WIP1 phosphatase as pharmacological target in cancer therapy

. 2017 Jun ; 95 (6) : 589-599. [epub] 20170424

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články, přehledy, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid28439615
Odkazy

PubMed 28439615
PubMed Central PMC5442293
DOI 10.1007/s00109-017-1536-2
PII: 10.1007/s00109-017-1536-2
Knihovny.cz E-zdroje

DNA damage response (DDR) pathway protects cells from genome instability and prevents cancer development. Tumor suppressor p53 is a key molecule that interconnects DDR, cell cycle checkpoints, and cell fate decisions in the presence of genotoxic stress. Inactivating mutations in TP53 and other genes implicated in DDR potentiate cancer development and also influence the sensitivity of cancer cells to treatment. Protein phosphatase 2C delta (referred to as WIP1) is a negative regulator of DDR and has been proposed as potential pharmaceutical target. Until recently, exploitation of WIP1 inhibition for suppression of cancer cell growth was compromised by the lack of selective small-molecule inhibitors effective at cellular and organismal levels. Here, we review recent advances in development of WIP1 inhibitors and discuss their potential use in cancer treatment.

Zobrazit více v PubMed

Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature. 2009;461:1071–1078. doi: 10.1038/nature08467. PubMed DOI PMC

Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science. 2008;319:1352–1355. doi: 10.1126/science.1140735. PubMed DOI

Bartek J, Bartkova J, Lukas J. DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene. 2007;26:7773–7779. doi: 10.1038/sj.onc.1210881. PubMed DOI

Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K, Guldberg P, Sehested M, Nesland JM, Lukas C, et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature. 2005;434:864–870. doi: 10.1038/nature03482. PubMed DOI

Polo SE, Jackson SP. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 2011;25:409–433. doi: 10.1101/gad.2021311. PubMed DOI PMC

Lammers T, Lavi S. Role of type 2C protein phosphatases in growth regulation and in cellular stress signaling. Crit Rev Biochem Mol Biol. 2007;42:437–461. doi: 10.1080/10409230701693342. PubMed DOI

Fiscella M, Zhang H, Fan S, Sakaguchi K, Shen S, Mercer WE, Vande Woude GF, O’Connor PM, Appella E. Wip1, a novel human protein phosphatase that is induced in response to ionizing radiation in a p53-dependent manner. Proc Natl Acad Sci U S A. 1997;94:6048–6053. doi: 10.1073/pnas.94.12.6048. PubMed DOI PMC

Yamaguchi H, Minopoli G, Demidov ON, Chatterjee DK, Anderson CW, Durell SR, Appella E. Substrate specificity of the human protein phosphatase 2Cdelta, Wip1. Biochemistry. 2005;44:5285–5294. doi: 10.1021/bi0476634. PubMed DOI

Macurek 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;29:2281–2291. doi: 10.1038/onc.2009.501. PubMed DOI

Lu X, Nannenga B, Donehower LA. PPM1D dephosphorylates Chk1 and p53 and abrogates cell cycle checkpoints. Genes Dev. 2005;19:1162–1174. doi: 10.1101/gad.1291305. PubMed DOI PMC

Lindqvist A, de Bruijn M, Macurek L, Bras A, Mensinga A, Bruinsma W, Voets O, Kranenburg O, Medema RH. Wip1 confers G2 checkpoint recovery competence by counteracting p53-dependent transcriptional repression. EMBO J. 2009;28:3196–3206. doi: 10.1038/emboj.2009.246. PubMed DOI PMC

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;27:123–135. doi: 10.1007/s10555-008-9127-x. PubMed DOI PMC

Le Guezennec X, Bulavin DV. WIP1 phosphatase at the crossroads of cancer and aging. Trends Biochem Sci. 2010;35:109–114. doi: 10.1016/j.tibs.2009.09.005. PubMed DOI

Harrison M, Li J, Degenhardt Y, Hoey T, Powers S. Wip1-deficient mice are resistant to common cancer genes. Trends Mol Med. 2004;10:359–361. doi: 10.1016/j.molmed.2004.06.010. PubMed DOI

Leslie PL, Zhang Y (2016) MDM2 oligomers: antagonizers of the guardian of the genome. Oncogene. doi:10.1038/onc.2016.88 PubMed PMC

Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature. 1997;387:296–299. doi: 10.1038/387296a0. PubMed DOI

Pei D, Zhang Y, Zheng J. Regulation of p53: a collaboration between Mdm2 and Mdmx. Oncotarget. 2012;3:228–235. doi: 10.18632/oncotarget.443. PubMed DOI PMC

Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett. 1997;420:25–27. doi: 10.1016/S0014-5793(97)01480-4. PubMed DOI

Zhang XP, Liu F, Cheng Z, Wang W. Cell fate decision mediated by p53 pulses. Proc Natl Acad Sci U S A. 2009;106:12245–12250. doi: 10.1073/pnas.0813088106. PubMed DOI PMC

