Dual role of CDKs in DNA repair: To be, or not to be

DNA Repair

Volumn 8, Issue 1, 2009, Pages 6-18

  Yata, Keiko ^a   Esashi, Fumiko ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Cell cycle; Cyclin dependent kinase; Double strand break repair; Homologous recombination; Repair regulation

Indexed keywords

BINDING PROTEIN; BRCA1 PROTEIN; CYCLIN DEPENDENT KINASE; PROTEIN P53; RAD51 PROTEIN; RECQ HELICASE; REPLICATION FACTOR A;

CELL CYCLE; COMPLEX FORMATION; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME REGULATION; HOMOLOGOUS RECOMBINATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TARGETING; REVIEW;

ANIMALS; BRCA2 PROTEIN; CELL CYCLE; CELL DIVISION; CYCLIN-DEPENDENT KINASES; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; HUMANS; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; RECQ HELICASES; REPLICATION PROTEIN A; TUMOR SUPPRESSOR PROTEIN P53;

EID: 56549096273     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.09.002     Document Type: Review

References (138)

1. Russell P., and Nurse P. Schizosaccharomyces pombe and Saccharomyces cerevisiae: a look at yeasts divided. Cell 45 (1986) 781-782
2. Lee M., and Nurse P. Cell cycle control genes in fission yeast and mammalian cells. Trends Genet. 4 (1988) 287-290
3. Lee M.G., and Nurse P. Complementation used to clone a human homologue of the fission yeast cell cycle control gene cdc2. Nature 327 (1987) 31-35
4. Tsai L.H., Harlow E., and Meyerson M. Isolation of the human cdk2 gene that encodes the cyclin A- and adenovirus E1A-associated p33 kinase. Nature 353 (1991) 174-177
5. Elledge S.J., and Spottswood M.R. A new human p34 protein kinase, CDK2, identified by complementation of a cdc28 mutation in Saccharomyces cerevisiae, is a homolog of Xenopus Eg1. EMBO J. 10 (1991) 2653-2659
6. Malumbres M., and Barbacid M. Mammalian cyclin-dependent kinases. Trends Biochem. Sci. 30 (2005) 630-641
7. Evans T., Rosenthal E.T., Youngblom J., Distel D., and Hunt T. Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33 (1983) 389-396
8. Murray A.W., and Kirschner M.W. Cyclin synthesis drives the early embryonic cell cycle. Nature 339 (1989) 275-280
9. Murray A.W. Recycling the cell cycle: cyclins revisited. Cell 116 (2004) 221-234
10. Dunphy W.G. The decision to enter mitosis. Trends Cell Biol. 4 (1994) 202-207
11. Bulavin D.V., Higashimoto Y., Demidenko Z.N., Meek S., Graves P., Phillips C., Zhao H., Moody S.A., Appella E., Piwnica-Worms H., et al. Dual phosphorylation controls Cdc25 phosphatases and mitotic entry. Nat. Cell Biol. 5 (2003) 545-551
12. Gu Y., Rosenblatt J., and Morgan D.O. Cell cycle regulation of CDK2 activity by phosphorylation of Thr160 and Tyr15. EMBO J. 11 (1992) 3995-4005
13. Nigg E.A. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays 17 (1995) 471-480
14. Ubersax J.A., Woodbury E.L., Quang P.N., Paraz M., Blethrow J.D., Shah K., Shokat K.M., and Morgan D.O. Targets of the cyclin-dependent kinase Cdk1. Nature 425 (2003) 859-864
15. Songyang Z., Blechner S., Hoagland N., Hoekstra M.F., Piwnica-Worms H., and Cantley L.C. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol. 4 (1994) 973-982
16. Diffley J.F. Regulation of early events in chromosome replication. Curr. Biol. 14 (2004) R778-786
17. Zou L., and Stillman B. Formation of a preinitiation complex by S-phase cyclin CDK-dependent loading of Cdc45p onto chromatin. Science 280 (1998) 593-596
18. Petersen B.O., Wagener C., Marinoni F., Kramer E.R., Melixetian M., Lazzerini Denchi E., Gieffers C., Matteucci C., Peters J.M., and Helin K. Cell cycle- and cell growth-regulated proteolysis of mammalian CDC6 is dependent on APC-CDH1. Genes Dev. 14 (2000) 2330-2343
19. Sugimoto N., Tatsumi Y., Tsurumi T., Matsukage A., Kiyono T., Nishitani H., and Fujita M. Cdt1 phosphorylation by cyclin A-dependent kinases negatively regulates its function without affecting geminin binding. J. Biol. Chem. 279 (2004) 19691-19697
