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Downregulation of Wip1 phosphatase modulates the cellular threshold of DNA damage signaling in mitosis

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Pages 251-262 | Published online: 15 Jan 2012

References

  • Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 2003; 3:155 - 68; http://dx.doi.org/10.1038/nrc1011; PMID: 12612651
  • 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; http://dx.doi.org/10.1038/ncb2344; PMID: 21968989
  • Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, Jackson SP. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 2005; 123:1213 - 26; http://dx.doi.org/10.1016/j.cell.2005.09.038; PMID: 16377563
  • Huen MSY, Grant R, Manke I, Minn K, Yu X, Yaffe MB, et al. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 2007; 131:901 - 14; http://dx.doi.org/10.1016/j.cell.2007.09.041; PMID: 18001825
  • Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, Lukas C, et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 2007; 131:887 - 900; http://dx.doi.org/10.1016/j.cell.2007.09.040; PMID: 18001824
  • 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; http://dx.doi.org/10.1016/j.cell.2008.12.041; PMID: 19203579
  • 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, 1-12; http://dx.doi.org/10.1038/ncb2008; PMID: 20023648
  • Moudry P, Lukas C, Macurek L, Hanzlikova H, Hodny Z, Lukas J, et al. Ubiquitin-activating enzyme UBA1 is required for cellular response to DNA damage. Cell Cycle 2012; 11:1573 - 82; http://dx.doi.org/10.4161/cc.19978; PMID: 22456334
  • Chapman JR, Taylor MR, Boulton SJ. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 2012; 47:497 - 510; http://dx.doi.org/10.1016/j.molcel.2012.07.029; PMID: 22920291
  • Lukas C, Savic V, Bekker-Jensen S, Doil C, Neumann B, Pedersen RS, et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol 2011; 13:243 - 53; http://dx.doi.org/10.1038/ncb2201; PMID: 21317883
  • Harrigan JA, Belotserkovskaya R, Coates J, Dimitrova DS, Polo SE, Bradshaw CR, et al. Replication stress induces 53BP1-containing OPT domains in G1 cells. J Cell Biol 2011; 193:97 - 108; http://dx.doi.org/10.1083/jcb.201011083; PMID: 21444690
  • Giunta S, Belotserkovskaya R, Jackson SP. DNA damage signaling in response to double-strand breaks during mitosis. J Cell Biol 2010; 190:197 - 207; http://dx.doi.org/10.1083/jcb.200911156; PMID: 20660628
  • Giunta S, Jackson SP. Give me a break, but not in mitosis: the mitotic DNA damage response marks DNA double-strand breaks with early signaling events. Cell Cycle 2011; 10:1215 - 21; http://dx.doi.org/10.4161/cc.10.8.15334; PMID: 21412056
  • Harris DR, Bunz F. Protein phosphatases and the dynamics of the DNA damage response. Cell Cycle 2010; 9:861 - 9; http://dx.doi.org/10.4161/cc.9.5.10862; PMID: 20348842
  • Shreeram S, Demidov ON, Hee WK, Yamaguchi H, Onishi N, Kek C, et al. Wip1 phosphatase modulates ATM-dependent signaling pathways. Mol Cell 2006; 23:757 - 64; http://dx.doi.org/10.1016/j.molcel.2006.07.010; PMID: 16949371
  • Fujimoto H, Onishi N, Kato N, Takekawa M, Xu XZ, Kosugi A, et al. Regulation of the antioncogenic Chk2 kinase by the oncogenic Wip1 phosphatase. Cell Death Differ 2006; 13:1170 - 80; http://dx.doi.org/10.1038/sj.cdd.4401801; PMID: 16311512
  • Lu X, Ma O, Nguyen T-A, Jones SN, Oren M, Donehower LA. The Wip1 Phosphatase acts as a gatekeeper in the p53-Mdm2 autoregulatory loop. Cancer Cell 2007; 12:342 - 54; http://dx.doi.org/10.1016/j.ccr.2007.08.033; PMID: 17936559
  • Lu X, Nannenga B, Donehower LA. PPM1D dephosphorylates Chk1 and p53 and abrogates cell cycle checkpoints. Genes Dev 2005; 19:1162 - 74; http://dx.doi.org/10.1101/gad.1291305; PMID: 15870257
