UVA-induced epigenetic regulation of P16INK4a in human epidermal keratinocytes and skin tumor derived cells

Photochemical and Photobiological Sciences

Volumn 11, Issue 1, 2012, Pages 180-190

  Chen, I Peng ^a   Henning, Stefan ^a   Faust, Alexandra ^a   Boukamp, Petra ^b   Volkmer, Beate ^a   Greinert, Rüdiger ^a  

^a Center of Dermatology   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84255160829     PISSN: 1474905X     EISSN: 14749092     Source Type: Journal    
DOI: 10.1039/c1pp05197k     Document Type: Article

References (87)

1. B. K. Armstrong A. Kricker The epidemiology of UV induced skin cancer J. Photochem. Photobiol., B 2001 63 8 18 (Pubitemid 33040718)
2. J. E. Cleaver E. Crowley UV damage, DNA repair and skin carcinogenesis Front. Biosci. 2002 7 d1024 1043
3. J. Ramos J. Villa A. Ruiz R. Armstrong J. Matta UV dose determines key characteristics of nonmelanoma skin cancer Cancer Epidemiol., Biomarkers Prev. 2004 13 2006 2011 (Pubitemid 40054293)
4. M. Norval A. P. Cullen F. R. de Gruijl J. Longstreth Y. Takizawa R. M. Lucas F. P. Noonan J. C. van der Leun The effects on human health from stratospheric ozone depletion and its interactions with climate change Photochem. Photobiol. Sci. 2007 6 232 251 (Pubitemid 46385676)
5. U. Leiter C. Garbe Epidemiology of melanoma and nonmelanoma skin cancer-the role of sunlight Adv. Exp. Med. Biol. 2008 624 89 103
6. R. Greinert Skin cancer: new markers for better prevention Pathobiology 2009 76 64 81
7. H. Ikehata T. Ono The mechanisms of UV mutagenesis J. Radiat. Res. 2011 52 115 125
8. J. Cadet E. Sage T. Douki Ultraviolet radiation-mediated damage to cellular DNA Mutat. Res., Fundam. Mol. Mech. Mutagen. 2005 571 3 17 (Pubitemid 40313428)
9. P. J. Rochette J. P. Therrien R. Drouin D. Perdiz N. Bastien E. A. Drobetsky 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. 2003 31 2786 2794 (Pubitemid 37442122)
10. S. Mouret M. Charveron A. Favier J. Cadet T. Douki Differential repair of UVB-induced cyclobutane pyrimidine dimers in cultured human skin cells and whole human skin DNA Repair 2008 7 704 712
11. T. Douki A. Reynaud-Angelin J. Cadet 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 2003 42 9221 9226 (Pubitemid 36935432)
12. E. D. Pleasance R. K. Cheetham P. J. Stephens D. J. McBride S. J. Humphray C. D. Greenman I. Varela M. L. Lin G. R. Ordonez G. R. Bignell K. Ye J. Alipaz M. J. Bauer D. Beare A. Butler R. J. Carter L. Chen A. J. Cox S. Edkins P. I. Kokko-Gonzales N. A. Gormley R. J. Grocock C. D. Haudenschild M. M. Hims T. James M. Jia Z. Kingsbury C. Leroy J. Marshall A. Menzies L. J. Mudie Z. Ning T. Royce O. B. Schulz-Trieglaff A. Spiridou L. A. Stebbings L. Szajkowski J. Teague D. Williamson L. Chin M. T. Ross P. J. Campbell D. R. Bentley P. A. Futreal M. R. Stratton A comprehensive catalogue of somatic mutations from a human cancer genome Nature 2010 463 191 196
13. 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)
14. S. Mouret C. Philippe J. Gracia-Chantegrel A. Banyasz S. Karpati D. Markovitsi T. Douki UVA-induced cyclobutane pyrimidine dimers in DNA: a direct photochemical mechanism? Org. Biomol. Chem. 2010 8 1706 1711
15. P. Boukamp Non-melanoma skin cancer: what drives tumor development and progression? Carcinogenesis 2005 26 1657 1667 (Pubitemid 41487981)
16. V. L. Brown C. A. Harwood T. Crook J. G. Cronin D. P. Kelsell C. M. Proby p16INK4a and p14ARF tumor suppressor genes are commonly inactivated in cutaneous squamous cell carcinoma J. Invest. Dermatol. 2004 122 1284 1292 (Pubitemid 38651105)
