Pertussis toxin and the adenylate cyclase toxin from Bordetella pertussis activate human monocyte-derived dendritic cells and dominantly inhibit cytokine production through a cAMP-dependent pathway

Journal of Leukocyte Biology

Volumn 72, Issue 5, 2002, Pages 962-969

  Bagley, Kenneth C ^a,b   Abdelwahab, Sayed F ^a,b   Tuskan, Robert G ^a   Fouts, Timothy R ^a   Lewis, George K ^a,b,c  

^a INSTITUTE OF HUMAN VIROLOGY   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

Adjuvant; Cholera toxin; Enterotoxin

Indexed keywords

8 BROMO CYCLIC AMP; ADENYLATE CYCLASE; BACTERIAL TOXIN; CD4 ANTIGEN; CHOLERA TOXIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYTOKINE; ENTEROTOXIN; FORSKOLIN; INTERLEUKIN 12; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PERTUSSIS TOXIN; TUMOR NECROSIS FACTOR ALPHA; VIRULENCE FACTOR;

ARTICLE; BACTERIAL VIRULENCE; BORDETELLA PERTUSSIS; CONTROLLED STUDY; DENDRITIC CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LYMPHOCYTE PROLIFERATION; MIXED LYMPHOCYTE REACTION; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TOXIN ANALYSIS;

ADENYLATE CYCLASE TOXIN; ADJUVANTS, IMMUNOLOGIC; ANTIGEN PRESENTATION; BORDETELLA PERTUSSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELLS, CULTURED; CYCLIC AMP; CYTOKINES; DENDRITIC CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; HUMANS; INTERLEUKIN-12; LIPOPOLYSACCHARIDES; LYMPHOCYTE CULTURE TEST, MIXED; MONOCYTES; PERTUSSIS TOXIN; PROTEIN STRUCTURE, TERTIARY; SECOND MESSENGER SYSTEMS; TUMOR NECROSIS FACTOR-ALPHA;

BACTERIA (MICROORGANISMS); BORDETELLA PERTUSSIS;

EID: 0036855441     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (42)

