IL-10 controls ultraviolet-induced carcinogenesis in mice

Journal of Immunology

Volumn 179, Issue 1, 2007, Pages 365-371

  Loser, Karin ^a   Apelt, Jenny ^a   Voskort, Maik ^a   Mohaupt, Mariette ^b   Balkow, Sandra ^a   Schwarz, Thomas ^a,c   Grabbe, Stephan ^a,d   Beissert, Stefan ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c UNIVERSITY OF KIEL   (Germany)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNE RESPONSE; IMMUNOMODULATION; MOUSE; NONHUMAN; PHOTOCHEMISTRY; PRIORITY JOURNAL; RADIATION CARCINOGENESIS; REGULATORY T LYMPHOCYTE; SKIN CANCER; TH1 CELL; ULTRAVIOLET RADIATION;

EID: 34250813631     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.179.1.365     Document Type: Article

References (47)

1. Howe, H. L., P. A. Wingo, M. J. Thun, L. A. Ries, H. M. Rosenberg, E. G. Feigal, and B. K. Edwards. 2001. Annual report to the nation on the status of cancer (1973 through 1998), featuring cancers with recent increasing trends. J. Natl. Cancer Inst. 93: 824-842.
2. Slaper, H., G. J. Velders, J. S. Daniel, F. R. de Gruijl, and J. C. van der Leun. 1996. Estimates of ozone depletion and skin cancer incidence to examine the Vienna Convention achievements. Nature 384: 256-258.
3. Urbach, F. 1997. Ultraviolet radiation and skin cancer of humans. J. Photochem. Photobiol. B. 40: 3-7.
4. Setlow, R. B., E. Grist, K. Thompson, and A. D. Woodhead. 1993. Wavelengths effective in induction of malignant melanoma. Proc. Natl. Acad. Sci. USA 90: 6666-6670.
5. Urbach, F. 1991. Potential health effects of climatic change: effects of increased ultraviolet radiation on man. Environ. Health Perspect. 96: 175-176.
6. van der Leun, J. C., F. R. de Gruijl, M. Tevini, and R. C. Worrest. 1993. Ultraviolet carcinogenesis: environmental effects of ozone depletion. Recent Res. Cancer Res. 128: 263-267.
7. Boyle, J., R. M. MacKie, J. D. Briggs, B. J. Junor, and T. C. Aitchison. 1984. Cancer, warts, and sunshine in renal transplant patients: a case-control study. Lancet 1: 702-705.
8. Marshall, V. 1974. Premalignant and malignant skin tumours in immunosuppressed patients. Transplantation 17: 272-275.
9. O'Donovan, P., C. M. Perrett, X. Zhang, B. Montaner, Y. Z. Xu, C. A. Harwood, J. M. McGregor, S. L. Walker, F. Hanaoka, and P. Karran. 2005. Azathioprine and UVA light generate mutagenic oxidative DNA damage. Science 309: 1871-1874.
10. Norbury, K. C., and M. L. Kripke. 1978. Ultraviolet carcinogenesis in T-cell-depleted mice. J. Natl. Cancer Inst. 61: 917-921.
11. Fisher, M. S., and M. L. Kripke. 1978. Further studies on the tumor-specific suppressor cells induced by ultraviolet radiation. J. Immunol. 121: 1139-1144.
12. Fisher, M. S., and M. L. Kripke. 1982. Suppressor T lymphocytes control the development of primary skin cancers in ultraviolet-irradiated mice. Science 216: 1133-1134.
13. Schwarz, A., S. Beissert, K. Grosse-Heitmeyer, M. Gunzer, J. A. Bluestone, S. Grabbe, and T. Schwarz. 2000. Evidence for functional relevance of CTLA-4 in ultraviolet-radiation-induced tolerance. J. Immunol. 165: 1824-1831.
14. Simon, J. C., H. Hara, R. W. Denfeld, and S. Martin. 2002. UVB-irradiated dendritic cells induce nonproliferating, regulatory type T cells. Skin Pharmacol. Appl. Skin Physiol. 15: 330-334.
15. Shreedhar, V. K., M. W. Pride, Y. Sun, M. L. Kripke, and F. M. Strickland. 1998. Origin and characteristics of ultraviolet-B radiation-induced suppressor T lymphocytes. J. Immunol. 161: 1327-1335.
