EMSY overexpression disrupts the BRCA2/RAD51 pathway in the DNA-damage response: Implications for chromosomal instability/recombination syndromes as checkpoint diseases

Molecular Genetics and Genomics

Volumn 285, Issue 4, 2011, Pages 325-340

  Cousineau, Isabelle ^a,b   Belmaaza, Abdellah ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b NOTRE DAME HOSPITAL   (Canada)

Author keywords

Aging; Development abortion; Estrogens; Oncogenes; Tumor suppressor genes

Indexed keywords

ATM PROTEIN; ATR PROTEIN; BINDING PROTEIN; BRCA1 PROTEIN; BRCA2 PROTEIN; DOUBLE STRANDED DNA; EMSY PROTEIN; MRE11 PROTEIN; NIBRIN; RAD50 PROTEIN; RAD51 PROTEIN; REPLICATION FACTOR A; REPRESSOR PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; EMSY PROTEIN, HUMAN; NUCLEAR PROTEIN; RAD51 PROTEIN, HUMAN; TUMOR PROTEIN;

ARTICLE; CANCER SUSCEPTIBILITY; CELL STRAIN MCF 7; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE MUTATION; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC SUSCEPTIBILITY; HOMOLOGOUS RECOMBINATION; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN STABILITY; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; BIOLOGICAL MODEL; DOUBLE STRANDED DNA BREAK; GENETIC RECOMBINATION; GENETICS; HUMAN; INVERTED REPEAT; METABOLISM; TUMOR CELL LINE;

BRCA2 PROTEIN; CELL LINE, TUMOR; CHROMOSOMAL INSTABILITY; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; HUMANS; INVERTED REPEAT SEQUENCES; MODELS, BIOLOGICAL; NEOPLASM PROTEINS; NUCLEAR PROTEINS; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

EID: 79957516181     PISSN: 16174615     EISSN: 16174623     Source Type: Journal    
DOI: 10.1007/s00438-011-0612-5     Document Type: Article

References (81)

