Activation of p38 MAP kinase and JNK pathways by UVA irradiation

Photochemical and Photobiological Sciences

Volumn 11, Issue 1, 2012, Pages 54-61

  Zhang, Jack ^a   Bowden, G Tim ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84255197202     PISSN: 1474905X     EISSN: 14749092     Source Type: Journal    
DOI: 10.1039/c1pp05133d     Document Type: Review

References (101)

1. G. T. Bowden Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling Nat. Rev. Cancer 2004 4 23 35 (Pubitemid 38082151)
2. A. I. Rubin E. H. Chen D. Ratner Basal-cell carcinoma N. Engl. J. Med. 2005 353 2262 2269 (Pubitemid 41697289)
3. R. V. Patel A. Frankel G. Goldenberg An update on nonmelanoma skin cancer J. Clin. Aesthet. Dermatol. 2011 4 20 27
4. J. A. Cafardi R. Shafi M. Athar C. A. Elmets Prospects for skin cancer treatment and prevention: the potential contribution of an engineered virus J. Invest. Dermatol. 2011 131 559 561
5. D. R. Bickers H. W. Lim D. Margolis M. A. Weinstock C. Goodman E. Faulkner C. Gould E. Gemmen T. Dall The burden of skin diseases: 2004 a joint project of the American Academy of Dermatology Association and the Society for Investigative Dermatology J. Am. Acad. Dermatol. 2006 55 490 500 (Pubitemid 44209289)
6. R. Marks An overview of skin cancers. Incidence and causation Cancer 1995 75 607 612
7. F. R. de Gruijl Photocarcinogenesis: UVA vs. UVB Methods Enzymol. 2000 319 359 366
8. B. Bellei A. Mastrofrancesco S. Briganti N. Aspite N. Ale-Agha H. Sies M. Picardo Ultraviolet A induced modulation of gap junctional intercellular communication by P38 MAPK activation in human keratinocytes Exp. Dermatol. 2008 17 115 124
9. S. Mouret C. Baudouin M. Charveron A. Favier J. Cadet T. Douki Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation Proc. Natl. Acad. Sci. U. S. A. 2006 103 13765 13770 (Pubitemid 44413982)
10. X. X. Huang F. Bernerd G. M. Halliday Ultraviolet A within sunlight induces mutations in the epidermal basal layer of engineered human skin Am. J. Pathol. 2009 174 1534 1543
11. Y. Y. He J. Pi J. L. Huang B. A. Diwan M. P. Waalkes C. F. Chignell Chronic UVA irradiation of human HaCaT keratinocytes induces malignant transformation associated with acquired apoptotic resistance Oncogene 2006 25 3680 3688 (Pubitemid 43980489)
12. M. Ming C. R. Shea L. Feng K. Soltani Y. Y. He UVA Induces Lesions Resembling Seborrheic Keratoses in Mice with Keratinocyte-Specific PTEN Downregulation J. Invest. Dermatol. 2011 131 1583 1586
13. A. de Laat J. C. van der Leun F. R. de Gruijl Carcinogenesis induced by UVA (365-nm) radiation: the dose-time dependence of tumor formation in hairless mice Carcinogenesis 1997 18 1013 1020 (Pubitemid 28132348)
14. H. J. van Kranen A. de Laat J. van de Ven P. W. Wester A. de Vries R. J. Berg C. F. van Kreijl F. R. de Gruijl Low incidence of p53 mutations in UVA (365-nm)-induced skin tumors in hairless mice Cancer Res. 1997 57 1238 1240 (Pubitemid 27152543)
15. D. Hanahan R. A. Weinberg The hallmarks of cancer Cell 2000 100 57 70 (Pubitemid 30046295)
16. F. R. de Gruijl p53 mutations as a marker of skin cancer risk: comparison of UVA and UVB effects Exp. Dermatol. 2002 11 s1 37 39 (Pubitemid 41759590)
17. H. J. van Kranen F. R. de Gruijl Mutations in cancer genes of UV-induced skin tumors of hairless mice J. Epidemiol. 1999 9 S58 65
