Differentiating human keratinocytes are deficient in p53 but retain global nucleotide excision repair following ultraviolet radiation

DNA Repair

Volumn 4, Issue 10, 2005, Pages 1149-1159

  Oh, Dennis H ^a,b   Yeh, Kelvin ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Differentiation; DNA repair; Keratinocyte; Thymine dimer; Ultraviolet rays

Indexed keywords

ASCORBIC ACID; CALCIUM; DNA; MESSENGER RNA; NUCLEOTIDE; PHORBOL ESTER; PROTEIN P53; PYRIMIDINE DIMER; PYRIMIDINONE DERIVATIVE;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL DIVISION; DNA DAMAGE; EXCISION REPAIR; GENOMICS; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN INDUCTION; RADIATION EXPOSURE; ULTRAVIOLET RADIATION;

CALCIUM; CELL DIFFERENTIATION; DNA REPAIR; DNA-BINDING PROTEINS; HUMANS; KERATINOCYTES; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS; UP-REGULATION;

EID: 24944572286     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2005.06.004     Document Type: Article

References (63)

1. Z. Nemes, and P.M. Steinert Bricks and mortar of the epidermal barrier Exp. Mol. Med. 31 1999 5 19
2. P.M. Elias The epidermal permeability barrier: from the early days at Harvard to emerging concepts J. Invest. Dermatol. 122 2004 xxxvi xxxix
3. E. Fuchs, and S. Raghavan Getting under the skin of epidermal morphogenesis Nat. Rev. Genet. 3 2002 199 209
4. S.-C. Liu, S. Parsons, and P.C. Hanawalt DNA repair in cultured keratinocytes J. Invest. Dermatol. 81 1983 179s 183s
5. Y. Tokura, R.L. Edelson, and F.P. Gasparro Formation and removal of 8-MOP-DNA photoadducts in keratinocytes: effects of calcium concentration and retinoids J. Invest. Dermatol. 96 1991 942 949
6. G. Li, V.C. Ho, D.L. Mitchell, M.J. Trotter, and V.A. Tron Differentiation-dependent p53 regulation of nucleotide excision repair in keratinocytes Am. J. Pathol. 150 1997 1457 1764
7. V.A. Bohr, C.A. Smith, D.S. Okumoto, and P.C. Hanawalt 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
8. I. Mellon, G. Spivak, and P.C. Hanawalt Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene Cell 51 1987 241 249
9. K. Sugasawa, J.M. Ng, C. Masutani, S. Iwai, P.J. Van der Spek, P.J. Eker, F. Hanaoka, D. Bootsma, and J.H. Hoeijmakers Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair Mol. Cell. 2 1998 223 232
10. B.J. Hwang, J.M. Ford, P.C. Hanawalt, and G. Chu Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair Proc. Natl. Acad. Sci. 96 1999 424 428
11. S. Emmert, N. Kobayashi, S.G. Khan, and K.H. Kraemer 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 2000 2151 2156
12. S. Adimoolam, and J.M. Ford p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene Proc. Natl. Acad. Sci. 99 2002 12985 12990
13. M. Volker, M.J. Mone, P. Karmakar, A. Van Hoffen, W. Schul, W. Vermeulen, J.H. Hoeijmakers, R. Van Driel, A.A. Van Zeeland, and L.H. Mullenders Sequential assembly of the nucleotide excision repair factors in vivo Mol. Cell. 8 2001 213 224
14. R.J.W. Berg, H. Rebel, G.T.J. Van der Horst, H.J. Van Kranen, L.H.F. Mullenders, W.A. Van Vloten, and F.R. De Gruijl Impact of global genome repair versus transcription-coupled repair on ultraviolet carcinogenesis in hairless mice Cancer Res. 60 2000 2858 2863
15. T. Nouspikel, and P.C. Hanawalt DNA repair in terminally differentiated cells DNA Repair 1 2002 59 75
16. C.G.C. Van der Wees, M.P.G. Vreeswijk, M. Persoon, A. Van der Laarse, A.A. Van Zeeland, and L.H.F. Mullenders Deficient global genome repair of UV-induced cyclobutane pyrimidine dimers in terminally differentiated myocytes and proliferating fibroblasts from the rat heart DNA Repair 2 2003 1297 1308
17. D.L. Mitchell, J.E. Cleaver, and J.H. Epstein Repair of pyrimidine(6,4)pyrimidone photoproducts in mouse skin J. Invest. Dermatol. 95 1990 55 59
18. S.M. D'Ambrosio, L. Slazinski, J.W. Whetstone, and E. Lowney Excision repair of UV-induced pyrimidine dimers in human skin in vivo J. Invest. Dermatol 77 1981 311 313
19. G. Eggset, G. Volden, and H. Krokan UV-induced DNA damage and its repair in human skin in vivo studied by sensitive immunohistochemical methods Carcinogenesis 4 1983 745 750
20. H. Hennings, D. Michael, C. Cheng, P.M. Steinert, K. Holbrook, and S.H. Yuspa Calcium regulation of growth and differentiation of mouse epidermal cells in culture Cell 19 1980 245 254