  • Macůrek L, Lindqvist A, Voets O, Kool J, Vos HR, Medema RH. Wip1 phosphatase is associated with chromatin and dephosphorylates gammaH2AX to promote checkpoint inhibition. Oncogene 2010; 29:2281 - 91; http://dx.doi.org/10.1038/onc.2009.501; PMID: 20101220
  • Moon S, Lin L, Zhang X, Nguyen T, Darlington Y, Waldman A. Wildtype p53-induced phosphatase 1 dephosphorylates histone variant {gamma}-H2AX and suppresses DNA double strand break repair. J Biol Chem 2010; 23:12935 - 47; http://dx.doi.org/10.1074/jbc.M109.071696
  • Cha H, Lowe JM, Li H, Lee J-S, Belova GI, Bulavin DV, et al. Wip1 directly dephosphorylates γ-H2AX and attenuates the DNA damage response. Cancer Res 2010; 70:4112 - 22; http://dx.doi.org/10.1158/0008-5472.CAN-09-4244; PMID: 20460517
  • Lu X, Nguyen TA, Moon SH, Darlington Y, Sommer M, Donehower LA. The type 2C phosphatase Wip1: an oncogenic regulator of tumor suppressor and DNA damage response pathways. Cancer Metastasis Rev 2008; 27:123 - 35; http://dx.doi.org/10.1007/s10555-008-9127-x; PMID: 18265945
  • Fiscella M, Zhang H, Fan S, Sakaguchi K, Shen S, Mercer WE, et al. Wip1, a novel human protein phosphatase that is induced in response to ionizing radiation in a p53-dependent manner. Proc Natl Acad Sci USA 1997; 94:6048 - 53; http://dx.doi.org/10.1073/pnas.94.12.6048; PMID: 9177166
  • Zhang X, Wan G, Mlotshwa S, Vance V, Berger FG, Chen H, et al. Oncogenic Wip1 phosphatase is inhibited by miR-16 in the DNA damage signaling pathway. Cancer Res 2010; 70:7176 - 86; http://dx.doi.org/10.1158/0008-5472.CAN-10-0697; PMID: 20668064
  • Lindqvist A, de Bruijn M, Macurek L, Brás A, Mensinga A, Bruinsma W, et al. Wip1 confers G2 checkpoint recovery competence by counteracting p53-dependent transcriptional repression. EMBO J 2009; 28:3196 - 206; http://dx.doi.org/10.1038/emboj.2009.246; PMID: 19713933
  • Nannenga B, Lu X, Dumble M, Van Maanen M, Nguyen T-A, Sutton R, et al. Augmented cancer resistance and DNA damage response phenotypes in PPM1D null mice. Mol Carcinog 2006; 45:594 - 604; http://dx.doi.org/10.1002/mc.20195; PMID: 16652371
  • Bulavin DV, Phillips C, Nannenga B, Timofeev O, Donehower LA, Anderson CW, et al. Inactivation of the Wip1 phosphatase inhibits mammary tumorigenesis through p38 MAPK-mediated activation of the p16(Ink4a)-p19(Arf) pathway. Nat Genet 2004; 36:343 - 50; http://dx.doi.org/10.1038/ng1317; PMID: 14991053
  • Shreeram S, Hee WK, Demidov ON, Kek C, Yamaguchi H, Fornace AJ Jr., et al. Regulation of ATM/p53-dependent suppression of myc-induced lymphomas by Wip1 phosphatase. J Exp Med 2006; 203:2793 - 9; http://dx.doi.org/10.1084/jem.20061563; PMID: 17158963
  • Rauta J, Alarmo E-L, Kauraniemi P, Karhu R, Kuukasjärvi T, Kallioniemi A. The serine-threonine protein phosphatase PPM1D is frequently activated through amplification in aggressive primary breast tumours. Breast Cancer Res Treat 2006; 95:257 - 63; http://dx.doi.org/10.1007/s10549-005-9017-7; PMID: 16254685
  • Bulavin DV, Demidov ON, Saito S, Kauraniemi P, Phillips C, Amundson SA, et al. Amplification of PPM1D in human tumors abrogates p53 tumor-suppressor activity. Nat Genet 2002; 31:210 - 5; http://dx.doi.org/10.1038/ng894; PMID: 12021785
  • Li J, Yang Y, Peng Y, Austin RJ, van Eyndhoven WG, Nguyen KCQ, et al. Oncogenic properties of PPM1D located within a breast cancer amplification epicenter at 17q23. Nat Genet 2002; 31:133 - 4; http://dx.doi.org/10.1038/ng888; PMID: 12021784
  • Castellino RC, De Bortoli M, Lu X, Moon S-H, Nguyen T-A, Shepard MA, et al. Medulloblastomas overexpress the p53-inactivating oncogene WIP1/PPM1D. J Neurooncol 2008; 86:245 - 56; http://dx.doi.org/10.1007/s11060-007-9470-8; PMID: 17932621
