The Mre11 complex and the response to dysfunctional telomeres

Molecular and Cellular Biology

Volumn 29, Issue 20, 2009, Pages 5540-5551

  Attwooll, Claire L ^a   Akpinar, Müge ^a,b   Petrini, John H J ^a,c  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b Gerstner Sloan Kettering Graduate School of Biomedical Sciences   (United States)

^c Weill Cornell Graduate School of Biomedical Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MRE11 PROTEIN; NIBRIN; TELOMERASE; TELOMERIC REPEAT BINDING FACTOR 2;

ANIMAL CELL; ARTICLE; CHROMATID; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA STRAND BREAKAGE; EMBRYO; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TELOMERE; WILD TYPE;

ANIMALS; CELL CYCLE PROTEINS; CHROMOSOMES, MAMMALIAN; DNA DAMAGE; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; FIBROBLASTS; MICE; NUCLEAR PROTEINS; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 2;

MAMMALIA;

EID: 70350455474     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00479-09     Document Type: Article

References (55)

1. Adelman, C. A., S. De, and J. H. Petrini. 2009. Rad50 is dispensable for the maintenance and viability of postmitotic tissues. Mol. Cell. Biol. 29:483-492.
2. Bailey, S. M., M. N. Cornforth, A. Kurimasa, D. J. Chen, and E. H. Goodwin. 2001. Strand-specific postreplicative processing of mammalian telomeres. Science 293:2462-2465.
3. 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.
4. 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.
5. Celli, G. B., and T. de Lange. 2005. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 7:712-718.
6. Chai, W., A. J. Sfeir, H. Hoshiyama, J. W. Shay, and W. E. Wright. 2006. The involvement of the Mre11/Rad50/Nbs1 complex in the generation of Goverhangs at human telomeres. EMBO Rep. 7:225-230.
7. de Lange, T. 2005. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19:2100-2110.
8. Denchi, E. L., and T. de Lange. 2007. Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1. Nature 448:1068-1071.
9. Deriano, L., T. H. Stracker, A. Baker, J. H. Petrini, and D. B. Roth. 2009. Roles for NBS1 in alternative and joining of V(D)J recombination intermediates. Mol. Cell 34:13-25.
10. Dull, T., R. Zufferey, M. Kelly, R. J. Mandel, M. Nguyen, D. Trono, and L. Naldini. 1998. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72:8463-8471. (Pubitemid 28471781)
11. Gilley, D., H. Tanaka, M. P. Hande, A. Kurimasa, G. C. Li, M. Oshimura, and D. J. Chen. 2001. DNA-PKcs is critical for telomere capping. Proc. Natl. Acad. Sci. USA 98:15084-15088.
12. Goudsouzian, L. K., C. T. Tuzon, and V. A. Zakian. 2006. S. cerevisiae Tel1p and Mre11p are required for normal levels of Est1p and Est2p telomere association. Mol. Cell 24:603-610.
13. 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.
14. Griffith, J. D., L. Comeau, S. Rosenfield, R. M. Stansel, A. Bianchi, H. Moss, and T. de Lange. 1999. Mammalian telomeres end in a large duplex loop. Cell 97:503-514.
15. Hackett, J. A., and C. W. Greider. 2003. End resection initiates genomic instability in the absence of telomerase. Mol. Cell. Biol. 23:8450-8461.
16. Hande, M. P., E. Samper, P. Lansdorp, and M. A. Blasco. 1999. Telomere length dynamics and chromosomal instability in cells derived from telomerase null mice. J. Cell Biol. 144:589-601.
17. Helmink, B. A., A. L. Bredemeyer, B. S. Lee, C. Y. Huang, G. G. Sharma, L. M. Walker, J. J. Bednarski, W. L. Lee, T. K. Pandita, C. H. Bassing, and B. P. Sleckman. 2009. MRN complex function in the repair of chromosomal Rag-mediated DNA double-strand breaks. J. Exp. Med. 206:669-679.
18. Karlseder, J., A. Smogorzewska, and T. de Lange. 2002. Senescence induced by altered telomere state, not telomere loss. Science 295:2446-2449. (Pubitemid 34270257)
19. Lansdorp, P. M., N. P. Verwoerd, F. M. van de Rijke, V. Dragowska, M. T. Little, R. W. Dirks, A. K. Raap, and H. J. Tanke. 1996. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 5:685-691.
20. Lazzerini Denchi, E., G. Celli, and T. de Lange. 2006. Hepatocytes with extensive telomere deprotection and fusion remain viable and regenerate liver mass through endoreduplication. Genes Dev. 20:2648-2653.
21. Lee, J. H., and T. T. Paull. 2007. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26:7741-7748.
22. Lee, S. E., D. A. Bressan, J. H. J. Petrini, and J. E. Haber. 2002. Complementation between N-terminal Saccharomyces cerevisiae mre11 alleles in DNA repair and telomere length maintenance. DNA Repair (Amsterdam) 1:27-40.
23. Liu, Y., B. E. Snow, M. P. Hande, D. Yeung, N. J. Erdmann, A. Wakeham, A. Itie, D. P. Siderovski, P. M. Lansdorp, M. O. Robinson, and L. Harrington. 2000. The telomerase reverse transcriptase is limiting and necessary for telomerase function in vivo. Curr. Biol. 10:1459-1462.
24. Loayza, D., and T. De Lange. 2003. POT1 as a terminal transducer of TRF1 telomere length control. Nature 423:1013-1018. (Pubitemid 36806919)
