Rapid repair of UVA-induced oxidized purines and persistence of UVB-induced dipyrimidine lesions determine the mutagenicity of sunlight in mouse cells

FASEB Journal

Volumn 22, Issue 7, 2008, Pages 2379-2392

  Besaratinia, Ahmad ^a   Kim, Sang In ^a   Pfeifer, Gerd P ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

DNA damage; Mutations; Skin cancer; Ultraviolet radiation

Indexed keywords

CYCLOBUTANE; PURINE DERIVATIVE; PYRIMIDINE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; GENE MUTATION; MELANOMA; MOUSE; MUTAGENICITY; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; SKIN CANCER; SPECTROMETRY; SUNLIGHT; ULTRAVIOLET A RADIATION; ULTRAVIOLET B RADIATION;

ANIMALS; DNA DAMAGE; DNA REPAIR; DOSE-RESPONSE RELATIONSHIP, RADIATION; EMBRYO, MAMMALIAN; GENOME; MICE; PURINES; PYRIMIDINES; SUNLIGHT; ULTRAVIOLET RAYS;

MUS MUSCULUS; RODENTIA;

EID: 46749087013     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.07-105437     Document Type: Article

References (124)

1. De Gruijl, F. R. (2002) Photocarcinogenesis: UVA vs. UVB radiation. Skin Pharmacol. Appl. Skin Physiol. 15, 316-320
2. Woodhead, A. D., Setlow, R. B., and Tanaka, M. (1999) Environmental factors in nonmelanoma and melanoma skin cancer. J. Epidemiol. 9, S102-S114
3. Setlow, R. B. (1974) The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc. Natl. Acad. Sci. U. S. A. 71, 3363-3366
4. Kelfkens, G., de Gruijl, F. R., and van der Leun, J. C. (1990) Ozone depletion and increase in annual carcinogenic ultraviolet dose. Photochem. Photobiol. 52, 819-823
5. Pfeifer, G. P., You, Y. H., and Besaratinia, A. (2005) Mutations induced by ultraviolet light. Mutat. Res. 571, 19-31
6. Brash, D. E., Seetharam, S., Kraemer, K. H., Seidman, M. M., and Bredberg, A. (1987) Photoproduct frequency is not the major determinant of UV base substitution hot spots or cold spots in human cells. Proc. Natl. Acad. Sci. U. S. A. 84, 3782-3786
7. Wang, Y. C., Maher, V. M., Mitchell, D. L., and McCormick, J. J. (1993) Evidence from mutation spectra that the UV hypermutability of xeroderma pigmentosum variant cells reflects abnormal, error-prone replication on a template containing photoproducts. Mol. Cell Biol. 13, 4276-4283
8. Pascucci, B., Versteegh, A., van Hoffen, A., van Zeeland, A. A., Mullenders, L. H., and Dogliotti, E. (1997) DNA repair of UV photoproducts and mutagenesis in human mitochondrial DNA. J. Mol. Biol. 273, 417-427
9. Otoshi, E., Yagi, T., Mori, T., Matsunaga, T., Nikaido, O., Kim, S. T., Hitomi, K., Ikenaga, M., and Todo, T. (2000) 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, 1729-1735
10. Shibutani, S., Takeshita, M., and Grollman, A. P. (1991) Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349, 431-434
11. Moriya, M. (1993) 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, 1122-1126
12. Besaratinia, A., and Pfeifer, G. P. (2006) Investigating human cancer etiology by DNA lesion footprinting and mutagenicity analysis. Carcinogenesis 27, 1526-1537
13. Kim, S. I., Pfeifer, G. P., and Besaratinia, A. (2007) Mutagenicity of ultraviolet A radiation in the lacI transgene in Big Blue mouse embryonic fibroblasts. Mutat. Res. 617, 71-78
14. Besaratinia, A., Bates, S. E., Synold, T. W., and Pfeifer, G. P. (2004) Similar mutagenicity of photoactivated porphyrins and ultraviolet A radiation in mouse embryonic fibroblasts: involvement of oxidative DNA lesions in mutagenesis. Biochemistry 43, 15557-15566
15. Besaratinia, A., Synold, T. W., Xi, B., and Pfeifer, G. P. (2004) G-to-T transversions and small tandem base deletions are the hallmark of mutations induced by ultraviolet a radiation in mammalian cells. Biochemistry 43, 8169-8177
