PARP activation regulates the RNA-binding protein NONO in the DNA damage response to DNA double-strand breaks

Nucleic Acids Research

Volumn 40, Issue 20, 2012, Pages 10287-10301

  Krietsch, Jana ^a,b   Caron, Marie Christine ^b   Gagné, Jean Philippe ^a   Ethier, Chantal ^a   Vignard, Julien ^b   Vincent, Michel ^a   Rouleau, Michéle ^a   Hendzel, Michael J ^c   Poirier, Guy G ^a   Masson, Jean Yves ^b  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NONO PROTEIN; POLY(ADENOSINE DIPHOSPHATE RIBOSE); RNA BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING COMPETITION; BINDING SITE; CELL STRAIN MCF 7; CELL SURVIVAL; CHROMATIN; CONTROLLED STUDY; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; HELA CELL; HOMOLOGOUS RECOMBINATION; IONIZING RADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MOTIF; RNA BINDING; RNA RECOGNITION MOTIF 1;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CHROMATIN; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; HELA CELLS; HOMOLOGOUS RECOMBINATION; HUMANS; MICE; NUCLEAR MATRIX-ASSOCIATED PROTEINS; OCTAMER TRANSCRIPTION FACTORS; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN INTERACTION DOMAINS AND MOTIFS; RADIATION, IONIZING; RNA-BINDING PROTEINS;

EID: 84869024542     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks798     Document Type: Article

References (61)

1. Vilenchik, M.M. and Knudson, A.G. (2003) Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc. Natl. Acad. Sci. USA, 100, 12871-12876.
2. Ciccia, A. and Elledge, S.J. (2010) The DNA damage response: making it safe to play with knives. Mol. Cell, 40, 179-204.
3. Wacker, D.A., Frizzell, K.M., Zhang, T. and Kraus, W.L. (2007) Regulation of chromatin structure and chromatin-dependent transcription by poly(ADP-ribose) polymerase-1: possible targets for drug-based therapies. Subcell Biochem., 41, 45-69.
4. Bouchard, V.J., Rouleau, M. and Poirier, G.G. (2003) PARP-1, a determinant of cell survival in response to DNA damage. Exp. Hematol., 31, 446-454.
5. Krishnakumar, R. and Kraus, W.L. (2010) The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol. Cell., 39, 8-24.
6. Haince, J.F., McDonald, D., Rodrigue, A., Dery, U., Masson, J.Y., Hendzel, M.J. and Poirier, G.G. (2008) PARP1-dependent kinetics of recruitment of MRE11 and NBS1 proteins to multiple DNA damage sites. J. Biol. Chem., 283, 1197-1208.
7. Slade, D., Dunstan, M.S., Barkauskaite, E., Weston, R., Lafite, P., Dixon, N., Ahel, M., Leys, D. and Ahel, I. (2011) The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature, 477, 616-620.
8. Takata, M., Sasaki, M.S., Sonoda, E., Morrison, C., Hashimoto, M., Utsumi, H., Yamaguchi-Iwai, Y., Shinohara, A. and Takeda, S. (1998) Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J., 17, 5497-5508.
9. Lieber, M.R. (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev. Biochem., 79, 181-211.
10. Gagne, J.P., Isabelle, M., Lo, K.S., Bourassa, S., Hendzel, M.J., Dawson, V.L., Dawson, T.M. and Poirier, G.G. (2008) Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res., 36, 6959-6976.
11. Li, B., Navarro, S., Kasahara, N. and Comai, L. (2004) Identification and biochemical characterization of a Werner's syndrome protein complex with Ku70/80 and poly(ADP-ribose) polymerase-1. J. Biol. Chem., 279, 13659-13667.
12. Meek, K., Dang, V. and Lees-Miller, S.P. (2008) DNA-PK: the means to justify the ends? Adv. Immunol., 99, 33-58.
13. Wang, J., Pluth, J.M., Cooper, P.K., Cowan, M.J., Chen, D.J. and Yannone, S.M. (2005) Artemis deficiency confers a DNA double-strand break repair defect and Artemis phosphorylation status is altered by DNA damage and cell cycle progression. DNA Repair (Amst), 4, 556-570.
