Protein phosphatase PP4 is involved in NHEJ-mediated repair of DNA double-strand breaks

Cell Cycle

Volumn 11, Issue 14, 2012, Pages 2643-2649

  Liu, Jinping ^a   Xu, Linli ^a   Zhong, Jianing ^a   Liao, Ji ^a   Li, Jing ^a   Xu, Xingzhi ^a  

^a CAPITAL NORMAL UNIVERSITY   (China)

Author keywords

DNA double strand break repair; DNA repair; KAP1; Nonhomologous end joining; Protein phosphatase PP4

Indexed keywords

DOUBLE STRANDED DNA; KRAB ASSOCIATED PROTEIN 1; PHOSPHOPROTEIN PHOSPHATASE; PP4C PROTEIN; PP4R2 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA REPAIR; GENE OVEREXPRESSION; IN VITRO STUDY; NONHUMAN; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

EID: 84864389301     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.20957     Document Type: Article

References (37)

1. Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell 2010; 40:179-204; PMID:20965415; http://dx.doi.org/10. 1016/j. molcel.2010.09.019.
2. Sonoda E, Sasaki MS, Buerstedde JM, Bezzubova O, Shinohara A, Ogawa H, et al. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J 1998; 17:598-608; PMID:9430650; http://dx.doi.org/10.1093/ emboj/17.2.598.
3. Takata M, Sasaki MS, Sonoda E, Morrison C, Hashimoto M, Utsumi H, et al. 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 1998; 17:5497-508; PMID:9736627; http://dx.doi.org/10.1093/ emboj/17.18.5497.
4. Rothkamm K, Krüger I, Thompson LH, Löbrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol Cell Biol 2003; 23:5706-15; PMID:12897142; http://dx.doi.org/10.1128/MCB.23.16.5706-15.2003.
5. 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; PMID:19133841; http://dx.doi.org/10.1042/BJ20080413.
6. Moynahan ME, Jasin M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol 2010; 11:196-207; PMID:20177395; http://dx.doi.org/10.1038/ nrm2851.
7. Hawtin RE, Stockett DE, Wong OK, Lundin C, Helleday T, Fox JA. Homologous recombination repair is essential for repair of vosaroxin-induced DNA double-strand breaks. Oncotarget 2010; 1:606-19; PMID:21317456.
8. Kruhlak MJ, Celeste A, Dellaire G, Fernandez- Capetillo O, Müller WG, McNally JG, et al. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J Cell Biol 2006; 172:823-34; PMID:16520385; http://dx.doi.org/10.1083/jcb.200510015.
9. Kruhlak MJ, Celeste A, Nussenzweig A. Spatio-temporal dynamics of chromatin containing DNA breaks. Cell Cycle 2006; 5:1910-2; PMID:16929171; http://dx.doi.org/10.4161/cc.5.17.3169.
10. Morrison AJ, Highland J, Krogan NJ, Arbel- Eden A, Greenblatt JF, Haber JE, et al. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 2004; 119:767-75; PMID:15607974; http://dx.doi.org/10.1016/j.cell.2004.11.037.
11. Noon AT, Shibata A, Rief N, Löbrich M, Stewart GS, Jeggo PA, et al. 53BP1-dependent robust localized KAP-1 phosphorylation is essential for heterochromatic DNA double-strand break repair. Nat Cell Biol 2010; 12:177-84; PMID:20081839; http://dx.doi.org/10.1038/ncb2017.
12. Tsukuda T, Fleming AB, Nickoloff JA, Osley MA. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 2005; 438:379-83; PMID:16292314; http://dx.doi.org/10.1038/ nature04148.
13. 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; PMID:16862143; http://dx.doi.org/10.1038/ncb1446.
14. Huntley S, Baggott DM, Hamilton AT, Tran-Gyamfi M, Yang S, Kim J, et al. A comprehensive catalog of human KRAB-associated zinc finger genes: insights into the evolutionary history of a large family of transcriptional repressors. Genome Res 2006; 16:669-77; PMID:16606702; http://dx.doi.org/10.1101/ gr.4842106.
15. Li X, Lee YK, Jeng JC, Yen Y, Schultz DC, Shih HM, et al. Role for KAP1 serine 824 phosphorylation and sumoylation/desumoylation switch in regulating KAP1-mediated transcriptional repression. J Biol Chem 2007; 282:36177-89; PMID:17942393; http:// dx.doi.org/10.1074/jbc.M706912200.
16. Goodarzi AA, Jeggo P, Lobrich M. The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax. DNA Repair (Amst) 2010; 9:1273-82; PMID:21036673; http:// dx.doi.org/10.1016/j.dnarep. 2010.09.013.
17. Moorhead GB, Trinkle-Mulcahy L, Ulke-Lemée A. Emerging roles of nuclear protein phosphatases. Nat Rev Mol Cell Biol 2007; 8:234-44; PMID:17318227; http://dx.doi.org/10.1038/nrm2126.
18. Chowdhury D, Keogh MC, Ishii H, Peterson CL, Buratowski S, Lieberman J. gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol Cell 2005; 20:801-9; PMID:16310392; http://dx.doi.org/10.1016/j.molcel.2005.10.003.