16. Besaratinia, A., Kim, S. I., Bates, S. E., and Pfeifer, G. P. (2007) Riboflavin activated by ultraviolet A1 irradiation induces oxidative DNA damage-mediated mutations inhibited by vitamin C. Proc. Natl. Acad. Sci. U. S. A. 104, 5953-5958
17. Dumaz, N., Drougard, C., Sarasin, A., and Daya-Grosjean, L. (1993) Specific UV-induced mutation spectrum in the p53 gene of skin tumors from DNA-repair-deficient xeroderma pigmentosum patients. Proc. Natl. Acad. Sci. U. S. A. 90, 10529-10533
18. Kanjilal, S., Pierceall, W. E., Cummings, K. K., Kripke, M. L., and Ananthaswamy, H. N. (1993) High frequency of p53 mutations in ultraviolet radiation-induced murine skin tumors: evidence for strand bias and tumor heterogeneity. Cancer Res. 53, 2961-2964
19. Yajima, H., Takao, M., Yasuhira, S., Zhao, J. H., Ishii, C., Inoue, H., and Yasui, A. (1995) A eukaryotic gene encoding an endonuclease that specifically repairs DNA damaged by ultraviolet light. EMBO J. 14, 2393-2399
20. Kanno, S., Iwai, S., Takao, M., and Yasui, A. (1999) Repair of apurinic/apyrimidinic sites by UV damage endonuclease; a repair protein for UV and oxidative damage. Nucleic Acids Res. 27, 3096-3103
21. Avery, A. M., Kaur, B., Taylor, J. S., Mello, J. A., Essigmann, J. M., and Doetsch, P. W. (1999) Substrate specificity of ultraviolet DNA endonuclease (UVDE/Uve1p) from Schizosaccharomyces pombe. Nucleic Acids Res. 27, 2256-2264
22. Boiteux, S., O'Connor, T. R., and Laval, J. (1987) Formamidopyrimidine- DNA glycosylase of Escherichia coli: cloning and sequencing of the fpg structural gene and overproduction of the protein. EMBO J. 6, 3177-3183
23. Cadet, J., Ravanat, J. L., Martinez, G., Medeiros, M., and Di Mascio, P. (2006) Singlet oxygen oxidation of isolated and cellular DNA: product formation and mechanistic insights. Photochem. Photobiol. 82, 1219-1225
24. Adams, W. T., and Skopek, T. R. (1987) Statistical test for the comparison of samples from mutational spectra. J. Mol. Biol. 194, 391-396
25. Busuttil, R. A., Rubio, M., Dolle, M. E., Campisi, J., and Vijg, J. (2003) Oxygen accelerates the accumulation of mutations during the senescence and immortalization of murine cells in culture. Aging Cell 2, 287-294
26. Busuttil, R. A., Rubio, M., Dolle, M. E., Campisi, J., and Vijg, J. (2006) Mutant frequencies and spectra depend on growth state and passage number in cells cultured from transgenic lacZ-plasmid reporter mice. DNA Repair (Amst.) 5, 52-60
27. Tommasi, S., Denissenko, M. F., and Pfeifer, G. P. (1997) Sunlight induces pyrimidine dimers preferentially at 5-methylcytosine bases. Cancer Res. 57, 4727-4730
28. Lambert, I. B., Singer, T. M., Boucher, S. E., and Douglas, G. R. (2005) Detailed review of transgenic rodent mutation assays. Mutat. Res. 590, 1-280
29. Mellon, I., Spivak, G., and Hanawalt, P. C. (1987) Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 51, 241-249
30. Davies, H., Bignell, G. R., Cox, C., Stephens, P., Edkins, S., Clegg, S., Teague, J., Woffendin, H., Garnett, M. J., Bottomley, W., Davis, N., Dicks, E., Ewing, R., Floyd, Y., Gray, K., Hall, S., Hawes, R., Hughes, J., Kosmidou, V., Menzies, A., Mould, C., Parker, A., Stevens, C., Watt, S., Hooper, S., Wilson, R., Jayatilake, H., Gusterson, B. A., Cooper, C., Shipley, J., Hargrave, D., Pritchard-Jones, K., Maitland, N., Chenevix-Trench, G., Riggins, G. J., Bigner, D. D., Palmieri, G., Cossu, A., Flanagan, A., Nicholson, A., Ho, J. W., Leung, S. Y., Yuen, S. T., Weber, B. L., Seigler, H. F., Darrow, T. L., Paterson, H., Marais, R., Marshall, C. J., Wooster, R., Stratton, M. R., and Futreal, P. A. (2002) Mutations of the BRAF gene in human cancer. Nature 417, 949-954
31. Lowy, D. R., and Willumsen, B. M. (1993) Function and regulation of ras. Annu. Rev. Biochem. 62, 851-891