18. A. Cuenda S. Rousseau p38 MAP-kinases pathway regulation, function and role in human diseases Biochim. Biophys. Acta, Mol. Cell Res. 2007 1773 1358 1375 (Pubitemid 47125981)
19. A. Cuadrado A. R. Nebreda Mechanisms and functions of p38 MAPK signalling Biochem. J. 2010 429 403 417
20. E. F. Wagner A. R. Nebreda Signal integration by JNK and p38 MAPK pathways in cancer development Nat. Rev. Cancer 2009 9 537 549
21. C. Johansen K. Kragballe M. Westergaard J. Henningsen K. Kristiansen L. Iversen The mitogen-activated protein kinases p38 and ERK1/2 are increased in lesional psoriatic skin Br. J. Dermatol. 2005 152 37 42
22. R. L. Eckert T. Efimova S. Balasubramanian J. F. Crish F. Bone S. Dashti p38 Mitogen-activated protein kinases on the body surface-a function for p38 delta J. Invest. Dermatol. 2003 120 823 828 (Pubitemid 36529085)
23. T. Finkel Oxygen radicals and signaling Curr. Opin. Cell Biol. 1998 10 248 253 (Pubitemid 28174767)
24. A. Kulisz N. Chen N. S. Chandel Z. Shao P. T. Schumacker Mitochondrial ROS initiate phosphorylation of p38 MAP kinase during hypoxia in cardiomyocytes Am. J. Physiol. Lung Cell Mol. Physiol. 2002 282 L1324 L1329
25. P. Heusch M. Canton S. Aker A. van de Sand I. Konietzka T. Rassaf S. Menazza O. E. Brodde F. Di Lisa G. Heusch R. Schulz The contribution of reactive oxygen species and p38 mitogen-activated protein kinase to myofilament oxidation and progression of heart failure in rabbits Br. J. Pharmacol. 2010 160 1408 1416
26. I. Dolado A. Swat N. Ajenjo G. De Vita A. Cuadrado A. R. Nebreda p38alpha MAP kinase as a sensor of reactive oxygen species in tumorigenesis Cancer Cell 2007 11 191 205 (Pubitemid 46209847)
27. P. J. Nadeau S. J. Charette M. B. Toledano J. Landry Disulfide Bond-mediated multimerization of Ask1 and its reduction by thioredoxin-1 regulate H(2)O(2)-induced c-Jun NH(2)-terminal kinase activation and apoptosis Mol. Biol. Cell 2007 18 3903 3913 (Pubitemid 47519483)
28. C. J. Staples D. M. Owens J. V. Maier A. C. Cato S. M. Keyse Cross-talk between the p38alpha and JNK MAPK pathways mediated by MAP kinase phosphatase-1 determines cellular sensitivity to UV radiation J. Biol. Chem. 2010 285 25928 25940
29. D. M. Owens S. M. Keyse Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases Oncogene 2007 26 3203 3213 (Pubitemid 46763015)
30. K. I. Patterson T. Brummer P. M. O'Brien R. J. Daly Dual-specificity phosphatases: critical regulators with diverse cellular targets Biochem. J. 2009 418 475 489
31. J. M. Denu K. G. Tanner Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation Biochemistry 1998 37 5633 5642 (Pubitemid 28241948)
32. H. Kamata S. Honda S. Maeda L. Chang H. Hirata M. Karin Reactive oxygen species promote TNFalpha-induced death and sustained JNK activation by inhibiting MAP kinase phosphatases Cell 2005 120 649 661 (Pubitemid 40343077)
33. A. Salmeen J. N. Andersen M. P. Myers T. C. Meng J. A. Hinks N. K. Tonks D. Barford Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate Nature 2003 423 769 773 (Pubitemid 36735701)
34. S. Gross A. Knebel T. Tenev A. Neininger M. Gaestel P. Herrlich F. D. Bohmer Inactivation of protein-tyrosine phosphatases as mechanism of UV-induced signal transduction J. Biol. Chem. 1999 274 26378 26386
35. Y. Xu Y. Shao J. J. Voorhees G. J. Fisher Oxidative inhibition of receptor-type protein-tyrosine phosphatase kappa by ultraviolet irradiation activates epidermal growth factor receptor in human keratinocytes J. Biol. Chem. 2006 281 27389 27397 (Pubitemid 44401766)
