53BP1: Function and mechanisms of focal recruitment

Biochemical Society Transactions

Volumn 37, Issue 4, 2009, Pages 897-904

  FitzGerald, Jennifer E ^a   Grenon, Muriel ^a   Lowndes, Noel F ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Dot1; Histone 2AX (H2AX); Histone methylation; Mediator of DNA damage checkpoint 1 (MDC1); P53 binding protein 1 (53BP1); Rad9

Indexed keywords

ADAPTOR PROTEIN; ATM PROTEIN; BRCA1 PROTEIN; CHECKPOINT KINASE 2; DNA; HISTONE H2AX; HISTONE H3; HISTONE H4; P53 BINDING PROTEIN 1; PROTEIN MDC1; PROTEIN RAD9; UNCLASSIFIED DRUG; HISTONE; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN; TRP53BP1 PROTEIN, MOUSE;

CARBOXY TERMINAL SEQUENCE; CELL CYCLE ARREST; CHROMATIN STRUCTURE; CONFERENCE PAPER; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HUMAN; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; METABOLISM; PHYSIOLOGY; REVIEW;

ANIMALS; DNA DAMAGE; DNA REPAIR; HISTONES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL;

EID: 70349308060     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0370897     Document Type: Conference Paper

References (90)

1. O'Driscoll, M. and Jeggo, P.A. (2005) The role of double-strand break repair: insights from human genetics. Nat. Rev. Genet. 7, 45-54
2. Kastan, M.B. and Bartek, J. (2004) Cell-cycle checkpoints and cancer. Nature 432, 316-323
3. d'Adda di Fagagna, F. (2008) Living on a break: cellular senescence as a DNA-damage response. Nat. Cancer Rev. 8, 512-522
4. Bartkova, J., Horejsi, Z., Koed, K., Kramer, A., Tort, F., Zieger, K., Guldberg, P., Sehested, M., Nesland, J.M., Lukas, C. et al. (2005) DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434, 864-870
5. Bartkova, J., Horejsi, Z., Sehested, M., Nesland, J.M., Rajpert-De Meyts, E., Skakkebaek, N.E., Stucki, M., Jackson, S., Lukas, J. and Bartek, J. (2007) DNA damage response mediators MDC1 and 53BP1: constitutive activation and aberrant loss in breast and lung cancer, but not in testicular germ cell tumours. Oncogene 26, 7414-7422
6. Gorgoulis, V.G., Vassiliou, L.V., Karakaidos, P., Zacharatos, P., Kotsinas, A., Liloglou, T., Venere, M., Ditullio, Jr, R.A., Kastrinakis, N.G., Levy, B. et al. (2005) Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434, 907-913
7. Harrison, J.C. and Haber, J.E. (2006) Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 40, 209-235
8. Nyberg, K.A., Michelson, R.J., Putman, C.W. and Weinert, T.A. (2002) Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36, 617-656
9. Rupnik, A., Grenon, M. and Lowndes, N. (2008) The MRN complex. Curr. Biol. 18, R455-R457
10. Stiff, T., O'Driscoll, M., Rief, N., Iwabuchi, K., Lobrich, M. and Jeggo, P.A. (2004) ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64, 2390-2396
11. Ward, I.M. and Chen, J. (2001) Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276, 47759-47762
12. Zhou, B.S. and Elledge, S.J. (2000) The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439
13. Li, L. and Zou, L. (2005) Sensing, signaling, and responding to DNA damage: organization of the checkpoint pathways in mammalian cells. J. Cell. Biochem. 94, 298-306
14. Koonin, E.V., Altschul, S.F. and Bork, P. (1996) BRCA1 protein products... functional motifs... Nat. Genet. 13, 266-268
15. Bork, P., Hofmann, K., Bucher, P., Neuwald, A.F., Altschul, S.F. and Koonin, E.V. (1997) A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. FASEB J. 11, 68-76