32. Van Elsas, A., Zerp, S. F., van der Flier, S., Kruse, K. M., Aarnoudse, C., Hayward, N. K., Ruiter, D. J., and Schrier, P. I. (1996) Relevance of ultraviolet-induced N-ras oncogene point mutations in development of primary human cutaneous melanoma. Am. J. Pathol. 149, 883-893
33. Olivier, M., Eeles, R., Hollstein, M., Khan, M. A., Harris, C. C., and Hainaut, P. (2002) The IARC TP53 database: new online mutation analysis and recommendations to users. Hum. Mutat. 19, 607-614
34. Castellano, M., Pollock, P. M., Walters, M. K., Sparrow, L. E., Down, L. M., Gabrielli, B. G., Parsons, P. G., and Hayward, N. K. (1997) CDKN2A/p16 is inactivated in most melanoma cell lines. Cancer Res. 57, 4868-4875
35. Flores, J. F., Walker, G. J., Glendening, J. M., Haluska, F. G., Castresana, J. S., Rubio, M. P., Pastorfide, G. C., Boyer, L. A., Kao, W. H., Bulyk, M. L., Barnhill, R. L., Hayward, N. K., Housman, D. E., and Fountain, J. W. (1996) Loss of the p16INK4a and p15INK4b genes, as well as neighboring 9p21 markers, in sporadic melanoma. Cancer Res. 56, 5023-5032
36. Fujimoto, A., Morita, R., Hatta, N., Takehara, K., and Takata, M. (1999) p16INK4a inactivation is not frequent in uncultured sporadic primary cutaneous melanoma. Oncogene 18, 2527-2532
37. Herbst, R. A., Gutzmer, R., Matiaske, F., Mommert, S., Kapp, A., Weiss, J., Arden, K. C., and Cavenee, W. K. (1997) Further evidence for ultraviolet light induction of CDKN2 (p16INK4) mutations in sporadic melanoma in vivo. J. Invest. Dermatol. 108, 950
38. Kumar, R., Lundh Rozell, B., Louhelainen, J., and Hemminki, K. (1998) Mutations in the CDKN2A (p16INK4a) gene in microdissected sporadic primary melanomas. Int. J. Cancer 75, 193-198
39. Lamperska, K., Karezewska, A., Kwiatkowska, E., and Mackiewicz, A. (2002) Analysis of mutations in the p16/CDKN2A gene in sporadic and familial melanoma in the Polish population. Acta Biochim. Pol. 49, 369-376
40. Piccinin, S., Doglioni, C., Maestro, R., Vukosavljevic, T., Gasparotto, D., D'Orazi, C., and Boiocchi, M. (1997) p16/CDKN2 and CDK4 gene mutations in sporadic melanoma development and progression. Int. J. Cancer 74, 26-30
41. Platz, A., Ringborg, U., Lagerlof, B., Lundqvist, E., Sevigny, P., and Inganas, M. (1996) Mutational analysis of the CDKN2 gene in metastases from patients with cutaneous malignant melanoma. Br. J. Cancer 73, 344-348
42. Pollock, P. M., Pearson, J. V., and Hayward, N. K. (1996) Compilation of somatic mutations of the CDKN2 gene in human cancers: non-random distribution of base substitutions. Genes Chromosomes Cancer 15, 77-88
43. Ruas, M., and Peters, G. (1998) The p16INK4a/CDKN2A tumor suppressor and its relatives. Biochim. Biophys. Acta 1378, F115-F177
44. Ruiz, A., Puig, S., Lynch, M., Castel, T., and Estivill, X. (1998) Retention of the CDKN2A locus and low frequency of point mutations in primary and metastatic cutaneous malignant melanoma. Int. J. Cancer 76, 312-316
45. Smith-Sørensen, B., and Hovig, E. (1996) CDKN2A (p16INK4A) somatic and germline mutations. Human Mutat. 7, 294-303
46. Walker, G. J., Flores, J. F., Glendening, J. M., Lin, A. H., Markl, I. D., and Fountain, J. W. (1998) Virtually 100% of melanoma cell lines harbor alterations at the DNA level within CDKN2A, CDKN2B, or one of their downstream targets. Genes Chromosomes Cancer 22, 157-163
47. D'Errico, M., Calcagnile, A., Canzona, F., Didona, B., Posteraro, P., Cavalieri, R., Corona, R., Vorechovsky, I., Nardo, T., Stefanini, M., and Dogliotti, E. (2000) UV mutation signature in tumor suppressor genes involved in skin carcinogenesis in xeroderma pigmentosum patients. Oncogene 19, 463- 467
48. Evans, T., Boonchai, W., Shanley, S., Smyth, I., Gillies, S., Georgas, K., Wainwright, B., Chenevix-Trench, G., and Wicking, C. (2000) The spectrum of patched mutations in a collection of Australian basal cell carcinomas. Hum. Mutat. 16, 43- 48
