BRCT domains: Phosphopeptide binding and signaling modules

Frontiers in Bioscience

Volumn 13, Issue 15, 2008, Pages 5905-5915

  Rodriguez, Maria C ^a   Zhou, Songyang ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Abraxas; BACH1; BRCA1; BRCT domains; Cancer mutations; Cell cycle; Crystal structure; CtIP; DNA damage; DNA repair; Missense mutations; Phosphopeptide binding; Phosphorylation; Phosphoserine binding domain; Protein folding; Protein protein interactions; RAP80; Review; Sequence homology; Signal transduction; Tumor suppressor

Indexed keywords

BACTERIA (MICROORGANISMS);

BRCA1 PROTEIN; CARRIER PROTEIN; FAM175A PROTEIN, HUMAN; NUCLEAR PROTEIN; PEPTIDE FRAGMENT; PHOSPHOPEPTIDE; PHOSPHOPROTEIN; RAP80 PROTEIN, HUMAN; RBBP8 PROTEIN, HUMAN;

BREAST TUMOR; CHEMISTRY; FEMALE; GENETIC PREDISPOSITION; GENETICS; HUMAN; METABOLISM; OVARY TUMOR; PHYSIOLOGY; PROTEIN BINDING; REVIEW; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

BRCA1 PROTEIN; BREAST NEOPLASMS; CARRIER PROTEINS; FEMALE; GENES, BRCA1; GENETIC PREDISPOSITION TO DISEASE; HUMANS; NUCLEAR PROTEINS; OVARIAN NEOPLASMS; PEPTIDE FRAGMENTS; PHOSPHOPEPTIDES; PHOSPHOPROTEINS; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 52049096814     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3125     Document Type: Review

References (79)

