MRE11-RAD50-NBS1 and ATM function as co-mediators of TRF1 in telomere length control

Nature Structural and Molecular Biology

Volumn 14, Issue 9, 2007, Pages 832-840

  Wu, Yili ^a   Xiao, Shujie ^a   Zhu, Xu Dong ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; DIMETHYL SULFOXIDE; ENZYME INHIBITOR; KU 55933; MRE11 PROTEIN; MUTANT PROTEIN; NIBRIN; RAD50 PROTEIN; TELOMERASE; TELOMERIC REPEAT BINDING FACTOR 1; UNCLASSIFIED DRUG;

ARTICLE; ATAXIA TELANGIECTASIA; COMPLEX FORMATION; DOWN REGULATION; ENZYME INHIBITION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; NIJMEGEN BREAKAGE SYNDROME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN TARGETING; TELOMERE; UPREGULATION; WILD TYPE; YEAST;

CELL CYCLE PROTEINS; CELL LINE; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; HUMANS; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 1; TUMOR SUPPRESSOR PROTEINS;

EID: 34548492016     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1286     Document Type: Article

References (60)

1. de Lange, T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19, 2100-2110 (2005).
2. van Steensel, B., Smogorzewska, A. & de Lange, T. TRF2 protects human telomeres from end-to-end fusions. Cell 92, 401-413 (1998).
3. van Steensel, B. & de Lange, T. Control of telomere length by the human telomeric protein TRF1. Nature 385, 740-743 (1997).
4. Ancelin, K. et al. Targeting assay to study the cis functions of human telomeric proteins: evidence for inhibition of telomerase by TRF1 and for activation of telomere degradation by TRF2. Mol. Cell. Biol. 22, 3474-3487 (2002).
5. Chong, L. et al. A human telomeric protein. Science 270, 1663-1667 (1995).
6. Cooper, J.P., Nimmo, E.R., Allshire, R.C. & Cech, T.R. Regulation of telomere length and function by a Myb-domain protein in fission yeast. Nature 385, 744-747 (1997).
7. Marcand, S., Gilson, E. & Shore, D. A protein-counting mechanism for telomere length regulation in yeast. Science 275, 986-990 (1997).
8. Verdun, R.E., Crabbe, L., Haggblom, C. & Karlseder, J. Functional human telomeres are recognized as DNA damage in G2 of the cell cycle. Mol. Cell 20, 551-561 (2005).
9. Verdun, R.E. & Karlseder, J. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell 127, 709-720 (2006).
10. Zhu, X.D., Kuster, B., Mann, M., Petrini, J.H. & Lange, T. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25, 347-352 (2000).
11. Xiao, Y. & Weaver, D.T. Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Res. 25, 2985-2991 (1997).
12. Luo, G. et al. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl. Acad. Sci. USA 96, 7376-7381 (1999).
13. Zhu, J., Petersen, S., Tessarollo, L. & Nussenzweig, A. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol. 11, 105-109 (2001).
14. Stewart, G.S. et al. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99, 577-587 (1999).
15. Varon, R. et al. Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell 93, 467-476 (1998).
16. Carney, J.P. et al. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93, 477-486 (1998).
17. Savitsky, K. et al. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268, 1749-1753 (1995).
18. D'Amours, D. & Jackson, S.P. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3, 317-327 (2002).
19. Haber, J.E. The many interfaces of Mre11. Cell 95, 583-586 (1998).
20. de Lange, T. & Petrini, J. A new connection at human telomeres: association of the Mre11 complex with TRF2. Cold Spring Harb. Symp. Quant. Biol. 65, 265-273 (2000).
21. Nugent, C.I. et al. Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr. Biol. 8, 657-660 (1998).
22. Tsukamoto, Y., Taggart, A.K. & Zakian, V.A. The role of the Mre11-Rad50-Xrs2 complex in telomerase- mediated lengthening of Saccharomyces cerevisiae telomeres. Curr. Biol. 11, 1328-1335 (2001).
23. Ritchie, K.B. & Petes, T.D. The Mre11p/Rad50p/Xrs2p complex and the Tel1p function in a single pathway for telomere maintenance in yeast. Genetics 155, 475-479 (2000).
24. Metcalfe, J.A. et al. Accelerated telomere shortening in ataxia telangiectasia. Nat. Genet. 13, 350-353 (1996).
25. Ranganathan, V. et al. Rescue of a telomere length defect of Nijmegen breakage syndrome cells requires NBS and telomerase catalytic subunit. Curr. Biol. 11, 962-966 (2001).
26. Kishi, S. et al. Telomeric protein Pin2/TRF1 as an important ATM target in response to double strand DNA breaks. J. Biol. Chem. 276, 29282-29291 (2001).
27. Wu, G., Lee, W.H. & Chen, P.L. NBS1 and TRF1 colocalize at PML bodies during late S/G2 phases in immortalized telomerase-negative cells: implication of NBS1 in alternative lengthening of telomeres. J. Biol. Chem. 275, 30618-30622 (2000).
