How DNA lesions are turned into powerful killing structures: Insights from UV-induced apoptosis

Mutation Research - Reviews in Mutation Research

Volumn 681, Issue 2-3, 2009, Pages 197-208

  Batista, Luís F Z ^a,b   Kaina, Bernd ^b   Meneghini, Rogério ^c   Menck, Carlos F M ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c Latin American and Caribbean Center on Health Sciences Information   (Brazil)

Author keywords

Apoptosis; Damage signaling; DNA damage; Photoproducts; Ultraviolet light

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; DEATH RECEPTOR; DOUBLE STRANDED DNA; LIPID PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PYRIMIDINE DERIVATIVE; PYRIMIDINE DIMER; PYRIMIDINONE DERIVATIVE; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; AUTOPHAGY; CANCER PREVENTION; CANCER THERAPY; CELL CYCLE S PHASE; CELL DEATH; CELL KILLING; CELL STRESS; DNA ADDUCT; DNA DAMAGE; DNA METABOLISM; DNA REPAIR; DNA REPLICATION; GENOTOXICITY; HUMAN; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; RADIATION ABSORPTION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ULTRAVIOLET A RADIATION; ULTRAVIOLET B RADIATION; ULTRAVIOLET C RADIATION; ULTRAVIOLET IRRADIATION;

ANIMALS; APOPTOSIS; AUTOPHAGY; BASE SEQUENCE; DNA DAMAGE; DNA REPLICATION; HUMANS; MOLECULAR SEQUENCE DATA; TRANSCRIPTION, GENETIC; ULTRAVIOLET RAYS;

MAMMALIA;

EID: 59349109196     PISSN: 13835742     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrrev.2008.09.001     Document Type: Review

References (173)

1. Cockell C.S., and Horneck G. The history of the UV radiation climate of the earth-theoretical and space-based observations. Photochem. Photobiol. 73 (2001) 447-451
2. Friedberg E.C. Correcting the Blueprint of Life: An Historical Account of the Discovery of DNA Repair Mechanisms (1997), Cold Spring Harbor Laboratory Press, Plainview, NY
3. van der Leun J.C. The ozone layer. Photodermatol. Photoimmunol. Photomed. 20 (2004) 159-162
4. Norval M. The mechanisms and consequences of ultraviolet-induced immunosuppression. Prog. Biophys. Mol. Biol. 92 (2006) 108-118
5. Woodhead A.D., Setlow R.B., and Tanaka M. Environmental factors in nonmelanoma and melanoma skin cancer. J. Epidemiol. 9 (1999) S102-S114
6. Svobodova A., Walterova D., and Vostalova J. Ultraviolet light induced alteration to the skin. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc Czech Repub. 150 (2006) 25-38
7. Melnikova V.O., and Ananthaswamy H.N. Cellular and molecular events leading to the development of skin cancer. Mutat. Res. 571 (2005) 91-106
8. Claerhout S., Van Laethem A., Agostinis P., and Garmyn M. Pathways involved in sunburn cell formation: deregulation in skin cancer. Photochem. Photobiol. Sci. 5 (2006) 199-207
9. Fisher M.S., and Kripke M.L. Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis. Proc. Natl. Acad. Sci. U.S.A. 74 (1977) 1688-1692
10. Mouret S., Baudouin C., Charveron M., Favier A., Cadet J., and Douki T. Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 13765-13770
11. Cadet J., Sage E., and Douki T. Ultraviolet radiation-mediated damage to cellular DNA. Mutat. Res. 571 (2005) 3-17
12. Pattison D.I., and Davies M.J. Actions of ultraviolet light on cellular structures. Exs (2006) 131-157
13. Ravanat J.L., Douki T., and Cadet J. Direct and indirect effects of UV radiation on DNA and its components. J. Photochem. Photobiol. B 63 (2001) 88-102
14. Douki T., Reynaud-Angelin A., Cadet J., and Sage E. 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
15. Perdiz D., Grof P., Mezzina M., Nikaido O., Moustacchi E., and Sage E. 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
16. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., and Ellenberger T. DNA Repair and Mutagenesis (2006), ASM Press, Washington
17. Mitchell D.L. The relative cytotoxicity of (6-4) photoproducts and cyclobutane dimers in mammalian cells. Photochem. Photobiol. 48 (1988) 51-57