14. Chappell, C., Hanakahi, L.A., Karimi-Busheri, F., Weinfeld, M. and West, S.C. (2002) Involvement of human polynucleotide kinase in double-strand break repair by non-homologous end joining. EMBO J., 21, 2827-2832.
15. Capp, J.P., Boudsocq, F., Bertrand, P., Laroche-Clary, A., Pourquier, P., Lopez, B.S., Cazaux, C., Hoffmann, J.S. and Canitrot, Y. (2006) The DNA polymerase lambda is required for the repair of non-compatible DNA double strand breaks by NHEJ in mammalian cells. Nucleic Acids Res., 34, 2998-3007.
16. Capp, J.P., Boudsocq, F., Besnard, A.G., Lopez, B.S., Cazaux, C., Hoffmann, J.S. and Canitrot, Y. (2007) Involvement of DNA polymerase mu in the repair of a specific subset of DNA double-strand breaks in mammalian cells. Nucleic Acids Res., 35, 3551-3560.
17. Ahnesorg, P., Smith, P. and Jackson, S.P. (2006) XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell, 124, 301-313.
18. Giffin, W., Torrance, H., Rodda, D.J., Prefontaine, G.G., Pope, L. and Hache, R.J. (1996) Sequence-specific DNA binding by Ku autoantigen and its effects on transcription. Nature, 380, 265-268.
19. Woodard, R.L., Lee, K.J., Huang, J. and Dynan, W.S. (2001) Distinct roles for Ku protein in transcriptional reinitiation and DNA repair. J. Biol. Chem., 276, 15423-15433.
20. Beck, B.D., Hah, D.S. and Lee, S.H. (2008) XPB and XPD between transcription and DNA repair. Adv. Exp. Med. Biol., 637, 39-46.
21. Adamson, B., Smogorzewska, A., Sigoillot, F.D., King, R.W. and Elledge, S.J. (2012) A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nat. Cell Biol., 14, 318-328.
22. Beli, P., Lukashchuk, N., Wagner, S.A., Weinert, B.T., Olsen, J.V., Baskcomb, L., Mann, M., Jackson, S.P. and Choudhary, C. (2012) Proteomic investigations reveal a role for RNA processing factor THRAP3 in the DNA damage response. Mol. Cell, 46, 212-225.
23. Paulsen, R.D., Soni, D.V., Wollman, R., Hahn, A.T., Yee, M.C., Guan, A., Hesley, J.A., Miller, S.C., Cromwell, E.F., Solow- Cordero, D.E. et al. (2009) A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol. Cell, 35, 228-239.
24. Peng, R., Dye, B.T., Perez, I., Barnard, D.C., Thompson, A.B. and Patton, J.G. (2002) PSF and p54nrb bind a conserved stem in U5 snRNA. RNA, 8, 1334-1347.
25. Zhang, Z. and Carmichael, G.G. (2001) The fate of dsRNA in the nucleus: a p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell, 106, 465-475.
26. Kaneko, S., Rozenblatt-Rosen, O., Meyerson, M. and Manley, J.L. (2007) The multifunctional protein p54nrb/PSF recruits the exonuclease XRN2 to facilitate pre-mRNA 30 processing and transcription termination. Genes Dev., 21, 1779-1789.
27. Amelio, A.L., Miraglia, L.J., Conkright, J.J., Mercer, B.A., Batalov, S., Cavett, V., Orth, A.P., Busby, J., Hogenesch, J.B. and Conkright, M.D. (2007) A coactivator trap identifies NONO (p54nrb) as a component of the cAMP-signaling pathway. Proc. Natl. Acad. Sci. USA, 104, 20314-20319.
28. Mathur, M., Tucker, P.W. and Samuels, H.H. (2001) PSF is a novel corepressor that mediates its effect through Sin3A and the DNA binding domain of nuclear hormone receptors. Mol. Cell Biol., 21, 2298-2311.
