Coupling of antigen to cholera toxin for dendritic cell vaccination promotes the induction of MHC class I-restricted cytotoxic T cells and the rejection of a cognate antigen-expressing model tumor

European Journal of Immunology

Volumn 34, Issue 5, 2004, Pages 1272-1281

  Eriksson, Kristina ^a   Sun, Jia Bin ^a   Nordström, Inger ^a   Fredriksson, Margareta ^a   Lindblad, Marianne ^a   Li, Bin Ling ^a   Holmgren, Jan ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Cholera toxin; Cytotoxic T cells; Dendritic cells; Tumor immunity; Vaccination

Indexed keywords

B7 ANTIGEN; CD8 ANTIGEN; CD86 ANTIGEN; CHOLERA TOXIN; CHOLERA TOXIN B SUBUNIT; GAMMA INTERFERON; INTERLEUKIN 1BETA; MACROPHAGE INFLAMMATORY PROTEIN 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OVALBUMIN; PEPTIDE DERIVATIVE; PROSTAGLANDIN E2; RECEPTOR SUBUNIT; ANTIGEN; HLA ANTIGEN CLASS 1; IMMUNOTOXIN; VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN SPECIFICITY; ARTICLE; CELL ACTIVATION; CELL MATURATION; CELL MEDIATED CYTOTOXICITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; DRUG CONJUGATION; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE COUNT; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; SKIN LYMPHOMA; T LYMPHOCYTE ACTIVATION; TUMOR CELL; TUMOR MODEL; TUMOR REJECTION; VACCINATION; ANIMAL; DRUG EFFECT; IMMUNOLOGY; NEOPLASM;

ANIMALS; ANTIGENS; CHOLERA TOXIN; DENDRITIC CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNOTOXINS; MICE; NEOPLASMS; T-LYMPHOCYTES, CYTOTOXIC; VACCINES;

EID: 2942752015     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200324368     Document Type: Article

References (48)

