Artemis and nonhomologous end joining-independent influence of DNA-dependent protein kinase catalytic subunit on chromosome stability

Molecular and Cellular Biology

Volumn 29, Issue 2, 2009, Pages 503-514

  Stracker, Travis H ^a   Williams, Bret R ^b,d   Deriano, Ludovic ^c   Theunissen, Jan W ^a,e   Adelman, Carrie A ^a   Roth, David B ^c   Petrini, John H J ^a  

^a Weill Cornell Graduate School of Biomedical Sciences

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e Nature Biotechnology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; DNA DEPENDENT PROTEIN KINASE; MRE11 PROTEIN;

ALLELE; ANIMAL CELL; ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CHROMOSOMAL INSTABILITY; DOUBLE STRANDED DNA BREAK; EMBRYO; ENZYME ACTIVE SITE; FEMALE; GENE; GENE INTERACTION; GENE MUTATION; IONIZING RADIATION; LETHALITY; MITOSIS; MOUSE; MRE11 GENE; NBS1 GENE; NONHUMAN; PRIORITY JOURNAL; PRKDC GENE; RADIOSENSITIVITY; REGULATORY MECHANISM;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL DEATH; CHROMOSOMAL INSTABILITY; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA REPAIR ENZYMES; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; EMBRYO, MAMMALIAN; G2 PHASE; MICE; MICE, TRANSGENIC; NUCLEAR PROTEINS; PROTEIN-SERINE-THREONINE KINASES; S PHASE; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 58249100111     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01354-08     Document Type: Article

References (58)

