Identification of filamin A as a BRCA1-interacting protein required for efficient DNA repair

Cell Cycle

Volumn 9, Issue 7, 2010, Pages 1421-1433

  Velkova, Aneliya ^a,b   Carvalho, Marcelo A ^a,d   Johnson, Joseph O ^a   Tavtigian, Sean V ^c   Monteiro, Alvaro N A ^a  

^a H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^d Instituto Federal Do Rio de Janeiro   (Brazil)

Author keywords

BRCA1; DNA damage; DNA repair; DNA PK; Filamin A; Non homologous end joining

Indexed keywords

BRCA1 PROTEIN; DNA; FILAMIN A; HOLOENZYME; HOLOENZYME KU86; PHOSPHATIDYLINOSITOL 3 KINASE; RAD51 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; CANCER SUSCEPTIBILITY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVE SITE; GENETIC CONSERVATION; HUMAN; HUMAN TISSUE; KINETICS; PROTEIN BINDING; PROTEIN INTERACTION; TWO HYBRID SYSTEM;

EID: 77953608382     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.7.11256     Document Type: Article

References (65)

1. Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature 2009; 461:1071-8.
2. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell 2007; 28:739-45.
3. Falck J, Coates J, Jackson SP. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005; 434:605-11.
4. Raderschall E, Golub EI, Haaf T. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc Natl Acad Sci USA 1999; 96:1921-6.
5. San Filippo J, Sung P, Klein H. Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 2008; 77:229-57.
6. Scully R, Chen J, Plug A, Xiao Y, Weaver D, Feunteun J, et al. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell 1997; 88:265-75.
7. Chen J, Silver DP, Walpita D, Cantor SB, Gazdar AF, Tomlinson G, et al. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol Cell 1998; 2:317-28.
8. Greenberg RA, Sobhian B, Pathania S, Cantor SB, Nakatani Y, Livingston DM. Multifactorial contributions to an acute DNA damage response by BRCA1/BARD1-containing complexes. Genes Dev 2006; 20:34-46.
9. Ford D, Easton DF, Bishop DT, Narod SA, Goldgar DE. Risks of cancer in BRCA1-mutation carriers. Breast Cancer Linkage Consortium. Lancet 1994; 343:692-5.
10. Easton DF, Bishop DT, Ford D, Crockford GP. Genetic linkage analysis in familial breast and ovarian cancer: results from 214 families. The Breast Cancer Linkage Consortium. Am J Hum Genet 1993; 52:678-701.
11. Miki Y, Swensen J, Shattuck-Eidens D, Futreal PA, Harshman K, Tavtigian S, et al. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 1994; 266:66-71. (Pubitemid 24345325)
12. Friedman LS, Ostermeyer EA, Szabo CI, Dowd P, Lynch ED, Rowell SE, et al. Confirmation of BRCA1 by analysis of germline mutations linked to breast and ovarian cancer in ten families. Nat Genet 1994; 8:399-404.
13. Narod SA, Foulkes WD. BRCA1 and BRCA2: 1994 and beyond. Nat Rev Cancer 2004; 4:665-76.
14. Scully R, Livingston D. In search of the tumour-suppressor functions of BRCA1 and BRCA2. Nature 2000; 408:429-32.
15. Venkitaraman AR. Cancer Susceptibility and the Functions of BRCA1 and BRCA2. Cell 2002; 108:171-82.
16. Moynahan ME, Chiu JW, Koller BH, Jasin M. Brca1 controls homology-directed DNA repair. Mol Cell 1999; 4:511-8.
17. Zhong Q, Chen CF, Chen PL, Lee WH. BRCA1 facilitates microhomology- mediated end joining of DNA double strand breaks. J Biol Chem 2002; 277:28641-7.
18. Zhuang J, Zhang J, Willers H, Wang H, Chung JH, van Gent DC, et al. Checkpoint kinase 2-mediated phosphorylation of BRCA1 regulates the fidelity of nonhomologous end-joining. Cancer Res 2006; 66:1401-8. (Pubitemid 43259920)
19. Wang HC, Chou WC, Shieh SY, Shen CY. Ataxia telangiectasia mutated and checkpoint kinase 2 regulate BRCA1 to promote the fidelity of DNA end-joining. Cancer Res 2006; 66:1391-400.