16. Minter-Dykhouse, K., Ward, I., Huen, M.S., Chen, J. and Lou, Z. (2008) Distinct versus overlapping functions of MDC1 and 53BP1 in DNA damage response and tumorigenesis. J. Cell Biol. 181, 727-735
17. Wilson, K.A. and Stern, D.F. (2008) NFBD1/MDC1, 53BP1 and BRCA1 have both redundant and unique roles in the ATM pathway. Cell Cycle 7, 3584-3594
18. Mochan, T.A., Venere, M., DiTullio, Jr, R.A. and Halazonetis, T.D. (2003) 53BP1 and NFBD1/MDC1-Nbs1 function in parallel interacting pathways activating ataxia-telangiectasia mutated (ATM) in response to DNA damage. Cancer Res. 63, 8586-8591
19. Hashizume, R., Fukuda, M., Maeda, I., Nishikawa, H., Oyake, D., Yabuki, Y., Ogata, H. and Ohta, T. (2001) The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer-derived mutation. J. Biol. Chem. 276, 14537-14540
20. Lukas, C., Melander, F., Stucki, M., Falck, J., Bekker-Jensen, S., Goldberg, M., Lerenthal, Y., Jackson, S.P., Bartek, J. and Lukas, J. (2004) Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23, 2674-2683
21. Alpha-Bazin, B., Lorphelin, A., Nozerand, N., Charier, G., Marchetti, C., Berenguer, F., Couprie, J., Gilquin, B., Zinn-Justin, S. and Quemeneur, E. (2005) Boundaries and physical characterization of a new domain shared between mammalian 53BP1 and yeast Rad9 checkpoint proteins. Protein Sci. 14, 1827-1839
22. Charier, G., Couprie, J., Alpha-Bazin, B., Meyer, V., Quemeneur, E., Guerois, R., Callebaut, I., Gilquin, B. and Zinn-Justin, S. (2004) The Tudor tandem of 53BP1: a new structural motif involved in DNA and RG-rich peptide binding. Structure 12, 1551-1562
23. Huyen, Y., Zgheib, O., Ditullio, Jr, R.A., Gorgoulis, V.G., Zacharatos, P., Petty, T.J., Sheston, E.A., Mellert, H.S., Stavridi, E.S. and Halazonetis, T.D. (2004) Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432, 406-411
24. Boisvert, F.M., Rhie, A., Richard, S. and Doherty, A.J. (2005) The GAR motif of 53BP1 is arginine methylated by PRMT1 and is necessary for 53BP1 DNA binding activity. Cell Cycle 4, 1834-1841
25. Adams, M.M., Wang, B., Xia, Z., Morales, J.C., Lu, X., Donehower, L.A., Bochar, D.A., Elledge, S.J. and Carpenter, P.B. (2005) 53BP1 oligomerization is independent of its methylation by PRMT1. Cell Cycle 4, 1854-1861
26. Ward, I.M., Minn, K., Jorda, K.G. and Chen, J. (2003) Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278, 19579-19582
27. Jowsey, P., Morrice, N.A., Hastie, C.J., McLauchlan, H., Toth, R. and Rouse, J. (2007) Characterisation of the sites of DNA damage-induced 53BP1 phosphorylation catalysed by ATM and ATR. DNA Repair 6, 1536-1544
28. Lee, H., Kwak, H.J., Cho, I.T., Park, S.H. and Lee, C.H. (2009) S1219 residue of 53BP1 is phosphorylated by ATM kinase upon DNA damage and required for proper execution of DNA damage response. Biochem. Biophys. Res. Commun. 378, 32-36
29. Munoz, I.M., Jowsey, P.A., Toth, R. and Rouse, J. (2007) Phospho-epitope binding by the BRCT domains of hPTIP controls multiple aspects of the cellular response to DNA damage. Nucleic Acids Res. 35, 5312-5322
30. Reference deleted
31. DiTullio, Jr, R.A., Mochan, T.A., Venere, M., Bartkova, J., Sehested, M., Bartek, J. and Halazonetis, T.D. (2002) 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat. Cell Biol. 4, 998-1002
32. Wang, B., Matsuoka, S., Carpenter, P.B. and Elledge, S.J. (2002) 53BP1, a mediator of the DNA damage checkpoint. Science 298, 1435-1438
33. Fernandez-Capetillo, O., Chen, H.T., Celeste, A., Ward, I., Romanienko, P.J., Morales, J.C., Naka, K., Xia, Z., Camerini-Otero, R.D., Motoyama, N. et al. (2002) DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4, 993-997