18. Douki T., and Cadet J. 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
19. Besaratinia A., Synold T.W., Chen H.H., Chang C., Xi B., Riggs A.D., and Pfeifer G.P. 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 (2005) 10058-10063
20. Costa R.M., Chigancas V., Galhardo Rda S., Carvalho H., and Menck C.F. The eukaryotic nucleotide excision repair pathway. Biochimie 85 (2003) 1083-1099
21. Proietti De Santis L., Garcia C.L., Balajee A.S., Latini P., Pichierri P., Nikaido O., Stefanini M., and Palitti F. Transcription coupled repair efficiency determines the cell cycle progression and apoptosis after UV exposure in hamster cells. DNA Repair (Amst.) 1 (2002) 209-223
22. Ford J.M. Regulation of DNA damage recognition and nucleotide excision repair: another role for p53. Mutat. Res. 577 (2005) 195-202
23. Volker M., Mone M.J., Karmakar P., van Hoffen A., Schul W., Vermeulen W., Hoeijmakers J.H., van Driel R., van Zeeland A.A., and Mullenders L.H. Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8 (2001) 213-224
24. Sarasin A., and Stary A. New insights for understanding the transcription-coupled repair pathway. DNA Repair (Amst.) 6 (2007) 265-269
25. Brueckner F., and Cramer P. DNA photodamage recognition by RNA polymerase II. FEBS Lett. 581 (2007) 2757-2760
26. Hanawalt P.C. Subpathways of nucleotide excision repair and their regulation. Oncogene 21 (2002) 8949-8956
27. Menck C.F. Shining a light on photolyases. Nat. Genet. 32 (2002) 338-339
28. Garinis G.A., Jans J., and van der Horst G.T. Photolyases: capturing the light to battle skin cancer. Future Oncol. 2 (2006) 191-199
29. Lehmann A.R. DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie 85 (2003) 1101-1111
30. Dunkern T.R., Fritz G., and Kaina B. Ultraviolet light-induced DNA damage triggers apoptosis in nucleotide excision repair-deficient cells via Bcl-2 decline and caspase-3/-8 activation. Oncogene 20 (2001) 6026-6038
31. Meunier J.R., Sarasin A., and Marrot L. Photogenotoxicity of mammalian cells: a review of the different assays for in vitro testing. Photochem. Photobiol. 75 (2002) 437-447
32. Jans J., Schul W., Sert Y.G., Rijksen Y., Rebel H., Eker A.P., Nakajima S., van Steeg H., de Gruijl F.R., Yasui A., Hoeijmakers J.H., and van der Horst G.T. Powerful skin cancer protection by a CPD-photolyase transgene. Curr. Biol. 15 (2005) 105-115
33. Schul W., Jans J., Rijksen Y.M., Klemann K.H., Eker A.P., de Wit J., Nikaido O., Nakajima S., Yasui A., Hoeijmakers J.H., and van der Horst G.T. Enhanced repair of cyclobutane pyrimidine dimers and improved UV resistance in photolyase transgenic mice. EMBO J. 21 (2002) 4719-4729
34. Courdavault S., Baudouin C., Charveron M., Canguilhem B., Favier A., Cadet J., and Douki T. Repair of the three main types of bipyrimidine DNA photoproducts in human keratinocytes exposed to UVB and UVA radiations. DNA Repair (Amst.) 4 (2005) 836-844
35. Mei Kwei J.S., Kuraoka I., Horibata K., Ubukata M., Kobatake E., Iwai S., Handa H., and Tanaka K. Blockage of RNA polymerase II at a cyclobutane pyrimidine dimer and 6-4 photoproduct. Biochem. Biophys. Res. Commun. 320 (2004) 1133-1138
36. Bohr V.A., Smith C.A., Okumoto D.S., and Hanawalt P.C. DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40 (1985) 359-369
37. Kusumoto R., Masutani C., Sugasawa K., Iwai S., Araki M., Uchida A., Mizukoshi T., and Hanaoka F. Diversity of the damage recognition step in the global genomic nucleotide excision repair in vitro. Mutat. Res. 485 (2001) 219-227
38. Chigancas V., Batista L.F., Brumatti G., Amarante-Mendes G.P., Yasui A., and Menck C.F. Photorepair of RNA polymerase arrest and apoptosis after ultraviolet irradiation in normal and XPB deficient rodent cells. Cell Death Differ. 9 (2002) 1099-1107
39. Chigancas V., Miyaji E.N., Muotri A.R., de Fatima Jacysyn J., Amarante-Mendes G.P., Yasui A., and Menck C.F. Photorepair prevents ultraviolet-induced apoptosis in human cells expressing the marsupial photolyase gene. Cancer Res. 60 (2000) 2458-2463
