Dancing on damaged chromatin: Functions of ATM and the RAD50/MRE11/NBS1 complex in cellular responses to DNA damage

Journal of Radiation Research

Volumn 49, Issue 5, 2008, Pages 451-464

  Iijima, Kenta ^a   Ohara, Maki ^a   Seki, Ryota ^a   Tauchi, Hiroshi ^a  

^a IBARAKI UNIVERSITY   (Japan)

Author keywords

ATM; Chromatin remodeling; Homologous recombination; NBS1

Indexed keywords

ACETYLATION; ACTIVATION ANALYSIS; ASSOCIATION REACTIONS; CELL SIGNALING; CHEMICAL ACTIVATION; DNA; GENES; INTERNET PROTOCOLS; PHOSPHORYLATION; REPAIR;

CELLULAR RESPONSE; CHROMATIN REMODELLING; COMMUNICATIONS NETWORKS; DNA DAMAGES; DNA DOUBLE STRAND BREAKS; EUKARYOTIC CELLS; GENETIC INFORMATION; HOMOLOGOUS RECOMBINATION; PROTEIN KINASE; SIGNALING NETWORKS;

PROTEINS;

EUKARYOTA;

EID: 52249091114     PISSN: 04493060     EISSN: 13499157     Source Type: Journal    
DOI: 10.1269/jrr.08065     Document Type: Review

References (102)

