Telomere-based crisis: Functional differences between telomerase activation and ALT in tumor progression

Genes and Development

Volumn 17, Issue 1, 2003, Pages 88-100

  Chang, Sandy ^a,c,d   Khoo, Christine M ^a,b   Naylor, Maria L ^a,b   Maser, Richard S ^a,b   DePinho, Ronald A ^a,b  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

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

Author keywords

ALT (alternative lengthening of telomeres); Chromosomal instability; Metastasis; SKY; Telomerase; Telomere

Indexed keywords

TELOMERASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL; CHROMOSOME ANALYSIS; CHROMOSOME DELETION; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; CYTOGENETICS; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; FIBROBLAST; METAPHASE; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TELOMERE; TUMOR GROWTH;

ANIMALIA;

EID: 0037224923     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1029903     Document Type: Article

References (72)

1. 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 fibroblasts. Proc. Natl. Acad. Sci. 89: 10114-10118.
2. Artandi, S.E., Chang, S., Lee, S.L., Alson, S., Gottlieb, G.J., Chin, L., and DePinho, R.A. 2000. Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice, Nature 406: 641-645,
3. Artandi, S.E., Alson, S., Tietze, M.K., Sharpless, N.E., Ye, S., Greenberg, R.A., Castrillon, D.H., Horner, J.W., Weiler, S.R., Carrasco, R.D., et al, 2002, Constitutive telomerase expression promotes mammary carcinomas in aging mice. Proc. Natl. Acad. Sci. 99: 8191-8196,
4. Balcom, J.H.T., Keck, T., Warshaw, A.L., Antoniu, B., Graeme-Cook, F., and Fernandez-del Castillo, C. 2001. Telomerase activity in periampullary tumors correlates with aggressive malignancy. Ann. Surg. 234: 344-350; discussion 350-351.
5. Blackburn, E.H. 2001. Switching and signaling at the telomere. Cell 106: 661-673.
6. Blasco, M.A., Lee, H.W., Hande, M.P., Samper, E., Lansdorp, P.M., DePinho, R.A., and Greider, C.W. 1997. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91: 25-34.
7. Bodnar, A.G., Ouellette, M., Frolkis, M., Holt, S.E., Chiu, C.P., Morin, G.B., Harley, C.B., Shay, J.W., Lichtsteiner, S., and Wright, W.E. 1998. Extension of life-span by introduction of telomerase into normal human cells. Science 279: 349-352.
8. Bohr, V.A. and Dianov, G.L. 1999. Oxidative DNA damage processing in nuclear and mitochondrial DNA. Biochimie 81:155-160.
9. Boklan, J., Nanjangud, G., MacKenzie, K.L., May, C., Sadelain, M., and Moore, M.A. 2002. Limited proliferation and telomere dysfunction following telomerase inhibition in immortal murine fibroblasts. Cancer Res. 62: 2104-2114.
10. Bryan, T.M., Englezou, A., Dalla-Pozza, L., Dunham, M.A., and Reddel, R.R. 1997. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med. 3: 1271-1274.
11. Chadeneau, C., Hay, K., Hirte, H.W., Gallinger, S., and Bacchetti, S. 1995. Telomerase activity associated with acquisition of malignancy in human colorectal cancer. Cancer Res. 55: 2533-2536.
12. Chang, S. and DePinho, R.A. 2002. Telomerase extracurricular activities. Proc. Natl. Acad. Sci. 99: 12520-12522.
13. Chin, L., Artandi, S.E., Shen, Q., Tam, A., Lee, S.L., Gottlieb, G.J., Greider, C.W., and DePinho, R.A. 1999. p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97: 527-538.
14. 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.
15. Counter, C.M., Hirte, H.W., Bacchetti, S., and Harley, C.B. 1994. Telomerase activity in human ovarian carcinoma. Proc. Natl. Acad. Sci. 91: 2900-2904.