34. Morales, J.C., Xia, Z., Lu, T., Aldrich, M.B., Wang, B., Rosales, C., Kellems, R.E., Hittelman, W.N., Elledge, S.J. and Carpenter, P.B. (2003) Role for the BRCA1 C-terminal repeats (BRCT) protein 53BP1 in maintaining genomic stability. J. Biol. Chem. 278, 14971-14977
35. Nakamura, K., Sakai, W., Kawamoto, T., Bree, R.T., Lowndes, N.F., Takeda, S. and Taniguchi, Y. (2006) Genetic dissection of vertebrate 53BP1: a major role in non-homologous end joining of DNA double strand breaks. DNA Repair 5, 741-749
36. 1 without Ku70 or Artemis. Genes Cells 11, 935-948
37. Ward, I.M., Minn, K., van Deursen, J. and Chen, J. (2003) p53 binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 23, 2556-2563
38. Pellicioli, A. and Foiani, M. (2005) Signal transduction: how rad53 kinase is activated. Curr. Biol. 15, R769-R771
39. Saka, Y., Esashi, F., Matsusaka, T., Mochida, S. and Yanagida, M. (1997) Damage and replication checkpoint control in fission yeast is ensured by interactions of Crb2, a protein with BRCT motif, with Cut5 and Chk1. Genes Dev. 11, 3387-3400
40. Weinert, T.A. and Hartwell, L.H. (1988) The RAD9 gene controls the cell cycle response to DNA damage in Saccaromyces cerevisiae. Science 241, 317-322
41. Gilbert, C.S., Green, C.M. and Lowndes, N.F. (2001) Budding yeast Rad9 is an ATP-dependent Rad53 activating machine. Mol. Cell 8, 129-136
42. Blankley, R.T. and Lydall, D. (2004) A domain of Rad9 specifically required for activation of Chk1 in budding yeast. J. Cell Sci. 117, 601-608
43. Peng, A. and Chen, P.L. (2003) NFBD1, like 53BP1, is an early and redundant transducer mediating Chk2 phosphorylation in response to DNA damage. J. Biol. Chem. 278, 8873-8876
44. Iwabuchi, K., Basu, B.P., Kysela, B., Kurihara, T., Shibata, M., Guan, D., Cao, Y., Hamada, T., Imamura, K., Jeggo, P.A. et al. (2003) Potential role for 53BP1 in DNA end-joining repair through direct interaction with DNA. J. Biol. Chem. 278, 36487-36495
45. Riballo, E., Kuhne, M., Rief, N., Doherty, A., Smith, G.C., Recio, M.J., Reis, C., Dahm, K., Fricke, A., Krempler, A. et al. (2004) A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to γ-H2AX foci. Mol. Cell 16, 715-724
46. Goodarzi, A.A., Noon, A.T., Deckbar, D., Ziv, Y., Shiloh, Y., Lobrich, M. and Jeggo, P.A. (2008) ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell 31, 167-177
47. de la Torre-Ruiz, M. and Lowndes, N.F. (2000) The Saccharomyces cerevisiae DNA damage checkpoint is required for efficient repair of double strand breaks by non-homologous end joining. FEBS Lett. 467, 311-315
48. Dimitrova, N., Chen, Y.C., Spector, D.L. and de Lange, T. (2008) 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456, 524-528
49. Manis, J.P., Morales, J.C., Xia, Z., Kutok, J.L., Alt, F.W. and Carpenter, P.B. (2004) 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nat. Immunol. 5, 481-487
50. Ward, I.M., Reina-San-Martin, B., Olaru, A., Minn, K., Tamada, K., Lau, J.S., Cascalho, M., Chen, L., Nussenzweig, A., Livak, F. et al. (2004) 53BP1 is required for class switch recombination. J. Cell Biol. 165, 459-464
51. Difilippantonio, S., Gapud, E., Wong, N., Huang, C.Y., Mahowald, G., Chen, H.T., Kruhlak, M.J., Callen, E., Livak, F., Nussenzweig, M.C. et al. (2008) 53BP1 facilitates long-range DNA end-joining during V(D)J recombination. Nature 456, 529-533
52. Lo, K.W., Kan, H.M., Chan, L.N., Xu, W.G., Wang, K.P., Wu, Z., Sheng, M. and Zhang, M. (2005) The 8-kDa dynein light chain binds to p53-binding protein 1 and mediates DNA damage-induced p53 nuclear accumulation. J. Biol. Chem. 280, 8172-8179