49. Gailani, M. R., Stahle-Backdahl, M., Leffell, D. J., Glynn, M., Zaphiropoulos, P. G., Pressman, C., Unden, A. B., Dean, M., Brash, D. E., Bale, A. E., and Toftgard, R. (1996) The role of the human homologue of Drosophila patched in sporadic basal cell carcinomas. Nat. Genet. 14, 78-81
50. Hahn, H., Wicking, C., Zaphiropoulous, P. G., Gailani, M. R., Shanley, S., Chidambaram, A., Vorechovsky, I., Holmberg, E., Unden, A. B., Gillies, S., Negus, K., Smyth, I., Pressman, C., Leffell, D. J., Gerrard, B., Goldstein, A. M., Dean, M., Toftgard, R., Chenevix-Trench, G., Wainwright, B., and Bale, A. E. (1996) Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 85, 841-851
51. Heitzer, E., Lassacher, A., Quehenberger, F., Kerl, H., and Wolf, P. (2007) UV fingerprints predominate in the PTCH mutation spectra of basal cell carcinomas independent of clinical phenotype. J. Invest. Dermatol. 127, 2872-2881
52. Kim, M. Y., Park, H. J., Baek, S. C., Byun, D. G., and Houh, D. (2002) Mutations of the p53 and PTCH gene in basal cell carcinomas: UV mutation signature and strand bias. J. Dermatol. Sci. 29, 1-9
53. Ratner, D., Peacocke, M., Zhang, H., Ping, X. L., and Tsou, H. C. (2001) UV-specific p53 and PTCH mutations in sporadic basal cell carcinoma of sun-exposed skin. J. Am. Acad. Dermatol. 44, 293-297
54. Reifenberger, J., Wolter, M., Knobbe, C. B., Kohler, B., Schonicke, A., Scharwachter, C., Kumar, K., Blaschke, B., Ruzicka, T., and Reifenberger, G. (2005) Somatic mutations in the PTCH, SMOH, SUFUH and TP53 genes in sporadic basal cell carcinomas. Br. J. Dermatol. 152, 43-51
55. Unden, A. B., Holmberg, E., Lundh-Rozell, B., Stahle-Backdahl, M., Zaphiropoulos, P. G., Toftgard, R., and Vorechovsky, I. (1996) Mutations in the human homologue of Drosophila patched (PTCH) in basal cell carcinomas and the Gorlin syndrome: different in vivo mechanisms of PTCH inactivation. Cancer Res. 56, 4562-4565
56. Wolter, M., Reifenberger, J., Sommer, C., Ruzicka, T., and Reifenberger, G. (1997) Mutations in the human homologue of the Drosophila segment polarity gene patched (PTCH) in sporadic basal cell carcinomas of the skin and primitive neuroectodermal tumors of the central nervous system. Cancer Res. 57, 2581-2585
57. Xie, J., Johnson, R. L., Zhang, X., Bare, J. W., Waldman, F. M., Cogen, P. H., Menon, A. G., Warren, R. S., Chen, L. C., Scott, M. P., and Epstein, E. H., Jr. (1997) Mutations of the PATCHED gene in several types of sporadic extracutaneous tumors. Cancer Res. 57, 2369-2372
58. Zhang, H., Ping, X. L., Lee, P. K., Wu, X. L., Yao, Y. J., Zhang, M. J., Silvers, D. N., Ratner, D., Malhotra, R., Peacocke, M., and Tsou, H. C. (2001) Role of PTCH and p53 genes in early-onset basal cell carcinoma. Am. J. Pathol. 158, 381-385
59. Greenman, C., Stephens, P., Smith, R., Dalgliesh, G. L., Hunter, C., Bignell, G., Davies, H., Teague, J., Butler, A., Stevens, C., Edkins, S., O'Meara, S., Vastrik, I., Schmidt, E. E., Avis, T., Barthorpe, S., Bhamra, G., Buck, G., Choudhury, B., Clements, J., Cole, J., Dicks, E., Forbes, S., Gray, K., Halliday, K., Harrison, R., Hills, K., Hinton, J., Jenkinson, A., Jones, D., Menzies, A., Mironenko, T., Perry, J., Raine, K., Richardson, D., Shepherd, R., Small, A., Tofts, C., Varian, J., Webb, T., West, S., Widaa, S., Yates, A., Cahill, D. P., Louis, D. N., Goldstraw, P., Nicholson, A. G., Brasseur, F., Looijenga, L., Weber, B. L., Chiew, Y. E., DeFazio, A., Greaves, M. F., Green, A. R., Campbell, P., Birney, E., Easton, D. F., Chenevix-Trench, G., Tan, M. H., Khoo, S. K., Teh, B. T., Yuen, S. T., Leung, S. Y., Wooster, R., Futreal, P. A., and Stratton, M. R. (2007) Patterns of somatic mutation in human cancer genomes. Nature 446, 153-158
