies in vaginal secretions by using a nontoxic mutant of heatlabile enterotoxin as a mucosal adjuvant. Infect. Immun. 1996, 64:974-979.
19. Dickinson B.L., Clements J.H. Dissociation of Escherichia coli heat-labile enterotoxin adjuvanticity from ADP-ribosyltransferase activity. Infect. Immun. 1995, 63:1617-1623.
20. Dotevall H., Jonson-Strömberg G., Sanyal S., Holmgren J. Characterization of enterotoxin and soluble hemagglutinin from Vibrio mimicus: identity with V. cholerae O1 toxin and hemagglutinin. FEMS Microbiol. Lett. 1985, 27:17-22.
21. Elson C.O., Ealding W. Cholera toxin feeding did not induce oral tolerance in mice and abrogated oral tolerance to an unrelated protein antigen. J. Immunol. 1984, 133:2892-2897.
22. Eriksson K., Fredriksson M., Nordström I., Holmgren J. Cholera toxin and its B subunit promote dendritic cell vaccination with different influence on Th1/Th2 development. Infect. Immun. 2003, 71:1740-1747.
23. Eriksson K., Sun J.B., Nordström I., Fredriksson M., Lindblad M., Li B.L., Holmgren J. Coupling of antigen to cholera toxin for dendritic cell vaccination promotes the induction of MHC class I-restricted cytotoxic T cells and the rejection of a cognate antigen-expressing model tumour. Eur. J. Immunol. 2004, 34:1272-1281.
24. Fujihashi K., Koga T., van Ginkel F.W., Hagiwara Y., McGhee J.R. A dilemma for mucosal vaccination: efficacy versus toxicity using enterotoxin-based adjuvants. Vaccine 2002, 20:2431-2438.
25. Gagliardi M., Sallusto F., Marinaro M., Vendetti S., Riccomi A., De Magistris M. Effects of the adjuvant cholera toxin on dendritic cells: stimulatory and inhibitory signals that result in the amplification of immune responses. Ing. J. Med. Microbiol. 2002, 291:571-575.
26. George-Chandy A., Eriksson K., Lebens M., Nordstrom I., Schön E., Holmgren J. Cholera toxin B subunit as a carrier molecule promotes antigen presentation and increases CD40 and CD86 expression on antigen-presenting cells. Infect. Immun. 2001, 69:5716-5725.
27. Guiliano M.M., Del Giudice G., Giannelli V., Dougan G., Douce G., Rappuoli R., Pizza M. Mucosal adjuvanticity and immunogenicity of LTR72, a novel mutant of Escherichia coli heat-labile enterotoxin with partial knockout of ADP-ribosyltransferase activity. J. Exp. Med. 1998, 187:1123-1132.
28. Harandi A.M., Holmgren J. CpG DNA as a potent inducer of mucosal immunity: implications for immunoprophylaxis and immunotherapy of mucosal infections. Curr. Opin. Invest. Drugs 2004, 5:141-145.
29. Harandi A.M., Eriksson K., Holmgren J. A protective role of locally administered immunostimulatory CpG oligodeoxynucleotide in a mouse model of genital herpes infection. J. Virol. 2003, 77:953-962.
30. Holmgren J. Actions of cholera toxin and the prevention and treatment of cholera. Nature 1981, 292:413-417.
31. Holmgren J., Bergquist C. Oral B subunit killed whole-cell cholera vaccines. New Generation Vaccines 2004, 499-510. Marcel Decker, New York. 3rd edn. M.M. Levine (Ed.).
32. Holmgren J., Czerkinsky C. Mucosal immunity and vaccines. Nature Med. 2005, 11(Suppl. 4):S45-S53.
33. Holmgren J., Fredman P., Lindblad M., Svennerholm A.-M., Svennerholm L. Rabbit intestinal glycoprotein receptor for Escherichia coli heat-labile enterotoxin lacking affinity for cholera toxin. Infect. Immun. 1982, 38:424-433.
34. Holmgren J., Lycke N., Czerkinsky C. Cholera toxin and cholera B subunit as oral-mucosal adjuvant and antigen vector system. Vaccine 1993, 11:1179-1184.
35. Johansson E.-L., Wassén L., Holmgren J., Jertborn M., Rudin A. Nasal and vaginal vaccinations have differential effects on antibody responses in vaginal and cervical secretions in humans. Infect. Immun. 2001, 69:7481-7486.
