Regulation of telomere length and suppression of genomic instability in human somatic cells by Ku86

Molecular and Cellular Biology

Volumn 24, Issue 11, 2004, Pages 5050-5059

  Myung, Kyungjae ^a   Ghosh, Goutam ^b   Fattah, Farjana J ^b   Li, Gang ^b,c   Kim, Haeyoung ^b   Dutia, Amalia ^a   Pak, Evgenia ^a   Smith, Stephanie ^a   Hendrickson, Eric A ^b  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; DNA DEPENDENT PROTEIN KINASE; KU ANTIGEN; KU86 PROTEIN; UNCLASSIFIED DRUG;

ANEUPLOIDY; ARTICLE; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE MUTATION; GENOME; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SOMATIC CELL; TELOMERE; TISSUE CULTURE;

ANTIGENS, NUCLEAR; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GENOMIC INSTABILITY; HETEROZYGOTE; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; KARYOTYPING; TELOMERE;

EUKARYOTA; GALLUS GALLUS; SACCHAROMYCETALES; SCHIZOSACCHAROMYCES POMBE;

EID: 2442688032     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.11.5050-5059.2004     Document Type: Article

References (84)

1. Abdel-Rahman, W. M., K. Katsura, W. Rens, P. A. Gorman, D. Sheer, D. Bicknell, W. F. Bodmer, M. J. Arends, A. H. Wyllie, and P. A. Edwards. 2001. Spectral karyotyping suggests additional subsets of colorectal cancers characterized by pattern of chromosome rearrangement. Proc. Natl. Acad. Sci. USA 98:2538-2543.
2. Bailey, S. M., J. Meyne, D. J. Chen, A. Kurimasa, G. C. Li, B. E. Lehnert, and E. H. Goodwin. 1999. DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc. Natl. Acad. Sci. USA 96:14899-14904.
3. Baumann, P., and T. R. Cech. 2001. Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292:1171-1175.
4. Baumann, P., and T. R. Cech. 2000. Protection of telomeres by the Ku protein in fission yeast. Mol. Biol. Cell 11:3265-3275.
5. Bayani, J. M., and J. A. Squire. 2002. Applications of SKY in cancer cytogenetics. Cancer Investig. 20:373-386.
6. Bertuch, A. A., and V. Lundblad. 2003. The Ku heterodimer performs separable activities at double-strand breaks and chromosome termini. Mol. Cell. Biol. 23:8202-8215.
7. Blackburn, E. H. 2001. Switching and signaling at the telomere. Cell 106: 661-673.
8. Blasco, M. A., W. Funk, B. Villeponteau, and C. W. Greider. 1995. Functional characterization and developmental regulation of mouse telomerase RNA. Science 269:1267-1270.
9. Blasco, M. A., H. W. Lee, M. P. Hande, E. Samper, P. M. Lansdorp, R. A. DePinho, and C. W. Greider. 1997. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91:25-34.
10. Bogue, M., C. Jhappan, and D. B. Roth. 1998. Analysis of variable (diversity) joining recombination in DNA-dependent protein kinase (DNA-PK)-deficient mice reveals DNA-PK-independent pathways for both signal and coding joint formation. Proc. Natl. Acad. Sci. USA 95:15559-15564.
11. Boulton, S. J., and S. P. Jackson. 1998. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17:1819-1828.
12. Broccoli, D., A. Smogorzewska, L. Chong, and T. de Lange. 1997. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet. 17:231-235.
13. 2 arrest after DNA damage. Science 282:1497-1501.
14. Bunz, F., C. Fauth, M. R. Speicher, A. Dutriaux, J. M. Sedivy, K. W. Kinzler, B. Vogelstein, and C. Lengauer. 2002. Targeted inactivation of p53 in human cells does not result in aneuploidy. Cancer Res. 62:1129-1133.
15. Carr, A. M. 2002. Checking that replication breakdown is not terminal. Science 297:557-558.
16. Chai, W., L. P. Ford, L. Lenertz, W. E. Wright, and J. W. Shay. 2002. Human Ku70/80 associates physically with telomerase through interaction with hTERT. J. Biol. Chem. 277:47242-47247.
17. Chan, S. W., and E. H. Blackburn. 2002. New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21:553-563.
18. Chong, L., B. van Steensel, D. Broccoli, H. Erdjument-Bromage, J. Hanish, P. Tempst, and T. de Lange. 1995. A human telomeric protein. Science 270:1663-1667.
