HP1α recruitment to DNA damage by p150CAF-1 promotes homologous recombination repair

Journal of Cell Biology

Volumn 193, Issue 1, 2011, Pages 81-95

  Baldeyron, Céline ^a,b,c   Soria, Gaston ^a,b   Roche, Danièle ^a,b   Cook, Adam J L ^a,b   Almouzni, Geneviève ^a,b  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

^c Translational Research Department   (France)

Author keywords

[No Author keywords available]

Indexed keywords

53BP1 PROTEIN; CHROMATIN ASSEMBLY FACTOR 1; HETEROCHROMATIN PROTEIN 1; NUCLEIC ACID BINDING PROTEIN; P150CAF 1 PROTEIN; PROTEIN SUBUNIT; RAD51 PROTEIN; UNCLASSIFIED DRUG; HETEROCHROMATIN SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP 1; HETEROCHROMATIN-SPECIFIC NONHISTONE CHROMOSOMAL PROTEIN HP-1; NONHISTONE PROTEIN;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; EUCHROMATIN; HETEROCHROMATIN; HOMOLOGOUS RECOMBINATION; LASER; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; CELL STRAIN 3T3; GENETICS; HUMAN; METABOLISM;

MAMMALIA;

ANIMALS; CELLS, CULTURED; CHROMATIN ASSEMBLY FACTOR-1; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA DAMAGE; DNA REPAIR; HUMANS; MICE; NIH 3T3 CELLS;

EID: 79955507697     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201101030     Document Type: Article

References (92)

