Effect of telomere proximity on telomere position effect, chromosome healing, and sensitivity to DNA double-strand breaks in a human tumor cell line

Molecular and Cellular Biology

Volumn 30, Issue 3, 2010, Pages 578-589

  Kulkarni, Avanti ^a   Zschenker, Oliver ^a   Reynolds, Gloria ^a   Miller, Douglas ^a   Murnane, John P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CARCINOMA CELL; CHROMOSOMAL INSTABILITY; CHROMOSOME; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; PLASMID; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; TELOMERE; TUMOR CELL LINE;

CELL LINE, TUMOR; CHROMOSOMAL INSTABILITY; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; HUMANS; SEQUENCE DELETION; TELOMERE;

MAMMALIA;

EID: 75149134005     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01137-09     Document Type: Article

References (67)

1. Aparicio, O. M., B. L. Billington, and D. E. Gottschling. 1991. Modifiers of position effect are shared between telomeric and silent mating-type loci in S. cerevisiae. Cell 66:1279-1287.
2. Aparicio, O. M., and D. E. Gottschling. 1994. Overcoming telomeric silencing: a trans-activator competes to establish gene expression in a cell cycledependent way. Genes Dev. 8:1133-1146.
3. Bartkova, J., Z. Horejsi, K. Koed, A. Kramer, F. Tort, K. Zieger, P. Guldberg, M. Sehested, J. M. Nesland, C. Lukas, T. Orntoft, J. Lukas, and J. Bartek. 2005. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434:864-870.
4. Baur, J. A., Y. Zou, J. W. Shay, and W. E. Wright. 2001. Telomere position effect in human cells. Science 292:2075-2077.
5. Bennardo, N., A. Cheng, N. Huang, and J. M. Stark. 2008. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 4:e1000110.
6. Blackburn, E. H., C. W. Greider, and J. W. Szostak. 2006. Telomeres and telomerase: the path from maize, Tetrahymena and yeast to human cancer and aging. Nat. Med. 12:1133-1138.
7. Blasco, M. A. 2005. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 6:611-622.
8. Brock, G. J., J. Charlton, and A. Bird. 1999. Densely methylated sequences that are preferentially localized at telomere-proximal regions of human chromosomes. Gene 240:269-277.
9. Clapp, J., D. J. Bolland, and J. E. Hewitt. 2003. Genomic analysis of facioscapulohumeral muscular dystrophy. Brief Funct. Genomic. Proteomic. 2:213-223.
10. Collins, C., J. M. Rommens, D. Kowbel, T. Godfrey, M. Tanner, S.-I. Hwang, D. Polikoff, G. Nonet, J. Cochran, K. Myambo, K. E. Jay, J. Froula, T. Cloutier, W.-L. Kou, P. Yaswen, S. Dairkee, J. Giovanola, G. B. Hutchinson, J. Isola, O.-P. Kallioniemi, M. Palazzolo, C. Martin, C. Ericsson, D. Pinkel, D. Albertson, W.-B. Li, and J. W. Gray. 1998. Positional cloning of ZNF217 and NABC1: Genes amplified at 20q13.2 and overexpressed in breast carcinoma. Proc. Natl. Acad. Sci. U. S. A. 95:8703-8708.
11. Counter, C. M., A. A. Avilion, C. E. LeFeuvre, N. G. Stewart, C. W. Greider, C. B. Harley, and S. Bacchetti. 1992. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 11:1921-1929.
12. de Lange, T. 1995. Telomere dynamics and genome instability in human cancer, p. 265-293. In E. H. Blackburn and C. W. Greider (ed.), Telomeres. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
13. Deng, Y., S. S. Chan, and S. Chang. 2008. Telomere dysfunction and tumour suppression: the senescence connection. Nat. Rev. Cancer 8:450-458.