19. Conway, C., R. McCulloch, M. L. Ginger, N. P. Robinson, A. Browitt, and J. D. Barry. 2002. Ku is important for telomere maintenance, but not for differential expression of telomeric VSG genes, in African trypanosomes. J. Biol. Chem. 277:21269-21277.
20. d'Adda di Fagagna, F., M. P. Hande, W.-M. Tong, D. B. Roth, P. M. Lansdorp, Z.-Q. Wang, and S. P. Jackson. 2001. Effects of DNA nonhomologous end-joining factors on telomere length and chromosomal stability in mammalian cells. Curr. Biol. 11:1192-1196.
21. d'Adda di Fagagna, F., G. R. Weller, A. J. Doherty, and S. P. Jackson. 2003. The Gam protein of bacteriophage Mu is an orthologue of eukaryotic Ku. EMBO Rep. 4:47-52.
22. Dai, Y., B. Kysela, L. A. Hanakahi, K. Manolis, E. Riballo, M. Stumm, T. O. Harville, S. C. West, M. A. Oettinger, and P. A. Jeggo. 2003. Nonhomologous end joining and V(D)J recombination require an additional factor. Proc. Natl. Acad. Sci. USA 100:2462-2467.
23. de Lange, T. 2001. Cell biology. Telomere capping-one strand fits all. Science 292:1075-1076.
24. de Lange, T. 2002. Protection of mammalian telomeres. Oncogene 21:532-540.
25. Difilippantonio, M. J., J. Zhu, H. T. Chen, E. Meffre, M. C. Nussenzweig, E. E. Max, T. Ried, and A. Nussenzweig. 2000. DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature 404:510-514.
26. Driller, L., R. J. Wellinger, M. Larrivee, E. Kremmer, S. Jaklin, and H. M. Feldmann. 2000. A short C-terminal domain of Yku70p is essential for telomere maintenance. J. Biol. Chem. 275:24921-24927.
27. Espejel, S., S. Franco, S. Rodriguez-Perales, S. D. Bouffler, J. C. Cigudosa, and M. A. Blasco. 2002. Mammalian Ku86 mediates chromosomal fusions and apoptosis caused by critically short telomeres. EMBO J. 21:2207-2219.
28. cs and telomerase in telomere length maintenance. EMBO J. 21:6275-6287.
29. Fellerhoff, B., F. Eckardt-Schupp, and A. A. Friedl. 2000. Subtelomeric repeat amplification is associated with growth at elevated temperature in yku70 mutants of Saccharomyces cerevisiae. Genetics 154:1039-1051.
30. cs-null mutation reveals DNA-PK-independent functions for Ku in V(D)J recombination. Immunity 9:367-376.
31. cs is critical for telomere capping. Proc. Natl. Acad. Sci. USA 98:15084-15088.
32. Goytisolo, F. A., E. Samper, S. Edmonson, G. E. Taccioli, and M. A. Blasco. 2001. The absence of the DNA-dependent protein kinase catalytic subunit in mice results in anaphase bridges and in increased telomeric fusions with normal telomere length and G-strand overhang. Mol. Cell. Biol. 21:3642-3651.
33. Gravel, S., M. Larrivee, P. Labrecque, and R. J. Wellinger. 1998. Yeast Ku as a regulator of chromosomal DNA end structure. Science 280:741-744.
34. Gravel, S., and R. J. Wellinger. 2002. Maintenance of double-stranded telomeric repeats as the critical determinant for cell viability in yeast cells lacking Ku. Mol. Cell. Biol. 22:2182-2193.
35. Greider, C. W., and E. H. Blackburn. 1985. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43:405-413.
36. Hande, P., P. Slijepcevic, A. Silver, S. Bouffler, P. van Buul, P. Bryant, and P. Lansdorp. 1999. Elongated telomeres in scid mice. Genomics 56:221-223.
37. Hemann, M. T., M. A. Strong, L. Y. Hao, and C. W. Grelder. 2001. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107:67-77.
38. Hoeijmakers, J. H. 2001. Genome maintenance mechanisms for preventing cancer. Nature 411:366-374.
39. Hopfner, K. P., C. D. Putnam, and J. A. Tainer. 2002. DNA double-strand break repair from head to tail. Curr. Opin. Struct. Biol. 12:115-122.
40. Hsu, H. L., D. Gilley, S. A. Galande, M. P. Hande, B. Allen, S. H. Kim, G. C. Li, J. Campisi, T. Kohwi-Shigematsu, and D. J. Chen. 2000. Ku acts in a unique way at the mammalian telomere to prevent end joining. Genes Dev. 14:2807-2812.
41. Jackson, S. P. 2002. Sensing and repairing DNA double-strand breaks. Carcinogenesis 23:687-696.
