Involvement of the nuclear proteasome activator PA28γ in the cellular response to DNA double-strand breaks

Cell Cycle

Volumn 10, Issue 24, 2011, Pages 4300-4310

  Levy Barda, Adva ^a   Lerenthal, Yaniv ^a   Davis, Anthony J ^b   Chung, Young Min ^c   Essers, Jeroen ^d   Shao, Zhengping ^b   Van Vliet, Nicole ^d   Chen, David J ^b   Hu, Mickey C T ^c   Kanaar, Roland ^d   Ziv, Yael ^a   Shiloh, Yosef ^a  

^a TEL AVIV UNIVERSITY   (Israel)

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

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

ATM; DNA repair; Double strand breaks; Genomic stability; PA28 (PSME3); Proteasome

Indexed keywords

2 MORPHOLINO 6 (1 THIANTHRENYL) 4 PYRANONE; PROTEASOME; PROTEASOME ACTIVATOR PA28 GAMMA; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; ZINOSTATIN;

ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FEMALE; FLOW CYTOMETRY; HELA CELL; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84055184842     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.24.18642     Document Type: Article

References (72)

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. Hiom K. Coping with DNA double strand breaks. DNA Repair (Amst) 2010; 9:1256-63; PMID:21115283; http://dx.doi.org/10.1016/j.dnarep.2010.09.018.
3. Lieber MR. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 2010; 79:181-211; PMID:20192759; http://dx.doi.org/10.1146/annurev. biochem.052308.093131.
4. Mladenov E, Iliakis G. Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways. Mutat Res 2011; 711:61-72; PMID:21329706; http://dx.doi. org/10.1016/j.mrfmmm.2011.02.005.
5. Holthausen JT, Wyman C, Kanaar R. Regulation of DNA strand exchange in homologous recombination. DNA Repair (Amst) 2010; 9:1264-72; PMID:20971042; http://dx.doi.org/10.1016/j. dnarep.2010.09.014.
6. Warmerdam DO, Kanaar R. Dealing with DNA damage: relationships between checkpoint and repair pathways. Mutat Res 2010; 704:2-11; PMID:20006736; http://dx.doi.org/10.1016/j.mrrev.2009.12.001.
7. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, Bartek J, et al. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol 2006; 173:195-206; PMID:16618811; http://dx.doi. org/10.1083/jcb.200510130.
8. Bekker-Jensen S, Rendtlew Danielsen J, Fugger K, Gromova I, Nerstedt A, Lukas C, et al. HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat Cell Biol 2010; 12:80-6.
9. Lukas J, Lukas C, Bartek J. More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 2011; 13:1161-9; PMID:21968989; http://dx.doi. org/10.1038/ncb2344.
10. Lovejoy CA, Cortez D. Common mechanisms of PIKK regulation. DNA Repair (Amst) 2009; 8:1004- 8; PMID:19464237; http://dx.doi.org/10.1016/j. dnarep.2009.04.006.
11. Bhatti S, Kozlov S, Farooqi AA, Naqi A, Lavin M, Khanna KK. ATM protein kinase: the linchpin of cellular defenses to stress. Cell Mol Life Sci 2011; 68:2977- 3006; PMID:21533982; http://dx.doi.org/10.1007/ s00018-011-0683-9.
12. Polo SE, Jackson SP. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 2011; 25:409-33; PMID:21363960; http://dx.doi.org/10.1101/ gad.2021311.
13. Ramaekers CH, Wouters BG. Regulatory functions of ubiquitin in diverse DNA damage responses. Curr Mol Med 2011; 11:152-69; PMID:21342128; http:// dx.doi.org/10.2174/156652411794859269.