14. Diede, S. J., and D. E. Gottschling. 1999. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerase α and δ Cell 99:723-733.
15. Ducray, C., J.-P. Pommier, L. Martins, F. Boussin, and L. Sabatier. 1999. Telomere dynamics, end-to-end fusions and telomerase activation during the human fibroblast immortalization process. Oncogene 18:4211-4223.
16. Fisher, J., and M. Upadhyaya. 1997. Molecular genetics of facioscapulohumeral muscular dystrophy (FSHD). Neuromuscul. Disord. 7:55-62.
17. Fouladi, B., D. Miller, L. Sabatier, and J. P. Murnane. 2000. The relationship between spontaneous telomere loss and chromosome instability in a human tumor cell line. Neoplasia 2:540-554.
18. Fourel, G., E. Revardel, C. E. Koering, and E. Gilson. 1999. Cohabitation of insulators and silencing elements in yeast subtelomeric regions. EMBO J. 18:2522-2537.
19. Gao, Q., G. E. Reynolds, A. Wilcox, D. Miller, P. Cheung, S. E. Artandi, and J. P. Murnane. 2008. Telomerase-dependent and -independent chromosome healing in mouse embryonic stem cells. DNA Repair 7:1233-1249.
20. Goodarzi, A. A., A. T. Noon, D. Deckbar, Y. Ziv, Y. Shiloh, M. Lobrich, and P. A. Jeggo. 2008. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 31:167-177.
21. Gorgoulis, V. G., L. V. Vassiliou, P. Karakaidos, P. Zacharatos, A. Kotsinas, T. Liloglou, M. Venere, R. A. Ditullio, Jr., N. G. Kastrinakis, B. Levy, D. Kletsas, A. Yoneta, M. Herlyn, C. Kittas, and T. D. Halazonetis. 2005. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434:907-913.
22. Gottschling, D. E., O. M. Aparicio, B. L. Billington, and V. A. Zakian. 1990. Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63:751-762.
23. Guirouilh-Barbat, J., E. Rass, I. Plo, P. Bertrand, and B. S. Lopez. 2007. Defects in XRCC4 and KU80 differentially affect the joining of distal nonhomologous ends. Proc. Natl. Acad. Sci. U. S. A. 104:20902- 20907.
24. Haarr, L., H. S. Marsden, C. M. Preston, J. R. Smiley, W. C. Summers, and W. P. Summers. 1985. Utilization of internal AUG codons for initiation of protein synthesis directed by mRNAs from normal and mutant genes encoding herpes simplex virus-specified thymidine kinase. J. Virol. 56:512-519.
25. Harley, C. B. 1995. Telomeres and aging, p. 247-263. In E. H. Blackburn and C. W. Greider (ed.), Telomeres. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
26. Harley, C. B., A. B. Futcher, and C. W. Greider. 1990. Telomeres shorten during ageing of human fibroblasts. Nature 345:458-460.
27. Honma, M., M. Sakuraba, T. Koizumi, Y. Takashima, H. Sakamoto, and M. Hayashi. 2007. Non-homologous end-joining for repairing I-SceI-induced DNA double strand breaks in human cells. DNA Repair (Amst.) 6:781-788.
28. Inoue, K., H. Osaka, V. C. Thurston, J. T. Clarke, A. Yoneyama, L. Rosenbarker, T. D. Bird, M. E. Hodes, L. G. Shaffer, and J. R. Lupski. 2002. Genomic rearrangements resulting in PLP1 deletion occur by nonhomologous end joining and cause different dysmyelinating phenotypes in males and females. Am. J. Hum. Genet. 71:838-853.
29. Irmiere, A. F., M. M. Manos, J. G. Jacobson, J. S. Gibbs, and D. M. Coen. 1989. Effect of an amber mutation in the herpes simplex virus thymidine kinase gene on polypeptide synthesis and stability. Virology 168:210-220.
