Mutant Escherichia coli heat-labile toxin B subunit that separates toxoid-mediated signaling and immunomodulatory action from trafficking and delivery functions

Infection and Immunity

Volumn 71, Issue 3, 2003, Pages 1527-1537

  Fraser, Sylvia A ^a   De Haan, Lolke ^a   Hearn, Arron R ^a   Bone, Heather K ^a   Salmond, Robert J ^a   Rivett, A Jennifer ^a   Williams, Neil A ^a   Hirst, Timothy R ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENTEROTOXIN; TOXOID;

ADSORPTION; ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIUM MUTANT; BETA CHAIN; CELL FUNCTION; CELL INTERACTION; COMPLEX FORMATION; DENDRITIC CELL; ESCHERICHIA COLI; GENE DELIVERY SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; LEUKOCYTE ADHERENCE; NONHUMAN; PRIORITY JOURNAL;

ADJUVANTS, IMMUNOLOGIC; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; APOPTOSIS; BACTERIAL TOXINS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; ENTEROTOXINS; ESCHERICHIA COLI PROTEINS; FEMALE; G(M1) GANGLIOSIDE; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTATION; NF-KAPPA B; PROTEIN TRANSPORT; STRUCTURE-ACTIVITY RELATIONSHIP; TOXOIDS;

EID: 0037369748     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.3.1527-1537.2003     Document Type: Article

References (61)

