Abstract
Skin exposure to solar ultraviolet radiation (UVR) has been a major public concern because of its genotoxicity. We established recently three action spectra of UVR biological effects using inflammation, mutagenicity, and mutation induction suppression (MIS) as indicators to evaluate UVR risk for mammalian skin. MIS is an antigenotoxic epidermis-specific response by which the increase of the mutant frequency (MF) levels off above a certain UVR dose. Here, based on these spectra, the mutation load of the skin after sunlight exposure was evaluated utilizing the spectral solar-UVR intensity data which had been measured at Tsukuba, Japan by the Japan Meteorological Agency. We estimated the daily variation of the solar-UVR effectiveness (effect per second) for the three indicators, and revealed that the effectiveness efficiency (effect per dose) of midday sunlight is 3–4-fold higher than those in the early morning and late afternoon. Based on the daily variations of mutagenicity and MIS effectiveness, we further estimated MFs induced after every one-hour sunlight exposure and reached a remarkable prediction that MFs should be suppressed to a constant level during 9:00–15:00 by MIS. The estimates agreed well with the equivalent values directly determined at Sendai, a site close to Tsukuba, although a small difference was detected for the epidermis at the dose range where the suppressed MFs were predicted. We propose the use of observed minimum inflammation/erythema doses to improve the difference. Our method could provide reliable estimates of sunlight genotoxicity to evaluate skin cancer probabilities.
Similar content being viewed by others
References
J. A. Parrish, K. F. Jaenicke, R. R. Anderson, Erythema and melanogenesis action spectra of normal human skin, Photochem. Photobiol., 1982, 36, 187–191.
A. F. McKinlay, B. L. Diffey, A reference action spectrum for ultra-violet induced erythema in human skin, CIE J., 1987, 6, 17–22.
A. Morita, Y. Shintani, E. Nishida, H. Kato, H. Yoshida, M. Minamoto, Y. Yamaguchi, A. Maeda, Feasibility and accuracy of a newly developed hand-held device with a flat-type fluorescent lamp for measuring the minimal erythema dose for narrow-band UVB therapy, Photodermatol. Photoimmunol. Photomed., 2009, 25, 41–44.
R. L. McKenzie, P. J. Aucamp, A. F. Bais, L. O. Björn, M. Ilyas, S. Madronich, Ozone depletion and climate change: impacts on UV radiation, Photochem. Photobiol. Sci., 2011, 10, 182–198.
H. Ikehata, S. Higashi, S. Nakamura, Y. Daigaku, Y. Furusawa, Y. Kamei, M. Watanabe, K. Yamamoto, K. Hieda, N. Munakata, T. Ono, Action spectrum analysis of UVR genotoxicity for skin: the border wavelengths between UVA and UVB can bring serious mutation loads to skin, J. Invest. Dermatol., 2013, 133, 1850–1856.
G. P. Pfeifer, Formation and processing of UV photoproducts: effects of DNA sequence and chromatin environment, Photochem. Photobiol., 1997, 65, 270–283.
H. Ikehata, T. Ono, The mechanisms of UV mutagenesis, J. Radiat. Res., 2011, 52, 115–125.
N. M. Wikonkal, D. E. Brash, Ultraviolet radiation induced signature mutations in Photocarcinogenesis, J. Invest. Dermatol. Symp. Proc., 1999, 4, 6–10.
S. E. Freeman, H. Hacham, R. W. Gange, D. J. Maytum, J. C. Sutherland, B. M. Sutherland, Wavelength dependence of pyrimidine dimer formation in DNA of human skin irradiated in situ with ultraviolet light, Proc. Natl. Acad. Sci. U. S. A., 1989, 86, 5605–5609.
A. R. Young, C. A. Chadwick, G. I. Harrison, O. Nikaido, J. Ramsden, C. S. Potten, The similarity of action spectra for thymine dimers in human epidermis and erythema suggests that DNA is the chromophores for erythema, J. Invest. Dermatol., 1998, 111, 982–988.
F. R. de Gruijl, H. J. C. M. Sterenborg, P. D. Forbes, R. E. Davies, C. Cole, G. Kelfkens, H. Van Weelden, H. Slaper, J. C. Van der Leun, Wavelength dependence of skin cancer induction by ultraviolet irradiation of albino hairless mice, Cancer Res., 1993, 53, 53–60.
H. Ikehata, T. Ono, Mutation induction with UVB in mouse skin epidermis is suppressed in acute high-dose exposure, Mutat. Res., 2002, 508, 41–47.
H. Ikehata, S. Nakamura, T. Asamura, T. Ono, Mutation spectrum in sunlight-exposed skin epidermis: small but appreciable contribution of oxidative stress-induced mutagenesis, Mutat. Res., 2004, 556, 11–24.
