Dual roles of telomere dysfunction in initiation and suppression of tumorigenesis

Experimental Cell Research

Volumn 314, Issue 9, 2008, Pages 1973-1979

  Cosme Blanco, Wilfredo ^a   Chang, Sandy ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Cancer; DNA damage; Genomic instability; Senescence; Telomeres

Indexed keywords

PROTEIN P53;

CANCER INHIBITION; CARCINOGENESIS; CHROMOSOME ABERRATION; CHROMOSOME STRUCTURE; DNA DAMAGE; GENE FUNCTION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENESCENCE; TELOMERE;

EID: 43049165666     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2008.03.011     Document Type: Review

References (69)

1. L. Hayflick P.S. Moorhead The serial cultivation of human diploid cell strains Exp. Cell Res. 25 1961 585 621
2. G.P. Dimri A biomarker that identifies senescent human cells in culture and in aging skin in vivo Proc. Natl. Acad. Sci. U. S. A. 92 20 1995 9363 9367
3. C.M. Counter Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity EMBO. J. 11 5 1992 1921 1929
4. W.E. Wright Telomerase activity in human germline and embryonic tissues and cells Dev. Genet. 18 2 1996 173 179
5. C.B. Harley A.B. Futcher C.W. Greider Telomeres shorten during ageing of human fibroblasts Nature 345 6274 1990 458 460
6. R.C. Allsopp Telomere length predicts replicative capacity of human fibroblasts Proc. Natl. Acad. Sci. U. S. A. 89 21 1992 10114 10118
7. C.B. Harley Telomerase, cell immortality, and cancer Cold Spring Harb. Symp. Quant. Biol. 59 1994 307 315
8. A.G. Bodnar Extension of life-span by introduction of telomerase into normal human cells Science 279 5349 1998 349 352
9. H. Vaziri S. Benchimol Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended replicative life span Curr. Biol. 8 5 1998 279 282
10. T. de Lange Shelterin: the protein complex that shapes and safeguards human telomeres Genes Dev. 19 18 2005 2100 2110
11. P. Baumann E. Podell T.R. Cech Human Pot1 (protection of telomeres) protein: cytolocalization, gene structure, and alternative splicing Mol. Cell Biol. 22 22 2002 8079 8087
12. B. van Steensel A. Smogorzewska T. de Lange TRF2 protects human telomeres from end-to-end fusions Cell 92 3 1998 401 413
13. G.B. Celli T. de Lange DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion Nat. Cell Biol. 7 7 2005 712 718
14. W.E. Wright J.W. Shay The two-stage mechanism controlling cellular senescence and immortalization Exp. Gerontol. 27 4 1992 383 389
15. F. d'Adda di Fagagna A DNA damage checkpoint response in telomere-initiated senescence Nature 426 6963 2003 194 198
16. H. Takai A. Smogorzewska T. de Lange DNA damage foci at dysfunctional telomeres Curr. Biol. 13 17 2003 1549 1556
17. U. Herbig Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a) Mol. Cell 14 4 2004 501 513
18. D. Churikov C.M. Price Pot1 and cell cycle progression cooperate in telomere length regulation Nat. Struct. Mol. Biol. 15 1 2008 79 84
19. X. Guo Dysfunctional telomeres activate an ATM–ATR-dependent DNA damage response to suppress tumorigenesis Embo. J. 26 22 2007 4709 4719
20. V. Gire Dysfunctional telomeres at senescence signal cell cycle arrest via Chk2 Cell Cycle 3 10 2004 1217 1220
21. H.W. Lee Essential role of mouse telomerase in highly proliferative organs Nature 392 6676 1998 569 574
22. K.L. Rudolph Longevity, stress response, and cancer in aging telomerase-deficient mice Cell 96 5 1999 701 712
23. W.Y. Kim N.E. Sharpless The regulation of INK4/ARF in cancer and aging Cell 127 2 2006 265 275
24. J.J. Jacobs T. de Lange Significant role for p16INK4a in p53-independent telomere-directed senescence Curr. Biol. 14 24 2004 2302 2308
25. A. Smogorzewska T. de Lange Different telomere damage signaling pathways in human and mouse cells Embo. J. 21 16 2002 4338 4348
26. J. Karlseder p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2 Science 283 5406 1999 1321 1325
27. L. Wu Pot1 deficiency initiates DNA damage checkpoint activation and aberrant homologous recombination at telomeres Cell 126 1 2006 49 62
28. E.L. Denchi T. de Lange Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1 Nature 448 7157 2007 1068 1071
29. E. Hara Cooperative effect of antisense-Rb and antisense-p53 oligomers on the extension of life span in human diploid fibroblasts, TIG-1 Biochem. Biophys. Res. Commun. 179 1 1991 528 534
30. J.W. Shay W.E. Wright H. Werbin Defining the molecular mechanisms of human cell immortalization Biochim. Biophys. Acta 1072 1 1991 1 7
31. J.W. Shay The frequency of immortalization of human fibroblasts and mammary epithelial cells transfected with SV40 large T-antigen Exp. Cell Res. 209 1 1993 45 52
32. N.W. Kim Specific association of human telomerase activity with immortal cells and cancer Science 266 5193 1994 2011 2015
33. J.W. Shay S. Bacchetti A survey of telomerase activity in human cancer Eur. J. Cancer 33 5 1997 787 791