16. de Lange, T. 1995. Telomere dynamics and genomic instability in human cancer. In Telomeres (eds. E.H. Blackburn and C.W. Greider), pp. 265-293. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
17. de Lange, T., Shiue, L., Myers, R.M., Cox, D.R., Naylor, S.L., Killery, A.M., and Varmus, H.E. 1990. Structure and variability of human chromosome ends. Mol. Cell. Biol. 10: 518-527.
18. Detke, S., Lichtler, A., Phillips, I., Stein, J., and Stein, G. 1979. Reassessment of histone gene expression during cell cycle in human cells by using homologous H4 histone cDNA. Proc. Natl. Acad. Sci. 76: 4995-4999.
19. Dunham, M.A., Neumann, A.A., Fasching, C.L., and Reddel, R.R. 2000. Telomere maintenance by recombination in human cells. Nat. Genet. 26:447-450.
20. Elledge, S.J. 1996. Cell cycle checkpoints: Preventing an identity crisis. Science 274: 1664-1672.
21. Espejel, S. and Blasco, M.A. 2002. Identification of telomeredependent "senescence-like" arrest in mouse embryonic fibroblasts. Exp. Cell Res. 276: 242-248.
22. Frank, K.M., Sharpless, N.E., Gao, Y., Sekiguchi, J.M., Ferguson, D.O., Zhu, C., Manis, J.P., Horner, J., DePinho, R.A., and Alt, F.W. 2000. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell 5: 993-1002.
23. Gisselsson, D., Pettersson, L., Hoglund, M., Heidenblad, M., Gorunova, L., Wiegant, J., Mertens, F., Dal Cin, P., Mitelman, F., and Mandahl, N. 2000. Chromosomal breakage-fusion-bridge events cause genetic intratumor heterogeneity. Proc. Natl. Acad. Sci. 97: 5357-5362.
24. Gonzalez-Suarez, E., Samper, E., Flores, J.M., and Blasco, M.A. 2000. Telomerase-deficient mice with short telomeres are resistant to skin tumorigenesis. Nat. Genet. 26: 114-117.
25. Gonzalez-Suarez, E., Samper, E., Ramirez, A., Flores, J.M., Martin-Caballero, J., Jorcano, J.L., and Blasco, M.A. 2001. Increased epidermal tumors and increased skin wound healing in transgenic mice overexpressing the catalytic subunit of telomerase, mTERT, in basal keratinocytes. EMBO J. 20: 2619-2630.
26. Greenberg, R.A., Allsopp, R.C., Chin, L., Morin, G.B., and DePinho, R.A. 1998. Expression of mouse telomerase reverse transcriptase during development, differentiation and proliferation. Oncogene 16: 1723-1730.
27. Greenberg, R.A., Chin, L., Femino, A., Lee, K.H., Gottlieb, G.J., Singer, R.H., Greider, C.W., and DePinho, R.A. 1999. Short dysfunctional telomeres impair tumorigenesis in the INK4a(δ2/3) cancer-prone mouse. Cell 97: 515-525.
28. Greider, C.W. 1996. Telomere length regulation. Annu. Rev. Biochem. 65: 337-365.
29. 2/M phase of the cell cycle. J. Cell Sci. 113 (Pt 24): 4577-4585.
30. Hahn, W.C., Counter, C.M., Lundberg, A.S., Beijersbergen, R.L., Brooks, M.W. and Weinberg, R.A. 1999a. Creation of human tumour cells with defined genetic elements. Nature 400: 464-468.
31. Hahn, W.C., Stewart, S.A., Brooks, M.W., York, S.G., Eaton, E., Kurachi, A., Beijersbergen, R.L., Knoll, J.H., Meyerson, M., and Weinberg, R.A. 1999b. Inhibition of telomerase limits the growth of human cancer cells. Nat. Med. 5: 1164-1170.
32. Hanahan, D. and Weinberg, R.A. 2000. The hallmarks of cancer. Cell 100: 57-70.
33. Hande, M.P., Samper, E., Lansdorp, P., and Blasco, M.A. 1999. Telomere length dynamics and chromosomal instability in cells derived from telomerase null mice. J. Cell Biol. 144: 589-601.
34. Hara, E., Tsurui, H., Shinozaki, A., Nakada, S., and Oda, K. 1991. 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: 528-534.