30. Ivessa, A. S., J.-Q. Zhou, V. P. Schulz, E. K. Monson, and V. A. Zakian. 2002. Saccharomyces Rrm3p, a 5' to 3' DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 16:1383-1396.
31. Karlseder, J., K. Hoke, O. K. Mirzoeva, C. Bakkenist, M. B. Kastan, J. H. Petrini, and T. de Lange. 2004. The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol. 2:E240.
32. Koering, C. E., A. Pollice, M. P. Zibella, S. Bauwens, A. Puisieux, M. Brunori, C. Brun, L. Martins, L. Sabatier, J. F. Pulitzer, and E. Gilson. 2002. Human telomeric position effect is determined by chromosomal context and telomeric chromatin integrity. EMBO Rep. 3:1055-1061.
33. Kramer, K. M., and J. E. Haber. 1993. New telomeres in yeast are initiated with a highly selected subset of TG1-3 repeats. Genes Dev. 7:2345-2356.
34. Lin, Y., and A. S. Waldman. 2001. Capture of DNA sequences at doublestrand breaks in mammalian cells. Genetics 158:1665-1674.
35. Little, J. B. 2003. Genomic instability and radiation. J. Radiol. Prot. 23:173-181.
36. Lo, A. W. I., L. Sabatier, B. Fouladi, G. Pottier, M. Ricoul, and J. P. Murnane. 2002. DNA amplification by breakage/fusion/bridge cycles initiated by spontaneous telomere loss in a human cancer cell line. Neoplasia 6:531-538.
37. Lo, A. W. I., C. N. Sprung, B. Fouladi, M. Pedram, L. Sabatier, M. Ricoul, G. E. Reynolds, and J. P. Murnane. 2002. Chromosome instability as a result of double-strand breaks near telomeres in mouse embryonic stem cells. Mol. Cell. Biol. 22:4836-4850.
38. Makovets, S., and E. H. Blackburn. 2009. DNA damage signalling prevents deleterious telomere addition at DNA breaks. Nat. Cell Biol. 11:1383-1386.
39. Mangahas, J. L., M. K. Alexander, L. L. Sandell, and V. A. Zakian. 2001. Repair of chromosome ends after telomere loss in Saccharomyces. Mol. Biol. Cell 12:4078-4089.
40. Michelson, R. J., S. Rosenstein, and T. Weinert. 2005. A telomeric repeat sequence adjacent to a DNA double-stranded break produces an anticheckpoint. Genes Dev. 19:2546-2559.
41. Murnane, J. P. 2006. Telomeres and chromosome instability. DNA Repair (Amst.) 5:1082-1092.
42. Nussenzweig, A., and M. C. Nussenzweig. 2007. A backup DNA repair pathway moves to the forefront. Cell 131:223-225.
43. O'Toole, C. M., S. Povey, P. Hepburn, and L. M. Franks. 1983. Identity of some human bladder cancer cell lines. Nature 301:429-430.
44. Pedram, M., C. N. Sprung, Q. Gao, A. W. I. Lo, G. Reynolds, and J. P. Murnane. 2006. Telomere position effect and silencing of transgenes near telomeres in the mouse. Mol. Cell. Biol. 26:1865-1878.
45. Pennaneach, V., C. D. Putnam, and R. D. Kolodner. 2006. Chromosome healing by de novo telomere addition in Saccharomyces cerevisiae. Mol. Microbiol. 59:1357-1368.
46. Pryde, F. E., and E. J. Louis. 1999. Limitations of silencing at native yeast telomeres. EMBO J. 18:2538-2550.
47. Rebuzzini, P., L. Khoriauli, C. M. Azzalin, E. Magnani, C. Mondello, and E. Giulotto. 2005. New mammalian cellular systems to study mutations introduced at the break site by non-homologous end-joining. DNA Repair (Amst.) 4:546-555.
48. Renauld, H., O. M. Aparicio, P. D. Zierath, B. L. Billington, S. K. Chhablani, and D. E. Gottschling. 1993. Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage. Genes Dev. 7:1133-1145.