36. I. A. Manke A. Nguyen D. Lim M. Q. Stewart A. E. Elia M. B. Yaffe MAPKAP kinase-2 is a cell cycle checkpoint kinase that regulates the G2/M transition and S phase progression in response to UV irradiation Mol. Cell 2005 17 37 48 (Pubitemid 40075363)
37. H. C. Reinhardt A. S. Aslanian J. A. Lees M. B. Yaffe p53-deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage Cancer Cell 2007 11 175 189 (Pubitemid 46209849)
38. H. C. Reinhardt M. B. Yaffe Kinases that control the cell cycle in response to DNA damage: Chk1, Chk2, and MK2 Curr. Opin. Cell Biol. 2009 21 245 255
39. B. B. Zhou S. J. Elledge The DNA damage response: putting checkpoints in perspective Nature 2000 408 433 439
40. C. Johansen C. Vestergaard K. Kragballe G. Kollias M. Gaestel L. Iversen MK2 regulates the early stages of skin tumor promotion Carcinogenesis 2009 30 2100 2108
41. Y. Zhang S. Zhong Z. Dong N. Chen A. M. Bode W. Ma UVA induces Ser381 phosphorylation of p90RSK/MAPKAP-K1 via ERK and JNK pathways J. Biol. Chem. 2001 276 14572 14580
42. L. O. Klotz C. Pellieux K. Briviba C. Pierlot J. M. Aubry H. Sies Mitogen-activated protein kinase (p38-, JNK-, ERK-) activation pattern induced by extracellular and intracellular singlet oxygen and UVA Eur. J. Biochem. 1999 260 917 922 (Pubitemid 29148661)
43. A. L. Silvers J. S. Finch G. T. Bowden Inhibition of UVA-induced c-Jun N-terminal kinase activity results in caspase-dependent apoptosis in human keratinocytes Photochem. Photobiol. 2006 82 423 431
44. M. A. Bachelor A. L. Silvers G. T. Bowden The role of p38 in UVA-induced cyclooxygenase-2 expression in the human keratinocyte cell line, HaCaT Oncogene 2002 21 7092 7099 (Pubitemid 35252983)
45. K. L. Cooper K. J. Liu L. G. Hudson Enhanced ROS production and redox signaling with combined arsenite and UVA exposure: contribution of NADPH oxidase Free Radical Biol. Med. 2009 47 381 388
46. A. Van Laethem S. Van Kelst S. Lippens W. Declercq P. Vandenabeele S. Janssens J. R. Vandenheede M. Garmyn P. Agostinis Activation of p38 MAPK is required for Bax translocation to mitochondria, cytochrome c release and apoptosis induced by UVB irradiation in human keratinocytes FASEB J. 2004 18 1946 1948 (Pubitemid 39602293)
47. K. Nys A. Van Laethem C. Michiels N. Rubio J. G. Piette M. Garmyn P. Agostinis A p38(MAPK)/HIF-1 pathway initiated by UVB irradiation is required to induce Noxa and apoptosis of human keratinocytes J. Invest. Dermatol. 2010 130 2269 2276
48. J. Hildesheim R. T. Awwad A. J. Fornace Jr. 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. 2004 122 497 502 (Pubitemid 38281075)
49. M. A. Bachelor G. T. Bowden Ultraviolet A-induced modulation of Bcl-XL by p38 MAPK in human keratinocytes: post-transcriptional regulation through the 3′-untranslated region J. Biol. Chem. 2004 279 42658 42668 (Pubitemid 39372151)
50. A. Mahns R. Wolber F. Stab L. O. Klotz H. Sies Contribution of UVB and UVA to UV-dependent stimulation of cyclooxygenase-2 expression in artificial epidermis Photochem. Photobiol. Sci. 2004 3 257 262 (Pubitemid 38849370)
51. S. Manandhar A. You E. S. Lee J. A. Kim M. K. Kwak Activation of the Nrf2-antioxidant system by a novel cyclooxygenase-2 inhibitor furan-2-yl-3-pyridin-2-yl-propenone: implication in anti-inflammatory function by Nrf2 activator J. Pharm. Pharmacol. 2008 60 879 887 (Pubitemid 351914026)
