Abstract
Irradiation with ultraviolet B (UVB; 290–320 nm) initiates systemic immunosuppression of contact hypersensitivity (CHS). UV dose-responses for suppression of CHS to trinitrochlorobenzene were established in 18 strains of inbred mice. Three phenotypes with significantly different susceptibilities to UV suppression were identified. The phenotypes were: high (HI) susceptibility, 50% suppression with 0.7–2.3 kJ/m2 UV (C57BL/6, C57BL/10, and C57L and NZB females); low (LO) susceptibility, 50% suppression with 9.6–12.3 kJ/m2 UV (BALB/c, AKR, SJL and NZW), and intermediate (INT) susceptibility, 50% suppression with 4.7–6.9 kJ/m2 UV (DBA/2, C57BR, C3H/HeJ, C3H/HeN, CBA/N and A/J). UV suppression was not correlated with skin pigmentation or with the magnitude of the CHS response in non-irradiated animals. Major histocompatibility complex (MHC) haplotype was not correlated with UV suppression in MHC congenic strains B10.D2/oSnJ, B10.D2/nSnJ, B10.BR/SgSnJ, and A.BY/SnJ. There were no sex differences in UV suppression in BALB/c, C57BL/6, or NZW animals. In the autoimmune NZB strain, however, male mice (LO) were seven times less sensitive to UV suppression than NZB female mice (HI). Both sexes of (NZB × NZW)F1 and (NZW × NZB)F1 mice were HI, supporting dominance of HI over LO. Thus there are genetic factors and interacting sex-limited factors determining susceptibility to UV suppression. These findings may be of relevance to UV-related diseases such as photosensitive lupus and skin cancer.
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Armstrong, B. K. and English, D. R. Epidemiologic studies. In C. M. Balch, A. N. Houghton, G. W. Milton, A. J. Sober, and S.-J. Soongs (eds.): Cutaneous Melanoma: Second Edition, pp. 12–26, J. B. Lippincott, Philadelphia, 1992.
Asherson, G. L., Zembala, M., and Barnes, R. M. R. The mechanism of immunological unresponsiveness to picryl chloride and the possible role of antibody mediated depression. Clin Exp Immunol 9: 111–121, 1971
Cooper, K. D., Oberhelman, L., Hamilton, T. A., Baadsgaard, O., Terhune, M., LeVee, G., Anderson, T., and Koren, H. UV expossure reduced immunization rates and promotes tolerance to epicutaneous antigens in humans-relationship to dose, CD1a-DR+ epidermal macrophage induction and Langerhans cell depletion. Proc Natl Acad Sci USA 89: 8497–8501, 1992
Crow, M. K. and Christian, C. L. Etiologic hypotheses for systemic lupus erythematosus. In R. G. Lahita (ed.): Systemic Lupus Erythematosus, pp 51–64, Churchill Livingstone, New York, 1992
Daynes, R. A. and Spellman, C. W. Evidence for the generation of suppressor cells by ultraviolet radiation. Cell Immunol 31: 182–187, 1977
De Fabo, E. C. and Kripke, M. L. Dose-response characteristics of immunologic unresponsiveness to UV-induced tumors produced by UV irradiation of mice. Photochem Photobiol 30: 385–390, 1979
De Fabo, E. C. and Kripke, M. L. Wavelength dependence and dose-rate independence of UV radiation induced suppression of immunologic unresponsiveness of mice to a UV-induced fibrosarcoma. Photochem Photobiol 32: 183–188, 1980
De Fabo, E. C. and Noonan, F. P. Mechanism of immune suppression by ultraviolet irradiation in vivo. I. Evidence for the existence of a unique photoreceptor in skin and its role in photoimmunology. J Exp Med 158: 84–98, 1983
De Fabo, E. C., Noonan, F. P., and Frederick, J. E. Biologically effective doses of sunlight for immune suppression at various latitudes and their relationship to changes in stratospheric ozone. Photochem Photobiol 52: 811–817, 1990
Fisher, M. S. and Kripke, M. L. Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis. Proc Natl Acad Sci USA 34: 1688–1692, 1977
Fisher, M. S. and Kripke, M. L. Suppressor T lymphocytes control the development of primary skin cancers in ultraviolet irradiated mice. Science 216: 1133–1134, 1982
Giannini, M. S. H. Suppression of pathogenesis in cutaneous Leishmaniasis by UV irradiation. Infect Immun 51: 838–843, 1986
Hersey, P., Hasic, E., Edwards, A., Bradley, M., and Haran, G. Immunological effects of solarium exposure. Lancet 1: 545–548, 1983
Hoffman, H. A. Genetic quality control in the laboratory mouse (Mus musculus). In H. C. Morse, III (ed.): Origins of Inbred Mice, pp. 217–234, Academic Press, New York, 1978