Leontieva OV, Gudkov AV, Blagosklonny MV. Weak p53 permits senescence during cell cycle arrest. Cell Cycle. 2010;9:4323–4327. doi: 10.4161/cc.9.21.13584. PubMed DOI

Lee Y-K, Thomas SN, Yang AJ, Ann DK. Doxorubicin down-regulates Krüppel-associated box domain-associated protein 1 sumoylation that relieves its transcription repression on p21WAF1/CIP1 in breast cancer MCF-7 cells. J Biol Chem. 2007;282:1595–1606. doi: 10.1074/jbc.M606306200. PubMed DOI

Blasius M, Forment JV, Thakkar N, Wagner SA, Choudhary C, Jackson SP. A phospho-proteomic screen identifies substrates of the checkpoint kinase Chk1. Genome Biol. 2011;12:R78–R78. doi: 10.1186/gb-2011-12-8-r78. PubMed DOI PMC

Chapman JR, Taylor Martin RG, Boulton Simon J. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell. 2012;47:497–510. doi: 10.1016/j.molcel.2012.07.029. PubMed DOI

Mamely I, van Vugt MATM, Smits VAJ, Semple JI, Lemmens B, Perrakis A, Medema RH, Freire R. Polo-like kinase-1 controls proteasome-dependent degradation of claspin during checkpoint recovery. Curr Biol. 2006;16:1950–1955. doi: 10.1016/j.cub.2006.08.026. PubMed DOI

Shaltiel IA, Krenning L, Bruinsma W, Medema RH. The same, only different—DNA damage checkpoints and their reversal throughout the cell cycle. J Cell Sci. 2015;128:607–620. doi: 10.1242/jcs.163766. PubMed DOI

Shaltiel IA, Aprelia M, Saurin AT, Chowdhury D, Kops GJ, Voest EE, Medema RH. Distinct phosphatases antagonize the p53 response in different phases of the cell cycle. Proc Natl Acad Sci U S A. 2014;111:7313–7318. doi: 10.1073/pnas.1322021111. PubMed DOI PMC

Lu X, Nguyen TA, Zhang X, Donehower LA. The Wip1 phosphatase and Mdm2: cracking the "Wip" on p53 stability. Cell Cycle. 2008;7:164–168. doi: 10.4161/cc.7.2.5299. PubMed DOI

Lu X, Ma O, Nguyen TA, Jones SN, Oren M, Donehower LA. The Wip1 phosphatase acts as a gatekeeper in the p53-Mdm2 autoregulatory loop. Cancer Cell. 2007;12:342–354. doi: 10.1016/j.ccr.2007.08.033. PubMed DOI

Zhang X, Lin L, Guo H, Yang J, Jones SN, Jochemsen A, Lu X. Phosphorylation and degradation of MdmX is inhibited by Wip1 phosphatase in the DNA damage response. Cancer Res. 2009;69:7960–7968. doi: 10.1158/0008-5472.CAN-09-0634. PubMed DOI PMC

Meulmeester E, Pereg Y, Shiloh Y, Jochemsen AG. ATM-mediated phosphorylations inhibit Mdmx/Mdm2 stabilization by HAUSP in favor of p53 activation. Cell Cycle. 2005;4:1166–1170. doi: 10.4161/cc.4.9.1981. PubMed DOI

Krenning L, Feringa Femke M, Shaltiel Indra A, van den Berg J, Medema René H. Transient activation of p53 in G2 phase is sufficient to induce senescence. Mol Cell. 2014;55:59–72. doi: 10.1016/j.molcel.2014.05.007. PubMed DOI

Müllers E, Cascales HS, Jaiswal H, Saurin AT, Lindqvist A. Nuclear translocation of cyclin B1 marks the restriction point for terminal cell cycle exit in G2 phase. Cell Cycle. 2014;13:2733–2743. doi: 10.4161/15384101.2015.945831. PubMed DOI PMC

Lee JS, Lee MO, Moon BH, Shim SH, Fornace AJ, Jr, Cha HJ. Senescent growth arrest in mesenchymal stem cells is bypassed by Wip1-mediated downregulation of intrinsic stress signaling pathways. Stem Cells. 2009;27:1963–1975. doi: 10.1002/stem.121. PubMed DOI

Sakai H, Fujigaki H, Mazur SJ, Appella E. Wild-type p53-induced phosphatase 1 (Wip1) forestalls cellular premature senescence at physiological oxygen levels by regulating DNA damage response signaling during DNA replication. Cell Cycle. 2014;13:1015–1029. doi: 10.4161/cc.27920. PubMed DOI PMC

Song JY, Ryu SH, Cho YM, Kim YS, Lee BM, Lee SW, Choi J. Wip1 suppresses apoptotic cell death through direct dephosphorylation of BAX in response to gamma-radiation. Cell Death Dis. 2013;4:e744. doi: 10.1038/cddis.2013.252. PubMed DOI PMC