20. Holt L.J., Krutchinsky A.N., and Morgan D.O. Positive feedback sharpens the anaphase switch. Nature 454 (2008) 353-357
21. Sullivan M., and Morgan D.O. Finishing mitosis, one step at a time. Nat. Rev. Mol. Cell Biol. 8 (2007) 894-903
22. Lindahl T. Instability and decay of the primary structure of DNA. Nature 362 (1993) 709-715
23. Khanna K.K., and Jackson S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27 (2001) 247-254
24. Weinert T.A., Kiser G.L., and Hartwell L.H. Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev. 8 (1994) 652-665
25. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15 (2001) 2177-2196
26. Durocher D., and Jackson S.P. DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme?. Curr. Opin. Cell Biol. 13 (2001) 225-231
27. Harper J.W., and Elledge S.J. The DNA damage response: ten years after. Mol. Cell 28 (2007) 739-745
28. Bakkenist C.J., and Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421 (2003) 499-506
29. Berkovich E., Monnat Jr. R.J., and Kastan M.B. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 9 (2007) 683-690
30. Mordes D.A., Glick G.G., Zhao R., and Cortez D. TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev. 22 (2008) 1478-1489
31. Jazayeri A., Falck J., Lukas C., Bartek J., Smith G.C., Lukas J., and Jackson S.P. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8 (2006) 37-45
32. Mailand N., Falck J., Lukas C., Syljuasen R.G., Welcker M., Bartek J., and Lukas J. Rapid destruction of human Cdc25A in response to DNA damage. Science 288 (2000) 1425-1429
33. Mailand N., Podtelejnikov A.V., Groth A., Mann M., Bartek J., and Lukas J. Regulation of G(2)/M events by Cdc25A through phosphorylation-dependent modulation of its stability. EMBO J. 21 (2002) 5911-5920
34. Agarwal S., Tafel A.A., and Kanaar R. DNA double-strand break repair and chromosome translocations. DNA Repair (Amst.) 5 (2006) 1075-1081
35. Smith G.C., and Jackson S.P. The DNA-dependent protein kinase. Genes Dev. 13 (1999) 916-934
36. Gottlieb T.M., and Jackson S.P. The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell 72 (1993) 131-142
37. Goodarzi A.A., Yu Y., Riballo E., Douglas P., Walker S.A., Ye R., Harer C., Marchetti C., Morrice N., Jeggo P.A., et al. DNA-PK autophosphorylation facilitates Artemis endonuclease activity. EMBO J. 25 (2006) 3880-3889
38. Ahnesorg P., Smith P., and Jackson S.P. XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 124 (2006) 301-313
39. Drouet J., Delteil C., Lefrancois J., Concannon P., Salles B., and Calsou P. DNA-dependent protein kinase and XRCC4-DNA ligase IV mobilization in the cell in response to DNA double strand breaks. J. Biol. Chem. 280 (2005) 7060-7069
40. Drouet J., Frit P., Delteil C., de Villartay J.P., Salles B., and Calsou P. Interplay between Ku, Artemis, and the DNA-dependent protein kinase catalytic subunit at DNA ends. J. Biol. Chem. 281 (2006) 27784-27793
41. West S.C. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4 (2003) 435-445
42. Wyman C., and Kanaar R. Homologous recombination: down to the wire. Curr. Biol. 14 (2004) R629-631
43. Williams R.S., and Tainer J.A. A nanomachine for making ends meet: MRN is a flexing scaffold for the repair of DNA double-strand breaks. Mol. Cell 19 (2005) 724-726
44. Moreau S., Morgan E.A., and Symington L.S. Overlapping functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 nucleases in DNA metabolism. Genetics 159 (2001) 1423-1433
45. Clerici M., Mantiero D., Lucchini G., and Longhese M.P. The Saccharomyces cerevisiae Sae2 protein promotes resection and bridging of double strand break ends. J. Biol. Chem. 280 (2005) 38631-38638
46. Sartori A.A., Lukas C., Coates J., Mistrik M., Fu S., Bartek J., Baer R., Lukas J., and Jackson S.P. Human CtIP promotes DNA end resection. Nature 450 (2007) 509-514
