Telomere Instability in a Human Tumor Cell Line Expressing NBS1 with Mutations at Sites Phosphorylated by ATM

Molecular Cancer Research

Volumn 1, Issue 14, 2003, Pages 1058-1069

  Bai, Yongli ^a   Murnane, John P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; TELOMERASE;

ARTICLE; CANCER CELL CULTURE; CAPPING PHENOMENON; CELL CLONE; CHROMOSOME BREAKAGE; CHROMOSOME LOSS; CHROMOSOME SIZE; CONTROLLED STUDY; DNA SYNTHESIS; GENE DELETION; GENE LOCATION; GENE MUTATION; GENETIC STABILITY; HUMAN; HUMAN CELL; MUTATION RATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RADIOSENSITIVITY; STOCHASTIC MODEL; TELOMERE;

ATAXIA TELANGIECTASIA; CELL CYCLE; CELL CYCLE PROTEINS; CELL SURVIVAL; CHROMOSOMAL INSTABILITY; DNA; DNA-BINDING PROTEINS; HUMANS; MUTATION; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RADIATION, IONIZING; RECOMBINATION, GENETIC; TELOMERASE; TELOMERE; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS;

EID: 0347990555     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (74)

1. Digweed, M. Human genetic instability syndromes: single gene defects with increased risk of cancer. Toxicol. Lett., 67: 259-281, 1993.
2. Shiloh, Y. Ataxia-telangiectasia and the Nijmegen breakage syndrome: related disorders but genes apart. Annu. Rev. Genet., 31: 635-662, 1997.
3. Carney, J. P., Maser, R. S., Olivares, H., Davis, E. M., Beau, M., Yates, J. R., Hays, L., Morgan, W. F., and Petrini, J. H. The hMre11/Rad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell, 93: 477-486, 1998.
4. Veron, R., Vissinga, C., Platzer, M., Cerosaletti, K. M., Chrzanowska, K. H., Saar, K., Beckmann, G., Seemanova, E., Cooper, P. R., Nowak, N. J., Stumm, M., Weemaes, C. M. R., Gatti, R. A., Wilson, R. K., Digweed, M., Rosenthal, A., Sperling, K., Concannon, P., and Reis, A. Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell, 93: 467-476, 1998.
5. Zhao, S., Weng, Y-C., Yuan, S-S. F., Lin, Y-T., Hsu, H-C., Lin, S-C. J., Gerbino, E., Song, M-H., Zdizienicka, M. Z., Gatti, R. A., Shay, J. W., Ziv, Y., Shiloh, Y., and Lee, E. Y-H. P. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature, 405: 473-477, 2000.
6. Lim, D. S., Kim, S. T., Xu, B., Maser, R. S., Lin, J., Petrini, J. H, and Kastan, M. B. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature, 404: 613-617, 2000.
7. Wu, X., Ranganathan, V., Weisman, D. S., F. H. W., Ciccone, D. N., O'Neill, T. B., Crick, K. E., Pierce, K. A., Lane, W. S., Rathbun, G., Livingston, D. M., and Weaver, D. T. ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature, 405: 477-482, 2000.
8. Stewert, G. S., Maser, R. S., Stankovic, T., Bressan, D. A., Kaplan, M. I., Jaspers, N. G., Raams, A., Byrd, P. J., Petrini, J. H., and Taylor, A. M. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell, 99: 577-587, 1999.
9. Petrini, J. H. The Mre11 complex and ATM: collaborating to navigate S phase. Curr. Opin. Cell Biol., 12: 293-296, 2000.
10. Taalman, R. D., Jaspers, N. G., Scheres, J. M., de Wit, J., and Hustinx, T. W. Hypersensitivity to ionizing radiation, in vitro, in a new chromosomal breakage disorder, the Nijmegen breakage syndrome. Mutat. Res., 112: 23-32, 1983.
11. Chen, L., Trujillo, K., Ramos, W., Sung, P., and Tomkinson, A. E. Promotion of Dn14-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes. Mol. Cell, 8: 1105-1015, 2001.
12. Lobachev, K. S., Shor, B. M., Tran, H. T., Taylor, W., Keen, J. D., Resnick, M. A., and Gordenin, D. A. Factors affecting inverted repeat stimulation of recombination and deletion in Saccharomyces cerevisiae. Genetics, 148: 1507-1524, 1998.
13. Tauchi, H., Matsuura, S., Kobayashi, J., Sakamoto, S., and Komatsu, K. Nijmegen breakage syndrome gene, NBS1, and molecular links to factors for genome stability. Oncogene, 21: 8967-8980, 2002.