1. Kobayashi, J., Iwabuchi, K., Miyagawa, K., Sonoda, E., Suzuki, K., Takata, M. and Tauchi, H. (2008) Current topics in DNA double-strand break repair. J. Radiat. Res. 49: 93-103.
2. Shiloh, Y. (2003) ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 3: 155-168.
3. Lee. J. H. and Paull, T. T. (2007) Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26: 7741-7748.
4. Wu, Y., Xiao, S. and Zhu, X. D. (2007) MRE11-RAD50-NBS1 and ATM function as co-mediators of TRF1 in telom-ere length control. Nat. Struct. Mol. Biol. 14: 832-840.
5. Matsuoka, S., Ballif, B. A., Smogorzewska, A., McDonald, E. R. 3rd, Hurov, K. E., Luo, J., Bakalarski, C. E., Zhao, Z., Sohmini, N., Lerenthal, Y., Shiloh, Y., Gygi, S. P. and Elledge, S. J. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316: 1160-1166.
6. Iijima, K., Komatsu, K., Matsuura, S. and Tauchi, H. (2004) The Nijmegen breakage syndrome gene and its role in genome stability. Chromosoma 113: 53-61.
7. Berkovich, E., Monnat, R. J. Jr. and Kastan, M. B. (2007) Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 9: 683-690.
8. Kolas, N. K., Chapman, J. R., Nakada, S., Ylanko, J., Chahwan, R., Sweeney, F. D., Panier, S., Mendez, M., Wildenhain, J., Thomson, T. M., Pelletier, L., Jackson, S. P. and Durocher, D. (2007) Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318: 1637-1640.
9. Huen, M. S., Grant, R., Manke, I., Minn, K., Yu, X., Yaffe, M. B. and Chen, J. (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131: 901-914.
10. Mailand, N., Bekker-Jensen, S., Faustrup, H., Melander, F., Bartek, J., Lukas, C. and Lukas, J. (2007) RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131: 887-900.
11. Abraham, R. T. (2004) PI 3-kinase related kinases: 'big' players in stress-induced signaling pathways. DNA Repair 3: 883-887.
12. You, Z., Chahwan, C., Bailis, J., Hunter, T. and Russell, P. (2005) ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell. Biol. 25: 5363-5379.
13. Bosotti, R., Isacchi, A. and Sonnhammer, E. L. (2000) FAT: a novel domain in PIK-related kinases. Trends Biochem. Sci. 25: 225-227.
14. Bakkenist, C. J. and Kastan, M. B. (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506.
15. Becker, E., Meyer, V., Madaoui, H. and Guerois, R. (2006) Detection of a tandem BRCT in Nbs1 and Xrs2 with functional implications in the DNA damage response. Bioinfor-matics 22: 1289-1292.
16. Kobayashi, J., Tauchi, H., Sakamoto, S., Nakamura, A., Morishima, K., Matsuura, S., Kobayashi, T., Tamai, K., Tanimoto, K. and Komatsu, K. (2002) NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12: 1846-1851.
17. Desai-Mehta, A., Cerosaletti, K. M. and Concannon, P. (2001) Distinct functional domains of nibrin mediate Mre11 binding, focus formation, and nuclear localization. Mol. Cell. Biol. 21: 2184-2191.
18. Falck, J., Coates, J. and Jackson, S. P. (2005) Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434: 605-611.
19. Zhou, J., Lim, C. U., Li, J. J., Cai, L. and Zhang, Y. (2006) The role of NBS1 in the modulation of PIKK family proteins ATM and ATR in the cellular response to DNA damage. Cancer Lett. 243: 9-15.
20. Zhang, Y., Zhou, J. and Lim, C. U. (2006) The role of NBS1 in DNA double strand break repair, telomere stability, and cell cycle checkpoint control. Cell Res. 16: 45-54.
21. Williams, R. S., Williams, J. S. and Tainer, J. A. (2007) Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chro-matin template. Biochem. Cell Biol. 85: 509-520.
22. Tmjillo, K. M., Yuan, S. S., Lee, E. Y. and Sung, P. (1998) Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95. J. Biol. Chem. 273: 21447-21450.
23. D' Amours, D. and Jackson, S. P. (2002) The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat. Rev. Mol. Cell Biol. 3: 317-327.
24. Paull, T. T. and Gellert, M. (1999) Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13: 1276-1288.
25. Hopfner, K. P. and Tainer, J. A. (2003) Rad50/SMC proteins and ABC transporters: unifying concepts from high-resolution structures. Curr. Opin. Struct. Biol. 13: 249-255.