J. A. Gossen, W. J. de Leeuw, C. H. Tan, E. C. Zwarthoff, F. Berends, P. H. M. Lohman, D. L. Knook, J. Vijg, Efficient rescue of integrated shuttle vectors from transgenic mice: a model for studying mutations in vivo, Proc. Natl. Acad. Sci. U. S. A., 1989, 86, 7971–7975.
G. Seckmeyer, R. L. Mckenzie, Increased ultraviolet radiation in New Zealand (45° S) relative to Germany (48° N), Nature, 1992, 359, 135–137.
N. Munakata, F. Morohoshi, K. Hieda, K. Suzuki, Y. Furusawa, H. Shimura, T. Ito, Experimental correspondence between spore dosimetry and spectral photometry of solar ultraviolet radiation, Photochem. Photobiol., 1996, 63, 74–78.
H. Ikehata, R. Okuyama, E. Ogawa, S. Nakamura, A. Usami, T. Mori, K. Tanaka, S. Aiba, T. Ono, Influences of p53 deficiency on the apoptotic response, DNA damage removal and mutagenesis in UVB-exposed mouse skin, Mutagenesis, 2010, 25, 397–405.
D. E. Godar, Light and death: photons and apoptosis, J. Invest. Dermatol. Symp. Proc., 1999, 4, 17–23.
C. Pourzand, R. M. Tyrell, Apoptosis, the role of oxidative stress and the example of solar UV radiation, Photochem. Photobiol., 1999, 70, 380–390.
L. F. Z. Batista, B. Kaina, R. Meneghini, C. F. M. Menck, How DNA lesions are turned into powerful killing structures: insights from UV-induced apoptosis, Mutat. Res., 2009, 681, 197–208.
H. E. Johns, M. L. Pearson, C. LeBlanc, C. W. Helleiner, The ultraviolet photochemistry of thymidylyl-(3′ → 5′)-thymidine, J. Mol. Biol., 1964, 9, 503–524.
J.-S. Taylor, M. P. Cohrs, DNA, light, and Dewar pyrimidones: the structure and biological significance of TpT3, J. Am. Chem. Soc., 1987, 109, 2834–2835.
R. B. Setlow, The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis, Proc. Natl. Acad. Sci. U. S. A., 1974, 71, 3363–3366.
W. A. G. Bruls, H. Slaper, J. C. Van der Leun, L. Berrens, Transmission of human epidermis and stratum corneum as a function of thickness in the ultraviolet and visible wavelengths, Photochem. Photobiol., 1984, 40, 485–494.
I. C. Enninga, R. T. L. Groenendijk, A. R. Filon, A. A. Van Zeeland, J. W. I. M. Simons, The wavelength dependence of UV-induced pyrimidine dimer formation, cell killing and mutation induction in human diploid skin fibroblasts, Carcinogenesis, 1986, 7, 1829–1836.
C. A. Jones, E. Huberman, M. L. Cunningham, M. J. Peak, Mutagenesis and cytotoxicity in human epithelial cells by far- and near-ultraviolet radiations: action spectra, Radiat. Res., 1987, 110, 244–254.
R. M. Tyrell, M. Pidoux, Action spectra for human skin cells: estimates of the relative cytotoxicity of the middle ultraviolet, near ultraviolet, and violet regions of sunlight on epidermal keratinocytes, Cancer Res., 1987, 47, 1825–1829.
F. R. de Gruijl, J. C. Van der Leun, Estimate of the wavelength dependency of ultraviolet carcinogenesis in humans and its relevance to the risk assessment of a stratospheric ozone depletion, Health Phys., 1994, 67, 319–325.
C. Kielbassa, L. Roza, B. Epe, Wavelength dependence of oxidative DNA damage induced by UV and visible light, Carcinogenesis, 1997, 18, 811–816.
N. Munakata, S. Kazadzis, A. F. Bais, K. Hieda, G. Rontó, P. Rettberg, G. Horneck, Comparisons of spore dosimetry and spectral photometry of solar-UV radiation at four sites in Japan and Europe, Photochem. Photobiol., 2000, 72, 739–745.
M. Aoki, Y. Furusawa, S. Higashi, M. Watanabe, Action spectra of apoptosis induction and reproductive cell death in L5178Y cells in the UV-B region, Photochem. Photobiol. Sci., 2004, 3, 268–272.
Author information
Authors and Affiliations
Corresponding author
Additional information
Electronic supplementary information (ESI) available.
Rights and permissions
About this article
Cite this article
Ikehata, H., Munakata, N. & Ono, T. Skin can control solar UVR-induced mutations through the epidermis-specific response of mutation induction suppression. Photochem Photobiol Sci 12, 2008–2015 (2013). https://doi.org/10.1039/c3pp50158b
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1039/c3pp50158b