  • Saito-Ohara F, Imoto I, Inoue J, Hosoi H, Nakagawara A, Sugimoto T, et al. PPM1D is a potential target for 17q gain in neuroblastoma. Cancer Res 2003; 63:1876 - 83; PMID: 12702577
  • Tan DSP, Lambros MBK, Rayter S, Natrajan R, Vatcheva R, Gao Q, et al. PPM1D is a potential therapeutic target in ovarian clear cell carcinomas. Clin Cancer Res 2009; 15:2269 - 80; http://dx.doi.org/10.1158/1078-0432.CCR-08-2403; PMID: 19293255
  • Bolderson E, Scorah J, Helleday T, Smythe C, Meuth M. ATM is required for the cellular response to thymidine induced replication fork stress. Hum Mol Genet 2004; 13:2937 - 45; http://dx.doi.org/10.1093/hmg/ddh316; PMID: 15459181
  • Sakaue-Sawano A, Kurokawa H, Morimura T, Hanyu A, Hama H, Osawa H, et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 2008; 132:487 - 98; http://dx.doi.org/10.1016/j.cell.2007.12.033; PMID: 18267078
  • Song JY, Han H-S, Sabapathy K, Lee B-M, Yu E, Choi J. Expression of a homeostatic regulator, Wip1 (wild-type p53-induced phosphatase), is temporally induced by c-Jun and p53 in response to UV irradiation. J Biol Chem 2010; 285:9067 - 76; http://dx.doi.org/10.1074/jbc.M109.070003; PMID: 20093361
  • Vassilev LT, Tovar C, Chen S, Knezevic D, Zhao X, Sun H, et al. Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc Natl Acad Sci USA 2006; 103:10660 - 5; http://dx.doi.org/10.1073/pnas.0600447103; PMID: 16818887
  • Skaar JR, Pagano M. Control of cell growth by the SCF and APC/C ubiquitin ligases. Curr Opin Cell Biol 2009; 21:816 - 24; http://dx.doi.org/10.1016/j.ceb.2009.08.004; PMID: 19775879
  • Koepp DM, Schaefer LK, Ye X, Keyomarsi K, Chu C, Harper JW, et al. Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 2001; 294:173 - 7; http://dx.doi.org/10.1126/science.1065203; PMID: 11533444
  • Chan EH, Santamaria A, Silljé HH, Nigg EA. Plk1 regulates mitotic Aurora A function through betaTrCP-dependent degradation of hBora. Chromosoma 2008; 117:457 - 69; http://dx.doi.org/10.1007/s00412-008-0165-5; PMID: 18521620
  • Wolthuis R, Clay-Farrace L, van Zon W, Yekezare M, Koop L, Ogink J, et al. Cdc20 and Cks direct the spindle checkpoint-independent destruction of cyclin A. Mol Cell 2008; 30:290 - 302; http://dx.doi.org/10.1016/j.molcel.2008.02.027; PMID: 18471975
  • den Elzen N, Pines J. Cyclin A is destroyed in prometaphase and can delay chromosome alignment and anaphase. J Cell Biol 2001; 153:121 - 36; http://dx.doi.org/10.1083/jcb.153.1.121; PMID: 11285279
  • Geley S, Kramer E, Gieffers C, Gannon J, Peters J-M, Hunt T. Anaphase-promoting complex/cyclosome-dependent proteolysis of human cyclin A starts at the beginning of mitosis and is not subject to the spindle assembly checkpoint. J Cell Biol 2001; 153:137 - 48; http://dx.doi.org/10.1083/jcb.153.1.137; PMID: 11285280
  • Yamada S, Nakamura H, Kinoshita E, Kinoshita-Kikuta E, Koike T, Shiro Y. Separation of a phosphorylated histidine protein using phosphate affinity polyacrylamide gel electrophoresis. Anal Biochem 2007; 360:160 - 2; http://dx.doi.org/10.1016/j.ab.2006.10.005; PMID: 17092477
  • Dinkel H, Michael S, Weatheritt RJ, Davey NE, Van Roey K, Altenberg B, et al. ELM--the database of eukaryotic linear motifs. Nucleic Acids Res 2012; 40:Database issue D242 - 51; http://dx.doi.org/10.1093/nar/gkr1064; PMID: 22110040
  • Moon S-H, Nguyen T-A, Darlington Y, Lu X, Donehower LA. Dephosphorylation of γ-H2AX by WIP1: an important homeostatic regulatory event in DNA repair and cell cycle control. Cell Cycle 2010; 9:2092 - 6; http://dx.doi.org/10.4161/cc.9.11.11810; PMID: 20495376