1. Pittman, M. (1979) Pertussis toxin: The cause of the harmful effects and prolonged immunity of whooping cough. A hypothesis. Rev. Infect. Dis. 1, 401-412.
2. Weiss, A. A., Hewlett, E. L. (1986) Virulence factors of Bordetella pertussis. Annu. Rev. Microbiol. 40, 661-686.
3. Tamura, M., Nogimori, K., Murai, S., Yajima, M., Ito, K., Katada, T., Ui, M., Ishii, S. (1982) Subunit structure of islet-activating protein, pertussis toxin, in conformity with the A-B model. Biochemistry 21, 5516-5522.
4. Tamura, M., Nogimori, K., Yajima, M., Ase, K., Ui, M. (1983) A role of the B-oligomer moiety of islet-activating protein, pertussis toxin, in development of the biological effects on intact cells. J. Biol. Chem. 258, 6756-6761.
5. Hazes, B., Read, R. J. (1997) Accumulating evidence suggests that several AB-toxins subvert the endoplasmic reticulum-associated protein degradation pathway to enter target cells. Biochemistry 36, 11051-11054.
6. Hazeki, O., Ui, M. (1981) Modification by islet-activating protein of receptor-mediated regulation of cyclic AMP accumulation in isolated rat heart cells. J. Biol. Chem. 256, 2856-2862.
7. Katada, T., Ui, M. (1979) Islet-activating protein. Enhanced insulin secretion and cyclic AMP accumulation in pancreatic islets due to activation of native calcium ionophores. J. Biol. Chem. 254, 469-479.
8. Katada, T., Ui, M. (1980) Slow interaction of islet-activating protein with pancreatic islets during primary culture to cause reversal of alpha-adrenergic inhibition of insulin secretion. J. Biol. Chem. 255, 9580-9588.
9. Katada, T., Amano, T., Ui, M. (1982) Modulation by islet-activating protein of adenylate cyclase activity in C6 glioma cells. J. Biol. Chem. 257, 3739-3746.
10. Heyningen, S. V. (1974) Cholera toxin: Interaction of subunits with ganglioside GM1. Science 183, 656-657.
11. Fukuta, S., Magnani, J. L., Twiddy, E. M., Holmes, R. K., Ginsburg, V. (1988) Comparison of the carbohydrate-binding specificities of cholera toxin and Escherichia coli heat-labile enterotoxins LTh-I, LT-IIa, and LT-IIb. Infect. Immun. 56, 1748-1753.
12. Cassel, D., Selinger, Z. (1977) Mechanism of adenylate cyclase activation by cholera toxin: Inhibition of GTP hydrolysis at the regulatory site. Proc. Natl. Acad. Sci. USA 74, 3307-3311.
13. Sakamoto, H., Bellalou, J., Sebo, P., Ladant, D. (1992) Bordetella pertussis adenylate cyclase toxin. Structural and functional independence of the catalytic and hemolytic activities. J. Biol. Chem. 267, 13598-13602.
14. Ladant, D., Ullmann, A. (1999) Bordatella pertussis adenylate cyclase: A toxin with multiple talents. Trends Microbiol. 7, 172-176.
15. Hewlett, E., Wolff, J. (1976) Soluble adenylate cyclase from the culture medium of Bordetella pertussis: Purification and characterization. J. Bacteriol. 127, 890-898.
16. Hewlett, E. L., Urban, M. A., Manclark, C. R., Wolff, J. (1976) Extracytoplasmic adenylate cyclase of Bordetella pertussis. Proc. Natl. Acad. Sci. USA 73, 1926-1930.
17. Guermonprez, P., Khelef, N., Blouin, E., Rieu, P., Ricciardi-Castagnoli, P., Guiso, N., Ladant, D., Leclerc, C. (2001) The adenylate cyclase toxin of Bordetella pertussis binds to target cells via the alpha(M)beta(2) integrin (CD11b/CD18). J. Exp. Med. 193, 1035-1044.
18. Rogel, A., Hanski, E. (1992) Distinct steps in the penetration of adenylate cyclase toxin of Bordetella pertussis into sheep erythrocytes. Translocation of the toxin across the membrane. J. Biol. Chem. 267, 22599-22605.
19. Lycke, N. (1997) The mechanism of cholera toxin adjuvanticity. Res. Immunol. 148, 504-520.
20. Roberts, M., Bacon, A., Rappuoli, R., Pizza, M., Cropley, I., Douce, G., Dougan, G., Marinaro, M., McGhee, J., Chatfield, S. (1995) A mutant pertussis toxin molecule that lacks ADP-ribosyltransferase activity, PT9K/129G, is an effective mucosal adjuvant for intranasally delivered proteins. Infect. Immun. 63, 2100-2108.
21. Ryan, M., McCarthy, L., Rappuoli, R., Mahon, B. P., Mills, K. H. (1998) Pertussis toxin potentiates Th1 and Th2 responses to co-injected antigen: Adjuvant action is associated with enhanced regulatory cytokine production and expression of the co-stimulatory molecules B7- 1, B7-2 and CD28. Int. Immunol. 10, 651-662.
22. Tamura, S., Funato, H., Nagamine, T., Aizawa, C., Kurata, T. (1989) Effectiveness of cholera toxin B subunit as an adjuvant for nasal influenza vaccination despite pre-existing immunity to CTB. Vaccine 7, 503-505.