1. Abaji C, Cousineau I, Belmaaza A (2005) BRCA2 regulates homologous recombination in response to DNA damage: implications for genome stability and carcinogenesis. Cancer Res 65:4117-4125 (Pubitemid 40775649)
2. Aboussekhra A, Al-Sharif IS (2005) Homologous recombination is involved in transcription-coupled repair of UV damage in Saccharomyces cerevisiae. EMBO J 24:1999-2010 (Pubitemid 40896171)
3. Akyuz N, Boehden GS, Susse S, Rimek A, Preuss U, Scheidtmann KH et al (2002) DNA substrate dependence of p53-mediated regulation of double-strand break repair. Mol Cell Biol 22:6306-6317 (Pubitemid 34857848)
4. Allen C, Kurimasa A, Brenneman MA, Chen DJ, Nickoloff JA (2002) DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination. Proc Natl Acad Sci USA 99:3758-3763 (Pubitemid 34252179)
5. Auclair Y, Rouget R, Affarel B, Drobetsky EA (2008) ATR kinase is required for global genomic nucleotide excision repair exclusively during S phase in human cells. Proc Natl Acad Sci USA 105:17896-17901
6. Belmaaza A, Chartrand P (1994) One-sided invasion events in homologous recombination at double-strand breaks. Mutat Res 314:199-208 (Pubitemid 24128664)
7. Bogliolo M, Taylor RM, Caldecott KW, Frosina G (2000) Reduced ligation during DNA base excision repair supported by BRCA2 mutant cells. Oncogene 19:5781-5787
8. Branzei D, Foiani M (2005) The DNA damage response during DNA replication. Curr Opin Cell Biol 17:568-575 (Pubitemid 41541967)
9. Branzei D, Foiani M (2007) Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst) 6:994-1003 (Pubitemid 46880479)
10. Branzei D, Foiani M (2008) Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol 9:297-308 (Pubitemid 351430844)
11. Chan KL, North PS, Hickson ID (2007) BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J 26:3397-3409 (Pubitemid 47123542)
12. Chan KL, Palmai-Pallag T, Ying S, Hickson ID (2009) Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat Cell Biol 11:753-760
13. Chan N, Koritzinsky M, Zhao H, Bindra R, Glazer PM, Powell S et al (2008) Chronic hypoxia decreases synthesis of homologous recombination proteins to offset chemoresistance and radioresistance. Cancer Res 68:605-614 (Pubitemid 351380090)
14. Chen L, Nievera CJ, Lee AY, Wu X (2008) Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J Biol Chem 283:7713-7720
15. Claybon A, Karia B, Bruce C, Bishop AJ (2010) PARP1 suppresses homologous recombination events in mice in vivo. Nucleic Acids Res 38:7538-7545
16. Conilleau S, Takizawa Y, Tachiwana H, Fleury F, Kurumizaka H, Takahashi M (2004) Location of tyrosine 315, a target for phosphorylation by cAbl tyrosine kinase, at the edge of the subunit-subunit interface of the human Rad51 filament. J Mol Biol 339:797-804 (Pubitemid 38691119)
17. Cousineau I, Abaji C, Belmaaza A (2005) BRCA1 regulates RAD51 function in response to DNA damage and suppresses spontaneous sister chromatid replication slippage: implications for sister chromatid cohesion, genome stability, and carcinogenesis. Cancer Res 65:11384-11391 (Pubitemid 41821695)
18. Cousineau I, Belmaaza A (2007) BRCA1 haploinsufficiency, but not heterozygosity for a BRCA1-truncating mutation, deregulates homologous recombination. Cell Cycle 6:962-971 (Pubitemid 46658751)
19. Daboussi F, Dumay A, Delacote F, Lopez BS (2002) DNA doublestrand break repair signalling: the case of RAD51 post-translational regulation. Cell Signal 14:969-975 (Pubitemid 35279421)
20. Deming PB, Cistulli CA, Zhao H, Graves PR, Piwnica-Worms H, Paules RS et al (2001) The human decatenation checkpoint. Proc Natl Acad Sci USA 98:12044-12049 (Pubitemid 32959823)
21. Donoho G, Brenneman MA, Cui TX, Donoviel D, Vogel H, Goodwin EH et al (2003) Deletion of Brca2 exon 27 causes hypersensitivity to DNA crosslinks, chromosomal instability, and reduced life span in mice. Genes Chromosomes Cancer 36:317-331 (Pubitemid 36314515)
22. Eszterhas SK, Bouhassira EE, Martin DI, Fiering S (2002) Transcriptional interference by independently regulated genes occurs in any relative arrangement of the genes and is influenced by chromosomal integration position. Mol Cell Biol 22:469-479 (Pubitemid 34027492)
23. Evers B, Jonkers J (2006) Mouse models of BRCA1 and BRCA2 deficiency: past lessons, current understanding and future prospects. Oncogene 25:5885-5897 (Pubitemid 44453444)
24. Forget AL, Kowalczykowski SC (2010) Single-molecule imaging brings Rad51 nucleoprotein filaments into focus. Trends Cell Biol 20:269-276
25. Friedberg EC, Meira LB (2006) Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage Version 7. DNA Repair (Amst) 5:189-209 (Pubitemid 43069520)
26. Golding SE, Rosenberg E, Khalil A, McEwen A, Holmes M, Neill S et al (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 (Pubitemid 38618939)
