Involvement of Matrin 3 and SFPQ/NONO in the DNA damage response

Cell Cycle

Volumn 9, Issue 8, 2010, Pages 1568-1576

  Salton, Maayan ^a   Lerenthal, Yaniv ^a   Wang, Shih Ya ^b   Chen, David J ^b   Shiloh, Yosef ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

ATM; Cell cycle checkpoint; DNA damage response; Matrin 3; NONO p54; SFPQ PSF

Indexed keywords

ATM PROTEIN; CELL PROTEIN; MATRILYSIN; MATRILYSIN 3; PROTEIN P54; SPLICING FACTOR, PROLINE AND GLUTAMINE RICH; UNCLASSIFIED DRUG; ZINOSTATIN;

ARTICLE; CELL CYCLE; CELL CYCLE S PHASE; CELL NUCLEUS MATRIX; DNA DAMAGE; DNA STRAND BREAKAGE; HUMAN; HUMAN CELL; LASER; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

EID: 77953564663     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.9.8.11298     Document Type: Article

References (74)

1. Hahn WC, Weinberg RA. Modelling the molecular circuitry of cancer. Nat Rev 2002; 2:1-3.
2. Murga M, Fernandez-Capetillo O. Genomic instability: on the birth and death of cancer. Clin Transl Oncol 2007; 9:216-20.
3. Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008; 319:1352-5. (Pubitemid 351354863)
4. Harrison JC, Haber JE. Surviving the breakup: the DNA damage checkpoint. Annu Rev Genet 2006; 40:209-35.
5. Su TT. Cellular responses to DNA damage: one signal, multiple choices. Annu Rev Genet 2006; 40:187-208. (Pubitemid 44956784)
6. Bartek J, Lukas J. DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 2007; 19:238-45. (Pubitemid 46386406)
7. Bassing CH, Alt FW. The cellular response to general and programmed DNA double strand breaks. DNA Repair 2004; 3:781-96.
8. Helleday T, Lo J, van Gent DC, Engelward BP. DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amst) 2007; 6:923-35. (Pubitemid 46880473)
9. van Gent DC, van der Burg M. Non-homologous endjoining, a sticky affair. Oncogene 2007; 26:7731-40.
10. Wyman C, Kanaar R. DNA double-strand break repair: all's well that ends well. Annu Rev Genet 2006; 40:363-83. (Pubitemid 44291620)
11. Lukas J, Bartek J. Watching the DNA repair ensemble dance. Cell 2004; 118:666-8. (Pubitemid 39221726)
12. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, Bartek J, Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. Journ Cell Biol 2006; 173:195-206.
13. Riches LC, Lynch AM, Gooderham NJ. Early events in the mammalian response to DNA double-strand breaks. Mutagenesis 2008; 23:331-9.
14. Shiloh Y. The ATM-mediated DNA-damage response: taking shape. Trends Biochem Sci 2006; 31:402-10. (Pubitemid 44038916)
15. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 2003; 3:155-68. (Pubitemid 37328868)
16. Lee JH, Paull TT. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 2007; 26:7741-8.
17. Lavin MF. ATM and the Mre11 complex combine to recognize and signal DNA double-strand breaks. Oncogene 2007; 26:7749-58.
18. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506.
19. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, 3rd, Hurov KE, Luo J, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 2007; 316:1160-6. (Pubitemid 46877472)
20. Mu JJ, Wang Y, Luo H, Leng M, Zhang J, Yang T, et al. A proteomic analysis of ataxia telangiectasia-mutated (ATM)/ATM-Rad3-related (ATR) substrates identifies the ubiquitin-proteasome system as a regulator for DNA damage checkpoints. J Biol Chem 2007; 282:17330-4.
21. Lavin MF, Kozlov S. DNA damage-induced signalling in ataxia- telangiectasia and related syndromes. Radiother Oncol 2007; 83:231-7.
22. Chun HH, Gatti RA. Ataxia-telangiectasia, an evolving phenotype. DNA Repair (Amst) 2004; 3:1187-96.
23. Lavin MF. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol 2008; 9:759-69.
24. Lovejoy CA, Cortez D. Common mechanisms of PIKK regulation. DNA Repair (Amst) 2009; 8:1004-8.
25. Weterings E, Chen DJ. DNA-dependent protein kinase in nonhomologous end joining: a lock with multiple keys? J Cell Biol 2007; 179:183-6.
26. Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008; 9:616-27.
27. 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.
28. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J, Jackson SP. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 2006; 8:37-45.