  • Ichijima Y, Sakasai R, Okita N, Asahina K, Mizutani S, Teraoka H. Phosphorylation of histone H2AX at M phase in human cells without DNA damage response. Biochem Biophys Res Commun 2005; 336:807 - 12; http://dx.doi.org/10.1016/j.bbrc.2005.08.164; PMID: 16153602
  • McManus KJ, Hendzel MJ. ATM-dependent DNA damage-independent mitotic phosphorylation of H2AX in normally growing mammalian cells. Mol Biol Cell 2005; 16:5013 - 25; http://dx.doi.org/10.1091/mbc.E05-01-0065; PMID: 16030261
  • Hickson I, Zhao Y, Richardson CJ, Green SJ, Martin NMB, Orr AI, et al. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res 2004; 64:9152 - 9; http://dx.doi.org/10.1158/0008-5472.CAN-04-2727; PMID: 15604286
  • Leahy JJJ, Golding BT, Griffin RJ, Hardcastle IR, Richardson C, Rigoreau L, et al. Identification of a highly potent and selective DNA-dependent protein kinase (DNA-PK) inhibitor (NU7441) by screening of chromenone libraries. Bioorg Med Chem Lett 2004; 14:6083 - 7; http://dx.doi.org/10.1016/j.bmcl.2004.09.060; PMID: 15546735
  • Reaper PM, Griffiths MR, Long JM, Charrier J-D, Maccormick S, Charlton PA, et al. Selective killing of ATM- or p53-deficient cancer cells through inhibition of ATR. Nat Chem Biol 2011; 7:428 - 30; http://dx.doi.org/10.1038/nchembio.573; PMID: 21490603
  • Le Guezennec X, Bulavin DV. WIP1 phosphatase at the crossroads of cancer and aging. Trends Biochem Sci 2010; 35:109 - 14; http://dx.doi.org/10.1016/j.tibs.2009.09.005; PMID: 19879149
  • Lu X, Nguyen T-A, Donehower LA. Reversal of the ATM/ATR-mediated DNA damage response by the oncogenic phosphatase PPM1D. Cell Cycle 2005; 4:1060 - 4; http://dx.doi.org/10.4161/cc.4.8.1876; PMID: 15970689
  • Zhu Y-H, Zhang C-W, Lu L, Demidov ON, Sun L, Yang L, et al. Wip1 regulates the generation of new neural cells in the adult olfactory bulb through p53-dependent cell cycle control. Stem Cells 2009; 27:1433 - 42; http://dx.doi.org/10.1002/stem.65; PMID: 19489034
  • Choi J, Nannenga B, Demidov ON, Bulavin DV, Cooney A, Brayton C, et al. Mice deficient for the wild-type p53-induced phosphatase gene (Wip1) exhibit defects in reproductive organs, immune function, and cell cycle control. Mol Cell Biol 2002; 22:1094 - 105; http://dx.doi.org/10.1128/MCB.22.4.1094-1105.2002; PMID: 11809801
  • Petermann E, Caldecott KW. Evidence that the ATR/Chk1 pathway maintains normal replication fork progression during unperturbed S phase. Cell Cycle 2006; 5:2203 - 9; http://dx.doi.org/10.4161/cc.5.19.3256; PMID: 16969104
  • Yang C, Tang X, Guo X, Niikura Y, Kitagawa K, Cui K, et al. Aurora-B mediated ATM serine 1403 phosphorylation is required for mitotic ATM activation and the spindle checkpoint. Mol Cell 2011; 44:597 - 608; http://dx.doi.org/10.1016/j.molcel.2011.09.016; PMID: 22099307
  • Hubackova S, Novakova Z, Krejcikova K, Kosar M, Dobrovolna J, Duskova P, et al. Regulation of the PML tumor suppressor in drug-induced senescence of human normal and cancer cells by JAK/STAT-mediated signaling. Cell Cycle 2010; 9:3085 - 99; http://dx.doi.org/10.4161/cc.9.15.12521; PMID: 20699642
  • Lindqvist A, van Zon W, Karlsson Rosenthal C, Wolthuis RMF. Cyclin B1-Cdk1 activation continues after centrosome separation to control mitotic progression. PLoS Biol 2007; 5:e123; http://dx.doi.org/10.1371/journal.pbio.0050123; PMID: 17472438
  • Kosar M, Bartkova J, Hubackova S, Hodny Z, Lukas J, Bartek J. Senescence-associated heterochromatin foci are dispensable for cellular senescence, occur in a cell type- and insult-dependent manner and follow expression of p16(ink4a). Cell Cycle 2011; 10:457 - 68; http://dx.doi.org/10.4161/cc.10.3.14707; PMID: 21248468

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