Shreeram S, Demidov ON, Hee WK, Yamaguchi H, Onishi N, Kek C, Timofeev ON, Dudgeon C, Fornace AJ, Anderson CW, et al. Wip1 phosphatase modulates ATM-dependent signaling pathways. Mol Cell. 2006;23:757–764. doi: 10.1016/j.molcel.2006.07.010. PubMed DOI

Moon SH, Lin L, Zhang X, Nguyen TA, Darlington Y, Waldman AS, Lu X, Donehower LA. Wild-type p53-induced phosphatase 1 dephosphorylates histone variant gamma-H2AX and suppresses DNA double strand break repair. J Biol Chem. 2010;285:12935–12947. doi: 10.1074/jbc.M109.071696. PubMed DOI PMC

Cha H, Lowe JM, Li H, Lee JS, Belova GI, Bulavin DV, Fornace AJ., Jr Wip1 directly dephosphorylates gamma-H2AX and attenuates the DNA damage response. Cancer Res. 2010;70:4112–4122. doi: 10.1158/0008-5472.CAN-09-4244. PubMed DOI PMC

Yoda A, Xu XZ, Onishi N, Toyoshima K, Fujimoto H, Kato N, Oishi I, Kondo T, Minami Y. Intrinsic kinase activity and SQ/TQ domain of Chk2 kinase as well as N-terminal domain of Wip1 phosphatase are required for regulation of Chk2 by Wip1. J Biol Chem. 2006;281:24847–24862. doi: 10.1074/jbc.M600403200. PubMed DOI

Takekawa M, Adachi M, Nakahata A, Nakayama I, Itoh F, Tsukuda H, Taya Y, Imai K. p53-inducible wip1 phosphatase mediates a negative feedback regulation of p38 MAPK-p53 signaling in response to UV radiation. EMBO J. 2000;19:6517–6526. doi: 10.1093/emboj/19.23.6517. PubMed DOI PMC

Chew J, Biswas S, Shreeram S, Humaidi M, Wong ET, Dhillion MK, Teo H, Hazra A, Fang CC, Lopez-Collazo E, et al. WIP1 phosphatase is a negative regulator of NF-[kappa]B signalling. Nat Cell Biol. 2009;11:659–666. doi: 10.1038/ncb1873. PubMed DOI

Macurek L, Benada J, Mullers E, Halim VA, Krejcikova K, Burdova K, Pechackova S, Hodny Z, Lindqvist A, Medema RH, et al. Downregulation of Wip1 phosphatase modulates the cellular threshold of DNA damage signaling in mitosis. Cell Cycle. 2013;12:251–262. doi: 10.4161/cc.23057. PubMed DOI PMC

Choi Dong W, Na W, Kabir Mohammad H, Yi E, Kwon S, Yeom J, Ahn J-W, Choi H-H, Lee Y, Seo Kyoung W, et al. WIP1, a homeostatic regulator of the DNA damage response, is targeted by HIPK2 for phosphorylation and degradation. Mol Cell. 2013;51(3):374–385. doi: 10.1016/j.molcel.2013.06.010. PubMed DOI

Petitjean A, Achatz MIW, Borresen-Dale AL, Hainaut P, Olivier M. TP53 mutations in human cancers: functional selection and impact on cancer prognosis and outcomes. Oncogene. 2007;26:2157–2165. doi: 10.1038/sj.onc.1210302. PubMed DOI

Wang X, Sun Q. TP53 mutations, expression and interaction networks in human cancers. Oncotarget. 2016 PubMed PMC

Natrajan R, Lambros MB, Rodríguez-Pinilla SM, Moreno-Bueno G, Tan DSP, Marchió C, Vatcheva R, Rayter S, Mahler-Araujo B, Fulford LG, et al. Tiling path genomic profiling of grade 3 invasive ductal breast cancers. Clin Cancer Res. 2009;15:2711. doi: 10.1158/1078-0432.CCR-08-1878. PubMed DOI

Li J, Yang Y, Peng Y, Austin RJ, van Eyndhoven WG, Nguyen KC, Gabriele T, McCurrach ME, Marks JR, Hoey T, et al. Oncogenic properties of PPM1D located within a breast cancer amplification epicenter at 17q23. Nat Genet. 2002;31:133–134. doi: 10.1038/ng888. PubMed DOI

Ciriello G, Gatza Michael L, Beck Andrew H, Wilkerson Matthew D, Rhie Suhn K, Pastore A, Zhang H, McLellan M, Yau C, Kandoth C et al Comprehensive molecular portraits of invasive lobular breast cancer. Cell 163:506–519 PubMed PMC

Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6:pl1–pl1. doi: 10.1126/scisignal.2004088. PubMed DOI PMC

Shih-Chu Ho E, Lai C-R, Hsieh Y-T, Chen J-T, Lin A-J, Hung M-J, Liu F-S. p53 mutation is infrequent in clear cell carcinoma of the ovary. Gynecol Oncol. 2001;80:189–193. doi: 10.1006/gyno.2000.6025. PubMed DOI

