Mutation spectrum in sunlight-exposed mouse skin epidermis: Small but appreciable contribution of oxidative stress-mediated mutagenesis

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 556, Issue 1-2, 2004, Pages 11-24

  Ikehata, Hironobu ^a   Nakamura, Shingo ^a,b   Asamura, Takaaki ^a   Ono, Tetsuya ^a  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b INSTITUTE FOR ENVIRONMENTAL SCIENCES   (Japan)

Author keywords

Muta mouse; Mutation; Skin cancer; Sunlight; UV

Indexed keywords

ADENINE NUCLEOTIDE; BASE; PYRIMIDINE NUCLEOTIDE; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CPG ISLAND; DERMIS; EPIDERMIS; GENE; GENE FREQUENCY; GENE ISOLATION; GENE MUTATION; GENETIC ASSOCIATION; GENOTOXICITY; IRRADIATION; JAPAN; LACZ GENE; MAMMAL; METHYLATION; MOUSE; MUTAGENESIS; MUTANT; MUTATION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; RADIATION DOSE; RADIATION INJURY; SKIN; SKIN INFLAMMATION; SPECTRUM; SUMMER; SUN EXPOSURE; SUNLIGHT; TIME; TRANSGENE; TRANSGENIC MOUSE; ULTRAVIOLET A RADIATION; ULTRAVIOLET B RADIATION;

ANIMALS; LAC OPERON; MICE; MICE, TRANSGENIC; MUTATION; OXIDATIVE STRESS; SKIN; SUNLIGHT;

MAMMALIA;

EID: 5644231166     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2004.06.038     Document Type: Article

References (66)