29. Callen E, Jankovic M, Wong N, Zha S, Chen HT, Difilippantonio S, et al. Essential role for DNA-PKcs in DNA double-strand break repair and apoptosis in ATM-deficient lymphocytes. Mol Cell 2009; 34:285-97.
30. Belgrader P, Dey R, Berezney R. Molecular cloning of matrin 3. A 125-kilodalton protein of the nuclear matrix contains an extensive acidic domain. J Biol Chem 1991; 266:9893-9. (Pubitemid 21906738)
31. Cohen TV, Hernandez L, Stewart CL. Functions of the nuclear envelope and lamina in development and disease. Biochem Soc Trans 2008; 36:1329-34.
32. Nakayasu H, Berezney R. Nuclear matrins: identification of the major nuclear matrix proteins. Proc Natl Acad Sci USA 1991; 88:10312-6.
33. Hisada-Ishii S, Ebihara M, Kobayashi N, Kitagawa Y. Bipartite nuclear localization signal of matrin 3 is essential for vertebrate cells. Biochem Biophys Res Commun 2007; 354:72-6.
34. Giordano G, Sanchez-Perez AM, Montoliu C, Berezney R, Malyavantham K, Costa LG, et al. Activation of NMDA receptors induces protein kinase A-mediated phosphorylation and degradation of matrin 3. Blocking these effects prevents NMDA-induced neuronal death. J Neurochem 2005; 94:808-18.
35. Fuchs D, Dirscherl B, Schroot JH, Daniel H, Wenzel U. Soy extract has different effects compared with the isolated isoflavones on the proteome of homocysteine-stressed endothelial cells. Mol Nutr Food Res 2006; 50:58-69.
36. Bernert G, Fountoulakis M, Lubec G. Manifold decreased protein levels of matrin 3, reduced motor protein HMP and hlark in fetal Down's syndrome brain. Proteomics 2002; 2:1752-7.
37. Bimpaki EI, Iliopoulos D, Moraitis A, Stratakis CA. MicroRNA signature in massive macronodular adrenocortical disease and implications for adrenocortical tumorigenesis. Clin Endocrinol (Oxf) 2009; In press.
38. Senderek J, Garvey SM, Krieger M, Guergueltcheva V, Urtizberea A, Roos A, et al. Autosomal-dominant distal myopathy associated with a recurrent missense mutation in the gene encoding the nuclear matrix protein, matrin 3. Am J Human Genet 2009; 84:511-8.
39. Zhang Z, Carmichael GG. The fate of dsRNA in the nucleus: a p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell 2001; 106:465-75.
40. Bond CS, Fox AH. Paraspeckles: nuclear bodies built on long noncoding RNA. J Cell Biol 2009; 186:637-44.
41. Sasaki YT, Ideue T, Sano M, Mituyama T, Hirose T. MENepsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc Natl Acad Sci USA 2009; 106:2525-30.
42. Fox AH, Lam YW, Leung AK, Lyon CE, Andersen J, Mann M, Lamond AI. Paraspeckles: a novel nuclear domain. Curr Biol 2002; 12:13-25.
43. Shav-Tal Y, Zipori D. PSF and p54(nrb)/NonO - multi-functional nuclear proteins. FEBS Lett 2002; 531:109-14.
44. Buxade M, Morrice N, Krebs DL, Proud CG. The PSF. p54nrb complex is a novel Mnk substrate that binds the mRNA for tumor necrosis factor alpha. J Biol Chem 2008; 283:57-65.
45. Hata K, Nishimura R, Muramatsu S, Matsuda A, Matsubara T, Amano K, et al. Paraspeckle protein p54nrb links Sox9-mediated transcription with RNA processing during chondrogenesis in mice. J Clin Invest 2008; 118:3098-108.
46. Dong X, Sweet J, Challis JR, Brown T, Lye SJ. Transcriptional activity of androgen receptor is modulated by two RNA splicing factors, PSF and p54nrb. Mol Cell Biol 2007; 27:4863-75.
47. Rosonina E, Ip JY, Calarco JA, Bakowski MA, Emili A, McCracken S, et al. Role for PSF in mediating transcriptional activator-dependent stimulation of pre-mRNA processing in vivo. Mol Cell Biol 2005; 25:6734-46.
48. Kaneko S, Rozenblatt-Rosen O, Meyerson M, Manley JL. The multifunctional protein p54nrb/PSF recruits the exonuclease XRN2 to facilitate pre-mRNA 3′ processing and transcription termination. Genes Dev 2007; 21:1779-89.
49. Ito T, Watanabe H, Yamamichi N, Kondo S, Tando T, Haraguchi T, et al. Brm transactivates the telomerase reverse transcriptase (TERT) gene and modulates the splicing patterns of its transcripts in concert with p54(nrb). Biochem J 2008; 411:201-9.
50. Kameoka S, Duque P, Konarska MM. p54(nrb) associates with the 5′ splice site within large transcription/splicing complexes. EMBO J 2004; 23:1782-91. (Pubitemid 38649641)