1. Banchereau, J. and Steinman, R. M., Dendritic cells and the control of immunity. Nature 1998. 392: 245-252.
2. Mayordomo, J. I., Zorina, T., Storkus, W. J., Zitvogel, L., Celluzzi, C., Falo, L. D., Melief, C. J., Ildstad, S. T., Kast, W. M., Deleo, A. B. and Lotze, M. T., Bone marrow-derived dendritic cells pulsed with synthetic peptides elicit protective and therapeutic antitumour immunity. Nature Med. 1995. 1: 1297-1302.
3. Nestle, F. O., Alijagic, S., Dilliet, M., Sun, Y., Grabbe, S., Dummer, R., Burg, G. and Schadendorf, D., Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nature Med. 1998. 4: 328-332.
4. Porgador, A. and Gilboa, E., Bone marrow-derived dendritic cells pulsed with a class I-restricted peptide are potent inducers of cytotoxic T lymphocytes. J. Exp. Med. 1995. 182: 255-260.
5. Sornasse, T., Flamand, V., De Becker, G., Bazin, H., Thielemans, F., Thielemans, K., Urbain, J., Leo, O. and Moser, M., Antigen-pulsed dendritic cells efficiently induce an antibody response in vivo. J. Exp. Med. 1992. 175: 15-21.
6. Ludewig, B., Ehl, S., Karrer, U., Odermatt, B., Hengartner, H. and Zinkernagel, R. M., Dendritic cells efficiently induce protective antiviral immunity. J. Virol, 1998. 72: 3812-3818.
7. Porgador, A., Snyder, D. and Gilboa, E., Induction of antitumor immunity using bone marrow-generated dendritic cells. J. Immunol. 1996. 156: 2918-2926.
8. Schön, E., Harandi, A. M., Nordström, I., Holmgren, J. and Eriksson, K., Dendritic cell vaccination protects mice against lethality caused by genital herpes virus type 2 infection. J. Reprod. Immunol. 2001. 50: 87-106.
9. Steinman, R. M. and Dhodapkar, M., Active immunization against cancer with dendritic cells: the near future. Int. J. Cancer 2001. 94: 459-473.
10. Labeur, M. S., Roters, B., Pers, B., Mehling, A., Luger, T. A., Schwarz, T. and Grabbe, S., Generation of tumor immunity by bone marrow-derived dendritic cells correlates with dendritic cell maturation. J. Immunol. 1999. 162: 168-175.
11. Shibagaki, N. and Udey, M. C., Dendritic cells transduced with protein antigens induce cytotoxic lymphocytes and elicit antitumor immunity. J. Immunol. 2002. 168: 2393-2401.
12. Cho, H. J., Takabayashi, K., Cheng, P. M., Nguyen, M.-D., Corr, M., Tuck, S. and Raz, E., Immunostimulatory DNA-based vaccines induce cytotoxic lymphocyte activation by a T-helper cell-independent mechanism. Nature Biotech. 2000. 18: 509-514.
13. Jeannin, P., Renno, T., Goetsch, L., Miconnet, I, Aubry, J.-P., Delneste, Y., Herbault, N., Baussant, T., Magistrelli, G., Soulas, C., Romero, P., Cerottini, J.-C. and Bonnefoy, J.-Y., OmpA targets dendritic cells, induces their maturation and delivers antigen into the MHC class I presentation pathway. Nature Immunol. 2000. 1: 502-509.
14. Kim, T. S., Chung, S. W., Kim, S. H., Kang, S. N. and Kang, B. Y., Therapeutic anti-tumor response induced with epitope-pulsed fibroblasts genetically engineered for B7.1 expression and IFN-γ secretion. Int. J. Cancer 2000. 87: 427-433.
15. Bellone, M., Cantarella, D., Castiglione, P., Crosti, M. C., Ronchetti, A., Moro, M., Garancini, M. P., Casorati, G. and Dellabone, P., Relevance of the tumor antigen in the validation of three vaccination strategies for melanoma. J. Immunol. 2000. 165: 2651-2656.
16. Elson, C. O. and Ealding, W., Generalized systemic and mucosal immunity in mice after mucosal stimulation with cholera toxin. J. Immunol. 1984. 132: 2736-2741.
17. Lycke, N. and Holmgren, J., Strong adjuvant properties of cholera toxin on gut mucosal immune responses to orally presented antigens. Immunology 1986. 59: 301-308.
18. Pierce, N. F. and Gowans, J. L., The role of antigen form and function in the primary and secondary intestinal immune responses to cholera toxin and toxoid in rats. J. Exp. Med. 1978. 148: 195-206.
19. Lycke, N., Tsuij, T. and Holmgren, J., The adjuvant effect of Vibrio cholera and Escherichia coli heat-labile enterotoxins is linked to their ADP-ribosyltransferase activity. Eur. J. Immunol. 1992. 22: 2277-2281.
20. Braun, M. C., He, J., Wu, C.-Y. and Kelsall, B. L., Cholera toxin suppresses interleukin (IL)-12 production and IL-12 receptor β 1 and β2 chain expression. J. Exp. Med. 1999. 189: 541-552.
21. Gagliardi, M. C., Sallusto, F., Marinaro, M., Langenkamp, A., Lanzavecchia, A. and De Magistris, M. T., Cholera toxin induces maturation of human dendritic cells and licenses them for Th2 priming. Eur. J. Immunol. 2000. 30: 2394-2403.
22. Bagley, K. C., Abdelwahab, S. F., Tuskan, R. G., Fouts, T. R. and Lewis, G. K., Cholera toxin and heat-labile enterotoxin activate human monocyte-derived dendritic cells and dominantly inhibit cytokine production through a cyclic AMP-dependent pathway. Infect. Immun. 2002. 70: 5533-5539.
23. George-Chandy, A., Eriksson, K., Lebens, M., Nordström, I., Schön, E. and Holmgren, J., Cholera toxin B subunit as a carrier protein promotes antigen presentation and increases CD40 and CD86 expression on antigen-presenting cells. Infect. Immun. 2001. 69: 5716-5725.
24. Eriksson, K., Fredriksson, M., Nordström, I. and Holmgren, J., Cholera toxin and its B subunit promote dendritic cell vaccination with different influence on Th1/Th2 development. Infect. Immun. 2003. 71: 1740-1747.