47. Limbo O., Chahwan C., Yamada Y., de Bruin R.A., Wittenberg C., and Russell P. Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell 28 (2007) 134-146
48. Furuse M., Nagase Y., Tsubouchi H., Murakami-Murofushi K., Shibata T., and Ohta K. Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J. 17 (1998) 6412-6425
49. Paull T.T., and Gellert M. The 3' to 5' exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell 1 (1998) 969-979
50. Trujillo K.M., Yuan S.S., Lee E.Y., and Sung P. Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95. J. Biol. Chem. 273 (1998) 21447-21450
51. Moreau S., Ferguson J.R., and Symington L.S. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19 (1999) 556-566
52. Haber J.E. The many interfaces of Mre11. Cell 95 (1998) 583-586
53. Petrini J.H. The mammalian Mre11-Rad50-nbs1 protein complex: integration of functions in the cellular DNA-damage response. Am. J. Hum. Genet. 64 (1999) 1264-1269
54. Wu X., Petrini J.H., Heine W.F., Weaver D.T., Livingston D.M., and Chen J. Independence of R/M/N focus formation and the presence of intact BRCA1. Science 289 (2000) 11
55. Lengsfeld B.M., Rattray A.J., Bhaskara V., Ghirlando R., and Paull T.T. Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell 28 (2007) 638-651
56. Benson F.E., Baumann P., and West S.C. Synergistic actions of Rad51 and Rad52 in recombination and DNA repair. Nature 391 (1998) 401-404
57. New J.H., Sugiyama T., Zaitseva E., and Kowalczykowski S.C. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391 (1998) 407-410
58. Petukhova G., Stratton S., and Sung P. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393 (1998) 91-94
59. Moynahan M.E., Chiu J.W., Koller B.H., and Jasin M. Brca1 controls homology-directed DNA repair. Mol. Cell 4 (1999) 511-518
60. Moynahan M.E., Pierce A.J., and Jasin M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell 7 (2001) 263-272
61. Modesti M., Budzowska M., Baldeyron C., Demmers J.A., Ghirlando R., and Kanaar R. RAD51AP1 is a structure-specific DNA binding protein that stimulates joint molecule formation during RAD51-mediated homologous recombination. Mol. Cell 28 (2007) 468-481
62. Rodrigue A., Lafrance M., Gauthier M.C., McDonald D., Hendzel M., West S.C., Jasin M., and Masson J.Y. Interplay between human DNA repair proteins at a unique double-strand break in vivo. EMBO J. 25 (2006) 222-231
63. Bugreev D.V., Yu X., Egelman E.H., and Mazin A.V. Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev. 21 (2007) 3085-3094
64. Hu Y., Raynard S., Sehorn M.G., Lu X., Bussen W., Zheng L., Stark J.M., Barnes E.L., Chi P., Janscak P., et al. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev. 21 (2007) 3073-3084
65. Heyer W.D., Ehmsen K.T., and Solinger J.A. Holliday junctions in the eukaryotic nucleus: resolution in sight?. Trends Biochem. Sci. 28 (2003) 548-557
66. Wu L., and Hickson I.D. DNA helicases required for homologous recombination and repair of damaged replication forks. Annu. Rev. Genet. 40 (2006) 279-306
67. Unal E., Heidinger-Pauli J.M., and Koshland D. DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317 (2007) 245-248
68. Strom L., Karlsson C., Lindroos H.B., Wedahl S., Katou Y., Shirahige K., and Sjogren C. Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science 317 (2007) 242-245
69. Unal E., Heidinger-Pauli J.M., Kim W., Guacci V., Onn I., Gygi S.P., and Koshland D.E. A molecular determinant for the establishment of sister chromatid cohesion. Science 321 (2008) 566-569
70. Ben-Shahar T.R., Heeger S., Lehane C., East P., Flynn H., Skehel M., and Uhlmann F. Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion. Science 321 (2008) 563-566
71. Zhang J., Shi X., Li Y., Kim B.J., Jia J., Huang Z., Yang T., Fu X., Jung S.Y., Wang Y., et al. Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. Mol. Cell 31 (2008) 143-151