Tan DS, Lambros MB, Rayter S, Natrajan R, Vatcheva R, Gao Q, Marchio C, Geyer FC, Savage K, Parry S, et al. PPM1D is a potential therapeutic target in ovarian clear cell carcinomas. Clin Cancer Res. 2009;15:2269–2280. doi: 10.1158/1078-0432.CCR-08-2403. PubMed DOI

Bulavin DV, Demidov ON, Saito S, Kauraniemi P, Phillips C, Amundson SA, Ambrosino C, Sauter G, Nebreda AR, Anderson CW, et al. Amplification of PPM1D in human tumors abrogates p53 tumor-suppressor activity. Nat Genet. 2002;31:210–215. doi: 10.1038/ng894. PubMed DOI

Liang C, Guo E, Lu S, Wang S, Kang C, Chang L, Liu L, Zhang G, Wu Z, Zhao Z, et al. Over-expression of wild-type p53-induced phosphatase 1 confers poor prognosis of patients with gliomas. Brain Res. 2012;1444:65–75. doi: 10.1016/j.brainres.2011.12.052. PubMed DOI

Rauta J, Alarmo EL, Kauraniemi P, Karhu R, Kuukasjarvi T, Kallioniemi A. The serine-threonine protein phosphatase PPM1D is frequently activated through amplification in aggressive primary breast tumours. Breast Cancer Res Treat. 2006;95:257–263. doi: 10.1007/s10549-005-9017-7. PubMed DOI

Peng TS, He YH, Nie T, Hu XD, Lu HY, Yi J, Shuai YF, Luo M. PPM1D is a prognostic marker and therapeutic target in colorectal cancer. Exp Ther Med. 2014;8:430–434. PubMed PMC

Castellino RC, De Bortoli M, Lu X, Moon SH, Nguyen TA, Shepard MA, Rao PH, Donehower LA, Kim JY. Medulloblastomas overexpress the p53-inactivating oncogene WIP1/PPM1D. J Neuro-Oncol. 2008;86:245–256. doi: 10.1007/s11060-007-9470-8. PubMed DOI PMC

Richter M, Dayaram T, Gilmartin AG, Ganji G, Pemmasani SK, Van Der Key H, Shohet JM, Donehower LA, Kumar R. WIP1 phosphatase as a potential therapeutic target in neuroblastoma. PLoS One. 2015;10:e0115635. doi: 10.1371/journal.pone.0115635. PubMed DOI PMC

Saito-Ohara F, Imoto I, Inoue J, Hosoi H, Nakagawara A, Sugimoto T, Inazawa J. PPM1D is a potential target for 17q gain in neuroblastoma. Cancer Res. 2003;63:1876–1883. PubMed

Satoh N, Maniwa Y, Bermudez VP, Nishimura K, Nishio W, Yoshimura M, Okita Y, Ohbayashi C, Hurwitz J, Hayashi Y. Oncogenic phosphatase Wip1 is a novel prognostic marker for lung adenocarcinoma patient survival. Cancer Sci. 2011;102:1101–1106. doi: 10.1111/j.1349-7006.2011.01898.x. PubMed DOI PMC

Fuku T, Semba S, Yutori H, Yokozaki H. Increased wild-type p53-induced phosphatase 1 (Wip1 or PPM1D) expression correlated with downregulation of checkpoint kinase 2 in human gastric carcinoma. Pathol Int. 2007;57:566–571. doi: 10.1111/j.1440-1827.2007.02140.x. PubMed DOI

Ruark E, Snape K, Humburg P, Loveday C, Bajrami I, Brough R, Rodrigues DN, Renwick A, Seal S, Ramsay E, et al. Mosaic PPM1D mutations are associated with predisposition to breast and ovarian cancer. Nature. 2013;493:406–410. doi: 10.1038/nature11725. PubMed DOI PMC

Kleiblova P, Shaltiel IA, Benada J, Sevcik J, Pechackova S, Pohlreich P, Voest EE, Dundr P, Bartek J, Kleibl Z, et al. Gain-of-function mutations of PPM1D/Wip1 impair the p53-dependent G1 checkpoint. J Cell Biol. 2013;201:511–521. doi: 10.1083/jcb.201210031. PubMed DOI PMC

Dudgeon C, Shreeram S, Tanoue K, Mazur SJ, Sayadi A, Robinson RC, Appella E, Bulavin DV. Genetic variants and mutations of PPM1D control the response to DNA damage. Cell Cycle. 2013;12:2656–2664. doi: 10.4161/cc.25694. PubMed DOI PMC

Swisher EM, Harrell MI, Norquist BM, et al. Somatic mosaic mutations in ppm1d and tp53 in the blood of women with ovarian carcinoma. JAMA Oncology. 2016;2:370–372. doi: 10.1001/jamaoncol.2015.6053. PubMed DOI PMC

