Telomerase-immortalized human fibroblasts retain UV-induced mutagenesis and p53-mediated DNA damage responses

DNA Repair

Volumn 5, Issue 1, 2006, Pages 61-70

  Porter, Paul C ^a   Clark, Denise R ^a   McDaniel, Lisa D ^b   McGregor, W Glenn ^a,c   States, J Christopher ^a,c  

^a University of Louisville School of Medicine   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

DNA damage response; HPRT mutagenesis; Immortalization; p53; Telomerase; UV

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLOBUTANE DERIVATIVE; CYCLOBUTANE PYRIMIDINE; DAMAGED DEOXYRIBONUCLEIC ACID BINDING PROTEIN 2; DIMER; DNA; DNA BINDING PROTEIN; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; PROTEIN; PROTEIN P48; PROTEIN P53; PYRIMIDINE; RETROVIRUS VECTOR; SMALL INTERFERING RNA; TELOMERASE; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL IMMORTALIZATION; CELL LINE; CELL SURVIVAL; COLONY FORMING UNIT; CONTROLLED STUDY; DNA BINDING; DNA DAMAGE; DNA PROBE; DNA REPAIR; DNA STRAND; ELECTROPHORETIC MOBILITY; EXCISION REPAIR; FIBROBLAST; GENETIC MANIPULATION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; LD 50; MALE; MUTAGENESIS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RADIATION DOSE; RADIATION EXPOSURE; REACTION TIME; SENESCENCE; ULTRAVIOLET RADIATION;

APOPTOSIS; CELL LINE, TRANSFORMED; CELL SURVIVAL; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; FIBROBLASTS; HUMANS; HYPOXANTHINE PHOSPHORIBOSYLTRANSFERASE; MALE; MUTAGENESIS; PHOSPHORYLATION; SERINE; TELOMERASE; TETRAHYDROFOLATE DEHYDROGENASE; TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

EID: 29244437495     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2005.07.005     Document Type: Article

References (56)