1. Aman, A. T., S. Fraser, E. A. Merritt, C. Rodigherio, M. Kenny, M. Ahn, W. G. J. Hol, N. A. Williams, W. I. Lencer, and T. R. Hirst. 2001. A mutant cholera toxin B subunit that binds GM1-ganglioside but lacks immunomodulatory or toxic activity. Proc. Natl. Acad. Sci. USA 98:8536-8541.
2. Amin, T., and T. R. Hirst. 1994. Purification of the B-subunit oligomer of Escherichia coli heat-labile enterotoxin by heterologous expression and secretion in a marine Vibrio. Protein Expr. Purif. 5:198-204.
3. Barton, N. W., and A. Rosenberg. 1973. Action of Vibrio cholerae neuraminidase (sialidase) upon the surface of intact cells and their isolated sialolipid components. J. Biol. Chem. 248:7353-7358.
4. Bergerot, I., C. Ploix, J. Petersen, V. Moulin, C. Rask, N. Fabien, M. Lindblad, A. Mayer, C. Czerkinsky, J. Holmgren, and C. Thivolet. 1997. A cholera toxoid-insulin conjugate as an oral vaccine against spontaneous autoimmune diabetes. Proc. Natl. Acad. Sci. USA 94:4610-4614.
5. Bone, H., S. Eckholdt, and N. A. Williams. 2002. Modulation of B lymphocyte signalling by the B subunit of Escherichia coli heat-labile enterotoxin. Int. Immunol. 14:647-658.
6. Bone, H., and N. A. Williams. 2001. Antigen-receptor cross-linking and lipopolysaccharide trigger distinct phosphoinositide 3-kinase-dependent pathways to NF-kappa B activation in primary B cells. Int. Immunol. 13: 807-816.
7. Braun, M. C., J. He, C. Y. Wu, and B. L. Kelsall. 1999. Cholera toxin suppresses interleukin (IL)-12 production and IL-12 receptor β1 and β2 chain expression. J. Exp. Med. 189:541-552.
8. 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.
9. De Haan, L, A. R. Hearn, A. J. Rivett, and T. R. Hirst. 2002. Enhanced delivery of exogenous peptides into the class I antigen processing and presentation pathway. Infect. Immun. 70:3249-3258.
10. De Haan, L., and T. R. Hirst. 2000. Cholera toxin and related enterotoxins: a cell biological and immunological perspective. J. Nat. Toxins 9:281-297.
11. De Haan, L., W. R. Verweij, I. K. Feil, M. Holtrop, W. G. J. Hol, E. Agsteribbe, and J. Wilschut. 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.
12. De Haan, L., W. R. Verweij, I. K. Feil, T. H. Lijnema, W. G. J. Hol, E. Agsteribbe, and J. Wilschut. 1996. Mutants of the Escherichia coli heat-labile enterotoxin with reduced ADP-ribosylation activity or no activity retain the immunogenic properties of the native holotoxin. Infect. Immun. 64:5413-5416.
13. De Wolf, M. J. S., M. Fridkin, and L. D. Kohn. 1981. Tryptophan residues of cholera toxin and its A and B protomers. Intrinsic fluorescence and solute quenching upon interacting with the ganglioside GM1, oligo-GM1, or dansylated oligo-GM1. J. Biol. Chem. 256:5489-5496.
14. Elson, C. O., and W. Ealding. 1984. Generalized systemic and mucosal immunity in mice after mucosal stimulation with cholera toxin. J. Immunol. 132:2736-2741.
15. Fishman, P. H., and E. E. Atikkan. 1980. Mechanism of action of cholera toxin: effect of receptor density and multivalent binding on activation of adenylate cyclase. J. Membr. Biol. 54:51-60.
16. Francis, M. L., J. Ryan, M. G. Jobling, R. K. Holmes, J. Moss, and J. J. Mond. 1992. Cyclic AMP-independent effects of cholera toxin on B cell activation. II: binding of GM1 induces B cell activation. J. Immunol. 148: 1999-2005.
17. Fukuta, S., J. L. Magnani, E. M. Twiddy, R. K. Holmes, and V. Ginsburg. 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.
18. Hasenkrug, K. J., and U. Dittmer. 2000. The role of CD4 and CD8 T cells in recovery and protection from retroviral infection: lessons from the Friend virus model. Virology 272:244-249.
19. Higuchi, R., B. Krummel, and R. K. Saiki. 1988. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 16:7351-7367.
20. 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.
21. Janes, P. W., S. C. Ley, and A. I. Magee. 1999. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147:447-461.
22. Kuziemko, G. M., M. Stroh, and R. C. Stevens. 1996. Cholera toxin binding affinity and specificity for gangliosides determined by surface plasmon resonance. Biochemistry 35:6375-6384.