1. Bork, P., K. Hofmann, P. Bucher, A. F. Neuwald, S. F. Altschul & E. V. Koonin: A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. Faseb J, 11, 68-76 (1997)
2. Wu, L. C., Z. W. Wang, J. T. Tsan, M. A. Spillman, A. Phung, X. L. Xu, M. C. Yang, L. Y. Hwang, A. M. Bowcock & R. Baer: Identification of a RING protein that can interact in vivo with the BRCA1 gene product. Nat Genet, 14, 430-40(1996) (Pubitemid 26414587)
3. Scully, R., S. Ganesan, K. Vlasakova, J. Chen, M. Socolovsky & D. M. Livingston: Genetic analysis of BRCA1 function in a defined tumor cell line. Mol Cell, 4, 1093-9 (1999) (Pubitemid 30054915)
4. Holt, J. T., M. E. Thompson, C. Szabo, C. Robinson-Benion, C. L. Arteaga, M. C. King & R. A. Jensen: Growth retardation and tumour inhibition by BRCA1. Nat Genet, 12, 298-302 (1996) (Pubitemid 26080089)
5. Rao, V. N., N. Shao, M. Ahmad & E. S. Reddy: Antisense RNA to the putative tumor suppressor gene BRCA1 transforms mouse fibroblasts. Oncogene, 12, 523-8 (1996) (Pubitemid 26059646)
6. Koonin, E. V., S. F. Altschul & P. Bork: BRCA1 protein products ... Functional motifs. Nat Genet, 13, 266-8 (1996)
7. Zhou, B. B. & S. J. Elledge: The DNA damage response: putting checkpoints in perspective. Nature, 408, 433-9 (2000)
8. Khanna, K. K. & S. P. Jackson: DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet, 27, 247-54 (2001) (Pubitemid 32201842)
9. Venkitaraman, A. R.: Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell, 108, 171-82 (2002) (Pubitemid 34161138)
10. Callebaut, I. & J. P. Mornon: From BRCA1 to RAP1: a widespread BRCT module closely associated with DNA repair. FEBS Lett, 400, 25-30 (1997) (Pubitemid 27046815)
11. Glover, J. N., R. S. Williams & M. S. Lee: Interactions between BRCT repeats and phosphoproteins: tangled up in two. Trends Biochem Sci, 29, 579-85 (2004) (Pubitemid 39389077)
12. Gayther, S. A., W. Warren, S. Mazoyer, P. A. Russell, P. A. Harrington, M. Chiano, S. Seal, R. Hamoudi, E. J. van Rensburg, A. M. Dunning, R. Love, G. Evans, D. Easton, D. Clayton, M. R. Stratton & B. A. Ponder: Germline mutations of the BRCA1 gene in breast and ovarian cancer families provide evidence for a genotype-phenotype correlation. Nat Genet, 11, 428-33 (1995)
13. Manke, I. A., D. M. Lowery, A. Nguyen & M. B. Yaffe: BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science, 302, 636-9 (2003) (Pubitemid 37310918)
14. Rodriguez, M., X. Yu, J. Chen & Z. Songyang: Phosphopeptide binding specificities of BRCA1 COOHterminal (BRCT) domains. J Biol Chem, 278, 52914-8 (2003) (Pubitemid 38035892)
15. Wu-Baer, F. & R. Baer: Effect of DNA damage on a BRCA1 complex. Nature, 414, 36 (2001)
16. Li, S., N. S. Ting, L. Zheng, P. L. Chen, Y. Ziv, Y. Shiloh, E. Y. Lee & W. H. Lee: Functional link of BRCA1 and ataxia telangiectasia gene product in DNA damage response. Nature, 406, 210-5 (2000) (Pubitemid 30469007)
17. Lee, J. S., K. M. Collins, A. L. Brown, C. H. Lee & J. H. Chung: hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature, 404, 201-4 (2000) (Pubitemid 30154490)
18. Cortez, D., Y. Wang, J. Qin & S. J. Elledge: Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science, 286, 1162-6 (1999)
19. Hartman, A. R. & J. M. Ford: BRCA1 induces DNA damage recognition factors and enhances nucleotide excision repair. Nat Genet, 32, 180-4 (2002) (Pubitemid 34977215)
20. Welcsh, P. L., M. K. Lee, R. M. Gonzalez-Hernandez, D. J. Black, M. Mahadevappa, E. M. Swisher, J. A. Warrington & M. C. King: BRCA1 transcriptionally regulates genes involved in breast tumorigenesis. Proc Natl Acad Sci U S A, 99, 7560-5 (2002) (Pubitemid 34568730)
21. Xu, X., W. Qiao, S. P. Linke, L. Cao, W. M. Li, P. A. Furth, C. C. Harris & C. X. Deng: Genetic interactions between tumor suppressors Brca1 and p53 in apoptosis, cell cycle and tumorigenesis. Nat Genet, 28, 266-71 (2001) (Pubitemid 32626030)
22. Ludwig, T., P. Fisher, S. Ganesan & A. Efstratiadis: Tumorigenesis in mice carrying a truncating Brca1 mutation. Genes Dev, 15, 1188-93 (2001) (Pubitemid 32472748)