Zhang L, Chen LH, Wan H, Yang R, Wang Z, Feng J, Yang S, Jones S, Wang S, Zhou W, et al. Exome sequencing identifies somatic gain-of-function PPM1D mutations in brainstem gliomas. Nat Genet. 2014;46:726–730. doi: 10.1038/ng.2995. PubMed DOI PMC

Zajkowicz A, Butkiewicz D, Drosik A, Giglok M, Suwinski R, Rusin M. Truncating mutations of PPM1D are found in blood DNA samples of lung cancer patients. Br J Cancer. 2015;112:1114–1120. doi: 10.1038/bjc.2015.79. PubMed DOI PMC

Cardoso M, Paulo P, Maia S, Teixeira MR. Truncating and missense PPM1D mutations in early-onset and/or familial/hereditary prostate cancer patients. Genes Chromosom Cancer. 2016;55:954–961. doi: 10.1002/gcc.22393. PubMed DOI

Yu E, Ahn YS, Jang SJ, Kim M-J, Yoon HS, Gong G, Choi J. Overexpression of the wip1 gene abrogates the p38 MAPK/p53/Wip1 pathway and silences p16 expression in human breast cancers. Breast Cancer Res Treat. 2007;101:269–278. doi: 10.1007/s10549-006-9304-y. PubMed DOI

Demidov ON, Kek C, Shreeram S, Timofeev O, Fornace AJ, Appella E, Bulavin DV. The role of the MKK6//p38 MAPK pathway in Wip1-dependent regulation of ErbB2-driven mammary gland tumorigenesis. Oncogene. 2006;26:2502–2506. doi: 10.1038/sj.onc.1210032. PubMed DOI

Demidov ON, Kek C, Shreeram S, Timofeev O, Fornace AJ, Appella E, Bulavin DV. The role of the MKK6/p38 MAPK pathway in Wip1-dependent regulation of ErbB2-driven mammary gland tumorigenesis. Oncogene. 2007;26:2502–2506. doi: 10.1038/sj.onc.1210032. PubMed DOI

Choi J, Nannenga B, Demidov ON, Bulavin DV, Cooney A, Brayton C, Zhang Y, Mbawuike IN, Bradley A, Appella E, 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;22:1094–1105. doi: 10.1128/MCB.22.4.1094-1105.2002. PubMed DOI PMC

Nannenga B, Lu X, Dumble M, Van Maanen M, Nguyen TA, Sutton R, Kumar TR, Donehower LA. Augmented cancer resistance and DNA damage response phenotypes in PPM1D null mice. Mol Carcinog. 2006;45:594–604. doi: 10.1002/mc.20195. PubMed DOI

Bulavin DV, Phillips C, Nannenga B, Timofeev O, Donehower LA, Anderson CW, Appella E, Fornace AJ., Jr Inactivation of the Wip1 phosphatase inhibits mammary tumorigenesis through p38 MAPK-mediated activation of the p16(Ink4a)-p19(Arf) pathway. Nat Genet. 2004;36:343–350. doi: 10.1038/ng1317. PubMed DOI

Shreeram S, Hee WK, Demidov ON, Kek C, Yamaguchi H, Fornace AJ, Jr, Anderson CW, Appella E, Bulavin DV. Regulation of ATM/p53-dependent suppression of myc-induced lymphomas by Wip1 phosphatase. J Exp Med. 2006;203:2793–2799. doi: 10.1084/jem.20061563. PubMed DOI PMC

Demidov ON, Timofeev O, Lwin HN, Kek C, Appella E, Bulavin DV. Wip1 phosphatase regulates p53-dependent apoptosis of stem cells and tumorigenesis in the mouse intestine. Cell Stem Cell. 2007;1:180–190. doi: 10.1016/j.stem.2007.05.020. PubMed DOI

Filipponi D, Muller J, Emelyanov A, Bulavin DV. Wip1 controls global heterochromatin silencing via ATM/BRCA1-dependent DNA methylation. Cancer Cell. 2013;24:528–541. doi: 10.1016/j.ccr.2013.08.022. PubMed DOI

Nguyen TA, Slattery SD, Moon SH, Darlington YF, Lu X, Donehower LA. The oncogenic phosphatase WIP1 negatively regulates nucleotide excision repair. DNA Repair (Amst) 2010;9:813–823. doi: 10.1016/j.dnarep.2010.04.005. PubMed DOI PMC

Lu X, Bocangel D, Nannenga B, Yamaguchi H, Appella E, Donehower LA. The p53-induced oncogenic phosphatase PPM1D interacts with uracil DNA glycosylase and suppresses base excision repair. Mol Cell. 2004;15:621–634. doi: 10.1016/j.molcel.2004.08.007. PubMed DOI

Zhang C, Lai L. Towards structure-based protein drug design. Biochem Soc Trans. 2011;39:1382–1386. doi: 10.1042/BST0391382. PubMed DOI