1. I. Mellon, D.K. Rajpal, M. Koi, C.R. Boland, and G.N. Champe Transcription-coupled repair deficiency and mutations in human mismatch repair genes Science 272 1996 557 560
2. P.C. Hanawalt Controlling the efficiency of excision repair Mutat. Res. 485 2001 3 13
3. E.C. Friedberg How nucleotide excision repair protects against cancer Nat. Rev. Cancer 1 2001 22 33
4. L.H. Mullenders, and M. Berneburg Photoimmunology and nucleotide excision repair: impact of transcription coupled and global genome excision repair J. Photochem. Photobiol. B 65 2001 97 100
5. 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 (Amst.) 1 2002 629 643
6. A.R. Lehmann DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy Biochimie 85 2003 1101 1111
7. M.F. Denissenko, A. Pao, G.P. Pfeifer, and M. Tang Slow repair of bulky DNA adducts along the nontranscribed strand of the human p53 gene may explain the strand bias of transversion mutations in cancers Oncogene 16 1998 1241 1247
8. M.S. Greenblatt, W.P. Bennett, M. Hollstein, and C.C. Harris Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis Cancer Res. 54 1994 4855 4878
9. J.A. Mietz, T. Unger, J.M. Huibregtse, and P.M. Howley The transcriptional transactivation function of wild-type p53 is inhibited by SV40 large T-antigen and by HPV-16 E6 oncoprotein EMBO J. 11 1992 5013 5020
10. J.S. Rhim Development of human cell lines from multiple organs Ann. NY Acad. Sci. 919 2000 16 25
11. T. Honda, N. Sadamori, M. Oshimura, I. Horikawa, H. Omura, K. Komatsu, and M. Watanabe Spontaneous immortalization of cultured skin fibroblasts obtained from a high-dose atomic bomb survivor Mutat. Res. 354 1996 15 26
12. K.K. Bowman, D.M. Sicard, J.M. Ford, and P.C. Hanawalt Reduced global genomic repair of ultraviolet light-induced cyclobutane pyrimidine dimers in simian virus 40-transformed human cells Mol. Carcinogen. 29 2000 17 24
13. S.A. Amundson, A. Patterson, K.T. Do, and A.J. Fornace Jr. A nucleotide excision repair master-switch: p53 regulated coordinate induction of global genomic repair genes Cancer Biol. Ther. 1 2002 145 149
14. M.A. Wani, M.A. El Mahdy, F.M. Hamada, G. Wani, Q. Zhu, Q.E. 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. 505 2002 13 25
15. J. Tang, and G. Chu Xeroderma pigmentosum complementation group E and UV-damaged DNA-binding protein DNA Repair (Amst.) 1 2002 601 616
16. 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 28073 28080
17. P. Lavia, A.M. Mileo, A. Giordano, and M.G. Paggi Emerging roles of DNA tumor viruses in cell proliferation: new insights into genomic instability Oncogene 22 2003 6508 6516
18. T.H. Chang, F.A. Ray, D.A. Thompson, and R. Schlegel Disregulation of mitotic checkpoints and regulatory proteins following acute expression of SV40 large T antigen in diploid human cells Oncogene 14 1997 2383 2393
19. J. Lukas, H. Muller, J. Bartkova, D. Spitkovsky, A.A. Kjerulff, P. Jansen-Durr, M. Strauss, and J. Bartek DNA tumor virus oncoproteins and retinoblastoma gene mutations share the ability to relieve the cell's requirement for cyclin D1 function in G1 J. Cell Biol. 125 1994 625 638
20. M. Jung, and A. Dritschilo Modification of the radiosensitivity of human testicular cancer cells by simian virus 40 sequences Radiat. Res. 140 1994 186 190
21. I. Mellon, T. Hock, R. Reid, P.C. Porter, and J.C. States Polymorphisms in the human xeroderma pigmentosum group A gene and their impact on cell survival and nucleotide excision repair DNA Repair (Amst.) 1 2002 531 546
22. P.C. Porter, I. Mellon, and J.C. States XP-A cells complemented with Arg228Gln and Val234Leu polymorphic XPA alleles repair BPDE-induced DNA damage better than cells complemented with the wild type allele DNA Repair (Amst.) 4 2005 341 349
23. H. Kim, J. Farris, S.A. Christman, B.W. Kong, L.K. Foster, S.M. O'Grady, and D.N. Foster Events in the immortalizing process of primary human mammary epithelial cells by the catalytic subunit of human telomerase Biochem. J. 365 2002 765 772
24. E.K. Parkinson, J. Munro, K. Steeghs, V. Morrison, H. Ireland, N. Forsyth, S. Fitzsimmons, and S. Bryce Replicative senescence as a barrier to human cancer Biochem. Soc. Trans. 28 2000 226 233
25. M.M. Ouellette, L.D. McDaniel, W.E. Wright, J.W. Shay, and R.A. Schultz The establishment of telomerase-immortalized cell lines representing human chromosome instability syndromes Hum. Mol. Genet. 9 2000 403 411
26. H. Vaziri, J.A. Squire, T.K. Pandita, G. Bradley, R.M. Kuba, H. Zhang, S. Gulyas, R.P. Hill, G.P. Nolan, and S. Benchimol Analysis of genomic integrity and p53-dependent G1 checkpoint in telomerase-induced extended-life-span human fibroblasts Mol. Cell Biol. 19 1999 2373 2379
27. C.P. Morales, S.E. Holt, M. Ouellette, K.J. Kaur, Y. Yan, K.S. Wilson, M.A. White, W.E. Wright, and J.W. Shay Absence of cancer-associated changes in human fibroblasts immortalized with telomerase Nat. Genet. 21 1999 115 118
28. L.W. Elmore, K.C. Turner, L.S. Gollahon, M.R. Landon, C.K. Jackson-Cook, and S.E. Holt Telomerase protects cancer-prone human cells from chromosomal instability and spontaneous immortalization Cancer Biol. Ther. 1 2002 391 397