26. Hopfner, K. P., Craig, L., Moncalian, G., Zinkel, R. A., Usui, T., Owen, B. A., Karcher, A., Henderson, B., Bodmer, J. L., McMurray, C. T., Carney, J. P., Petrini, J. H. and Tainer, J. A. (2002) The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418: 562-566.
27. Paull, T. T. and Gellert, M. (1998) The 3' to 5' exonuclease activity of Mre11 facilitates repair of DNA double-strand breaks. Mol. Cell 1: 969-979.
28. Lee, J. H. and Paull, T. T. (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308: 551-554.
29. Pellegrini, M., Celeste, A., Difilippantonio, S., Guo, R., Wang, W., Feigenbaum, L. and Nussenzweig, A. (2006) Autophosphorylation at serine 1987 is dispensable for murine Atm activation in vivo. Nature 443: 222-225.
30. Kozlov, S. V., Graham, M. E., Peng, C., Chen, P., Robinson, P. J. and Lavin, M. F. (2006) Involvement of novel autophosphorylation sites in ATM activation. EMBO J. 25: 3504-3514.
31. Goodarzi, A. A., Jonnalagadda, J. C., Douglas, P., Young, D., Ye, R., Moorhead, G. B., Lees-Miller, S. P. and Khanna, K. K. (2004) Autophosphorylation of ataxia-telangiectasia mutated is regulated by protein phosphatase 2A. EMBO J. 23: 4451-4461.
32. Ali, A., Zhang, J., Bao, S., Liu, I., Otterness, D., Dean, N. M., Abraham, R. T. and Wang, X. F. (2004) Requirement of protein phosphatase 5 in DNA-damage-induced ATM activation. Genes Dev. 18: 249-254.
33. Shreeram, S., Demidov, O. N., Hee, W. K., Yamaguchi, H., Onishi, N., Kek, C., Timofeev, O. N., Dudgeon, C., Fornace, A. J., Anderson, C. W., Minami, Y., Appella, E. and Bulavin, D. V. (2006) Wip1 phosphatase modulates ATM-dependent signaling pathways. Mol. Cell 23: 757-764.
34. Sun, Y., Jiang, X., Chen, S., Femandes, N. and Price, B. D. (2005) A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc. Natl. Acad. Sci. USA. 102: 13182-13187.
35. Sun, Y., Xu, Y., Roy, K. and Price, B. D. (2007) DNA damage-induced acetylation of lysine 3016 of ATM activates ATM kinase activity. Mol. Cell. Biol. 27: 8502-8509.
36. Uziel, T., Lerenthal, Y., Moyal, L., Andegeko, Y., Mittelman, L. and Shiloh, Y. (2003) Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22: 5612-5621.
37. Carson, C. T., Schwartz, R. A., Stacker, T. H., Lilley, C. E., Lee, D. V. and Weitzman, M. D. (2003) The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22: 6610-6620.
38. Lee. J. H. and Paull, T. T. (2004) Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304: 93-96.
39. Nakada, D., Matsumoto, K. and Sugimoto, K. (2003) ATM-related Tel1 associates with double-strand breaks through an Xrs2-dependent mechanism. Genes Dev. 17: 1957-1962.
40. Stracker, T. H., Morales, M., Couto, S. S., Hussein, H. and Petrini, J. H. (2007) The carboxy terminus of NBS1 is required for induction of apoptosis by the MRE11 complex. Nature 447: 218-221.
41. Difilippantonio, S., Celeste, A., Kruhlak, M. J., Lee, Y., Difilippantonio, M. J., Feigenbaum, L., Jackson, S. P., McKinnon, P. J. and Nussenzweig, A. (2007) Distinct domains in Nbs1 regulate irradiation-induced checkpoints and apoptosis. J. Exp. Med. 204: 1003-1011.
42. Lou, Z., Minter-Dykhouse, K., Franco, S., Gostissa, M., Rivera, M. A., Celeste, A., Manis, J. P., van Deursen. J., Nussenzweig, A., Paull, T. T., Alt, F. W. and Chen, J. (2006) MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell 21: 187-200.
43. Spycher, C., Miller, E. S., Townsend, K., Pavic, L., Morrice, N. A., Janscak, P., Stewart, G. S. and Stucki, M. (2008) Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin. J. Cell Biol. 181: 227-240.
44. Melander, F., Bekker-Jensen, S., Falck, J., Bartek, J., Mailand, N. and Lukas, J. (2008) Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J. Cell Biol. 181: 213-226.
45. Chapman, J. R. and Jackson, S. P. (2008) Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep. online publication, doi: 10.1038/embor.2008.103.
