The Wip1 Phosphatase Acts as a Gatekeeper in the p53-Mdm2 Autoregulatory Loop

Cancer Cell

Volumn 12, Issue 4, 2007, Pages 342-354

  Lu, Xiongbin ^a,b   Ma, Ou ^a   Nguyen, Thuy Ai ^a   Jones, Stephen N ^c   Oren, Moshe ^d   Donehower, Lawrence A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

CELLCYCLE; PROTEINS

Indexed keywords

ATM PROTEIN; PHOSPHATASE; PROTEASOME; PROTEIN MDM2; PROTEIN P53; SERINE; UNCLASSIFIED DRUG; WILD TYPE P53 INDUCED PHOSPHATASE 1;

ARTICLE; AUTOREGULATION; BINDING AFFINITY; CONTROLLED STUDY; DOWN REGULATION; FEEDBACK SYSTEM; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; UBIQUITINATION;

PYRONIA TITHONUS;

EID: 35148893194     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2007.08.033     Document Type: Article

References (51)

1. Appella E., and Anderson C.W. Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem. 268 (2001) 2764-2772
2. Belova G.I., Demidov O.N., Fornace Jr. A.J., and Bulavin D.V. Chemical inhibition of Wip1 phosphatase contributes to suppression of tumorigenesis. Cancer Biol. Ther. 4 (2005) 1154-1158
3. Bode A.M., and Dong Z. Post-translational modification of p53 in tumorigenesis. Nat. Rev. Cancer 4 (2004) 793-805
4. Bond G.L., Hu W., and Levine A.J. MDM2 is a central node in the p53 pathway: 12 years and counting. Curr. Cancer Drug Targets 5 (2005) 3-8
5. Bulavin D.V., Demidov O.N., Saito S., Kauraniemi P., Phillips C., Amundson S.A., Ambrosino C., Sauter G., Nebreda A.R., Anderson C.W., et al. Amplification of PPM1D in human tumors abrogates p53 tumor-suppressor activity. Nat. Genet. 31 (2002) 210-215
6. Bulavin D.V., Phillips C., Nannenga B., Timofeev O., Donehower L.A., Anderson C.W., Appella E., and Fornace Jr. A.J. Inactivation of the Wip1 phosphatase inhibits mammary tumorigenesis through p38 MAPK-mediated activation of the p16(Ink4a)-p19(Arf) pathway. Nat. Genet. 36 (2004) 343-350
7. Canman C.E., Lim D.S., Cimprich K.A., Taya Y., Tamai K., Sakaguchi K., Appella E., Kastan M.B., and Siliciano J.D. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281 (1998) 1677-1679
8. Chehab N.H., Malikzay A., Appel M., and Halazonetis T.D. Chk2/hCds1 functions as a DNA damage checkpoint in G(1) by stabilizing p53. Genes Dev. 14 (2000) 278-288
9. Choi J., Appella E., and Donehower L.A. The structure and expression of the murine wildtype p53-induced phosphatase 1 (Wip1) gene. Genomics 64 (2000) 298-306
10. Choi J., Nannenga B., Demidov O.N., Bulavin D.V., Cooney A., Brayton C., Zhang Y., Mbawuike I.N., Bradley A., Appella E., and Donehower L.A. 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. 22 (2002) 1094-1105
11. Crook T., Marston N.J., Sara E.A., and Vousden K.H. Transcriptional activation by p53 correlates with suppression of growth but not transformation. Cell 79 (1994) 817-827
12. Demidov O.N., Kek C., Shreeram S., Timofeev O., Fornace A.J., Appella E., and Bulavin D.V. The role of the MKK6/p38 MAPK pathway in Wip1-dependent regulation of ErbB2-driven mammary gland tumorigenesis. Oncogene 26 (2007) 2502-2506 10.1038/sj.onc.1210032 Published online October 2, 2006
13. Fiscella M., Zhang H., Fan S., Sakaguchi K., Shen S., Mercer W.E., Vande Woude G.F., O'Connor P.M., and 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. USA 94 (1997) 6048-6053
14. Fujimoto H., Onishi N., Kato N., Takekawa M., Xu X.Z., Kosugi A., Kondo T., Imamura M., Oishi I., Yoda A., and Minami Y. Regulation of the antioncogenic Chk2 kinase by the oncogenic Wip1 phosphatase. Cell Death Differ. 13 (2006) 1170-1180 10.1038/sj.cdd.4401801 Published online November 25, 2005