21. S. Pillai, D.D. Bikle, M. Hincenbergs, and P.M. Elias Biochemical and morphological characterization of growth and differentiation of normal human neonatal keratinocytes in a serum-free medium J. Cell. Physiol. 134 1988 229 237
22. P.M. Elias, S.K. Ahn, M. Denda, B.E. Brown, D. Crumrine, L.K. Kimutai, L. Komuves, S.H. Lee, and K.R. Feingold Modulations in epidermal calcium regulate the expression of differentiation-specific markers J. Invest. Dermatol. 119 2002 1128 1136
23. A.A. Dlugosz, and S.H. Yuspa Protein kinase C regulates keratinocyte transglutaminase (TGK) gene expression in cultured primary mouse epidermal keratinocytes induced to terminally differentiate by calcium J. Invest. Dermatol. 102 1994 409 414
24. P.T. La Celle, and R. Polakowska Human homeobox HOXA7 regulates keratinocyte transglutaminase type 1 and inhibits differentiation J. Biol. Chem. 276 2001 32844 32853
25. D.C. Ng, S. Shafaee, D. Lee, and D.D. Bikle Requirement of an AP-1 site in the calcium response region of the involucrin promoter J. Biol. Chem. 275 2000 24080 24088
26. Y. Uchida, M. Behne, D. Quiec, P.M. Elias, and W.M. Holleran Vitamin C stimulates sphingolipid synthesis in submerged human keratinocyte cultures J. Invest. Dermatol. 112 1999 578
27. I. Savini, M.V. Catani, A. Rossi, G. Duranti, G. Melino, and L. Avigliano Characterization of keratinocyte differentiation induced by ascorbic acid: protein kinase C involvement and Vitamin C homeostasis J. Invest. Dermatol. 118 2002 372 379
28. G. Spivak, and P.C. Hanawalt Determination of damage and repair in specific DNA sequences Meth.: Companion Meth. Enzymol. 7 1995 147 161
29. S.M. Thacher, and R.H. Rice Keratinocyte-specific transglutaminase of cultured human epidermal cells: relation to cross-linked envelope formation and terminal differentiation Cell 40 1985 685 695
30. J.M. Ford, and P.C. Hanawalt Expression of wild-type p53 is required for efficient global genomic nucleotide excision repair in UV-irradiated human fibroblasts J. Biol. Chem. 272 1997 28078 28080
31. J.M.H. Vos Analysis of psoralen monoadducts and interstrand crosslinks in defined genomic sequences E.C. Friedberg P.C. Hanawalt DNA Repair: A Laboratory Manual of Research Procedures 1988 Marcel Dekker New York 367 398
32. J. Sambrook, and D.W. Russel Fluorometric quantitation of DNA using Hoechst 33258 Molecular Cloning: A Laboratory Manual 2001 Cold Spring Harbor Laboratory Press Cold Spring Harbor pp. A8.22-A8.23
33. T. Mori, M. Nakane, T. Hattori, T. Matsunaga, M. Ihara, and O. Nikaido Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6,4) photoproduct from the same mouse immunized with ultraviolet-irradiated DNA Photochem. Photobiol. 54 1991 225 232
34. S.G. Khan, V. Muniz-Medina, T. Shahlavi, C.C. Baker, H. Inui, T. Ueda, S. Emmert, T.D. Schneider, and K.H. Kraemer The human XPC DNA repair gene: arrangement, splice site information content and influence of a single nucleotide polymorphism in a splic acceptor site on alternative splicing and function Nucleic Acids Res. 30 2002 3624 3631
35. T. Mosmann Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays J. Immunol. Meth. 65 1983 55 63
36. M.L. Smith, I.T. Chen, Q. Zhan, P.M. O'Connor, and A.J. Fornace Involvement of the p53 tumor suppressor in repair of UV-type DNA damage Oncogene 10 1995 1053 1059
37. D.R. Lloyd, and P.C. Hanawalt p53-dependent global genomic repair of benzo[a]pyrene-7,8-diol-9,10-epoxide adducts in human cells Cancer Res. 60 2000 517 521
38. M.A. Wani, M.A. El-Mahdy, F.M. Hamada, G. Wani, Q. Zhu, Q. Wang, and A.A. Wani Efficient repair of bulky anti-BPDE DNA adducts from non-transcribed DNA strand requires functional p53 but not p21(waf1/cip1) and pRb Mutat. Res. 515 2002 13 25
39. G. Mathonnet, C. Leger, J. Desnoyers, R. Drouin, J.P. Therrien, and E.A. Drobetsky UV wavelength-dependent regulation of transcription-coupled nucleotide excision repair in p53-deficient human cells Proc. Natl. Acad. Sci. 100 2003 7219 7224
40. B.J. Hwang, S. Toering, U. Francke, and G. Chu p48 activates a UV-damaged-DNA binding factor and is defective in xeroderma pigmentosum group E cells that lack binding activity Mol. Cell. Biol. 18 1998 4391 4399