46. Dupré, A., Boyer-Chatenet, L. and Gautier, J. (2006) Two-step activation of ATM by DNA and the Mre11-Rad50-Nbs1 complex. Nat. Struct. Mol. Biol. 13: 451-457.
47. Kanu, N. and Behrens, A. (2007) ATMIN defines an NBS1-independent pathway of ATM signalling. EMBO J. 26: 2933-2941.
48. van Gent, D. C. and van der Burg, M. (2007) Non-homologous end-joining, a sticky affair. Oncogene 26: 7731-7740.
49. Li, X. and Heyer, W. D. (2008) Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 18: 99-113.
50. Tauchi, H., Matsuura, S., Kobayashi, J., Sakamoto, S. and Komatsu, K. (2002) Nijmegen breakage syndrome gene, NBS1, and molecular links to factors for genome stability. Oncogene 21: 8967-8980.
51. Golding, S. E., Rosenberg, E., Khalil, A., McEwen, A., Holmes, M., Neill, S., Povirk, L. F. and Valerie, K. (2004) Double strand break repair by homologous recombination is regulated by cell cycle-independent signaling via ATM in human glioma cells. J. Biol. Chem. 279: 15402-15410.
52. Bolderson, E., Scorah, J., Helleday, T., Smythe, C. and Meuth, M. (2004) ATM is required for the cellular response to thymidine induced replication fork stress. Hum. Mol. Genet. 13: 2937-2945.
53. Sakamoto, S., Iijima, K., Mochizuki, D., Nakamura, K., Teshigawara, K., Kobayashi, J., Matsuura, S., Tauchi, H. and Komatsu, K. (2007) Homologous recombination repair is regulated by domains at the N- and C-terminus of NBS1 and is dissociated with ATM functions. Oncogene 26: 6002-6009.
54. Sarkaria, J. N., Busby, E. C., Tibbetts, R. S., Roos, P., Taya, Y., Kamitz, L. M. and Abraham, R. T. (1999) Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59: 4375-4382.
55. Kraakman-van der Zwet, M., Overkamp, W. J., Friedl, A. A., Klein, B., Verhaegh, G. W., Jaspers, N. G., Midr, A. T., Eckardt-Schupp, F., Lohman, P. H. and Zdzienicka, M. Z. (1999) Immortalization and characterization of Nijmegen Breakage syndrome fibroblasts. Mutat. Res. 434: 17-27.
56. Morrison, C., Sonoda, E., Takao, N., Shinohara, A., Yamamoto, K. and Takeda, S. (2000) The controlling role of ATM in homologous recombinational repair of DNA damage. EMBO J. 19: 463-471.
57. Riballo, E., Kühne, M., Rief, N., Doheity, A., Smith, G. C., Recio, M. J., Reis, C., Dahm, K., Fricke, A., Rrempler, A., Parker, A. R., Jackson, S. P., Gennery, A., Jeggo, P. A. and Löbrich, M. (2004) A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell 16: 715-724.
58. Wang, H., Wang, H., Powell, S. N., Iliakis, G. and Wang, Y. (2004) ATR affecting cell radiosensitivity is dependent on homologous recombination repair but independent of nonho-mologous end joining. Cancer Res. 64: 7139-7143.
59. Sørensen, C. S., Hansen. L. T., Dziegielewski, J., Syljuåsen, R. G., Lundin, C., Bartek, J. and Helleday, T. (2005) The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat. Cell Biol. 7: 195-201.
60. Bahassi, E. M., Ovesen, J. L., Riesenberg, A. L., Bernstein, W. Z., Hasty, P. E. and Stambrook, P. J. (2008) The checkpoint kinases Chk1 and Chk2 regulate the functional associations between hBRCA2 and Rad51 in response to DNA damage. Oncogene 27: 3977-3985.
61. Jazayeri, A., Falck, J., Lukas, C., Bartek, J., Smith, G. C., Lukas, J. and Jackson, S. P. (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8: 37-45.
62. Esashi, F., Christ, N., Gannon, J., Liu, Y., Hunt, T., Jasin, M. and West, S. C. (2005) CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434: 598-604.
63. Tauchi, H., Kobayashi, J., Morishima, K., Matsuura, S., Nakamura, A., Shiraishi, T., Ito, E., Masnada, D., Delia, D. and Komatsu, K. (2001) The forkhead-associated domain of NBS1 is essential for nuclear foci formation after irradiation but not essential for hRAD50 hMRE11 NBS1 complex DNA repair activity. J. Biol. Chem. 276: 12-15.
64. Sartori, A. A., Lukas, C., Coates, J., Mistrik, M., Fu, S., Bartek, J., Baer, R., Lukas, J. and Jackson, S. P. (2007) Human CtIP promotes DNA end resection. Nature 450: 509-514.