23. Lencer, W. I., T. R. Hirst, and R. K. Holmes. 1999. Membrane traffic and the cellular uptake of cholera toxin. Biochim. Biophys. Acta 1450:177-190.
24. 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 action in vivo. J. Immunol. 142:20-27.
25. Lycke, N., and J. Holmgren. 1986. Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens, Immunology 59:301-308.
26. MacKenzie, C. R., T. Hirama, K. K. Lee, E. Altman, and N. M. Young. 1997, Quantitative analysis of bacterial toxin affinity and specificity for glycolipid receptors by surface ptasmon resonance. J. Biol. Chem. 272:5533-5538.
27. 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.
28. Merritt, E. A., T. K. Sixma, K. H. Kalk, B. A. M. Van Zanten, and W. G. J. Hol. 1994. Galactose-binding site in Escherichia coli heat-labile enterotoxin (LT) and cholera toxin (CT). Mol. Microbiol. 13:745-753.
29. Millar, D. G., and T. R. Hirst. 2001. Cholera toxin and Escherichia coli enterotoxin B-subunits inhibit macrophage-mediated antigen processing and presentation: evidence for antigen persistence in non-acidic recycling endosomal compartments. Cell. Microbiol. 3:311-329.
30. Millar, D. G., T. R. Hirst, and D. P. Snider. 2001. Escherichia coli heat-labile enterotoxin B subunit is a more potent mucosal adjuvant than its closely related homologue, the B subunit of cholera toxin. Infect. Immun. 69:3476-3482.
31. Nashar, T. O., T. R. Hirst, and N. A. Williams. 1997. Modulation of B-cell activation by the B subunit of Escherichia coli enterotoxin: receptor interaction up-regulates MHC class II, B7, CD40, CD25 and ICAM-1. Immunology 91:572-578.
32. Nashar, T. O., H. M. Webb, S. Eaglestone, N. A. Williams, and T. R. Hirst. 1996. Potent immunogenicity of the B subunits of Escherichia coli heat-labile enterotoxin: Receptor binding is essential and induces differential modulation of lymphocyte subsets. Proc. Natl. Acad. Sci. USA 93:226-230.
33. Nashar, T. O., N. A. Williams, and T. R. Hirst. 1996. Cross-linking of cell surface ganglioside GM1 induces the selective apoptosis of mature CD8+ T lymphocytes. Int. Immunol, 8:731-736.
34. Orlandi, P. A., D. R. Critchley, and P. H. Fishman. 1994. The heat-labile enterotoxin of Escherichia coli binds to polylactosaminoglycan-containing receptors in CaCo-2 human intestinal epithelial cells. Biochemistry 33:12886-12895.
35. Pacuszka, T., R. M. Bradley, and P. H. Fishan. 1991. Neoglycolipid analogues of ganglioside GM1 as functional receptors of cholera toxin. Biochemistry 30:2563-2570.
36. Rappuoli, R., M. Pizza, G. Douce, and G. Dougan. 1999. Structure and mucosal adjuvanticity of cholera and Escherichia coli heat-labile enterotoxins. Immunol. Today 20:493-500.
37. Richards, C. M., A. T. Aman, T. R. Hirst, T. J. Hill, and N. A. Williams. 2001. Protective mucosal immunity to ocular herpes simplex virus type 1 infection in mice by using Escherichia coli heat-labile enterotoxin B subunit as an adjuvant. J. Virol, 75:1664-1671.
38. Rock, K. L., L. Rothstein, and S. Gamble. 1990. Generation of class I MHC-restricted T-T hybridomas. J. Immunol. 145:804-811.
39. Rodighiero, C., Y. Fujinaga, T. R. Hirst, and W. I. Lencer. 2001. A cholera toxin B-subunit variant that binds ganglioside GM1 but fails to induce toxicity. J. Biol. Chem. 276:36939-36945.
40. Ruddock, L. W., S. P. Ruston, S. M. Kelly, N. C. Price, R. B. Freedman, and T. R. Hirst. 1995. Kinetics of acid-mediated disassembly of the B subunit pentamer of Escherichia coli heat-labile enterotoxin. Molecular basis of pH stability. J. Biol. Chem. 270:29953-29958.
41. Ruddock, L. W., H. M. Webb, S. P. Ruston, C. Cheesman, R. B. Freedman, and T. R. Hirst. 1996. A pH-dependent conformational change in the Bsubunit pentamer of Escherichia coli heat-labile enterotoxin: structural basis and possible functional role for a conserved feature of the AB(5) toxin family. Biochemistry 35:16069-16076.
42. Salmond, R. J., R. S. Pitman, E. Jimi, M. Soriani, T. R. Hirst, S. Ghosh, M. Rincon, and N. A. Williams. 2002. CD8+ T cell apoptosis induced by Escherichia coli heat-labilenterotoxin B subunit occurs via a novel pathway involving NF-κB-dependent caspase activation. Eur. J. Immunol. 32:1737-1747.