40. Broughton B.C., Lehmann A.R., Harcourt S.A., Arlett C.F., Sarasin A., Kleijer W.J., Beemer F.A., Nairn R., and Mitchell D.L. Relationship between pyrimidine dimers, 6-4 photoproducts, repair synthesis and cell survival: studies using cells from patients with trichothiodystrophy. Mutat. Res. 235 (1990) 33-40
41. Nishigaki R., Mitani H., and Shima A. Evasion of UVC-induced apoptosis by photorepair of cyclobutane pyrimidine dimers. Exp. Cell Res. 244 (1998) 43-53
42. Lima-Bessa K.M., and Menck C.F. Skin cancer: lights on genome lesions. Curr. Biol. 15 (2005) R58-R61
43. Nakajima S., Lan L., Kanno S., Takao M., Yamamoto K., Eker A.P., and Yasui A. UV light-induced DNA damage and tolerance for the survival of nucleotide excision repair-deficient human cells. J. Biol. Chem. 279 (2004) 46674-46677
44. Lo H.L., Nakajima S., Ma L., Walter B., Yasui A., Ethell D.W., and Owen L.B. Differential biologic effects of CPD and 6-4PP UV-induced DNA damage on the induction of apoptosis and cell-cycle arrest. BMC Cancer 5 (2005) 135
45. Lima-Bessa K.M., Armelini M.G., Chigancas V., Jacysyn J.F., Amarante-Mendes G.P., Sarasin A., and Menck C.F. CPDs and 6-4PPs play different roles in UV-induced cell death in normal and NER-deficient human cells. DNA Repair (Amst.) 7 (2008) 303-312
46. Green D.R. At the gates of death. Cancer Cell 9 (2006) 328-330
47. Ljungman M., and Zhang F. Blockage of RNA polymerase as a possible trigger for u.v. light-induced apoptosis. Oncogene 13 (1996) 823-831
48. Garssen J., van Steeg H., de Gruijl F., de Boer J., van der Horst G.T., van Kranen H., van Loveren H., van Dijk M., Fluitman A., Weeda G., and Hoeijmakers J.H. Transcription-coupled and global genome repair differentially influence UV-B-induced acute skin effects and systemic immunosuppression. J. Immunol. 164 (2000) 6199-6205
49. McKay B.C., Becerril C., Spronck J.C., and Ljungman M. Ultraviolet light-induced apoptosis is associated with S-phase in primary human fibroblasts. DNA Repair (Amst.) 1 (2002) 811-820
50. Dunkern T.R., and Kaina B. Cell proliferation and DNA breaks are involved in ultraviolet light-induced apoptosis in nucleotide excision repair-deficient Chinese hamster cells. Mol. Biol. Cell 13 (2002) 348-361
51. Carvalho H., da Costa R.M., Chigancas V., Weinlich R., Brumatti G., Amarante-Mendes G.P., Sarasin A., and Menck C.F. Effect of cell confluence on ultraviolet light apoptotic responses in DNA repair deficient cells. Mutat. Res. 544 (2003) 159-166
52. Carvalho H., Ortolan T.G., Depaula T., Leite R.A., Weinlich R., Amarante-Mendes G.P., and Menck C.F. Sustained activation of p53 in confluent nucleotide excision repair-deficient cells resistant to ultraviolet-induced apoptosis. DNA Repair (Amst.) (2008)
53. da Costa R.M., Quayle C., de Fatima Jacysyn J., Amarante-Mendes G.P., Sarasin A., and Menck C.F. Resistance to ultraviolet-induced apoptosis in DNA repair deficient growth arrested human fibroblasts is not related to recovery from RNA transcription blockage. Mutat. Res. 640 (2008) 1-7
54. Batista L.F., Chigancas V., Brumatti G., Amarante-Mendes G.P., and Menck C.F. Involvement of DNA replication in ultraviolet-induced apoptosis of mammalian cells. Apoptosis 11 (2006) 1139-1148
55. Roos W.P., and Kaina B. DNA damage-induced cell death by apoptosis. Trends Mol. Med. 12 (2006) 440-450
56. Wang T.C., and Smith K.C. Postreplication repair in ultraviolet-irradiated human fibroblasts: formation and repair of DNA double-strand breaks. Carcinogenesis 7 (1986) 389-392
57. Schumacher R.I., Menck C.F., and Meneghini R. Sites sensitive to S1 nuclease and discontinuities in DNA nascent strands of ultraviolet irradiated mouse cells. Photochem. Photobiol. 37 (1983) 605-610
58. Lips J., and Kaina B. DNA double-strand breaks trigger apoptosis in p53-deficient fibroblasts. Carcinogenesis 22 (2001) 579-585