14. Derheimer FA, Kastan MB. Multiple roles of ATM in monitoring and maintaining DNA integrity. FEBS Lett 2010; 584:3675-81; PMID:20580718; http://dx.doi. org/10.1016/j.febslet.2010.05.031.
15. 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; PMID:18813293; http:// dx.doi.org/10.1038/nrm2514.
16. Perlman SL, Boder Deceased E, Sedgewick RP, Gatti RA. Ataxia-telangiectasia. Handb Clin Neurol 2011; 103:307-32; PMID:21827897; http://dx.doi. org/10.1016/B978-0-444-51892-7.00019-X.
17. Neal JA, Meek K. Choosing the right path: Does DNAPK help make the decision? Mutat Res 2011; 711:73- 86; PMID:21376743; http://dx.doi.org/10.1016/ j. mrfmmm.2011.02.010.
18. Nam EA, Cortez D. ATR signalling: more than meeting at the fork. Biochem J 2011; 436:527- 36; PMID:21615334; http://dx.doi.org/10.1042/ BJ20102162.
19. 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.
20. Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, Lobrich M, et al. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol Cell 2008; 31:167-77; PMID:18657500; http://dx.doi.org/10. 1016/j.molcel.2008.05.017.
21. Rechsteiner M, Hill CP. Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends Cell Biol 2005; 15:27- 33; PMID:15653075; http://dx.doi.org/10.1016/j. tcb.2004.11.003.
22. Hill CP, Masters EI, Whitby FG. The 11S regulators of 20S proteasome activity. Curr Top Microbiol Immunol 2002; 268:73-89; PMID:12083009; http://dx.doi. org/10.1007/978-3-642-59414-4-4.
23. Mao I, Liu J, Li X, Luo H. REGgamma, a proteasome activator and beyond? Cell Mol Life Sci 2008; 65:3971-80; PMID:18679578; http://dx.doi. org/10.1007/s00018-008-8291-z.
24. Stadtmueller BM, Hill CP. Proteasome activators. Mol Cell 2011; 41:8-19; PMID:21211719; http://dx.doi. org/10.1016/j.molcel.2010.12.020.
25. Li X, Lonard DM, Jung SY, Malovannaya A, Feng Q, Qin J, et al. The SRC-3/AIB1 coactivator is degraded in a ubiquitin- and ATP-independent manner by the REGgamma proteasome. Cell 2006; 124:381- 92; PMID:16439211; http://dx.doi.org/10.1016/j. cell.2005.11.037.
26. Nie J, Wu M, Wang J, Xing G, He F, Zhang L. REGgamma proteasome mediates degradation of the ubiquitin ligase Smurf1. FEBS Lett 2010; 584:3021- 7; PMID:20580715; http://dx.doi.org/10.1016/j.febslet. 2010.05.034.
27. Moriishi K, Shoji I, Mori Y, Suzuki R, Suzuki T, Kataoka C, et al. Involvement of PA28gamma in the propagation of hepatitis C virus. Hepatology 2010; 52:411-20; PMID:20683941; http://dx.doi. org/10.1002/hep.23680.
28. Suzuki R, Moriishi K, Fukuda K, Shirakura M, Ishii K, Shoji I, et al. Proteasomal turnover of hepatitis C virus core protein is regulated by two distinct mechanisms: a ubiquitin-dependent mechanism and a ubiquitinindependent but PA28gamma-dependent mechanism. J Virol 2009; 83:2389-92; PMID:19091860; http:// dx.doi.org/10.1128/JVI.01690-08.
29. Mori Y, Moriishi K, Matsuura Y. Hepatitis C virus core protein: its coordinate roles with PA28gamma in metabolic abnormality and carcinogenicity in the liver. Int J Biochem Cell Biol 2008; 40:1437-42; PMID:18321762; http://dx.doi.org/10.1016/j.biocel. 2008.01.027.
30. Ying H, Furuya F, Zhao L, Araki O, West BL, Hanover JA, et al. Aberrant accumulation of PTTG1 induced by a mutated thyroid hormone beta receptor inhibits mitotic progression. J Clin Invest 2006; 116:2972- 84; PMID:17039256; http://dx.doi.org/10.1172/ JCI28598.