36. Lencer W.I., Tsai B. The intracellular voyage of cholera toxin: going retro. Trends Biochem. Sci. 2003, 12:639-645.
37. Li B.-L., Sun J.-B., Holmgren J. Adoptive transfer of mucosal T cells or dendritic cells from animals fed with cholera toxin B subunit alloantigen conjugate induces allogeneic T cell tolerance. Adv. Exp. Med. Biol. 2001, 495:271-275.
38. Lu X., Clements J.D., Katz J.M. Mutant Escherichia coli heat-labile enterotoxin [LT(R192G)], enhances protective humoral and cellular immune responses to orally administered inactivated influenza vaccine. Vaccine 2002, 20:1019-1029.
39. Lucas M., et al. High-level effectiveness of a mass oral cholera vaccination in Beira, Mozambique. N. Engl. J. Med. 2005, 352:757-767.
40. Luross J.A., Heaton T., Hirst T.R., Day M.J., Williams N.A. Escherichia coli heat-labile enterotoxin B subunit prevents autoimmune arthritis through induction of regulatory CD4+ T cells. Arthritis Rheum. 2002, 46:1671-1682.
41. Lycke N. The mechanism of cholera toxin adjuvanticity. Res. Immunol. 1997, 148:504-520.
42. Lycke N., Holmgren J. Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens. Immunology 1986, 59:301-308.
43. Ma D., Mellon J., Niederkorn J. Conditions affecting enhanced corneal allograft survival by oral immunization. Invest. Ophthalmol. Vis. Sci. 1998, 39:1835-1846.
44. Marchetti M., Rossi M., Giannelli V., Giuliani M.M., Pizza M., Censini S., Covacci A., Massari P., Pagliaccia C., Manetti R., Telford J.L., Douce G., Dougan G., Rappuoli R., Ghiara P. Protection against Helicobacter pylori infection in mice by intragastric vaccination with H. pylori antigens is achieved using a non-toxic mutant of E. coli heat-labile enterotoxin (LT) as adjuvant. Vaccine 1998, 16:33-37.
45. Mastrandrea F. The potential role of allergen-specific sublingual immunotherapy in atopic dermatitis. Am. J. Clin. Dermatol. 2004, 5:281-294.
46. Mowat A.M., Donachie A.M., Jagewall S., Schön K., Lowenadler B., Dalström K., Kaastrup P., Lycke N. CTA1-DD-immune stimulating complexes: a novel, rationally designed combined mucosal vaccine adjuvant effective with nanogram doses of antigen. J. Immunol. 2001, 167:3398-3405.
47. NIAID Conference. Safety evaluation of toxin adjuvants delivered intranasally 2001, http://www.niaid.nih.gov/dmid/enteric/intranasal.htm.
48. Phipps P.A., Stanford M.R., Sun J.-B., Xiao B.G., Holmgren J., Shinnic T., Hasa A., Mizushima Y., Lehner T. Prevention of mucosally induced uveitis with a HSP60-derived peptide linked to cholera toxin B subunit. Eur. J. Immunol. 2003, 33:224-232.
49. Pizza M., Giuliani M., Fontana M., Monaci E., Douce G., Dougan G., Mills K.H., Rappuoli R., Del Giudice G. Mucosal vaccines: non toxic derivatives of LT and CT as mucosal adjuvants. Vaccine 2001, 19:2534-2541.
50. Plant A., Williams N.A. Modulation of the immune response by the cholera-like enterotoxins. Curr. Top. Med. Chem. 2004, 4:509-519.
51. Postlethwaite A.E. Can we induce tolerance in rheumatoid arthritis?. Curr. Rheumatol. Rep. 2001, 3:64-69.
52. Rask C., Holmgren J., Fredriksson M., Lindblad M., Nordström I., Sun J.-B., Czerkinsky C. Prolonged oral treatment with low doses of allergen conjugated to cholera toxin B subunit suppresses immunoglobulin E antibody responses in sensitized mice. Clin. Exp. Allergy 2000, 30:1024-1032.
53. Rudin A., Johansson E.-L., Bergquist C., Holmgren J. Differential kinetics and distribution of antibodies in serum and nasal and vaginal secretions after nasal and oral vaccination in humans. Infect. Immun. 1998, 66:3390-3396.
54. Rudin A., Riise G.C., Holmgren J. Antibody responses in the lower respiratory tract and male urogenital tract in humans after nasal and oral vaccination with cholera toxin B subunit. Infect. Immun. 1999, 67:2884-2890.
