ATM-dependent telomere loss in aging human diploid fibroblasts and DNA damage lead to the post-translational activation of p53 protein involving poly(ADP-ribose) polymerase

EMBO Journal

Volumn 16, Issue 19, 1997, Pages 6018-6033

  Vaziri, Homayoun ^a   West, Michael D ^b   Allsopp, Richard C ^b   Davison, Timothy S ^a   Wu, Yu Sung ^a   Arrowsmith, Cheryl H ^a   Poirier, Guy G ^c   Benchimol, Samuel ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b GERON CORPORATION   (United States)

^c LAVAL UNIVERSITY   (Canada)

Author keywords

ATM; p21(WAF1); p53; PARP; Telomeres

Indexed keywords

CELL DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN P21; PROTEIN P53;

ARTICLE; CELL CYCLE G1 PHASE; CELL DIVISION; CELL SURVIVAL; CONTROLLED STUDY; DIPLOIDY; DNA DAMAGE; ENZYME ACTIVITY; FIBROBLAST; HUMAN; HUMAN CELL; HYPEROXIA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; SOMATIC CELL; TELOMERE; TRANSCRIPTION INITIATION;

ALLELES; CELL AGING; CELL CYCLE PROTEINS; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA; DNA DAMAGE; DNA-BINDING PROTEINS; ENZYME INHIBITORS; FIBROBLASTS; HUMANS; NUCLEAR PROTEINS; OXYGEN; POLY(ADP-RIBOSE) POLYMERASES; PROMOTER REGIONS (GENETICS); PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; PROTEINS; TELOMERE; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 0030761351     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.19.6018     Document Type: Article

References (70)