59. Nitiss J.L., Nitiss K.C., Rose A., and Waltman J.L. Overexpression of type I topoisomerases sensitizes yeast cells to DNA damage. J. Biol. Chem. 276 (2001) 26708-26714
60. Soe K., Rockstroh A., Schache P., and Grosse F. The human topoisomerase I damage response plays a role in apoptosis. DNA Repair (Amst.) 3 (2004) 387-393
61. Corbett A.H., Zechiedrich E.L., Lloyd R.S., and Osheroff N. Inhibition of eukaryotic topoisomerase II by ultraviolet-induced cyclobutane pyrimidine dimers. J. Biol. Chem. 266 (1991) 19666-19671
62. Tomicic M.T., Christmann M., and Kaina B. Topotecan-triggered degradation of topoisomerase I is p53-dependent and impacts cell survival. Cancer Res. 65 (2005) 8920-8926
63. Ljungman M., and Lane D.P. Transcription-guarding the genome by sensing DNA damage. Nat. Rev. Cancer 4 (2004) 727-737
64. McGlynn P., and Lloyd R.G. Recombinational repair and restart of damaged replication forks. Nat. Rev. Mol. Cell. Biol. 3 (2002) 859-870
65. Pouget J.P., Douki T., Richard M.J., and Cadet J. 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
66. Sies H., and Menck C.F. Singlet oxygen induced DNA damage. Mutat. Res. 275 (1992) 367-375
67. Wilson D.M., and Bohr III V.A. The mechanics of base excision repair, and its relationship to aging and disease. DNA Repair (Amst.) 6 (2007) 544-559
68. Hirano T., Kawai K., Ootsuyama Y., Orimo H., and Kasai H. Detection of a mouse OGG1 fragment during caspase-dependent apoptosis: oxidative DNA damage and apoptosis. Cancer Sci. 95 (2004) 634-638
69. Daroui P., Desai S.D., Li T.K., Liu A.A., and Liu L.F. Hydrogen peroxide induces topoisomerase I-mediated DNA damage and cell death. J. Biol. Chem. 279 (2004) 14587-14594
70. Kielbassa C., Roza L., and Epe B. Wavelength dependence of oxidative DNA damage induced by UV and visible light. Carcinogenesis 18 (1997) 811-816
71. Tornaletti S., Maeda L.S., and Hanawalt P.C. Transcription arrest at an abasic site in the transcribed strand of template DNA. Chem. Res. Toxicol. 19 (2006) 1215-1220
72. Larsen E., Kwon K., Coin F., Egly J.M., and Klungland A. Transcription activities at 8-oxoG lesions in DNA. DNA Repair (Amst.) 3 (2004) 1457-1468
73. Kathe S.D., Shen G.P., and Wallace S.S. Single-stranded breaks in DNA but not oxidative DNA base damages block transcriptional elongation by RNA polymerase II in HeLa cell nuclear extracts. J. Biol. Chem. 279 (2004) 18511-18520
74. Marnett L.J. Lipid peroxidation-DNA damage by malondialdehyde. Mutat. Res. 424 (1999) 83-95
75. Marnett L.J. Oxyradicals and DNA damage. Carcinogenesis 21 (2000) 361-370
76. Wenk J., Brenneisen P., Meewes C., Wlaschek M., Peters T., Blaudschun R., Ma W., Kuhr L., Schneider L., and Scharffetter-Kochanek K. UV-induced oxidative stress and photoaging. Curr. Probl. Dermatol. 29 (2001) 83-94
77. Bongarzone E.R., Pasquini J.M., and Soto E.F. Oxidative damage to proteins and lipids of CNS myelin produced by in vitro generated reactive oxygen species. J. Neurosci. Res. 41 (1995) 213-221
78. de Kok T.M., ten Vaarwerk F., Zwingman I., van Maanen J.M., and Kleinjans J.C. Peroxidation of linoleic, arachidonic and oleic acid in relation to the induction of oxidative DNA damage and cytogenetic effects. Carcinogenesis 15 (1994) 1399-1404
79. Girotti A.W. Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms. J. Photochem. Photobiol. B 63 (2001) 103-113
80. Farber J.L. Mechanisms of cell injury by activated oxygen species. Environ. Health Perspect. 102 Suppl. 10 (1994) 17-24
81. Adams J.M. Ways of dying: multiple pathways to apoptosis. Genes Dev. 17 (2003) 2481-2495
82. Chipuk J.E., Bouchier-Hayes L., and Green D.R. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ. 13 (2006) 1396-1402
83. Li J.L., Liu N., Chen X.H., Sun M., and Wang C.B. Inhibition of UVA-induced apoptotic signaling pathway by polypeptide from Chlamys farreri in human HaCaT keratinocytes. Radiat. Environ. Biophys. 46 (2007) 263-268