42. Jacob, N. K., K. E. Kirk, and C. M. Price. 2003. Generation of telomeric G strand overhangs involves both G and C strand cleavage. Mol. Cell 11:1021-1032.
43. Jhappan, C., H. C. Morse, R. D. Fleischmann, M. M. Gottesman, and G. Merlino. 1997. DNA-PKcs: a T-cell tumor suppressor encoded at the mouse scid locus. Nat. Genet. 17:483-486.
44. Karanjawala, Z. E., U. Grawunder, C. L. Hsieh, and M. R. Lieber. 1999. The nonhomologous DNA end joining pathway is important for chromosome stability in primary fibroblasts. Curr. Biol. 9:1501-1504.
45. Karlseder, J., A. Smogorzewska, and T. de Lange. 2002. Senescence induced by altered telomere state, not telomere loss. Science 295:2446-2449.
46. Kolodner, R. D., C. D. Putnam, and K. Myung. 2002. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297:552-557.
47. Leri, A., S. Franco, A. Zacheo, L. Barlucchi, S. Chimenti, F. Limana, B. Nadal-Ginard, J. Kajstura, P. Anversa, and M. A. Blasco. 2003. Ablation of telomerase and telomere loss leads to cardiac dilatation and heart failure associated with p53 upregulation. EMBO J. 22:131-139.
48. Li, G., C. Nelsen, and E. A. Hendrickson. 2002. Ku86 is essential in human somatic cells. Proc. Natl. Acad. Sci. USA 99:832-837.
49. Li, G. C., H. Ouyang, X. Li, H. Nagasawa, J. B. Little, D. J. Chen, C. C. Ling, Z. Fuks, and C. Cordon-Cardo. 1998. Ku70: a candidate tumor suppressor gene for murine T cell lymphoma. Mol. Cell 2:1-8.
50. Lieber, M. R., Y. Ma, U. Pannicke, and K. Scharz. 2003. Mechanism and regulation of human non-homologous DNA end-joining. Nat. Mol. Cell. Biol. Rev. 4:712-720.
51. Loeb, L. A., K. R. Loeb, and J. P. Anderson. 2003. Multiple mutations and cancer. Proc. Natl. Acad. Sci. USA 100:776-781.
52. Manolis, K. G., E. R. Nimmo, E. Hartsuiker, A. M. Carr, P. A. Jeggo, and R. C. Allshire. 2001. Novel functional requirements for non-homologous DNA end joining in Schizosaccharomyces pombe. EMBO J. 20:210-221.
53. Marx, J. 2002. Debate surges over the origins of genomic defects in cancer. Science 297:544-546.
54. Maser, R. S., and R. A. DePinho. 2002. Connecting chromosomes, crisis, and cancer. Science 297:565-569.
55. Mason, P. J. 2003. Stem cells, telomerase and dyskeratosis congenita. Bioessays 25:126-133.
56. Masramon, L., M. Ribas, P. Cifuentes, R. Arribas, F. Garcia, J. Egozcue, M. A. Peinado, and R. Miro. 2000. Cytogenetic characterization of two colon cell lines by using conventional G-banding, comparative genomic hybridization, and whole chromosome painting. Cancer Genet. Cytogenet. 121:17-21.
57. McElligott, R., and R. J. Wellinger. 1997. The terminal DNA structure of mammalian chromosomes. EMBO J. 16:3705-3714.
58. Mitchell, J. R., E. Wood, and K. Collins. 1999. A telomerase component is defective in the human disease dyskeratosis congenita. Nature 402:551-555.
59. Nussenzweig, A., C. Chen, V. da Costa Soares, M. Sanchez, K. Sokol, M. C. Nussenzweig, and G. C. Li. 1996. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382:551-555.
60. Nussenzweig, A., K. Sokol, P. Burgnian, L. Li, and G. C. Li. 1997. Hyper-sensitivity of Ku80-deficient cell lines and mice to DNA damage: the effects of ionizing radiation on growth, survival and development. Proc. Natl. Acad. Sci. USA 94:13588-13593.
61. Ouyang, H., A. Nussenzweig, A. Kurimasa, V. C. Soares, X. Li, C. Cordon-Cardo, W. H. Li, N. Cheong, M. Nussenzweig, G. Iliakis, D. Chen, and G. Li. 1997. Ku70 is required for DNA repair but not for T cell antigen receptor gene recombination In vivo. J. Exp. Med. 15:921-929.
62. Peterson, S. E., A. E. Stellwagen, S. J. Diede, M. S. Singer, Z. W. Haimberger, C. O. Johnson, M. Tzoneva, and D. E. Gottschling. 2001. The function of a stem-loop in telomerase RNA is linked to the DNA repair protein Ku. Nat. Genet. 27:64-67.
63. Polotnianka, R. M., J. Li, and A. J. Lustig. 1998. The yeast Ku heterodimer is essential for protection of the telomere against nucleolytic and recombinational activities. Curr. Biol. 8:831-834.