60. Thomas, D. C., Okumoto, D. S., Sancar, A., and Bohr, V. A. (1989) Preferential DNA repair of (6-4) photoproducts in the dihydrofolate reductase gene of Chinese hamster ovary cells. J. Biol. Chem. 264, 18005-18010
61. Mitchell, D. L., Brash, D. E., and Nairn, R. S. (1990) Rapid repair kinetics of pyrimidine(6-4)pyrimidone photoproducts in human cells are due to excision rather than conformational change. Nucleic Acids Res. 18, 963-971
62. Vreeswijk, M. P., van Hoffen, A., Westland, B. E., Vrieling, H., van Zeeland, A. A., and Mullenders, L. H. (1994) Analysis of repair of cyclobutane pyrimidine dimers and pyrimidine 6-4 pyrimidone photoproducts in transcriptionally active and inactive genes in Chinese hamster cells. J. Biol. Chem. 269, 31858-31863
63. Van Hoffen, A., Venema, J., Meschini, R., van Zeeland, A. A., and Mullenders, L. H. (1995) Transcription-coupled repair removes both cyclobutane pyrimidine dimers and 6-4 photoproducts with equal efficiency and in a sequential way from transcribed DNA in xeroderma pigmentosum group C fibroblasts. EMBO J. 14, 360-367
64. Mitchell, D. L., Byrom, M., Chiarello, S., and Lowery, M. G. (2001) Effects of chronic exposure to ultraviolet B radiation on DNA repair in the dermis and epidermis of the hairless mouse. J. Invest. Dermatol. 116, 209-215
65. Van der Wees, C. G., Vreeswijk, M. P., Persoon, M., van der Laarse, A., van Zeeland, A. A., and Mullenders, L. H. (2003) Deficient global genome repair of UV-induced cyclobutane pyrimidine dimers in terminally differentiated myocytes and proliferating fibroblasts from the rat heart. DNA Repair (Amst.) 2, 1297-1308
66. Courdavault, S., Baudouin, C., Sauvaigo, S., Mouret, S., Candeias, S., Charveron, M., Favier, A., Cadet, J., and Douki, T. (2004) Unrepaired cyclobutane pyrimidine dimers do not prevent proliferation of UV-B-irradiated cultured human fibroblasts. Photochem. Photobiol. 79, 145-151
67. Franklin, W. A., Doetsch, P. W., and Haseltine, W. A. (1985) Structural determination of the ultraviolet light-induced thymine-cytosine pyrimidine-pyrimidone (6-4) photoproduct. Nucleic Acids Res. 13, 5317-5325
68. Rao, S. N., and Kollman, P. A. (1985) Conformations of deoxydodecanucleotides with pyrimidine (6-4)-pyrimidone photoadducts. Photochem. Photobiol. 42, 465-475
69. Pearlman, D. A., Holbrook, S. R., Pirkle, D. H., and Kim, S. H. (1985) Molecular models for DNA damaged by photoreaction. Science 227, 1304-1308
70. Szymkowski, D. E., Lawrence, C. W., and Wood, R. D. (1993) Repair by human cell extracts of single (6-4) and cyclobutane thymine-thymine photoproducts in DNA. Proc. Natl. Acad. Sci. U. S. A. 90, 9823-9827
71. Mitchell, D. L., Nguyen, T. D., and Cleaver, J. E. (1990) Nonrandom induction of pyrimidine-pyrimidone (6-4) photoproducts in ultraviolet-irradiated human chromatin. J. Biol. Chem. 265, 5353-5356
72. Gale, J. M., and Smerdon, M. J. (1990) UV induced (6-4) photoproducts are distributed differently than cyclobutane dimers in nucleosomes. Photochem. Photobiol. 51, 411-417
73. Koehler, D. R., Courcelle, J., and Hanawalt, P. C. (1996) Kinetics of pyrimidine(6-4)pyrimidone photoproduct repair in Escherichia coli. J. Bacteriol. 178, 1347-1350
74. Buterin, T., Hess, M. T., Gunz, D., Geacintov, N. E., Mullenders, L. H., and Naegeli, H. (2002) Trapping of DNA nucleotide excision repair factors by nonrepairable carcinogen adducts. Cancer Res. 62, 4229-4235
75. Ruven, H. J., Seelen, C. M., Lohman, P. H., van Kranen, H., van Zeeland, A. A., and Mullenders, L. H. (1994) Strand-specific removal of cyclobutane pyrimidine dimers from the p53 gene in the epidermis of UVB-irradiated hairless mice. Oncogene 9, 3427-3432
76. Tu, Y., Bates, S., and Pfeifer, G. P. (1997) Sequence-specific and domain-specific DNA repair in xeroderma pigmentosum and Cockayne syndrome cells. J. Biol. Chem. 272, 20747-22055