84. Basu-Modak S., Gordon M.J., Dobson L.H., Spencer J.P., Rice-Evans C., and Tyrrell R.M. Epicatechin and its methylated metabolite attenuate UVA-induced oxidative damage to human skin fibroblasts. Free Radical Biol. Med. 35 (2003) 910-921
85. Offord E.A., Gautier J.C., Avanti O., Scaletta C., Runge F., Kramer K., and Applegate L.A. Photoprotective potential of lycopene, beta-carotene, vitamin E, vitamin C and carnosic acid in UVA-irradiated human skin fibroblasts. Free Radical Biol. Med. 32 (2002) 1293-1303
86. Chung J.H., Han J.H., Hwang E.J., Seo J.Y., Cho K.H., Kim K.H., Youn J.I., and Eun H.C. Dual mechanisms of green tea extract (EGCG)-induced cell survival in human epidermal keratinocytes. FASEB J. 17 (2003) 1913-1915
87. Ibuki Y., Allanson M., Dixon K.M., and Reeve V.E. Radiation sources providing increased UVA/UVB ratios attenuate the apoptotic effects of the UVB waveband UVA-dose-dependently in hairless mouse skin. J. Invest. Dermatol. 127 (2007) 2236-2244
88. Tyrrell R.M. Solar ultraviolet A radiation: an oxidizing skin carcinogen that activates heme oxygenase-1. Antioxid. Redox Signal. 6 (2004) 835-840
89. Reeve V.E., and Tyrrell R.M. Heme oxygenase induction mediates the photoimmunoprotective activity of UVA radiation in the mouse. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 9317-9321
90. Kulms D., Zeise E., Poppelmann B., and Schwarz T. DNA damage, death receptor activation and reactive oxygen species contribute to ultraviolet radiation-induced apoptosis in an essential and independent way. Oncogene 21 (2002) 5844-5851
91. Kulms D., and Schwarz T. Independent contribution of three different pathways to ultraviolet-B-induced apoptosis. Biochem. Pharmacol. 64 (2002) 837-841
92. Ashkenazi A., and Dixit V.M. Death receptors: signaling and modulation. Science 281 (1998) 1305-1308
93. Gaur U., and Aggarwal B.B. Regulation of proliferation, survival and apoptosis by members of the TNF superfamily. Biochem. Pharmacol. 66 (2003) 1403-1408
94. Peter M.E., and Krammer P.H. Mechanisms of CD95 (APO-1/Fas)-mediated apoptosis. Curr. Opin. Immunol. 10 (1998) 545-551
95. Chinnaiyan A.M., O'Rourke K., Tewari M., and Dixit V.M. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 81 (1995) 505-512
96. Chinnaiyan A.M., Tepper C.G., Seldin M.F., O'Rourke K., Kischkel F.C., Hellbardt S., Krammer P.H., Peter M.E., and Dixit V.M. FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271 (1996) 4961-4965
97. Rosette C., and Karin M. Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274 (1996) 1194-1197
98. Aragane Y., Kulms D., Metze D., Wilkes G., Poppelmann B., Luger T.A., and Schwarz T. Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/APO-1) independently of its ligand CD95L. J. Cell. Biol. 140 (1998) 171-182
99. Rehemtulla A., Hamilton C.A., Chinnaiyan A.M., and Dixit V.M. Ultraviolet radiation-induced apoptosis is mediated by activation of CD-95 (Fas/APO-1). J. Biol. Chem. 272 (1997) 25783-25786
100. Ouhtit A., Gorny A., Muller H.K., Hill L.L., Owen-Schaub L., and Ananthaswamy H.N. Loss of Fas-ligand expression in mouse keratinocytes during UV carcinogenesis. Am. J. Pathol. 157 (2000) 1975-1981
101. Mlakar V., and Glavac D. DNA microarrays and their use in dermatology. Acta Derm. Venerol. Alp Panonica Adriat 16 (2007) 7-12
102. Sesto A., Navarro M., Burslem F., and Jorcano J.L. Analysis of the ultraviolet B response in primary human keratinocytes using oligonucleotide microarrays. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 2965-2970
103. da Costa R.M., Riou L., Paquola A., Menck C.F., and Sarasin A. Transcriptional profiles of unirradiated or UV-irradiated human cells expressing either the cancer-prone XPB/CS allele or the noncancer-prone XPB/TTD allele. Oncogene 24 (2005) 1359-1374
104. McGowan C.H., and Russell P. The DNA damage response: sensing and signaling. Curr. Opin. Cell Biol. 16 (2004) 629-633
