Cholera toxin suppresses interleukin (IL)-12 production and IL-12 receptor β1 and β2 chain expression

Journal of Experimental Medicine

Volumn 189, Issue 3, 1999, Pages 541-552

  Braun, Michael C ^a   He, Jianping ^a   Wu, Chang You ^a   Kelsall, Brian L ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Cholera toxin; Dendritic cells; Interleukin 12; Monocytes; Th1 and Th2 cells

Indexed keywords

CHOLERA TOXIN; GAMMA INTERFERON; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12 RECEPTOR; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; PROSTAGLANDIN E2; PROTEIN SUBUNIT; RECEPTOR SUBUNIT; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; AUTOCRINE EFFECT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DENDRITIC CELL; DRUG MECHANISM; HELPER CELL; HUMAN; HUMAN CELL; MITOSIS INHIBITION; MOLECULAR DYNAMICS; MONONUCLEAR CELL; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; TRANSCRIPTION REGULATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS, CD3; CHOLERA TOXIN; DENDRITIC CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; HUMANS; INTERFERON TYPE II; INTERLEUKIN-12; LIPOPOLYSACCHARIDES; MICE; MONOCYTES; MUCOUS MEMBRANE; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-12; RNA, MESSENGER; TH1 CELLS; TH2 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 0033081332     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.3.541     Document Type: Article

References (89)

1. Strober, W., B. Kelsall, and T. Marth. 1998. Oral tolerance. J. Clin. Immunol. 18:1-30.
2. Weiner, H.L. 1997. Oral tolerance: immune mechanisms and treatment of autoimmune diseases. Immunol. Today. 18:335-343.
3. Reese, R.T., and J.J. Cebra. 1975. Anti-dinitrophenyl antibody production in strain 13 guinea pigs fed or sensitized with dinitrochlorobenzene. J. Immunol. 114:863-871.
4. Husby, S., J. Mestecky, Z. Moldoveanu, S. Holland, and C.O. Elson. 1994. Oral tolerance in humans: T cell but not B cell tolerance after antigen feeding. J. Immunol. 152:4663-4670.
5. Elson, C.O. 1996. Cholera toxin as a mucosal adjuvant. In Mucosal Vaccines. Academic Press, San Diego. 59-72.
6. Snider, D.P. 1995. The mucosal adjuvant activities of ADP-ribosylating bacterial enterotoxins. Crit. Rev. Immunol. 15: 317-348.
7. Lycke, N. 1997. The mechanism of cholera toxin adjuvanticity. Res. Immunol. 148:504-520.
8. Spangler, B.D. 1992. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56:622-647.
9. Lycke, N., U. Karlsson, A. Sjolander, and K.E. Magnusson. 1991. The adjuvant action of cholera toxin is associated with an increased intestinal permeability for luminal antigens. Scand. J. Immunol. 33:691-698.
10. Bromander, A.K., M. Kjerrulf, J. Holmgren, and N. Lycke. 1993. Cholera toxin enhances alloantigen presentation by cultured intestinal epithelial cells. Scand. J. Immunol. 37:452-458.
11. Bromander, A., J. Holmgren, and N. Lycke. 1991. Cholera toxin stimulates IL-1 production and enhances antigen presentation by macrophages in vitro. J. Immunol. 146:2908-2914.
12. Cong, Y., C.T. Weaver, and C.O. Elson. 1997. The mucosal adjuvanticity of cholera toxin involves enhancement of co-stimulatory activity by selective up-regulation of B7.2 expression. J. Immunol. 159:5301-5308.
13. Lycke, N., and W. Strober. 1989. Cholera toxin promotes B cell isotype differentiation. J. Immunol. 142:3781-3787.
14. Kim, P., L. Eckman, W.J. Lee, W. Han, and M.F. Kagnoff. 1998. Cholera toxin and cholera toxin B subunit induce IgA switching through the action of TGF-β1. J. Immunol. 160: 1198-1203.