52. J. Zhang G. Tsaprailis G. T. Bowden Nucleolin stabilizes Bcl-X L messenger RNA in response to UVA irradiation Cancer Res. 2008 68 1046 1054 (Pubitemid 351272222)
53. E. Espel The role of the AU-rich elements of mRNAs in controlling translation Semin. Cell Dev. Biol. 2005 16 59 67 (Pubitemid 40136538)
54. M. R. Fabian N. Sonenberg W. Filipowicz Regulation of mRNA translation and stability by microRNAs Annu. Rev. Biochem. 2010 79 351 379
55. J. Houseley D. Tollervey The many pathways of RNA degradation Cell 2009 136 763 776
56. M. Srivastava H. B. Pollard Molecular dissection of nucleolin's role in growth and cell proliferation: new insights FASEB J. 1999 13 1911 1922 (Pubitemid 29517621)
57. C. Y. Chen R. Gherzi J. S. Andersen G. Gaietta K. Jurchott H. D. Royer M. Mann M. Karin Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation Genes Dev. 2000 14 1236 1248 (Pubitemid 30327504)
58. T. K. Sengupta S. Bandyopadhyay D. J. Fernandes E. K. Spicer Identification of nucleolin as an AU-rich element binding protein involved in bcl-2 mRNA stabilization J. Biol. Chem. 2004 279 10855 10863 (Pubitemid 38401575)
59. Y. Zhang D. Bhatia H. Xia V. Castranova X. Shi F. Chen Nucleolin links to arsenic-induced stabilization of GADD45alpha mRNA Nucleic Acids Res. 2006 34 485 495 (Pubitemid 43245430)
60. C. Yang D. A. Maiguel F. Carrier Identification of nucleolin and nucleophosmin as genotoxic stress-responsive RNA-binding proteins Nucleic Acids Res. 2002 30 2251 2260 (Pubitemid 34567946)
61. J. L. Dean G. Sully A. R. Clark J. Saklatvala The involvement of AU-rich element-binding proteins in p38 mitogen-activated protein kinase pathway-mediated mRNA stabilisation Cell. Signalling 2004 16 1113 1121 (Pubitemid 38900514)
62. M. Lasa K. R. Mahtani A. Finch G. Brewer J. Saklatvala A. R. Clark Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade Mol. Cell. Biol. 2000 20 4265 4274 (Pubitemid 30346621)
63. M. Gaestel MAPKAP kinases-MKs-two's company, three's a crowd Nat. Rev. Mol. Cell Biol. 2006 7 120 130 (Pubitemid 43278295)
64. K. Abdelmohsen A. Lal H. H. Kim M. Gorospe Posttranscriptional orchestration of an anti-apoptotic program by HuR Cell Cycle 2007 6 1288 1292 (Pubitemid 47327958)
65. J. Zhang G. T. Bowden UVB irradiation regulates Cox-2 mRNA stability through AMPK and HuR in human keratinocytes Mol. Carcinog. 2008 47 974 983
66. N. S. Fernau D. Fugmann M. Leyendecker K. Reimann S. Grether-Beck S. Galban N. Ale-Agha J. Krutmann L. O. Klotz Role of HuR and p38MAPK in ultraviolet B-induced post-transcriptional regulation of COX-2 expression in the human keratinocyte cell line HaCaT J. Biol. Chem. 2010 285 3896 3904
67. F. Farooq S. Balabanian X. Liu M. Holcik A. MacKenzie p38 Mitogen-activated protein kinase stabilizes SMN mRNA through RNA binding protein HuR Hum. Mol. Genet. 2009 18 4035 4045
68. V. Lafarga A. Cuadrado I. Lopez de Silanes R. Bengoechea O. Fernandez-Capetillo A. R. Nebreda p38 Mitogen-activated protein kinase- and HuR-dependent stabilization of p21(Cip1) mRNA mediates the G(1)/S checkpoint Mol. Cell. Biol. 2009 29 4341 4351
69. J. S. Mudgett J. Ding L. Guh-Siesel N. A. Chartrain L. Yang S. Gopal M. M. Shen Essential role for p38alpha mitogen-activated protein kinase in placental angiogenesis Proc. Natl. Acad. Sci. U. S. A. 2000 97 10454 10459