43. Schneider, U., H. U. Schwenk, and G. Bornkamm. 1977. Characterization of EBV-genome negative "null" and "T" cell lines derived from children with acute lymphoblastic leukemia and leukemic transformed non-Hodgkin lymphoma. Int. J. Cancer 19:621-626.
44. Sears, C. L., and J. B. Kaper. 1996. Enteric bacterial toxins: mechanisms of action and linkage to intestinal secretion. Microbiol. Rev. 60:167-215.
45. Soriani, M., L. Bailey, and T. R. Hirst. 2002. Contribution of the ADPribosylating and receptor-binding properties of cholera-like enterotoxins in modulating cytokine secretion by human intestinal epithelial cells. Microbiology 148:667-676.
46. Soriani, M., N. A. Williams, and T. R. Hirst. 2001. Escherichia coli enterotoxin B subunit triggers apoptosis of CD8+ T cells by activating transcription factor c-Myc. Infect. Immun. 69:4923-4930.
47. Spangler, B. D. 1992. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56:622-647.
48. Sun, J. B., C. Rask, T. Olsson, J. Holmgren, and C. Czerkinsky. 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.
49. Tarlakoff, A. M., and P. Vassalli. 1983. Lectin-binding sites as markers of Golgi subcompartments: proximal-to-distal maturation of oligosaccharides. J. Cell Biol. 97:1243-1248.
50. Teneberg, S., T. R. Hirst, J. Angstrom, and K. A. Karlsson. 1994. Comparison of the glycolipid-binding specificities of cholera toxin and porcine Escherichia coli heat-labile enterotoxin: identification of a receptor-active nonganglioside glycolipid for the heat-labile toxin in infant rabbit small intestine. Glycoconj. J. 11:533-540.
51. Tochikubo, K., M. Isaka, Y. Yasuda, S. Kozuka, K. Matano, Y. Miura, and T. Taniguchi. 1998. Recombinant cholera toxin B subunit acts as an adjuvant for the mucosal and systemic responses of mice to mucosally co-administered bovine serum albumin. Vaccine 16:150-155.
52. Truitt, R. L., C. Hanke, J. Radke, R. Mueller, and J. T. Barbieri. 1998. Glycosphingolipids as novel targets for T-cell suppression by the B subunit of recombinant heat-labile enterotoxin. Infect. Immun. 66:1299-1308.
53. Turcanu, V., T. R. Hirst, and N. A. Williams. 2002. Modulation of human monocytes by Escherichia coli heat-labile enterotoxin B-subunit; altered cytokine production and its functional consequences. Immunology 106:316-325.
54. Verweij, W. R., L. de Haan, M. Holtrop, R. Brands, G. J. M. van Scharrenburg, E. Agsteribbe, and J. Wilschut. 1998. Mucosal immunoadjuvant activity of the recombinant Escherichia coli heat-labile enterotoxin and its B subunit: Induction of systemic IgG and secretory IgA responses in mice by intranasal immunization with influenza surface antigen. Vaccine 16:2069-2076.
55. Williams, N. A., T. R. Hirst, and T. O. Nashar. 1999. Immune modulation by the cholera-like enterotoxins: from adjuvant to therapeutic. Immunol. Today 20:95-101.
56. Williams, N. A., L. M. Stasiuk, T. O. Nashar, C. M. Richards, A. K. Lang, M. J. Day, and T. R. Hirst, 1997. Prevention of autoimmune disease due to lymphocyte modulation by the B-subunit of Escherichia coli heat-labile enterotoxin. Proc. Natl. Acad. Sci. USA 94:5290-5295.
57. Wolf, A. A., M. G. Jobling, S. Wimer Mackin, M. Ferguson Maltzman, J. L. Madara, R. K. Holmes, and W. I. Lencer. 1998. Ganglioside structure dictates signal transduction by cholera toxin and association with caveolae-like membrane domains in polarized epithelia. J. Cell Biol. 141:917-927.
58. 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.
59. Wu, H. Y., and M. W. Russell. 1998. Induction of mucosal and systemic immune responses by intranasal immunization using recombinant cholera toxin B subunit as an adjuvant. Vaccine 16:286-292.
60. Yankelevich, B., V. A. Soldatenkov, J. Hodgson, A. J. Polotsky, K. Creswell, and A. Mazumder. 1996. Differential induction of programmed cell death in CD8+ and CD4+ T cells by the B subunit of cholera toxin. Cell. Immunol. 168:229-234.
61. Yu, J., H. Webb, and T. R. Hirst. 1992. A homologue of the Escherichia coli DsbA protein involved in disulphide bond formation is required for enterotoxin biogenesis in Vibrio cholerae. Mol. Microbiol. 6:1949-1958.