14. Tauchi, H., Kobayashi, J., Morishima, K., van Gent, D. C., Shiraishi, T., Verkaik, N. S., vanHeems, D., Ito, E., Nakamura, A., Sonoda, E., Takata, M., Takeda, S., Matsuura, S., and Komatsu, K. Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature, 420: 93-98, 2002.
15. Comforth, M. N. and Bedford, J. S. On the nature of a defect in cells from individuals with ataxia-telangiectasia. Science, 227: 1589-1591, 1985.
16. Pandita, T. K. and Hittelman, W. N. Initial chromosome damage but not DNA damage is greater in ataxia telangiectasia cells. Radiat. Res., 130: 94-103, 1992.
17. Sullivan, K. E., Veksler, E., Lederman, H., and Lees-Miller, S. P. Cell cycle checkpoints and DNA repair in Nijmegen breakage syndrome. Clin. Immunol. Immunopathol., 82: 43-48, 1997.
18. Kraakman-van der Zwet, M., Overkamp, W. J., Friedl, A. A., Klein, B., Verhaegh, G. W., Jaspers, N. G., Midro, A. T., Eckardt-Schupp, F., Lohman, P. H., and Zdzienicka, M. Z. Immortalization and characterization of Nijmegen breakage syndrome fibroblasts. Mutat. Res., 434: 17-27, 1999.
19. Maser, R. S., Monsen, K. J., Nelms, B. E., and Petrini, J. H. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol. Cell. Biol., 17: 6087-6096, 1997.
20. Nelms, B. E., Maser, R. S., MacKay, J. F., Lagally, M. G., and Petrini, J. H. In situ visualization of DNA double-strand break repair in human fibroblasts. Science, 280: 590-592, 1998.
21. Wu, X., Petrini, J. H., Heine, W. F., Weaver, D. T., Livingston, D. M., and Chen, J. Independence of R/M/N focus formation and the presence of intact BRCA1. Science, 289: 11, 2000.
22. Zhong, Q., Chen, C. F., Li, S., Chen, Y., Wang, C. C., Xiao, J., Chen, P. L., Sharp, Z. D., and Lee, W. H. Association of BRCA1 with the hRad50-hMre11-p95 complex and the DNA damage response. Science, 285: 747-750, 1999.
23. Kobayashi, J., Tauchi, H., Sakamoto, S., Nakamura, A., Morishima, K., Matsuura, S., Kobayashi, T., Tamai, K., Tanimoto, K., and Komatsu, K. NBS1 localizes to γ-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol., 12: 1846-1851, 2002.
24. McEachem, M. J., Krauskopf, A., and Blackbum, E. H. Telomeres and their control. Annu. Rev. Genet., 34: 331-358, 2000.
25. Blackbum, E. H. Switching and signaling at the telomere. Cell, 106: 661-673, 2001.
26. de Lange, T. Telomere dynamics and genome instability in human cancer. In: E. H. Blackbum and C. W. Greider (eds.), Telomeres, pp. 265-293. Plainview, NY: Cold Spring Harbor Press, 1995.
27. Harley, C. B. Telomeres and aging. In: E. H. Blackbum and C. W. Greider (eds.), Telomeres, pp. 247-263. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 1995.
28. 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. Extension of life-span by introduction of telomerase into normal human cells. Science, 279: 349-352, 1998.
29. Counter, C. M., Avilion, A. A., LeFeuvre, C. E., Stewart, N. G., Greider, C. W., Harley, C. B., and Bacchetti, S. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J., 11: 1921-1929, 1992.
30. van Steensel, B., Smogorzewska, A., and de Lange, T. TRF2 protects human telomeres from end-to-end fusions. Cell, 92: 401-413, 1998.
31. Hsu, H-L., Gilley, D., Galande, S. A., Hande, M. P., Allen, B., Kim, S-H., Li, G. C., Campisi, J., Kohwi-Shigematsu, T., and Chen, D. J. Ku acts in a unique way at the mammalian telomere to prevent end joining. Genes Dev., 14: 2807-2812, 2000.
32. Bailey, S. M., Meyne, J., Chen, D. J., Kurimasa, A., Li, G. C., Lehnert, B. E., and Goodwin, E. H. DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc. Natl. Acad. Sci. USA, 96: 14899-14904, 1999.
33. Gilley, D., Tanaka, H., Hande, M. P., Kurimasa, A., Li, G. C., Oshimura, M., and Chen, D. J. DNA-PKcs is critical for telomere capping. Proc. Natl. Acad. Sci. USA, 98: 15084-15088, 2001.