1. Ahnesorg, P., P. Smith, and S.P. Jackson. 2006. XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell. 124:301-313. doi:10.1016/j.cell.2005.12.031
2. Ayoub, N., A.D. Jeyasekharan, J.A. Bernal, and A.R. Venkitaraman. 2008. HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response. Nature. 453:682-686. doi:10.1038/nature06875
3. Ayoub, N., A.D. Jeyasekharan, and A.R. Venkitaraman. 2009. Mobilization and recruitment of HP1: a bimodal response to DNA breakage. Cell Cycle. 8:2945-2950.
4. Bakkenist, C.J., and M.B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 421:499-506. doi:10.1038/nature01368
5. Bekker-Jensen, S., and N. Mailand. 2010. Assembly and function of DNA doublestrand break repair foci in mammalian cells. DNA Repair (Amst.). 9:1219-1228. doi:10.1016/j.dnarep.2010.09.010
6. Bekker-Jensen, S., C. Lukas, R. Kitagawa, F. Melander, M.B. Kastan, J. Bartek, and J. Lukas. 2006. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173:195-206. doi:10.1083/jcb.200510130
7. Bogliolo, M., A. Lyakhovich, E. Callén, M. Castellà, E. Cappelli, M.J. Ramírez, A. Creus, R. Marcos, R. Kalb, K. Neveling, et al. 2007. Histone H2AX and Fanconi anemia FANCD2 function in the same pathway to maintain chromosome stability. EMBO J. 26:1340-1351. doi:10.1038/sj.emboj.7601574
8. Bunting, S.F., E. Callén, N. Wong, H.T. Chen, F. Polato, A. Gunn, A. Bothmer, N. Feldhahn, O. Fernandez-Capetillo, L. Cao, et al. 2010. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell. 141:243-254. doi:10.1016/j.cell.2010.03.012
9. Chen, L., C.J. Nievera, A.Y. Lee, and X. Wu. 2008. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J. Biol. Chem. 283:7713-7720. doi:10.1074/jbc.M710245200
10. Corpet, A., and G. Almouzni. 2009. A histone code for the DNA damage response in mammalian cells? EMBO J. 28:1828-1830. doi:10.1038/emboj.2009.180
11. Cowell, I.G., N.J. Sunter, P.B. Singh, C.A. Austin, B.W. Durkacz, and M.J. Tilby. 2007. gammaH2AX foci form preferentially in euchromatin after ionisingradiation. PLoS ONE. 2:e1057. doi:10.1371/journal.pone.0001057
12. De Koning, L., A. Savignoni, C. Boumendil, H. Rehman, B. Asselain, X. Sastre-Garau, and G. Almouzni. 2009. Heterochromatin protein 1alpha: a hallmark of cell proliferation relevant to clinical oncology. EMBO Mol Med. 1:178-191. doi:10.1002/emmm.200900022
13. Difilippantonio, S., E. Gapud, N. Wong, C.Y. Huang, G. Mahowald, H.T. Chen, M.J. Kruhlak, E. Callen, F. Livak, M.C. Nussenzweig, et al. 2008. 53BP1 facilitates long-range DNA end-joining during V(D)J recombination. Nature. 456:529-533. doi:10.1038/nature07476
14. Dimitrova, N., Y.C. Chen, D.L. Spector, and T. de Lange. 2008. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature. 456:524-528. doi:10.1038/nature07433
15. Dinant, C., and M.S. Luijsterburg. 2009. The emerging role of HP1 in the DNA damage response. Mol. Cell. Biol. 29:6335-6340. doi:10.1128/MCB.01048-09
16. Drouet, J., C. Delteil, J. Lefrançois, P. Concannon, B. Salles, and P. Calsou. 2005. DNA-dependent protein kinase and XRCC4-DNA ligase IV mobilization in the cell in response to DNA double strand breaks. J. Biol. Chem. 280:7060-7069. doi:10.1074/jbc.M410746200
17. Essers, J., R.W. Hendriks, S.M. Swagemakers, C. Troelstra, J. de Wit, D. Bootsma, J.H. Hoeijmakers, and R. Kanaar. 1997. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell. 89:195-204. doi:10.1016/S0092-8674(00)80199-3
18. FitzGerald, J.E., M. Grenon, and N.F. Lowndes. 2009. 53BP1: function and mechanisms of focal recruitment. Biochem. Soc. Trans. 37:897-904. doi:10.1042/BST0370897
19. Garcia-Higuera, I., T. Taniguchi, S. Ganesan, M.S. Meyn, C. Timmers, J. Hejna, M. Grompe, and A.D. D'Andrea. 2001. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell. 7:249-262. doi:10.1016/S1097-2765(01)00173-3