16. Loser, K., A. Scherer, M. B. Krummen, G. Varga, T. Higuchi, T. Schwarz, A. H. Sharpe, S. Grabbe, J. A. Bluestone, and S. Beissert. 2005. An important role of CD80/CD86-CTLA-4 signaling during photocarcinogenesis in mice. J. Immunol. 174: 5298-5305.
17. Schwarz, A., A. Maeda, M. K. Wild, K. Kernebeck, N. Gross, Y. Aragane, S. Beissert, D. Vestweber, and T. Schwarz. 2004. Ultraviolet radiation-induced regulatory T cells not only inhibit the induction but can suppress the effector phase of contact hypersensitivity. J. Immunol. 172: 1036-1043.
18. Grabbe, S., S. Bruvers, A. M. Lindgren, J. Hosoi, K. C. Tan, and R. D. Granstein. 1992. Tumor antigen presentation by epidermal antigen-presenting cells in the mouse: modulation by granulocyte-macrophage colony-stimulating factor, tumor necrosis factor α, and ultraviolet radiation. J. Leukocyte Biol. 52: 209-217.
19. Grabbe, S., S. Bruvers, R. L. Gallo, T. L. Knisely, R. Nazareno, and R. D. Granstein. 1991. Tumor antigen presentation by murine epidermal cells. J. Immunol. 146: 3656-3661.
20. Beissert, S., S. E. Ullrich, J. Hosoi, and R. D. Granstein. 1995. Supernatants from UVB radiation-exposed keratinocytes inhibit Langerhans cell presentation of tumor-associated antigens via IL-10 content. J. Leukocyte Biol. 58: 234-240.
21. Kim, J., R. L. Modlin, R. L. Moy, S. M. Dubinett, T. McHugh, B. J. Nickoloff, and K. Uyemura. 1995. IL-10 production in cutaneous basal and squamous cell carcinomas: a mechanism for evading the local T cell immune response. J. Immunol. 155: 2240-2247.
22. Dummer, W., B. C. Bastian, N. Ernst, C. Schanzle, A. Schwaaf, and E. B. Brocker. 1996. Interleukin-10 production in malignant melanoma: preferential detection of IL-10-secreting tumor cells in metastatic lesions. Int. J. Cancer 66: 607-610.
23. Dummer, W., J. C. Becker, A. Schwaaf, M. Leverkus, T. Moll, and E. B. Brocker. 1995. Elevated serum levels of interleukin-10 in patients with metastatic malignant melanoma. Melanoma Res. 5: 67-68.
24. Krüger-Krasagakes, S., K. Krasagakis, C. Garbe, E. Schmitt, C. Huls, T. Blankenstein, and T. Diamantstein. 1994. Expression of interleukin 10 in human melanoma. Br. J. Cancer 70: 1182-1185.
25. Richter, G., S. Krüger-Krasagakes, G. Hein, C. Huls, E. Schmitt, T. Diamantstein, and T. Blankenstein. 1993. Interleukin 10 transfected into Chinese hamster ovary cells prevents tumor growth and macrophage infiltration. Cancer Res. 53: 4134-4137.
26. Ding, W., S. Beissert, L. Deng, E. Miranda, C. Cassetty, K. Seiffert, K. L. Campton, Z. Yan, G. F. Murphy, J. A. Bluestone, and R. D. Granstein. 2003. Altered cutaneous immune parameters in transgenic mice overexpressing viral IL-10 in the epidermis. J. Clin. Invest. 111: 1923-1931.
27. Kühn, R., J. Löhler, D. Rennick, K. Rajewsky, and W. Müller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75: 263-274.
28. Kripke, M. L. 1977. Latency, histology, and antigenicity of tumors induced by ultraviolet light in three inbred mouse strains. Cancer Res. 37: 1395-1400.
29. Kripke, M. L., and M. S. Fisher. 1978. Immunologic aspects of tumor induction by ultraviolet radiation. Natl. Cancer Inst. Monogr. 179-183.
30. Beissert, S., H. T. He, A. O. Hueber, A. C. Lellouch, D. Metze, A. Mehling, T. A. Luger, T. Schwarz, and S. Grabbe. 1998. Impaired cutaneous immune responses in Thy-1-deficient mice. J. Immunol. 161: 5296-5302.