53. Anderson, L., Henderson, C. and Adachi, Y. (2001) Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage. Mol. Cell. Biol. 21, 1719-1729
54. Xia, Z., Morales, J.C., Dunphy, W.G. and Carpenter, P.B. (2001) Negative cell cycle regulation and DNA damage-inducible phosphorylation of the BRCT protein 53BP1. J. Biol. Chem. 276, 2708-2718
55. Rappold, I., Iwabuchi, K., Date, T. and Chen, J. (2001) Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J. Cell Biol. 153, 613-620
56. Schultz, L.B., Chehab, N.H., Malikzay, A. and Halazonetis, T.D. (2000) p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol. 151, 1381-1390
57. Adams, M.M. and Carpenter, P.B. (2006) Tying the loose ends together in DNA double strand break repair with 53BP1. Cell Div. 1, 19
58. Celeste, A., Fernandez-Capetillo, O., Kruhlak, M.J., Pilch, D.R., Staudt, D.W., Lee, A., Bonner, R.F., Bonner, W.M. and Nussenzweig, A. (2003) Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5, 675-679
59. Bekker-Jensen, S., Lukas, C., Melander, F., Bartek, J. and Lukas, J. (2005) Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J. Cell Biol. 170, 201-211
60. 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. et al. (2006) MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell 21, 187-200
61. Stewart, G.S., Wang, B., Bignell, C.R., Taylor, A.M. and Elledge, S.J. (2003) MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421, 961-966
62. 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
63. Kolas, N.K., Chapman, J.R., Nakada, S., Ylanko, J., Chahwan, R., Sweeney, F.D., Panier, S., Mendez, M., Wildenhain, J., Thomson, T.M. et al. (2007) Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318, 1637-1640
64. 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
65. Botuyan, M.V., Lee, J., Ward, I.M., Kim, J.E., Thompson, J.R., Chen, J. and Mer, G. (2006) Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127, 1361-1373
66. 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
67. Rogakou, E.P., Boon, C., Redon, C. and Bonner, W.M. (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146, 905-916
68. Stucki, M. and Jackson, S.P. (2006) γH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair 5, 534-543
69. Ikura, T., Tashiro, S., Kakino, A., Shima, H., Jacob, N., Amunugama, R., Yoder, K., Izumi, S., Kuraoka, I., Tanaka, K. et al. (2007) DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 27, 7028-7040
70. Wang, B. and Elledge, S.J. (2007) Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl. Acad. Sci. U.S.A. 104, 20759-20763
71. Celeste, A., Petersen, S., Romanienko, P.J., Fernandez-Capetillo, O., Chen, H.T., Sedelnikova, O.A., Reina-San-Martin, B., Coppola, V., Meffre, E., Difilippantonio, M.J. et al. (2002) Genomic instability in mice lacking histone H2AX. Science 296, 922-927
72. Eliezer, Y., Argaman, L., Rhie, A., Doherty, A.J. and Goldberg, M. (2009) The direct interaction between 53BP1 and MDC1 is required for the recruitment of 53PB1 to sites of damage. J. Biol. Chem. 284, 426-435
73. Zgheib, O., Pataky, K., Brugger, J. and Halazonetis, T.D. (2009) An oligomerized 53BP1 tudor domain suffices for recognition of DNA double-strand breaks. Mol. Cell. Biol. 29, 1050-1058
74. Du, L.L., Moser, B.A. and Russell, P. (2004) Homo-oligomerization is the essential function of the tandem BRCT domains in the checkpoint protein Crb2. J. Biol. Chem. 279, 38409-38414