29. Dong, X., Sweet, J., Challis, J.R., Brown, T. and Lye, S.J. (2007) Transcriptional activity of androgen receptor is modulated by two RNA splicing factors, PSF and p54nrb. Mol. Cell Biol., 27, 4863-4875.
30. Ishitani, K., Yoshida, T., Kitagawa, H., Ohta, H., Nozawa, S. and Kato, S. (2003) p54nrb acts as a transcriptional coactivator for activation function 1 of the human androgen receptor. Biochem. Biophys. Res. Commun., 306, 660-665.
31. Salton, M., Lerenthal, Y., Wang, S.Y., Chen, D.J. and Shiloh, Y. (2010) Involvement of Matrin 3 and SFPQ/NONO in the DNA damage response. Cell Cycle, 9, 1568-1576.
32. Bladen, C.L., Udayakumar, D., Takeda, Y. and Dynan, W.S. (2005) Identification of the polypyrimidine tract binding protein-associated splicing factor.p54(nrb) complex as a candidate DNA double-strand break rejoining factor. J. Biol. Chem., 280, 5205-5210.
33. Li, S., Kuhne, W.W., Kulharya, A., Hudson, F.Z., Ha, K., Cao, Z. and Dynan, W.S. (2009) Involvement of p54(nrb), a PSF partner protein, in DNA double-strand break repair and radioresistance. Nucleic Acids Res., 37, 6746-6753.
34. Gagne, J.P., Haince, J.F., Pic, E. and Poirier, G.G. (2011) Affinity-based assays for the identification and quantitative evaluation of noncovalent poly(ADP-ribose)-binding proteins. Methods Mol. Biol., 780, 93-115.
35. Xie, A., Kwok, A. and Scully, R. (2009) Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol., 16, 814-818.
36. Pierce, A.J., Johnson, R.D., Thompson, L.H. and Jasin, M. (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev., 13, 2633-2638.
37. Duriez, P.J., Desnoyers, S., Hoflack, J.C., Shah, G.M., Morelle, B., Bourassa, S., Poirier, G.G. and Talbot, B. (1997) Characterization of anti-peptide antibodies directed towards the automodification domain and apoptotic fragment of poly (ADP-ribose) polymerase. Biochim. Biophys. Acta, 1334, 65-72.
38. Zou, L., Cortez, D. and Elledge, S.J. (2002) Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev., 16, 198-208.
39. Rodrigue, A., Lafrance, M., Gauthier, M.C., McDonald, D., Hendzel, M., West, S.C., Jasin, M. and Masson, J.Y. (2006) Interplay between human DNA repair proteins at a unique double-strand break in vivo. EMBO J., 25, 222-231.
40. Ismail, I.H., Gagne, J.P., Caron, M.C., McDonald, D., Xu, Z., Masson, J.Y., Poirier, G.G. and Hendzel, M.J. (2012) CBX4-mediated SUMO modification regulates BMI1 recruitment at sites of DNA damage. Nucleic Acids Res., 40, 5497-5510.
41. Gagne, J.P., Hunter, J.M., Labrecque, B., Chabot, B. and Poirier, G.G. (2003) A proteomic approach to the identification of heterogeneous nuclear ribonucleoproteins as a new family of poly(ADP-ribose)-binding proteins. Biochem. J., 371, 331-340.
42. Gagne, J.P., Pic, E., Isabelle, M., Krietsch, J., Ethier, C., Paquet, E., Kelly, I., Boutin, M., Moon, K.M., Foster, L.J. et al. (2012) Quantitative proteomics profiling of the poly(ADP-ribose)-related response to genotoxic stress. Nucleic Acids Res, 40, 7788-7805.
43. Smith, B.L., Bauer, G.B. and Povirk, L.F. (1994) DNA damage induced by bleomycin, neocarzinostatin, and melphalan in a precisely positioned nucleosome. Asymmetry in protection at the periphery of nucleosome-bound DNA. J. Biol. Chem., 269, 30587-30594.
44. Povirk, L.F. (1996) DNA damage and mutagenesis by radiomimetic DNA-cleaving agents: bleomycin, neocarzinostatin and other enediynes. Mutat. Res., 355, 71-89.