65. Chen, B. P., Uematsu, N., Kobayashi, J., Lerenthal, Y., Rrempler, A., Yajima, H., Löbrich, M., Shiloh, Y. and Chen, D. J. (2007) Ataxia telangiectasia mutated (ATM) is essential for DNA-PKcs phosphorylations at the Thr-2609 cluster upon DNA double strand break. J. Biol. Chem. 282: 6582-6587.
66. Goodarzi, A. A., Yu, Y., Riballo, E., Douglas, P., Walker, S. A., Ye, R., Härer, C., Marchetti, C., Morrice, N., Jeggo, P. A. and Lees-Miller, S. P. (2006) DNA-PK autophosphorylation facilitates Artemis endonuclease activity. EMBO J. 25: 3880-3889.
67. Bredemeyer, A. L., Sharma, G. G., Huang, C. Y., Helmink, B. A., Walker, L. M., Khor, K. C., Nuskey, B., Sullivan, K. E., Pandita, T. K., Bassing, C. H. and Sleckman, B. P. (2006) ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature 442: 466-470.
68. Chen, L., Trujillo, K., Ramos, W., Sung, P. and Tomkinson, A. E. (2001) Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes. Mol. Cell. 8: 1105-1115.
69. Palmbos, P. L., Daley, J. M. and Wilson, T. E. (2005) Mutations of the Yku80 C terminus and Xrs2 FHA domain specifically block yeast nonhomologous end joining. Mol. Cell. Biol. 25: 10782-10790.
70. Zhang, Y., Hefferin, M. L., Chen, L., Shim, E. Y., Tseng, H. M., Kwon, Y., Sung, P., Lee, S. E. and Tomkinson, A. E. (2007) Role of Dnl4-Lif1 in nonhomologous end-joining repair complex assembly and suppression of homologous recombination. Nat. Struct. Mol. Biol. 14: 639-646.
71. de Jager, M., Dronkert, M. L., Modesti, M., Beerens, C. E., Kanaar, R. and van Gent, D. C. (2001) DNA-binding and strand-annealing activities of human Mre11: implications for its roles in DNA double-strand break repair pathways. Nucleic Acids Res. 29: 1317-1325.
72. Howlett, N. G., Scuric, Z., D' Andrea, A. D. and Schiestl, R. H. (2006) Impaired DNA double strand break repair in cells from Nijmegen breakage syndrome patients. DNA Repair 5: 251-257.
73. Zhang, X., Succi, J., Feng, Z., Prithivirajsingh, S., Story, M. D. and Legerski, R. J. (2004) Artemis is a phosphorylation target of ATM and ATR and is involved in the G2/M DNA damage checkpoint response. Mol. Cell. Biol. 24: 9207-9220.
74. Chen, L., Mono, T., Minegishi, Y., Nakada, S., Nagasawa, M., Komatsu, K., Chessa, L., Villa, A., Lecis, D., Delia, D. and Mizutani, S. (2005) Ataxia-telangiectasia-mutated dependent phosphorylation of Artemis in response to DNA damage. Cancer Sci. 96: 134-141.
75. Yang, Y. G., Saidi, A., Frappart, P. O., Min, W., Barrucand, C., Dumon-Jones, V., Michelon, J., Herceg, Z. and Wang, Z. Q. (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.
76. Vissers, J. H., Nicassio, F., van Lohuizen, M., Di Fiore, P. P. and Citterio, E. (2008) The many faces of ubiquitinated histone H2A: insights from the DUBs. Cell Div. 3: 8.
77. van Attikum, H. and Gasser, S. M. (2005) The histone code at DNA breaks: a guide to repair? Nat. Rev. Mol. Cell Biol. 6: 757-765.
78. Downs. J. A., Nussenzweig, M. C. and Nussenzweig, A. (2007) Chromatin dynamics and the preservation of genetic information. Nature 447: 951-958.
79. Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128: 693-705.
80. Shim, E. Y., Ma, J. L., Oum, J. H., Yanez, Y. and Lee, S. E. (2005) The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol. Cell. Biol. 25: 3934-3944.
81. Shim, E. Y., Hong, S. J., Oum, J. H., Yanez, Y., Zhang, Y. and Lee, S. E. (2007) RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell. Biol. 27: 1602-1613.
82. Jin, J., Cai, Y., Yao, T., Gottschalk, A. J., Florens, L., Swanson, S. K., Gutiérrez, J. L., Coleman, M. K., Workman, J. L., Mushegian, A., Washburn, M. P., Conaway, R. C. and Conaway, J. W. (2005) A mammalian chromatin remodeling complex with similarities to the yeast INO80 complex. J. Biol. Chem. 280: 41207-41212.
83. Downs, J. A., Allard, S., Jobin-Robitaille, O., Javaheri, A., Auger, A., Bouchard, N., Kron, S. J., Jackson, S. P. and Côté, J. (2004) Binding of chromatin-modifying activities to phos-phorylated histone H2A at DNA damage sites. Mol.Cell 16: 979-990.
