1,298
Views
12
CrossRef citations to date
0
Altmetric
Report

LZAP is a novel Wip1 binding partner and positive regulator of its phosphatase activity in vitro

ORCID Icon, , ORCID Icon, , &
Pages 213-223 | Received 16 Aug 2016, Accepted 11 Nov 2016, Published online: 27 Dec 2016

References

  • 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; 94:6048-53; PMID:9177166; http://dx.doi.org/10.1073/pnas.94.12.6048
  • Yamaguchi H, Durell SR, Chatterjee DK, Anderson CW, Appella E. The Wip1 phosphatase PPM1D dephosphorylates SQ/TQ motifs in checkpoint substrates phosphorylated by PI3K-like kinases. Biochemistry 2007; 46:12594-603; PMID:17939684; http://dx.doi.org/10.1021/bi701096s
  • 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; 44:5285-94; PMID:15807522; http://dx.doi.org/10.1021/bi0476634
  • 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. The EMBO journal 2000; 19:6517-26; PMID:11101524; http://dx.doi.org/10.1093/emboj/19.23.6517
  • Lu X, Nannenga B, Donehower LA. PPM1D dephosphorylates Chk1 and p53 and abrogates cell cycle checkpoints. Genes Dev 2005; 19:1162-74; PMID:15870257; http://dx.doi.org/10.1101/gad.1291305
  • Oliva-Trastoy M, Berthonaud V, Chevalier A, Ducrot C, Marsolier-Kergoat MC, Mann C, Leteurtre F. The Wip1 phosphatase (PPM1D) antagonizes activation of the Chk2 tumour suppressor kinase. Oncogene 2007; 26:1449-58; PMID:16936775; http://dx.doi.org/10.1038/sj.onc.1209927
  • 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; 23:757-64; PMID:16949371; http://dx.doi.org/10.1016/j.molcel.2006.07.010
  • Cha H, Lowe JM, Li H, Lee J-S, Belova GI, Bulavin DV, Fornace AJ. Wip1 directly dephosphorylates gamma-H2AX and attenuates the DNA damage response. Cancer Res 2010; 70:4112-22; PMID:20460517; http://dx.doi.org/10.1158/0008-5472.CAN-09-4244
  • Moon S-H, Lin L, Zhang X, Nguyen T-A, 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; 285:12935-47; PMID:20118229; http://dx.doi.org/10.1074/jbc.M109.071696
  • 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 γ-radiation. Cell Death Dis 2013; 4:e744-e; PMID:23907458; http://dx.doi.org/10.1038/cddis.2013.252
  • 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; PMID:17936559; http://dx.doi.org/10.1016/j.ccr.2007.08.033
  • 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; 69:7960-8; PMID:19808970; http://dx.doi.org/10.1158/0008-5472.CAN-09-0634
  • Bulavin DV, Demidov ON, Saito Si, 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; 31:210-5; PMID:12021785; http://dx.doi.org/10.1038/ng894
  • Belova GI, Demidov ON, Fornace AJ, Bulavin DV. Chemical inhibition of Wip1 phosphatase contributes to suppression of tumorigenesis. Cancer Biol Ther 2005; 4:1154-8; PMID:16258255; http://dx.doi.org/10.4161/cbt.4.10.2204
  • Bulavin DV, Phillips C, Nannenga B, Timofeev O, Donehower LA, Anderson CW, Appella E, Fornace AJ. 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; PMID:14991053; http://dx.doi.org/10.1038/ng1317
  • Nannenga B, Lu X, Dumble M, Van Maanen M, Nguyen T-A, Sutton R, Kumar TR, Donehower LA. Augmented cancer resistance and DNA damage response phenotypes in PPM1D null mice. Mol Carcinog 2006; 45:594-604; PMID:16652371; http://dx.doi.org/10.1002/mc.20195
  • Li J, Yang Y, Peng Y, Austin RJ, van Eyndhoven WG, Nguyen KCQ, 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; 31:133-4; PMID:12021784; http://dx.doi.org/10.1038/ng888