34. T.M. Nakamura Telomerase catalytic subunit homologs from fission yeast and human Science 277 5328 1997 955 959
35. V. Lundblad E.H. Blackburn An alternative pathway for yeast telomere maintenance rescues est1-senescence Cell 73 2 1993 347 360
36. J.A. Hackett D.M. Feldser C.W. Greider Telomere dysfunction increases mutation rate and genomic instability Cell 106 3 2001 275 286
37. M.A. Blasco Telomere shortening and tumor formation by mouse cells lacking telomerase RNA Cell 91 1 1997 25 34
38. R.S. Maser R.A. DePinho Connecting chromosomes, crisis, and cancer Science 297 5581 2002 565 569
39. M.P. Hande Telomere length dynamics and chromosomal instability in cells derived from telomerase null mice J. Cell. Biol. 144 4 1999 589 601
40. S.E. Artandi Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice Nature 406 6796 2000 641 645
41. S. Chang Telomere-based crisis: functional differences between telomerase activation and ALT in tumor progression Genes Dev. 17 1 2003 88 100
42. K. Masutomi Telomerase maintains telomere structure in normal human cells Cell 114 2 2003 241 253
43. N.P. Weng L. Granger R.J. Hodes Telomere lengthening and telomerase activation during human B cell differentiation Proc. Natl. Acad. Sci. U. S. A. 94 20 1997 10827 10832
44. R.F. Newbold, Genetic control of telomerase and replicative senescence in human and rodent cells. Ciba Found Symp, 1997. 211: p. 177–89; discussion 189–97.
45. M. Meyerson hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization Cell 90 4 1997 785 795
46. J.M. Zijlmans Telomeres in the mouse have large inter-chromosomal variations in the number of T2AG3 repeats Proc. Natl. Acad. Sci. U. S. A. 94 14 1997 7423 7428
47. L. Martin-Rivera Expression of mouse telomerase catalytic subunit in embryos and adult tissues Proc. Natl. Acad. Sci. U. S. A. 95 18 1998 10471 10476
48. R.A. Greenberg Expression of mouse telomerase reverse transcriptase during development, differentiation and proliferation Oncogene 16 13 1998 1723 1730
49. D. Kipling H.J. Cooke Hypervariable ultra-long telomeres in mice Nature 347 6291 1990 400 402
50. K.R. Prowse C.W. Greider Developmental and tissue-specific regulation of mouse telomerase and telomere length Proc. Natl. Acad. Sci. U. S. A. 92 11 1995 4818 4822
51. S. Chang C. Khoo R.A. DePinho Modeling chromosomal instability and epithelial carcinogenesis in the telomerase-deficient mouse Semin. Cancer Biol. 11 3 2001 227 239
52. E. Herrera A.C. Martinez M.A. Blasco Impaired germinal center reaction in mice with short telomeres Embo. J. 19 3 2000 472 481
53. M.T. Hemann The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability Cell 107 1 2001 67 77
54. E. Samper J.M. Flores M.A. Blasco Restoration of telomerase activity rescues chromosomal instability and premature aging in Terc−/− mice with short telomeres EMBO Rep. 2 9 2001 800 807
55. L. Chin p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis Cell 97 4 1999 527 538
56. M. Hollstein p53 mutations in human cancers Science 253 5015 1991 49 53
57. M.S. Greenblatt Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis Cancer Res. 54 18 1994 4855 4878
58. M. Veloso p53 gene status and expression of p53, mdm2, and p21Waf1/Cip1 proteins in colorectal cancer Virchows Arch. 437 3 2000 241 247
59. M. Serrano Role of the INK4a locus in tumor suppression and cell mortality Cell 85 1 1996 27 37
60. T. Kamijo Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF Cell 91 5 1997 649 659
61. R.A. Greenberg Short dysfunctional telomeres impair tumorigenesis in the INK4a(delta2/3) cancer-prone mouse Cell 97 4 1999 515 525
62. E. Gonzalez-Suarez Telomerase-deficient mice with short telomeres are resistant to skin tumorigenesis Nat. Genet. 26 1 2000 114 117
63. K.L. Rudolph Telomere dysfunction and evolution of intestinal carcinoma in mice and humans Nat. Genet. 28 2 2001 155 159
64. W.F. Dove The intestinal epithelium and its neoplasms: genetic, cellular and tissue interactions Philos. Trans. R. Soc. Lond. B. Biol. Sci. 353 1370 1998 915 923
65. P.A. Farazi Differential impact of telomere dysfunction on initiation and progression of hepatocellular carcinoma Cancer Res. 63 16 2003 5021 5027
66. D.M. Feldser C.W. Greider Short telomeres limit tumor progression in vivo by inducing senescence Cancer Cell 11 5 2007 461 469
67. W. Cosme-Blanco Telomere dysfunction suppresses spontaneous tumorigenesis in vivo by initiating p53-dependent cellular senescence EMBO Rep. 8 5 2007 497 503
68. G. Liu Chromosome stability, in the absence of apoptosis, is critical for suppression of tumorigenesis in Trp53 mutant mice Nat. Genet. 36 1 2004 63 68
69. A.R. Choudhury Cdkn1a deletion improves stem cell function and lifespan of mice with dysfunctional telomeres without accelerating cancer formation Nat. Genet. 39 1 2007 99 105