84. van Attikum, H., Fritsch, O., Hohn, B. and Gasser, S. M. (2004) Recruitment of the INO80 complex by H2A phospho-rylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119: 777-788.
85. Morrison, A. J., Kim, J. A., Person, M. D., Highland, J., Xiao, J., Wehr, T. S., Hensley, S., Bao, Y., Shen, J., Collins, S. R., Weissman, J. S., Delrow, J., Krogan, N. J., Haber, J. E. and Shen, X. (2007) Mec1/Tel1 phosphorylation of the INO80 chromatin remodeling complex influences DNA damage checkpoint responses. Cell 130: 499-511.
86. Tsukuda, T., Fleming, A. B., Nickoloff, J. A. and Osley, M. A. (2005) Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438: 379-383.
87. Unal, E., Arbel-Eden, A., Sattler, U., Shroff, R., Lichten, M., Haber, J. E. and Koshland, D. (2004) DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 16: 991-1002.
88. Robert, F., Hardy, S., Nagy, Z., Baldeyron, C., Murr, R., Déry, U., Masson, J. Y., Papadopoulo, D., Herceg, Z. and Tora, L. (2006) The transcriptional histone acetyltransferase cofactor TRRAP associates with the MRN repair complex and plays a role in DNA double-strand break repair. Mol. Cell. Biol. 26: 402-412.
89. Murr, R., Loizou, J. I., Yang, Y. G., Cuenin, C., Li, H., Wang, Z. Q. and Herceg, Z. (2006) Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell Biol. 8: 91-99.
90. Ulrich, H. D., and Jentsch, S. (2000) Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J. 19: 3388-3397.
91. Zhao, G. Y., Sonoda, E., Barber, L. J., Oka, H., Murakawa, Y., Yamada, K., Ikura, T., Wang, X., Kobayashi, M., Yamamoto, K., Boulton, S. J. and Takeda, S. (2007) A critical role for the ubiquitin-conjugating enzyme Ubc13 in initiating homologous recombination. Mol. Cell 25: 663-675.
92. Xie, A., Puget, N., Shim, I., Odate, S., Jarzyna, I., Bassing, C. H., Alt, F. W. and Scully, R. (2004) Control of sister chromatid recombination by histone H2AX. Mol. Cell 16: 1017-1025.
93. Ikura, T., Tashiro, S., Kakino, A., Shima, H., Jacob, N., Amunugama, R., Yoder, K., Izumi, S., Kuraoka, I., Tanaka, K., Kimura, H., Ikura, M., Nishikubo, S., Ito, T., Muto, A., Miyagawa, K., Takeda, S., Fishel, R., Igarashi, K. and Kamiya, K. (2007) DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 27: 7028-7040.
94. Kim, H., Chen, J. and Yu, X. (2007) Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316: 1202-1205.
95. Sobhian, B., Shao, G., Lilli, D. R., Culhane, A. C., Moreau, L. A., Xia, B., Livingston, D. M. and Greenberg, R. A. (2007) RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316: 1198-1202.
96. Wang, B., Matsuoka, S., Ballif, B. A., Zhang, D., Smogorzewska, A., Gygi, S. P. and Elledge, S. J. (2007) Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316: 1194-1198.
97. Polanowska, J., Martin, J. S., Garcia-Muse, T., Petalcorin, M. I. and Boulton, S. J. (2006) A conserved pathway to activate BRCA1-dependent ubiquitylation at DNA damage sites. EMBO J. 25: 2178-2188.
98. Xie, A., Hartlerode, A., Stucki, M., Odate, S., Puget, N., Kwok, A., Nagaraju, G., Yan, C., Alt, F. W., Chen, J., Jackson, S. P. and Scully, R. (2007) Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol. Cell 28: 1045-1057.
99. Ziv, Y., Bielopolski, D., Galanty, Y., Lukas, C., Taya, Y., Schultz, D. C., Lukas, J., Bekker-Jensen, S., Bartek, J. and Shiloh, Y. (2006) Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat. Cell Biol. 8: 870-876.
100. Li, X., Lee, Y. K, Jeng, J. C., Yen, Y., Schultz, D. C., Shih, H. M. and Ann, D. K. (2007) Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J. Biol. Chem. 282: 36177-36189.
101. Chai, B., Huang, J., Caims, B. R. and Laurent, B. C. (2005) Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19: 1656-1661.
102. Park, J. H., Park, E. J., Lee, H. S., Kim, S. J., Hur, S. K., Imbalzano, A. N. and Kwon, J. (2006) Mammalian SWI/SNF complexes facilitate DNA double-strand break repair by promoting gamma-H2AX induction. EMBO J. 25: 3986-3997.