25. Lois, C., E. J. Hong, S. Pease, E. J. Brown, and D. Baltimore. 2002. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868-872. (Pubitemid 34118370)
26. Makarov, V. L., Y. Hirose, and J. P. Langmore. 1997. Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell 88:657-666.
27. Maser, R. S., and R. A. DePinho. 2002. Connecting chromosomes, crisis, and cancer. Science 297:565-569.
28. Mimitou, E. P., and L. S. Symington. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770-774.
29. Morales, M., J. W. Theunissen, C. F. Kim, R. Kitagawa, M. B. Kastan, and J. H. Petrini. 2005. The Rad50S allele promotes ATM-dependent DNA damage responses and suppresses ATM deficiency: implications for the Mre11 complex as a DNA damage sensor. Genes Dev. 19:3043-3054. (Pubitemid 41798119)
30. Moreau, S., J. R. Ferguson, and L. S. Symington. 1999. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19:556-566.
31. Moreau, S., E. A. Morgan, and L. S. Symington. 2001. Overlapping functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 nucleases in DNA metabolism. Genetics 159:1423-1433.
32. Nikitina, T., and C. L. Woodcock. 2004. Closed chromatin loops at the ends of chromosomes. J. Cell Biol. 166:161-165. (Pubitemid 38988768)
33. Palm, W., and T. de Lange. 2008. How shelterin protects mammalian telomeres. Annu Rev. Genet. 42:301-334.
34. Paull, T. T., and M. Gellert. 1998. The 3′ to 5′ exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks. Mol. Cell 1:969-979. (Pubitemid 128379258)
35. Poon, S. S., and P. M. Lansdorp. 2001. Quantitative fluorescence in situ hybridization (Q.-FISH). Curr. Protoc. Cell Biol. Chapter 18, unit 18.4.
36. Ranganathan, V., W. F. Heine, D. N. Ciccone, K. L. Rudolph, X. Wu, S. Chang, H. Hai, I. M. Ahearn, D. M. Livingston, I. Resnick, F. Rosen, E. Seemanova, P. Jarolim, R. A. DePinho, and D. T. Weaver. 2001. Rescue of a telomere length defect of Nijmegen breakage syndrome cells requires NBS and telomerase catalytic subunit. Curr. Biol. 11:962-966.
37. Sartori, A. A., C. Lukas, J. Coates, M. Mistrik, S. Fu, J. Bartek, R. Baer, J. Lukas, and S. P. Jackson. 2007. Human CtIP promotes DNA end resection. Nature 450:509-514.
38. Stracker, T. H., S. S. Couto, C. Cordon-Cardo, T. Matos, and J. H. Petrini. 2008. Chk2 suppresses the oncogenic potential of DNA replication-associated DNA damage. Mol. Cell 31:21-32.
39. Stracker, T. H., J. W. Theunissen, M. Morales, and J. H. Petrini. 2004. The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair (Amsterdam) 3:845-854.
40. Stracker, T. H., B. R. Williams, L. Deriano, J. W. Theunissen, C. A. Adelman, D. B. Roth, and J. H. Petrini. 2009. Artemis and nonhomologous end joining-independent influence of DNA-dependent protein kinase catalytic subunit on chromosome stability. Mol. Cell. Biol. 29:503-514.
41. Takai, H., A. Smogorzewska, and T. de Lange. 2003. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:1549-1556.
42. ATLD1/ATLD1 mice. Mol. Cell 12:1511-1523.
43. Theunissen, J. W., and J. H. Petrini. 2006. Methods for studying the cellular response to DNA damage: influence of the Mre11 complex on chromosome metabolism. Methods Enzymol. 409:251-284.
44. Todaro, G. J., and H. Green. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17:299-313.
45. Tsukamoto, Y., A. K. Taggart, and V. A. Zakian. 2001. The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr. Biol. 11:1328-1335.
46. van Steensel, B., and T. de Lange. 1997. Control of telomere length by the human telomeric protein TRF1. Nature 385:740-743.
47. Verdun, R. E., L. Crabbe, C. Haggblom, and J. Karlseder. 2005. Functional human telomeres are recognized as DNA damage in G2 of the cell cycle. Mol. Cell 20:551-561.
48. Wang, R. C., A. Smogorzewska, and T. de Lange. 2004. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119:355-368.
49. Williams, B. R., O. K. Mirzoeva, W. F. Morgan, J. Lin, W. Dunnick, and J. H. Petrini. 2002. A murine model of nijmegen breakage syndrome. Curr. Biol. 12:648-653.
50. Williams, R. S., G. Moncalian, J. S. Williams, Y. Yamada, O. Limbo, D. S. Shin, L. M. Groocock, D. Cahill, C. Hitomi, G. Guenther, D. Moiani, J. P. Carney, P. Russell, and J. A. Tainer. 2008. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 135:97-109.
51. Wiltzius, J. J., M. Hohl, J. C. Fleming, and J. H. Petrini. 2005. The Rad50 hook domain is a critical determinant of Mre11 complex functions. Nat. Struct. Mol. Biol. 12:403-407.
52. Wyman, C., and R. Kanaar. 2006. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40:363-383.
53. Ye, J. Z., D. Hockemeyer, A. N. Krutchinsky, D. Loayza, S. M. Hooper, B. T. Chait, and T. de Lange. 2004. POT1-interacting protein PIP1: a telomere length regulator that recruits POT1 to the TIN2/TRF1 complex. Genes Dev. 18:1649-1654.
54. Zhu, X. D., B. Kuster, M. Mann, J. H. Petrini, and T. Lange. 2000. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25:347-352.
55. Zhu, Z., W. H. Chung, E. Y. Shim, S. E. Lee, and G. Ira. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981-994.