1. R.B. Setlow The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis Proc. Natl. Acad. Sci. U.S.A. 71 1974 3363 3366
2. F.R. De Gruijl, and 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. 67 1994 319 325
3. R.B. Setlow, and W.L. Carrier Pyrimidine dimers in ultraviolet-irradiated DNA's J. Mol. Biol. 17 1966 237 254
4. F. Bourre, G. Renault, and A. Sarasin Sequence effect on alkali-sensitive sites in UV-induced SV40 DNA Nucl. Acids Res. 15 1987 8861 8875
5. E.C. Friedberg G.C. Walker W. Siede DNA Repair and Mutagenesis 1995 ASM Press Washington, DC
6. J.H. Miller Mutagenic specificity of ultraviolet light J. Mol. Biol. 182 1985 45 68
7. H.C. Hsia, J.S. Lebkowski, P.-M. Leong, M.P. Calos, and J.H. Miller Comparison of ultraviolet irradiation-induced mutagenesis of the lacI gene in Escherichia coli and in human 293 cells J. Mol. Biol. 205 1989 103 113
8. D.E. Brash, J.A. Rudolph, J.A. Simon, A. Lin, G.J. McKenna, H.P. Baden, A.J. Halperin, and J. Pontén A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma Proc. Natl. Acad. Sci. U.S.A. 88 1991 10124 10128
9. A. Ziegler, D.J. Leffell, S. Kunala, H.W. Sharma, M. Gailani, J.A. Simon, A.J. Halperin, H.P. Baden, P.E. Shapiro, A.E. Bale, and D.E. Brash Mutation hotspots due to sunlight in the p53 gene of nonmelanoma skin cancers Proc. Natl. Acad. Sci. U.S.A. 90 1993 4216 4220
10. L. Daya-Grosjean, N. Dumaz, and A. Sarasin The specificity of p53 mutation spectra in sunlight induced human cancers J. Photochem. Photobiol. B Biol. 28 1995 115 124
11. S.P. Hussain, and C.C. Harris Molecular epidemiology and carcinogenesis: endogenous and exogenous carcinogens Mutat. Res. 462 2000 311 322
12. T. Matsunaga, K. Hieda, and O. Nikaido 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 1991 403 410
13. C. Kielbassa, L. Roza, and B. Epe Wavelength dependence of oxidative DNA damage induced by UV and visible light Carcinogenesis 18 1997 811 816
14. H. Ikehata, H. Kudo, T. Masuda, and T. Ono UVA induces C → T transitions at methyl-CpG-associated dipyrimidine sites in mouse skin epidermis more frequently than UVB Mutagenesis 18 2003 511 519
15. H. Ikehata, T. Masuda, H. Sakata, and T. Ono Analysis of mutation spectra in UVB-exposed mouse skin epidermis and dermis: frequent occurrence of C → T transition at methylated CpG-associated dipyrimidine sites Environ. Mol. Mutagen. 41 2003 280 292
16. A.P. Grollman, and M. Moriya Mutagenesis by 8-oxoguanine: an enemy within Trends Genet. 9 1993 246 279
17. J.-P. Mols, C. Moyret, B. Guillot, P. Jeanteur, J.-J. Guilhou, C. Theillet, and N. Basset-Sguin p53 gene mutations in human epithelial skin cancers Oncogene 8 1993 583 588
18. M. Sato, C. Nishigori, M. Zghal, T. Yagi, and H. Takebe Ultraviolet-specific mutations in p53 gene in skin tumors in xeroderma pigmentosum patients Cancer Res. 53 1993 2944 2946
19. Y. Matsumura, M. Sato, C. Nishigori, M. Zghal, T. Yagi, S. Imamura, and H. Takebe High prevalence of mutations in the p53 gene in poorly differentiated squamous cell carcinomas in xeroderma pigmentosum patients J. Invest. Dermatol. 105 1995 399 401
20. G. Giglia, N. Dumaz, C. Drougard, M.-F. Avril, L. Daya-Grosjean, and A. Sarasin p53 mutations in skin and internal tumors of xeroderma pigmentosum patients belonging to the complementation group C Cancer Res. 58 1998 4402 4409
21. E.A. Drobetsky, E. Moustacchi, B.W. Glickman, and E. Sage The mutational specificity of simulated sunlight at the aprt locus in rodent cells Carcinogenesis 15 1994 1577 1583
22. Y.-H. You, C. Li, and G.P. Pfeifer Involvement of 5-methylcytosine in sunlight-induced mutagenesis J. Mol. Biol. 293 1999 493 503
23. Y.-H. You, and G.P. Pfeifer Similarities in sunlight-induced mutational spectra of CpG-methylated transgenes and the p53 gene in skin cancer point to an important role of 5-methylcytosine residues in solar UV mutagenesis J. Mol. Biol. 305 2001 389 399
24. J.A. Gossen, W.J.F. de Leeuw, C.H.T. Tan, E.C. Zwarthoff, F. Berends, P.H.M. Lohman, D.L. Knook, and 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. 86 1989 7971 7975