20. Carvalho MA, Marsillac SM, Karchin R, Manoukian S, Grist S, Swaby RF, et al. Determination of Cancer Risk Associated with Germ Line BRCA1 Missense Variants by Functional Analysis. Cancer Res 2007; 67:1494-501.
21. Orelli BJ, Logsdon JM Jr, Bishop DK. Nine novel conserved motifs in BRCA1 identified by the chicken orthologue. Oncogene 2001; 20:4433-8.
22. Abkevich V, Zharkikh A, Deffenbaugh AM, Frank D, Chen Y, Shattuck D, et al. Analysis of missense variation in human BRCA1 in the context of interspecific sequence variation. J Med Genet 2004; 41:492-507.
23. 2 arrest requires actin-binding protein filamin-A/actin-binding protein 280. J Biol Chem 2004; 279:6098-105.
24. Yue J, Wang Q, Lu H, Brenneman M, Fan F, Shen Z. The cytoskeleton protein filamin-A is required for an efficient recombinational DNA double strand break repair. Cancer Res 2009; 69:7978-85.
25. Yuan Y, Shen Z. Interaction with BRCA2 suggests a role for filamin-1 (hsFLNa) in DNA damage response. J Biol Chem 2001; 276:48318-24.
26. Feng Y, Walsh CA. The many faces of filamin: a versatile molecular scaffold for cell motility and signalling. Nat Cell Biol 2004; 6:1034-8. (Pubitemid 39468003)
27. Rodriguez JA, Henderson BR. Identification of a functional nuclear export sequence in BRCA1. J Biol Chem 2000; 275:38589-96.
28. Thompson ME, Robinson-Benion CL, Holt JT. An amino-terminal motif functions as a second nuclear export sequence in BRCA1. J Biol Chem 2005; 280:21854-7.
29. Cunningham CC, Gorlin JB, Kwiatkowski DJ, Hartwig JH, Janmey PA, Byers HR, et al. Actin-binding protein requirement for cortical stability and efficient locomotion. Science 1992; 255:325-7.
30. Rogakou EP, Boon C, Redon C, Bonner WM. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 1999; 146:905-16. (Pubitemid 29430435)
31. Dimitrova DS, Gilbert DM. Stability and nuclear distribution of mammalian replication protein A heterotrimeric complex. Exp Cell Res 2000; 254:321-7.
32. Tomlinson GE, Chen TT, Stastny VA, Virmani AK, Spillman MA, Tonk V, et al. Characterization of a breast cancer cell line derived from a germ-line BRCA1 mutation carrier. Cancer Res 1998; 58:3237-42.
33. Eccles DM, Barker S, Pilz DT, Kennedy C. Neuronal migration defect in a BRCA1 gene carrier: possible focal nullisomy? J Med Genet 2003; 40:24.
34. Eccles D, Bunyan D, Barker S, Castle B. BRCA1 mutation and neuronal migration defect: implications for chemoprevention. J Med Genet 2005; 42:42.
35. Tavtigian SV, Deffenbaugh AM, Yin L, Judkins T, Scholl T, Samollow PB, et al. Comprehensive statistical study of 452 BRCA1 missense substitutions with classification of eight recurrent substitutions as neutral. J Med Genet 2006; 43:295-305.
36. Caligo MA, Bonatti F, Guidugli L, Aretini P, Galli A. A yeast recombination assay to characterize human BRCA1 missense variants of unknown pathological significance. Hum Mutat 2009; 30:123-33.
37. Judkins T, Hendrickson BC, Deffenbaugh AM, Eliason K, Leclair B, Norton MJ, et al. Application of embryonic lethal or other obvious phenotypes to characterize the clinical significance of genetic variants found in trans with known deleterious mutations. Cancer Res 2005; 65:10096-103.
38. Wei L, Lan L, Hong Z, Yasui A, Ishioka C, Chiba N. Rapid recruitment of BRCA1 to DNA double-strand breaks is dependent on its association with Ku80. Mol Cell Biol 2008; 28:7380-93.
39. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506.
40. Matsuoka S, Rotman G, Ogawa A, Shiloh Y, Tamai K, Elledge SJ. Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proc Natl Acad Sci USA 2000; 97:10389-94.