70. R. H. Adams A. Porras G. Alonso M. Jones K. Vintersten S. Panelli A. Valladares L. Perez R. Klein A. R. Nebreda Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development Mol. Cell 2000 6 109 116
71. S. E. Dickinson E. R. Olson J. Zhang S. J. Cooper T. Melton P. J. Criswell A. Casanova Z. Dong C. Hu K. Saboda E. T. Jacobs D. S. Alberts G. T. Bowden p38 MAP kinase plays a functional role in UVB-induced mouse skin carcinogenesis Mol. Carcinog. 2011 50 469 478
72. J. G. Einspahr G. T. Bowden D. S. Alberts N. McKenzie K. Saboda J. Warneke S. Salasche J. Ranger-Moore C. Curiel-Lewandrowski R. B. Nagle B. J. Nickoloff C. Brooks Z. Dong S. P. Stratton Cross-validation of murine UV signal transduction pathways in human skin Photochem. Photobiol. 2008 84 463 476 (Pubitemid 351421399)
73. J. G. Einspahr S. P. Stratton G. T. Bowden D. S. Alberts Chemoprevention of human skin cancer Crit. Rev. Oncol. Hematol. 2002 41 269 285 (Pubitemid 34203664)
74. V. A. Beardmore H. J. Hinton C. Eftychi M. Apostolaki M. Armaka J. Darragh J. McIlrath J. M. Carr L. J. Armit C. Clacher L. Malone G. Kollias J. S. Arthur Generation and characterization of p38beta (MAPK11) gene-targeted mice Mol. Cell. Biol. 2005 25 10454 10464 (Pubitemid 41681967)
75. G. Sabio J. S. Arthur Y. Kuma M. Peggie J. Carr V. Murray-Tait F. Centeno M. Goedert N. A. Morrice A. Cuenda p38gamma regulates the localisation of SAP97 in the cytoskeleton by modulating its interaction with GKAP EMBO J. 2005 24 1134 1145 (Pubitemid 40516597)
76. E. M. Schindler A. Hindes E. L. Gribben C. J. Burns Y. Yin M. H. Lin R. J. Owen G. D. Longmore G. E. Kissling J. S. Arthur T. Efimova p38delta Mitogen-activated protein kinase is essential for skin tumor development in mice Cancer Res. 2009 69 4648 4655
77. A. S. Haider S. B. Peters H. Kaporis I. Cardinale J. Fei J. Ott M. Blumenberg A. M. Bowcock J. G. Krueger J. A. Carucci Genomic analysis defines a cancer-specific gene expression signature for human squamous cell carcinoma and distinguishes malignant hyperproliferation from benign hyperplasia J. Invest. Dermatol. 2006 126 869 881
78. M. R. Junttila R. Ala-Aho T. Jokilehto J. Peltonen M. Kallajoki R. Grenman P. Jaakkola J. Westermarck V. M. Kahari p38alpha and p38delta mitogen-activated protein kinase isoforms regulate invasion and growth of head and neck squamous carcinoma cells Oncogene 2007 26 5267 5279 (Pubitemid 47237627)
79. A. M. Bode Z. Dong The functional contrariety of JNK Mol. Carcinog. 2007 46 591 598 (Pubitemid 47255173)
80. S. Lawler Y. Fleming M. Goedert P. Cohen Synergistic activation of SAPK1/JNK1 by two MAP kinase kinases in vitro Curr. Biol. 1998 8 1387 1390 (Pubitemid 29020147)
81. A. L. Silvers M. A. Bachelor G. T. Bowden The role of JNK and p38 MAPK activities in UVA-induced signaling pathways leading to AP-1 activation and c-Fos expression Neoplasia 2003 5 319 329 (Pubitemid 37048609)
82. H. S. Choi A. M. Bode J. H. Shim S. Y. Lee Z. Dong c-Jun N-terminal kinase 1 phosphorylates Myt1 to prevent UVA-induced skin cancer Mol. Cell. Biol. 2009 29 2168 2180
83. K. Sabapathy K. Hochedlinger S. Y. Nam A. Bauer M. Karin E. F. Wagner Distinct roles for JNK1 and JNK2 in regulating JNK activity and c-Jun-dependent cell proliferation Mol. Cell 2004 15 713 725 (Pubitemid 39194902)
84. E. F. Wagner AP-1-Introductory remarks Oncogene 2001 20 2334 2335
85. P. Angel M. Karin The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation Biochim. Biophys. Acta 1991 1072 129 157 (Pubitemid 121007534)