25. H. Ikehata, and T. Ono Mutation induction with UVB in mouse skin epidermis is suppressed in acute high-dose exposure Mutat. Res. 508 2002 41 47
26. N. Munakata, F. Morohoshi, K. Hieda, K. Suzuki, Y. Furusawa, H. Shimura, and T. Ito Experimental correspondence between spore dosimetry and spectral photometry of solar ultraviolet radiation Photochem. Photobiol. 63 1996 74 78
27. H. Ikehata, S. Aiba, H. Ozawa, and T. Ono Thermolysin improves mutation analysis in skin epidermis from ultraviolet light-irradiated Muta™ mouse Environ. Mol. Mutagen. 38 2001 55 58
28. T. Ono, H. Ikehata, S. Nakamura, Y. Saito, Y. Hosoi, Y. Takai, S. Yamada, J. Onodera, and K. Yamamoto Age-associated increase of spontaneous mutant frequency and molecular nature of mutation in newborn and old lacZ-transgenic mouse Mutat. Res. 447 2000 165 177
29. W.T. Adams, and T.R. Skopek Statistical test for the comparison of samples from mutational spectra J. Mol. Biol. 194 1987 391 396
30. N.F. Cariello, W.W. Piegorsch, W.T. Adams, and T.R. Skopek Computer program for the analysis of mutational spectra: application to p53 mutations Carcinogenesis 15 1994 2281 2285
31. A. Razin, and H. Cedar DNA methylation in eukaryotic cells Int. Rev. Cytol. 92 1984 159 185
32. M.J. Peak, J.G. Peak, M.P. Moehring, and R.B. Webb Ultraviolet action spectra for DNA dimer induction, lethality, and mutagenesis in Escherichia coli with emphasis on the UVB region Photochem. Photobiol. 40 1984 613 620
33. F. Suzuki, A. Han, G.R. Lankas, H. Utsumi, and M.M. Elkind Spectral dependencies of killing, mutation, and transformation in mammalian cells and their relevance to hazards caused by solar ultraviolet radiation Cancer Res. 41 1981 4916 4924
34. F. Zolzer, and J. Kiefer Wavelength dependence of inactivation and mutation induction to 6-thioguanine-resistance in V79-Chinese hamster fibroblasts Photochem. Photobiol. 40 1984 49 53
35. W.A.G. Bruls, H. Slaper, J.C. Van der Leun, and L. Berrens Transmission of human epidermis and stratum corneum as a function of thickness in the ultraviolet and visible wavelengths Photochem. Photobiol. 40 1984 485 494
36. R.J.W. Berg, F.R. De Gruijl, and J.C. Van der Leun Interaction between ultraviolet A and ultraviolet B radiations in skin cancer induction in hairless mice Cancer Res. 53 1993 4212 42117
37. F.R. De Gruijl Photocarcinogenesis: UVA vs. UVB radiation Skin Pharmacol. Appl. Skin Physiol. 15 2002 316 320
38. R.M. Tyrrell Role for singlet oxygen in biological effects of ultraviolet A radiation Methods Enzymol. 319 2000 290 296
39. D. Decuyper-Debergh, J. Piette, and A. Van de Vorst Singlet oxygen-induced mutations in M13 lacZ phage DNA EMBO J. 6 1987 3155 3261
40. R.C. De Oliveira, D.T. Ribeiro, R.G. Nigro, P. Di Mascio, and C.F.M. Menck Singlet oxygen induced mutation spectrum in mammalian cells Nucl. Acids Res. 20 1992 4319 4323
41. J. Cadet, T. Douki, J.-P. Pouget, and J.-L. Ravanat Singlet oxygen DNA damage products: formation and measurement Methods Enzymol. 319 2000 143 153
42. S. Shibutani, M. Takeshita, and A.P. Grollman Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG Nature 349 1991 431 434
43. K.C. Cheng, D.S. Cahill, H. Kasai, S. Nishimura, and L.A. Loeb 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G → T and A → C substitutions J. Biol. Chem. 267 1992 166 172
44. M. Moriya Single-stranded shuttle phagemid for mutagenesis studies in mammalian cells: 8-oxoguanine in DNA induces targeted G:C → T:A transversions in simian kidney cells Proc. Natl. Acad. Sci. U.S.A. 90 1993 1122 1126
45. C. Kielbassa, L. Roza, and B. Epe Wavelength dependence of oxidative DNA damage induced by UV and visible light Carcinogenesis 18 1997 811 816
46. E. Kvam, and R.M. Tyrell Induction of oxidative DNA base damage in human skin cells by UV and near visible radiation Carcinogenesis 18 1997 2379 2384
47. T. Douki, A. Reynaud-Angelin, J. Cadet, and E. Sage Bipyrimidine photoproducts rather than oxidative lesions are the main type of DNA damage involved in the genotoxic effect of solar UVA radiation Biochemistry 42 2003 9221 9226
