Zonula occludens toxin is a powerful mucosal adjuvant for intranasally delivered antigens

Infection and Immunity

Volumn 67, Issue 3, 1999, Pages 1287-1291

  Marinaro, Mariarosaria ^a   Di Tommaso, Annalisa ^b   Uzzau, Sergio ^c   Fasano, Alessio ^c   De Magistris, Maria Teresa ^a,b  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b CHIRON VACCINES   (Italy)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CHOLERA TOXIN; ESCHERICHIA COLI ENTEROTOXIN; IMMUNOGLOBULIN G; OVALBUMIN;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; DRUG DELIVERY SYSTEM; ESCHERICHIA COLI; FEMALE; IMMUNOGLOBULIN BLOOD LEVEL; INTRANASAL DRUG ADMINISTRATION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; NOSE MUCOSA; PRIORITY JOURNAL; TIGHT JUNCTION; VACCINATION; VIBRIO CHOLERAE;

EID: 0033050297     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.3.1287-1291.1999     Document Type: Article

References (31)

1. Baudry, B., A. Fasano, J. Ketley, and J. B. Kaper. 1992. Cloning of a gene (zot) encoding a new toxin produced by Vibrio cholerae. Infect. Immun 60: 428-434.
2. Clements, J. D., N. M. Hartzog, and F. L. Lyon. 1988. Adjuvant activity of Escherichia coli heat-labile enterotoxin and effect on the induction of oral tolerance in mice to unrelated protein antigens. Vaccine 6:269-277.
3. Cong, Y., C. T. Weaver, and C. O. Elson. 1997. The mucosal adjuvanticity of cholera toxin involves enhancement of costimulatory activity by selective up-regulation of B7.2 expression. J. Immunol. 159:5301-5308.
4. Di Tommaso, A., G. Saletti, M. Pizza, R. Rappuoli, G. Dougan, S. Abrignani, G. Douce, and M. T. De Magistris. 1996. Induction of antigen-specific antibodies in vaginal secretions by using a nontoxic mutant of heat-labile enterotoxin as a mucosal adjuvant. Infect. Immun. 64:974-979.
5. Douce, G., C. Turcotte, I. Cropley, M. Roberts, M. Pizza, M. Domenighini, R. Rappuoli, and G. Dougan. 1995. Mutants of Escherichia coli heat-labile toxin lacking ADP-ribosyltransferase activity act as nontoxic, mucosal adjuvants. Proc. Natl. Acad. Sci. USA 92:1644-1648.
6. Douce, G., M. Fontana, M. Pizza, R. Rappuoli, and G. Dougan. 1997. Intranasal immunogenicity and adjuvanticity of site-directed mutant derivatives of cholera toxin. Infect. Immun. 65:2821-2828.
7. Fando, R., J. L. Pérez, B. L. Rodriguez, J. Campos, A. Robert, L. García, A. Silva, and J. A. Benitez. 1997. Promoter activities in Vibrio cholerae ctxΦ prophage. Infect. Immun. 65:1561-1565.
8. Fasano, A., B. Baudry, D. W. Pumplin, S. S. Wasserman, B. D. Tall, J. M. Ketley, and J. B. Kaper. 1991. Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions. Proc. Natl. Acad. Sci. USA 88:5242-5246.
9. Fasano, A., C. Fiorentini, G. Donelli, S. Uzzau, J. B. Kaper, K. Margaretten, X. Ding, S. Guandalini, L. Comstock, and S. E. Goldblum. 1995. Zonula occludens toxin modulates tight junctions through protein kinase C-dependent actin reorganization, in vitro. J. Clin. Investig. 96:710-720.
10. Fasano, A., and S. Uzzau. 1997. Modulation of intestinal tight junctions by zonula occludens toxin permits enterai administration of insulin and other macromolecules in an animal model. J. Clin. Investig. 99:1158-1164.
11. Fasano, A., S. Uzzau, C. Fiore, and K. Margaretten. 1997. The enterotoxic effect of zonula occludens toxin (ZOT) on rabbit small intestine involves the paracellular pathway. Gastroenterology 112:839-846.
12. Fasano, A. Unpublished data.
13. Finkelman, F. D., J. Holmes, I. M. Katona, J. F. J. Urban, M. P. Beckman, L. S. Park, K. A. Schooley, R. L. Coffman, T. R. Mosmann, and W. E. Paul. 1990. Lymphokine control of in vivo immunoglohulin isotype selection. Annu. Rev. Immunol. 8:303-333.
14. Giuliani, M. M., G. Del Giudice, V. Giannelli, G. Douce, G. Dougan, R. Rappuoli, and M. Pizza. 1998. 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. 187:1123-1132.
15. Gizurarson, S., S. Tamura, C. Aizawa, and T. Kurata. 1992. Stimulation of the transepithelial flux of influenza HA vaccine by cholera toxin B subunit. Vaccine 10:101-106.
16. Haneberg, B., D. Kendall, H. M. Amerongen, F. M. Apter, J.-P. Kraehenbuhl, and M. R. Neutra. 1994. Induction of specific immunoglobulin A in the small intestine, colon-rectum, and vagina measured by a new method for collection of secretions from local mucosal surfaces. Infect. Immun. 62: 15-23.
17. Li, T.-K., and B. S. Fox. 1918. Cholera toxin B subunit binding to an antigen-presenting cell directly co-stimulates cytokine production from a T cell clone. Int. Immunol. 8:1849-1856.
18. 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.
19. Lycke, N. 1997. The mechanism of cholera toxin adjuvanticity. Res Immunol. 148:504-520.
20. 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.
21. McGhee, J. R., J. Mestecky, M. T. Dertzbaugh, J. H. Eldridge, M. Hirasawa, and H. Kiyono. 1992. The mucosal immune system: from fundamental concepts to vaccine development. Vaccine 10:75-88.
22. Mosmann, T. R., and R. L. Coffman. 1989. Th1 and Th2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7:145-174.
23. Nashar, T. O., H. M. Webb, S. Eaglestone, N. A. Williams, and T. R. Hirst. 1996. Potent immunogenicity of the B subunit 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.
24. Roberts, M., A. Bacon, R. Rappuoli, M. Pizza, I. Cropley, G. Douce, G. Dougan, M. Marinaro, J. R. McGhee, and S. Chatfield. 1995. A mutant pertussis toxin molecule that lacks ADP-ribosyltransferase activity, PT9K/129G, is an effective mucosal adjuvant for intranasally delivered proteins. Infect. Immun. 53:2100-2108.
25. Ryan, M., L. McCarthy, R. Rappuoli, B. P. Mahon, and K. H. G. Mills. 1998. Pertussin 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.
26. Spangler, B. D. 1992. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56:622-647.
27. Staats, H. F., R. J. Jackson, M. Marinaro, I. Takahashi, H. Kiyono, and J. R. McGhee. 1994. Mucosal immunity to infection with implications for vaccine development. Curr. Opin. Immunol. 6:572-583.
28. 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.
29. Uzzau, S., and A. Fasano. Unpublished data.
30. Waldor, M. K., and J. J. Mekalanos. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910-1914.
31. 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.