72. Hou F., and Zou H. Two human orthologues of Eco1/Ctf7 acetyltransferases are both required for proper sister-chromatid cohesion. Mol. Biol. Cell 16 (2005) 3908-3918
73. Watrin E., and Peters J.M. Cohesin and DNA damage repair. Exp. Cell Res. 312 (2006) 2687-2693
74. Richardson C., Stark J.M., Ommundsen M., and Jasin M. Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability. Oncogene 23 (2004) 546-553
75. van Gent D.C., Hoeijmakers J.H., and Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2 (2001) 196-206
76. Bishop A.J., and Schiestl R.H. Homologous recombination and its role in carcinogenesis. J. Biomed. Biotechnol. 2 (2002) 75-85
77. Zierhut C., and Diffley J.F. Break dosage, cell cycle stage and DNA replication influence DNA double strand break response. EMBO J. 27 (2008) 1875-1885
78. Maggiorella L., Deutsch E., Frascogna V., Chavaudra N., Jeanson L., Milliat F., Eschwege F., and Bourhis J. Enhancement of radiation response by roscovitine in human breast carcinoma in vitro and in vivo. Cancer Res. 63 (2003) 2513-2517
79. Deans A.J., Khanna K.K., McNees C.J., Mercurio C., Heierhorst J., and McArthur G.A. Cyclin-dependent kinase 2 functions in normal DNA repair and is a therapeutic target in BRCA1-deficient cancers. Cancer Res. 66 (2006) 8219-8226
80. Ongkeko W., Ferguson D.J., Harris A.L., and Norbury C. Inactivation of Cdc2 increases the level of apoptosis induced by DNA damage. J. Cell Sci. 108 (1995) 2897-2904
81. Caspari T., Murray J.M., and Carr A.M. Cdc2-cyclin B kinase activity links Crb2 and Rqh1-topoisomerase III. Genes Dev. 16 (2002) 1195-1208
82. Ira G., Pellicioli A., Balijja A., Wang X., Fiorani S., Carotenuto W., Liberi G., Bressan D., Wan L., Hollingsworth N.M., et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431 (2004) 1011-1017
83. Ferreira M.G., and Cooper J.P. Two modes of DNA double-strand break repair are reciprocally regulated through the fission yeast cell cycle. Genes Dev. 18 (2004) 2249-2254
84. Sonoda E., Hochegger H., Saberi A., Taniguchi Y., and Takeda S. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst.) 5 (2006) 1021-1029
85. Linding R., Jensen L.J., Ostheimer G.J., van Vugt M.A., Jorgensen C., Miron I.M., Diella F., Colwill K., Taylor L., Elder K., et al. Systematic discovery of in vivo phosphorylation networks. Cell 129 (2007) 1415-1426
86. Manke I.A., Lowery D.M., Nguyen A., and Yaffe M.B. BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302 (2003) 636-639
87. Yu X., Chini C.C., He M., Mer G., and Chen J. The BRCT domain is a phospho-protein binding domain. Science 302 (2003) 639-642
88. Saka Y., Esashi F., Matsusaka T., Mochida S., and Yanagida M. 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 (1997) 3387-3400
89. Kilkenny M.L., Dore A.S., Roe S.M., Nestoras K., Ho J.C., Watts F.Z., and Pearl L.H. Structural and functional analysis of the Crb2-BRCT2 domain reveals distinct roles in checkpoint signaling and DNA damage repair. Genes Dev. 22 (2008) 2034-2047
90. 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. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432 (2004) 406-411
91. Botuyan M.V., Lee J., Ward I.M., Kim J.E., Thompson J.R., Chen J., and Mer G. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127 (2006) 1361-1373
92. Esashi F., and Yanagida M. Cdc2 phosphorylation of Crb2 is required for reestablishing cell cycle progression after the damage checkpoint. Mol. Cell 4 (1999) 167-174
93. Anderson L., Henderson C., and Adachi Y. Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage. Mol. Cell. Biol. 21 (2001) 1719-1729
94. Bonilla C.Y., Melo J.A., and Toczyski D.P. Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage. Mol. Cell 30 (2008) 267-276
95. Du L.L., Nakamura T.M., and Russell P. Histone modification-dependent and -independent pathways for recruitment of checkpoint protein Crb2 to double-strand breaks. Genes Dev. 20 (2006) 1583-1596