75. Soulier, J. and Lowndes, N.F. (1999) The BRCT domain of the S. cerevisiae checkpoint protein Rad9 mediates a Rad9-Rad9 interaction after DNA damage. Curr. Biol. 9, 551-554
76. Grenon, M., Costelloe, T., Jimeno, S., O'Shaughnessy, A., FitzGerald, J., Zgheib, O., Degerth, L. and Lowndes, N.F. (2007) Docking onto chromatin via the Saccharomyces cerevisiae Rad9 Tudor domain. Yeast 24, 105-119
77. Wysocki, R., Javaheri, A., Allard, S., Sha, F., Cote, J. and Kron, S.J. (2005) Role of Dot1-dependent histone H3 methylation in G1 and S phase DNA damage checkpoint functions of Rad9. Mol. Cell. Biol. 25, 8430-8443
78. Sanders, S.L., Portoso, M., Mata, J., Bahler, J., Allshire, R.C. and Kouzarides, T. (2004) Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119, 603-614
79. Allis, C.D., Berger, S.L., Cote, J., Dent, S., Jenuwien, T., Kouzarides, T., Pillus, L., Reinberg, D., Shi, Y., Shiekhattar, R. et al. (2007) New nomenclature for chromatin-modifying enzymes. Cell 131, 633-636
80. Giannattasio, M., Lazzaro, F., Plevani, P. and Muzi-Falconi, M. (2005) The DNA damage checkpoint response requires histone H2B ubiquitination by Rad6-Bre1 and H3 methylation by Dot1. J. Biol. Chem. 280, 9879-9886
81. Steger, D.J., Lefterova, M.I., Ying, L., Stonestrom, A.J., Schupp, M., Zhuo, D., Vakoc, A., Kim, J., Chen, J., Lazar, M.A. et al. (2008) DOT1L/ KMT4 recruitment and H3K79 methylation are ubiquitously coupled with gene transcription in mammalian cells. Mol. Cell. Biol. 28, 2825-2839
82. Yang, H., Pesavento, J.J., Starnes, T.W., Cryderman, D.E., Wallrath, L.L., Kelleher, N.L. and Mizzen, C.A. (2008) Preferential dimethylation of histone h4 lysine 20 by suv4-20. J. Biol. Chem. 283, 12085-12092
83. Schotta, G., Sengupta, R., Kubicek, S., Malin, S., Kauer, M., Callen, E., Celeste, A., Pagani, M., Opravil, S., De La Rosa-Velazquez, I.A. et al. (2008) A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev. 22, 2048-2061
84. Fang, J., Feng, Q., Ketel, C.S., Wang, H., Cao, R., Xia, L., Erdjument-Bromage, H., Tempst, P., Simon, J.A. and Zhang, Y. (2002) Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr. Biol. 12, 1086-1099
85. Du, L.L., Nakamura, T.M. and Russell, P. (2006) Histone modification-dependent and -independent pathways for recruitment of checkpoint protein Crb2 to double-strand breaks. Genes Dev. 20, 1583-1596
86. Toh, G.W., O'Shaughnessy A, M., Jimeno, S., Dobbie, I.M., Grenon, M., Maffini, S., O'Rorke, A. and Lowndes, N.F. (2006) Histone H2A phosphorylation and H3 methylation are required for a novel Rad9 DSB repair function following checkpoint activation. DNA Repair 5, 693-703
87. Costelloe, T., FitzGerald, J., Murphy, N., Flaus, A. and Lowndes, N.F. (2006) Chromatin modulation and the DNA damage response Exp. Cell Res. 312, 2677-2686
88. Ward, I., Kim, J.E., Minn, K., Chini, C.C., Mer, G. and Chen, J. (2006) The tandem BRCT domain of 53BP1 is not required for its repair function. J. Biol. Chem. 281, 38472-38477
89. Xie, A., Hartlerode, A., Stucki, M., Odate, S., Puget, N., Kwok, A., Nagaraju, G., Yan, C., Alt, F.W., Chen, J. et al. (2007) Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol. Cell 28, 1045-1057
90. Puddu, F., Granata, M., Di Nola, L., Balestrini, A., Piergiovanni, G., Lazzaro, F., Giannattasio, M., Plevani, P. and Muzi-Falconi, M. (2008) Phosphorylation of the budding yeast 9-1-1 complex is required for Dpb11 function in the full activation of the UV-induced DNA damage checkpoint. Mol. Cell. Biol. 28, 4782-4793