Effects of cholera toxin on innate and adaptive immunity and its application as an immunomodulatory agent

Journal of Leukocyte Biology

Volumn 75, Issue 5, 2004, Pages 756-763

  Lavelle, Ed C ^a   Jarnicki, Andrew ^a   McNeela, Edel ^a   Armstrong, Michelle E ^a   Higgins, Sarah C ^a   Leavy, Olive ^a   Mills, Kingston H G ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Dendritic cell; Innate immunity; Regulatory T cell; Th1 Th2 cell; Tolerance suppression anergy; Vaccination

Indexed keywords

CHOLERA TOXIN; GAMMA INTERFERON; IMMUNOMODULATING AGENT; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANTIGEN SPECIFICITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLULAR IMMUNITY; CONFERENCE PAPER; CYTOKINE PRODUCTION; DENDRITIC CELL; IMMUNITY; IMMUNIZATION; IMMUNOMODULATION; IMMUNOPHARMACOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TH1 CELL; TH2 CELL; VACCINATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; CHOLERA TOXIN; CYTOKINES; DENDRITIC CELLS; HUMANS; IMMUNITY; T-LYMPHOCYTES, HELPER-INDUCER;

ANIMALIA;

EID: 2342450639     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1103534     Document Type: Conference Paper

References (72)