105. Durocher D., and Jackson S.P. DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme?. Curr. Opin. Cell Biol. 13 (2001) 225-231
106. Abraham R.T. PI 3-kinase related kinases: 'big' players in stress-induced signaling pathways. DNA Repair (Amst.) 3 (2004) 883-887
107. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3 (2003) 155-168
108. Falck J., Coates J., and Jackson S.P. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434 (2005) 605-611
109. Zou L., Liu D., and Elledge S.J. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 13827-13832
110. Zou L., and Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300 (2003) 1542-1548
111. Cortez D., Guntuku S., Qin J., and Elledge S.J. ATR and ATRIP: partners in checkpoint signaling. Science 294 (2001) 1713-1716
112. Sancar A., Lindsey-Boltz L.A., Unsal-Kacmaz K., and Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73 (2004) 39-85
113. Jazayeri A., Falck J., Lukas C., Bartek J., Smith G.C., Lukas J., and Jackson S.P. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8 (2006) 37-45
114. Myers J.S., and Cortez D. Rapid activation of ATR by ionizing radiation requires ATM and Mre11. J. Biol. Chem. 281 (2006) 9346-9350
115. Stiff T., Walker S.A., Cerosaletti K., Goodarzi A.A., Petermann E., Concannon P., O'Driscoll M., and Jeggo P.A. ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J. 25 (2006) 5775-5782
116. Zhang Y., Ma W.Y., Kaji A., Bode A.M., and Dong Z. Requirement of ATM in UVA-induced signaling and apoptosis. J. Biol. Chem. 277 (2002) 3124-3131
117. Derheimer F.A., O'Hagan M.H., Krueger H.M., Hanasoge S., Paulsen M.T., and Ljungman M. RPA and ATR link transcriptional stress to p53. Proc. Natl. Acad. Sci. U.S.A. (2007)
118. Latonen L., and Laiho M. Cellular UV damage responses-functions of tumor suppressor p53. Biochim. Biophys. Acta 1755 (2005) 71-89
119. Efeyan A., and Serrano M. p53: guardian of the genome and policeman of the oncogenes. Cell Cycle 6 (2007) 1006-1010
120. Oren M. Decision making by p53: life, death and cancer. Cell Death Differ. 10 (2003) 431-442
121. Yamaizumi M., and Sugano T. U.v.-induced nuclear accumulation of p53 is evoked through DNA damage of actively transcribed genes independent of the cell cycle. Oncogene 9 (1994) 2775-2784
122. Dumaz N., Duthu A., Ehrhart J.C., Drougard C., Appella E., Anderson C.W., May P., Sarasin A., and Daya-Grosjean L. Prolonged p53 protein accumulation in trichothiodystrophy fibroblasts dependent on unrepaired pyrimidine dimers on the transcribed strands of cellular genes. Mol. Carcinogen. 20 (1997) 340-347
123. Das S., Boswell S.A., Aaronson S.A., and Lee S.W. P53 promoter selection: choosing between life and death. Cell Cycle 7 (2008) 154-157
124. Halazonetis T.D., Gorgoulis V.G., and Bartek J. An oncogene-induced DNA damage model for cancer development. Science 319 (2008) 1352-1355
125. Janicke R.U., Sohn D., and Schulze-Osthoff K. The dark side of a tumor suppressor: anti-apoptotic p53. Cell Death Differ. (2008)
126. Boldrup L., Bourdon J.C., Coates P.J., Sjostrom B., and Nylander K. Expression of p53 isoforms in squamous cell carcinoma of the head and neck. Eur. J. Cancer 43 (2007) 617-623
127. Bourdon J.C. p53 and its isoforms in cancer. Br. J. Cancer 97 (2007) 277-282
128. Hildesheim J., and Fornace Jr. A.J. The dark side of light: the damaging effects of UV rays and the protective efforts of MAP kinase signaling in the epidermis. DNA Repair (Amst.) 3 (2004) 567-580
129. Lu Z., and Xu S. ERK1/2 MAP kinases in cell survival and apoptosis. IUBMB Life 58 (2006) 621-631
130. Owens D.M., and Keyse S.M. Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene 26 (2007) 3203-3213
131. Cuevas B.D., Abell A.N., and Johnson G.L. Role of mitogen-activated protein kinase kinase kinases in signal integration. Oncogene 26 (2007) 3159-3171
132. Raman M., Chen W., and Cobb M.H. Differential regulation and properties of MAPKs. Oncogene 26 (2007) 3100-3112