55. Sack D.A., Sack B.R., Nair G.B., Siddique A.K. Cholera. Lancet 2004, 363:223-233.
56. Sanchez J., Wallerstrom G., Fredriksson M., Angstrom J., Holmgren J. Detoxification of cholera toxin without removal of its immunoadjuvanticity by the addition of (STa-related) peptides to the catalytic subunit. A potential new strategy to generate immunostimulants for vaccination. J. Biol. Chem. 2002, 277:33369-33377.
57. Staats H.F., Ennis F.A. IL-1 is an effective adjuvant for mucosal and systemic immune responses when co-administered with protein immunogens. J. Immunol. 1999, 162:6141-6147.
58. Stanford M., Whittall T., Bergmeier L.A., Lindblad M., Lundin S., Shinnick T., Mizushima Y., Holmgren J., Lehner T. Oral tolerization with peptide 336-351 linked to cholera toxin B subunit in preventing relapses of uveitis in Behcet's disease. Clin. Exp. Immunol. 2004, 137:201-208.
59. Stephenson I., Nicholson K.G., Rudin A., Colegate A., Podda A., Bugarini R., del Giudice G., Minutello A., Bonnington S., Holmgren J., Mills K.H.G., Zambon M.C. Trivalent nasal inactivated influenza vaccine with non-toxigenic Escherichia coli enterotoxin and novel biovector as mucosal adjuvants: a randomised phase I trial. Vaccine 2005, in press.
60. Sun J.-B., Holmgren J., Czerkinsky C. Cholera toxin B subunit: an efficient transmucosal carrier-delivery system for induction of peripheral immunological tolerance. Proc. Natl. Acad. Sci. USA 1994, 91:10795-10799.
61. Sun J.-B., Rask C., Olsson T., Holmgren J., Czerkinsky C. Treatment of experimental autoimmune encephalomyelitis by feeding myelin basic protein conjugated to cholera toxin B subunit. Proc. Natl. Acad. Sci. USA 1996, 93:7196-7201.
62. Sun J.-B., Li B.-L., Czerkinsky C., Holmgren J. Enhanced immunological tolerance against allograft rejection by oral administration of allogeneic antigen linked to cholera toxin B subunit. J. Clin. Immunol. 2000, 97:130-139.
63. Sun J.-B., Xiao B.-G., Lindblad M., Li B.-L., Link H., Czerkinsky C., Holmgren J. Oral administration of cholera toxin B subunit conjugated to myelin basic protein protects against experimental autoimmune encephalomyelitis by inducing transforming growth factor-b-secreting cells and suppressing chemokine expression. Int. Immunol. 2000, 12:1449-1457.
64. Sun J.-B., Eriksson K., Li B.-L., Lindblad M., Azem J., Holmgren J. Vaccination with dendritic cells pulsed in vitro with tumor antigen conjugated to cholera toxin efficiently induces specific tumoricidal CD8+ cytotoxic lymphocytes dependant on cyclic AMP activation of dendritic cells. Clin. Immunol. 2004, 112:35-44.
65. Svennerholm A.-M., Jertborn M., Gothefors L., Karim A.M.M.M., Sack D.A., Holmgren J. Mucosal antitoxic and antibacterial immunity after cholera disease and after immunization with a combined, B subunit-whole cell vaccine. J. Infect. Dis. 1984, 149:884-893.
66. Tamura S., Hatori E., Tsuruhara T., Aizawa C., Kurata T. Suppression of delayed-type hyper-sensitivity and IgE antibody responses to ovalbumin by intranasal administration of Escherichia coli heat-labile enterotoxin B subunit-conjugated ovalbumin. Vaccine 1997, 15:225-229.
67. Tarkowski A., Sun J.-B., Holmdahl R., Holmgren J., Czerkinsky C. Treatment of experimental autoimmune arthritis by nasal administration of a type II collagen-cholera toxoid conjugate vaccine. Arthritis Rheum 1999, 42:1628-1634.
68. Wiendl H., Hohlfeld R. Therapeutic approaches in multiple sclerosis: lessons from failed and interrupted treatment trials. BioDrugs 2002, 16:183-200.
69. Wilson D.R., Torres Lima M., Dirham S.R. Sublingual immunotherapy for allergic rhinitis: systematic review and meta-analysis. Allergy 2005, 60:4-12.
70. Wu H.Y., Weiner H.L. Oral tolerance. Immunol. Res. 2003, 28:265-284.