1. Zhang, R. G., Scott, D. L., Westbrook, M. L., Nance, S., Spangler, B. D., Shipley, G. G., Westbrook, E. M. (1995) The three-dimensional crystal structure of cholera toxin. J. Mol. Biol. 251, 563-573.
2. Rappuoli, R., Pizza, M., Douce, G., Dougan, G. (1999) Structure and mucosal adjuvanticity of cholera and Escherichia coli heat-labile enterotoxins. Immunol. Today 20, 493-500.
3. Pizza, M., Giuliani, M. M., Fontana, M. R., Monaci, E., Douce, G., Dougan, G., Mills, K. H., Rappuoli, R., Del Giudice, G. (2001) Mucosal vaccines: nontoxic derivatives of LT and CT as mucosal adjuvants. Vaccine 19, 2534-2541.
4. Williams, N. A., Hirst, T. R., Nashar, T. O. (1999) Immune modulation by the cholera-like enterotoxins: from adjuvant to therapeutic. Immunol. Today 20, 95-101.
5. Holmgren, J., Lonnroth, I., Svennerholm, L. (1973) Tissue receptor for cholera exotoxin: postulated structure from studies with GM1 ganglioside and related glycolipids. Infect. Immun. 8, 208-214.
6. Spangler, B. D. (1992) Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56, 622-647.
7. Gill, D. M., Rappaport, R. S. (1979) Origin of the enzymatically active Al fragment of cholera toxin. J. Infect. Dis. 139, 674-680.
8. Kawamura, Y. I., Kawashima, R., Shirai, Y., Kato, R., Hamabata, T., Yamamoto, M., Furukawa, K., Fujihashi, K., McGhee, J. R., Hayashi, H., Dohi, T. (2003) Cholera toxin activates dendritic cells through dependence on GM1-ganglioside which is mediated by NF-κB translocation. Eur. J. Immunol. 33, 3205-3212.
9. Field, M., Rao, M. C., Chang, E. B. (1989) Intestinal electrolyte transport and diarrheal disease (2). N. Engl. J. Med 321, 879-883.
10. Pelham, H. R. (1992) The Florey Lecture, 1992. The secretion of proteins by cells. Proc. R. Soc. Lond. B. Biol. Sci. 250, 1-10.
11. Tsai, S. C., Noda, M., Adamik, R., Chang, P. P., Chen, H. C., Moss, J., Vaughan, M. (1988) Stimulation of choleragen enzymatic activities by GTP and two soluble proteins purified from bovine brain. J. Biol. Chem. 263, 1768-1772.
12. Lavelle, E. C., Grant, G., Pusztai, A., Pfuller, U., O'Hagan, D. T. (2000) Mucosal immunogenicity of plant lectins in mice. Immunology 99, 30-37.
13. + T cell responses. J. Immunol. 166, 1106-1113.
14. Simmons, C. P., Mastroeni, P., Fowler, R., Ghaem-maghami, M., Lycke, N., Pizza, M., Rappuoli, R., Dougan, G. (1999) MHC class I-restricted cytotoxic lymphocyte responses induced by enterotoxin-based mucosal adjuvants. J. Immunol. 163, 6502-6510.
15. Bowen, J. C., Nair, S. K., Reddy, R., Rouse, B. T. (1994) Cholera toxin acts as a potent adjuvant for the induction of cytotoxic T-lymphocyte responses with non-replicating antigens. Immunology 81, 338-342.
16. Simecka, J. W., Jackson, R. J., Kiyono, H., McGhee, J. R. (2000) Mucosally induced immunoglobulin E-associated inflammation in the respiratory tract. Infect. Immun. 68, 672-679.
17. Yamamoto, M., Rennert, P., McGhee, J. R., Kweon, M. N., Yamamoto, S., Dohi, T., Otake, S., Bluethmann, H., Fujihashi, K., Kiyono, H. (2000) Alternate mucosal immune system: organized Peyer's patches are not required for IgA responses in the gastrointestinal tract. J. Immunol. 164, 5184-5191.
18. Yamamoto, S., Kiyono, H., Yamamoto, M., Imaoka, K., Fujihashi, K., Van Ginkel, F. W., Noda, M., Takeda, Y., McGhee, J. R. (1997) A nontoxic mutant of cholera toxin elicits Th2-type responses for enhanced mucosal immunity. Proc. Natl. Acad. Sci. USA 94, 5267-5272.
19. Yamamoto, S., Takeda, Y., Yamamoto, M., Kurazono, H., Imaoka, K., Fujihashi, K., Noda, M., Kiyono, H., McGhee, J. R. (1997) Mutants in the ADP-ribosyltransferase cleft of cholera toxin lack diarrheagenicity but retain adjuvanticity. J. Exp. Med. 185, 1203-1210.
20. Clarke, C. J., Wilson, A. D., Williams, N. A., Stokes, C. R. (1991) Mucosal priming of T-lymphocyte responses to fed protein antigens using cholera toxin as an adjuvant. Immunology 72, 323-328.
21. Xu-Amano, J., Kiyono, H., Jackson, R. J., Staats, H. F., Fujihashi, K., Burrows, P. D., Elson, C. O., Pillai, S., McGhee, J. R. (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.
22. Marinaro, M., Staats, H. F., Hiroi, T., Jackson, R. J., Coste, M., Boyaka, P. N., Okahashi, N., Yamamoto, M., Kiyono, H., Bluethmann, H., 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.
23. Douce, G., Fontana, M., Pizza, M., Rappuoli, R., Dougan, G. (1997) Intranasal immunogenicity and adjuvanticity of site-directed mutant derivatives of cholera toxin. Infect. Immun. 65, 2821-2828.
24. Pierre, P., Denis, O., Bazin, H., Mbongolo Mbella, E., Vaerman, J. P. (1992) Modulation of oral tolerance to ovalbumin by cholera toxin and its B subunit. Eur. J. Immunol. 22, 3179-3182.
25. Glenn, G. M., Scharton-Kersten, T., Vassell, R., Mallett, C. P., Hale, T. L., Alving, C. R. (1998) Transcutaneous immunization with cholera toxin protects mice against lethal mucosal toxin challenge. J. Immunol. 161, 3211-3214.