15. Harris S.L., and Levine A.J. The p53 pathway: Positive and negative feedback loops. Oncogene 24 (2005) 2899-2908
16. Hirao A., Kong Y.Y., Matsuoka S., Wakeham A., Ruland J., Yoshida H., Liu D., Elledge S.J., and Mak T.W. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287 (2000) 1824-1827
17. Hirasawa A., Saito-Ohara F., Inoue J., Aoki D., Susumu N., Yokoyama T., Nozawa S., Inazawa J., and 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. 9 (2003) 1995-2004
18. Jones S.N., Sands A.T., Hancock A.R., Vogel H., Donehower L.A., Linke S.P., Wahl G.M., and Bradley A. The tumorigenic potential and cell growth characteristics of p53-deficient cells are equivalent in the presence or absence of Mdm2. Proc. Natl. Acad. Sci. USA 93 (1996) 14106-14111
19. Lane D.P. Exploiting the p53 pathway for the diagnosis and therapy of human cancer. Cold Spring Harb. Symp. Quant. Biol. 70 (2005) 489-497
20. Lavin M.F., and Gueven N. The complexity of p53 stabilization and activation. Cell Death Differ. 13 (2006) 941-950
21. Li J., Yang Y., Peng Y., Austin R.J., van Eyndhoven W.G., Nguyen K.C., Gabriele T., McCurrach M.E., Marks J.R., Hoey T., et al. Oncogenic properties of PPM1D located within a breast cancer amplification epicenter at 17q23. Nat. Genet. 31 (2002) 133-134
22. Li M., Brooks C.L., Kon N., and Gu W. A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol. Cell 13 (2004) 879-886
23. Lu X., Bocangel D., Nannenga B., Yamaguchi H., Appella E., and Donehower L.A. The p53-induced oncogenic phosphatase PPM1D interacts with uracil DNA glycosylase and suppresses base excision repair. Mol. Cell 15 (2004) 621-634
24. Lu X., Nguyen T.A., and Donehower L.A. Reversal of the ATM/ATR-mediated DNA damage response by the oncogenic phosphatase PPM1D. Cell Cycle 4 (2005) 1060-1064
25. Martin A.C., Facchiano A.M., Cuff A.L., Hernandez-Boussard T., Olivier M., Hainaut P., and Thornton J.M. Integrating mutation data and structural analysis of the TP53 tumor-suppressor protein. Hum. Mutat. 19 (2002) 149-164
26. Maya R., Balass M., Kim S.T., Shkedy D., Leal J.F., Shifman O., Moas M., Buschmann T., Ronai Z., Shiloh Y., et al. ATM-dependent phosphorylation of Mdm2 on serine 395: Role in p53 activation by DNA damage. Genes Dev. 15 (2001) 1067-1077
27. Meek D.W., and Knippschild U. Posttranslational modification of MDM2. Mol. Cancer Res. 1 (2003) 1017-1026
28. Mendrzyk F., Radlwimmer B., Joos S., Kokocinski F., Benner A., Stange D.E., Neben K., Fiegler H., Carter N.P., Reifenberger G., et al. Genomic and protein expression profiling identifies CDK6 as novel independent prognostic marker in medulloblastoma. J. Clin. Oncol. 23 (2005) 8853-8862
29. Meulmeester E., Maurice M.M., Boutell C., Teunisse A.F., Ovaa H., Abraham T.E., Dirks R.W., and Jochemsen A.G. Loss of HAUSP-mediated deubiquitination contributes to DNA damage-induced destabilization of Hdmx and Hdm2. Mol. Cell 18 (2005) 565-576
30. Michael D., and Oren M. The p53-Mdm2 module and the ubiquitin system. Semin. Cancer Biol. 13 (2003) 49-58
31. Moll U.M., and Petrenko O. The MDM2-p53 interaction. Mol. Cancer Res. 1 (2003) 1001-1008
32. Momand J., Jung D., Wilczynski S., and Niland J. The MDM2 gene amplification database. Nucleic Acids Res. 26 (1998) 3453-3459
33. Mumby M.C., and Walter G. Protein serine/threonine phosphatases: Structure, regulation, and functions in cell growth. Physiol. Rev. 73 (1993) 673-699