133. Herrlich P., Karin M., and Weiss C. Supreme EnLIGHTenment: damage recognition and signaling in the mammalian UV response. Mol. Cell 29 (2008) 279-290
134. Fritz G., and Kaina B. Late activation of stress kinases (SAPK/JNK) by genotoxins requires the DNA repair proteins DNA-PKcs and CSB. Mol. Biol. Cell 17 (2006) 851-861
135. Devary Y., Rosette C., DiDonato J.A., and Karin M. NF-kappa B activation by ultraviolet light not dependent on a nuclear signal. Science 261 (1993) 1442-1445
136. Coffer P.J., Burgering B.M., Peppelenbosch M.P., Bos J.L., and Kruijer W. UV activation of receptor tyrosine kinase activity. Oncogene 11 (1995) 561-569
137. Nehme A., Baskaran R., Aebi S., Fink D., Nebel S., Cenni B., Wang J.Y., Howell S.B., and Christen R.D. Differential induction of c-Jun NH2-terminal kinase and c-Abl kinase in DNA mismatch repair-proficient and -deficient cells exposed to cisplatin. Cancer Res. 57 (1997) 3253-3257
138. Nehme A., Baskaran R., Nebel S., Fink D., Howell S.B., Wang J.Y., and Christen R.D. Induction of JNK and c-Abl signalling by cisplatin and oxaliplatin in mismatch repair-proficient and -deficient cells. Br. J. Cancer 79 (1999) 1104-1110
139. She Q.B., Ma W.Y., Zhong S., and Dong Z. Activation of JNK1, RSK2, and MSK1 is involved in serine 112 phosphorylation of Bad by ultraviolet B radiation. J. Biol. Chem. 277 (2002) 24039-24048
140. She Q.B., Ma W.Y., and Dong Z. Role of MAP kinases in UVB-induced phosphorylation of p53 at serine 20. Oncogene 21 (2002) 1580-1589
141. Hildesheim J., Awwad R.T., and Fornace Jr. A.J. p38 mitogen-activated protein kinase inhibitor protects the epidermis against the acute damaging effects of ultraviolet irradiation by blocking apoptosis and inflammatory responses. J. Invest. Dermatol. 122 (2004) 497-502
142. Tournier C., Hess P., Yang D.D., Xu J., Turner T.K., Nimnual A., Bar-Sagi D., Jones S.N., Flavell R.A., and Davis R.J. Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288 (2000) 870-874
143. Behrens A., Sibilia M., and Wagner E.F. Amino-terminal phosphorylation of c-Jun regulates stress-induced apoptosis and cellular proliferation. Nat. Genet. 21 (1999) 326-329
144. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 103 (2000) 239-252
145. Lei K., Nimnual A., Zong W.X., Kennedy N.J., Flavell R.A., Thompson C.B., Bar-Sagi D., and Davis R.J. The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH(2)-terminal kinase. Mol. Cell Biol. 22 (2002) 4929-4942
146. Tsuruta F., Sunayama J., Mori Y., Hattori S., Shimizu S., Tsujimoto Y., Yoshioka K., Masuyama N., and Gotoh Y. JNK promotes Bax translocation to mitochondria through phosphorylation of 14-3-3 proteins. EMBO J. 23 (2004) 1889-1899
147. Weston C.R., and Davis R.J. The JNK signal transduction pathway. Curr. Opin. Cell Biol. 19 (2007) 142-149
148. Faris M., Latinis K.M., Kempiak S.J., Koretzky G.A., and Nel A. Stress-induced Fas ligand expression in T cells is mediated through a MEK kinase 1-regulated response element in the Fas ligand promoter. Mol. Cell Biol. 18 (1998) 5414-5424
149. Kolbus A., Herr I., Schreiber M., Debatin K.M., Wagner E.F., and Angel P. c-Jun-dependent CD95-L expression is a rate-limiting step in the induction of apoptosis by alkylating agents. Mol. Cell Biol. 20 (2000) 575-582
150. Hess J., Angel P., and Schorpp-Kistner M. AP-1 subunits: quarrel and harmony among siblings. J. Cell Sci. 117 (2004) 5965-5973
151. Christmann M., Tomicic M.T., Aasland D., and Kaina B. A role for UV-light-induced c-Fos: stimulation of nucleotide excision repair and protection against sustained JNK activation and apoptosis. Carcinogenesis 28 (2007) 183-190
152. Muller M., Wilder S., Bannasch D., Israeli D., Lehlbach K., Li-Weber M., Friedman S.L., Galle P.R., Stremmel W., Oren M., and Krammer P.H. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J. Exp. Med. 188 (1998) 2033-2045