86. R. Eferl E. F. Wagner AP-1: a double-edged sword in tumorigenesis Nat. Rev. Cancer 2003 3 859 868 (Pubitemid 37383716)
87. A. L. Silvers G. T. Bowden UVA irradiation-induced activation of activator protein-1 is correlated with induced expression of AP-1 family members in the human keratinocyte cell line HaCaT Photochem. Photobiol. 2002 75 302 310
88. W. Chen A. H. Borchers Z. Dong M. B. Powell G. T. Bowden UVB irradiation-induced activator protein-1 activation correlates with increased c-fos gene expression in a human keratinocyte cell line J. Biol. Chem. 1998 273 32176 32181 (Pubitemid 29177163)
89. F. E. Domann J. P. Levy M. J. Birrer G. T. Bowden Stable expression of a c-JUN deletion mutant in two malignant mouse epidermal cell lines blocks tumor formation in nude mice Cell Growth Differ. 1994 5 9 16 (Pubitemid 24256929)
90. F. E. Domann, Jr. J. P. Levy J. S. Finch G. T. Bowden Constitutive AP-1 DNA binding and transactivating ability of malignant but not benign mouse epidermal cells Mol. Carcinog. 1994 9 61 66 (Pubitemid 24099075)
91. Z. Dong M. J. Birrer R. G. Watts L. M. Matrisian N. H. Colburn Blocking of tumor promoter-induced AP-1 activity inhibits induced transformation in JB6 mouse epidermal cells Proc. Natl. Acad. Sci. U. S. A. 1994 91 609 613 (Pubitemid 24041451)
92. M. R. Young J. J. Li M. Rincon R. A. Flavell B. K. Sathyanarayana R. Hunziker N. Colburn Transgenic mice demonstrate AP-1 (activator protein-1) transactivation is required for tumor promotion Proc. Natl. Acad. Sci. U. S. A. 1999 96 9827 9832 (Pubitemid 29398817)
93. S. J. Cooper J. MacGowan J. Ranger-Moore M. R. Young N. H. Colburn G. T. Bowden Expression of dominant negative c-jun inhibits ultraviolet B-induced squamous cell carcinoma number and size in an SKH-1 hairless mouse model Mol. Cancer Res. 2003 1 848 854 (Pubitemid 37174456)
94. R. M. Tyrrell S. M. Keyse New trends in photobiology. The interaction of UVA radiation with cultured cells J. Photochem. Photobiol., B 1990 4 349 361
95. J. G. Einspahr D. S. Alberts J. A. Warneke P. Bozzo J. Basye T. M. Grogan M. A. Nelson G. T. Bowden Relationship of p53 mutations to epidermal cell proliferation and apoptosis in human UV-induced skin carcinogenesis Neoplasia 1999 1 468 475
96. S. Euvrard J. Kanitakis A. Claudy Skin cancers after organ transplantation N. Engl. J. Med. 2003 348 1681 1691 (Pubitemid 36459475)
97. X. Zhang G. Jeffs X. Ren P. O'Donovan B. Montaner C. M. Perrett P. Karran Y. Z. Xu Novel DNA lesions generated by the interaction between therapeutic thiopurines and UVA light DNA Repair 2007 6 344 354 (Pubitemid 46329614)
98. Q. Gueranger A. Kia D. Frith P. Karran Crosslinking of DNA repair and replication proteins to DNA in cells treated with 6-thioguanine and UVA Nucleic Acids Res. 2011 39 5057 5066
99. T. G. Rossman A. N. Uddin F. J. Burns Evidence that arsenite acts as a cocarcinogen in skin cancer Toxicol. Appl. Pharmacol. 2004 198 394 404 (Pubitemid 38969968)
100. T. G. Rossman A. N. Uddin F. J. Burns M. C. Bosland Arsenite is a cocarcinogen with solar ultraviolet radiation for mouse skin: an animal model for arsenic carcinogenesis Toxicol. Appl. Pharmacol. 2001 176 64 71 (Pubitemid 32977291)
101. C. H. Tseng Arsenic methylation, urinary arsenic metabolites and human diseases: current perspective J. Environ. Sci. Health C: Environ. Carcinog. Ecotoxicol. Rev. 2007 25 1 22