41. Melchionna R, Chen XB, Blasina A, McGowan CH. Threonine 68 is required for radiation-induced phosphorylation and activation of Cds1. Nat Cell Biol 2000; 2:762-5.
42. Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008; 9:616-27.
43. Gatei M, Young D, Cerosaletti KM, Desai-Mehta A, Spring K, Kozlov S, et al. ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat Genet 2000; 25:115-9.
44. D'Amours D, Jackson SP. The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat Rev Mol Cell Biol 2002; 3:317-27.
45. Yue J, Wang Q, Lu H, Brenneman M, Fan F, Shen Z. The cytoskeleton protein filamin-A is required for an efficient recombinational DNA double strand break repair. Cancer Res 2009; 69:7978-85.
46. Iftode C, Daniely Y, Borowiec JA. Replication protein A (RPA): the eukaryotic SSB. Crit Rev Biochem Mol Biol 1999; 34:141-80. (Pubitemid 29326003)
47. Golub EI, Gupta RC, Haaf T, Wold MS, Radding CM. Interaction of human rad51 recombination protein with single-stranded DNA binding protein, RPA. Nucleic Acids Res 1998; 26:5388-93.
48. Vassin VM, Wold MS, Borowiec JA. Replication protein A (RPA) phosphorylation prevents RPA association with replication centers. Mol Cell Biol 2004; 24:1930-43.
49. Karlsson KH, Stenerlow B. Extensive ssDNA end formation at DNA double-strand breaks in nonhomologous end-joining deficient cells during the S phase. BMC Mol Biol 2007; 8:97.
50. Mahaney BL, Meek K, Lees-Miller SP. Repair of ionizing radiation-induced DNA double-strand breaks by non-homologous end-joining. Biochem J 2009; 417:639-50.
51. Weterings E, Chen DJ. DNA-dependent protein kinase in nonhomologous end joining: a lock with multiple keys? J Cell Biol 2007; 179:183-6.
52. Calsou P, Frit P, Humbert O, Muller C, Chen DJ, Salles B. The DNA-dependent protein kinase catalytic activity regulates DNA end processing by means of Ku entry into DNA. J Biol Chem 1999; 274:7848-56.
53. Reddy YV, Ding Q, Lees-Miller SP, Meek K, Ramsden DA. Non-homologous end joining requires that the DNA-PK complex undergo an autophosphorylation- dependent rearrangement at DNA ends. J Biol Chem 2004; 279:39408-13.
54. Yun MH, Hiom K. CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature 2009; 459:460-3.
55. Wu X, Petrini JH, Heine WF, Weaver DT, Livingston DM, Chen J. Independence of R/M/N focus formation and the presence of intact BRCA1. Science 2000; 289:11.
56. Zhong Q, Chen CF, Li S, Chen Y, Wang CC, Xiao J, et al. Association of BRCA1 with the hRad50-hMre11-p95 complex and the DNA damage response. Science 1999; 285:747-50.
57. Paull TT, Cortez D, Bowers B, Elledge SJ, Gellert M. Direct DNA binding by Brca1. Proc Natl Acad Sci USA 2001; 98:6086-91.
58. Chen JJ, Silver D, Cantor S, Livingston DM, Scully R. BRCA1, BRCA2 and Rad51 operate in a common DNA damage response pathway. Cancer Res 1999; 59:1752-6.
59. Cousineau I, Abaji C, Belmaaza A. 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 2005; 65:11384-91.
60. Lisby M, Mortensen UH, Rothstein R. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 2003; 5:572-7.
61. Misteli T, Soutoglou E. The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat Rev Mol Cell Biol 2009; 10:243-54.
62. Soutoglou E, Dorn JF, Sengupta K, Jasin M, Nussenzweig A, Ried T, et al. Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 2007; 9:675-82.
63. Tanaka M, Gupta R, Mayer BJ. Differential inhibition of signaling pathways by dominant-negative SH2/SH3 adapter proteins. Mol Cell Biol 1995; 15:6829-37.
64. 1-phase prereplication complex. J Cell Biol 1999; 146:709-22.
65. Editorial. How robust is your data? Nat Cell Biol 2009; 11:667-70.