1. 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.
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. Bressan, D. A., B. K. Baxter, and J. H. Petrini. 1999. The Mre11-Rad50-Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:7681-7687.
4. Buscemi, G., C. Savio, L. Zannini, F. Micciche, D. Masnada, M. Nakanishi, H. Tauchi, K. Komatsu, S. Mizutani, K. Khanna, P. Chen, P. Concannon, L. Chessa, and D. Delia. 2001. Chk2 activation dependence on Nbs1 after DNA damage. Mol. Cell. Biol. 21:5214-5222.
5. Carney, J. P., R. S. Maser, H. Olivares, E. M. Davis, M. Le Beau, J. R. Yates III, L. Hays, W. F. Morgan, and J. H. Petrini. 1998. 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.
6. Carson, C. T., R. A. Schwartz, T. H. Stracker, C. E. Lilley, D. V. Lee, and M. D. Weitzman. 2003. The Mre11 complex is required for ATM activation and the G(2)/M checkpoint. EMBO J. 22:6610-6620.
7. Celli, G. B., E. L. Denchi, and T. de Lange. 2006. Ku 70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination. Nat. Cell Biol. 8:885-890.
8. Chen, B. P., D. W. Chan, J. Kobayashi, S. Burma, A. Asaithamby, K. Morotomi-Yano, E. Botvinick, J. Qin, and D. J. Chen. 2005. Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. J. Biol. Chem. 280:14709-14715.
9. Couedel, C., K. D. Mills, M. Barchi, L. Shen, A. Olshen, R. D. Johnson, A. Nussenzweig, J. Essers, R. Kanaar, G. C. Li, F. W. Alt, and M. Jasin. 2004. Collaboration of homologous recombination and nonhomologous end-joining factors for the survival and integrity of mice and cells. Genes Dev. 18:1293-1304.
10. de Jager, M., J. van Noort, D. C. van Gent, C. Dekker, R. Kanaar, and C. Wyman. 2001. Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell 8:1129-1135.
11. Difilippantonio, S., A. Celeste, M. J. Kruhlak, Y. Lee, M. J. Difilippantonio, L. Feigenbaum, S. P. Jackson, P. J. McKinnon, and A. Nussenzweig. 2007. Distinct domains in Nbs1 regulate irradiation-induced checkpoints and apoptosis. J. Exp. Med. 204:1003-1011.
12. Di Virgilio, M., and J. Gautier. 2005. Repair of double-strand breaks by nonhomologous end joining in the absence of Mre11. J. Cell Biol. 171:765-771.
13. Essers, J., H. van Steeg, J. de Wit, S. M. Swagemakers, M. Vermeij, J. H. Hoeijmakers, and R. Kanaar. 2000. Homologous and non-homologous recombination differentially affect DNA damage repair in mice. EMBO J. 19:1703-1710.
14. Falck, J., J. Coates, and S. P. Jackson. 2005. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605-611.
15. Frank, K. M., N. E. Sharpless, Y. Gao, J. M. Sekiguchi, D. O. Ferguson, C. Zhu, J. P. Manis, J. Horner, R. A. DePinho, and F. W. Alt. 2000. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell 5:993-1002.
16. Fukushima, T., M. Takata, C. Morrison, R. Araki, A. Fujimori, M. Abe, K. Tatsumi, M. Jasin, P. K. Dhar, E. Sonoda, T. Chiba, and S. Takeda. 2001. Genetic analysis of the DNA-dependent protein kinase reveals an inhibitory role of Ku in late S-G2 phase DNA double-strand break repair. J. Biol. Chem. 276:44413-44418.
17. Gao, Y., J. Chaudhuri, C. Zhu, L. Davidson, D. T. Weaver, and F. W. Alt. 1998. A targeted DNA-PKcs-null mutation reveals DNA-PK-independent functions for KU in V(D)J recombination. Immunity 9:367-376.
18. 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.
19. Gladdy, R. A., L. M. Nutter, T. Kunath, J. S. Danska, and C. J. Guidos. 2006. p53-independent apoptosis disrupts early organogenesis in embryos lacking both ataxia-telangiectasia mutated and Prkdc. Mol. Cancer Res. 4:311-318.
20. Goodarzi, A. A., Y. Yu, E. Riballo, P. Douglas, S. A. Walker, R. Ye, C. Harer, C. Marchetti, N. Morrice, P. A. Jeggo, and S. P. Lees-Miller. 2006. DNA-PK autophosphorylation facilitates Artemis endonuclease activity. EMBO J. 25: 3880-3889.
21. 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.
22. Gurley, K. E., and C. J. Kemp. 2001. Synthetic lethality between mutation in Atm and DNA-PK(cs) during murine embryogenesis. Curr. Biol. 11:191-194.
23. Hopfner, K. P., L. Craig, G. Moncalian, R. A. Zinkel, T. Usui, B. A. Owen, A. Karcher, B. Henderson, J. L. Bodmer, C. T. McMurray, J. P. Carney, J. H. Petrini, and J. A. Tainer. 2002. The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418:562-566.
24. Ivanov, E. L., V. G. Korolev, and F. Fabre. 1992. XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics 132:651-664.
25. Jimenez, G. S., F. Bryntesson, M. I. Torres-Arzayus, A. Priestley, M. Beeche, S. Saito, K. Sakaguchi, E. Appella, P. A. Jeggo, G. E. Taccioli, G. M. Wahl, and M. Hubank. 1999. DNA-dependent protein kinase is not required for the p53-dependent response to DNA damage. Nature 400:81-83.
26. Kim, S.-T., B. Xu, and M. B. Kastan. 2002. Involvement of the cohesin protein Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev. 16:560-570.
27. Kitagawa, R., C. J. Bakkenist, P. J. McKinnon, and M. B. Kastan. 2004. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev. 18:1423-1438.
28. 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.
29. 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.