49. Ricchetti, M., B. Dujon, and C. Fairhead. 2003. Distance from the chromosome end determines the efficiency of double-strand break repair in subtelomeres of haploid yeast. J. Mol. Biol. 328:847-862.
50. Richardson, C., M. E. Moynahan, and M. Jasin. 1998. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev. 12:3831-3842.
51. Sabatier, L., M. Ricoul, G. Pottier, and J. P. Murnane. 2005. The loss of a single telomere can result in genomic instability involving multiple chromosomes in a human tumor cell line. Mol. Cancer Res. 3:139-150.
52. Sargent, R. G., M. A. Brenneman, and J. H. Wilson. 1997. Repair of sitespecific double-strand breaks in a mammalian chromosome by homologous and illegitimate recombination. Mol. Cell. Biol. 17:267-277.
53. Sauer, B., and N. Henderson. 1990. Targeted insertion of exogenous DNA into the eukaryotic genome by the Cre recombinase. New Biol. 2:441-449.
54. Schulz, V. P., and V. A. Zakian. 1994. The Saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell 76:145-155.
55. Sfeir, A., S. T. Kosiyatrakul, D. Hockemeyer, S. L. MacRae, J. Karlseder, C. L. Schildkraut, and T. de Lange. 2009. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138:90-103.
56. Sprung, C. N., G. E. Reynolds, M. Jasin, and J. P. Murnane. 1999. Chromosome healing in mouse embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 96:6781-6786.
57. Tham, W. H., and V. A. Zakian. 2002. Transcriptional silencing at Saccharomyces telomeres: implications for other organisms. Oncogene 21:512-521.
58. van der Weyden, L., D. J. Adams, and A. Bradley. 2002. Tools for targeted manipulation of the mouse genome. Physiol. Genomics 11:133-164.
59. Van Deursen, J., M. Fornerod, B. Van Rees, and G. Grosveld. 1995. Cremediated site-specific translocation between nonhomologous mouse chromosomes. Proc. Natl. Acad. Sci. U. S. A. 92:7376-7380.
60. van Geel, M., M. C. Dickson, A. F. Beck, D. J. Bolland, R. R. Frants, S. M. van der Maarel, P. J. de Jong, and J. E. Hewitt. 2002. Genomic analysis of human chromosome 10q and 4q telomeres suggests a common origin. Genomics 79:210-217.
61. van Karnebeek, C. D., S. Quik, S. Sluijter, M. M. Hulsbeek, J. M. Hoovers, and R. C. Hennekam. 2002. Further delineation of the chromosome 14q terminal deletion syndrome. Am. J. Med. Genet. 110:65-72.
62. Varga, T., and P. D. Aplan. 2005. Chromosomal aberrations induced by double strand DNA breaks. DNA Repair (Amst.) 4:1038-1046.
63. Weinstock, D. M., E. Brunet, and M. Jasin. 2007. Formation of NHEJderived reciprocal chromosomal translocations does not require Ku70. Nat. Cell Biol. 9:978-981.
64. Xie, A., A. Kwok, and R. Scully. 2009. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol. 16:814-818.
65. Zhou, J.-Q., E. K. Monson, S.-C. Teng, V. P. Schultz, and V. A. Zakian. 2000. Pif1p helicase, a catalytic inhibitor of telomerase in yeast. Science 289:771-774.
66. Zierhut, C., and J. F. Diffley. 2008. Break dosage, cell cycle stage and DNA replication influence DNA double strand break response. EMBO J. 27:1875-1885.
67. Zschenker, O., A. Kulkarni, D. Miller, G. E. Reynolds, M. Granger-Locatelli, G. Pottier, L. Sabatier, and J. P. Murnane. 2009. Increased sensitivity of subtelomeric regions to DNA double-strand breaks in a human tumor cell line. DNA Repair 8:886-900.