25. De Haan, L., Hearn, A. R., Rivett, A. J. and Hirst, T. R., Enhanced delivery of exogenous peptides into the class I antigen processing and presentation pathway. Infect. Immun. 2002. 70: 3249-3258.
26. Moore, M. W., Carbone, F. R. and Bevan, M. J., Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 1988. 54: 777-785.
27. Helmich, B. K. and Dutton, R. W., The role of adoptively transferred CD8 T cells and host cells in the control of the growth of the EG7 thymoma: factors that determine the relative effectiveness and homing properties of Tc1 and Tc2 effectors. J. Immunol. 2001. 166: 6500-6508.
28. Dobrzanski, M. J., Reome, J. B. and Dutton, R. W., Therapeutic effects of tumor-reactive type 1 and type 2 CD8+ T cell subpopulations in established pulmonary metastases. J. Immunol. 1999. 162: 6671-6680.
29. Dalyot-Herman, N., Bathe, O. F. and Malek, T. R., Reversal of CD8+ T cell ignorance and induction of anti-tumor immunity by peptide-pulsed APC. J. Immunol. 2000. 165: 6731-6737.
30. Lencer, W. I., Hirst, T. R. and Holmes, R. K., Membrane traffic and the cellular uptake of cholera toxin. Biochim. Biophys. Acta 1999. 1450: 177-190.
31. Lavelle, E. C., McNeela, E., Armstrong, M. E., Leavy, O., Higgins, S. C. and Mills, K. H., Cholera toxin promotes the induction of regulatory T cells specific for bystander antigens by modulating dendritic cell activation. J. Immunol. 2003. 171: 2384-2392.
32. Jonuleit, H., Kuhn, U., Muller, G., Steinbrink, K., Paragnik, L., Schmitt, E., Knop, J. and Enk, A. H., Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur. J. Immunol. 1997. 27: 3135-3142.
33. Scandella, E., Men, Y., Gillessen, S., Förster, R. and Groettrup, M., Prostaglandin E2 is a key factor for CCR7 surface expression and migration of monocyte-derived dendritic cells. Blood 2002. 100: 1354-1361.
34. Luft, T., Jefford, M., Luetjens, P., Toy, T, Hochrein, H., Masterman, K. A., Maliszewski, C., Shortman, K., Cebon, J. and Maraskovsky, E., Functionally distinct dendritic cell (DC) populations induced by physiologic stimuli: prostaglandin E(2) regulates the migratory capacity of specific DC subsets. Blood 2002. 100: 1362-1372.
35. Rieser, C., Bock, G., Klocker, H., Bartsch, G. and Thurnher, M., Prostaglandin E2 and tumor necrosis factor alpha cooperate to activate human dendritic cells: synergistic activation of interleukin 12 production. J. Exp. Med. 1997. 186: 1603-1608.
36. Hörnquist, E. and Lycke, N., Cholera toxin adjuvant greatly promotes antigen priming of T cells. Eur. J. Immunol. 1993. 23: 2136-2143.
37. Kjerrulf, M., Grdic, D., Ekman, L., Schön, K., Vajdy, M. and Lycke, N., Interferon-γ receptor-deficient mice exhibit impaired gut mucosal immune responses but intact oral tolerance. Immunology 1997. 92: 60-68.
38. Sun, J. B., Holmgren, J. and Czerkinsky, C., Cholera toxin B subunit: An efficient transmucisal carrier-delivery system for induction of peripheral immunological tolerance. Proc. Natl. Acad. Sci. USA 1994. 91: 10795-10799.
39. Porgador, A., Staats, H. F., Faiola, B., Gilboa, E. and Palker, T. J., Intranasal immunization with CTL epitope peptides from HIV-1 or ovalbumin and the mucosal adjuvant cholera toxin induces peptide-specific CTL and protection against tumor development in vivo. J. Immunol. 1997. 158: 834-841.
40. Jang, M. H., Kweon, M. N., Hiroi, T., Yamamoto, M., Takahashi, I. and Kiyono, H., Induction of cytotoxic T lymphocyte responses by cholera toxin-treated bone marrow-derived dendritic cells. Vaccine 2003. 21: 1613-1619.
41. Okada, N., Tsujino, M., Hagiwara, Y., Tada, A., Tamura, Y., Mori, K., Sait, T., Nakagawa, S., Mayumi, T., Fujita, T. and Yamamoto, A., Administration route-dependent vaccine efficacy of murine dendritic cells pulsed with antigens. Br. J. Cancer 2001. 84: 1564-1570.
42. Lambert, L. A., Gibson, G. R., Maloney, M., Durell, B., Noelle, R. J. and Barth, R. J. Jr., Intranodal immunization with tumor lysate-pulsed dendritic cells enhances protective antitumor immunity. Cancer Res. 2001. 61: 641-646.
43. Hogquist, K. A., Jameson, S. C., Heath, W. R., Howard, J. L., Bevan, M. J. and Carbone, F. R., T cell receptor antagonist peptides induce positive selection. Cell 1994. 76: 17-27.
44. Fung-Leung, W.-P., Schilham, M. W., Rahemtulla, A., Kuendig, T. M., Vollenwieder, M., Potter, J., van Ewijk, W. and Mak, T. W., CD8 is needed for development of cytotoxic T cells but not helper T cells. Cell 1991. 65: 443-449.
45. Lebens, M., Johansson, S., Osek, J., Lindblad, M. and Holmgren, J., Large-scale production of Vibrio cholerae toxin B subunit for use in oral vaccines. Biotechnology 1993. 11: 1574-1578.
46. Rask, C., Holmgren, J., Fredriksson, M., Lindblad, M., Nordström, I., Sun, J.-B. and Czerkinsky, C., Prolonged oral treatment with low doses of allergen conjugated to cholera toxin B subunit suppresses immunoglobulin E antibody responses in sensitized mice. Clin. Exp. Allergy 2000. 30: 1024-1032.
47. Svennerholm, A.-M. and Holmgren, J., Identification of Escherichia coli heat-labile enterotoxin by means of a ganglioside immunosorbant assay (GM1-ELISA) procedure. Curr. Microbiol. 1978. 1: 19-23.
48. Beech, J. T., Bainbridge, T. and Thompson, S. J., Incorporation of cells into an ELISA system enhances antigen-driven lymphokine detection. J. Immunol. Methods 1997. 205: 163-168.