15. Xu-Amano, J., H. Kioyno, R.L. Jackson, H.F. Staats, K. Fujihashi, P.D. Burrows, C.O. Elson, S. Pillai, and J.R. McGhee. 1993. Helper T cell subsets for immunoglobulin A responses: oral immunization with tetanus toxoid and cholera toxin as adjuvant selectively induces Th2 cells in mucosa-associated tissues. J. Exp. Med. 178:1309-1320.
16. Yamamoto, S., H. Kiyono, M. Yamamoto, K. Imaoka, K. Fujihashi, F.W. Van Ginkel, M. Noda, Y. Takeda, and J.R. McGhee. 1997. A nontoxic mutant of cholera toxin elicits TH2-type responses for enhanced mucosal immunity. Proc. Natl. Acad. Sci. USA. 94:5267-5272.
17. Marinaro, M., H.F. Staats, T. Hiroi, R.J. Jackson, M. Coste, P.N. Boyaka, N. Okahashi, M. Yamamoto, H. Kiyono, H. Bluethmann, et al. 1995. Mucosal adjuvant effect of cholera toxin in mice results from induction of T helper 2 (Th2) cells and IL-4. J. Immunol. 155:4621-4629.
18. Marinaro, M., P.N. Boyaka, F.D. Finkelman, H. Kiyono, R.J. Jackson, E. Jirillo, and J.R. McGhee. 1997. Oral but not parenteral interleukin (IL)-12 redirects T helper 2 (Th2)-type responses to an oral vaccine without altering mucosal IgA responses. J. Exp. Med. 185:415-427.
19. Kjerrulf, M., D. Grdic, L. Ekman, K. Schon, M. Vajdy, and N.Y. Lycke. 1997. Interferon-γ receptor-deficient mice exhibit impaired gut mucosal immune responses but intact oral tolerance. Immunology. 92:60-68.
20. Snider, D.P., J.S. Marshall, M.H. Perdue, and H. Liang. 1994. Production of IgE antibody and allergic sensitization of intestinal and peripheral-tissues after oral immunization with protein Ag and cholera-toxin. J. Immunol. 153:647-657.
21. Vajdy, M., M.H. Kosco-Vilbois, M. Kopf, G. Kohler, and N. Lycke. 1995. Impaired mucosal immune responses in interleukin 4-targeted mice. J. Exp. Med. 181:41-53.
22. Okahashi, N., M. Yamamoto, J.L. Vancott, S.N. Chatfield, M. Roberts, H. Bluethmann, T. Hiroi, H. Kiyono, and J.R. McGhee. 1996. Oral immunization of interleukin-4 (IL-4) knockout mice with a recombinant Salmonella strain or cholera toxin reveals that CD4(+) Th2 cells producing IL-6 and IL-10 are associated with mucosal immunoglobulin A responses. Infect. Immun. 64:1516-1525.
23. Tamura, S., Y. Shoji, K. Hasiguchi, C. Aizawa, and T. Kurata. 1994. Effects of cholera-toxin adjuvant on IgE antibody-response to orally or nasally administered ovalbumin. Vaccine. 12:1238-1240.
24. Kjerrulf, M., D. Grdic, M. Kopf, and N. Lycke. 1998. Induction of gut mucosal immune responses: importance of genetic background and Th1/Th2 cross-regulation. Scand. J. Immunol. 47:401-407.
25. Trinchieri, G. 1998. Proinflammatory and immunoregulatory functions of interleukin-12. Int. Rev. Immunol. 16:365-396.
26. Trinchieri, G. 1998. Immunobiology of interleukin-12. Immunol. Res. 17:269-278.
27. Bender, A., M. Sapp, G. Schuler, R.M. Steinman, and N. Bhardwaj. 1996. Improved methods for the generation of dendritic cells from nonproliferating progenitors in human blood. J. Immunol. Methods. 196:121-135.