34. Goytisolo, F. A., Samper, E., Edmonson, S., Taccioli, G. E., and Blasco, M. A. The absence of the DNA-dependent protein kinase catalytic subunit in mice results in anaphase bridges and increased telomeric fusions with normal telomere length and G-strand overhang. Mol. Cell. Biol., 21: 3642-3651, 2001.
35. Boulton, S. J. and Jackson, S. P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J., 17: 1819-1828, 1998.
36. Kironmai, K. M. and Muniyappa, K. Alteration of telomeric sequences and senescence caused by mutations in RAD50 of Saccharomyces cerevisiae. Genes Cells, 2: 443-455, 1997.
37. Lustig, A. J. and Petes, T. D. Identification of yeast mutants with altered telomere structure. Proc. Natl. Acad. Sci. USA, 83: 1398-1402, 1986.
38. Ritchie, K. B., Mallory, J. C., and Petes, T. D. Interactions of TLC1 (which encodes the RNA subunit of telomerase), TEL1, and MEC1 in regulating telomere length in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol., 19: 6065-6075, 1999.
39. Ritchie, K. B. and Petes, T. D. The Mre11p/Rad50p/Xrs2p complex and the Te11p function in a single pathway for telomere maintenance in yeast. Genetics, 155: 475-479, 2000.
40. Ranganathan, V., Heine, W. F., Ciccone, D. N., Rudolph, K. L., Wu, X., Chang, S., Hai, H., Ahem, I. M., Livingston, D. M., Resnick, I., Rosen, F., Seemanova, E., Jarolim, P., DePinho, R. A., and Weaver, D. T. Rescue of a telomere length defect in Nijmegen breakage syndrome cells requires NBS and the telomerase catalytic subunit. Curr. Biol., 11: 962-966, 2001.
41. Metcalfe, J. A., Parkhill, J., Campbell, L., Stacey, M., Biggs, P., Byrd, P. J., and Taylor, A. M. R. Accelerated telomere shortening in ataxia telangiectasia. Nat. Genet., 13: 350-353, 1996.
42. Wong, K. K., Maser, R. S., Bachoo, R. M., Menon, J., Carrasco, D. R., Gu Y., Alt, F. W., and DePinho, R. A. Telomere dysfunction and Atm deficiency compromises organ homeostasis and accelerates aging. Nature, 421: 643-648, 2003.
43. Zhu, X-D., Kuster, B., Mann, M., Petrini, J. H. J., and de Lange, T. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet., 25: 347-352, 2000.
44. Karlseder, J., Smogorzewska, A., and de Lange, T. Senescence induced by altered telomere state, not telomere loss. Science, 295: 2446-2449, 2002.
45. Stansel, R. M., de Lange, T., and Griffith, J. D. T-loop assembly in vitro involves binding of TRF2 near the 3′ telomeric overhang. EMBO J., 20: 5532-5540, 2001.
46. Fouladi, B., Miller, D., Sabatier, L., and Murnane, J. P. The relationship between spontaneous telomere loss and chromosome instability in a human tumor cell line. Neoplasia, 2: 540-554, 2000.
47. Lo, A. W. I., Sabatier, L., Fouladi, B., Pottier, G., Ricoul, M., and Murnane, J. P. DNA amplification by breakage/fusion/bridge cycles initiated by spontaneous telomere loss in a human cancer cell line. Neoplasia, i6: 531-538, 2002.
48. Hanish, J. P., Yanowitz, J. L., and De Lange, T. Stringent sequence requirements for the formation of human telomeres. Proc. Natl. Acad. Sci. USA, 91: 8861-8865, 1994.
49. Barnett, M. A., Buckle, J., Evans, E. P., Porter, A. C. G., Rout, D., Smith, A. G., and Brown, W. R. A. Telomere directed fragmentation of mammalian chromosomes. Nucleic Acids Res., 21: 27-36, 1993.
50. Farr, C., Fantes, J., Goodfellow, P., and Cooke, H. Functional reintroduction of human telomeres into mammalian cells. Proc. Natl. Acad. Sci. USA, 88: 7006-7010, 1991.
51. Sprung, C. N., Sabatier, L., and Murnane, J. P. Telomere dynamics in human cancer cell line. Exp. Cell Res., 247: 29-37, 1999.
52. Sprung, C. N., Afshar, G., Chavez, E. A., Lansdorp, P., Sabatier, L., and Murnane, J. P. Telomere instability in a human cancer cell line. Mutat. Res., 429: 209-223, 1999.
53. Lo, A. W. I., Sprung, C. N., Fouladi, B., Pedram, M., Sabatier, L., Ricoul, M., Reynolds, G. E., and Murnane, J. P. Chromosome instability as a result of double-strand breaks near telomeres in mouse embryonic stem cells. Mol. Cell. Biol., 22: 4836-4850, 2002.