19. Chowdhury D, Xu X, Zhong X, Ahmed F, Zhong J, Liao J, et al. A PP4-phosphatase complex dephosphorylates gamma-H2AX generated during DNA replication. Mol Cell 2008; 31:33-46; PMID:18614045; http://dx.doi.org/10.1016/ j.molcel.2008.05.016.
20. Lee DH, Pan Y, Kanner S, Sung P, Borowiec JA, Chowdhury DA. A PP4 phosphatase complex dephosphorylates RPA2 to facilitate DNA repair via homologous recombination. Nat Struct Mol Biol 2010; 17:365-72; PMID:20154705; http://dx.doi.org/10.1038/nsmb.1769.
21. Yu YM, Pace SM, Allen SR, Deng CX, Hsu LCA. A PP1-binding motif present in BRCA1 plays a role in its DNA repair function. Int J Biol Sci 2008; 4:352-61; PMID:18953404; http://dx.doi.org/10.7150/ ijbs.4.352.
22. Zhong J, Liao J, Liu X, Wang P, Liu J, Hou W, et al. Protein phosphatase PP6 is required for homology-directed repair of DNA double-strand breaks. Cell Cycle 2011; 10:1411-9; PMID:21451261; http:// dx.doi.org/10.4161/cc.10.9.15479.
23. Moon SH, Lin L, Zhang X, Nguyen TA, Darlington Y, Waldman AS, et al. Wild-type p53-induced phosphatase- 1-dephosphorylates histone variant gamma-H2AX and suppresses DNA double strand break repair. J Biol Chem 2010; 285:12935-47; PMID:20118229; http:// dx.doi.org/10.1074/jbc.M109.071696.
24. Douglas P, Moorhead GB, Ye R, Lees-Miller SP. Protein phosphatases regulate DNA-dependent protein kinase activity. J Biol Chem 2001; 276:18992-8; PMID:11376007; http://dx.doi.org/10.1074/jbc.M011703200.
25. Douglas P, Moorhead G, Xu X, Lees-Miller S. Choreographing the DNA damage response: PP6 joins the dance. Cell Cycle 2010; 9:1221-2; PMID:20234171; http://dx.doi.org/10.4161/cc.9.7.11321.
26. Douglas P, Zhong J, Ye R, Moorhead GB, Xu X, Lees-Miller SP. Protein phosphatase 6 interacts with the DNA-dependent protein kinase catalytic subunit and dephosphorylates gamma-H2AX. Mol Cell Biol 2010; 30:1368-81; PMID:20065038; http://dx.doi.org/10.1128/MCB.00741-09.
27. Mi J, Dziegielewski J, Bolesta E, Brautigan DL, Larner JM. Activation of DNA-PK by ionizing radiation is mediated by protein phosphatase 6. PLoS One 2009; 4:4395; PMID:19198648; http://dx.doi.org/10.1371/ journal.pone.0004395.
28. Wechsler T, Chen BP, Harper R, Morotomi-Yano K, Huang BC, Meek K, et al. DNA-PKcs function regulated specifically by protein phosphatase 5. Proc Natl Acad Sci USA 2004; 101:1247-52; PMID:14734805; http://dx.doi.org/10.1073/pnas. 0307765100.
29. Bennardo N, Cheng A, Huang N, Stark JM. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 2008; 4:1000110; PMID:18584027; http://dx.doi.org/10.1371/journal.pgen. 1000110.
30. Gingras AC, Caballero M, Zarske M, Sanchez A, Hazbun TR, Fields S, et al. A novel, evolutionarily conserved protein phosphatase complex involved in cisplatin sensitivity. Mol Cell Proteomics 2005; 4:1725-40; PMID:16085932; http://dx.doi.org/10.1074/mcp. M500231-MCP200.
31. Rahal EA, Henricksen LA, Li Y, Williams RS, Tainer JA, Dixon K. ATM regulates Mre11-dependent DNA end-degradation and microhomology-mediated end joining. Cell Cycle 2010; 9:2866-77; PMID:20647759; http://dx.doi.org/10.4161/ cc.9.14.12363.
32. Levy-Barda A, Lerenthal Y, Davis AJ, Chung YM, Essers J, Shao Z, et al. Involvement of the nuclear proteasome activator PA28γ in the cellular response to DNA double-strand breaks. Cell Cycle 2011; 10:4300-10; PMID:22134242; http://dx.doi.org/10.4161/ cc.10.24.18642.
33. Hu C, Zhang S, Gao X, Xu X, Lv Y, Zhang Y, et al. Roles of the KRAB-associated co-repressor KAP1 S473 phosphorylation in DNA damage response. J Biol Chem 2012; PMID:22496453; http://dx.doi.org/10.1074/jbc.M111.313262.
34. Lee DH, Goodarzi AA, Adelmant GO, Pan Y, Jeggo PA, Marto JA, et al. Phosphoproteomic analysis reveals that PP4 dephosphorylates KAP-1 impacting the DNA damage response. EMBO J 2012; 31:2403-15; PMID:22491012; http://dx.doi.org/10.1038/ emboj.2012.86.
35. Xu X, Stern DF. NFBD1/KIAA0170 is a chromatin-associated protein involved in DNA damage signaling pathways. J Biol Chem 2003; 278:8795-803; PMID:12499369; http://dx.doi.org/10.1074/jbc.M211392200.
36. Xu X, Tsvetkov LM, Stern DF. Chk2 activation and phosphorylation- dependent oligomerization. Mol Cell Biol 2002; 22:4419-32; PMID:12024051; http:// dx.doi.org/10.1128/MCB.22.12.4419-32.2002.
37. 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; PMID:20016603; http://dx.doi.org/10.1038/ nature08657.