153. Roos W.P., Batista L.F., Naumann S.C., Wick W., Weller M., Menck C.F., and Kaina B. Apoptosis in malignant glioma cells triggered by the temozolomide-induced DNA lesion O6-methylguanine. Oncogene 26 (2007) 186-197
154. Haas S., and Kaina B. c-Fos is involved in the cellular defence against the genotoxic effect of UV radiation. Carcinogenesis 16 (1995) 985-991
155. Kaina B., Haas S., and Kappes H. A general role for c-Fos in cellular protection against DNA-damaging carcinogens and cytostatic drugs. Cancer Res. 57 (1997) 2721-2731
156. Christmann M., Tomicic M.T., Origer J., Aasland D., and Kaina B. c-Fos is required for excision repair of UV-light induced DNA lesions by triggering the re-synthesis of XPF. Nucleic Acids Res. (2006)
157. Brozovic A., Fritz G., Christmann M., Zisowsky J., Jaehde U., Osmak M., and Kaina B. Long-term activation of SAPK/JNK, p38 kinase and fas-L expression by cisplatin is attenuated in human carcinoma cells that acquired drug resistance. Int. J. Cancer 112 (2004) 974-985
158. Mansouri A., Ridgway L.D., Korapati A.L., Zhang Q., Tian L., Wang Y., Siddik Z.H., Mills G.B., and Claret F.X. Sustained activation of JNK/p38 MAPK pathways in response to cisplatin leads to Fas ligand induction and cell death in ovarian carcinoma cells. J. Biol. Chem. 278 (2003) 19245-19256
159. Schuler M., and Green D.R. Mechanisms of p53-dependent apoptosis. Biochem. Soc. Trans. 29 (2001) 684-688
160. Levine B. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120 (2005) 159-162
161. Levine B., and Klionsky D.J. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6 (2004) 463-477
162. Vicencio J.M., Galluzzi L., Tajeddine N., Ortiz C., Criollo A., Tasdemir E., Morselli E., Ben Younes A., Maiuri M.C., Lavandero S., and Kroemer G. Senescence, apoptosis or autophagy? When a damaged cell must decide its path-a mini-review. Gerontology 54 (2008) 92-99
163. Gozuacik D., and Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23 (2004) 2891-2906
164. Paglin S., Hollister T., Delohery T., Hackett N., McMahill M., Sphicas E., Domingo D., and Yahalom J. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 61 (2001) 439-444
165. Jia L., Dourmashkin R.R., Allen P.D., Gray A.B., Newland A.C., and Kelsey S.M. Inhibition of autophagy abrogates tumour necrosis factor alpha induced apoptosis in human T-lymphoblastic leukaemic cells. Br. J. Haematol. 98 (1997) 673-685
166. Espert L., Denizot M., Grimaldi M., Robert-Hebmann V., Gay B., Varbanov M., Codogno P., and Biard-Piechaczyk M. Autophagy is involved in T cell death after binding of HIV-1 envelope proteins to CXCR4. J. Clin. Invest. 116 (2006) 2161-2172
167. Canu N., Tufi R., Serafino A.L., Amadoro G., Ciotti M.T., and Calissano P. Role of the autophagic-lysosomal system on low potassium-induced apoptosis in cultured cerebellar granule cells. J. Neurochem. 92 (2005) 1228-1242
168. Ding W.X., Ni H.M., Gao W., Hou Y.F., Melan M.A., Chen X., Stolz D.B., Shao Z.M., and Yin X.M. Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J. Biol. Chem. 282 (2007) 4702-4710
169. Wang Y., Singh R., Massey A.C., Kane S.S., Kaushik S., Grant T., Xiang Y., Cuervo A.M., and Czaja M.J. Loss of macroautophagy promotes or prevents fibroblast apoptosis depending on the death stimulus. J. Biol. Chem. 283 (2008) 4766-4777
170. Yue Z., Jin S., Yang C., Levine A.J., and Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 15077-15082
171. Mills K.R., Reginato M., Debnath J., Queenan B., and Brugge J.S. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is required for induction of autophagy during lumen formation in vitro. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 3438-3443
172. Pattingre S., Tassa A., Qu X., Garuti R., Liang X.H., Mizushima N., Packer M., Schneider M.D., and Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122 (2005) 927-939
173. Miller D.L., and Weinstock M.A. Nonmelanoma skin cancer in the United States: incidence. J. Am. Acad. Dermatol. 30 (1994) 774-778