54. Rossi, F. M. V., Guicherit, O. M., Spicher, A., Kringstein, A. M., Fatyol, K., Blakely, B. T., and Blau, H. M. Tetracycline-regulatable factors with distinct dimerization domains allow reversible growth inhibition by p16. Nat. Genet., 20: 389-393, 1998.
55. Gossen, M. and Bujard, H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA, 89: 5547-5551, 1992.
56. 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. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet., 5: 685-691, 1996.
57. Gisselsson, D., Jonson, T., Petersen, A., Strombeck, B., Dal Cin, P., Hoglund, M., Mitelman, F., Mertens, F., and Mandahl, N. Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc. Natl. Acad. Sci. USA, 98: 12683-12688, 2001.
58. Gatei, M., Young, D., Cerosaletti, K. M., Desai-Mehta, A., Spring, K., Kozlov, S., Lavin, M. F., Gatti, R. A., Concannon, P., and Khanna, K. K. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat. Genet., 25: 115-119, 2000.
59. Lee, J. H., Xu, B., Lee, C-H., Ahn, J-Y., Song, M. S., Lee, H., Canman, C. E., Lee, J-S., Kastan, M. B., and Lim, D-S. Distinct functions of Nijmegen breakage syndrome in ataxia telangiectasia mutated-dependent responses to DNA damage. Mol. Cancer Res., 1: 674-681, 2003.
60. Sprung, C. N., Bryan, T. M., Reddel, R. R., and Murnane, J. P. Normal telomere maintenance in immortal ataxia telangiectasia cell lines. Mutat. Res., 379: 177-184, 1997.
61. Kojis, T. L., Gatti, R. A., and Sparkes, R. S. The cytogenetics of ataxia telangiectasia. Cancer Genet. Cytogenet., 56: 143-156, 1991.
62. Pandita, T. K., Pathak, S., and Geard, C. Chromosome end associations, telomeres and telomerase activity in ataxia telangiectasia cells. Cytogenet. Cell Genet., 71: 86-93, 1995.
63. Costanzo, V., Robertson, K., Bibikova, M., Kim, E., Grieco, D., Gottesman, M., Carroll, D., and Gautier, J. Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell, 8: 137-147, 2001.
64. Maser, R. S., Mirzoeva, O. K., Wells, J., Olivares, H., Williams, B. R., Zinkel, R. A., Farnham, P. J., and Petrini, J. H. Mre11 complex and DNA replication: linkage to E2F and sites of DNA synthesis. Mol. Cell. Biol., 21: 6006-6016, 2001.
65. Limoli, C. L., Giedzinski, E., Morgan, W. F., and Cleaver, J. E. Inaugural article: polymerase η deficiency in the xeroderma pigmentosum variant uncovers an overlap between the S phase checkpoint and double-strand break repair. Proc. Natl. Acad. Sci. USA, 97: 7939-7946, 2002.
66. Tchirkov, A. and Lansdorp, P. M. Role of oxidative stress in telomere shortening in cultured fibroblasts from normal individuals and patients with ataxia-telangiectasia. Hum. Mol. Genet., 12: 227-232, 2003.
67. Griffith, J. D., Comeau, L., Rosenfield, S., Stansel, R. M., Bianchi, A., Moss, H., and de Lange, T. Mammalian telomeres end in a large duplex loop. Cell, 97: 503-514, 1999.
68. de Lange, T. and Petrini, J. H. J. A new connection at human telomeres: association of the Mre11 complex with TRF2. Cold Spring Harbor Symp. Quant. Biol., 65: 265-273, 2000.
69. Bai, Y. and Murnane, J. P. Telomere instability in a human tumor cell line expressing a dominant-negative WRN protein. Hum. Genet., 113: 337-347, 2003.
70. Opresko, P. L., von Kobbe, C., Laine, J-P., Harrigan, J., Hickson, I. D., and Bohr, V. A. Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem., 277: 41110-41119, 2002.
71. O'Toole, C. M., Povey, S., Hepbum, P., and Franks, L. M. Identity of some human bladder cancer cell lines. Nature, 301: 429-430, 1983.
72. --transformed ataxia-telangiectasia cell line. Exp. Cell Res., 158: 119-126, 1985.
73. Luria, S. E. and Delbruck, M. Mutations of bacteria from virus sensitivity to virus resistance. Genetics, 28: 491-511, 1943.
74. Capizzi, R. L. and Jameson, J. W. A table for the estimation of the spontaneous mutation rate of cells in culture. Mutat. Res., 17: 147-148, 1972.