64. Riha, K., and D. E. Shippen. 2003. Ku is required for telomeric C-rich strand maintenance but not for end-to-end chromosome fusions in Arabidopsis. Proc. Natl. Acad. Sci. USA 100:611-615.
65. Riha, K., J. M. Watson, J. Parkey, and D. E. Shippen. 2002. Telomere length deregulation and enhanced sensitivity to genotoxic stress in Arabidopsis mutants deficient in Ku70. EMBO J. 21:2819-2826.
66. Romanov, S. R., B. K. Kozakiewicz, C. R. Holst, M. R. Stampfer, L. M. Haupt, and T. D. Tlsty. 2001. Normal human mammary epithelial cells spontaneously escape senescence and acquire genomic changes. Nature 409: 633-637.
67. Samper, E., F. A. Goytisolo, P. Slijepcevic, P. P. W. van Buul, and M. A. Blasco. 2000. Mammalian Ku86 protein prevents telomeric fusions independently of the length of TTAGGG repeats and the G-strand overhang. EMBO Rep. 1:244-252.
68. Schar, P. 2001. Spontaneous DNA damage, genome instability, and cancer-when DNA replication escapes control. Cell 104:329-332.
69. Slijepcevic, P., M. P. Hande, S. D. Bouffier, P. Lansdorp, and P. E. Bryant. 1997. Telomere length, chromatin structure and chromosome fusigenic potential. Chromosoma 106:413-421.
70. Smogorzewska, A., B. van Steensel, A. Bianchi, S. Oelmann, M. R. Schaefer, G. Schnapp, and T. de Lange. 2000. Control of human telomere length by TRF1 and TRF2. Mol. Cell. Biol. 20:1659-1668.
71. Song, K., D. Jung, Y. Jung, S. G. Lee, and I. Lee. 2000. Interaction of human Ku70 with TRF2. FEBS Lett. 481:81-85.
72. Stellwagen, A. E., Z. W. Haimberger, J. R. Veatch, and D. E. Gottschling. 2003. Ku interacts with telomerase RNA to promote telomere addition at native and broken chromosome ends. Genes Dev. 17:2384-2395.
73. Taccioli, G. E., A. G. Amatucci, H. J. Beamish, D. Gell, X. H. Xiang, M. I. Torres Arzayus, A. Priestley, S. P. Jackson, A. M. Rothstein, P. A. Jeggo, and V. L. M. Herrera. 1998. Targeted disruption of the catalytic subunit of the DNA-PK gene in mice confers severe combined immunodeficiency and radiosensitivity. Immunity 9:355-366.
74. Teo, S. H., and S. P. Jackson. 2001. Telomerase subunit overexpression suppresses telomere-specific checkpoint activation in the yeast yku80 mutant. EMBO Rep. 2:197-202.
75. Tuteja, R., and N. Tuteja. 2000. Ku autoantigen: a multifunctional DNA-binding protein. Crit. Rev. Biochem. Mol. Biol. 35:1-33.
76. van Steensel, B., and T. de Lange. 1997. Control of telomere length by the human telomeric protein TRF1. Nature 385:740-743.
77. van Steensel, B., A. Smogorzewska, and T. de Lange. 1998. TRF2 protects human telomeres from end-to-end fusions. Cell 92:401-413.
78. Venkitaraman, A. R. 2002. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108:171-182.
79. Vogel, H., D.-S. Lim, G. Karsenty, M. Finegold, and P. Hasty. 1999. Deletion of Ku86 causes early onset of senescence in mice. Proc. Natl. Acad. Sci. USA 96:10770-10775.
80. Vulliamy, T., A. Marrone, F. Goldman, A. Dearlove, M. Bessler, P. J. Mason, and I. Dokal. 2001. The RNA component of telomerase is mutated in autosomal dominant dyskeratosis congenita. Nature 413:432-435.
81. Wei, C., R. Skopp, M. Takata, S. Takeda, and C. M. Price. 2002. Effects of double-strand break repair proteins on vertebrate telomere structure. Nucleic Acids Res. 30:2862-2870.
82. Weller, G. R., B. Kysela, R. Roy, L. M. Tonkin, E. Scanlan, M. Della, S. K. Devine, J. P. Day, A. Wilkinson, F. di Fagagna, K. M. Devine, R. P. Bowater, P. A. Jeggo, S. P. Jackson, and A. J. Doherty. 2002. Identification of a DNA nonhomologous end-joining complex in bacteria. Science 297:1686-1689.
83. Zhang, X., V. Mar, W. Zhou, L. Harrington, and M. O. Robinson. 1999. Telomere shortening and apoptosis in telomerase-inhibited human tumor cells. Genes Dev. 13:2388-2399.
84. Zhu, C., M. A. Bogue, D.-S. Lim, P. Hasty, and D. B. Roth. 1996. Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell 86:379-389.