  • 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; PMID:16254685; http://dx.doi.org/10.1007/s10549-005-9017-7
  • Hirasawa A, Saito-Ohara F, Inoue J, Aoki D, Susumu N, Yokoyama T, Nozawa S, Inazawa J, Imoto I. Association of 17q21-q24 gain in ovarian clear cell adenocarcinomas with poor prognosis and identification of PPM1D and APPBP2 as likely amplification targets. Clin Cancer Res 2003; 9:1995-2004; PMID:12796361
  • Loukopoulos P, Shibata T, Katoh H, Kokubu A, Sakamoto M, Yamazaki K, Kosuge T, Kanai Y, Hosoda F, Imoto I, et al. Genome-wide array-based comparative genomic hybridization analysis of pancreatic adenocarcinoma: identification of genetic indicators that predict patient outcome. Cancer Sci 2007; 98:392-400; PMID:17233815; http://dx.doi.org/10.1111/j.1349-7006.2007.00395.x
  • 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; 57:566-71; PMID:17685927; http://dx.doi.org/10.1111/j.1440-1827.2007.02140.x
  • Buss MC, Remke M, Lee J, Gandhi K, Schniederjan MJ, Kool M, Northcott PA, Pfister SM, Taylor MD, Castellino RC. The WIP1 oncogene promotes progression and invasion of aggressive medulloblastoma variants. Oncogene 2015; 34:1126-40; PMID:24632620; http://dx.doi.org/10.1038/onc.2014.37
  • 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; 63:1876-83; PMID:12702577
  • 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; 493:406-10; PMID:23242139; http://dx.doi.org/10.1038/nature11725
  • Zajkowicz A, Butkiewicz D, Drosik A, Giglok M, Suwiński R, Rusin M. Truncating mutations of PPM1D are found in blood DNA samples of lung cancer patients. Br J Cancer 2015; 112:1114-20; PMID:25742468; http://dx.doi.org/10.1038/bjc.2015.79
  • Kleiblova P, Shaltiel IA, Benada J, Ševčík J, Pecháčková 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; 201:511-21; PMID:23649806; http://dx.doi.org/10.1083/jcb.201210031
  • 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; 46:726-30; PMID:24880341; http://dx.doi.org/10.1038/ng.2995
  • Chew J, Biswas S, Shreeram S, Humaidi M, Wong ET, Dhillion MK, Teo H, Hazra A, Fang CC, López-Collazo E, et al. WIP1 phosphatase is a negative regulator of NF-kappaB signalling. Nat Cell Biol 2009; 11:659-66; PMID:19377466; http://dx.doi.org/10.1038/ncb1873
  • Lu X, Yarbrough WG. Negative regulation of RelA phosphorylation: emerging players and their roles in cancer. Cytokine Growth Factor Rev 2015; 26:7-13; PMID:25438737; http://dx.doi.org/10.1016/j.cytogfr.2014.09.003
  • Lu X, Nguyen T-A, Moon S-H, 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; PMID:18265945; http://dx.doi.org/10.1007/s10555-008-9127-x
  • Ching YP, Qi Z, Wang JH. Cloning of three novel neuronal Cdk5 activator binding proteins. Gene 2000; 242:285-94; PMID:10721722; http://dx.doi.org/10.1016/S0378-1119(99)00499-0
  • Wang J, He X, Luo Y, Yarbrough WG. A novel ARF-binding protein (LZAP) alters ARF regulation of HDM2. Biochem J 2006; 393:489-501; PMID:16173922; http://dx.doi.org/10.1042/BJ20050960
  • Wang J, An H, Mayo MW, Baldwin AS, Yarbrough WG. LZAP, a putative tumor suppressor, selectively inhibits NF-kappaB. Cancer Cell 2007; 12:239-51; PMID:17785205; http://dx.doi.org/10.1016/j.ccr.2007.07.002
  • Kwon J, Cho HJ, Han SH, No JG, Kwon JY, Kim H. A novel LZAP-binding protein, NLBP, inhibits cell invasion. J Biol Chem 2010; 285:12232-40; PMID:20164180; http://dx.doi.org/10.1074/jbc.M109.065920