31. Chen X, Barton LF, Chi Y, Clurman BE, Roberts JM. Ubiquitin-independent degradation of cell-cycle inhibitors by the REGgamma proteasome. Mol Cell 2007; 26:843-52; PMID:17588519; http://dx.doi. org/10.1016/j.molcel.2007.05.022.
32. Li X, Amazit L, Long W, Lonard DM, Monaco JJ, O'Malley BW. Ubiquitin- and ATP-independent proteolytic turnover of p21 by the REGgammaproteasome pathway. Mol Cell 2007; 26:831-42; PMID:17588518; http://dx.doi.org/10.1016/j.molcel. 2007.05.028.
33. Liu J, Yu G, Zhao Y, Zhao D, Wang Y, Wang L, et al. REGgamma modulates p53 activity by regulating its cellular localization. J Cell Sci 2010; 123:4076- 84; PMID:21084564; http://dx.doi.org/10.1242/ jcs.067405.
34. Zannini L, Lecis D, Buscemi G, Carlessi L, Gasparini P, Fontanella E, et al. REGgamma proteasome activator is involved in the maintenance of chromosomal stability. Cell Cycle 2008; 7:504-12; PMID:18235248; http:// dx.doi.org/10.4161/cc.7.4.5355.
35. Zannini L, Buscemi G, Fontanella E, Lisanti S, Delia D. REGgamma/PA28gamma proteasome activator interacts with PML and Chk2 and affects PML nuclear bodies number. Cell Cycle 2009; 8:2399- 407; PMID:19556897; http://dx.doi.org/10.4161/ cc.8.15.9084.
36. Xie A, Odate S, Chandramouly G, Scully R. H2AX post-translational modifications in the ionizing radiation response and homologous recombination. Cell Cycle 2010; 9:3602-10; PMID:20703100; http:// dx.doi.org/10.4161/cc.9.17. 12884.
37. Liao W, McNutt MA, Zhu WG. The comet assay: a sensitive method for detecting DNA damage in individual cells. Methods 2009; 48:46-53; PMID:19269328; http://dx.doi.org/10.1016/j.ymeth.2009.02.016.
38. Tsai WB, Chung YM, Takahashi Y, Xu Z, Hu MC. Functional interaction between FOXO3a and ATM regulates DNA damage response. Nat Cell Biol 2008; 10:460-7; PMID:18344987; http://dx.doi. org/10.1038/ncb1709.
39. Moyal L, Lerenthal Y, Gana-Weisz M, Mass G, So S, Wang SY, et al. Requirement of ATM-Dependent Monoubiquitylation of Histone H2B for Timely Repair of DNA Double-Strand Breaks. Mol Cell 2011; 41:529-42; PMID:21362549; http://dx.doi. org/10.1016/j.molcel.2011.02.015.
40. Stap J, Krawczyk PM, Van Oven CH, Barendsen GW, Essers J, Kanaar R, et al. Induction of linear tracks of DNA double-strand breaks by alpha-particle irradiation of cells. Nat Methods 2008; 5:261- 6; PMID:18309310; http://dx.doi.org/10.1038/ nmeth.f.206.
41. Kinoshita E, Kinoshita-Kikuta E, Ujihara H, Koike T. Mobility shift detection of phosphorylation on large proteins using a Phos-tag SDS-PAGE gel strengthened with agarose. Proteomics 2009; 9:4098- 101; PMID:19658103; http://dx.doi.org/10.1002/ pmic.200900020.
42. Hagemann C, Patel R, Blank JL. MEKK3 interacts with the PA28 gamma regulatory subunit of the proteasome. Biochem J 2003; 373:71-9; PMID:12650640; http://dx.doi.org/10.1042/BJ20021758.
43. Wu Y, Wang L, Zhou P, Wang G, Zeng Y, Wang Y, et al. Regulation of REGgamma cellular distribution and function by SUMO modification. Cell Res 2011; 21:807-16; PMID:21445096; http://dx.doi. org/10.1038/cr.2011.57.
44. Blickwedehl J, Agarwal M, Seong C, Pandita RK, Melendy T, Sung P, et al. Role for proteasome activator PA200 and postglutamyl proteasome activity in genomic stability. Proc Natl Acad Sci USA 2008; 105:16165-70; PMID:18845680; http://dx.doi. org/10.1073/pnas.0803145105.
