Zonula occludens toxin acts as an adjuvant through different mucosal routes and induces protective immune responses

Infection and Immunity

Volumn 71, Issue 4, 2003, Pages 1897-1902

  Marinaro, Mariarosaria ^a   Fasano, Alessio ^b   De Magistris, Maria Teresa ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ESCHERICHIA COLI ENTEROTOXIN; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; MEMBRANE RECEPTOR; OVALBUMIN; TETANUS TOXOID; UNCLASSIFIED DRUG; VACCINE; ZONULA OCCLUDENS TOXIN; ZONULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BINDING SITE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG MECHANISM; FEMALE; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; IMMUNOGLOBULIN BLOOD LEVEL; INTRANASAL DRUG ADMINISTRATION; MEMBRANE PERMEABILITY; MOUSE; MUCOSA PERMEABILITY; NONHUMAN; NOSE MUCOSA; PRIORITY JOURNAL; SPLEEN CELL; TIGHT JUNCTION; VACCINE PRODUCTION; VIBRIO CHOLERAE;

ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ADMINISTRATION, RECTAL; ANIMALS; ANTIBODIES, BACTERIAL; CHOLERA TOXIN; CLOSTRIDIUM TETANI; FEMALE; IMMUNITY, MUCOSAL; IMMUNIZATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; OVALBUMIN; RECOMBINANT PROTEINS; TETANUS; TETANUS TOXIN; TETANUS TOXOID;

EID: 0345268671     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.71.4.1897-1902.2003     Document Type: Article

References (27)

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. Belyakov, I. M., Z. Hel, B. Kelsall, V. A. Kuznetsov, J. D. Ahlers, J. Nacsa, D. I. Watkins, T. M. Allen, A. Sette, J. Altman, R. Woodward, P. D. Markham, J. D. Clements, G. Franchini, W. Strober, and J. A. Berzofsky. 2001. Mucosal AIDS vaccine reduces disease and viral load in gut reservoir and blood after mucosal infection of macaques. Nat. Med. 7:1320-1326.
3. Di Pierro, M., R. Lu, S. Uzzau, W. Wang, K. Margaretten, C. Pazzani, F. Maimone, and A. Fasano. 2001. Zonula occludens toxin structure-function analysis. J. Biol. Chem. 276:19160-19165.
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. Elson, C. O., and M. T. Dertzbaugh. 1994. Mucosal adjuvants, p. 391-401. In P. L. Ogra, J. Mestecky, M. E. Lamm, W. Strober, J. R. McGhee, and J. Bienenstock (ed.), Handbook of mucosal immunology. Academic Press, Inc., San Diego, Calif.
6. Fasano, A. 1998. Innovative strategies for the oral delivery of drugs and peptides. Trends Biotechnol. 16:152-157.
7. Fasano, A. 2000. Regulation of intercellular tight junctions by Zonula occludens toxin and its eukaryotic analogue zonulin. Ann. N. Y. Acad. Sci. 915:214-222.
8. Fasano, A. 2001. Intestinal zonulin: open sesame! Gut 49:159-162.
9. 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.
10. 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.
11. Fasano, A., and S. Uzzau. 1997. Modulation of intestinal tight junctions by Zonula occludens toxin permits enteral administration of insulin and other macromolecules in an animal model. J. Clin. Investig. 99:1158-1164.
12. 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.
13. Gagliardi, M. C., F. Sallusto, M. Marinaro, A. Langenkamp, A. Lanzavecchia, and M. T. De Magistris. 2000. Cholera toxin induces maturation of human dendritic cells and licences them for Th2 priming. Eur. J. Immunol. 30:2394-2403.
14. 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.
15. Marinaro, M., A. Di Tommaso, S. Uzzau, A. Fasano, and M. T. De Magistris. 1999. Zonula occludens toxin is a powerful mucosal adjuvant for intranasally delivered antigens. Infect. Immun. 67:1287-1291.
16. Rappuoli, R., M. Pizza, G. Douce, and G. Dougan. 1999. A relationship between the structure and function of cholera and Escherichia coli heat-labile enterotoxins and their immunological activity at mucosal surfaces. Immunol. Today 20:493-500.
17. Ryan, E. J., L. M. Daly, and K. H. G. Mills. 2001. Immunomodulators and delivery systems for vaccination by mucosal routes. Trends Biotechnol. 19:293-304.
18. Spangler, B. D. 1992. Structure and function of cholera toxin and the related Escherichia coli heat-labile enterotoxin. Microbiol. Rev. 56:622-647.
19. 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.
20. 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.
21. Tamura, S., H. Funato, T. Nagamine, C. Aizawa, and T. Kurata. 1989. Effectiveness of cholera toxin B subunit as an adjuvant for nasal influenza vaccination despite pre-existing immunity to CTB. Vaccine 7:503-505.
22. Uzzau, S., R. Lu, W. Wang, C. Fiore, and A. Fasano. 2001. Purification and preliminary characterization of the zonula occludens toxin receptor from human (CaCo2) and murine (IEC6) intestinal cell lines. FEMS Microbiol. Lett. 194:1-5.
23. van Ginkel, F. W., R. J. Jackson, Y. Yuki, and J. R. McGhee. 2000. The mucosal adjuvant cholera toxin redirects vaccine proteins into olfactory tissues. J. Immunol. 165:4778-4782.
24. Vines, R. R., S. S. Perdue, J. S. Moncrief, D. R. Sentz, L. A. Barroso, R. L. Wright, and T. D. Wilkins. 2000. Fragilysin, the enterotoxin from Bacteroides fragilis, enhances the serum antibody response to antigen co-administered by the intranasal route. Vaccine 19:655-660.
25. Waldor, M. K., and J. J. Mekalanos. 1996. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910-1914.
26. Wang, W., S. Uzzau, S. E. Goldblum, and A. Fasano. 2000. Human zonulin, a potential modulator of intestinal tight junctions. J. Cell Sci. 24:4435-4440.
27. 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.