Ku70 prevents genome instability resulting from heterozygosity of the telomerase RNA component in a vertebrate tumour line

DNA Repair

Volumn 7, Issue 5, 2008, Pages 713-724

  Faure, Virginie ^a   Wenner, Thomas ^a   Cooley, Carol ^a   Bourke, Emer ^a   Farr, Christine J ^b   Takeda, Shunichi ^c   Morrison, Ciaran G ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

DNA double strand break repair; Gene targeting; Homologous recombination; Nonhomologous end joining; Telomerase; Telomere

Indexed keywords

KU ANTIGEN; RAD54 PROTEIN; RNA; TELOMERASE; TELOMERASE REVERSE TRANSCRIPTASE;

ALLELE; ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CHROMOSOME; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; GENE DELETION; GENE DISRUPTION; GENE TARGETING; GENOMIC INSTABILITY; HETEROZYGOSITY; HOMOLOGOUS RECOMBINATION; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN INTERACTION; RNA SEQUENCE; TELOMERE; VERTEBRATE;

ANIMALS; ANTIGENS, NUCLEAR; CELL LINE, TUMOR; CELL PROLIFERATION; CHICKENS; CHROMOSOME ABERRATIONS; DNA DAMAGE; DNA-BINDING PROTEINS; GENOMIC INSTABILITY; HETEROZYGOTE; RNA; TELOMERASE; TELOMERE; TELOMERE-BINDING PROTEINS;

VERTEBRATA;

EID: 42249098413     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.01.008     Document Type: Article

References (50)