28. 2/M checkpoint defect of ataxia-telangiectasia cells. J. Biol. Chem. 277, 7420-7429 (2002).
29. Li, B., Oestreich, S. & de Lange, T. Identification of human Rap1: implications for telomere evolution. Cell 101, 471-483 (2000).
30. Evans, S.K. & Lundblad, V. Est1 and Cdc13 as comediators of telomerase access. Science 286, 117-120 (1999).
31. Hopfner, K.P. et al. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101, 789-800 (2000).
32. Paull, T.T. & Gellert, M. Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13, 1276-1288 (1999).
33. Moncalian, G. et al. The rad50 signature motif: essential to ATP binding and biological function. J. Mol. Biol. 335, 937-951 (2004).
34. Alani, E., Padmore, R. & Kleckner, N. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61, 419-436 (1990).
35. Lee, J.H. & Paull, T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308, 551-554 (2005).
36. Smogorzewska, A. et al. Control of human telomere length by TRF1 and TRF2. Mol. Cell. Biol. 20, 1659-1668 (2000).
37. Kraakman-van der Zwet, M. et al. Immortalization and characterization of Nijmegen Breakage syndrome fibroblasts. Mutat. Res. 434, 17-27 (1999).
38. Hickson, I. et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64, 9152-9159 (2004).
39. Jazayeri, A. et al. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8, 37-45 (2006).
40. Bianchi, A., Smith, S., Chong, L., Elias, P. & de Lange, T. TRF1 is a dimer and bends telomeric DNA. EMBO J. 16, 1785-1794 (1997).
41. Ziv, Y. et al. Cellular and molecular characteristics of an immortalized ataxia-telangiectasia (group AB) cell line. Cancer Res. 49, 2495-2501 (1989).
42. Chai, W., Sfeir, A.J., Hoshiyama, H., Shay, J.W. & Wright, W.E. The involvement of the Mre11/Rad50/Nbs1 complex in the generation of G-overhangs at human telomeres. EMBO Rep. 7, 225-230 (2006).
43. Lee, J.H. & Paull, T.T. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304, 93-96 (2004).
44. Falck, J., Coates, J. & Jackson, S.P. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434, 605-611 (2005).
45. You, Z., Chahwan, C., Bailis, J., Hunter, T. & Russell, P. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell. Biol. 25, 5363-5379 (2005).
46. Robison, J.G., Elliott, J., Dixon, K. & Oakley, G.G. Replication protein A and the Mre11·Rad50·Nbs1 complex co-localize and interact at sites of stalled replication forks. J. Biol. Chem. 279, 34802-34810 (2004).
47. Trenz, K., Smith, E., Smith, S. & Costanzo, V. ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J. 25, 1764-1774 (2006).
48. Masutomi, K. et al. Telomerase maintains telomere structure in normal human cells. Cell 114, 241-253 (2003).
49. Chamankhah, M. & Xiao, W. Formation of the yeast Mre11-Rad50-Xrs2 complex is correlated with DNA repair and telomere maintenance. Nucleic Acids Res. 27, 2072-2079 (1999).
50. Kironmai, K.M. & Muniyappa, K. Alteration of telomeric sequences and senescence caused by mutations in RAD50 of Saccharomyces cerevisiae. Genes Cells 2, 443-455 (1997).
51. Ritchie, K.B., Mallory, J.C. & 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).
52. Ray, A. & Runge, K.W. Varying the number of telomere-bound proteins does not alter telomere length in tel1Δ cells. Proc. Natl. Acad. Sci. USA 96, 15044-15049 (1999).
53. Craven, R.J. & Petes, T.D. Dependence of the regulation of telomere length on the type of subtelomeric repeat in the yeast Saccharomyces cerevisiae. Genetics 152, 1531-1541 (1999).
54. Wilson, S., Warr, N., Taylor, D.L. & Watts, F.Z. The role of Schizosaccharomyces pombe Rad32, the Mre11 homologue, and other DNA damage response proteins in non-homologous end joining and telomere length maintenance. Nucleic Acids Res. 27, 2655-2661 (1999).
55. + gene involved in DNA repair and telomere maintenance. Mol. Cell. Biol. 23, 6553-6563 (2003).
56. Hartsuiker, E., Vaessen, E., Carr, A.M. & Kohli, J. Fission yeast Rad50 stimulates sister chromatid recombination and links cohesion with repair. EMBO J. 20, 6660-6671 (2001).
57. Manolis, K.G. et al. Novel functional requirements for non-homologous DNA end joining in Schizosaccharomyces pombe. EMBO J. 20, 210-221 (2001).
58. Nakamura, T.M., Moser, B.A. & Russell, P. Telomere binding of checkpoint sensor and DNA repair proteins contributes to maintenance of functional fission yeast telomeres. Genetics 161, 1437-1452 (2002).
59. Wang, R.C., Smogorzewska, A. & de Lange, T. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119, 355-368 (2004).
60. Loayza, D. & De Lange, T. POT1 as a terminal transducer of TRF1 telomere length control. Nature 423, 1013-1018 (2003).