31. + T cells from murine spleen via nylon wool adherence and an optimized antibody cocktail. J. Immunol. Methods 258: 55-63.
32. Peto, R., M. C. Pike, P. Armitage, N. E. Breslow, D. R. Cox, S. V. Howard, N. Mantel, K. McPherson, J. Peto, and P. G. Smith. 1977. Design and analysis of randomized clinical trials requiring prolonged observation of each patient, II: analysis and examples. Br. J. Cancer 35: 1-39.
33. Kripke, M. L. 1974. Antigenicity of murine skin tumors induced by ultraviolet light. J. Natl. Cancer Inst. 53: 1333-1336.
34. Elmets, C. A., P. R. Bergstresser, R. E. Tigelaar, P. J. Wood, and J. W. Streilein. 1983. Analysis of the mechanism of unresponsiveness produced by haptens painted on skin exposed to low dose ultraviolet radiation. J. Exp. Med. 158: 781-794.
35. Toews, G. B., P. R. Bergstresser, and J. W. Streilein. 1980. Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follows skin painting with DNFB. J. Immunol. 124: 445-453.
36. Ziegler, S. F. 2006. FOXP3: of mice and men. Annu. Rev. Immunol. 24: 209-226.
37. Kripke, M. L. 1977. Ultraviolet radiation and tumor immunity. J. Reticuloendothel. Soc. 22: 217-222.
38. Shreedhar, V., T. Giese, V. W. Sung, and S. E. Ullrich. 1998. A cytokine cascade including prostaglandin E2, IL-4, and IL-10 is responsible for UV-induced systemic immune suppression. J. Immunol. 160: 3783-3789.
39. Ullrich, S. E. 1985. Suppression of lymphoproliferation by hapten-specific suppressor T lymphocytes from mice exposed to ultraviolet radiation. Immunology 54: 343-352.
40. Beissert, S., J. Hosoi, R. Kühn, K. Rajewsky, W. Muller, and R. D. Granstein. 1996. Impaired immunosuppressive response to ultraviolet radiation in interleukin-10-deficient mice. J. Invest. Dermatol. 107: 553-557.
41. Ullrich, S. E. 1995. Modulation of immunity by ultraviolet radiation: key effects on antigen presentation. J. Invest. Dermatol. 105: 30S-36S.
42. Ullrich, S. E. 1995. The role of epidermal cytokines in the generation of cutaneous immune reactions and ultraviolet radiation-induced immune suppression. Photochem. Photobiol. 62: 389-401.
43. Ullrich, S. E. 1994. Mechanism involved in the systemic suppression of antigen-presenting cell function by UV irradiation: keratinocyte-derived IL-10 modulates antigen-presenting cell function of splenic adherent cells. J. Immunol. 152: 3410-3416.
44. Moodycliffe, A. M., D. Nghiem, G. Clydesdale, and S. E. Ullrich. 2000. Immune suppression and skin cancer development: regulation by NKT cells. Nat. Immunol. 1: 521-525.
45. Beissert, S., J. A. Bluestone, I. Mindt, M. Voskort, D. Metze, A. Mehling, T. A. Luger, T. Schwarz, and S. Grabbe. 1999. Reduced ultraviolet-induced carcinogenesis in mice with a functional disruption in B7-mediated costimulation. J. Immunol. 163: 6725-6731.
46. Hock, H., M. Dorsch, U. Kunzendorf, Z. Qin, T. Diamantstein, and T. Blankenstein. 1993. Mechanisms of rejection induced by tumor cell-targeted gene transfer of interleukin 2, interleukin 4, interleukin 7, tumor necrosis factor, or interferon γ. Proc. Natl. Acad. Sci. USA 90: 2774-2778.
47. Qin, Z., H. J. Kim, J. Hemme, and T. Blankenstein. 2002. Inhibition of methylcholanthrene-induced carcinogenesis by an interferon γ receptor-dependent foreign body reaction. J. Exp. Med. 195: 1479-1490.