28. Fotino, M., E.J. Merson, and F.H. Allen. 1971. Instant lymphocytes. Vox Sang. 21:469-470.
29. Rogge, L., D. D'Ambrosio, M. Biffi, G. Penna, L.J. Minetti, D.H. Presky, L. Adorini, and F. Sinigaglia. 1998. The role of Stat4 in species-specific regulation of T helper cell development by type 1 interferons. J. Immunol. 161:6567-6574.
30. Steinman, R.M., M. Pack, and K. Inaba. 1997. Dendritic cells in the T-cell areas of lymphoid organs. Immunol. Rev. 156:25-37.
31. Banchereau, J., and R.M. Steinman. 1998. Dendritic cells and the control of immunity. Nature. 392:245-252.
32. Moller, D.R., M. Wysocka, B.M. Greenlee, X. Ma, L. Wahl, D.A. Flockhart, G. Trinchieri, and C.L. Karp. 1997. Inhibition of IL-12 production by thalidomide. J. Immunol. 159:5157-5161.
33. Moller, D.R., M. Wysocka, B.M. Greenlee, X. Ma, L. Wahl, G. Trinchieri, and C.L. Karp. 1997. Inhibition of human interleukin-12 production by pentoxifylline. Immunology. 91:197-203.
34. Marth, T., and B.L. Kelsall. 1997. Regulation of interleukin-12 by complement receptor 3 signaling. J. Exp. Med. 185: 1987-1995.
35. Karp, C.L., M. Wysocka, L.M. Wahl, J.M. Ahearn, P.J. Cuomo, B. Sherry, G. Trinchieri, and D.E. Griffin. 1996. Mechanism of suppression of cell-mediated immunity by measles virus. Science. 273:228-231. (Published erratum appears 275:1053.)
36. Sutterwala, F.S., G.J. Noel, R. Clynes, and D.M. Messer. 1997. Selective suppression of interleukin-12 induction after macrophage receptor ligation. J. Exp. Med. 185:1977-1985.
37. 2 is a potent inhibitor of human interleukin 12 production. J. Exp. Med. 181:775-779.
38. 2-agonists prevent Th1 development by selective inhibition of interleukin 12. J. Clin. Invest. 100:1513-1519.
39. Ma, X., J.M. Chow, G. Gri, G. Carra, F. Gerosa, S.F. Wolf, R. Dzialo, and G. Trinchieri. 1996. The interleukin 12 p40 gene promoter is primed by interferon γ in monocytic cells. J. Exp. Med. 183:147-157.
40. Aste-Amezaga, M., X. Ma, A. Sartori, and G. Trinchieri. 1998. Molecular mechanisms of the induction of IL-12 and its inhibition by IL-10. J. Immunol. 160:5936-5944.
41. Heinzel, F.P., R.M. Rerko, P. Ling, J. Hakimi, and D.S. Schoenhaut. 1994. Interleukin 12 is produced in vivo during endotoxemia and stimulates synthesis of gamma interferon. Inject. Immun. 62:4244-4249.
42. Wysocka, M., M. Kubin, L.Q. Vieira, L. Ozmen, G. Garotta, P. Scott, and G. Trinchieri. 1995. Interleukin-12 is required for interferon-gamma production and lethality in lipopolysaccharide-induced shock in mice. Eur. J. Immunol. 25:672-676.
43. Heinzel, P.P., A.M. Hujer, F.N. Ahmed, and R.M. Rerko. 1997. In vivo production and function of IL-12 p40 homodimers. J. Immunol. 158:4381-4388.
44. Heinzel, F.P., R.M. Rerko, F. Ahmed, and A.M. Hujer. 1996. IFN-γ-independent production of IL-12 during murine endotoxemia. J. Immunol. 157:4521-4528.
45. Mattner, F., L. Ozmen, F.J. Podlaski, V.L. Wilkinson, D.H. Presky, M.K. Gately, and G. Alber. 1997. Treatment with homodimeric interleukin-12 (IL-12) p40 protects mice from IL-12 dependent but not from tumor necrosis factor alpha-dependent shock. Infect. Immun. 65:4734-1737.