1. Allsopp,R.C. and Harley,C.B. (1995) Evidence for a critical telomere length in senescent human fibroblasts. Exp. Cell Res., 219, 130-136.
2. Allsopp,R.C., Vaziri,H., Patterson,C., Goldstein,S., Younglai,E.V., Futcher,A.B., Greider,C.W. and Harley,C.B. (1992) Telomere length predicts replicative capacity of human nbroblasts. Proc. Natl Acad. Sci. USA, 89, 10114-10118.
3. Anderson,C.W. (1993) DNA damage and the DNA-activated protein kinase. Trends Biochem. Sci., 18, 433-137.
4. Atadja,P., Wong,H., Garkavtsev,I., Veillette,C. and Riabowol,K. (1995) Increased activity of p53 in senescing fibroblasts. Proc. Natl Acad. Sci. USA, 92, 8348-8352.
5. Banasik,M., Homura,H., Shimoyama,M. and Ueda,K. (1992) Specific inhibitors of poly(ADP-ribose) synthesis and mono(ADP-ribosyl) transferase. J. Biol. Chem., 267, 1569-1575.
6. Barbeau,D., Charbonneau,R., Whalen,S.G., Bayley,S.T. and Branton,P.E. (1994) Functional interactions within adenovirus E1A protein complexes. Oncogene, 9, 359-373.
7. Benn,P. (1976) Specific chromosome alterations in senescent fibroblast cell lines derived form human embryos. Am. J. Hum. Genet., 28, 465-473.
8. Bischoff,F.Z., Yim,S.O., Pathak,S., Grant,G., Siciliano,M.J., Giovanella, B.C., Strong,L.C. and Tainsky,M.A. (1990) Spontaneous abnormalities in normal fibroblasts from patients with Li-Fraumeni cancer syndrome: aneuploidy and immortalization. Cancer Res., 50, 7979-7984.
9. Bond,J.A., Wyllie,F.S. and Wynford-Thomas,D. (1994) Escape from senescence in human diploid fibroblasts induced directly by mutant p53. Oncogene, 9, 1885-1889.
10. Buckbinder,L., Talbott,R., Velasco-Miguel,S., Takenaka,I., Faha,B., Seizinger,B.R. and Kley,N. (1995) Induction of the growth inhibitor IGF-binding protein 3 by p53. Nature, 377, 646-649.
11. Chen,Q., Fischer,A., Reagan,J.D., Yan,L.J. and Ames,B.N. (1995) Oxidative DNA damage and senescence of human diploid fibroblast cells. Proc. Natl Acad. Sci. USA, 92, 4337-4341.
12. Counter,C.M., Avilion,A.A., LeFeuvre,C.E., Stewart,N.G., Greider,C.W., Harley,C.B. and Bacchetti,S. (1992) Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J., 11, 1921-1929.
13. Datto,M.B., Li,Y., Panus,J.F., Howe,D.J., Xiong,Y. and Wang,X.F. (1995) Transforming growth factor beta induces the cyclin-dependent kinase inhibitor p21 through a p53-independent mechanism. Proc. Natl Acad. Sci. USA, 92, 5545-5549.
14. 1 arrest and long-term induction of Cip1 in normal human fibroblasts. Genes Dev., 8, 2540-2551.
15. Dimri,G.P. et al. (1995) A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl Acad. Sci. USA, 92, 9363-9367.
16. 1 arrest. Cell, 76, 1013-1023.
17. El-Deiry,W.S. et al. (1993) WAF1, a potential mediator of p53 tumour suppression. Cell, 75, 817-825.
18. Friend,S. (1994) p53: a glimpse at the puppet behind the shadow play. Science, 265, 334-335.
19. Fu,L., Minden,M.D. and Benchimol,S. (1996) Translational regulation of human p53 gene expression. EMBO J., 15, 4392-4401.
20. Funk,W.D., Pak,D.T., Karas,R.H., Wright,W.E. and Shay,J.W. (1992) A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol., 12, 2866-2871.
21. Goldstein,S., Moerman,E.J., Jones,R.A. and Baxter,R.C. (1991) Insulin-like growth factor binding protein 3 accumulates to high levels in culture medium of senescent and quiescent human fibroblasts. Proc. Natl Acad. Sci. USA, 88, 9680-9684.
22. Gollahon,L.S. and Shay,J.W. (1996) Immortalization of human mammary epithelial cells transfected with mutant p53 (273his). Oncogene, 12, 715-725.
23. Greenwell,P.W., Kronmal,S.L., Poner,S.E., Gassenhuber.J., Obermaier,B. and Petes,T.D. (1995) TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene. Cell, 82, 823-829.
24. Grube,K and Burkle,A. (1992) Poly(ADP-ribose) polymerase activity in mononuclear leukocytes of 13 mammalian species correlates with species-specific life span. Proc. Natl Acad. Sci. USA, 89, 11759-11763.
25. Harley,C.B. (1991) Telomere loss: mitotic clock or genetic time bomb? Mutat. Res., 256, 271-282.
26. Harley,C.B., Futcher,A.B. and Greider,C.W. (1990) Telomeres shorten during ageing of human fibroblasts. Nature, 345, 458-460.
