Abstract
The purpose of this study was to compare fluence-response relationships for the production of cyclobutane pyrimidine dimers in epidermal or dermal DNA of platyfishXiphophorus hybrids irradiated with UVB, and to determine photoreactivation from black light on dimers producedin situ. This was accomplished by quantitative gel electrophoresis of unlabeled DNA following extraction of the DNA and treatment with an enzyme specific for the detection of pyrimidine dimers. The dermis was the target tissue for UV-induced DNA damage inXiphophorus hybrid fish skin. Shapes of dimer-fluence response data following filtered sunlamp irradiation (λ > 290 nm) or monochromatic wavelength 302 nm in the epidermis or dermis were different. In the epidermis there was an initial steep upward slope followed by a plateau, whereas in the dermis a linear relationship was observed. The final values of dimers at the high doses were, however, nearly equal in the epidermis and dermis exposed to either radiation. These differences in fluence-response relationships are probably attributable to the intertwining of the epidermis and to the shielding effect of the epidermal layer, with scales leading to a heterogenous population of cells which are exposed to different UV doses. Photoreversal of dimers was readily observed by black light irradiation in both epidermis and dermis irradiated with eitherλ > 290 nm or 302 nm.
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References
Achey PM, Woodhead AD, Setlow RB (1979) Photoreactivation of pyrimidine dimers in DNA from thyroid cells of the teleostPoecilia formosa. Photochem Photobiol 29:305–310
Ahmed FE, Setlow RB (1979) Saturation of DNA repair in mammalian cells. Photochem Photobiol 29:983–989
Ahmed FE, Setlow RB (1992) DNA damage and repair inXiphophorus fish skin exposed to UV. In: Abstracts of 11th International Congress on Photobiology, 7–12 September, Kyoto, Japan, p 203
Anders A, Anders F (1978) Etiology of cancer as studied in the platyfish-swordtail system. Biochem Biophys Acta 516:61–95
Anders F, Schartl M, Barenkow A, Anders A (1984)Xiphophorus as an in vivo model for studies on normal and defective control of oncogenes. Adv Cancer Res 42:191–275
Brash DE (1988) UV mutagenic photoproducts inEscherichia coli and human cells: a molecular genetics prespective on human skin cancer. Photochem Photobiol 48:59–66
Carrier WL, Setlow RB (1970) Endonuclease fromMicrococcus luteus which has activity towards ultraviolet irradiated deoxyribonucleic acid: purification and properties. J Bacteriol 102:178–186
Chen C-Z, Sutherland JC (1989) Gel electrophoresis method for quantitation of gamma ray induced single- and double-strand breaks in DNA irradiated in vitro. Electrophoresis 10:318–326
Cleaver JE, Cortes F, Karentz D, Lutze LH, Morgan WF, Player AN, Vuksanovic L, Mitchelle D (1988) The relative biological importance of cyclobutane and (6-4) pyrimidine-pyrimidone dimer photoproducts in human cells: evidence from a xeroderma pigmentosum revertant. Photochem Photobiol 48:41–49
Concar D (1992) The resistible rise of skin cancer. New Sci 1821:23–28
Ehmann UK, Lett JT (1973) Review and evaluation of molecular weight calculations from the sedimentation profiles of irradiated DNA. Radiat Res 54:152–162
Elkind MM, Han A, Chang-Liu C-M (1978) “Sunlight”-induced mammalian cell killing: a comparative study of ultraviolet and near-ultraviolet inactivation. Photochem Photobiol 27:709–715
Fedoroff N, Wellauer PK, Wall R (1977) Intermolecular duplexes in heterogenous nuclear RNA from HeLa cells. Cell 10:597–610
Freeman SE, Blackett AD, Monteleone DC, Setlow RB, Sutherland BM, Sutherland JC (1986) Quantitation of radiation-, chemical-, or enzyme-induced single strand breaks in nonradioactive DNA by alkaline gel electrophoresis: application to pyrimidine dimers. Anal Biochem 158:119–129
Gordon M (1928) Pigment inheritance in the Mexican killifish. J Hered 19:551–556
Hansen MF, Cavenee WK (1987) Genetics of cancer predisposition. Cancer Res 47:5518–5527
Hariharan PV, Cerutti PA (1977) Formation of products of the 5,6- dihydroxy dihydrothymine type by ultraviolet light in HeLa cells. Biochemistry 16:2791–2795
Hart RW, Setlow RB, Woodhead AD (1977) Evidence that pyrimidine dimers in DNA can give rise to tumors. Proc Natl Acad Sci USA 74:5574–5578
Häussler G (1928) Über Melanombildungen bei Bastarden vonXiphophorus maculatus undPlatypoecilus maculatus var. rubra. Klin Wochenschr 7:1561–1562
Hill HZ (1992) The function of melanin, or six blind people examine an elephant. BioEssay 14:49–56
Jagger J (1985) Solar-UV action on living cells. Prager Scientific, New York, p 115
Kallman KD (1975) The platyfish,Xiphophorus maculatus. In: King RC (ed) Handbook of genetics. Plenum Press, New York, pp 81–132
Kantor GJ, Setlow RB (1982) Correlation between inactivation of human cells and numbers of pyrimidine dimers induced by a sun lamp and 254 nm radiation. Photochem Photobiol 35:269–274