17. M. Serrano G. J. Hannon D. Beach A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4 Nature 1993 366 704 707 (Pubitemid 24036021)
18. L. Sigalotti A. Covre E. Fratta G. Parisi F. Colizzi A. Rizzo R. Danielli H. J. Nicolay S. Coral M. Maio Epigenetics of human cutaneous melanoma: setting the stage for new therapeutic strategies J. Transl. Med. 2010 8 56
19. D. E. Freedberg S. H. Rigas J. Russak W. Gai M. Kaplow I. Osman F. Turner J. A. Randerson-Moor A. Houghton K. Busam D. Timothy Bishop B. C. Bastian J. A. Newton-Bishop D. Polsky Frequent p16-independent inactivation of p14ARF in human melanoma J. Natl. Cancer Inst. 2008 100 784 795 (Pubitemid 351809672)
20. K. Ranade C. J. Hussussian R. S. Sikorski H. E. Varmus A. M. Goldstein M. A. Tucker M. Serrano G. J. Hannon D. Beach N. C. Dracopoli Mutations associated with familial melanoma impair p16INK4 function Nat. Genet. 1995 10 114 116
21. J. W. Rocco D. Sidransky p16(MTS-1/CDKN2/INK4a) in cancer progression Exp. Cell Res. 2001 264 42 55 (Pubitemid 32989080)
22. J. Campisi Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors Cell 2005 120 513 522 (Pubitemid 40269765)
23. C. J. Collins J. M. Sedivy Involvement of the INK4a/Arf gene locus in senescence Aging Cell 2003 2 145 150
24. P. Kanellou A. Zaravinos M. Zioga D. A. Spandidos Deregulation of the tumour suppressor genes p14(ARF), p15(INK4b), p16(INK4a) and p53 in basal cell carcinoma Br. J. Dermatol. 2009 160 1215 1221
25. A. Pacifico G. Leone Role of p53 and CDKN2A inactivation in human squamous cell carcinomas J. Biomed. Biotechnol. 2007 2007 43418
26. N. Soufir J. P. Moles C. Vilmer C. Moch O. Verola J. Rivet A. Tesniere L. Dubertret N. Basset-Seguin P16 UV mutations in human skin epithelial tumors Oncogene 1999 18 5477 5481 (Pubitemid 29469236)
27. R. van Doorn N. A. Gruis R. Willemze P. A. van der Velden C. P. Tensen Aberrant DNA methylation in cutaneous malignancies Semin. Oncol. 2005 32 479 487 (Pubitemid 41396425)
28. N. Popov J. Gil Epigenetic regulation of the INK4b-ARF-INK4a locus: in sickness and in health Epigenetics 2010 5 685 690
29. G. Palmieri M. Capone M. L. Ascierto G. Gentilcore D. F. Stroncek M. Casula M. C. Sini M. Palla N. Mozzillo P. A. Ascierto Main roads to melanoma J. Transl. Med. 2009 7 86
30. E. Gronniger B. Weber O. Heil N. Peters F. Stab H. Wenck B. Korn M. Winnefeld F. Lyko Aging and chronic sun exposure cause distinct epigenetic changes in human skin PLoS Genet. 2010 6 e1000971
31. U. G. Sathyanarayana A. Y. Moore L. Li A. Padar K. Majmudar V. Stastny P. Makarla M. Suzuki J. D. Minna Z. Feng A. F. Gazdar Sun exposure related methylation in malignant and non-malignant skin lesions Cancer Lett. 2007 245 112 120 (Pubitemid 44959343)
32. M. Kulis M. Esteller DNA methylation and cancer Adv. Genet. 2010 70 27 56
33. M. Berdasco M. Esteller Aberrant epigenetic landscape in cancer: how cellular identity goes awry Dev. Cell 2010 19 698 711
34. V. Davalos M. Esteller MicroRNAs and cancer epigenetics: a macrorevolution Curr. Opin. Oncol. 2010 22 35 45
35. A. Portela M. Esteller Epigenetic modifications and human disease Nat. Biotechnol. 2010 28 1057 1068
36. S. S. Oliver J. M. Denu Dynamic interplay between histone H3 modifications and protein interpreters: emerging evidence for a "histone language" ChemBioChem 2011 12 299 307
37. T. Kouzarides Chromatin modifications and their function Cell 2007 128 693 705 (Pubitemid 46273577)