29. X.R. Jiang, G. Jimenez, E. Chang, M. Frolkis, B. Kusler, M. Sage, M. Beeche, A.G. Bodnar, G.M. Wahl, T.D. Tlsty, and C.P. Chiu Telomerase expression in human somatic cells does not induce changes associated with a transformed phenotype Nat. Genet. 21 1999 111 114
30. K.H. Shin, M.K. Kang, E. Dicterow, A. Kameta, M.A. Baluda, and N.H. Park Introduction of human telomerase reverse transcriptase to normal human fibroblasts enhances DNA repair capacity Clin. Cancer Res. 10 2004 2551 2560
31. 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
32. P. Chomczynski, and N. Sacchi Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal. Biochem. 162 1987 156 159
33. 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. U.S.A. 96 1999 424 428
34. A.P. Feinberg, and B. Vogelstein A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity Anal. Biochem. 137 1984 266 267 (addendum)
35. F. Oberhammer, G. Fritsch, M. Schmied, M. Pavelka, D. Printz, T. Purchio, H. Lassmann, and R. Schulte-Hermann Condensation of the chromatin at the membrane of an apoptotic nucleus is not associated with activation of an endonuclease J. Cell Sci. 104 Pt 2 1993 317 326
36. W.G. McGregor, R.H. Chen, L. Lukash, V.M. Maher, and J.J. McCormick Cell cycle-dependent strand bias for UV-induced mutations in the transcribed strand of excision repair-proficient human fibroblasts but not in repair-deficient cells Mol. Cell Biol. 11 1991 1927 1934
37. B.J. Hwang, V. Smider, and G. Chu The use of electrophoretic mobility shift assays to study DNA repair Meth. Mol. Biol. 113 103-20 1999 103 120
38. T. Basic-Zaninovic, R. Meschini, A.S. Calcagnile, F. Palombo, M. D'Errico, L. Proietti-De Sanctis, and D. Dogliotti Strand bias of ultraviolet light-induced mutations in a transcriptionally active gene in human cells Mol. Carcinogen. 14 1995 214 225
39. M.A. Dickson, W.C. Hahn, Y. Ino, V. Ronfard, J.Y. Wu, R.A. Weinberg, D.N. Louis, F.P. Li, and J.G. Rheinwald Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics Mol. Cell Biol. 20 2000 1436 1447
40. H. Nakamura, H. Fukami, Y. Hayashi, T. Kiyono, S. Nakatsugawa, M. Hamaguchi, and K. Ishizaki Establishment of immortal normal and ataxia telangiectasia fibroblast cell lines by introduction of the hTERT gene J. Radiat. Res. (Tokyo) 43 2002 167 174
41. J. Yang, E. Chang, A.M. Cherry, C.D. Bangs, Y. Oei, A. Bodnar, A. Bronstein, C.P. Chiu, and G.S. Herron Human endothelial cell life extension by telomerase expression J. Biol. Chem. 274 1999 26141 26148
42. S. Drayton, and G. Peters Immortalisation and transformation revisited Curr. Opin. Genet. Dev. 12 2002 98 104
43. G. Saretzki, N. Sitte, U. Merkel, R.E. Wurm, and T. von Zglinicki Telomere shortening triggers a p53-dependent cell cycle arrest via accumulation of G-rich single stranded DNA fragments Oncogene 18 1999 5148 5158
44. S. Di Donna, K. Mamchaoui, R.N. Cooper, S. Seigneurin-Venin, J. Tremblay, G.S. Butler-Browne, and V. Mouly Telomerase can extend the proliferative capacity of human myoblasts, but does not lead to their immortalization Mol. Cancer Res. 1 2003 643 653
45. E.L. Ostler, C.V. Wallis, B. Aboalchamat, and R.G. Faragher Telomerase and the cellular lifespan: implications of the aging process J. Pediatr. Endocrinol. Metab. 13 Suppl. 6 2000 1467 1476
46. N.E. Crompton Telomeres, senescence and cellular radiation response Cell. Mol. Life Sci. 53 1997 568 575
47. W.G. McGregor, R.H. Chen, L. Lukash, V.M. Maher, and J.J. McCormick Cell cycle-dependent strand bias for UV-induced mutations in the transcribed strand of excision repair-proficient human fibroblasts but not in repair-deficient cells Mol. Cell Biol. 11 1991 1927 1934
48. M. Diaz, N.B. Watson, G. Turkington, L.K. Verkoczy, N.R. Klinman, and W.G. McGregor Decreased frequency and highly aberrant spectrum of ultraviolet-induced mutations in the HPRT gene of mouse fibroblasts expressing antisense RNA to DNA polymerase zeta Mol. Cancer Res. 1 2003 836 847
49. C. Roscheisen, S. Haupter, U. Zechner, and G. Speit Characterization of spontaneous and induced mutations in SV40-transformed normal and ataxia telangiectasia cell lines Somat. Cell Mol. Genet. 20 1994 493 504
50. D.R. Clark, W. Zacharias, L. Panaitescu, and W.G. McGregor Ribozyme-mediated REV1 inhibition reduces the frequency of UV-induced mutations in the human HPRT gene Nucl. Acids Res. 31 2003 4981 4988
51. S. Mukhopadhyay, D.R. Clark, N.B. Watson, W. Zacharias, and W.G. McGregor REV1 accumulates in DNA damage-induced nuclear foci in human cells and is implicated in mutagenesis by benzo[a]pyrenediolepoxide Nucl. Acids Res. 32 2004 5820 5826
52. M. Ljungman, and F. Zhang Blockage of RNA polymerase as a possible trigger for UV light-induced apoptosis Oncogene 13 1996 823 831
53. 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. U.S.A. 100 2003 7219 7224
54. R.W. Hart, and R.B. Setlow DNA repair in late-passage human cells Mech. Ageing Dev. 5 1976 67 77
55. E.G. Nette, Y.P. Xi, Y.K. Sun, A.D. Andrews, and D.W. King A correlation between aging and DNA repair in human epidermal cells Mech. Ageing Dev. 24 1984 283 292
56. K.L. MacKenzie, S. Franco, C. May, M. Sadelain, and M.A. Moore Mass cultured human fibroblasts overexpressing hTERT encounter a growth crisis following an extended period of proliferation Exp. Cell Res. 259 2000 336 350