77. Ford, J. M., Lommel, L., and Hanawalt, P. C. (1994) Preferential repair of ultraviolet light-induced DNA damage in the transcribed strand of the human p53 gene. Mol. Carcinog. 10, 105-109
78. Tung, B. S., McGregor, W. G., Wang, Y. C., Maher, V. M., and McCormick, J. J. (1996) Comparison of the rate of excision of major UV photoproducts in the strands of the human HPRT gene of normal and xeroderma pigmentosum variant cells. Mutat. Res. 362, 65-74
79. Kobayashi, T., Takeuchi, S., Saijo, M., Nakatsu, Y., Morioka, H., Otsuka, E., Wakasugi, M., Nikaido, O., and Tanaka, K. (1998) Mutational analysis of a function of xeroderma pigmentosum group A (XPA) protein in strand-specific DNA repair. Nucleic Acids Res. 26, 4662-4668
80. Therrien, J. P., Drouin, R., Baril, C., and Drobetsky, E. A. (1999) Human cells compromised for p53 function exhibit defective global and transcription-coupled nucleotide excision repair, whereas cells compromised for pRb function are defective only in global repair. Proc. Natl. Acad. Sci. U. S. A. 96, 15038-15043
81. Riou, L., Eveno, E., van Hoffen, A., van Zeeland, A. A., Sarasin, A., and Mullenders, L. H. (2004) Differential repair of the two major UV-induced photolesions in trichothiodystrophy fibroblasts. Cancer Res. 64, 889-894
82. Emmert, S., Kobayashi, N., Khan, S. G., and Kraemer, K. H. (2000) The xeroderma pigmentosum group C gene leads to selective repair of cyclobutane pyrimidine dimers rather than 6-4 photoproducts. Proc. Natl. Acad. Sci. U. S. A. 97, 2151-2216
83. Mathonnet, G., Leger, C., Desnoyers, J., Drouin, R., Therrien, J. P., and Drobetsky, E. A. (2003) UV wavelength-dependent regulation of transcription-coupled nucleotide excision repair in p53-deficient human cells. Proc. Natl. Acad. Sci. U. S. A. 100, 7219-7224
84. Courdavault, S., Baudouin, C., Charveron, M., Canguilhem, B., Favier, A., Cadet, J., and Douki, T. (2005) Repair of the three main types of bipyrimidine DNA photoproducts in human keratinocytes exposed to UVB and UVA radiations. DNA Repair (Amst.) 4, 836-844
85. Mouret, S., Baudouin, C., Charveron, M., Favier, A., Cadet, J., and Douki, T. (2006) Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc. Natl. Acad. Sci. U. S. A. 103, 13765-13770
86. Pflaum, M., Boiteux, S., and Epe, B. (1994) Visible light generates oxidative DNA base modifications in high excess of strand breaks in mammalian cells. Carcinogenesis 15, 297-300
87. Spencer, J. P., Jenner, A., Aruoma, O. I., Cross, C. E., Wu, R., and Halliwell, B. (1996) Oxidative DNA damage in human respiratory tract epithelial cells. Time course in relation to DNA strand breakage. Biochem. Biophys. Res. Commun. 224, 17-22
88. Grishko, V. I., Driggers, W. J., LeDoux, S. P., and Wilson, G. L. (1997) Repair of oxidative damage in nuclear DNA sequences with different transcriptional activities. Mutat. Res. 384, 73-80
89. Lan, L., Nakajima, S., Oohata, Y., Takao, M., Okano, S., Masutani, M., Wilson, S. H., and Yasui, A. (2004) In situ analysis of repair processes for oxidative DNA damage in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 101, 13738-13743
90. D'Errico, M., Parlanti, E., Teson, M., de Jesus, B. M., Degan, P., Calcagnile, A., Jaruga, P., Bjoras, M., Crescenzi, M., Pedrini, A. M., Egly, J. M., Zambruno, G., Stefanini, M., Dizdaroglu, M., and Dogliotti, E. (2006) New functions of XPC in the protection of human skin cells from oxidative damage. EMBO J. 25, 4305-4315
91. Hollenbach, S., Dhenaut, A., Eckert, I., Radicella, J. P., and Epe, B. (1999) Overexpression of Ogg1 in mammalian cells: effects on induced and spontaneous oxidative DNA damage and mutagenesis. Carcinogenesis 20, 1863-1868