26. Ruedl, C., Rieser, C., Kofler, N., Wick, G., Wolf, H. (1996) Humoral and cellular immune responses in the murine respiratory tract following oral immunization with cholera toxin or Escherichia coli heat-labile enterotoxin. Vaccine 14, 792-798.
27. Richards, C. M., Shimeld, C., Williams, N. A., Hill, T. J. (1998) Induction of mucosal immunity against herpes simplex virus type 1 in the mouse protects against ocular infection and establishment of latency. J. Infect. Dis. 177, 1451-1457.
28. Hornquist, E., Lycke, N. (1993) Cholera toxin adjuvant greatly promotes antigen priming of T cells. Eur. J. Immunol. 23, 2136-2143.
29. Pacheco, S. E., Gibbs, R. A., Ansari-Lari, A., Rogers, P. (2000) Intranasal immunization with HIV reverse transcriptase: effect of dose in the induction of helper T cell type 1 and 2 immunity. AIDS Res. Hum. Retroviruses 16, 2009-2017.
30. Schaffeler, M. P., Brokenshire, J. S., Snider, D. P. (1997) Detection of precursor Th cells in mesenteric lymph nodes after oral immunization with protein antigen and cholera toxin. Int. Immunol. 9, 1555-1562.
31. Yanagita, M., Hiroi, T., Kitagaki, N., Hamada, S., Ito, H. O., Shimauchi, H., Murakami, S., Okada, H., Kiyono, H. (1999) Nasopharyngeal-associated lymphoreticular tissue (NALT) immunity: fimbriae-specific Th1 and Th2 cell-regulated IgA responses for the inhibition of bacterial attachment to epithelial cells and subsequent inflammatory cytokine production. J. Immunol. 162, 3559-3565.
32. Lavelle, E. C., McNeela, E., Armstrong, M. E., Leavy, O., Higgins, S. C., Mills, K. H. (2003) Cholera toxin promotes the induction of regulatory T cells specific for bystander antigens by modulating dendritic cell activation. J. Immunol. 171, 2384-2392.
33. McGuirk, P., Mills, K. H. (2002) Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases. Trends Immunol. 23, 450-455.
34. Doetze, A., Satoguina, J., Burchard, G., Rau, T., Loliger, C., Fleischer, B., Hoerauf, A. (2000) Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by T(h)3/T(r)1-type cytokines IL-10 and transforming growth factor-β but not by a T(h)1 to T(h)2 shift. Int. Immunol. 12, 623-630.
35. Mendel, I., Shevach, E. M. (2002) The IL-10-producing competence of Th2 cells generated in vitro is IL-4 dependent. Eur. J. Immunol. 32, 3216-3224.
36. Phipps, P. A., Stanford, M. R., Sun, J. B., Xiao, B. G., Holmgren, J., Shinnick, T., Hasan, A., Mizushima, Y., Lehner, T. (2003) Prevention of mucosally induced uveitis with a HSP60-derived peptide linked to cholera toxin B subunit. Eur. J. Immunol. 33, 224-232.
37. Sun, J. B., Xiao, B. G., Lindblad, M., Li, B. L., Link, H., Czerkinsky, C., Holmgren, J. (2000) Oral administration of cholera toxin B subunit conjugated to myelin basic protein protects against experimental autoimmune encephalomyelitis by inducing transforming growth factor-β-secreting cells and suppressing chemokine expression. Int. Immunol. 12, 1449-1457.
38. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188, 287-296.
39. + regulatory T cells in vivo. J. Exp. Med. 198, 249-258.
40. + regulatory T cells by antigen-processing dendritic cells. J. Exp. Med. 198, 235-247.
41. Jonuleit, H., Schmitt, E., Steinbrink, K., Enk, A. H. (2001) Dendritic cells as a tool to induce anergic and regulatory T cells. Trends Immunol. 22, 394-400.
42. Rissoan, M. C., Soumelis, V., Kadowaki, N., Grouard, G., Briere, F., de Waal Malefyt, R., Liu, Y. J. (1999) Reciprocal control of T helper cell and dendritic cell differentiation. Science 283, 1183-1186.
43. Boonstra, A., Asselin-Paturel, C., Gilliet, M., Crain, C., Trinchieri, G., Liu, Y. J., O'Garra, A. (2003) Flexibility of mouse classical and plasma-cytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential Toll-like receptor ligation. J. Exp. Med. 197, 101-109.
44. de Jong, E. C., Vieira, P. L., Kalinski, P., Schuitemaker, J. H., Tanaka, Y., Wierenga, E. A., Yazdanbakhsh, M., Kapsenberg, M. L. (2002) Microbial compounds selectively induce Th1 cell-promoting or Th2 cell-promoting dendritic cells in vitro with diverse Th cell-polarizing signals. J. Immunol. 168, 1704-1709.
45. Gagliardi, M. C., Sallusto, F., Marinaro, M., Langenkamp, A., Lanzavecchia, A., De Magistris, M. T. (2000) Cholera toxin induces maturation of human dendritic cells and licences them for Th2 priming. Eur. J. Immunol. 30, 2394-2403.
46. MacDonald, A. S., Straw, A. D., Dalton, N. M., Pearce, E. J. (2002) Cutting edge: Th2 response induction by dendritic cells: a role for CD40. J. Immunol. 168, 537-540.
47. Lespagnard, L., Mettens, P., De Smedt, T., Bazin, H., Urbain, J., Leo, O., Moser, M. (1998) The immune response induced in vivo by dendritic cells is dependent on B7-1 or B7-2, but the inhibition of both signals does not lead to tolerance. Int. Immunol. 10, 295-304.