35. Harley, C.B., Futcher, A.B., and Greider, C.W. 1990. Telomeres shorten during ageing of human fibroblasts. Nature 345: 458-460.
36. 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.
37. Hemann, M.T., Strong, M.A., Hao, L.Y., and Greider, C.W. 2001. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107: 67-77.
38. Kamijo, T., Weber, J.D., Zambetti, G., Zindy, F., Roussel, M.F., and Sherr, C.J. 1998. Functional and physical interactions of the ARF tumor suppressor with p53 and Mdm2. Proc. Natl. Acad. Sci. 95: 8292-8297.
39. Kim, N.W., Piatyszek, M.A., Prowse, K.R., Harley, C.B., West, M.D., Ho, P.L., Coviello, G.M., Wright, W.E., Weinrich, S.L., and Shay, J.W. 1994. Specific association of human telomerase activity with immortal cells and cancer. Science 266: 2011-2015.
40. Lansdorp, P.M., Verwoerd, N.P., van de Rijke, F.M., Dragowska, V., Little, M.T., Dirks, R.W., Raap, A.K., and Tanke, H.J. 1996. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 5: 685-691.
41. Lansdorp, P.M., Poon, S., Chavez, E., Dragowska, V., Zijlmans, M., Bryan, T., Reddel, R., Egholm, M., Bacchetti, S., and Martens, U. 1997. Telomeres in the haemopoietic system. Ciba Found. Symp. 211: 209-218.
42. Lengauer, C., Kinzler, K.W., and Vogelstein, B. 1998. Genetic instabilities in human cancers. Nature 396: 643-649.
43. Maser, R.S. and DePinho, R.A. 2002. Connecting chromosomes, crisis, and cancer. Science 297: 565-569.
44. McClintock, B. 1941. The stability of broken ends of chromosomes in Zea mays. Genetics 26: 234-282.
45. Murnane, J.P., Sabatier, L., Marder, B.A., and Morgan, W.F. 1994. Telomere dynamics in an immortal human cell line. EMBO J. 13: 4953-4962.
46. Nakabayashi, K., Ogata, T., Fujii, M., Tahara, H., Ide, T., Wadhwa, R., Kaul, S.C., Mitsui, Y., and Ayusawa, D. 1997. Decrease in amplified telomeric sequences and induction of senescence markers by introduction of human chromosome 7 or its segments in SUSM-1. Exp. Cell Res. 235: 345-353.
47. Niida, H., Matsumoto, T., Satoh, H., Shiwa, M., Tokutake, Y., Furuichi, Y., and Shinkai, Y. 1998. Severe growth defect in mouse cells lacking the telomerase RNA component. Nat. Genet. 19: 203-206.
48. Niida, H., Shinkai, Y., Hande, M.P., Matsumoto, T., Takehara, S., Tachibana, M., Oshimura, M., Lansdorp, P.M., and Furuichi, Y. 2000. Telomere maintenance in telomerase-deficient mouse embryonic stem cells: Characterization of an amplified telomeric DNA. Mol. Cell. Biol. 20: 4115-4127.
49. O'Driscoll, M., Cerosaletti, K.M., Girard, P.M., Dai, Y., Stumm, M., Kysela, B., Hirsch, B., Gennery, A., Palmer, S.E., Seidel, J., et al. 2001. DNA ligase IV mutations identified in patients exhibiting developmental delay and immunodeficiency. Mol. Cell 8: 1175-1185.
50. O'Hagan, R., Chang, S., Maser, R., Mohan, R., Artandi, S., Chin, L., and DePinho, R. 2002. Telomere dysfunction provokes regional amplification and deletion in cancer genomes. Cancer Cell 2: 149.
51. Perrem, K., Bryan, T.M., Englezou, A., Hackl, T., Moy, E.L., and Reddel, R.R. 1999. Repression of an alternative mechanism for lengthening of telomeres in somatic cell hybrids. Oncogene 18: 3383-3390.
52. Perrem, K., Colgin, L.M., Neumann, A.A., Yeager, T.R., and Reddel, R.R. 2001. Coexistence of alternative lengthening of telomeres and telomerase in hTERT-transfected GM847 cells. Mol. Cell. Biol. 21: 3862-3875.