46. Roberts, M., A. Bacon, R. Rappuoli, M. Pizza, I. Cropley, G. Douce, G. Dougan, M. Marinaro, J. McGhee, and S. Chatfield. 1995. A mutant pertussis toxin molecule that lacks ADP-ribosyltransferase activity, PT-9K/129G, is an effective mucosal adjuvant for intranasally delivered proteins. Infect. Immun. 63:2100-2108.
47. Hornquist, E., and N. Lycke. 1993. Cholera toxin adjuvant greatly promotes antigen priming of T cells. Eur. J. Immunol. 23:2136-2143.
48. Sutterwala, F.S., G.J. Noel, P. Salgame, and D.M. Mosser. 1998. Reversal of proinflammatory responses by ligating the macrophage Fc gamma receptor type 1. J. Exp. Med. 188: 217-222.
49. Imboden, J.B., D.M. Shoback, G. Pattison, and J.D. Stobo. 1986. Cholera toxin inhibits the T-cell antigen receptor-mediated increases in inositol trisphosphate and cytoplasmic free calcium. Proc. Natl. Acad. Sci. USA. 83:5673-5677.
50. Krakauer, T. 1996. Evidence for protein kinase C pathway in the response of human peripheral blood mononuclear cells to cholera toxin. Cell. Immunol. 72:224-228.
51. Neurath, M.F., I. Fuss, B.L. Kelsall, E. Stuber, and W. Strober. 1995. Antibodies to interleukin 12 abrogate established experimental colitis in mice. J. Exp. Med. 182:1281-1290.
52. Anderson, D.L., and C.D. Tsoukas. 1989. Cholera toxin inhibits resting human T cell activation via a cAMP-independent pathway. J. Immunol. 143:3647-3652.
53. Lycke, N., A.K. Bromander, L. Ekman, U. Karlsson, and J. Holmgren. 1989. Cellular basis of immunomodulation by cholera toxin in vitro with possible association to the adjuvant function in vivo. J. Immunol. 142:20-27.
54. Woogen, S.D., W. Ealding, and C.O. Elson. 1987. Inhibition of murine lymphocyte proliferation by the B subunit of cholera toxin. J. Immunol. 139:3764-3770.
55. Munoz, E., A.M. Zubiaga, M. Merrow, N.P. Sauter, and B.T. Huber. 1990. Cholera toxin discriminates between T helper 1 and T helper 2 cells in T cell receptor mediated activation: role of cAMP in T cell proliferation. J. Exp. Med. 172:95-103.
56. Woogen, S.D., K. Turo, L.A. Dieleman, K.W. Beagley, and C.O. Elson. 1993. Inhibition of murine T cell activation by cholera toxin B subunit is not mediated through the phosphatidylinositol second messenger system. J. Immunol. 150: 3274-3283.
57. Elson, C.O., S.P. Holland, M.T. Dertzbaugh, C.F. Cuff, and A.O. Anderson. 1995. Morphologic and functional alterations of mucosal T cells by cholera toxin and its B subunit. J. Immunol. 154:1032-1040.
58. Lacour, M., J.F. Arnghi, K.M. Muller, C. Carlberg, J.H. Saurat, and C. Hauser. 1994. cAMP up-regulates IL-4 and IL-5 production from activated CD4+ T cells while decreasing IL-2 release and NF-AT induction. Int. Immunol. 6:1333-1343.
59. Murphy, E., K. Shibuya, N. Hosken, P. Openshaw, V. Maino, K. Davis, K. Murphy, and A. O'Garra. 1996. Reversibility of T helper 1 and 2 populations is lost after long-term stimulation. J. Exp. Med. 183:901-913.
60. + T cells, analyzed at the single-cell level. J. Exp. Med. 184:473-483.