20. Gérard, A., S.E. Polo, D. Roche, and G. Almouzni. 2006. Methods for studying chromatin assembly coupled to DNA repair. Methods Enzymol. 409:358-374. doi:10.1016/S0076-6879(05)09021-X
21. Goldberg, M., M. Stucki, J. Falck, D. D'Amours, D. Rahman, D. Pappin, J. Bartek, and S.P. Jackson. 2003. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature. 421:952-956. doi:10.1038/nature01445
22. Goodarzi, A.A., J.C. Jonnalagadda, P. Douglas, D. Young, R. Ye, G.B. Moorhead, S.P. Lees-Miller, and K.K. Khanna. 2004. Autophosphorylation of ataxiatelangiectasia mutated is regulated by protein phosphatase 2A. EMBO J. 23:4451-4461. doi:10.1038/sj.emboj.7600455
23. Goodarzi, A.A., A.T. Noon, D. Deckbar, Y. Ziv, Y. Shiloh, M. Löbrich, and P.A. Jeggo. 2008. ATM signaling facilitates repair of DNA doublestrand breaks associated with heterochromatin. Mol. Cell. 31:167-177. doi:10.1016/j.molcel.2008.05.017
24. Green, C.M., and G. Almouzni. 2003. Local action of the chromatin assembly factor CAF-1 at sites of nucleotide excision repair in vivo. EMBO J. 22:5163-5174. doi:10.1093/emboj/cdg478
25. Groth, A., D. Ray-Gallet, J.P. Quivy, J. Lukas, J. Bartek, and G. Almouzni. 2005. Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell. 17:301-311. doi:10.1016/j.molcel.2004.12.018
26. Groth, A., A. Corpet, A.J. Cook, D. Roche, J. Bartek, J. Lukas, and G. Almouzni. 2007a. Regulation of replication fork progression through histone supply and demand. Science. 318:1928-1931. doi:10.1126/science.1148992
27. Groth, A., W. Rocha, A. Verreault, and G. Almouzni. 2007b. Chromatin challenges during DNA replication and repair. Cell. 128:721-733. doi:10.1016/j.cell.2007.01.030
28. Hashiguchi, K., Y. Matsumoto, and A. Yasui. 2007. Recruitment of DNA repair synthesis machinery to sites of DNA damage/repair in living human cells. Nucleic Acids Res. 35:2913-2923. doi:10.1093/nar/gkm115
29. Hoeijmakers, J.H. 2001. DNA repair mechanisms. Maturitas. 38:17-22, discussion:22-23. doi:10.1016/S0378-5122(00)00188-2
30. Holthausen, J.T., C. Wyman, and R. Kanaar. 2010. Regulation of DNA strand exchange in homologous recombination. DNA Repair (Amst.). 9:1264-1272. doi:10.1016/j.dnarep.2010.09.014
31. Houlard, M., S. Berlivet, A.V. Probst, J.P. Quivy, P. Héry, G. Almouzni, and M. Gérard. 2006. CAF-1 is essential for heterochromatin organization in pluripotent embryonic cells. PLoS Genet. 2:e181. doi:10.1371/journal.pgen.0020181
32. Inoue, A., J. Hyle, M.S. Lechner, and J.M. Lahti. 2008. Perturbation of HP1 localization and chromatin binding ability causes defects in sister-chromatid cohesion. Mutat. Res. 657:48-55.
33. Ishii, S., A. Koshiyama, F.N. Hamada, T.Y. Nara, K. Iwabata, K. Sakaguchi, and S.H. Namekawa. 2008. Interaction between Lim15/Dmc1 and the homologue of the large subunit of CAF-1: a molecular link between recombination and chromatin assembly during meiosis. FEBS J. 275:2032-2041. doi:10.1111/j.1742-4658.2008.06357.x
34. Jackson, S.P., and J. Bartek. 2009. The DNA-damage response in human biology and disease. Nature. 461:1071-1078. doi:10.1038/nature08467
35. Jin, S., and D.T. Weaver. 1997. Double-strand break repair by Ku70 requires heterodimerization with Ku80 and DNA binding functions. EMBO J. 16:6874-6885. doi:10.1093/emboj/16.22.6874
36. Kim, J.A., M. Kruhlak, F. Dotiwala, A. Nussenzweig, and J.E. Haber. 2007. Heterochromatin is refractory to gamma-H2AX modification in yeast and mammals. J. Cell Biol. 178:209-218. doi:10.1083/jcb.200612031
37. Kimura, H., and P.R. Cook. 2001. Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J. Cell Biol. 153:1341-1353. doi:10.1083/jcb.153.7.1341
38. Kinner, A., W. Wu, C. Staudt, and G. Iliakis. 2008. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36:5678-5694. doi:10.1093/nar/gkn550