27. 1 cyclin-dependent kinases. Cell, 75, 805-816.
28. Hastie,N.D., Dempster,M., Dunlop,M.G., Thompson,A.M., Green,D.K. and Allshire,R.C. (1990) Telomere reduction in human colorectal carcinoma and with ageing. Nature, 346, 866-868.
29. Hayflick,L. and Moorhead,P. (1961) The serial cultivation of human diploid strains. Exp. Cell Res., 25, 585-621.
30. Holliday,R. (1991) A re-examination of the effects of ionizing radiation on lifespan and transformation of human diploid fibroblasts. Mutat. Res., 256, 295-302.
31. Howe,J.A., Mymryk,J.S., Egan,C., Branton,P.E. and Bayley,S.T. (1990) Retinoblastoma growth suppressor and a 300-kDa protein appear to regulate cellular DNA synthesis. Proc. Natl Acad. Sci. USA, 87, 5883-5887.
32. 1 arrest. Proc. Natl Acad. Sci. USA, 93, 4827-4832.
33. Huletsky,A., de Murcia,G., Muller,S., Hengartner,M., Lamarre,D. and Poirier,G.G. (1989) The effect of poly(ADP-ribosyl)ation on native and H1-depleted chromatin. A role of poly(ADP-ribosyl)ation on core nucleosome structure, J. Biol. Chem., 264, 8878-8886.
34. Kastan,M.B., Onyekwere,O., Sidransky,D., Vogelstein,B. and Craig,R.W. (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res., 51, 6304-6311.
35. Kastan,M.B., Zhan,Q., El-Deiry,W.S., Carrier,F., Jacks,T., WaIsh,W.V., Plunkett,B.S., Vogelstein,B. and Fornace,A.J.Jr (1992) A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell, 71, 587-597.
36. Kim,N.W. et al. (1994) Specific association of human telomerase activity with immortal cells and cancer. Science, 266, 2011-2015.
37. Kriegler,M. (1991) Gene Transfer and Expression. Stockton Press, New York.
38. Kulju,K.S. and Lehman,J.M. (1995) Increased p53 protein associated with aging in human diploid fibroblasts. Exp. Cell Res., 217, 336-345.
39. Lindahl,T., Satoh,M.S., Poirier,G.G. and Klungland,A. (1995) Post-translational modification of poly(ADP-ribose) polymerase induced by DNA strand breaks. Trends Biochem. Sci., 20, 405-411.
40. Lindsey,J., McGill,N.I., Lindsey,L.A., Green,D.K. and Cooke,H.J. (1991) In vivo loss of telomeric repeats with age in humans. Mutat. Res., 256, 45-48.
41. Lu,X. and Lane,D.P. (1993) Differential induction of transcriptionally active p53 following UV or ionizing radiation: defects in chromosome instability syndromes? Cell, 75, 765-778.
42. Matsuoka,M., Yoshida,K., Maeda,T., Usuda,S. and Sakano,H. (1990) Switch circular DNA formed in cytokine-treated mouse splenocytes: evidence for intramolecular DNA deletion in immunoglobulin class switching. Cell, 62, 135-142.
43. Metcalfe,J.A., Parkhill,J., Campbell,L., Stacey,M., Biggs,P., Byrd,P.J, and Taylor,A.M. (1996) Accelerated telomere shortening in ataxia telangiectasia. Nature Genet., 13, 350-353.
44. Michieli,P., Chedid,M., Lin,D., Pierce,J.H., Mercer,W.E. and Givol,D. (1994) Induction of WAF1/C1P1 by a p53-independent pathway. Cancer Res., 54, 3391-3395.
45. Mirzayans,R., Aubin,R.A., Bosnich,W., Blattner,W.A. and Paterson,M.C. (1995) Abnormal pattern of post-gamma-ray DNA replication in radioresistant fibroblast strains from affected members of a cancer-prone family with Li-Fraumeni syndrome. Br. J. Cancer, 71, 1221-1230.
46. Missero,C. Calaulti,E., Eckner,R., Chin,J., Tsai,L.H., Livingston,D.M. and Dotto,G.P. (1995) Involvement of the cell-cycle inhibitor Cip1/WAF1 and the E1A-associated p300 protein in terminal differentiation. Proc. Natl Acad. Sci. USA, 92, 5451-5455.
47. Mitsudomi,T. et al. (1992) p53 gene mutations in non-small-cell lung cancer lines and their correlation with the presence of ras mutations and clinical features. Oncogene, 7, 171-180.
48. Morin,G.B. (1989) The human telomere terminal transferase enzyme is a ribonucleoprotein that synthesizes TTAGGG repeats. Cell, 59, 521-529.
49. Noda,A., Ning,Y., Venable,S.F., Pereira-Smith,O.M. and Smith,J.R. (1994) Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res., 211, 90-98.
50. Reed,M., Woelker,B., Wang,P., Wang,Y., Anderson,M.E. and Tegtmeyer,P. (1995) The C-terminal domain of p53 recognizes DNA damaged by ionizing radiation. Proc. Natl Acad. Sci. USA, 92, 9455-9459.