30. Lee, S. E., R. A. Mitchell, A. Chieng, and E. A. Hendrickson. 1997. Evidence for DNA-PK-dependent and -independent DNA double-strand break repair pathways in mammalian cells as a function of the cell cycle. Mol. Cell. Biol. 17:1425-1433.
31. Lee, Y., D. E. Barnes, T. Lindahl, and P. J. McKinnon. 2000. Defective neurogenesis resulting from DNA ligase IV deficiency requires Atm. Genes Dev. 14:2576-2580.
32. Lim, D. S., S. T. Kim, B. Xu, R. S. Maser, J. Lin, J. H. Petrini, and M. B. Kastan. 2000. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404:613-617.
33. Ma, Y., U. Pannicke, K. Schwarz, and M. R. Lieber. 2002. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108:781-794.
34. 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.
35. Maser, R. S., O. K. Mirzoeva, J. Wells, H. Olivares, B. R. Williams, R. Zinkel, P. J. Farnham, and J. H. J. Petrini. 2001. The MRE11 complex and DNA replication: linkage to E2F and sites of DNA synthesis. Mol. Cell. Biol. 21:6006-6016.
36. Matsuoka, S., B. A. Ballif, A. Smogorzewska, E. R. McDonald III, K. E. Hurov, J. Luo, C. E. Bakalarski, Z. Zhao, N. Solimini, Y. Lerenthal, Y. Shiloh, S. P. Gygi, and S. J. Elledge. 2007. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316:1160-1166.
37. Mills, K. D., D. O. Ferguson, J. Essers, M. Eckersdorff, R. Kanaar, and F. W. Alt. 2004. Rad54 and DNA ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev. 18:1283-1292.
38. Mirzoeva, O. K., and J. H. Petrini. 2003. DNA replication- dependent nuclear dynamics of the Mre11 complex. Mol. Cancer Res. 1:207-218.
39. Riballo, E., M. Kuhne, N. Rief, A. Doherty, G. C. Smith, M. J. Recio, C. Reis, K. Dahm, A. Fricke, A. Krempler, A. R. Parker, S. P. Jackson, A. Gennery, P. A. Jeggo, and M. Lobrich. 2004. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell 16:715-724.
40. Rooney, S., F. W. Alt, J. Sekiguchi, and J. P. Manis. 2005. Artemis-independent functions of DNA-dependent protein kinase in Ig heavy chain class switch recombination and development. Proc. Natl. Acad. Sci. USA 102:2471-2475.
41. Rooney, S., J. Sekiguchi, C. Zhu, H. L. Cheng, J. Manis, S. Whitlow, J. DeVido, D. Foy, J. Chaudhuri, D. Lombard, and F. W. Alt. 2002. Leaky Scid phenotype associated with defective V(D)J coding end processing in Artemis-deficient mice. Mol. Cell 10:1379-1390.
42. Sekiguchi, J., D. O. Ferguson, H. T. Chen, E. M. Yang, J. Earle, K. Frank, S. Whitlow, Y. Gu, Y. Xu, A. Nussenzweig, and F. W. Alt. 2001. Genetic interactions between ATM and the nonhomologous end-joining factors in genomic stability and development. Proc. Natl. Acad. Sci. USA 98:3243-3248.
43. Siloh, Y. 2003. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3:155-168.
44. Smogorzewska, A., J. Karlseder, H. Holtgreve-Grez, A. Jauch, and T. de Lange. 2002. DNA ligase IV-dependent NHEJ of deprotected mammalian telomeres in G1 and G2. Curr. Biol. 12:1635-1644.
45. Stewart, G. S., R. S. Maser, T. Stankovic, D. A. Bressan, M. I. Kaplan, N. G. Jaspers, A. Raams, P. J. Byrd, J. H. Petrini, and A. M. Taylor. 1999. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell 99:577-587.
46. 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.
47. Stracker, T. H., M. Morales, S. S. Couto, H. Hussein, and J. H. Petrini. 2007. The carboxy terminus of NBS1 is required for induction of apoptosis by the MRE11 complex. Nature 447:218-221.
48. 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.
49. Theunissen, J. W., M. I. Kaplan, P. A. Hunt, B. R. Williams, D. O. Ferguson, F. W. Alt, and J. H. Petrini. 2003. Checkpoint failure and chromosomal instability without lymphomagenesis in Mre11(ATLD1/ATLD1) mice. Mol. Cell 12:1511-1523.
50. 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.
51. Uziel, T., Y. Lerenthal, L. Moyal, Y. Andegeko, L. Mittelman, and Y. Shiloh. 2003. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22:5612-5621.
52. 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.
53. 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.
54. Wu, X., V. Ranganathan, D. S. Weisman, W. F. Heine, D. N. Ciccone, T. B. O'Neill, K. E. Crick, K. A. Pierce, W. S. Lane, G. Rathbun, D. M. Livingston, and D. T. Weaver. 2000. ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature 405:477-482.
55. 2/M checkpoints are induced by ionizing irradiation. Mol. Cell. Biol. 22:1049-1059.
56. Yamaguchi-Iwai, Y., E. Sonoda, M. S. Sasaki, C. Morrison, T. Haraguchi, Y. Hiraoka, Y. M. Yamashita, T. Yagi, M. Takata, C. Price, N. Kakazu, and S. Takeda. 1999. Mre11 is essential for the maintenance of chromosomal DNA in vertebrate cells. EMBO J. 18:6619-6629.
57. Yang, Y. G., A. Saidi, P. O. Frappart, W. Min, C. Barrucand, V. Dumon-Jones, J. Michelon, Z. Herceg, and Z. Q. Wang. 2006. Conditional deletion of Nbs1 in murine cells reveals its role in branching repair pathways of DNA double-strand breaks. EMBO J. 25:5527-5538.
58. You, Z., C. Chahwan, J. Bailis, T. Hunter, and P. Russell. 2005. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell. Biol. 25:5363-5379.