Kosswig C (1928) Über Kreuzungen zwischen den TeleostiernXiphophorus helleri undPlatypoecilus maculatus. Z Indukt Abstammungs Vererbungsl 47:150–158
Kripke ML, Fisher MS (1976) Immunologic parameters of ultraviolet carcinogenesis. J Natl Cancer Inst 57:211–215
Ley RD, Applegate LA, Padilla RS, Stuart TD (1989) Ultraviolet radiation-induced malignant melanoma inMonodelphis domestica. Photochem Photobiol 50:1–5
Matsunaqa T, Kotaro H, Nikaido O (1991) Wavelength dependent formation of thymine dimers and (6-4) photoproducts in DNA by monochromatic ultraviolet light ranging from 150 to 365 nm. Photochem Photobiol 54:403–410
Mitchell DL (1988) The relative cytotoxicity of (6-4) photoproducts and cyclobutane dimers in mammalian cells. Photochem Photobiol 48:51–57
Paterson MC (1978) Use of purified lesion-recognizing enzymes to monitor DNA repair in vivo. Adv Radiat Biol 7:1–53
Powers DA (1989) Fish as model systems. Science 246:352–358
Roberts RJ (1978) Fish pathology. Bailliere Tindall, London, p 15
Rosenstein BS, Mitchell DL (1987) Action spectra for the induction of pyrimidine (6–4) pyrimidone photoproducts and cyclobutane pyrimidine dimers in normal human skin fibroblasts. Photochem Photobiol 45:775–780
Rothman RH, Setlow RB (1979) An action spectrum for cell killing and pyrimidine dimer formation in Chinese hamster V-79 cells. Photochem Photobiol 29:57–61
Rupert CS (1975) Enzymatic photoreactivation: overview. In: Hanawalt PC, Setlow RB (eds) Molecular mechanisms for repair. Plenum Press, New York, pp 73–87
Schwab M (1989) Genetic principles of tumor suppression. Biochim Biophys Acta 939:49–64
Schwab M, Kollinger G, Haas J, Ahuja MR, Abdo S, Anders A, Anders F (1979) Genetic basis of susceptibility to neuroblastoma following treatment withN-methyl-N-nitrosourea and X-rays inXiphophorus. Cancer Res 39:519–526
Scott EL, Straf ML (1977) Ultraviolet radiation as a cause of cancer. In: Hiatt HH, Watson JD, Winsten JA (eds) Origins of human cancer, book A: incidence of cancer in humans. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y., pp 529–546
Setlow RB (1968) Photoproducts in DNA irradiated in vivo. Photochem Photobiol 7:643–649
Setlow RB (1974) The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc Natl Acad Sci USA 71:3363–3366
Setlow RB, Woodhead AD, Grist E (1989) Animal model for ultraviolet radiation-induced melanoma: platyfish-swordtail hybrid. Proc Natl Acad Sci USA 86:8922–8926
Shima A, Setlow RB (1984) Survival and pyrimidine dimers in cultured fish cells exposed to concurrent sunlamp ultraviolet and photoreactivating radiations. Photochem Photobiol 39:49–56
Smith PJ, Paterson MC (1981) Abnormal responses to mid-ultraviolet light of cultured fibroblasts from patients with disorders featuring sunlight sensitivity. Cancer Res 41:511–518
Sutherland BM, Delihas NC, Oliver RP, Sutherland J (1981) Action spectra for ultraviolet light-induced transformation of human cells to anchorage-independent growth. Cancer Res 41:2211–2214
Sutherland BM, Hacham H, Gange RW, Maytum D, Sutherland JC (1990) DNA damage and repair in human skin: pathways and questions. In: Sutherland M, Woodhead AD (eds) DNA damage and repair in human tissues. Plenum Press, New York, pp 149–160
Sutherland JC, Sutherland BM, Emrick A, Monteleone DC, Ribeiro EA, Trunk J, Son M, Serwer P, Poddar SK, Maniloff J (1991) Quantitative electronic imaging of gel fluorescence with CDC cameras: applications in molecular biology. BioTechniques 10:492–497
Urbach F (1975) Ultraviolet radiation and skin cancer. In: Smith KC (ed) Topics in photomedicine. Plenum Press, New York, pp 39–142
Vielkind JR, Kallman KD, Morizot DC (1989) Genetics of melanoma inXiphophorus fishes. J Aquat Anim Health 1:69–77
Woodhead AC, Achey P, Setlow RB, Grist E (1978) Photoenzymatic repair of ultraviolet-irradiated DNA in the cells of a shark,Prionace gluca. Biochem Physiol 60B:205–208
Zechel CU, Schlenbecker U, Anders A, Anders F (1988) v-erb B related sequences inXiphophorus that map to melanoma determining Mendelian loci and overexpress in a melanoma cell line. Oncogene 3:605–617
Zelle B, Reynolds RJ, Kottenhagen MJ, Schuite A, Lohman PHM (1980) The influence of the wavelength of ultraviolet radiation on survival, mutation induction and repair in irradiated Chinese hamster cells. Mutat Res 72:491–509
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This research was supported by the Office of Health and Environmental Research of the U.S. Department of Energy
The author is recipient of the National Academy of Sciences' Kobelt Fund Grant
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Ahmed, F.E. Different rates of ultraviolet-induced DNA damage in the epidermis and dermis of a platyfish model for carcinogenesis. Radiat Environ Biophys 32, 259–270 (1993). https://doi.org/10.1007/BF01209775
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DOI: https://doi.org/10.1007/BF01209775