51. Rogan,E.M. et al. (1995) Alterations in p53 and p16INK4 expression and telomere length during spontaneous immortalization of Li-Fraumeni syndrome fibroblasts. Mol. Cell. Biol., 15, 4745-4753.
52. Rovinski,B. and Benchimol,S. (1988) Immortalization of rat embryo fibroblasts by the cellular p53 oncogene. Oncogene, 2, 445-452.
53. Rubelj,I. and Pereira-Smith,O.M. (1994) SV40-transformed human cells in crisis exhibit changes that occur in normal cellular senescence. Exp. Cell Res., 211, 82-89.
54. Saito,H., Hammond,A.T. and Moses,R.E. (1995) The effect of low oxygen tension on the in vitro-replicative life span of human diploid fibroblast cells and their transformed derivatives. Exp. Cell Res., 217, 272-279.
55. Shah,G.M., Poirier,D., Desnoyers,S., Saint-Martin,S., Hoflack,J., Rong,P., Apsimon,M., Kirkland,J.B. and Poirier,G.G. (1996) Complete inhibition of poly(ADP-ribose) polymerase activity prevents the recovery of C3H10T1/2 cells from oxidative stress. Biochim. Biophys. Acta, 1312, 1-7.
56. Shay,J.W., Wright,W.E., Brasiskyte,D. and Van der Haegen,B.A. (1993) E6 of human papillomavirus type 16 can overcome the M1 stage of immortalization in human mammary epithelial cells but not in human fibroblasts. Oncogene, 8, 1407-1413.
57. Sherwood,S.W., Rush,D., Ellsworth,J.L. and Schimke,R.T. (1988) Defining cellular senescence in IMR-90 cells: a flow cytometric analysis. Proc. Natl Acad. Sci. USA, 85, 9086-9090.
58. Shiloh,Y., Tabor,E. and Becker,Y (1982) Colony-forming ability of ataxia-telangiectasia skin fibroblasts is an indicator of their early senescence and increased demand for growth factors. Exp.Cell Res., 140, 191-199.
59. Srivastava,S., Zou,Z.Q., Pirollo,K., Blattner,W. and Chang,E.H. (1990) Germ-line transmission of a mutated p53 gene in a cancer-prone family with Li-Fraumeni syndrome. Nature, 348, 747-749.
60. Vaziri,H. and Benchimol,S. (1996) From telomere loss to p53 induction and activation of a DNA-damage pathway at senescence: the telomere loss/DNA damage model of cell aging. Exp. Gerontol, 31, 295-301.
61. Vaziri,H., Schachter,F., Uchida,I., Wei,L., Zhu,X., Effros,R., Cohen,D. and Harley,C.B. (1993) Loss of telomeric DNA during aging of normal and trisomy 21 human lymphocytes. Am. J. Hum. Genet., 52, 661-667.
62. Vaziri,H., Dragowska,W., Allsopp,R.C., Thomas,T.E., Harley,C.B. and Lansdorp, P.M. (1994) Evidence for a mitotic clock in human hematopoietic stem cells: loss of telomeric DNA with age. Proc. Natl Acad. Sci. USA, 91, 9857-9860.
63. von Zglinicki,T., Saretzki,G., Docke,W. and Lotze,C. (1995) Mild hyperoxia shortens telomeres and inhibits proliferation of fibroblasts: a model for senescence? Exp. Cell Res., 220, 186-193.
64. Wang,Z.Q., Auer,B., Stingl,L., Berghammer,H., Haidacher,D., Schweiger,M. and Wagner,E.F. (1995) Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev., 9, 509-520.
65. Watanabe,S., Tadahito,K. and Yoshiike,K. (1989) Human papillomavirus type 16 transformation of primary human embryonic fibroblasts requires expression of open reading frames E6 and E7. J. Virol., 63, 965-969.
66. Wesierska,J., Schmid,G. and Cerni,C. (1996) ADP-ribosylation of wild-type p53 in vitro: binding of p53 to specific p53 consensus sequence prevents its modification. Biochem. Biophys. Res. Commun., 224, 96-102.
67. Whitacre,C.M., Hashimoto,H., Tsai,M.L., Chatterjee,S., Berger,S.J. and Berger,N.A. (1995) Involvement of NAD-poly(ADP-ribose) metabolism in p53 regulation and its consequences. Cancer Res., 55, 3697-3701.
68. Xu,Y. and Baltimore,D. (1996) Dual roles of ATM in the cellular response to radiation and in cell growth control. Genes Dev., 10, 2401-2410.
69. Yang,Z., Perkins,N., Ohno,T., Nabel,E.G. and Nabel,G.J. (1995) The p21 cyclin-dependent kinase inhibitor suppresses tumorigenicity in vivo. Nature Med., 1, 1052-1056.
70. Zhang,J., Dawson,V.L., Dawson,T.M. and Snyder,S.H. (1994) Nitric oxide activation of poly(ADP-ribose) synthetase in neurotoxicity. Science, 263, 687-689.