27. Greenberg RA, Sobhian B, Pathania S, Cantor SB, Nakatani Y, Livingston DM (2006) Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev 20:34-46 (Pubitemid 43042666)
28. Groth A, Rocha W, Verreault A, Almouzni G (2007) Chromatin challenges during DNA replication and repair. Cell 128:721-733 (Pubitemid 46273574)
29. Gudmundsdottir K, Ashworth A (2006) The roles of BRCA1 and BRCA2 and associated proteins in the maintenance of genomic stability. Oncogene 25:5864-5874 (Pubitemid 44453442)
30. Halazonetis TD, Gorgoulis VG, Bartek J (2008) An oncogene-induced DNA damage model for cancer development. Science 319:1352-1355 (Pubitemid 351354863)
31. Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28:739-745 (Pubitemid 350217064)
32. Henikoff S (1998) Conspiracy of silence among repeated transgenes. Bioessays 20:532-535
33. Hong S, Pusapati RV, Powers JT, Johnson DG (2006) Oncogenes and the DNA damage response: Myc and E2F1 engage the ATM signaling pathway to activate p53 and induce apoptosis. Cell Cycle 5:801-803 (Pubitemid 44145570)
34. Hughes-Davies L, Huntsman D, Ruas M, Fuks F, Bye J, Chin SF et al (2003) EMSY links the BRCA2 pathway to sporadic breast and ovarian cancer. Cell 115:523-535 (Pubitemid 37506042)
35. Igoucheva O, Alexeev V, Yoon K (2006) Differential cellular responses to exogenous DNA in mammalian cells and its effect on oligonucleotide-directed gene modification. Gene Ther 13:266-275 (Pubitemid 43148649)
36. Jasin M (2002) Homologous repair of DNA damage and tumorigenesis: the BRCA connection. Oncogene 21:8981-8993
37. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J et al (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 8:37-45 (Pubitemid 43064795)
38. Kastan MB, Bartek J (2004) Cell-cycle checkpoints and cancer. Nature 432:316-323 (Pubitemid 39551659)
39. Kenemans P, Verstraeten RA, Verheijen RH (2004) Oncogenic pathways in hereditary and sporadic breast cancer. Maturitas 49:34-43 (Pubitemid 39209369)
40. Le Page F, Randrianarison V, Marot D, Cabannes J, Perricaudet M, Feunteun J et al (2000) BRCA1 and BRCA2 are necessary for the transcription-coupled repair of the oxidative 8-oxoguanine lesion in human cells. Cancer Res 60:5548-5552
41. Lemelin JF, Abaji C, Cousineau I, Belmaaza A (2005) Disruption of p53 by the viral oncoprotein HPV16-E6 does not deregulate chromosomal homologous recombination in a transcriptional interference-free assay system. Cell Cycle 4:831-837 (Pubitemid 41353837)
42. Litman R, Peng M, Jin Z, Zhang F, Zhang J, Powell S et al (2005) BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell 8:255-265 (Pubitemid 41317595)
43. Lomonosov M, Anand S, Sangrithi M, Davies R, Venkitaraman AR (2003) Stabilization of stalled DNA replication forks by the BRCA2 breast cancer susceptibility protein. Genes Dev 17:3017-3022 (Pubitemid 38040765)
44. Marmorstein LY, Ouchi T, Aaronson SA (1998) The BRCA2 gene product functionally interacts with p53 and RAD51. Proc Natl Acad Sci USA 95:13869-13874 (Pubitemid 28523065)
45. Mazloum N, Zhou Q, Holloman WK (2007) DNA binding, annealing, and strand exchange activities of Brh2 protein from Ustilago maydis. Biochemistry 46:7163-7173 (Pubitemid 46973990)
46. Meyn MS (1997) Chromosome instability syndromes: lessons for carcinogenesis. Curr Top Microbiol Immunol 221:71-148
47. Morimatsu M, Donoho G, Hasty P (1998) Cells deleted for Brca2 COOH terminus exhibit hypersensitivity to gamma-radiation and premature senescence. Cancer Res 58:3441-3447 (Pubitemid 28371088)
48. Moynahan ME, Jasin M (2010) Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol 11:196-207
49. Olson E, Nievera CJ, Liu E, Lee AY, Chen L, Wu X (2007) The Mre11 complex mediates the S-phase checkpoint through an interaction with replication protein A. Mol Cell Biol 27:6053-6067 (Pubitemid 47326694)
50. Petalcorin MI, Sandall J, Wigley DB, Boulton SJ (2006) CeBRC-2 stimulates D-loop formation by RAD-51 and promotes DNA single-strand annealing. J Mol Biol 361:231-242 (Pubitemid 44092785)
51. Petiniot LK, Weaver Z, Vacchio M, Shen R, Wangsa D, Barlow C et al (2002) RAG-mediated V(D)J recombination is not essential for tumorigenesis in Atm-deficient mice. Mol Cell Biol 22:3174-3177
52. Raouf A, Brown L, Vrcelj N, To K, Kwok W, Huntsman D et al (2005) Genomic instability of human mammary epithelial cells overexpressing a truncated form of EMSY. J Natl Cancer Inst 97:1302-1306 (Pubitemid 41535371)
53. Scully R, Livingston DM (2000) In search of the tumour-suppressor functions of BRCA1 and BRCA2. Nature 408:429-432
54. Shen WH, Balajee AS, Wang J, Wu H, Eng C, Pandolfi PP et al (2007) Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell 128:157-170 (Pubitemid 46048887)
