MHC class I-restricted cytotoxic lymphocyte responses induced by enterotoxin-based mucosal adjuvants

Journal of Immunology

Volumn 163, Issue 12, 1999, Pages 6502-6510

  Simmons, Cameron P ^a   Mastroeni, Pietro ^a   Fowler, Ray ^a   Ghaem Maghami, Marjan ^a   Lycke, Nils ^c   Pizza, Mariagrazia ^b   Rappuoli, Rino ^b   Dougan, Gordon ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b CHIRON VACCINES   (Italy)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLERA TOXIN; ESCHERICHIA COLI ENTEROTOXIN; GAMMA INTERFERON; INTERLEUKIN 12; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; IMMUNIZATION; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ADENOSINE DIPHOSPHATE RIBOSE; ADJUVANTS, IMMUNOLOGIC; ADMINISTRATION, INTRANASAL; ADMINISTRATION, ORAL; AMINO ACID SUBSTITUTION; ANIMALS; ARGININE; BACTERIAL TOXINS; CHOLERA TOXIN; CYTOTOXICITY, IMMUNOLOGIC; ENTEROTOXINS; EPITOPES, T-LYMPHOCYTE; ESCHERICHIA COLI PROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS I; INJECTIONS, SUBCUTANEOUS; INTERFERON TYPE II; INTERLEUKIN-12; LYMPHOCYTE ACTIVATION; LYSINE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NASAL MUCOSA; OVALBUMIN; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, HELPER-INDUCER; TUMOR CELLS, CULTURED;

EID: 0032735818     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. 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.
2. Lycke, N., and J. Holmgren. 1986. Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens. Immunology 59:301.
3. Pizza, M., M. R. Fontana, M. M. Giuliani, M. Domenighini, C. Magagnoli, V. Giannelli, D. Nucci, W. Hol, R. Manetti, and R. Rappuoli. 1994. A genetically detoxified derivative of heat-labile Escherichia coli enterotoxin induces neutralizing antibodies against the A subunit. J. Exp. Med. 180:2147.
4. Giuliani, M. M., G. Del Giudice, V. Giannelli, G. Dougan, G. Douce, 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.
5. 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.
6. Yamamoto, S., Y. Takeda, M. Yamamoto, H. Kurazono, K. Imaoka, K. Fujihashi, M. Noda, H. Kiyono, and J. R. McGhee. 1997. Mutants in the ADP-ribosyltransferase cleft of cholera toxin lack diarrheagenicity but retain adjuvanticity. J. Exp. Med. 185:1203.
7. 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.
8. Agren, L. C., L. Ekman, B. Lowenadler, and N. Y. Lycke. 1997. Genetically engineered nontoxic vaccine adjuvant that combines B cell targeting with immunomodulation by cholera toxin A1 subunit. J. Immunol. 158:3936.
9. Douce, G., M. M. Giuliani, V. Giannelli, M. G. Pizza, R. Rappuoli, and G. Dougan. 1998. Mucosal immunogenicity of genetically detoxified derivatives of heat labile toxin from Escherichia coli. Vaccine 16:1065.
10. Marchetti, M., M. Rossi, V. Giannelli, M. M. Giuliani, M. Pizza, S. Censini, A. Covacci, P. Massari, C. Pagliaccia, R. Manetti, et al. 1998. Protection against Helicobacter pylori infection in mice by intragastric vaccination with H. pylori antigens is achieved using a nontoxic mutant of E. coli heat-labile enterotoxin (LT) as adjuvant. Vaccine 16:33.
11. Chong, C., M. Friberg, and J. D. Clements. 1998. LT(R192G), a non-toxic mutant of the heat-labile enterotoxin of Escherichia coli, elicits enhanced humoral and cellular immune responses associated with protection against lethal oral challenge with Salmonella spp. Vaccine 16:732.
12. Yamamoto, M., D. E. Briles, S. Yamamoto, M. Ohmura, H. Kiyono, and J. R. McGhee. 1998. A nontoxic adjuvant for mucosal immunity to pneumococcal surface protein A. J. Immunol. 161:4115.
13. Cardenas-Freytag, L., E. Cheng, P. Mayeux, J. E. Domer, and J. D. Clements. 1999. Effectiveness of a vaccine composed of heat-killed Candida albicans and a novel mucosal adjuvant, LT(R192G), against systemic candidiasis. Infect. Immun. 67:826.
14. + cytotoxic T lymphocytes for resistance to mucosal viral transmission in mice and enhancement of resistance by local administration of IL-12. J. Clin. Invest. 102:2072.
15. Bowen, J. C., S. K. Nair, R. Reddy, and B. T. Rouse. 1994. Cholera toxin acts as a potent adjuvant for the induction of cytotoxic T-lymphocyte responses with non-replicating antigens. Immunology 81:338.