1. Autexier C., and Lue N.F. The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75 (2006) 493-517
2. 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. Specific association of human telomerase activity with immortal cells and cancer. Science 266 (1994) 2011-2015
3. Bryan T.M., Englezou A., Gupta J., Bacchetti S., and Reddel R.R. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J. 14 (1995) 4240-4248
4. 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 (1999) 503-514
5. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19 (2005) 2100-2110
6. Blackburn E.H. Switching and signaling at the telomere. Cell 106 (2001) 661-673
7. Celli G.B., Denchi E.L., and de Lange T. Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination. Nat. Cell. Biol. 8 (2006) 885-890
8. Celli G.B., and de Lange T. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell. Biol. 7 (2005) 712-718
9. Takai H., Smogorzewska A., and de Lange T. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13 (2003) 1549-1556
10. van Steensel B., Smogorzewska A., and de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell 92 (1998) 401-413
11. Verdun R.E., and Karlseder J. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127 (2006) 709-720
12. d'Adda di Fagagna F., Teo S.H., and Jackson S.P. Functional links between telomeres and proteins of the DNA-damage response. Genes Dev. 18 (2004) 1781-1799
13. Sonoda E., Hochegger H., Saberi A., Taniguchi Y., and Takeda S. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst) 5 (2006) 1021-1029
14. d'Adda di Fagagna F., Hande M.P., Tong W.M., Roth D., Lansdorp P.M., Wang Z.Q., and Jackson S.P. Effects of DNA nonhomologous end-joining factors on telomere length and chromosomal stability in mammalian cells. Curr. Biol. 11 (2001) 1192-1196
15. Bianchi A., and de Lange T. Ku binds telomeric DNA in vitro. J. Biol. Chem. 274 (1999) 21223-21227
16. Hsu H.L., Gilley D., Blackburn E.H., and Chen D.J. Ku is associated with the telomere in mammals. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 12454-12458
17. 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 (2000) 2807-2812
18. Myung K., Ghosh G., Fattah F.J., Li G., Kim H., Dutia A., Pak E., Smith S., and Hendrickson E.A. Regulation of telomere length and suppression of genomic instability in human somatic cells by Ku86. Mol. Cell. Biol. 24 (2004) 5050-5059
19. 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. U.S.A. 96 (1999) 14899-14904
20. Espejel S., Franco S., Rodriguez-Perales S., Bouffler S.D., Cigudosa J.C., and Blasco M.A. Mammalian Ku86 mediates chromosomal fusions and apoptosis caused by critically short telomeres. EMBO J. 21 (2002) 2207-2219
21. Samper E., Goytisolo F.A., Slijepcevic P., van Buul P.P., and Blasco M.A. Mammalian Ku86 protein prevents telomeric fusions independently of the length of TTAGGG repeats and the G-strand overhang. EMBO Rep. 1 (2000) 244-252
22. Blasco M.A. Telomeres and human disease: ageing, cancer and beyond. Nat. Rev. Genet. 6 (2005) 611-622
23. Niida H., Matsumoto T., Satoh H., Shiwa M., Tokutake Y., Furuichi Y., and Shinkai Y. Severe growth defect in mouse cells lacking the telomerase RNA component. Nat. Genet. 19 (1998) 203-206
24. Liu Y., Snow B.E., Hande M.P., Yeung D., Erdmann N.J., Wakeham A., Itie A., Siderovski D.P., Lansdorp P.M., Robinson M.O., and Harrington L. The telomerase reverse transcriptase is limiting and necessary for telomerase function in vivo. Curr. Biol. 10 (2000) 1459-1462
25. Liu Y., Kha H., Ungrin M., Robinson M.O., and Harrington L. Preferential maintenance of critically short telomeres in mammalian cells heterozygous for mTert. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 3597-3602
26. Hathcock K.S., Hemann M.T., Opperman K.K., Strong M.A., Greider C.W., and Hodes R.J. Haploinsufficiency of mTR results in defects in telomere elongation. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 3591-3596
27. Chiang Y.J., Hemann M.T., Hathcock K.S., Tessarollo L., Feigenbaum L., Hahn W.C., and Hodes R.J. Expression of telomerase RNA template, but not telomerase reverse transcriptase, is limiting for telomere length maintenance in vivo. Mol. Cell. Biol. 24 (2004) 7024-7031
28. Goldman F., Bouarich R., Kulkarni S., Freeman S., Du H.Y., Harrington L., Mason P.J., Londono-Vallejo A., and Bessler M. The effect of TERC haploinsufficiency on the inheritance of telomere length. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 17119-17124
29. Shay J.W., and Wright W.E. Telomerase therapeutics for cancer: challenges and new directions. Nat. Rev. Drug Discov. 5 (2006) 577-584
30. Chen J.L., Blasco M.A., and Greider C.W. Secondary structure of vertebrate telomerase RNA. Cell 100 (2000) 503-514
31. Takata M., Sasaki M.S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., and Takeda S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17 (1998) 5497-5508
32. Dodson H., Bourke E., Jeffers L.J., Vagnarelli P., Sonoda E., Takeda S., Earnshaw W.C., Merdes A., and Morrison C. Centrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM. EMBO J. 23 (2004) 3864-3873
33. Gallant P., and Nigg E.A. Cyclin B2 undergoes cell cycle-dependent nuclear translocation and, when expressed as a non-destructible mutant, causes mitotic arrest in HeLa cells. J. Cell. Biol. 117 (1992) 213-224
34. Kaminker P., Plachot C., Kim S.H., Chung P., Crippen D., Petersen O.W., Bissell M.J., Campisi J., and Lelievre S.A. Higher-order nuclear organization in growth arrest of human mammary epithelial cells: a novel role for telomere-associated protein TIN2. J. Cell. Sci. 118 (2005) 1321-1330
35. Kim N.W., and Wu F. Advances in quantification and characterization of telomerase activity by the telomeric repeat amplification protocol (TRAP). Nucleic Acids Res. 25 (1997) 2595-2597
36. Dionne I., and Wellinger R.J. Cell cycle-regulated generation of single-stranded G-rich DNA in the absence of telomerase. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 13902-13907
37. Wellinger R.J., Wolf A.J., and Zakian V.A. Structural and temporal analysis of telomere replication in yeast. Cold Spring Harb. Symp. Quant. Biol. 58 (1993) 725-732
38. Wei C., Skopp R., Takata M., Takeda S., and Price C.M. Effects of double-strand break repair proteins on vertebrate telomere structure. Nucleic Acids Res. 30 (2002) 2862-2870
39. Buerstedde J.-M., and Takeda S. Increased ration of targeted to random integration after transfection of chicken B cell lines. Cell 67 (1991) 179-188
40. Swanberg S.E., Payne W.S., Hunt H.D., Dodgson J.B., and Delany M.E. Telomerase activity and differential expression of telomerase genes and c-myc in chicken cells in vitro. Dev. Dyn. 231 (2004) 14-21
41. Bezzubova O., Silbergleit A., Yamaguchi-Iwai Y., Takeda S., and Buerstedde J.M. Reduced X-ray resistance and homologous recombination frequencies in a RAD54-/- mutant of the chicken DT40 cell line. Cell 89 (1997) 185-193
42. Sancar A., Lindsey-Boltz L.A., Unsal-Kacmaz K., and Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73 (2004) 39-85
43. Niida H., Shinkai Y., Hande M.P., Matsumoto T., Takehara S., Tachibana M., Oshimura M., Lansdorp P.M., and Furuichi Y. Telomere maintenance in telomerase-deficient mouse embryonic stem cells: characterization of an amplified telomeric DNA. Mol. Cell. Biol. 20 (2000) 4115-4127
44. Akiyama K., Yusa K., Hashimoto H., Poonepalli A., Hande M.P., Kakazu N., Takeda J., Tachibana M., and Shinkai Y. Rad54 is dispensable for the ALT pathway. Genes Cells 11 (2006) 1305-1315
45. Hande M.P., Samper E., Lansdorp P., and Blasco M.A. Telomere length dynamics and chromosomal instability in cells derived from telomerase null mice. J. Cell. Biol. 144 (1999) 589-601
46. Blasco M.A., Lee H.W., Hande M.P., Samper E., Lansdorp P.M., DePinho R.A., and Greider C.W. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91 (1997) 25-34
47. Hockemeyer D., Sfeir A.J., Shay J.W., Wright W.E., and de Lange T. POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end. EMBO J. 24 (2005) 2667-2678
48. Churikov D., Wei C., and Price C.M. Vertebrate POT1 restricts G-overhang length and prevents activation of a telomeric DNA damage checkpoint but is dispensable for overhang protection. Mol. Cell. Biol. 26 (2006) 6971-6982
49. Wang R.C., Smogorzewska A., and de Lange T. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119 (2004) 355-368
50. Ting N.S., Yu Y., Pohorelic B., Lees-Miller S.P., and Beattie T.L. Human Ku70/80 interacts directly with hTR, the RNA component of human telomerase. Nucleic Acids Res. 33 (2005) 2090-2098