Gilmartin AG, Faitg TH, Richter M, Groy A, Seefeld MA, Darcy MG, Peng X, Federowicz K, Yang J, Zhang SY, et al. Allosteric Wip1 phosphatase inhibition through flap-subdomain interaction. Nat Chem Biol. 2014;10:181–187. doi: 10.1038/nchembio.1427. PubMed DOI

Chuman Y, Yagi H, Fukuda T, Nomura T, Matsukizono M, Shimohigashi Y, Sakaguchi K. Characterization of the active site and a unique uncompetitive inhibitor of the PPM1-type protein phosphatase PPM1D. Protein Pept Lett. 2008;15:938–948. doi: 10.2174/092986608785849236. PubMed DOI

Nakagawa H, Wardell CP, Furuta M, Taniguchi H, Fujimoto A. Cancer whole-genome sequencing: present and future. Oncogene. 2015;34:5943–5950. doi: 10.1038/onc.2015.90. PubMed DOI

Chuman Y, Kurihashi W, Mizukami Y, Nashimoto T, Yagi H, Sakaguchi K. PPM1D430, a novel alternative splicing variant of the human PPM1D, can dephosphorylate p53 and exhibits specific tissue expression. J Biochem. 2009;145:1–12. doi: 10.1093/jb/mvn135. PubMed DOI

Yoda A, Toyoshima K, Watanabe Y, Onishi N, Hazaka Y, Tsukuda Y, Tsukada J, Kondo T, Tanaka Y, Minami Y. Arsenic trioxide augments Chk2/p53-mediated apoptosis by inhibiting oncogenic Wip1 phosphatase. J Biol Chem. 2008;283:18969–18979. doi: 10.1074/jbc.M800560200. PubMed DOI

Miller WH, Schipper HM, Lee JS, Singer J, Waxman S. Mechanisms of action of arsenic trioxide. Cancer Res. 2002;62:3893–3903. PubMed

Belova GI, Demidov ON, Fornace AJ, Jr, Bulavin DV. Chemical inhibition of Wip1 phosphatase contributes to suppression of tumorigenesis. Cancer Biol Ther. 2005;4:1154–1158. doi: 10.4161/cbt.4.10.2204. PubMed DOI

Rayter S, Elliott R, Travers J, Rowlands MG, Richardson TB, Boxall K, Jones K, Linardopoulos S, Workman P, Aherne W, et al. A chemical inhibitor of PPM1D that selectively kills cells overexpressing PPM1D. Oncogene. 2008;27:1036–1044. doi: 10.1038/sj.onc.1210729. PubMed DOI

Lee JS, Park JR, Kwon OS, Kim H, Fornace AJ, Jr, Cha HJ. Off-target response of a Wip1 chemical inhibitor in skin keratinocytes. J Dermatol Sci. 2014;73:125–134. doi: 10.1016/j.jdermsci.2013.09.003. PubMed DOI

Pechackova S, Burdova K, Benada J, Kleiblova P, Jenikova G, Macurek L. Inhibition of WIP1 phosphatase sensitizes breast cancer cells to genotoxic stress and to MDM2 antagonist nutlin-3. Oncotarget. 2016;7(12):14458–14475. PubMed PMC

Yagi H, Chuman Y, Kozakai Y, Imagawa T, Takahashi Y, Yoshimura F, Tanino K, Sakaguchi K. A small molecule inhibitor of p53-inducible protein phosphatase PPM1D. Bioorg Med Chem Lett. 2012;22:729–732. doi: 10.1016/j.bmcl.2011.10.084. PubMed DOI

Ogasawara S, Kiyota Y, Chuman Y, Kowata A, Yoshimura F, Tanino K, Kamada R, Sakaguchi K. Novel inhibitors targeting PPM1D phosphatase potently suppress cancer cell proliferation. Bioorg Med Chem. 2015;23:6246–6249. doi: 10.1016/j.bmc.2015.08.042. PubMed DOI

Kozakai Y, Kamada R, Kiyota Y, Yoshimura F, Tanino K, Sakaguchi K. Inhibition of C-terminal truncated PPM1D enhances the effect of doxorubicin on cell viability in human colorectal carcinoma cell line. Bioorg Med Chem Lett. 2014;24:5593–5596. doi: 10.1016/j.bmcl.2014.10.093. PubMed DOI

Hayashi R, Tanoue K, Durell SR, Chatterjee DK, Jenkins LM, Appella DH, Appella E. Optimization of a cyclic peptide inhibitor of Ser/Thr phosphatase PPM1D (Wip1) Biochemistry. 2011;50:4537–4549. doi: 10.1021/bi101949t. PubMed DOI PMC

Yamaguchi H, Durell SR, Feng H, Bai Y, Anderson CW, Appella E. Development of a substrate-based cyclic phosphopeptide inhibitor of protein phosphatase 2Cdelta, Wip1. Biochemistry. 2006;45:13193–13202. doi: 10.1021/bi061356b. PubMed DOI