23. Benarroch, D. & S. Shuman: Characterization of mimivirus NAD+-dependent DNA ligase. Virology, 353, 133-43 (2006) (Pubitemid 44291775)
24. Taylor, R. M., B. Wickstead, S. Cronin & K. W. Caldecott: Role of a BRCT domain in the interaction of DNA ligase III-alpha with the DNA repair protein XRCC1. Curr Biol, 8, 877-80 (1998) (Pubitemid 28356048)
25. Yu, X., L. C. Wu, A. M. Bowcock, A. Aronheim & R. Baer: 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, 25388-92 (1998) (Pubitemid 28443306)
26. Cantor, S. B., D. W. Bell, S. Ganesan, E. M. Kass, R. Drapkin, S. Grossman, D. C. Wahrer, D. C. Sgroi, W. S. Lane, D. A. Haber & D. M. Livingston: BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell, 105, 149-60 (2001) (Pubitemid 32323924)
27. Williams, R. S., R. Green & J. N. Glover: Crystal structure of the BRCT repeat region from the breast cancerassociated protein BRCA1. Nat Struct Biol, 8, 838-42 (2001) (Pubitemid 32923600)
28. Critchlow, S. E., R. P. Bowater & S. P. Jackson: Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV. Curr Biol, 7, 588-98 (1997) (Pubitemid 27335654)
29. Derbyshire, D. J., B. P. Basu, L. C. Serpell, W. S. Joo, T. Date, K. Iwabuchi & A. J. Doherty: Crystal structure of human 53BP1 BRCT domains bound to p53 tumour suppressor. Embo J, 21, 3863-72 (2002) (Pubitemid 34787058)
30. Joo, W. S., P. D. Jeffrey, S. B. Cantor, M. S. Finnin, D. M. Livingston & N. P. Pavletich: Structure of the 53BP1 BRCT region bound to p53 and its comparison to the Brca1 BRCT structure. Genes Dev, 16, 583-93 (2002) (Pubitemid 34212491)
31. Beernink, P. T., M. Hwang, M. Ramirez, M. B. Murphy, S. A. Doyle & M. P. Thelen: Specificity of protein interactions mediated by BRCT domains of the XRCC1 DNA repair protein. J Biol Chem, 280, 30206-13 (2005) (Pubitemid 41216200)
32. Yamane, K. & T. Tsuruo: Conserved BRCT regions of TopBP1 and of the tumor suppressor BRCA1 bind strand breaks and termini of DNA. Oncogene, 18, 5194-203 (1999) (Pubitemid 29460655)
33. Yu, X., C. C. Chini, M. He, G. Mer & J. Chen: The BRCT domain is a phospho-protein binding domain. Science, 302, 639-42 (2003) (Pubitemid 37310919)
34. Soulier, J. & N. F. Lowndes: The BRCT domain of the S. cerevisiae checkpoint protein Rad9 mediates a Rad9-Rad9 interaction after DNA damage. Curr Biol, 9, 551-4 (1999) (Pubitemid 29257113)
35. Matsuoka, S., B. A. Ballif, A. Smogorzewska, E. R. McDonald, 3rd, K. E. Hurov, J. Luo, C. E. Bakalarski, Z. Zhao, N. Solimini, Y. Lerenthal, Y. Shiloh, S. P. Gygi & S. J. Elledge: ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science, 316, 1160-6 (2007) (Pubitemid 46877472)
36. Stucki, M., J. A. Clapperton, D. Mohammad, M. B. Yaffe, S. J. Smerdon & S. P. Jackson: MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell, 123, 1213-26 (2005) (Pubitemid 41821780)
37. Lee, M. S., R. A. Edwards, G. L. Thede & J. N. Glover: Structure of the BRCT repeat domain of MDC1 and its specificity for the free COOH-terminal end of the gamma-H2AX histone tail. J Biol Chem, 280, 32053-6 (2005) (Pubitemid 41361809)
38. Botuyan, M. V., Y. Nomine, X. Yu, N. Juranic, S. Macura, J. Chen & G. Mer: Structural basis of BACH1 phosphopeptide recognition by BRCA1 tandem BRCT domains. Structure, 12, 1137-46 (2004) (Pubitemid 38900756)
39. Williams, R. S., M. S. Lee, D. D. Hau & J. N. Glover: Structural basis of phosphopeptide recognition by the BRCT domain of BRCA1. Nat Struct Mol Biol, 11, 519-25 (2004) (Pubitemid 38691918)
40. Clapperton, J. A., I. A. Manke, D. M. Lowery, T. Ho, L. F. Haire, M. B. Yaffe & S. J. Smerdon: Structure and mechanism of BRCA1 BRCT domain recognition of phosphorylated BACH1 with implications for cancer. Nat Struct Mol Biol, 11, 512-8 (2004) (Pubitemid 38691917)
41. Varma, A. K., R. S. Brown, G. Birrane & J. A. Ladias: Structural basis for cell cycle checkpoint control by the BRCA1-CtIP complex. Biochemistry, 44, 10941-6 (2005) (Pubitemid 41209030)