38. A. Barski S. Cuddapah K. Cui T. Y. Roh D. E. Schones Z. Wang G. Wei I. Chepelev K. Zhao High-resolution profiling of histone methylations in the human genome Cell 2007 129 823 837 (Pubitemid 46802390)
39. C. Sawan Z. Herceg Histone modifications and cancer Adv. Genet. 2010 70 57 85
40. H. Hashimoto P. M. Vertino X. Cheng Molecular coupling of DNA methylation and histone methylation Epigenomics 2010 2 657 669
41. P. W. Laird Cancer epigenetics Hum. Mol. Genet. 2005 14 Spec No 1 R65 76
42. A. Sharonov T. Gustavsson S. Marguet D. Markovitsi Photophysical properties of 5-methylcytidine Photochem. Photobiol. Sci. 2003 2 362 364 (Pubitemid 41646686)
43. G. P. Pfeifer p53 mutational spectra and the role of methylated CpG sequences Mutat. Res., Fundam. Mol. Mech. Mutagen. 2000 450 155 166 (Pubitemid 30323640)
44. G. P. Pfeifer Mutagenesis at methylated CpG sequences Curr. Top. Microbiol. Immunol. 2006 301 259 281 (Pubitemid 43022676)
45. M. F. Denissenko J. X. Chen M. S. Tang G. P. Pfeifer Cytosine methylation determines hot spots of DNA damage in the human P53 gene Proc. Natl. Acad. Sci. U. S. A. 1997 94 3893 3898 (Pubitemid 27180469)
46. Y. H. You G. P. Pfeifer Similarities in sunlight-induced mutational spectra of CpG-methylated transgenes and the p53 gene in skin cancer point to an important role of 5-methylcytosine residues in solar UV mutagenesis J. Mol. Biol. 2001 305 389 399 (Pubitemid 33032848)
47. V. Nandakumar M. Vaid T. O. Tollefsbol S. K. Katiyar Aberrant DNA hypermethylation patterns lead to transcriptional silencing of tumor suppressor genes in UVB-exposed skin and UVB-induced skin tumors of mice Carcinogenesis 2011 32 597 604
48. K. Wischermann S. Popp S. Moshir K. Scharfetter-Kochanek M. Wlaschek F. de Gruijl W. Hartschuh R. Greinert B. Volkmer A. Faust A. Rapp P. Schmezer P. Boukamp UVA radiation causes DNA strand breaks, chromosomal aberrations and tumorigenic transformation in HaCaT skin keratinocytes Oncogene 2008 27 4269 4280 (Pubitemid 352010001)
49. M. LeBoeuf A. Terrell S. Trivedi S. Sinha J. A. Epstein E. N. Olson E. E. Morrisey S. E. Millar Hdac1 and Hdac2 act redundantly to control p63 and p53 functions in epidermal progenitor cells Dev. Cell 2010 19 807 818
50. T. Abbas A. Dutta p21 in cancer: intricate networks and multiple activities Nat. Rev. Cancer 2009 9 400 414
51. J. C. Heng Y. L. Orlov H. H. Ng Transcription factors for the modulation of pluripotency and reprogramming Cold Spring Harbor Symp. Quant. Biol. 2010 75 237 244
52. P. Zhang R. Andrianakos Y. Yang C. Liu W. Lu Kruppel-like factor 4 (Klf4) prevents embryonic stem (ES) cell differentiation by regulating Nanog gene expression J. Biol. Chem. 2010 285 9180 9189
53. J. L. Cox S. K. Mallanna X. Luo A. Rizzino Sox2 uses multiple domains to associate with proteins present in Sox2-protein complexes PLoS One 2010 5 e15486
54. S. R. Viswanathan J. T. Powers W. Einhorn Y. Hoshida T. L. Ng S. Toffanin M. O'Sullivan J. Lu L. A. Phillips V. L. Lockhart S. P. Shah P. S. Tanwar C. H. Mermel R. Beroukhim M. Azam J. Teixeira M. Meyerson T. P. Hughes J. M. Llovet J. Radich C. G. Mullighan T. R. Golub P. H. Sorensen G. Q. Daley Lin28 promotes transformation and is associated with advanced human malignancies Nat. Genet. 2009 41 843 848
55. S. R. Kinney S. Pradhan Regulation of expression and activity of DNA (cytosine-5) methyltransferases in mammalian cells Prog. Mol. Biol. Transl. Sci. 2011 101 311 333