92. Drobetsky, E. A., Turcotte, J., and Chateauneuf, A. (1995) A role for ultraviolet A in solar mutagenesis. Proc. Natl. Acad. Sci. U. S. A. 92, 2350-2354
93. Sage, E., Lamolet, B., Brulay, E., Moustacchi, E., Chateauneuf, A., and Drobetsky, E. A. (1996) Mutagenic specificity of solar UV light in nucleotide excision repair-deficient rodent cells. Proc. Natl. Acad. Sci. U. S. A. 93, 176-180
94. DeMarini, D. M., Shelton, M. L., and Stankowski, L. F., Jr. (1995) Mutation spectra in Salmonella of sunlight, white fluorescent light, and light from tanning salon beds: induction of tandem mutations and role of DNA repair. Mutat. Res. 327, 131-149
95. Robert, C., Muel, B., Benoit, A., Dubertret, L., Sarasin, A., and Stary, A. (1996) Cell survival and shuttle vector mutagenesis induced by ultraviolet A and ultraviolet B radiation in a human cell line. J. Invest. Dermatol. 106, 721-728
96. Palmer, C. M., Serafini, D. M., and Schellhorn, H. E. (1997) Near ultraviolet radiation (UVA and UVB) causes a formamidopyrimidine glycosylase-dependent increase in G to T transversions. Photochem. Photobiol. 65, 543-549
97. Ananthaswamy, H. N., Fourtanier, A., Evans, R. L., Tison, S., Medaisko, C., Ullrich, S. E., and Kripke, M. L. (1998) p53 Mutations in hairless SKH-hr1 mouse skin tumors induced by a solar simulator. Photochem. Photobiol. 67, 227-232
98. Izumizawa, Y., Yang, S. J., Negishi, T., and Negishi, K. (2000) DNA lesion and mutagenesis induced in phageM13mp2 by UVA, UVB, and UVC irradiation. Nucleic Acids Symp. Ser. 73-74
99. Perdiz, D., Grof, P., Mezzina, M., Nikaido, O., Moustacchi, E., and Sage, E. (2000) Distribution and repair of bipyrimidine photoproducts in solar UV-irradiated mammalian cells. Possible role of Dewar photoproducts in solar mutagenesis. J. Biol. Chem. 275, 26732-26742
100. Rochette, P. J., Therrien, J. P., Drouin, R., Perdiz, D., Bastien, N., Drobetsky, E. A., and Sage, E. (2003) UVA-induced cyclobutane pyrimidine dimers form predominantly at thyminethymine dipyrimidines and correlate with the mutation spectrum in rodent cells. Nucleic Acids Res. 31, 2786-2794
101. Douki, T., Reynaud-Angelin, A., Cadet, J., and Sage, E. (2003) Bipyrimidine photoproducts rather than oxidative lesions are the main type of DNA damage involved in the genotoxic effect of solar UVA radiation. Biochemistry 42, 9221-9226
102. Ikehata, H., Kudo, H., Masuda, T., and Ono, T. (2003) UVA induces C->T transitions at methyl-CpG-associated dipyrimidine sites in mouse skin epidermis more frequently than UVB. Mutagenesis 18, 511-519
103. Agar, N. S., Halliday, G. M., Barnetson, R. S., Ananthaswamy, H. N., Wheeler, M., and Jones, A. M. (2004) The basal layer in human squamous tumors harbors more UVA than UVB fingerprint mutations: a role for UVA in human skin carcinogenesis. Proc. Natl. Acad. Sci. U. S. A. 101, 4954-4959
104. Courdavault, S., Baudouin, C., Charveron, M., Favier, A., Cadet, J., and Douki, T. (2004) Larger yield of cyclobutane dimers than 8-oxo-7,8- dihydroguanine in the DNA of UVA-irradiated human skin cells. Mutat. Res. 556, 135-142
105. Kappes, U. P., and Runger, T. M. (2005) No major role for 7,8-dihydro-8-oxoguanine in ultraviolet light-induced mutagenesis. Radiat. Res. 164, 440-445
106. Kozmin, S., Slezak, G., Reynaud-Angelin, A., Elie, C., de Rycke, Y., Boiteux, S., and Sage, E. (2005) UVA radiation is highly mutagenic in cells that are unable to repair 7,8-dihydro-8-oxoguanine in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 102, 13538-13543
107. Kappes, U. P., Luo, D., Potter, M., Schulmeister, K., and Runger, T. M. (2006) Short- and long-wave UV light (UVB and UVA) induce similar mutations in human skin cells. J. Invest. Dermatol. 126, 667-675