45. Tartier, L., Spenlehauer, C., Newman, H.C., Folkard, M., Prise, K.M., Michael, B.D., Menissier-de Murcia, J. and de Murcia, G. (2003) Local DNA damage by proton microbeam irradiation induces poly(ADP-ribose) synthesis in mammalian cells. Mutagenesis, 18, 411-416.
46. Rulten, S.L., Cortes-Ledesma, F., Guo, L., Iles, N.J. and Caldecott, K.W. (2008 Jul) APLF (C2orf13) is a novel component of poly(ADP-ribose) signaling in mammalian cells. Mol Cell Biol., 28, 4620-4628.
47. Ahel, D., Horejsi, Z., Wiechens, N., Polo, S.E., Garcia-Wilson, E., Ahel, I., Flynn, H., Skehel, M., West, S.C., Jackson, S.P. et al. (2009) Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science, 325, 1240-1243.
48. Fahrer, J., Kranaster, R., Altmeyer, M., Marx, A. and Burkle, A. (2007) Quantitative analysis of the binding affinity of poly(ADP-ribose) to specific binding proteins as a function of chain length. Nucleic Acids Res., 35, e143.
49. Malanga, M., Czubaty, A., Girstun, A., Staron, K. and Althaus, F.R. (2008) Poly(ADP-ribose) binds to the splicing factor ASF/SF2 and regulates its phosphorylation by DNA topoisomerase I. J. Biol. Chem., 283, 19991-19998.
50. Haince, J.F., Ouellet, M.E., McDonald, D., Hendzel, M.J. and Poirier, G.G. (2006) Dynamic relocation of poly(ADP-ribose) glycohydrolase isoforms during radiation-induced DNA damage. Biochim. Biophys. Acta, 1763, 226-237.
51. Shav-Tal, Y. and Zipori, D. (2002) PSF and p54(nrb)/ NonO-multi- functional nuclear proteins. FEBS Lett., 531, 109-114.
52. Pankotai, T., Bonhomme, C., Chen, D. and Soutoglou, E. (2012) DNAPKcs-dependent arrest of RNA polymerase II transcription in the presence of DNA breaks. Nat. Struct. Mol. Biol., 19, 276-282.
53. Polo, S.E., Blackford, A.N., Chapman, J.R., Baskcomb, L., Gravel, S., Rusch, A., Thomas, A., Blundred, R., Smith, P., Kzhyshkowska, J. et al. (2012) Regulation of DNA-end resection by hnRNPU-like proteins promotes DNA double-strand break signaling and repair. Mol. Cell, 45, 505-516.
54. Kraus, W.L. (2008) Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr. Opin. Cell. Biol., 20, 294-302.
55. Wang, M., Wu, W., Rosidi, B., Zhang, L., Wang, H. and Iliakis, G. (2006) PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res., 34, 6170-6182.
56. Mansour, W.Y., Rhein, T. and Dahm-Daphi, J. (2010) The alternative end-joining pathway for repair of DNA double-strand breaks requires PARP1 but is not dependent upon microhomologies. Nucleic Acids Res., 38, 6065-6077.
57. El-Khamisy, S.F., Masutani, M., Suzuki, H. and Caldecott, K.W. (2003) A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res., 31, 5526-5533.
58. Polo, S.E., Kaidi, A., Baskcomb, L., Galanty, Y. and Jackson, S.P. (2010) Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J., 29, 3130-3139.
59. Chou, D.M., Adamson, B., Dephoure, N.E., Tan, X., Nottke, A.C., Hurov, K.E., Gygi, S.P., Colaiacovo, M.P. and Elledge, S.J. (2010) A chromatin localization screen reveals poly(ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc. Natl. Acad. Sci. USA, 107, 18475-18480.
60. Shanbhag, N.M., Rafalska-Metcalf, I.U., Balane-Bolivar, C., Janicki, S.M. and Greenberg, R.A. (2010) ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell, 141, 970-981.
61. Schiffner, S., Zimara, N., Schmid, R. and Bosserhoff, A.K. (2011) p54nrb is a new regulator of progression of malignant melanoma. Carcinogenesis, 32, 1176-1182.