61. Szabo, S.J., N.G. Jacobson, A.S. Dighe, U. Gubler, and K.M. Murphy. 1995. Developmental commitment to the Th2 lineage by extinction of IL-12 signaling. Immunity. 2:665-675.
62. Belyakov, I.M., M.A. Derby, J.D. Ahlers, B.L. Kelsall, P. Earl, B. Moss, W. Strober, and J.A. Berzofsky. 1998. Mucosal immunization with HIV-1 peptide vaccine induces mucosal and systemic cytotoxic T lymphocytes and protective immunity in mice against intrarectal recombinant HIV-vaccinia challenge. Proc. Natl. Acad. Sci. USA. 95:1709-1714.
63. Porgador, A., H.F. Staats, B. Faiola, E. Gilboa, and T.J. Palker. 1997. Intranasal immunization with CTL epitope peptides from HIV-1 or ovalbumin and the mucosal adjuvant cholera toxin induces peptide-specific CTLs and protection against tumor development in vivo. J. Immunol. 158:834-841.
64. Bowen, J.C., S.K. Nair, R. Reddy, and B.T. Rouse. 1994. Cholera toxin acts as a potent adjuvant for the induction of cytotoxic T-lymphocyte responses with non-replicating antigens. Immunology. 81:338-342.
65. Trinchieri, G. 1994. Interleukin-12: a cytokine produced by antigen-presenting cells with immunoregulatory functions in the generation of T-helper cells type 1 and cytotoxic lymphocytes. Blood. 84:4008-4027.
66. Piccotti, J.R., K. Li, S.Y. Chan, J. Ferrante, J. Magram, E.J. Eichwald, and K.D. Bishop. 1998. Alloantigen-reactive Th1 development in IL-12-deficient mice. J. Immunol. 160:1132-1138.
67. Magram, J., J. Sfarra, S. Connaughton, D. Faherty, R. Warrier, D. Carvajal, C.Y. Wu, C. Stewart, U. Sarmiento, and M.K. Gately. 1996. IL-12-deficient mice are defective but not devoid of type 1 cytokine responses. Ann. NY Acad. Sci. 795:60-70.
68. Magram, J., S. Connaughton, R. Warrier, D. Carvajal, C.Y. Wu, J. Ferrante, C. Stewart, U. Sarmiento, D. Faherty, and M.K. Gately. 1996. IL-12-deficient mice are defective in IFN-γ production and type 1 cytokine responses. Immunity. 4:471-481.
69. Matousek, M.P., J.G. Nedrud, and C.V. Harding. 1996. Distinct effects of recombinant cholera toxin B subunit and holotoxin on different stages of class II MHC antigen processing and presentation by macrophages. J. Immunol. 156:4137-4145.
70. Matousek, M.P., J.G. Nedrud, W.J. Cieplak, and C.V. Harding. 1998. Inhibition of class II major histocompatibility complex antigen processing by Escherichia coli heat-labile enterotoxin requires an enzymatically active A subunit. Infect. Immun. 66:3480-3484.
71. Takahashi, I., M. Marinaro, H. Kiyono, R.J. Jackson, I. Nakagawa, K. Fujihashi, S. Hamada, J.D. Clements, K.L. Bost, and J.R. McGhee. 1996. Mechanisms for mucosal immunogenicity and adjuvancy of Escherichia coli labile enterotoxin. J. Infect. Dis. 173:627-635.
72. Holmgren, J., M. Lindblad, P. Fredman, L. Svennerholm, and H. Myrvold. 1985. Comparison of receptors for cholera and Escherichia coli enterotoxins in human intestine. Gastroenterology. 89:27-35.
73. Holmgren, J., P. Fredman, M. Lindblad, A.M. Svennerholm, and L. Svennerholm. 1982. Rabbit intestinal glycoprotein receptor for Escherichia coli heat-labile enterotoxin lacking affinity for cholera toxin. Infect. Immun. 38:424-433.