96. Sanders S.L., Portoso M., Mata J., Bahler J., Allshire R.C., and Kouzarides T. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119 (2004) 603-614
97. Esashi F., Mochida S., Matsusaka T., Obara T., Ogawa A., Tamai K., and Yanagida M. Establishment of and recovery from damage checkpoint requires sequential interactions of Crb2 with protein kinases Rad3, Chk1, and Cdc2. Cold Spring Harb. Symp. Quant. Biol. 65 (2000) 443-449
98. Mochida S., Esashi F., Aono N., Tamai K., O'Connell M.J., and Yanagida M. Regulation of checkpoint kinases through dynamic interaction with Crb2. EMBO J. 23 (2004) 418-428
99. Mochida S., and Yanagida M. Distinct modes of DNA damage response in S. pombe G0 and vegetative cells. Genes Cells 11 (2006) 13-27
100. Lazzaro F., Sapountzi V., Granata M., Pellicioli A., Vaze M., Haber J.E., Plevani P., Lydall D., and Muzi-Falconi M. Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J. 27 (2008) 1502-1512
101. Xie A., Hartlerode A., Stucki M., Odate S., Puget N., Kwok A., Nagaraju G., Yan C., Alt F.W., Chen J., et al. Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol. Cell 28 (2007) 1045-1057
102. Yu X., Wu L.C., Bowcock A.M., Aronheim A., and Baer R. 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 (1998) 25388-25392
103. Scully R., Chen J., Plug A., Xiao Y., Weaver D., Feunteun J., Ashley T., and Livingston D.M. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 88 (1997) 265-275
104. Greenberg R.A., Sobhian B., Pathania S., Cantor S.B., Nakatani Y., and Livingston D.M. Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev. 20 (2006) 34-46
105. Cantor S.B., Bell D.W., Ganesan S., Kass E.M., Drapkin R., Grossman S., Wahrer D.C., Sgroi D.C., Lane W.S., Haber D.A., et al. BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell 105 (2001) 149-160
106. Wang B., Matsuoka S., Ballif B.A., Zhang D., Smogorzewska A., Gygi S.P., and Elledge S.J. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316 (2007) 1194-1198
107. Wu L.C., Wang Z.W., Tsan J.T., Spillman M.A., Phung A., Xu X.L., Yang M.C., Hwang L.Y., Bowcock A.M., and Baer R. Identification of a RING protein that can interact in vivo with the BRCA1 gene product. Nat. Genet. 14 (1996) 430-440
108. Baer R., and Ludwig T. The BRCA1/BARD1 heterodimer, a tumor suppressor complex with ubiquitin E3 ligase activity. Curr. Opin. Genet. Dev. 12 (2002) 86-91
109. Wu-Baer F., and Baer R. Effect of DNA damage on a BRCA1 complex. Nature 414 (2001) 36
110. Yu X., Fu S., Lai M., Baer R., and Chen J. BRCA1 ubiquitinates its phosphorylation-dependent binding partner CtIP. Genes Dev. 20 (2006) 1721-1726
111. Li S., Ting N.S., Zheng L., Chen P.L., Ziv Y., Shiloh Y., Lee E.Y., and Lee W.H. Functional link of BRCA1 and ataxia telangiectasia gene product in DNA damage response. Nature 406 (2000) 210-215
112. Foray N., Marot D., Gabriel A., Randrianarison V., Carr A.M., Perricaudet M., Ashworth A., and Jeggo P. A subset of ATM- and ATR-dependent phosphorylation events requires the BRCA1 protein. EMBO J. 22 (2003) 2860-2871
113. Yu X., and Chen J. DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylation-dependent binding partner of BRCA1 C-terminal domains. Mol. Cell. Biol. 24 (2004) 9478-9486
114. Chen L., Nievera C.J., Lee A.Y., and Wu X. Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J. Biol. Chem. 283 (2008) 7713-7720
115. Huertas P., Cortes-Ledesma F., Sartori A.A., Aguilera A., and Jackson S.P. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature (2008)
116. Bochkareva E., Korolev S., Lees-Miller S.P., and Bochkarev A. Structure of the RPA trimerization core and its role in the multistep DNA-binding mechanism of RPA. EMBO J. 21 (2002) 1855-1863
117. Anantha R.W., Vassin V.M., and Borowiec J.A. Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J. Biol. Chem. 282 (2007) 35910-35923