34. Nannenga B., Lu X., Dumble M., Van Maanen M., Nguyen T.A., Sutton R., Kumar T.R., and Donehower L.A. Augmented cancer resistance and DNA damage response phenotypes in PPM1D null mice. Mol. Carcinog. 45 (2006) 594-604
35. Ofek P., Ben-Meir D., Kariv-Inbal Z., Oren M., and Lavi S. Cell cycle regulation and p53 activation by protein phosphatase 2C alpha. J. Biol. Chem. 278 (2003) 14299-14305
36. Okamoto K., Li H., Jensen M.R., Zhang T., Taya Y., Thorgeirsson S.S., and Prives C. Cyclin G recruits PP2A to dephosphorylate Mdm2. Mol. Cell 9 (2002) 761-771
37. Oliva-Trastoy M., Berthonaud V., Chevalier A., Ducrot C., Marsolier-Kergoat M.C., Mann C., and Leteurtre F. The Wip1 phosphatase (PPM1D) antagonizes activation of the Chk2 tumour suppressor kinase. Oncogene 26 (2006) 1449-1458
38. Saito-Ohara F., Imoto I., Inoue J., Hosoi H., Nakagawara A., Sugimoto T., and Inazawa J. PPM1D is a potential target for 17q gain in neuroblastoma. Cancer Res. 63 (2003) 1876-1883
39. Sanchez-Prieto R., Rojas J.M., Taya Y., and Gutkind J.S. A role for the p38 mitogen-acitvated protein kinase pathway in the transcriptional activation of p53 on genotoxic stress by chemotherapeutic agents. Cancer Res. 60 (2000) 2464-2472
40. Sekiguchi J., Ferguson D.O., Chen H.T., Yang E.M., Earle J., Frank K., Whitlow S., Gu Y., Xu Y., Nussenzweig A., and Alt F.W. Genetic interactions between ATM and the nonhomologous end-joining factors in genomic stability and development. Proc. Natl. Acad. Sci. USA 98 (2001) 3243-3248
41. Shiloh Y. ATM and related protein kinases: Safeguarding genome integrity. Nat. Rev. Cancer 3 (2003) 155-168
42. Shreeram S., Demidov O.N., Hee W.K., Yamaguchi H., Onishi N., Kek C., Timofeev O.N., Dudgeon C., Fornace A.J., Anderson C.W., et al. Wip1 phosphatase modulates ATM-dependent signaling pathways. Mol. Cell 23 (2006) 757-764
43. Sluss H.K., Armata H., Gallant J., and Jones S.N. Phosphorylation of serine 18 regulates distinct p53 functions in mice. Mol. Cell. Biol. 24 (2004) 976-984
44. Stommel J.M., and Wahl G.M. A new twist in the feedback loop: Stress-activated MDM2 destabilization is required for p53 activation. Cell Cycle 4 (2005) 411-417
45. Takekawa M., Adachi M., Nakahata A., Nakayama I., Itoh F., Tsukuda H., Taya Y., and Imai K. p53-inducible wip1 phosphatase mediates a negative feedback regulation of p38 MAPK-p53 signaling in response to UV radiation. EMBO J. 19 (2000) 6517-6526
46. Tibbetts R.S., Brumbaugh K.M., Williams J.M., Sarkaria J.N., Cliby W.A., Shieh S.Y., Taya Y., Prives C., and Abraham R.T. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 13 (1999) 152-157
47. Toledo F., and Wahl G.M. Regulating the p53 pathway: In vitro hypotheses, in vivo veritas. Nat. Rev. Cancer 6 (2006) 909-923
48. Vogelstein B., Lane D., and Levine A.J. Surfing the p53 network. Nature 408 (2000) 307-310
49. Yamaguchi H., Durell S.R., Feng H., Bai Y., Anderson C.W., and Appella E. Development of a substrate-based cyclic phosphopeptide inhibitor of protein phosphatase 2Cdelta, Wip1. Biochemistry 45 (2006) 13193-13202
50. Yoda A., Xu X.Z., Onishi N., Toyoshima K., Fujimoto H., Kato N., Oishi I., Kondo T., and 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. 281 (2006) 24847-24862
51. Yu Q., La Rose J., Zhang H., Takemura H., Kohn K.W., and Pommier Y. UCN-01 inhibits p53 up-regulation and abrogates gamma-radiation-induced G(2)-M checkpoint independently of p53 by targeting both of the checkpoint kinases, Chk2 and Chk1. Cancer Res. 62 (2002) 5743-5748