16. Porgador, A., H. F. Staats, B. Faiola, E. Gilboa, and T. J. Palker. 1997. Intranasal immunization with CTL epitope peptides from HIV-1 or ovalbumin and the mucosal adjuvant cholera toxin induces peptide-specific CTLs and protection against tumor development in vivo. J. Immunol. 158:834.
17. Partidos, C. D., M. Pizza, R. Rappuoli, and M. W. Steward. 1996. The adjuvant effect of a non-toxic mutant of heat-labile enterotoxin of Escherichia coli for the induction of measles virus-specific CTL responses after intranasal co-immunization with a synthetic peptide. Immunology 89:483.
18. Moore, M. W., F. R. Carbone, and M. J. Bevan. 1988. Introduction of soluble protein into the class 1 pathway of antigen processing and presentation. Cell 54:777.
19. Rotzschke, O., K. Falk, S. Stevanovic, G. Jung, P. Walden, and H. G. Rammensee. 1991. Exact prediction of a natural T cell epitope. Eur. J. Immunol. 21:2891.
20. Magram, J., S. E. Connaughton, R. R. Warrier, D. M. Carvajal, C. Y. Wu, J. Ferrante, C. Stewart, U. Sarmiento, D. A. Faherty, and M. K. Gately. 1996. IL-12-deficient mice are defective in IFN-γ production and type 1 cytokine responses. Immunity 4:471.
21. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune cell function in mice with disrupted interferon-γ genes. Science 259:1739.
22. Murphy, M. L., C. R. Engwerda, P. M. Gorak, and P. M. Kaye. 1997. B7-2 blockade enhances T cell responses to Leishmania donovani. J. Immunol. 159: 4460.
23. Partidos, C. D., P. Vohra, and M. W. Steward. 1996. Induction of measles virus-specific cytotoxic T-cell responses after intranasal immunization with synthetic peptides. Immunology 87:179.
24. Carbone, F. R., C. Kurts, S. R. Bennett, J. F. Miller, and W. R. Heath. 1998. Cross-presentation: a general mechanism for CTL immunity and tolerance. Immunol. Today 19:368.
25. + T cell help. J. Exp. Med. 186:65.
26. Chouaib, S., J. Chehimi, L. Bani, N. Genetet, T. Tursz, F. Gay, G. Trinchieri, and F. Mami-Chouaib. 1994. Interleukin 12 induces the differentiation of major histocompatibility complex class I-primed cytotoxic T-lymphocyte precursors into allospecific cytotoxic effectors. Proc. Natl. Acad. Sci. USA 91:12659.
27. 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.
28. Peterson, J. W., R. A. Finkelstein, J. Cantu, D. L. Gessell, and A. K. Chopra. 1999. Cholera toxin B subunit activates arachidonic acid metabolism. Infect. Immun. 67:794.
29. Stevens, L. A., J. Moss, M. Vaughan, M. Pizza, and R. Rappuoli. 1999. Effects of site-directed mutagenesis of Escherichia coli heat-labile enterotoxin on ADP-ribosyltransferase activity and interaction with ADP-ribosylation factors. Infect. Immun. 67:259.
30. Rothman, J. E. 1994. Mechanisms of intracellular protein transport. Nature 372:55.
31. Moss, J., and M. Vaughan. 1995. Structure and function of ARF proteins: activators of cholera toxin and critical components of intracellular vesicular transport processes. J. Biol. Chem. 270:12327.
32. Xu-Amano, J., R. J. Jackson, K. Fujihashi, H. Kiyono, H. F. Staats, and J. R. McGhee. 1994. Helper Th1 and Th2 cell responses following mucosal or systemic immunization with cholera toxin. Vaccine 12:903.
33. Belyakov, I. M., M. A. Derby, J. D. Ahlers, B. L. Kelsall, P. Earl, B. Moss, W. Strober, and J. A. Berzofsky. 1998. Mucosal immunization with HIV-1 peptide vaccine induces mucosal and systemic cytotoxic T lymphocytes and protective immunity in mice against intrarectal recombinant HIV-vaccinia challenge. Proc. Natl. Acad. Sci. USA 95:1709.
34. Maecker, H. T., D. T. Umetsu, R. H. DeKruyff, and S. Levy. 1998. Cytotoxic T cell responses to DNA vaccination: dependence on antigen presentation via class II MHC. J. Immunol. 161:6532.
35. Schoenberger, S. P., R. E. Toes, E. I. van der Voort, R. Offringa, and C. J. Melief. 1998. T-cell help for cytotoxic T lymphocytes is mediated by CD40-CD40L interactions. Nature 393:480.