Howie, S. E. M., Norval, M., and Maingay, J. Exposure to low-dose ultraviolet radiation suppresses delayed-type hypersensitivity to Herpes Simplex in mice. J Invest Dermatol 86: 125–128, 1986
Kalimo, K., Koulu, L., and Jansen, C. T. Effect of a single UVB or PUV A exposure on immediate and delayed skin hypersensitivity reactions in humans. Arch Dermatol Res 275: 374–378, 1983
Kochevar, I. E. Action spectrum and mechanisms of UV radiation-induced injury in Lupus Erythematosus. J Invest Dermatol 85: 140s–143s, 1985
Lee, J. A. H. Epidemiology of malignant melanoma. In N. Kirkham, D. W. K. Cotton, R. C. Lallemand, J. E. White, and R. D. Rosins (eds.): Diagnosis and Management of Melanoma in Clinical Practice, pp. 1–9, Springer-Verlag, London Berlin Heidelberg, 1992
Mottram, P. L., Mirosklavos, A., Clunie, G. J. A., and Noonan, F. P. A Single dose of UV radiation suppressed delayed type hypersensitivity responses to alloantigens and prolongs heart allograft acceptance in mice. Immunol Cell Biol 66: 377–385, 1988
Noonan, F. P. and De Fabo, E. C. Ultraviolet-B dose-response curves for local and systemic immunosuppression are identical. Photochem Photobiol 52: 801–810, 1990
Noonan, F. P. and De Fabo, E. C. Immunosuppression by ultraviolet B radiation: initiation by urocanic acid. Immunol Today 13: 250–254, 1992
Noonan, F. P., De Fabo, E. C., and Kripke, M. L. Suppression of contact hypersensitivity by UV radiation and its relationship to UV-induced suppression of tumor immunity. Photochem Photobiol 34: 683–690, 1981a
Noonan, F. P., De Fabo, E. C., and Kripke, M. L. Suppression of contact hypersensitivity by ultraviolet radiation: an experimental model. Springer Semin Immunopathol 4: 293–304, 1981b
Parish, C. R. The relationship between humoral and cell-mediated immunity. Transplant Rev 13: 35–66, 1972
Quevedo, W. C., Fitzpatrick, T. B., Szabo, G., and Jinbow, K. Biology of melanocytes. In T. B. Fitzpatrick, A. Z. Eisen, K. Wolff, I. M. Freedberg, and K. F. Austens (eds.): Dermatology in General Medicine, pp. 224–251, McGraw-Hill, New York, 1987
Raveche, E. S., Tjio, J. H., Boegel, W., and Steinberg, A. D. Studies of the effects of sex hormones and X-linked genetic control of induced and spontaneous antibody production. Arthritis Rheum 22: 1177–1187, 1979
Roubinian, J. R., Paporan, R., and Talal, N. Androgenic hormones modulate autoantibody responses and improve survival in murine lupus. J Clin Invest 59: 1066–1070, 1977
Schultz, L. D. and Bailey, D. W. Genetic controlof contact sensitivity in mice: effect of H-2 and non H-2 loci. Immunogenetics 1: 570–583, 1975
Snedecor, G. W. and Cochran, W. G. Statistical Methods, Ch. 4, 14, pp. 160–164, 432–436, Iowa State University Press, Ames, 1967
Streilein, J. W. and Bergstresser, P. R. Genetic basis of ultraviolet B effects on contact hypersensitivity. Immunogenetics 27: 252–258, 1988
Theofilopoulos, A. N. Murine models of lupus. In R. G. Lahita (ed.): Systemic lupus erythematosus, pp. 121–194, Churchill Livingstone, New York, 1992
Vermeer, M., Schmieder, G. J., Yoshikawa, T., van den Berg, J.-W., Metzman, M. S., Taylor, J. R., and Streilein, J. W. Effects of ultraviolet B light on cutaneous immune responses of humans with deeply pigmented skin. J Invest Dermatol 97: 729–734, 1991
Wolfe, H. G. and Coleman, D. L. Pigmentation. In E. L. Green (ed.): Biology of the Laboratory Mouse, pp. 405–425, Dover, New York, 1966
Yasumoto, S., Hayashi, Y., and Aurelian, L. Immunity to Herpes simplex virus Type 2. Suppression of virus-induced immune responses in ultraviolet B-irradiated mice. J Immunol 139: 2788–2793, 1987
Yoshikawa, T. and Streilein, J. W. Genetic basis of the effects of ultraviolet light B on cutaneous immunity. Evidence that polymorphism at Tnfa and Lps loci governs susceptibility. Immunogenetics 32: 398–405, 1990
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Correspondence to: F. P. Noonan.
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Noonan, F.P., Hoffman, H.A. Susceptibility to immunosuppression by ultraviolet B radiation in the mouse. Immunogenetics 39, 29–39 (1994). https://doi.org/10.1007/BF00171794
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DOI: https://doi.org/10.1007/BF00171794