39. Kornberg, R.D., and A. Klug. 1981. The nucleosome. Sci. Am. 244:52-64. doi:10.1038/scientificamerican0281-52
40. Kruhlak, M.J., A. Celeste, G. Dellaire, O. Fernandez-Capetillo, W.G. Müller, J.G. McNally, D.P. Bazett-Jones, and A. Nussenzweig. 2006. Changes in chromatin structure and mobility in living cells at sites of DNA doublestrand breaks. J. Cell Biol. 172:823-834. doi:10.1083/jcb.200510015
41. Le Douarin, B., A.L. Nielsen, J.M. Garnier, H. Ichinose, F. Jeanmougin, R. Losson, and P. Chambon. 1996. A possible involvement of TIF1 alpha and TIF1 beta in the epigenetic control of transcription by nuclear receptors. EMBO J. 15:6701-6715.
42. Lewis, L.K., G. Karthikeyan, J. Cassiano, and M.A. Resnick. 2005. Reduction of nucleosome assembly during new DNA synthesis impairs both major pathways of double-strand break repair. Nucleic Acids Res. 33:4928-4939. doi:10.1093/nar/gki806
43. Lisby, M., and R. Rothstein. 2009. Choreography of recombination proteins during the DNA damage response. DNA Repair (Amst.). 8:1068-1076. doi:10.1016/j.dnarep.2009.04.007
44. Lou, Z., C.C. Chini, K. Minter-Dykhouse, and J. Chen. 2003. Mediator of DNA damage checkpoint protein 1 regulates BRCA1 localization and phosphorylation in DNA damage checkpoint control. J. Biol. Chem. 278:13599-13602. doi:10.1074/jbc.C300060200
45. Loyola, A., H. Tagami, T. Bonaldi, D. Roche, J.P. Quivy, A. Imhof, Y. Nakatani, S.Y. Dent, and G. Almouzni. 2009. The HP1alpha-CAF1-SetDB1-containing complex provides H3K9me1 for Suv39-mediated K9me3 in pericentric heterochromatin. EMBO Rep. 10:769-775. doi:10.1038/embor.2009.90
46. Luijsterburg, M.S., C. Dinant, H. Lans, J. Stap, E. Wiernasz, S. Lagerwerf, D.O. Warmerdam, M. Lindh, M.C. Brink, J.W. Dobrucki, et al. 2009. Heterochromatin protein 1 is recruited to various types of DNA damage. J. Cell Biol. 185:577-586. doi:10.1083/jcb.200810035
47. Lukas, C., J. Falck, J. Bartkova, J. Bartek, and J. Lukas. 2003. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat. Cell Biol. 5:255-260. doi:10.1038/ncb945
48. Mailand, N., S. Bekker-Jensen, H. Faustrup, F. Melander, J. Bartek, C. Lukas, and J. Lukas. 2007. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell. 131:887-900. doi:10.1016/j.cell.2007.09.040
49. Maison, C., and G. Almouzni. 2004. HP1 and the dynamics of heterochromatin maintenance. Nat. Rev. Mol. Cell Biol. 5:296-304. doi:10.1038/nrm1355
50. Maison, C., D. Bailly, A.H. Peters, J.P. Quivy, D. Roche, A. Taddei, M. Lachner, T. Jenuwein, and G. Almouzni. 2002. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30:329-334. doi:10.1038/ng843
51. Maison, C., D. Bailly, D. Roche, R.M. de Oca, A.V. Probst, I. Vassias, F. Dingli, B. Lombard, D. Loew, J.P. Quivy, and G. Almouzni. 2011. SUMOylation promotes de novo targeting of HP1( to pericentric heterochromatin. Nat. Genet. 43:220-227. doi:10.1038/ng.765
52. Mari, P.O., B.I. Florea, S.P. Persengiev, N.S. Verkaik, H.T. Brüggenwirth, M. Modesti, G. Giglia-Mari, K. Bezstarosti, J.A. Demmers, T.M. Luider, et al. 2006. Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc. Natl. Acad. Sci. USA. 103:18597-18602. doi:10.1073/pnas.0609061103
53. Martini, E., D.M. Roche, K. Marheineke, A. Verreault, and G. Almouzni. 1998. Recruitment of phosphorylated chromatin assembly factor 1 to chromatin after UV irradiation of human cells. J. Cell Biol. 143:563-575. doi:10.1083/jcb.143.3.563
54. McManus, K.J., and M.J. Hendzel. 2005. ATM-dependent DNA damageindependent mitotic phosphorylation of H2AX in normally growing mammalian cells. Mol. Biol. Cell. 16:5013-5025. doi:10.1091/mbc.E05-01-0065
55. Misteli, T., and E. Soutoglou. 2009. The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat. Rev. Mol. Cell Biol. 10:243-254. doi:10.1038/nrm2651