48. E.A. Drobetsky, J. Turctte, and A. Châteauneuf A role for ultraviolet A in solar mutagenesis Proc. Natl. Acad. Sci. U.S.A. 92 1995 2350 2354
49. C. Robert, B. Muel, A. Benoit, L. Dubertret, A. Sarasin, and A. Stary Cell survival and shuttle vector mutagenesis induced by ultraviolet A and ultraviolet B radiation in a human cell line J. Invest. Dermatol. 106 1996 721 728
50. H.J. Van Kranen, A. De Laat, J. Van de Ven, P.W. Wester, A. De Vries, R.J.W. Berg, C.F. Van Kreijl, and F.R. De Gruijl Low incidence of p53 mutations in UVA (365 nm)-induced skin tumors in hairless mice Cancer Res. 57 1997 1238 1240
51. M. Olivier, R. Eeles, M. Hollstein, M.A. Khan, C.C. Harris, and P. Hainaut The IARC TP53 database: new online mutation analysis and recommendations to users Hum. Mutat. 19 2002 607 614
52. H.N. Ananthaswamy, A. Fourtanier, R.L. Evans, S. Tison, C. Medaisko, S.E. Ullrich, and M.L. Kripke p53 mutations in hairless SKH-hr1 mouse skin tumors induced by a solar simulator Photochem. Photobiol. 67 1998 227 232
53. H. Ikehata, M. Takatsu, Y. Saito, and T. Ono Distribution of spontaneous CpG-associated G:C → A:T mutations in the lacZ gene of Muta™ mice: effects of CpG methylation, the sequence context of CpG sites, and severity of mutations on the activity of the lacZ gene product Environ. Mol. Mutagen. 36 2000 301 311
54. S. Tommasi, M.F. Denissenko, and G.P. Pfeifer Sunlight induces pyrimidine dimers preferentially at 5-methylcytosine bases Cancer Res. 57 1997 4727 4730
55. R. Drouin, and J.-P. Therrien UVB-induced cyclobutane pyrimidine dimer frequency correlates with skin cancer mutational hotspots in p53 Photochem. Photobiol. 66 1997 719 726
56. S. Tornaletti, and G.P. Pfeifer Complete and tissue-independent methylation of CpG sites in the p53 gene: implications for mutations in human cancers Oncogene 10 1995 1493 1499
57. R. Stein, N. Sciaky-Gallili, A. Razin, and H. Ceder Pattern of methylation of two genes coding for housekeeping functions Proc. Natl. Acad. Sci. U.S.A. 80 1983 2422 2426
58. T. Douki, and J. Cadet Individual determination of the yield of the main UV-induced dimeric pyrimidine photoproducts in DNA suggests a high mutagenicity of CC photolesions Biochemistry 40 2001 2495 2501
59. Y.-H. You, D.-H. Lee, J.-H. Yoon, S. Nakajima, A. Yasui, and G.P. Pfeifer Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells J. Biol. Chem. 276 2001 44688 44694
60. E. Otoshi, T. Yagi, T. Mori, T. Matsunaga, O. Nikaido, S.-T. Kim, K. Hitomi, M. Ikenaga, and T. Todo Respective roles of cyclobutane pyrimidine dimers, (6-4)photoproducts, and minor photoproducts in ultraviolet mutagenesis of repair-deficient xeroderma pigmentosum A cells Cancer Res. 60 2000 1729 1735
61. B.W. Glickman, R.M. Schaaper, W.A. Haseltine, R.L. Dunn, and D.E. Brash The C-C (6-4) UV photoproduct is mutagenic in Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 83 1986 6945 6949
62. G.P. Pfeifer, R. Drouin, A.D. Riggs, and G.P. Holmquist In vivo mapping of a DNA adduct at nucleotide resolution: detection of pyrimidine (6-4) pyrimidone photoproducts by ligation-mediated polymerase chain reaction Proc. Natl. Acad. Sci. U.S.A. 88 1991 1374 1378
63. T. Douki, and J. Cadet Formation of cyclobutane dimers and (6-4) photoproducts upon far-UV photolysis of 5-methylcytosine-containing dinucleotide monophosphates Biochemistry 33 1994 11942 11950
64. N. Jiang, and J.-S. Taylor In vivo evidence that UV-induced C → T mutations at dipyrimidine sites could result from the replicative bypass of cis-syn cyclobutane dimers or their deamination products Biochemistry 32 1993 472 481
65. C. Masutani, R. Kusumoto, S. Iwai, and F. Hanaoka Mechanisms of accurate translesion synthesis by human DNA polymerase η EMBO J. 19 2000 3100 3109
66. D.-H. Lee, and G.P. Pfeifer Deamination of 5-methylcytosines within cyclobutane pyrimidine dimers is an important component of UVB mutagenesis J. Biol. Chem. 278 2003 10314 10321