45. Blickwedehl J, McEvoy S, Wong I, Kousis P, Clements J, Elliott R, et al. Proteasomes and proteasome activator 200 kDa (PA200) accumulate on chromatin in response to ionizing radiation. Radiat Res 2007; 167:663-74; PMID:17523843; http://dx.doi. org/10.1667/RR0690.1.
46. Russell SJ, Reed SH, Huang W, Friedberg EC, Johnston SA. The 19S regulatory complex of the proteasome functions independently of proteolysis in nucleotide excision repair. Mol Cell 1999; 3:687-95; PMID:10394357; http://dx.doi.org/10.1016/S1097- 2765(01)80001-0.
47. Jacquemont C, Taniguchi T. Proteasome function is required for DNA damage response and fanconi anemia pathway activation. Cancer Res 2007; 67:7395-405; PMID:17671210; http://dx.doi.org/10.1158/0008-5472.CAN-07-1015.
48. Ben-Aroya S, Agmon N, Yuen K, Kwok T, McManus K, Kupiec M, et al. Proteasome nuclear activity affects chromosome stability by controlling the turnover of Mms22, a protein important for DNA repair. PLoS Genet 2010; 6:1000852; PMID:20174551; http:// dx.doi.org/10.1371/journal.pgen.1000852.
49. Gudmundsdottir K, Lord CJ, Ashworth A. The proteasome is involved in determining differential utilization of double-strand break repair pathways. Oncogene 2007; 26:7601-6; PMID:17563742; http://dx.doi. org/10.1038/sj.onc. 1210579.
50. Lin CP, Ban Y, Lyu YL, Desai SD, Liu LF. A ubiquitin- proteasome pathway for the repair of topoisomerase I-DNA covalent complexes. J Biol Chem 2008; 283:21074-83; PMID:18515798; http://dx.doi. org/10.1074/jbc.M803493200.
51. Ju D, Wang X, Ha SW, Fu J, Xie Y. Inhibition of proteasomal degradation of rpn4 impairs nonhomologous end-joining repair of DNA double-strand breaks. PLoS ONE 2010; 5:9877; PMID:20376190; http://dx.doi. org/10.1371/journal.pone. 0009877.
52. Schauber C, Chen L, Tongaonkar P, Vega I, Lambertson D, Potts W, et al. Rad23 links DNA repair to the ubiquitin/ proteasome pathway. Nature 1998; 391:715-8; PMID:9490418; http://dx.doi.org/10.1038/35661.
53. Krogan NJ, Lam MH, Fillingham J, Keogh MC, Gebbia M, Li J, et al. Proteasome involvement in the repair of DNA double-strand breaks. Mol Cell 2004; 16:1027-34; PMID:15610744; http://dx.doi. org/10.1016/j.molcel.2004.11.033.
54. Raman M, Havens CG, Walter JC, Harper JW. A Genome-wide Screen Identifies p97 as an Essential Regulator of DNA Damage-Dependent CDT1 Destruction. Mol Cell 2011; 44:72-84; PMID:21981919; http://dx.doi.org/10.1016/j.molcel. 2011.06.036.
55. Wagner SA, Beli P, Weinert BT, Nielsen ML, Cox J, Mann M, Choudhary C. A. Proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 2011; 10:111.013284; PMID:21890473; http://dx.doi. org/10.1074/mcp.M111.013284.
56. Cabrera R, Sha Z, Vadakkan TJ, Otero J, Kriegenburg F, Hartmann-Petersen R, et al. Proteasome nuclear import mediated by Arc3 can influence efficient DNA damage repair and mitosis in Schizosaccharomyces pombe. Mol Biol Cell 2010; 21:3125-36; PMID:20668161; http:// dx.doi.org/10.1091/mbc.E10-06-0506.
57. Chen S, Blank JL, Peters T, Liu XJ, Rappoli DM, Pickard MD, et al. Genome-wide siRNA screen for modulators of cell death induced by proteasome inhibitor bortezomib. Cancer Res 2010; 70:4318-26; PMID:20460535; http://dx.doi.org/10.1158/0008-5472.CAN-09-4428.
58. Zecevic A, Hagan E, Reynolds M, Poage G, Johnston T, Zhitkovich A. XPA impacts formation but not proteasome-sensitive repair of DNA-protein cross-links induced by chromate. Mutagenesis 2010; 25:381-8; PMID:20410141; http://dx.doi.org/10.1093/mutage/ geq017.