  • Wu J, Lei G, Mei M, Tang Y, Li H. A novel C53/LZAP-interacting protein regulates stability of C53/LZAP and DDRGK domain-containing Protein 1 (DDRGK1) and modulates NF-kappaB signaling. J Biol Chem 2010; 285:15126-36; PMID:20228063; http://dx.doi.org/10.1074/jbc.M110.110619
  • Jiang H, Luo S, Li H. Cdk5 activator-binding protein C53 regulates apoptosis induced by genotoxic stress via modulating the G2/M DNA damage checkpoint. J Biol Chem 2005; 280:20651-9; PMID:15790566; http://dx.doi.org/10.1074/jbc.M413431200
  • Jiang H, Wu J, He C, Yang W, Li H. Tumor suppressor protein C53 antagonizes checkpoint kinases to promote cyclin-dependent kinase 1 activation. Cell Res 2009; 19:458-68; PMID:19223857; http://dx.doi.org/10.1038/cr.2009.14
  • An H, Lu X, Liu D, Yarbrough WG. LZAP inhibits p38 MAPK (p38) phosphorylation and activity by facilitating p38 association with the wild-type p53 induced phosphatase 1 (WIP1). PLoS One 2011; 6:e16427-e; PMID:21283629; http://dx.doi.org/10.1371/journal.pone.0016427
  • Liu D, Wang W-D, Melville DB, Cha YI, Yin Z, Issaeva N, Knapik EW, Yarbrough WG. Tumor suppressor Lzap regulates cell cycle progression, doming, and zebrafish epiboly. Developmental dynamics: an official publication of the American Association of Anatomists 2011; 240:1613-25; PMID:21523853; http://dx.doi.org/10.1002/dvdy.22644
  • Tong L, Tergaonkar V. Rho protein GTPases and their interactions with NFkappaB: crossroads of inflammation and matrix biology. Biosci Rep 2014; 34; PMID:24877606
  • Cildir G, Low KC, Tergaonkar V. Noncanonical NF-kappaB Signaling in Health and Disease. Trends Mol Med 2016; 22:414-29; PMID:27068135; http://dx.doi.org/10.1016/j.molmed.2016.03.002
  • Dey A, Wong E, Kua N, Teo HL, Tergaonkar V, Lane D. Hexamethylene bisacetamide (HMBA) simultaneously targets AKT and MAPK pathway and represses NF kappaB activity: implications for cancer therapy. Cell Cycle 2008; 7:3759-67; PMID:19029824; http://dx.doi.org/10.4161/cc.7.23.7213
  • Teo H, Ghosh S, Luesch H, Ghosh A, Wong ET, Malik N, Orth A, de Jesus P, Perry AS, Oliver JD, et al. Telomere-independent Rap1 is an IKK adaptor and regulates NF-kappaB-dependent gene expression. Nat Cell Biol 2010; 12:758-67; PMID:20622870; http://dx.doi.org/10.1038/ncb2080
  • Kim HH, Abdelmohsen K, Gorospe M. Regulation of HuR by DNA Damage Response Kinases. J Nucleic Acids 2010; 2010; PMID:20798862; http://dx.doi.org/10.4061/2010/981487
  • Butch ER, Guan K-L. Characterization of ERK1 Activation Site Mutants and the Effect on Recognition by MEK1 and MEK2. J Biol Chem 1996; 271:4230-5; PMID:8626767; http://dx.doi.org/10.1074/jbc.271.8.4230
  • Lowe J, Cha H, Lee M-O, Mazur SJ, Appella E, Fornace AJ. Regulation of the Wip1 phosphatase and its effects on the stress response. Frontiers in bioscience (Landmark edition) 2012; 17:1480-98; PMID:22201816; http://dx.doi.org/10.2741/3999
  • Choi DW, Na W, Kabir MH, Yi E, Kwon S, Yeom J, Ahn J-W, Choi H-H, 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; 51:374-85; PMID:23871434; http://dx.doi.org/10.1016/j.molcel.2013.06.010
  • Macurek L, Benada J, Müllers E, Halim VA, Krejčíková K, Burdová K, Pecháčková S, Hodný Z, Lindqvist A, Medema RH, et al. Downregulation of Wip1 phosphatase modulates the cellular threshold of DNA damage signaling in mitosis. Cell cycle (Georgetown, Tex) 2013; 12:251-62; PMID:23255129; http://dx.doi.org/10.4161/cc.23057
  • Grassmann R, Aboud M, Jeang K-T. Molecular mechanisms of cellular transformation by HTLV-1 Tax. Oncogene 2005; 24:5976-85; PMID:16155604; http://dx.doi.org/10.1038/sj.onc.1208978
