Repair of the three main types of bipyrimidine DNA photoproducts in human keratinocytes exposed to UVB and UVA radiations

DNA Repair

Volumn 4, Issue 7, 2005, Pages 836-844

  Courdavault, Sophie ^a   Baudouin, Caroline ^b   Charveron, Marie ^b   Canguilhem, Bruno ^b   Favier, Alain ^a   Cadet, Jean ^a   Douki, Thierry ^a  

^a CEA GRENOBLE   (France)

^b INSTITUT DE RECHERCHE PIERRE FABRE   (France)

Author keywords

Apoptosis; DNA damage; Proliferation; UV carcinogenesis

Indexed keywords

CYCLOBUTANE DERIVATIVE; DNA; PYRIMIDINE DIMER; THYMINE DERIVATIVE;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL POPULATION; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IRRADIATION; ISOMER; KERATINOCYTE; NORMAL HUMAN; PRECURSOR; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RADIATION EXPOSURE; TANDEM MASS SPECTROMETRY; ULTRAVIOLET A RADIATION; ULTRAVIOLET B RADIATION;

APOPTOSIS; CELLS, CULTURED; DNA REPAIR; HUMANS; KERATINOCYTES; PYRIMIDINE DIMERS; ULTRAVIOLET RAYS;

EID: 20644446271     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2005.05.001     Document Type: Article

References (55)