41. F. Bernerd, D. Asselineau, C. Vious, O. Chevallier-Lagente, B. Bouadjar, A. Sarasin, and T. Magnaldo Clues to epidermal cancer proneness revealed by reconstruction of DNA repair-deficient xeroderma pigmentosum skin in vitro Proc. Natl. Acad. Sci. 98 2001 7817 7822
42. R.R. Anderson, and J.A. Parrish The optics of human skin J. Invest. Dermatol. 77 1981 13 19
43. A. Li, N. Pouliot, R. Redvers, and P. Kaur Extensive tissue-regenerative capacity of neonatal human keratinocyte stem cells and their progeny J. Clin. Invest. 113 2004 390 400
44. M. Yamaizumi, and T. Sugano UV-induced nuclear accumulation of p53 is evoked through DNA damage of actively transcribed genes independent of the cell cycle Oncogene 9 1994 2775 2784
45. M. Ljungman, and F. Zhang Blockage of RNA polymerase as a possible trigger for UV light-induced apoptosis Oncogene 13 1996 823 831
46. L.L. Hill, A. Ouhtit, S.M. Loughlin, M.L. Kripke, H.N. Anananthaswamy, and L.B. Owen-Schaub Fas ligand: a sensor for DNA damage critical in skin cancer etiology Science 285 1999 898 900
47. A. Ziegler, A.S. Jonason, D.J. Leffell, J.A. Simon, H.W. Sharma, J. Kimmelman, L. Remington, T. Jacks, and D.E. Brash Sunburn and p53 in the onset of skin cancer Nature 372 1994 773 776
48. F. Hebra, and M. Kaposi On Diseases of the Skin Including Exanthemata vol. 61 1874 The New Sydenham Society pp. 252-258
49. J.M. Ford, E.L. Baron, and P.C. Hanawalt Human fibroblasts expressing the human papillomavirus E6 gene are deficient in global genomic nucleotide excision repair and sensitive to ultraviolet irradiation Cancer Res. 58 1998 599 603
50. G. Li, D.L. Mitchell, V.C. Ho, J.C. Reed, and V.A. Tron Decreased DNA repair but normal apoptosis in ultraviolet-irradiated skin of p53 transgenic mice Am. J. Pathol. 148 1996 1113 1123
51. M.A. El-Mahdy, F.M. Hamada, M.A. Wani, Q. Zhu, and A.A. Wani p53-degradation by HPV-16 E6 preferentially affects the removal of cyclobutane pyrimidine dimeers from non-transcribed strand and sensitizes mammary epithelial cells to UV-radiation Mutat. Res. 459 2000 135 145
52. T. Itoh, C. O'Shea, and S. Linn Impaired regulation of tumor suppressor p53 caused by mutations in the Xeroderma Pigmentosum DDB2 gene: mutual regulator interactions between p48DDB2 and p53 Mol. Cell. Biol. 23 2003 7540 7553
53. W.C. Weinberg, C.G. Azzoli, K. Chapman, A.J. Levine, and S.H. Yuspa p53-mediated transcriptional activity increases in differentiating epidermal keratinocytes in association with decreased p53 protein Oncogene 10 1995 2271 2279
54. M. Yamaizumi, T. Sugano, H. Asahina, Y. Okada, and T. Uchida Microinjection of partially purified protein factor restores DNA damage specifically in group A of xeroderma pigmentosum cells Proc. Natl. Acad. Sci. 83 1986 1476 1479
55. X. Chen, Y. Zhang, L. Douglas, and P. Zhou UV-damaged DNA-binding proteins are targets of CUL-4A-mediated ubiquitination and degradation J. Biol. Chem. 276 2001 48175 48182
56. M.E. Fitch, I.V. Cross, S.J. Turner, S. Adimoolam, C.X. Lin, K.G. Wiliams, and J.M. Ford The DDB2 nucleotide excision repair gene product p48 enhances global genomic repair in p53 deficient human fibroblasts DNA Repair 2 2003 819 826
57. L. Lommel, T. Ortolan, L. Chen, K. Madura, and K.S. Sweder Proteolysis of a nucleotide excision repair protein by the 26S proteasome Curr. Genet. 42 2002 9 20
58. A. Nag, T. Bondar, S. Shiv, and P. Raychaudhuri The xeroderma pigmentosum group E gene product DDB2 is a specific target of cullin 4A in mammalian cells Mol. Cell. Biol. 21 2001 6738 6747
59. V. Rapic-Otrin, M.P. McLenigan, D.C. Bisi, M. Gonzalez, and A.S. Levine Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation Nucleic Acids Res. 30 2002 2588 2598
60. F.P. Li, J.F. Fraumeni, J.J. Mulvihill, W.A. Blattner, M.G. Dreyfus, M.A. Tucker, and R.W. Miller A cancer family syndrome in 24 kindreds Cancer Res. 48 1988 5358 5362
61. A.F. Nichols, T. Itoh, J.A. Graham, W. Liu, M. Yamaizumi, and S. Linn Human damage-specific DNA binding protein p48 J. Biol. Chem. 275 2000 21422 21428
62. K.E. Rieger, and G. Chu Portrait of transcriptional responses to ultraviolet and ionizing radiation in human cells Nucleic Acids Res. 32 2004 4786 4803
63. 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