Bang J, Yamaguchi H, Durell SR, Appella E, Appella DH (2008) A small molecular scaffold for selective inhibition of Wip1 phosphatase(). ChemMedChem 3. doi:10.1002/cmdc.200700281 PubMed PMC

Chen Z, Wang L, Yao D, Yang T, Cao WM, Dou J, Pang JC, Guan S, Zhang H, Yu Y, et al. Wip1 inhibitor GSK2830371 inhibits neuroblastoma growth by inducing Chk2/p53-mediated apoptosis. Sci Rep. 2016;6:38011. doi: 10.1038/srep38011. PubMed DOI PMC

Kojima K, Maeda A, Yoshimura M, Nishida Y, Kimura S. The pathophysiological significance of PPM1D and therapeutic targeting of PPM1D-mediated signaling by GSK2830371 in mantle cell lymphoma. Oncotarget. 2016 PubMed PMC

Sriraman A, Radovanovic M, Wienken M, Najafova Z, Li Y, Dobbelstein M. Cooperation of Nutlin-3a and a Wip1 inhibitor to induce p53 activity. Oncotarget. 2016;7:31623–31638. PubMed PMC

Ventura A, Kirsch DG, McLaughlin ME, Tuveson DA, Grimm J, Lintault L, Newman J, Reczek EE, Weissleder R, Jacks T. Restoration of p53 function leads to tumour regression in vivo. Nature. 2007;445:661–665. doi: 10.1038/nature05541. PubMed DOI

Kong W, Jiang X, Mercer WE. Downregulation of Wip-1 phosphatase expression in MCF-7 breast cancer cells enhances doxorubicin-induced apoptosis through p53-mediated transcriptional activation of Bax. Cancer Biol Ther. 2009;8:555–563. doi: 10.4161/cbt.8.6.7742. PubMed DOI

Ali AY, Abedini MR, Tsang BK. The oncogenic phosphatase PPM1D confers cisplatin resistance in ovarian carcinoma cells by attenuating checkpoint kinase 1 and p53 activation. Oncogene. 2012;31:2175–2186. doi: 10.1038/onc.2011.399. PubMed DOI

Rochette L, Guenancia C, Gudjoncik A, Hachet O, Zeller M, Cottin Y, Vergely C. Anthracyclines/trastuzumab: new aspects of cardiotoxicity and molecular mechanisms. Trends Pharmacol Sci. 2015;36:326–348. doi: 10.1016/j.tips.2015.03.005. PubMed DOI

Derek WE, Rashmi N, Simon C, Kyle M-B, Jonathan PJM, Amadeo MP. Role of drug metabolism in the cytotoxicity and clinical efficacy of anthracyclines. Curr Drug Metab. 2015;16:412–426. doi: 10.2174/1389200216888150915112039. PubMed DOI PMC

Qin L, Yang F, Zhou C, Chen Y, Zhang H, Su Z. Efficient reactivation of p53 in cancer cells by a dual MdmX/Mdm2 inhibitor. J Am Chem Soc. 2014;136:18023–18033. doi: 10.1021/ja509223m. PubMed DOI

Brown CJ, Lain S, Verma CS, Fersht AR, Lane DP. Awakening guardian angels: drugging the p53 pathway. Nat Rev Cancer. 2009;9:862–873. doi: 10.1038/nrc2763. PubMed DOI

Khoo KH, Verma CS, Lane DP. Drugging the p53 pathway: understanding the route to clinical efficacy. Nat Rev Drug Discov. 2014;13:217–236. doi: 10.1038/nrd4288. PubMed DOI

Zhang Q, Zeng SX, Lu H. Targeting p53-MDM2-MDMX loop for cancer therapy. Subcell Biochem. 2014;85:281–319. doi: 10.1007/978-94-017-9211-0_16. PubMed DOI PMC

Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z, Kong N, Kammlott U, Lukacs C, Klein C, et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science. 2004;303:844–848. doi: 10.1126/science.1092472. PubMed DOI

Ding Q, Zhang Z, Liu JJ, Jiang N, Zhang J, Ross TM, Chu XJ, Bartkovitz D, Podlaski F, Janson C, et al. Discovery of RG7388, a potent and selective p53-MDM2 inhibitor in clinical development. J Med Chem. 2013;56:5979–5983. doi: 10.1021/jm400487c. PubMed DOI

Chen L, Rousseau RF, Middleton SA, Nichols GL, Newell DR, Lunec J, Tweddle DA. Pre-clinical evaluation of the MDM2-p53 antagonist RG7388 alone and in combination with chemotherapy in neuroblastoma. Oncotarget. 2015;6:10207–10221. doi: 10.18632/oncotarget.3504. PubMed DOI PMC

Higgins B, Glenn K, Walz A, Tovar C, Filipovic Z, Hussain S, Lee E, Kolinsky K, Tannu S, Adames V, et al. Preclinical optimization of MDM2 antagonist scheduling for cancer treatment by using a model-based approach. Clin Cancer Res. 2014;20:3742–3752. doi: 10.1158/1078-0432.CCR-14-0460. PubMed DOI