42. Yu, X. & J. Chen: DNA damage-induced cell cycle checkpoint control requires CtIP, a phosphorylationdependent binding partner of BRCA1 C-terminal domains. Mol Cell Biol, 24, 9478-86 (2004) (Pubitemid 39391684)
43. Li, S., P. L. Chen, T. Subramanian, G. Chinnadurai, G. Tomlinson, C. K. Osborne, Z. D. Sharp & W. H. Lee: Binding of CtIP to the BRCT repeats of BRCA1 involved in the transcription regulation of p21 is disrupted upon DNA damage. J Biol Chem, 274, 11334-8 (1999)
44. Magnard, C., R. Bachelier, A. Vincent, M. Jaquinod, S. Kieffer, G. M. Lenoir & N. D. Venezia: BRCA1 interacts with acetyl-CoA carboxylase through its tandem of BRCT domains. Oncogene, 21, 6729-39 (2002) (Pubitemid 35221915)
45. Tong, L. & H. J. Harwood, Jr.: Acetyl-coenzyme A carboxylases: versatile targets for drug discovery. J Cell Biochem, 99, 1476-88 (2006) (Pubitemid 44845709)
46. Wakil, S. J.: The relationship between structure and function for and the regulation of the enzymes of fatty acid synthesis. Ann N Y Acad Sci, 478, 203-19 (1986) (Pubitemid 17011001)
47. Moreau, K., E. Dizin, H. Ray, C. Luquain, E. Lefai, F. Foufelle, M. Billaud, G. M. Lenoir & N. D. Venezia: BRCA1 affects lipid synthesis through its interaction with acetyl-CoA carboxylase. J Biol Chem, 281, 3172-81 (2006) (Pubitemid 43845927)
48. Milgraum, L. Z., L. A. Witters, G. R. Pasternack & F. P. Kuhajda: Enzymes of the fatty acid synthesis pathway are highly expressed in in situ breast carcinoma. Clin Cancer Res, 3, 2115-20 (1997) (Pubitemid 27505140)
49. Wang, B., S. Matsuoka, B. A. Ballif, D. Zhang, A. Smogorzewska, S. P. Gygi & S. J. Elledge: Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science, 316, 1194-8 (2007) (Pubitemid 46877482)
50. Kim, H., J. Huang & J. Chen: CCDC98 is a BRCA1-BRCT domain-binding protein involved in the DNA damage response. Nat Struct Mol Biol, 14, 710-5 (2007) (Pubitemid 47220062)
51. Liu, Z., J. Wu & X. Yu: CCDC98 targets BRCA1 to DNA damage sites. Nat Struct Mol Biol, 14, 716-20 (2007) (Pubitemid 47220064)
52. Sobhian, B., G. Shao, D. R. Lilli, A. C. Culhane, L. A. Moreau, B. Xia, D. M. Livingston & R. A. Greenberg: RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science, 316, 1198-202 (2007) (Pubitemid 46877483)
53. Kim, H., J. Chen & X. Yu: Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science, 316, 1202-5 (2007) (Pubitemid 46877484)
54. Stewart, G. S., B. Wang, C. R. Bignell, A. M. Taylor & S. J. Elledge: MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature, 421, 961-6 (2003) (Pubitemid 36288029)
55. Goldberg, M., M. Stucki, J. Falck, D. D'Amours, D. Rahman, D. Pappin, J. Bartek & S. P. Jackson: MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature, 421, 952-6 (2003) (Pubitemid 36288027)
56. Lou, Z., K. Minter-Dykhouse, X. Wu & J. Chen: MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature, 421, 957-61(2003) (Pubitemid 36288028)
57. Downs, J. A., N. F. Lowndes & S. P. Jackson: A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature, 408, 1001-4 (2000) (Pubitemid 32101649)
58. Hammet, A., C. Magill, J. Heierhorst & S. P. Jackson: Rad9 BRCT domain interaction with phosphorylated H2AX regulates the G1 checkpoint in budding yeast. EMBO Rep, 8, 851-7 (2007) (Pubitemid 350001429)
59. Cho, E. A., M. J. Prindle & G. R. Dressler: BRCT domain-containing protein PTIP is essential for progression through mitosis. Mol Cell Biol, 23, 1666-73 (2003) (Pubitemid 36246048)
60. Jowsey, P. A., A. J. Doherty & J. Rouse: Human PTIP facilitates ATM-mediated activation of p53 and promotes cellular resistance to ionizing radiation. J Biol Chem, 279, 55562-9 (2004) (Pubitemid 40066559)
61. Munoz, I. M., P. A. Jowsey, R. Toth & J. Rouse: Phospho-epitope binding by the BRCT domains of hPTIP controls multiple aspects of the cellular response to DNA damage. Nucleic Acids Res, 35, 5312-22 (2007) (Pubitemid 47423906)