55. Shiloh Y (2003) ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3:155-168
56. Sleeth KM, Sorensen CS, Issaeva N, Dziegielewski J, Bartek J, Helleday T (2007) RPA mediates recombination repair during replication stress and is displaced from DNA by checkpoint signalling in human cells. J Mol Biol 373:38-47 (Pubitemid 47390721)
57. Sorensen CS, Hansen LT, Dziegielewski J, Syljuasen RG, Lundin C, Bartek J et al (2005) The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 7:195-201 (Pubitemid 40268135)
58. Stauffer ME, Chazin WJ (2004) Physical interaction between replication protein A and Rad51 promotes exchange on single-stranded DNA. J Biol Chem 279:25638-25645 (Pubitemid 38756826)
59. Stiff T, Walker SA, Cerosaletti K, Goodarzi AA, Petermann E, Concannon P et al (2006) ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. EMBO J 25:5775-5782 (Pubitemid 44967761)
60. Thorslund T, West SC (2007) BRCA2: a universal recombinase regulator. Oncogene 26:7720-7730 (Pubitemid 350242452)
61. Venkitaraman AR (2002) Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108:171-182
62. Villemure JF, Abaji C, Cousineau I, Belmaaza A (2003) MSH2-deficient human cells exhibit a defect in the accurate termination of homology-directed repair of DNA double-strand breaks. Cancer Res 63:3334-3339 (Pubitemid 36735891)
63. Villemure JF, Belmaaza A, Chartrand P (1997) The processing of DNA ends at double-strand breaks during homologous recombination: different roles for the two ends. Mol Gen Genet 256:533-538
64. Villemure JF, Savard N, Belmaaza A (2001) Promoter suppression in cultured mammalian cells can be blocked by the chicken beta-globin chromatin insulator 50HS4 and matrix/scaffold attachment regions. J Mol Biol 312:963-974 (Pubitemid 32980318)
65. Vogelstein B, Kinzler KW (2004) Cancer genes and the pathways they control. Nat Med 10:789-799 (Pubitemid 39070849)
66. Walsh T, King MC (2007) Ten genes for inherited breast cancer. Cancer Cell 11:103-105 (Pubitemid 46209856)
67. Wang H, Powell SN, Iliakis G, Wang Y (2004) ATR affecting cell radiosensitivity is dependent on homologous recombination repair but independent of nonhomologous end joining. Cancer Res 64:7139-7143 (Pubitemid 39331028)
68. Wang Y, Cortez D, Yazdi P, Neff N, Elledge SJ, Qin J (2000) BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev 14:927-939 (Pubitemid 30253002)
69. Weaver BA, Silk AD, Montagna C, Verdier-Pinard P, Cleveland DW (2007) Aneuploidy acts both oncogenically and as a tumor suppressor. Cancer Cell 11:25-36 (Pubitemid 46070223)
70. Welcsh PL, King MC (2001) BRCA1 and BRCA2 and the genetics of breast and ovarian cancer. Hum Mol Genet 10:705-713 (Pubitemid 32331579)
71. Westermark UK, Reyngold M, Olshen AB, Baer R, Jasin M, Moynahan ME (2003) BARD1 participates with BRCA1 in homology-directed repair of chromosome breaks. Mol Cell Biol 23:7926-7936 (Pubitemid 37271488)
72. Wong JM, Ionescu D, Ingles CJ (2003) Interaction between BRCA2 and replication protein A is compromised by a cancer-predisposing mutation in BRCA2. Oncogene 22:28-33 (Pubitemid 36152880)
73. Xia B, Sheng Q, Nakanishi K, Ohashi A, Wu J, Christ N et al (2006) Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Mol Cell 22:719-729
74. Yajima H, Lee KJ, Chen BP (2006) ATR-dependent phosphorylation of DNA-dependent protein kinase catalytic subunit in response to UV-induced replication stress. Mol Cell Biol 26:7520-7528 (Pubitemid 44547702)
75. Yang YG, Saidi A, Frappart PO, Min W, Barrucand C, Dumon-Jones V et al (2006) Conditional deletion of Nbs1 in murine cells reveals its role in branching repair pathways of DNA doublestrand breaks. EMBO J 25:5527-5538 (Pubitemid 44847193)
76. Ye X, Franco AA, Santos H, Nelson DM, Kaufman PD, Adams PD (2003) Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol Cell 11:341-351 (Pubitemid 36293829)
77. Yu DS, Sonoda E, Takeda S, Huang CL, Pellegrini L, Blundell TL et al (2003) Dynamic control of Rad51 recombinase by self-association and interaction with BRCA2. Mol Cell 12:1029-1041 (Pubitemid 37352793)
78. Yuan ZM, Huang Y, Ishiko T, Nakada S, Utsugisawa T, Kharbanda S et al (1998) Regulation of Rad51 function by c-Abl in response to DNA damage. J Biol Chem 273:3799-3802 (Pubitemid 28103233)
79. Zhang F, Ma J, Wu J, Ye L, Cai H, Xia B et al (2009) PALB2 links BRCA1 and BRCA2 in the DNA-damage response. Curr Biol 19:524-529
80. Zhang J, Willers H, Feng Z, Ghosh JC, Kim S, Weaver DT et al (2004) Chk2 phosphorylation of BRCA1 regulates DNA doublestrand break repair. Mol Cell Biol 24:708-718 (Pubitemid 38057922)
81. Zhou T, Chou J, Mullen TE, Elkon R, Zhou Y, Simpson DA et al (2007) Identification of primary transcriptional regulation of cell cycle-regulated genes upon DNA damage. Cell Cycle 6:972-981 (Pubitemid 46658752)