48. Martin, E., O'Sullivan, B., Low, P., Thomas, R. (2003) Antigen-specific suppression of a primed immune response by dendritic cells mediated by regulatory T cells secreting interleukin-10. Immunity 18, 155-167.
49. Fontana, S., Moratto, D., Mangal, S., De Francesco, M., Vermi, W., Ferrari, S., Facchetti, F., Kutukculer, N., Fiorini, C., Duse, M., Das, P. K., Notarangelo, L. D., Plebani, A., Badolato, R. (2003) Functional defects of dendritic cells in patients with CD40 deficiency. Blood 102, 4099-4106.
50. O'Garra, A. (1998) Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8, 275-283.
51. Murphy, K. M., Reiner, S. L. (2002) The lineage decisions of helper T cells. Nat. Rev. Immunol. 2, 933-944.
52. Iwasaki, A., Kelsall, B. L. (1999) Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J. Exp. Med. 190, 229-239.
53. + T cells. J. Exp. Med. 185, 461-469.
54. + dendritic cells to prime Th1/Th2 cells in vivo. J. Immunol. 167, 4345-4350.
55. Chen, Y., Kuchroo, V. K., Inobe, J., Hafler, D. A., Weiner, H. L. (1994) Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 265, 1237-1240.
56. + T cells: IL-4 and IFN-γ have opposing effects, while TGF-β positively regulates its own production. J. Immunol. 160, 5719-5728.
57. Cong, Y., Oliver, A. O., Elson, C. O. (2001) Effects of cholera toxin on macrophage production of co-stimulatory cytokines. Eur. J. Immunol. 31, 64-71.
58. Diehl, S., Rincon, M. (2002) The two faces of IL-6 on Th1/Th2 differentiation. Mol. Immunol. 39, 531-536.
59. Constant, S. L., Brogdon, J. L., Piggott, D. A., Herrick, C. A., Visintin, I., Ruddle, N. H., Bottomly, K. (2002) Resident lung antigen-presenting cells have the capacity to promote Th2 T cell differentiation in situ. J. Clin. Invest. 110, 1441-1448.
60. Nakae, S., Komiyama, Y., Yokoyama, H., Nambu, A., Umeda, M., Iwase, M., Homma, I., Sudo, K., Horai, R., Asano, M., Iwakura, Y. (2003) IL-1 is required for allergen-specific Th2 cell activation and the development of airway hypersensitivity response. Int. Immunol. 15, 483-490.
61. Braun, M. C., He, J., Wu, C. Y., Kelsall, B. L. (1999) Cholera toxin suppresses interleukin (IL)-12 production and IL-12 receptor β1 and β2 chain expression. J. Exp. Med. 189, 541-552.
62. Burkart, V., Kim, Y. E., Hartmann, B., Ghiea, I., Syldath, U., Kauer, M., Fingberg, W., Hanifi-Moghaddam, P., Muller, S., Kolb, H. (2002) Cholera toxin B pretreatment of macrophages and monocytes diminishes their proinflammatory responsiveness to lipopolysaccharide. J. Immunol. 168, 1730-1737.
63. Yura, M., Takahashi, I., Terawaki, S., Hiroi, T., Kweon, M. N., Yuki, Y., Kiyono, H. (2001) Nasal administration of cholera toxin (CT) suppresses clinical signs of experimental autoimmune encephalomyelitis (EAE). Vaccine 20, 134-139.
64. Gaupp, S., Hartung, H. P., Toyka, K., Jung, S. (1.997) Modulation of experimental autoimmune neuritis in Lewis rats by oral application of myelin antigens. J. Neuroimmunol. 79, 129-137.
65. Tsuru, S., Taniguchi, M., Shinomiya, N., Fujisawa, H., Zinnaka, Y., Nomoto, K. (1987) Cholera toxin-induced tolerance to allografts in mice. Immunology 61, 77-83.
66. Sun, J. B., Li, B. L., Czerkinsky, C., Holmgren, J. (2000) Enhanced immunological tolerance against allograft rejection by oral administration of allogeneic antigen linked to cholera toxin B subunit. Clin. Immunol. 97, 130-139.
67. Sun, J. B., Rask, C., Olsson, T., Holmgren, J., Czerkinsky, C. (1996) Treatment of experimental autoimmune encephalomyelitis by feeding myelin basic protein conjugated to cholera toxin B subunit. Proc. Natl. Acad. Sci. USA 93, 7196-7201.
68. Aspord, C., Czerkinsky, C., Durand, A., Stefanutti, A., Thivolet, C. (2002) α4 Integrins and L-selectin differently orchestrate T-cell activity during diabetes prevention following oral administration of CTB-insulin. J. Autoimmun. 19, 223-232.
69. Boirivant, M., Fuss, I. J., Ferroni, L., De Pascale, M., Strober, W. (2001) Oral administration of recombinant cholera toxin subunit B inhibits IL-12-mediated-murine experimental (trinitrobenzene sulfonic acid) colitis. J. Immunol. 166, 3522-3532.
70. Kim, N., Cheng, K. C., Kwon, S. S., Mora, R., Barbieri, M., Yoo, T. J. (2001) Oral administration of collagen conjugated with cholera toxin induces tolerance to type II collagen and suppresses chondritis in an animal model of autoimmune ear disease. Ann. Otol. Rhinol. Laryngol. 110, 646-654.
71. Bregenholt, S., Wang, M., Wolfe, T., Hughes, A., Baerentzen, L., Dyrberg, T., von Herrath, M. G., Petersen, J. S. (2003) The cholera toxin B subunit is a mucosal adjuvant for oral tolerance induction in type 1 diabetes. Scand. J. Immunol. 57, 432-438.
72. + T cells. Arthritis Rheum. 46, 1671-1682.