  • Dayaram T, Lemoine FJ, Donehower LA, Marriott SJ. Activation of WIP1 phosphatase by HTLV-1 Tax mitigates the cellular response to DNA damage. PLoS One 2013; 8:e55989-e; PMID:23405243; http://dx.doi.org/10.1371/journal.pone.0055989
  • Hayden MS, Ghosh S. Shared principles in NF-kappaB signaling. Cell 2008; 132:344-62; PMID:18267068; http://dx.doi.org/10.1016/j.cell.2008.01.020
  • Tergaonkar V. p53 and NFkappaB: fresh breath in the cross talk. Cell Res 2009; 19:1313-5; PMID:19956183; http://dx.doi.org/10.1038/cr.2009.132
  • Tergaonkar V, Perkins ND. p53 and NF-kappaB crosstalk: IKKalpha tips the balance. Mol Cell 2007; 26:158-9; PMID:17466617; http://dx.doi.org/10.1016/j.molcel.2007.04.006
  • Janssens S, Tschopp J. Signals from within: the DNA-damage-induced NF-kappaB response. Cell Death Differ 2006; 13:773-84; PMID:16410802; http://dx.doi.org/10.1038/sj.cdd.4401843
  • Bohuslav J, Chen LF, Kwon H, Mu Y, Greene WC. p53 induces NF-kappaB activation by an IkappaB kinase-independent mechanism involving phosphorylation of p65 by ribosomal S6 kinase 1. J Biol Chem 2004; 279:26115-25; PMID:15073170; http://dx.doi.org/10.1074/jbc.M313509200
  • Benoit V, Hellin AC, Huygen S, Gielen J, Bours V, Merville MP. Additive effect between NF-kappaB subunits and p53 protein for transcriptional activation of human p53 promoter. Oncogene 2000; 19:4787-94; PMID:11032029; http://dx.doi.org/10.1038/sj.onc.1203831
  • Tergaonkar V, Pando M, Vafa O, Wahl G, Verma I. p53 stabilization is decreased upon NFkappaB activation: a role for NFkappaB in acquisition of resistance to chemotherapy. Cancer Cell 2002; 1:493-503; PMID:12124178; http://dx.doi.org/10.1016/S1535-6108(02)00068-5
  • Dey A, Wong ET, Bist P, Tergaonkar V, Lane DP. Nutlin-3 inhibits the NFkappaB pathway in a p53-dependent manner: implications in lung cancer therapy. Cell Cycle 2007; 6:2178-85; PMID:17786042; http://dx.doi.org/10.4161/cc.6.17.4643
  • Mak GW-Y, Chan MM-L, Leong VY-L, Lee JM-F, Yau T-O, Ng IO-L, Ching Y-P. Overexpression of a novel activator of PAK4, the CDK5 kinase-associated protein CDK5RAP3, promotes hepatocellular carcinoma metastasis. Cancer Res 2011; 71:2949-58; PMID:21385901; http://dx.doi.org/10.1158/0008-5472.CAN-10-4046
  • Zhao J-j, Pan K, Li J-j, Chen Y-b, Chen J-g, Lv L, Wang D-d, Pan Q-z, Chen M-s, Xia J-c. Identification of LZAP as a new candidate tumor suppressor in hepatocellular carcinoma. PLoS One 2011; 6:e26608-e; PMID:22028922
  • Chen J, Shi Y, Li Z, Yu H, Han Y, Wang X, Sun K, Yang T, Lou K, Song Y, et al. A functional variant of IC53 correlates with the late onset of colorectal cancer. Molecular medicine (Cambridge, Mass) 2011; 17:607-18; PMID:21394385
  • Stav D, Bar I, Sandbank J. Usefulness of CDK5RAP3, CCNB2, and RAGE genes for the diagnosis of lung adenocarcinoma. Int J Biol Markers 2007; 22:108-13; PMID:17549666
  • Lu X, An H, Jin R, Zou M, Guo Y, Su PF, Liu D, Shyr Y, Yarbrough WG. PPM1A is a RelA phosphatase with tumor suppressor-like activity. Oncogene 2014; 33:2918-27; PMID:23812431; http://dx.doi.org/10.1038/onc.2013.246
  • Han J, Lee JD, Jiang Y, Li Z, Feng L, Ulevitch RJ. Characterization of the Structure and Function of a Novel MAP Kinase Kinase (MKK6). J Biol Chem 1996; 271:2886-91; PMID:8621675; http://dx.doi.org/10.1074/jbc.271.6.2886

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.