56. G. L. Sen J. A. Reuter D. E. Webster L. Zhu P. A. Khavari DNMT1 maintains progenitor function in self-renewing somatic tissue Nature 2010 463 563 567
57. M. Frye A. G. Fisher F. M. Watt Epidermal stem cells are defined by global histone modifications that are altered by Myc-induced differentiation PLoS One 2007 2 e763
58. M. G. Lee C. Wynder D. A. Bochar M. A. Hakimi N. Cooch R. Shiekhattar Functional interplay between histone demethylase and deacetylase enzymes Mol. Cell. Biol. 2006 26 6395 6402 (Pubitemid 44277880)
59. V. Dehennaut D. Leprince Implication of HIC1 (Hypermethylated In Cancer 1) in the DNA damage response Bull. Cancer 2009 96 E66 72
60. S. B. Baylin J. E. Ohm Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat. Rev. Cancer 2006 6 107 116 (Pubitemid 43361543)
61. R. L. Zinn K. Pruitt S. Eguchi S. B. Baylin J. G. Herman hTERT is expressed in cancer cell lines despite promoter DNA methylation by preservation of unmethylated DNA and active chromatin around the transcription start site Cancer Res. 2007 67 194 201 (Pubitemid 46142775)
62. E. A. Attia L. S. Seada M. H. El-Sayed S. M. El-Shiemy Study of telomerase reverse transcriptase (hTERT) expression in normal, aged, and photo-aged skin Int. J. Dermatol. 2010 49 886 893
63. J. A. Dahl P. Collas A rapid micro chromatin immunoprecipitation assay (microChIP) Nat. Protoc. 2008 3 1032 1045 (Pubitemid 351818692)
64. J. Vandesompele K. De Preter F. Pattyn B. Poppe N. Van Roy A. De Paepe F. Speleman Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes GenomeBiology 2002 3 RESEARCH0034
65. F. El Ghissassi R. Baan K. Straif Y. Grosse B. Secretan V. Bouvard L. Benbrahim-Tallaa N. Guha C. Freeman L. Galichet V. Cogliano A review of human carcinogens-part D: radiation Lancet Oncol. 2009 10 751 752
66. F. Fuks W. A. Burgers A. Brehm L. Hughes-Davies T. Kouzarides DNA methyltransferase Dnmt1 associates with histone deacetylase activity Nat. Genet. 2000 24 88 91 (Pubitemid 30041428)
67. J. S. You J. K. Kang E. K. Lee J. C. Lee S. H. Lee Y. J. Jeon D. H. Koh S. H. Ahn D. W. Seo H. Y. Lee E. J. Cho J. W. Han Histone deacetylase inhibitor apicidin downregulates DNA methyltransferase 1 expression and induces repressive histone modifications via recruitment of corepressor complex to promoter region in human cervix cancer cells Oncogene 2008 27 1376 1386 (Pubitemid 351317464)
68. J. A. Segre Epidermal barrier formation and recovery in skin disorders J. Clin. Invest. 2006 116 1150 1158
69. J. A. Segre C. Bauer E. Fuchs Klf4 is a transcription factor required for establishing the barrier function of the skin Nat. Genet. 1999 22 356 360 (Pubitemid 29369526)
70. Y. C. Chew G. Adhikary G. M. Wilson E. A. Reece R. L. Eckert Protein Kinase C (PKC) {delta} Suppresses Keratinocyte Proliferation by Increasing p21Cip1 Level by a KLF4 Transcription Factor-dependent Mechanism J. Biol. Chem. 2011 286 28772 28782
71. W. J. Choi S. H. Youn J. H. Back S. Park E. J. Park K. J. Kim H. R. Park A. L. Kim K. H. Kim The role of KLF4 in UVB-induced murine skin tumor development and its correlation with cyclin D1, p53, and p21(Waf1/Cip1) in epithelial tumors of the human skin Arch. Dermatol. Res. 2011 303 191 200
72. A. Banito S. T. Rashid J. C. Acosta S. Li C. F. Pereira I. Geti S. Pinho J. C. Silva V. Azuara M. Walsh L. Vallier J. Gil Senescence impairs successful reprogramming to pluripotent stem cells Genes Dev. 2009 23 2134 2139