108. De Gruijl, F. R., Sterenborg, H. J., Forbes, P. D., Davies, R. E., Cole, C., Kelfkens, G., van Weelden, H., Slaper, H., and van der Leun, J. C. (1993) Wavelength dependence of skin cancer induction by ultraviolet irradiation of albino hairless mice. Cancer Res. 53, 53-60
109. Woollons, A., Kipp, C., Young, A. R., Petit-Frere, C., Arlett, C. F., Green, M. H., and Clingen, P. H. (1999) The 0.8% ultraviolet B content of an ultraviolet A sunlamp induces 75% of cyclobutane pyrimidine dimers in human keratinocytes in vitro. Br. J. Dermatol. 140, 1023-1030
110. Besaratinia, A., Synold, T. W., Chen, H. H., Chang, C., Xi, B., Riggs, A. D., and Pfeifer, G. P. (2005) DNA lesions induced by UV A1 and B radiation in human cells: comparative analyses in the overall genome and in the p53 tumor suppressor gene. Proc. Natl. Acad. Sci. U. S. A. 102, 10058-10063
111. Cadet, J., Sage, E., and Douki, T. (2005) Ultraviolet radiation-mediated damage to cellular DNA. Mutat. Res. 571, 3-17
112. Kim, S. I., Pfeifer, G. P., and Besaratinia, A. (2007) Lack of mutagenicity of acrolein-induced DNA adducts in mouse and human cells. Cancer Res. 67, 11640-11647
113. Ley, R. D. (1997) Ultraviolet radiation A-induced precursors of cutaneous melanoma in Monodelphis domestica. Cancer Res. 57, 3682-3684
114. Setlow, R. B., Grist, E., Thompson, K., and Woodhead, A. D. (1993) Wavelengths effective in induction of malignant melanoma. Proc. Natl. Acad. Sci. U. S. A. 90, 6666-6670
115. International Agency for Research on Cancer Working Group on artificial ultraviolet (UV) light and skin cancer (2007) The association of use of sunbeds with cutaneous malignant melanoma and other skin cancers: A systematic review. Int. J. Cancer 120, 1116-1122
116. Jakubczak, J. L., Merlino, G., French, J. E., Muller, W. J., Paul, B., Adhya, S., and Garges, S. (1996) Analysis of genetic instability during mammary tumor progression using a novel selection-based assay for in vivo mutations in a bacteriophage lambda transgene target. Proc. Natl. Acad. Sci. U. S. A. 93, 9073-9078
117. Lommel, L., and Hanawalt, P. C. (1993) Increased UV resistance of a xeroderma pigmentosum revertant cell line is correlated with selective repair of the transcribed strand of an expressed gene. Mol. Cell Biol. 13, 970-976
118. Dutt, A., and Wong, K. K. (2006) Mouse models of lung cancer. Clin. Cancer Res. 12, 4396S-4402S
119. Denissenko, M. F., Pao, A., Tang, M., and Pfeifer, G. P. (1996) Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53. Science 274, 430-432
120. Smith, L. E., Denissenko, M. F., Bennett, W. P., Li, H., Amin, S., Tang, M., and Pfeifer, G. P. (2000) Targeting of lung cancer mutational hotspots by polycyclic aromatic hydrocarbons. J. Natl. Cancer Inst. 92, 803-811
121. Feng, Z., Hu, W., Chen, J. X., Pao, A., Li, H., Rom, W., Hung, M. C., and Tang, M. S. (2002) Preferential DNA damage and poor repair determine ras gene mutational hotspot in human cancer J. Natl. Cancer Inst. 94, 1527-1536
122. Yoon, J. H., Smith, L. E., Feng, Z., Tang, M., Lee, C. S., and Pfeifer, G. P. (2001) Methylated CpG dinucleotides are the preferential targets for G-to-T transversion mutations induced by benzo[a]pyrene diol epoxide in mammalian cells: similarities with the p53 mutation spectrum in smoking-associated lung cancers. Cancer Res. 61, 7110-7117
123. Besaratinia, A., Bates, S. E., and Pfeifer, G. P. (2002) Mutational signature of the proximate bladder carcinogen N-hydroxy-4- acetylaminobiphenyl: inconsistency with the p53 mutational spectrum in bladder cancer Cancer Res. 62, 4331-4338
124. Yoon, J. H., Besaratinia, A., Feng, Z., Tang, M. S., Amin, S., Luch, A., and Pfeifer, G. P. (2004) DNA damage, repair, and mutation induction by (+)-Syn and (-)-anti-dibenzo-[a,l]pyrene-11,12-diol-13,14-epoxides in mouse cells. Cancer Res. 64, 7321-7328