36. Bennett, S. R., F. R. Carbone, F. Karamalis, R. A. Flavell, J. F. Miller, and W. R. Heath. 1998. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature 393:478.
37. + T-helper and a T-killer cell. Nature 393:474.
38. von Herrath, M. G., M. Yokoyama, J. Dockter, M. B. Oldstone, and J. L. Whitton. 1996. CD4-deficient mice have reduced levels of memory cytotoxic T lymphocytes after immunization and show diminished resistance to subsequent virus challenge. J. Virol. 70:1072.
39. + T cells. J. Exp. Med. 184:863.
40. Sauzet, J. P., H. Gras-Masse, J. G. Guillet, and E. Gomard. 1996. Influence of strong CD4 epitope on long-term virus-specific cytotoxic T cell responses induced in vivo with peptides. Int. Immunol. 8:457.
41. Porgador, A., H. F. Staats, Y. Itoh, and B. L. Kelsall. 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.
42. Norbury, C. C., B. J. Chambers, A. R. Prescott, H. G. Ljunggren, and C. Watts. 1997. Constitutive macropinocytosis allows TAP-dependent major histocompatibility complex class I presentation of exogenous soluble antigen by bone marrow-derived dendritic cells. Eur. J. Immunol. 27:280.
43. Smith, R. E., A. M. Donachie, D. Grdic, N. Lycke, and A. M. Mowat. 1999. Immune-stimulating complexes induce an IL-12-dependent cascade of innate immune responses. J. Immunol. 162:5536.
44. Ahlers, J. D., N. Dunlop, D. W. Alling, P. L. Nara, and J. A. Berzofsky. 1997. Cytokine-in-adjuvant steering of the immune response phenotype to HIV-1 vaccine constructs: granulocyte-macrophage colony-stimulating factor and TNF-α synergize with IL-12 to enhance induction of cytotoxic T lymphocytes. J. Immunol. 158:3947.
45. Iwasaki, A., B. J. Stiernholm, A. K. Chan, N. L. Berinstein, and B. H. Barber. 1997. Enhanced CTL responses mediated by plasmid DNA immunogens encoding costimulatory molecules and cytokines. J. Immunol. 158:4591.
46. Irvine, K. R., J. B. Rao, S. A. Rosenberg, and N. P. Restifo. 1996. Cytokine enhancement of DNA immunization leads to effective treatment of established pulmonary metastases. J. Immunol. 156:238.
47. Magram, J., S. E. Connaughton, R. R. Warrier, D. M. Carvajal, C. Y. Wu, J. Ferrante, C. Stewart, U. Sarmiento, D. A. Faherty, and M. K. Gately. 1996. IL-12-deficient mice are defective in IFN γ production and type 1 cytokine responses. Immunity 4:471.
48. Oxenius, A., U. Karrer, R. M. Zinkernagel, and H. Hengartner. 1999. IL-12 is not required for induction of type 1 cytokine responses in viral infections. J. Immunol. 162:965.
49. Grdic, D., R. Smith, A. Donachie, M. Kjerrulf, E. Hornquist, A. Mowat, and N. Lycke. 1999. The mucosal adjuvant effects of cholera toxin and immune-stimulating complexes differ in their requirement for IL-12, indicating different pathways of action. Eur. J. Immunol. 29:1774.
50. Schijns, V. E., B. L. Haagmans, C. M. Wierda, B. Kruithof, I. A. Heijnen, G. Alber, and M. C. Horzinek. 1998. Mice lacking IL-12 develop polarized Th1 cells during viral infection. J. Immunol. 160:3958.
51. Wille, A., A. Gessner, H. Lother, and F. Lehmann-Grube. 1989. Mechanism of recovery from acute virus infection. VIII. Treatment of lymphocytic choriomeningitis virus-infected mice with anti-interferon-γ monoclonal antibody blocks generation of virus-specific cytotoxic T lymphocytes and virus elimination. Eur. J. Immunol. 19:1283.
52. Graham, M. B., D. K. Dalton, D. Giltinan, V. L. Braciale, T. A. Stewart, and T. J. Braciale. 1993. Response to influenza infection in mice with a targeted disruption in the interferon γ gene. J. Exp. Med. 178:1725.
53. Sarawar, S. R., R. D. Cardin, J. W. Brooks, M. Mehrpooya, A. M. Hamilton-Easton, X. Y. Mo, and P. C. Doherty. 1997. γ-Interferon is not essential for recovery from acute infection with murine gammaherpesvirus 68. J. Virol. 71:3916.
54. Bot, A., S. Bot, and C. A. Bona. 1998. Protective role of γ interferon during the recall response to influenza virus. J. Virol. 72:6637.