74. Griffiths, S.L., R.A. Finkelstein, and D.R. Critchley. 1986. Characterization of the receptor for cholera toxin and Escherichia coli heat-labile toxin in rabbit intestinal brush borders. Biochem. J. 238:313-322.
75. Coffman, R.L., D.A. Lebman, and B. Shrader. 1989. Transforming growth factor-β specifically enhances IgA production by lipopolysaccharide-stimulated murine B-lymphocytes. J. Exp. Med. 170:1039-1044.
76. MacIntyre, T., and W. Strober. 1999. Gut-associated lymphoid tissue: regulation of IgA B cell development. In Mucosal Immunology, Second Edition. P. Ogra, J. Mestecky, M. Lamm, W. Strober, J.R. McGhee, and J. Bienenstock, editors. Academic Press, San Diego. 319-356.
77. 1 positively regulates its own production. J. Immunol. 160:5719-5728.
78. Groux, H., A. O'Garra, M. Bigler, M. Rouleau, S. Antonenko, V.E. de Vries, and M.G. Roncarolo. 1997. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 389:737-742.
79. Marth, T., W. Strober, R.A. Seder, and B.L. Kelsall. 1997. Regulation of transforming growth factor-beta production by interleukin-12. Eur. J. Immunol. 27:1213-1220.
80. Marth, T., W. Strober, and B.L. Kelsall. 1996. High dose oral tolerance in ovalbumin TCR-transgenic mice: systemic neutralization of IL-12 augments TGF-beta secretion and T cell apoptosis. J. Immunol. 157:2348-2357.
81. Elson, C.O., S.P. Holland, M.T. Dertzbaugh, C.F. Cuff, and A.O. Anderson. 1995. Morphologic and functional alterations of mucosal T cells by cholera toxin and its B subunit. J. Immunol. 154:1032-1040.
82. Elson, C.O., and W. Ealding. 1984. Cholera toxin feeding did not induce oral tolerance in mice and abrogated oral tolerance to an unrelated protein antigen. J. Immunol. 133: 2892-2897.
83. Chen, Y., J. Inobe, V.K. Kuchroo, J.L. Baron, C.J. Janeway, and H.L. Weiner. 1996. Oral tolerance in myelin basic protein T-cell receptor transgenic mice: suppression of autoimmune encephalomyelitis and dose-dependent induction of regulatory cells. Proc. Natl. Acad. Sci. USA. 93:388-391.
84. Friedman, A., and H.L. Weiner. 1994. Induction of anergy or active suppression following oral tolerance is determined by antigen dosage. Proc. Natl. Acad. Sci. USA. 91:6688-6692.
85. Kay, R.A., and A. Ferguson. 1989. The immunological consequences of feeding cholera toxin. 1. Feeding cholera toxin suppresses the induction of systemic delayed-type hypersensitivity but not humoral immunity. Immunology. 66:410-415.
86. Kay, R.A., and A. Ferguson. 1989. The immunological consequences of feeding cholera toxin. II. Mechanisms responsible for the induction of oral tolerance for DTH. Immunology. 66:416-421.
87. Sun, J.B., J. Holmgren, and C. Czerkinsky. 1994. Choleratoxin B-subunit: an efficient transmucosal carrier-delivery system for induction of peripheral immunological tolerance. Proc. Natl. Acad. Sci. USA. 91:10795-10799.
88. Presky, D.H., L.J. Minetti, S. Gillessen, V.L. Wilkinson, C.Y. Wu, U. Gubler, R. Chizzonite, and M.K. Gately. 1998. Analysis of the multiple interactions between IL-12 and the high affinity IL-12 receptor complex. J. Immunol. 160:2174-2179.
89. Wu, C., J. Ferrante, M.K. Gately, and J. Magram. 1997. Characterization of IL-12 recetor beta1 chain (IL-12Rβ1)-deficient mice: IL-12Rβ1 is an essential component of the functional mouse IL-12 receptor. J. Immunol. 159:1658-1665.