73. S. Svensson K. Nilsson A. Ringberg G. Landberg Invade or proliferate? Two contrasting events in malignant behavior governed by p16(INK4a) and an intact Rb pathway illustrated by a model system of basal cell carcinoma Cancer Res. 2003 63 1737 1742 (Pubitemid 36460829)
74. I. Conscience N. Jovenin C. Coissard M. Lorenzato A. Durlach F. Grange P. Birembaut C. Clavel P. Bernard P16 is overexpressed in cutaneous carcinomas located on sun-exposed areas Eur. J. Dermatol. 2006 16 518 522 (Pubitemid 44861826)
75. L. N. Tyler L. Ai C. Zuo C. Y. Fan B. R. Smoller Analysis of promoter hypermethylation of death-associated protein kinase and p16 tumor suppressor genes in actinic keratoses and squamous cell carcinomas of the skin Mod. Pathol. 2003 16 660 664 (Pubitemid 36871498)
76. J. L. Arbiser C. Y. Fan X. Su B. O. Van Emburgh F. Cerimele M. S. Miller J. Harvell M. P. Marinkovich Involvement of p53 and p16 tumor suppressor genes in recessive dystrophic epidermolysis bullosa-associated squamous cell carcinoma J. Invest. Dermatol. 2004 123 788 790 (Pubitemid 39281622)
77. D. Lodygin A. S. Yazdi C. A. Sander T. Herzinger H. Hermeking Analysis of 14-3-3sigma expression in hyperproliferative skin diseases reveals selective loss associated with CpG-methylation in basal cell carcinoma Oncogene 2003 22 5519 5524 (Pubitemid 37072207)
78. T. Takeuchi S. B. Liang N. Matsuyoshi S. Zhou Y. Miyachi H. Sonobe Y. Ohtsuki Loss of T-cadherin (CDH13, H-cadherin) expression in cutaneous squamous cell carcinoma Lab. Invest. 2002 82 1023 1029
79. M. C. Chiles L. Ai C. Zuo C. Y. Fan B. R. Smoller E-cadherin promoter hypermethylation in preneoplastic and neoplastic skin lesions Mod. Pathol. 2003 16 1014 1018 (Pubitemid 37280817)
80. M. F. Fraga M. Herranz J. Espada E. Ballestar M. F. Paz S. Ropero E. Erkek O. Bozdogan H. Peinado A. Niveleau J. H. Mao A. Balmain A. Cano M. Esteller A mouse skin multistage carcinogenesis model reflects the aberrant DNA methylation patterns of human tumors Cancer Res. 2004 64 5527 5534 (Pubitemid 39095543)
81. D. L. Mitchell Effects of cytosine methylation on pyrimidine dimer formation in DNA Photochem. Photobiol. 2000 71 162 165
82. D. Dardalhon A. R. Angelin G. Baldacci E. Sage S. Francesconi Unconventional effects of UVA radiation on cell cycle progression in S. pombe Cell Cycle 2008 7 611 622 (Pubitemid 351499000)
83. A. Mittal C. Piyathilake Y. Hara S. K. Katiyar Exceptionally high protection of photocarcinogenesis by topical application of (-)- epigallocatechin-3-gallate in hydrophilic cream in SKH-1 hairless mouse model: relationship to inhibition of UVB-induced global DNA hypomethylation Neoplasia 2003 5 555 565 (Pubitemid 38045092)
84. E. J. Peterson O. Bogler S. M. Taylor p53-mediated repression of DNA methyltransferase 1 expression by specific DNA binding Cancer Res. 2003 63 6579 6582 (Pubitemid 37322935)
85. J. G. Herman J. R. Graff S. Myohanen B. D. Nelkin S. B. Baylin Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands Proc. Natl. Acad. Sci. U. S. A. 1996 93 9821 9826 (Pubitemid 26296693)
86. T. Valenta J. Lukas L. Doubravska B. Fafilek V. Korinek HIC1 attenuates Wnt signaling by recruitment of TCF-4 and beta-catenin to the nuclear bodies EMBO J. 2006 25 2326 2337 (Pubitemid 44012216)
87. J. M. Martinez C. A. Afshari P. R. Bushel A. Masuda T. Takahashi N. J. Walker Differential toxicogenomic responses to 2,3,7,8-tetrachlorodibenzo-p- dioxin in malignant and nonmalignant human airway epithelial cells Toxicol. Sci. 2002 69 409 423 (Pubitemid 35244215)