51. Patton JG, Porro EB, Galceran J, Tempst P, Nadal-Ginard B. Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev 1993; 7:393-406. (Pubitemid 23139233)
52. Bladen CL, Udayakumar D, Takeda Y, Dynan WS. 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 2005; 280:5205-10. (Pubitemid 40279991)
53. Morozumi Y, Takizawa Y, Takaku M, Kurumizaka H. Human PSF binds to RAD51 and modulates its homologous-pairing and strand-exchange activities. Nucleic Acids Res 2009; 37:4296-307.
54. Mu JJ, Wang Y, Luo H, Leng M, Zhang J, Yang T, et al. A proteomic analysis of ataxia telangiectasia-mutated (ATM)/ATM-Rad3-related (ATR) substrates identifies the ubiquitin-proteasome system as a regulator for DNA damage checkpoints. J Biol Chem 2007; 282:17330-4. (Pubitemid 47100266)
55. Williams RS, Williams JS, Tainer JA. Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template. Biochem Cell Biol 2007; 85:509-20.
56. FitzGerald JE, Grenon M, Lowndes NF. 53BP1: function and mechanisms of focal recruitment. Biochem Soc Trans 2009; 37:897-904.
57. Liu L, Lee S, Zhang J, Peters SB, Hannah J, Zhang Y, et al. CUL4A abrogation augments DNA damage response and protection against skin carcinogenesis. Mol Cell 2009; 34:451-60.
58. Zhang WW, Zhang LX, Busch RK, Farres J, Busch H. Purification and characterization of a DNA-binding heterodimer of 52 and 100 kDa from HeLa cells. Biochem J 1993; 290:267-72. (Pubitemid 23081228)
59. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell 2007; 28:739-45.
60. Doil C, Mailand N, Bekker-Jensen S, Menard P, Larsen DH, Pepperkok R, et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 2009; 136:435-46.
61. Galanty Y, Belotserkovskaya R, Coates J, Polo S, Miller KM, Jackson SP. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 2009; 462:935-9.
62. Stewart GS, Panier S, Townsend K, Al-Hakim AK, Kolas NK, Miller ES, et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 2009; 136:420-34.
63. Pinato S, Scandiuzzi C, Arnaudo N, Citterio E, Gaudino G, Penengo L. RNF168, a new RING finger, MIU-containing protein that modifies chromatin by ubiquitination of histones H2A and H2AX. BMC Mol Biol 2009; 10:55.
64. Gagne JP, Isabelle M, Lo KS, Bourassa S, Hendzel MJ, Dawson VL, et al. Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADPribose)-associated protein complexes. Nucleic Acids Res 2008; 36:6959-76.
65. Quenet D, El Ramy R, Schreiber V, Dantzer F. The role of poly(ADP-ribosyl)ation in epigenetic events. Int J Biochem Cell Biol 2009; 41:60-5.
66. Zegerman P, Diffley JF. DNA replication as a target of the DNA damage checkpoint. DNA Repair 2009; 8:1077-88.
67. Bi X, Barkley LR, Slater DM, Tateishi S, Yamaizumi M, Ohmori H, Vaziri C. Rad18 regulates DNA polymerase kappa and is required for recovery from S-phase checkpoint-mediated arrest. Mol Cell Biol 2006; 26:3527-40.
68. Shtam TA, Varfolomeeva I, Semenova EV, Filatov MV. Human RAD51 recombinase: the role in the cell cycle checkpoint and cellular survival. Tsitologiia 2008; 50:958-63.
69. Rajesh C, Gruver AM, Basrur V, Pittman DL. The interaction profile of homologous recombination repair proteins RAD51C, RAD51D and XRCC2 as determined by proteomic analysis. Proteomics 2009; 9:4071-86.
70. Zhao Y, Thomas HD, Batey MA, Cowell IG, Richardson CJ, Griffin RJ, et al. Preclinical evaluation of a potent novel DNA-dependent protein kinase inhibitor NU7441. Cancer Res 2006; 66:5354-62. (Pubitemid 43844961)
71. Paulsen RD, Soni DV, Wollman R, Hahn AT, Yee MC, Guan A, et al. A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol Cell 2009; 35:228-39.
72. Ziv Y, Bielopolski D, Galanty Y, Lukas C, Taya Y, Schultz DC, et al. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat Cell Biol 2006; 8:870-6.
73. Uematsu N, Weterings E, Yano K, Morotomi-Yano K, Jakob B, Taucher-Scholz G, et al. Autophosphorylation of DNA-PKCS regulates its dynamics at DNA doublestrand breaks. J Cell Biol 2007; 177:219-29. (Pubitemid 46658634)
74. Dinant C, de Jager M, Essers J, van Cappellen WA, Kanaar R, Houtsmuller AB, Vermeulen W. Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J Cell Sci 2007; 120:2731-40.