1. J. Cadet, and P. Vigny Photochemistry of nucleic acids H. Morrison Bioorganic Photochemistry 1990 Wiley New York 1 272
2. J.-L. Ravanat, T. Douki, and J. Cadet Direct and indirect effects of UV radiation on DNA and its components J. Photochem. Photobiol. B: Biol. 63 2001 88 102
3. A. Ziegler, D.J. Leffel, S. Kunala, H.W. Sharma, 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
4. N. Dumaz, C. Drougard, A. Sarasin, and A.L. Daya-Grosjean 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 1993 10529 10533
5. N.S. Agar, G.M. Haliday, R.S. Bernetson, H.N. Ananthaswamy, M. Wheeler, and A.M. Jones 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 2004 4954 4959
6. 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 11942 11950
7. M.J. Peak, J.G. Peak, and B.A. Carnes Induction of direct and indirect single-strand breaks in human cell DNA by far- and near-ultraviolet radiations: action spectrum and mechanisms Photochem. Photobiol. 45 1987 381 387
8. J.G. Peak, and M.J. Peak Comparison of initial yields of DNA-to-protein crosslinks and single-strand breaks induced in cultured human cells by far- and near-ultraviolet light, blue light and X-rays Mutat. Res. 246 1991 187 191
9. Y. Hattori-Nakakuki, C. Nishigori, K. Okamoto, S. Imamura, H. Hiai, and S. Toyokuni Formation of 8-hydroxy-2′-deoxyguanosine in epidermis of hairless mice exposed to near-UV Biochem. Biophys. Res. Commun. 201 1994 1132 1139
10. 2 alone or with UVB or UVA irradiation Photochem. Photobiol. 64 1996 117 122
11. J.-P. Pouget, T. Douki, M.-J. Richard, and J. Cadet DNA damage induced in cells by gamma and UVA radiation as measured by HPLC/GC-MS and HPLC-EC and comet assay Chem. Res. Toxicol. 13 2000 541 549
12. R.M. Tyrrell Induction of pyrimidine dimers in bacterial DNA by 365 nm radiation Photochem. Photobiol. 17 1973 69 73
13. E. Kvam, and R.M. Tyrrell Induction of oxidative DNA base damage in human skin cells by UV and near visible radiation Carcinogenesis 18 1997 2379 2384
14. D. Perdiz, P. Grof, M. Mezzina, O. Nikaido, E. Moustacchi, and E. Sage Distribution and repair of bipyrimidine photoproducts in solar UV-irradiated mammalian cells. Possible role of Dewar photoproducts in solar mutagenesis J. Biol. Chem. 275 2000 26732 26742
15. S.E. Freeman, and S.L. Ryan Wavelength dependence for UV-induced pyrimidine dimer formation in DNA of human peripheral blood lymphocytes Mutat. Res. 235 1990 181 186
16. S.E. Freeman, H. Hacham, R.W. Gange, D.J. Maytum, J.C. Sutherland, and 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. 86 1989 5605 5609
17. A.R. Young, C.S. Potten, O. Nikaido, P.G. Parsons, J. Boenders, J.M. Ramsden, and C.A. Chadwick Human melanocytes and keratinocytes exposed to UVB or UVA in vivo show comparable levels of thymine dimers J. Invest. Dermatol. 111 1998 936 940
18. R. Burren, C. Scaletta, E. Frenk, R.G. Panizzon, and L.A. Applegate Sunlight and carcinogenesis: expression of p53 and pyrimidine dimers in human skin following UVA I, UVA I + II and solar simulating radiations Int. J. Cancer 76 1998 201 206
19. L.A. Applegate, C. Scaletta, R. Panizzon, H. Niggli, and E. Frenk In vivo induction of pyrimidine dimers in human skin by UVA radiation: initiation of cell damage and/or intercellular communication? Int. J. Mol. Med. 3 1999 467 472
20. C. Kielbassa, L. Roza, and B. Epe Wavelength dependence of oxidative DNA damage induced by UV and visible light Carcinogenesis 18 1997 811 816
21. T. Douki, D. Perdiz, P. Grof, Z. Kuluncsics, E. Moustacchi, J. Cadet, and E. Sage Oxidation of guanine in cellular DNA by solar UV radiation: biological role Photochem. Photobiol. 70 1999 184 190
22. 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
23. S. Courdavault, C. Baudouin, M. Charveron, A. Favier, J. Cadet, and T. Douki Larger yield of cyclobutane dimers than 8-oxo-7,8-hydroguanine in the DNA of UVA-irradiated human skin cells Mutat. Res. 556 2004 135 142
24. T. Douki, M. Court, and J. Cadet Electrospray-mass spectrometry characterization and measurement of far-UV-induced thymine photoproducts Photochem. Photobiol. B: Biol. 54 2000 145 154
25. T. Douki, M. Court, S. Sauvaigo, F. Odin, and J. Cadet Formation of the main UV-induced thymine dimeric lesions within isolated and cellular DNA as measured by high performance liquid chromatography J. Biol. Chem. 275 2000 11678 11685
26. J.-L. Ravanat, T. Douki, P. Duez, E. Gremaud, K. Herbert, T. Hofer, L. Lasserre, C. Saint-Pierre, A. Favier, and J. Cadet Cellular background level of 8-oxo-7,8-dihydro-2′-deoxyguanosine: an isotope based method to evaluate artefactual oxidation of DNA during its extraction and subsequent work-up Carcinogenesis 23 2002 1911 1918
27. S. Courdavault, C. Baudouin, S. Sauvaigo, S. Mouret, S. Candéias, M. Charveron, A. Favier, J. Cadet, and T. Douki Unrepaired cyclobutane pyrimidine dimers do not prevent proliferation of UV-B-irradiated cultured human fibroblasts Photochem. Photobiol. 79 2004 145 151
28. R. Greinert, O. Boguhn, D. Harder, E.W. Breitbart, D.L. Mitchell, and B. Volkmer The dose dependence of cyclobutane dimer induction and repair in UVB-irradiated human keratinocytes Photochem. Photobiol. 72 2000 701 708