56. Moggs, J.G., P. Grandi, J.P. Quivy, Z.O. Jónsson, U. Hübscher, P.B. Becker, and G. Almouzni. 2000. A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol. Cell. Biol. 20:1206-1218. doi:10.1128/MCB.20.4.1206-1218.2000
57. Moné, M.J., M. Volker, O. Nikaido, L.H. Mullenders, A.A. van Zeeland, P.J. Verschure, E.M. Manders, and R. van Driel. 2001. Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep. 2:1013-1017. doi:10.1093/embo-reports/kve224
58. Mortusewicz, O., and H. Leonhardt. 2007. XRCC1 and PCNA are loading platforms with distinct kinetic properties and different capacities to respond to multiple DNA lesions. BMC Mol. Biol. 8:81. doi:10.1186/1471-2199-8-81
59. Murzina, N., A. Verreault, E. Laue, and B. Stillman. 1999. Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol. Cell. 4:529-540. doi:10.1016/S1097-2765(00)80204-X
60. Obuse, C., O. Iwasaki, T. Kiyomitsu, G. Goshima, Y. Toyoda, and M. Yanagida. 2004. A conserved Mis12 centromere complex is linked to heterochromatic HP1 and outer kinetochore protein Zwint-1. Nat. Cell Biol. 6:1135-1141. doi:10.1038/ncb1187
61. Peters, A.H., D. O'Carroll, H. Scherthan, K. Mechtler, S. Sauer, C. Schöfer, K. Weipoltshammer, M. Pagani, M. Lachner, A. Kohlmaier, et al. 2001. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell. 107:323-337. doi:10.1016/S0092-8674(01)00542-6
62. Pierce, A.J., P. Hu, M. Han, N. Ellis, and M. Jasin. 2001. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15:3237-3242. doi:10.1101/gad.946401
63. Polo, S.E., and G. Almouzni. 2007. DNA damage leaves its mark on chromatin. Cell Cycle. 6:2355-2359. doi:10.4161/cc.6.19.4756
64. Polo, S.E., D. Roche, and G. Almouzni. 2006. New histone incorporation marks sites of UV repair in human cells. Cell. 127:481-493. doi:10.1016/j.cell.2006.08.049
65. Pommier, Y., C. Redon, V.A. Rao, J.A. Seiler, O. Sordet, H. Takemura, S. Antony, L. Meng, Z. Liao, G. Kohlhagen, et al. 2003. Repair of and checkpoint response to topoisomerase I-mediated DNA damage. Mutat. Res. 532:173-203. doi:10.1016/j.mrfmmm.2003.08.016
66. Quivy, J.P., D. Roche, D. Kirschner, H. Tagami, Y. Nakatani, and G. Almouzni. 2004. A CAF-1 dependent pool of HP1 during heterochromatin duplication. EMBO J. 23:3516-3526. doi:10.1038/sj.emboj.7600362
67. Quivy, J.P., A. Gérard, A.J. Cook, D. Roche, and G. Almouzni. 2008. The HP1-p150/CAF-1 interaction is required for pericentric heterochromatin replication and S-phase progression in mouse cells. Nat. Struct. Mol. Biol. 15:972-979. doi:10.1038/nsmb.1470
68. Rogakou, E.P., D.R. Pilch, A.H. Orr, V.S. Ivanova, and W.M. Bonner. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273:5858-5868. doi:10.1074/jbc.273.10.5858
69. Rogakou, E.P., C. Boon, C. Redon, and W.M. Bonner. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:905-916. doi:10.1083/jcb.146.5.905
70. Rolef Ben-Shahar, T., A.G. Castillo, M.J. Osborne, K.L. Borden, J. Kornblatt, and A. Verreault. 2009. Two fundamentally distinct PCNA interaction peptides contribute to chromatin assembly factor 1 function. Mol. Cell. Biol. 29:6353-6365. doi:10.1128/MCB.01051-09
71. Ryan, R.F., D.C. Schultz, K. Ayyanathan, P.B. Singh, J.R. Friedman, W.J. Fredericks, and F.J. Rauscher III. 1999. KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Krüppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol. Cell. Biol. 19:4366-4378.
72. 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. doi:10.1038/nature06337
73. Schultz, L.B., N.H. Chehab, A. Malikzay, and T.D. Halazonetis. 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. doi:10.1083/jcb.151.7.1381
74. Scully, R., S. Ganesan, M. Brown, J.A. De Caprio, S.A. Cannistra, J. Feunteun, S. Schnitt, and D.M. Livingston. 1996. Location of BRCA1 in human breast and ovarian cancer cells. Science. 272:123-126. doi:10.1126/science.272.5258.123