53. Rudolph, K.L., Chang, S., Lee, H.W., Blasco, M., Gottlieb, G.J., Greider, C., and DePinho, R.A. 1999. Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96: 701-712.
54. Rudolph, K.L., Chang, S., Millard, M., Schreiber-Agus, N., and DePinho, R.A. 2000. Inhibition of experimental liver cirrhosis in mice by telomerase gene delivery. Science 287: 1253-1258.
55. Saito, Y., Kosugi, S., Suda, T., Wakabayashi, Y., Mishima, Y., Hatakeyama, K., and Kominami, R. 1997. Telomerase activity and metastasis: Expansion of cells having higher telomerase activity within culture lines and tumor tissues. Jpn. J. Cancer Res. 88: 732-737.
56. -/- mice with short telomeres. EMBO Rep. 2: 800-807.
57. Shay, J.W. and Bacchetti, S. 1997. A survey of telomerase activity in human cancer. Eur. J. Cancer 33: 787-791.
58. Shay, J.W., Pereira-Smith, O.M., and Wright, W.E. 1991. A role for both RB and p53 in the regulation of human cellular senescence. Exp. Cell Res. 196: 33-39.
59. Shay, J.W., Van Der Haegen, B.A., Ying, Y., and Wright, W.E. 1993. The frequency of immortalization of human fibroblasts and mammary epithelial cells transfected with SV40 large T-antigen. Exp. Cell Res. 209: 45-52.
60. Shen, C.Y., Yu, J.C., Lo, Y.L., Kuo, C.H., Yue, C.T., Jou, Y.S., Huang, C.S., Lung, J.C., and Wu, C.W. 2000. Genome-wide search for loss of heterozygosity using laser capture microdissected tissue of breast carcinoma: An implication for mutator phenotype and breast cancer pathogenesis. Cancer Res. 60: 3884-3892.
61. Stackpole, C.W. 1981. Distinct lung-colonizing and lung-metastasizing cell populations in B16 mouse melanoma. Nature 289: 798-800.
62. - human mammary epithelial cells. Proc. Natl. Acad. Sci. 98: 4498-503.
63. Stewart, S.A., Hahn, W.C., O'Connor, B.F., Banner, E.N., Lundberg, A.S., Modha, P., Mizuno, H., Brooks, M.W., Fleming, M., Zimonjic, D.B., et al. 2002. Telomerase contributes to tumorigenesis by a telomere length-independent mechanism. Proc. Natl. Acad. Sci. USA. 99:12606-12611.
64. Tang, R., Cheng, A.J., Wang, J.Y., and Wang, T.C. 1998. Close correlation between telomerase expression and adenomatous polyp progression in multistep colorectal carcinogenesis. Cancer Res. 58: 4052-4054.
65. Todaro, G.J. and Green, H. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17: 299-313.
66. Vaziri, H. and Benchimol, S. 1998. Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended replicative life span. Curr. Biol. 8: 279-282.
67. Wright, W.E. and Shay, J.W. 1992. The two-stage mechanism controlling cellular senescence and immortalization. Exp. Gerontol. 27: 383-389.
68. 2 phases in immortalized telomerase-negative cells: Implication of NBS1 in alternative lengthening of telomeres. J. Biol. Chem. 275: 30618-30622
69. Yan, P., Coindre, J.M., Benhattar, J., Bosman, F.T., and Guillou, L. 1999. Telomerase activity and human telomerase reverse transcriptase mRNA expression in soft tissue tumors: Correlation with grade, histology, and proliferative activity. Cancer Res. 59: 3166-3170.
70. Yeager, T.R., Neumann, A.A., Englezou, A., Huschtscha, L.I., Noble, J.R., and Reddel, R.R. 1999. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59: 4175-4179.
71. Zhang, X., Mar, V., Zhou, W., Harrington, L., and Robinson, M.O. 1999. Telomere shortening and apoptosis in telomerase-inhibited human tumor cells. Genes & Dev. 13: 2388-2399.
72. Zhu, C., Mills, K.D., Ferguson, D.O., Lee, C., Manis, J., Fleming, J., Gao, Y., Morton, C.C., and Alt, F.W. 2002. Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell 109: 811-821.