62. Jackson, A. P., H. Eastwood, S. M. Bell, J. Adu, C. Toomes, I. M. Carr, E. Roberts, D. J. Hampshire, Y. J. Crow, A. J. Mighell, G. Karbani, H. Jafri, Y. Rashid, R. F. Mueller, A. F. Markham & C. G. Woods: Identification of microcephalin, a protein implicated in determining the size of the human brain. Am J Hum Genet, 71, 136-42 (2002) (Pubitemid 34734714)
63. Xu, X., J. Lee & D. F. Stern: Microcephalin is a DNA damage response protein involved in regulation of CHK1 and BRCA1. J Biol Chem, 279, 34091-4 (2004) (Pubitemid 39318029)
64. O'Driscoll, M., A. P. Jackson & P. A. Jeggo: Microcephalin: a causal link between impaired damage response signalling and microcephaly. Cell Cycle, 5, 2339-44 (2006) (Pubitemid 44785842)
65. Lin, S. Y., R. Rai, K. Li, Z. X. Xu & S. J. Elledge: BRIT1/MCPH1 is a DNA damage responsive protein that regulates the Brca1-Chk1 pathway, implicating checkpoint dysfunction in microcephaly. Proc Natl Acad Sci U S A, 102, 15105-9 (2005) (Pubitemid 41513342)
66. Wood, J. L., N. Singh, G. Mer & J. Chen: MCPH1 Functions in an H2AX-dependent but MDC1-independent Pathway in Response to DNA Damage. J Biol Chem, 282, 35416-35423 (2007) (Pubitemid 350232410)
67. Brunk, K., B. Vernay, E. Griffith, N. L. Reynolds, D. Strutt, P. W. Ingham & A. P. Jackson: Microcephalin coordinates mitosis in the syncytial Drosophila embryo. J Cell Sci, 120, 3578-88 (2007) (Pubitemid 350120950)
68. Shiozaki, E. N., L. Gu, N. Yan & Y. Shi: Structure of the BRCT repeats of BRCA1 bound to a BACH1 phosphopeptide: implications for signaling. Mol Cell, 14, 405-12 (2004) (Pubitemid 38591411)
69. Vallon-Christersson, J., C. Cayanan, K. Haraldsson, N. Loman, J. T. Bergthorsson, K. Brondum-Nielsen, A. M. Gerdes, P. Moller, U. Kristoffersson, H. Olsson, A. Borg & A. N. Monteiro: Functional analysis of BRCA1 C-terminal missense mutations identified in breast and ovarian cancer families. Hum Mol Genet, 10, 353-60 (2001) (Pubitemid 32166546)
70. Williams, R. S. & J. N. Glover: Structural consequences of a cancer-causing BRCA1-BRCT missense mutation. J Biol Chem, 278, 2630-5 (2003) (Pubitemid 36801342)
71. Williams, R. S., D. I. Chasman, D. D. Hau, B. Hui, A. Y. Lau & J. N. Glover: Detection of protein folding defects caused by BRCA1-BRCT truncation and missense mutations. J Biol Chem, 278, 53007-16 (2003) (Pubitemid 38035903)
72. Zhang, X., S. Morera, P. A. Bates, P. C. Whitehead, A. I. Coffer, K. Hainbucher, R. A. Nash, M. J. Sternberg, T. Lindahl & P. S. Freemont: Structure of an XRCC1 BRCT domain: a new protein-protein interaction module. Embo J, 17, 6404-11 (1998) (Pubitemid 28497812)
73. Krishnan, V. V., K. H. Thornton, M. P. Thelen & M. Cosman: Solution structure and backbone dynamics of the human DNA ligase IIIalpha BRCT domain. Biochemistry, 40, 13158-66 (2001) (Pubitemid 33043530)
74. Sibanda, B. L., S. E. Critchlow, J. Begun, X. Y. Pei, S. P. Jackson, T. L. Blundell & L. Pellegrini: Crystal structure of an Xrcc4-DNA ligase IV complex. Nat Struct Biol, 8, 1015-9 (2001) (Pubitemid 33101619)
75. Jeon, H. J., H. J. Shin, J. J. Choi, H. S. Hoe, H. K. Kim, S. W. Suh & S. T. Kwon: Mutational analyses of the thermostable NAD+-dependent DNA ligase from Thermus filiformis. FEMS Microbiol Lett, 237, 111-8 (2004) (Pubitemid 38980012)
76. Birrane, G., A. K. Varma, A. Soni & J. A. Ladias: Crystal structure of the BARD1 BRCT domains. Biochemistry, 46, 7706-12 (2007) (Pubitemid 47016055)
77. Dulic, A., P. A. Bates, X. Zhang, S. R. Martin, P. S. Freemont, T. Lindahl & D. E. Barnes: BRCT domain interactions in the heterodimeric DNA repair protein XRCC1-DNA ligase III. Biochemistry, 40, 5906-13 (2001) (Pubitemid 32466292)
78. Lin, S. Y. & S. J. Elledge: Multiple tumor suppressor pathways negatively regulate telomerase. Cell, 113, 881-9(2003) (Pubitemid 36798050)
79. Rai, R., H. Dai, A. S. Multani, K. Li, K. Chin, J. Gray, J. P. Lahad, J. Liang, G. B. Mills, F. Meric-Bernstam & S. Y. Lin: BRIT1 regulates early DNA damage response, chromosomal integrity, and cancer. Cancer Cell, 10, 145-57(2006) (Pubitemid 44175904)