75. Shibahara, K., and B. Stillman. 1999. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell. 96:575-585. doi:10.1016/S0092-8674(00)80661-3
76. Song, Y., F. He, G. Xie, X. Guo, Y. Xu, Y. Chen, X. Liang, I. Stagljar, D. Egli, J. Ma, and R. Jiao. 2007. CAF-1 is essential for Drosophila development and involved in the maintenance of epigenetic memory. Dev. Biol. 311:213-222. doi:10.1016/j.ydbio.2007.08.039
77. Soria, G., J. Speroni, O.L. Podhajcer, C. Prives, and V. Gottifredi. 2008. p21 differentially regulates DNA replication and DNA-repair-associated processes after UV irradiation. J. Cell Sci. 121:3271-3282. doi:10.1242/jcs.027730
78. Soria, G., L. Belluscio, W.A. van Cappellen, R. Kanaar, J. Essers, and V. Gottifredi. 2009. DNA damage induced Pol eta recruitment takes place independently of the cell cycle phase. Cell Cycle. 8:3340-3348. doi:10.4161/cc.8.20.9836
79. Soutoglou, E., J.F. Dorn, K. Sengupta, M. Jasin, A. Nussenzweig, T. Ried, G. Danuser, and T. Misteli. 2007. Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol. 9:675-682. doi:10.1038/ncb1591
80. Stucki, M., J.A. Clapperton, D. Mohammad, M.B. Yaffe, S.J. Smerdon, and S.P. Jackson. 2005. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell. 123:1213-1226. doi:10.1016/j.cell.2005.09.038
81. Taniguchi, T., I. Garcia-Higuera, P.R. Andreassen, R.C. Gregory, M. Grompe, and A.D. D'Andrea. 2002. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood. 100:2414-2420. doi:10.1182/blood-2002-01-0278
82. Thiru, A., D. Nietlispach, H.R. Mott, M. Okuwaki, D. Lyon, P.R. Nielsen, M. Hirshberg, A. Verreault, N.V. Murzina, and E.D. Laue. 2004. Structural basis of HP1/PXVXL motif peptide interactions and HP1 localisation to heterochromatin. EMBO J. 23:489-499. doi:10.1038/sj.emboj.7600088
83. van Attikum, H., and S.M. Gasser. 2009. Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol. 19:207-217. doi:10.1016/j.tcb.2009.03.001
84. van Gent, D.C., J.H. Hoeijmakers, and R. Kanaar. 2001. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2:196-206. doi:10.1038/35056049
85. van Veelen, L.R., J. Essers, M.W. van de Rakt, H. Odijk, A. Pastink, M.Z. Zdzienicka, C.C. Paulusma, and R. Kanaar. 2005. Ionizing radiationinduced foci formation of mammalian Rad51 and Rad54 depends on the Rad51 paralogs, but not on Rad52. Mutat. Res. 574:34-49. doi:10.1016/j.mrfmmm.2005.01.020
86. Wang, H., L. Wang, H. Erdjument-Bromage, M. Vidal, P. Tempst, R.S. Jones, and Y. Zhang. 2004. Role of histone H2A ubiquitination in Polycomb silencing. Nature. 431:873-878. doi:10.1038/nature02985
87. Wyman, C., and R. Kanaar. 2006. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 40:363-383. doi:10.1146/annurev.genet.40.110405.090451
88. Xie, A., A. Hartlerode, M. Stucki, S. Odate, N. Puget, A. Kwok, G. Nagaraju, C. Yan, F.W. Alt, J. Chen, et al. 2007. Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol. Cell. 28:1045-1057. doi:10.1016/j.molcel.2007.12.005
89. Yu, X., and J. Chen. 2004. DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol. Cell. Biol. 24:9478-9486. doi:10.1128/MCB.24.21.9478-9486.2004
90. Yu, X., L.C. Wu, A.M. Bowcock, A. Aronheim, and R. Baer. 1998. The C-terminal (BRCT) domains of BRCA1 interact in vivo with CtIP, a protein implicated in the CtBP pathway of transcriptional repression. J. Biol. Chem. 273:25388-25392. doi:10.1074/jbc.273.39.25388
91. Zarebski, M., E. Wiernasz, and J.W. Dobrucki. 2009. Recruitment of heterochromatin protein 1 to DNA repair sites. Cytometry A. 75:619-625.
92. Ziv, Y., D. Bielopolski, Y. Galanty, C. Lukas, Y. Taya, D.C. Schultz, J. Lukas, S. Bekker-Jensen, J. Bartek, and Y. Shiloh. 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. doi:10.1038/ncb1446