118. Lo T., Pellegrini L., Venkitaraman A.R., and Blundell T.L. Sequence fingerprints in BRCA2 and RAD51: implications for DNA repair and cancer. DNA Repair (Amst.) 2 (2003) 1015-1028
119. Thorslund T., and West S.C. BRCA2: a universal recombinase regulator. Oncogene 26 (2007) 7720-7730
120. Yang H., Jeffrey P.D., Miller J., Kinnucan E., Sun Y., Thoma N.H., Zheng N., Chen P.L., Lee W.H., and Pavletich N.P. BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science 297 (2002) 1837-1848
121. Donoho G., Brenneman M.A., Cui T.X., Donoviel D., Vogel H., Goodwin E.H., Chen D.J., and Hasty P. Deletion of Brca2 exon 27 causes hypersensitivity to DNA crosslinks, chromosomal instability, and reduced life span in mice. Genes Chromosomes Cancer 36 (2003) 317-331
122. Tutt A., Bertwistle D., Valentine J., Gabriel A., Swift S., Ross G., Griffin C., Thacker J., and Ashworth A. Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. EMBO J. 20 (2001) 4704-4716
123. Wang X., Andreassen P.R., and D'Andrea A.D. Functional interaction of monoubiquitinated FANCD2 and BRCA2/FANCD1 in chromatin. Mol. Cell. Biol. 24 (2004) 5850-5862
124. Davies A.A., Masson J.Y., McIlwraith M.J., Stasiak A.Z., Stasiak A., Venkitaraman A.R., and West S.C. Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol. Cell 7 (2001) 273-282
125. Pellegrini L., Yu D.S., Lo T., Anand S., Lee M., Blundell T.L., and Venkitaraman A.R. Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 420 (2002) 287-293
126. Galkin V.E., Esashi F., Yu X., Yang S., West S.C., and Egelman E.H. BRCA2 BRC motifs bind RAD51-DNA filaments. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 8537-8542
127. Shivji M.K., Davies O.R., Savill J.M., Bates D.L., Pellegrini L., and Venkitaraman A.R. A region of human BRCA2 containing multiple BRC repeats promotes RAD51-mediated strand exchange. Nucleic Acids Res. 34 (2006) 4000-4011
128. Esashi F., Galkin V.E., Yu X., Egelman E.H., and West S.C. Stabilization of RAD51 nucleoprotein filaments by the C-terminal region of BRCA2. Nat. Struct. Mol. Biol. 14 (2007) 468-474
129. Davies O.R., and Pellegrini L. Interaction with the BRCA2 C terminus protects RAD51-DNA filaments from disassembly by BRC repeats. Nat. Struct. Mol. Biol. 14 (2007) 475-483
130. Esashi F., Christ N., Gannon J., Liu Y., Hunt T., Jasin M., and West S.C. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434 (2005) 598-604
131. Dupaigne P., Le Breton C., Fabre F., Gangloff S., Le Cam E., and Veaute X. The Srs2 helicase activity is stimulated by Rad51 filaments on dsDNA: implications for crossover incidence during mitotic recombination. Mol. Cell 29 (2008) 243-254
132. Krejci L., Van Komen S., Li Y., Villemain J., Reddy M.S., Klein H., Ellenberger T., and Sung P. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423 (2003) 305-309
133. Branzei D., and Foiani M. RecQ helicases queuing with Srs2 to disrupt Rad51 filaments and suppress recombination. Genes Dev. 21 (2007) 3019-3026
134. Ira G., Malkova A., Liberi G., Foiani M., and Haber J.E. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115 (2003) 401-411
135. Chiolo I., Carotenuto W., Maffioletti G., Petrini J.H., Foiani M., and Liberi G. Srs2 and Sgs1 DNA helicases associate with Mre11 in different subcomplexes following checkpoint activation and CDK1-mediated Srs2 phosphorylation. Mol. Cell. Biol. 25 (2005) 5738-5751
136. Liberi G., Chiolo I., Pellicioli A., Lopes M., Plevani P., Muzi-Falconi M., and Foiani M. Srs2 DNA helicase is involved in checkpoint response and its regulation requires a functional Mec1-dependent pathway and Cdk1 activity. EMBO J. 19 (2000) 5027-5038
137. Matsuoka S., Rotman G., Ogawa A., Shiloh Y., Tamai K., and Elledge S.J. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 10389-10394
138. Stegmeier F., and Amon A. Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu. Rev. Genet. 38 (2004) 203-232