59. Kim W, Bennett EJ, Huttlin EL, Guo A, Li J, Possemato A, et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol Cell 2011; 44:325-40; PMID:21906983; http://dx.doi. org/10.1016/j.molcel.2011. 08.025.
60. Ramadan K, Meerang M. Degradation-linked ubiquitin signal and proteasome are integral components of DNA double strand break repair: New perspectives for anti-cancer therapy. FEBS Lett 2011; 585:2868-75; PMID:21536036; http://dx.doi.org/10.1016/j.febslet. 2011.04.046.
61. Shi W, Ma Z, Willers H, Akhtar K, Scott SP, Zhang J, et al. Disassembly of MDC1 foci is controlled by ubiquitin-proteasome-dependent degradation. J Biol Chem 2008; 283:31608-16; PMID:18757370; http:// dx.doi.org/10.1074/jbc. M801082200.
62. Shi W, Ma Z, Willers H, Akhtar K, Scott SP, Zhang J, et al. Disassembly of MDC1 foci is controlled by ubiquitin-proteasome-dependent degradation. J Biol Chem 2008; 283:31608-16; PMID:18757370; http:// dx.doi.org/10.1074/jbc. M801082200.
63. Murakawa Y, Sonoda E, Barber LJ, Zeng W, Yokomori K, Kimura H, et al. Inhibitors of the proteasome suppress homologous DNA recombination in mammalian cells. Cancer Res 2007; 67:8536-43; PMID:17875693; http://dx.doi.org/10.1158/ 0008-5472.CAN-07-1166.
64. Al-Hakim A, Escribano-Diaz C, Landry MC, O'Donnell L, Panier S, Szilard RK, et al. The ubiquitous role of ubiquitin in the DNA damage response. DNA Repair (Amst) 2010; 9:1229-40; PMID:21056014; http://dx.doi.org/10.1016/j. dnarep.2010.09.011.
65. Lukas J. The interface between the ubiquitin family and the DNA damage response. EMBO Rep 2010; 11:907-9; PMID:21072060; http://dx.doi. org/10.1038/embor.2010.180.
66. Moriishi K, Okabayashi T, Nakai K, Moriya K, Koike K, Murata S, et al. Proteasome activator PA28gammadependent nuclear retention and degradation of hepatitis C virus core protein. J Virol 2003; 77:10237- 49; PMID:12970408; http://dx.doi.org/10.1128/ JVI.77.19.10237-49.2003.
67. Salton M, Lerenthal Y, Wang SY, Chen DJ, Shiloh Y. Involvement of matrin 3 and SFPQ/NONO in the DNA damage response. Cell Cycle 2010; 9:1568- 76; PMID:20421735; http://dx.doi.org/10.4161/ cc.9.8.11298.
68. Agarwal S, van Cappellen WA, Guenole A, Eppink B, Linsen SE, Meijering E, et al. ATP-dependent and independent functions of Rad54 in genome maintenance. J Cell Biol 2011; 192:735-50; PMID:21357745; http:// dx.doi.org/10.1083/jcb. 201011025.
69. Puget N, Knowlton M, Scully R. Molecular analysis of sister chromatid recombination in mammalian cells. DNA Repair (Amst) 2005; 4:149-61; PMID:15590323; http://dx.doi.org/10.1016/j. dnarep.2004.08.010.
70. Mansour WY, Schumacher S, Rosskopf R, Rhein T, Schmidt-Petersen F, Gatzemeier F, et al. Hierarchy of nonhomologous end-joining, single-strand annealing and gene conversion at site-directed DNA doublestrand breaks. Nucleic Acids Res 2008; 36:4088- 98; PMID:18539610; http://dx.doi.org/10.1093/nar/ gkn347.
71. Pierce AJ, Johnson RD, Thompson LH, Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 1999; 13:2633-8; PMID:10541549; http://dx.doi. org/10.1101/gad.13.20.2633.
72. Vindeløv LL, Christensen IJ. A review of techniques and results obtained in one laboratory by an integrated system of methods designed for routine clinical flow cytometric DNA analysis. Cytometry 1990; 11:753-70; PMID:2272241; http://dx.doi.org/10.1002/ cyto.990110702.