29. C. Petit-Frère, E. Capulas, D.A. Lyon, C.J. Norbury, J.E. Lowe, P.H. Clingen, E. Riballo, M.H.L. Green, and C.F. Arlett Apoptosis and cytokine release induced by ionising or ultraviolet B radiation in primary and immortalized human keratinocytes Carcinogenesis 21 2000 1087 1095
30. K. Tsuru, T. Horikawa, A. Butiyanto, I. Hikita, M. Ueda, and M. Ichihashi Low-dose ultraviolet B radiation synergizes with TNF-α to induce apoptosis of keratinocytes J. Dermatol. Sci. 26 2001 209 216
31. A. Sesto, M. Navarro, F. Burslem, and J.L. Jorcano Analysis of the ultraviolet B response in primary human keratinocytes using oligonucleotide microarrays Proc. Natl. Acad. Sci. U.S.A. 99 2002 2965 2970
32. L. Benassi, D. Ottani, F. Fantini, A. Marconi, C. Chiodino, A. Giannetti, and C. Pincelli 1,25-Dihydroxyvitamin D3, transforming growth factor beta1, calcium, and ultraviolet B radiation induce apoptosis in cultured human keratinocytes J. Invest. Dermatol. 109 1997 276 282
33. S.A. Hurwitz, and D.F. Spandau Quantitative analysis of UVB-induced apoptosis in human epidermis Exp. Dermatol. 9 2000 185 191
34. T. Maeda, P.P.S. Chua, M.T. Chong, A.B.T. Sim, O. Nikaido, and V.A. Tron Nucleotide excision repair genes are upregulated by low-dose artificial ultraviolet B: evidence of a photoprotective SOS response J. Invest. Dermatol. 117 2001 1490 1497
35. D.A. Lewis, S.A. Hurwitz, and D.F. Spandau UVB-induced apoptosis in normal human keratinocytes: role of the erbB receptor family Exp. Cell. Res. 284 2003 316 327
36. D.L. Mitchell, C.A. Haipek, and J.M. Clarkson (6-4) Photoproducts are removed from the DNA of UV-irradiated mammalian cells more efficiently than cyclobutane pyrimidine dimers Mutat. Res. 143 1985 109 112
37. D.L. Mitchell The relative cytotoxicity of (6-4) photoproducts and cyclobutane dimers in mammalian cells Photochem. Photobiol. 48 1988 51 57
38. C. Suquet, D.L. Mitchell, and M.J. Smerdon Repair of UV-induced (6-4) photoproducts in nucleosome core DNA J. Biol. Chem. 270 1995 16507 16509
39. G. Xu, E. Snellman, C.T. Jansen, and K. Hemminki Levels and repair of cyclobutane pyrimidine dimers and 6-4-photoproducts in skin of sporadic basal cell carcinoma patients J. Invest. Dermatol. 115 2000 95 99
40. K.S. Katiyar, M.S. Matsui, and H. Mukhutar Kinetics of UV light-induced cyclobutane pyrimidine dimers in human skin in vivo: an immunohistochemical analysis of both epidermis and dermis Photochem. Photobiol. 72 2000 788 793
41. D.L. Mitchell, M. Byrom, S. Chiarello, and M.G. Lowery Effects of chronic exposure to ultraviolet B radiation on DNA repair in the dermis and epidermis of the hairless mouse J. Invest. Dermatol. 116 2001 209 215
42. 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
43. W. Peng, and B.R. Shaw Accelerated deamination of cytosine residues in UV-induced cyclobutane pyrimidine dimers leads to CC→TT transitions Biochemistry 35 1996 10172 10181
44. P.E. Gibbs, and C.W. Lawrence U-U and T-T cyclobutane dimers have different mutational properties Nucleic Acids Res. 21 1993 4059 4065
45. K.H. Kraemer Sunlight and skin cancer: another link revealed Proc. Natl. Acad. Sci. U.S.A. 94 1997 11 14
46. J. Cotton, and D.F. Spandau Ultraviolet B-radiation dose influences the induction of apoptosis and p53 in human keratinocytes Radiat. Res. 147 1997 148 155
47. A. Stary, P. Kannouche, A.R. Lehmann, and A. Sarasin Role of DNA polymerase eta in the UV mutation spectrum in human cells J. Biol. Chem. 278 2003 18767 18775
48. N. Nikolaishvili-Feinberg, and M. Cordeiro-Stone Discrimination between translesion synthesis and template switching during bypass replication of thymine dimers in duplex DNA J. Biol. Chem. 275 2000 30943 30950
49. M. Ljungman, and F. Zhang Blockage of RNA polymerase as a possible trigger for u.v. light-induced apoptosis Oncogene 13 1996 823 831
50. B.C. McKay, M. Ljungman, and A.J. Rainbow Persistent DNA damage induced by ultraviolet light inhibits p21waf1 and bax expression: implications for DNA repair, UV sensitivity and the induction of apoptosis Oncogene 17 1998 545 555
51. M. van Oosten, H. Rebel, E.C. Friedberg, H. van Steeg, G.T. van der Horst, H.J. van Kranen, A. Westerman, A.A. van Zeeland, L.H. Mullenders, and F.R. de Gruijl Differential role of transcription-coupled repair in UVB-induced G2 arrest and apoptosis in mouse epidermis Proc. Natl. Acad. Sci. U.S.A. 97 2000 11268 11273
52. L. Proietti De Santis, C.L. Garcia, A.S. Balajee, P. Latini, P. Pichierri, O. Nikaido, M. Stefanini, and F. Palitti Transcription coupled repair efficiency determines the cell cycle progression and apoptosis after UV exposure in hamster cells DNA Repair 1 2002 209 223
53. G. Spivak, T. Itoh, T. Matsunaga, O. Nikaido, P. Hanawalt, and M. Yamaizumi Ultraviolet-sensitive syndrome cells are defective in transcription-coupled repair of cyclobutane pyrimidine dimers DNA Repair 1 2002 629 643
54. B.S. Rosenstein, and D.L. Mitchell The repair of DNA damages induced in normal human skin fibroblasts exposed to simulated sunlight Radiat. Res. 126 1991 338 342
55. P.J. Rochette, J.P. Therrien, R. Drouin, D. Perdiz, N. Bastien, E.A. Drobetsky, and E. Sage UVA-induced cyclobutane pyrimidine dimers form predominantly at thymine-thymine dipyrimidines and correlate with the mutation spectrum in rodent cells Nucleic Acids Res. 31 2003 2786 2794