Makii C, Oda K, Ikeda Y, Sone K, Hasegawa K, Uehara Y, Nishijima A, Asada K, Koso T, Fukuda T et al (2016) MDM2 is a potential therapeutic target and prognostic factor for ovarian clear cell carcinomas with wild type TP53. Oncotarget 7(46) PubMed PMC

Esfandiari A, Hawthorne TA, Nakjang S, Lunec J. Chemical inhibition of wild-type p53-induced phosphatase 1 (WIP1/PPM1D) by GSK2830371 potentiates the sensitivity to MDM2 inhibitors in a p53-dependent manner. Mol Cancer Ther. 2016;15:379–391. doi: 10.1158/1535-7163.MCT-15-0651. PubMed DOI PMC

Wanzel M, Vischedyk JB, Gittler MP, Gremke N, Seiz JR, Hefter M, Noack M, Savai R, Mernberger M, Charles JP, et al. CRISPR-Cas9-based target validation for p53-reactivating model compounds. Nat Chem Biol. 2016;12:22–28. doi: 10.1038/nchembio.1965. PubMed DOI PMC

Goloudina AR, Mazur SJ, Appella E, Garrido C, Demidov ON. Wip1 sensitizes p53-negative tumors to apoptosis by regulating the Bax/Bcl-xL ratio. Cell Cycle. 2012;11:1883–1887. doi: 10.4161/cc.19901. PubMed DOI PMC

Goloudina AR, Tanoue K, Hammann A, Fourmaux E, Le Guezennec X, Bulavin DV, Mazur SJ, Appella E, Garrido C, Demidov ON. Wip1 promotes RUNX2-dependent apoptosis in p53-negative tumors and protects normal tissues during treatment with anticancer agents. Proc Natl Acad Sci U S A. 2012;109:E68–E75. doi: 10.1073/pnas.1107017108. PubMed DOI PMC

Choi DW, Na W, Kabir MH, Yi E, Kwon S, Yeom J, Ahn JW, Choi HH, Lee Y, Seo KW, et al. WIP1, a homeostatic regulator of the DNA damage response, is targeted by HIPK2 for phosphorylation and degradation. Mol Cell. 2013;51:374–385. doi: 10.1016/j.molcel.2013.06.010. PubMed DOI

Clausse V, Goloudina AR, Uyanik B, Kochetkova EY, Richaud S, Fedorova OA, Hammann A, Bardou M, Barlev NA, Garrido C, et al. Wee1 inhibition potentiates Wip1-dependent p53-negative tumor cell death during chemotherapy. Cell Death Dis. 2016;7:e2195. doi: 10.1038/cddis.2016.96. PubMed DOI PMC

Perez-Pinera P, Ousterout DG, Brunger JM, Farin AM, Glass KA, Guilak F, Crawford GE, Hartemink AJ, Gersbach CA. Synergistic and tunable human gene activation by combinations of synthetic transcription factors. Nat Methods. 2013;10:239–242. doi: 10.1038/nmeth.2361. PubMed DOI PMC

Shen X-F, Zhao Y, Jiang J-P, Guan W-X, Du J-F. Phosphatase Wip1 in immunity: an overview and update. Front Immunol. 2017;8:8. doi: 10.3389/fimmu.2017.00008. PubMed DOI PMC

Uyanik B, Grigorash BB, Goloudina AR, Demidov ON. DNA damage-induced phosphatase Wip1 in regulation of hematopoiesis, immune system and inflammation. Cell Death Discov. 2017;3:17018. doi: 10.1038/cddiscovery.2017.18. PubMed DOI PMC

Schito ML, Demidov ON, Saito S, Ashwell JD, Appella E. Wip1 phosphatase-deficient mice exhibit defective T cell maturation due to sustained p53 activation. J Immunol. 2006;176:4818–4825. doi: 10.4049/jimmunol.176.8.4818. PubMed DOI

Yi W, Hu X, Chen Z, Liu L, Tian Y, Chen H, Cong YS, Yang F, Zhang L, Rudolph KL, et al. Phosphatase Wip1 controls antigen-independent B-cell development in a p53-dependent manner. Blood. 2015;126:620–628. doi: 10.1182/blood-2015-02-624114. PubMed DOI PMC

Chen Z, Yi W, Morita Y, Wang H, Cong Y, Liu J-P, Xiao Z, Rudolph KL, Cheng T, Ju Z. Wip1 deficiency impairs haematopoietic stem cell function via p53 and mTORC1 pathways. Nat Commun. 2015;6:6808. doi: 10.1038/ncomms7808. PubMed DOI

Zhang Q, Zhang C, Chang F, Liang K, Yin X, Li X, Zhao K, Niu Q, Tian Z. Wip 1 inhibits intestinal inflammation in inflammatory bowel disease. Cell Immunol. 2016;310:63–70. doi: 10.1016/j.cellimm.2016.07.012. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...