23. Dickinson, B. L., Clements, J. D. (1995) Dissociation of Escherichia coli heat-labile enterotoxin adjuvanticity from ADP-ribosyltransferase activity. Infect. Immun. 63, 1617-1623.
24. Douce, G., Turcotte, C., Cropley, I., Roberts, M., Pizza, M., Domenghini, M., Rappuoli, R., Dougan, G. (1995) Mutants of Escherichia coli heatlabile toxin lacking ADP-ribosyltransferase activity act as nontoxic, mucosal adjuvants. Proc. Natl. Acad. Sci. USA 92, 1644-1648.
25. 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.
26. de Haan, L., Verweij, W. R., Feil, I. K., Holtrop, M., Hol, W. G., Agsteribbe, E., Wilschut, J. (1998) Role of GM1 binding in the mucosal immunogenicity and adjuvant activity of the Escherichia coli heat-labile enterotoxin and its B subunit. Immunology 94, 424-430.
27. Isaka, M., Yasuda, Y., Kozuka, S., Miura, Y., Taniguchi, T., Matano, K., Goto, N., Tochikubo, K. (1998) Systemic and mucosal immune responses of mice to aluminium-adsorbed or aluminium-non-adsorbed tetanus toxoid administered intranasally with recombinant cholera toxin B subunit. Vaccine 16, 1620-1626.
28. Wu, H. Y., Russell, M. W. (1998) Induction of mucosal and systemic immune responses by intranasal immunization using recombinant cholera toxin B subunit as an adjuvant. Vaccine 16, 286-292.
29. Blanchard, T. G., Lycke, N., Czinn, S. J., Nedrud, J. G. (1998) Recombinant cholera toxin B subunit is not an effective mucosal adjuvant for oral immunization of mice against Helicobacter felis. Immunology 94, 22-27.
30. Lycke, N., Holmgren, J. (1986) Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens. Immunology 59, 301-308.
31. Vajdy, M., Lycke, N. Y. (1992) Cholera toxin adjuvant promotes long-term immunological memory in the gut mucosa to unrelated immunogens after oral immunization. Immunology 75, 488-492.
32. Carbonetti, N. H., Irish, T. J., Chen, C. H., O'Connell, C. B., Hadley, G. A., McNamara, U., Tuskan, R. G., Lewis, G. K. (1999) Intracellular delivery of a cytolytic T-lymphocyte epitope peptide by pertussis toxin to major histocompatibility complex class I without involvement of the cytosolic class I antigen processing pathway. Infect. Immun. 67, 602-607.
33. Carbonetti, N. H., Tuskan, R. G., Lewis, G. K. (2001) Stimulation of HIV gp120-specific cytolytic T lymphocyte responses in vitro and in vivo using a detoxified pertussis toxin vector. AIDS Res. Hum. Retrovir. 17, 819-827.
34. Ryan, E. J., McNeela, E., Pizza, M., Rappuoli, R., O'Neill, L., Mills, K. H. (2000) Modulation of innate and acquired immune responses by Escherichia coli heat-labile toxin: Distinct pro- and anti-inflammatory effects of the nontoxic AB complex and the enzyme activity. J. Immunol. 165, 5750-5759.
35. Porgador, A., Staats, H. F., Itoh, Y., Kelsall, B. L. (1998) Intranasal immunization with cytotoxic T-lymphocyte epitope peptide and mucosal adjuvant cholera toxin: Selective augmentation of peptide-presenting dendritic cells in nasal mucosa-associated lymphoid tissue. Infect. Immun. 66, 5876-5881.
36. Williamson, E., Westrich, G. M., Viney, J. L. (1999) Modulating dendritic cells to optimize mucosal immunization protocols. J. Immunol. 163, 3668-3675.
37. 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.
38. Sallusto, F., Lanzavecchia, A. (1994) Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179, 1109-1118.
39. Verhasselt, V., Buelens, C., Willems, F., De Groote, D., Haeffner-Cavaillon, N., Goldman, M. (1997) Bacterial lipopolysaccharide stimulates the production of cytokines and the expression of costimulatory molecules by human peripheral blood dendritic cells: EVidence for a soluble CD14-dependent pathway. J. Immunol. 158, 2919-2925.
40. Braun, M. C., He, J., Wu, C. Y., Kelsall, B. L. (1999) Cholera toxin suppresses interleukin (IL)-12 production and IL-12 receptor beta1 and beta2 chain expression. J. Exp. Med. 189, 541-552.
41. Gjertsen, B. T., Mellgren, G., Otten, A., Maronde, E., Genieser, H. G., Jastorff, B., Vintermyr, O. K., McKnight, G. S., Doskeland, S. O. (1995) Novel (Rp)-cAMPS analogs as tools for inhibition of cAMP-kinase in cell culture. Basal cAMP-kinase activity modulates interleukin-1 beta action. J. Biol. Chem. 270, 20599-20607.
42. Chijiwa, T., Mishima, A, Hagiwara, M., Sano, M., Hayashi, K., Inoue, T., Naito, K., Toshioka, T., Hidaka, H. (1990) Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(pbromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J. Biol. Chem. 265, 5267-5272.