The oncogenic phosphatase PPM1D confers cisplatin resistance in ovarian carcinoma cells by attenuating checkpoint kinase 1 and p53 activation

Oncogene

Volumn 31, Issue 17, 2012, Pages 2175-2186

  Ali, A Y ^a   Abedini, M R ^a,b   Tsang, B K ^a,c,d  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b BIRJAND UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c UNIVERSITY OF OTTAWA   (Canada)

^d Seoul National University   (South Korea)

Author keywords

apoptosis; Chk1; cisplatin resistance; ovarian cancer; p53; PPM1D

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; CISPLATIN; PHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P53; PROTEIN PHOSPHATASE MAGNESIUM DEPENDENT 1; UNCLASSIFIED DRUG;

ARTICLE; CARCINOMA CELL; CONTROLLED STUDY; HUMAN; HUMAN CELL; OVARY CARCINOMA; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS; CELL CYCLE; CELL LINE, TUMOR; CISPLATIN; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; OVARIAN NEOPLASMS; PHOSPHOPROTEIN PHOSPHATASES; PROTEIN KINASES; TUMOR SUPPRESSOR PROTEIN P53;

ATAXIA TELANGIECTASIA;

EID: 84860286309     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.399     Document Type: Article

References (55)

1. Abedini MR, Muller EJ, Bergeron R, Gray DA, Tsang BK. (2010). Akt promotes chemoresistance in human ovarian cancer cells by modulating cisplatin-induced, p53-dependent ubiquitination of FLICE-like inhibitory protein. Oncogene 29: 11-25.
2. Abedini MR, Muller EJ, Brun J, Bergeron R, Gray DA, Tsang BK. (2008). Cisplatin induces p53-dependent FLICE-like inhibitory protein ubiquitination in ovarian cancer cells. Cancer Res 68: 4511-4517.
3. Bulavin DV, Demidov ON, Saito S, Kauraniemi P, Phillips C, Amundson SA. et al. (2002). Amplification of PPM1D in human tumors abrogates p53 tumor-suppressor activity. Nat Genet 31: 210-215.
4. Bunch RT, Eastman A. (1996). Enhancement of cisplatin-induced cytotoxicity by 7-hydroxystaurosporine (UCN-01), a new G2- checkpoint inhibitor. Clin Cancer Res 2: 791-797.
5. Busby EC, Leistritz DF, Abraham RT, Karnitz LM, Sarkaria JN. (2000). The radiosensitizing agent 7-hydroxystaurosporine (UCN- 01) inhibits the DNA damage checkpoint kinase hChk1. Cancer Res 60: 2108-2112.
6. Canadian Cancer Society 2009. Canadian Cancer Statistics. Available from:www.cancer.ca.
7. Capasso H, Palermo C, Wan S, Rao H, John UP, O'Connell MJ. et al. (2002). Phosphorylation activates Chk1 and is required for checkpoint-mediated cell cycle arrest. J Cell Sci 115: 4555-4564.
8. Carrassa L, Broggini M, Erba E, Damia G. (2004). Chk1, but not Chk2, is involved in the cellular response to DNA damaging agents: differential activity in cells expressing or not p53. Cell Cycle 3: 1177-1181.
9. Chen Z, Xiao Z, Gu WZ, Xue J, Bui MH, Kovar P. et al. (2006). Selective Chk1 inhibitors differentially sensitize p53-deficient cancer cells to cancer therapeutics. Int J Cancer 119: 2784-2794.
10. Chew J, Biswas S, Sheeram S, Humaidi M, Wong ET, Dhillion MK. et al. (2009). WIP1 phosphatase is a negative regulator of NFkappaB signalling. Nat Cell Bio 11: 659-666.
11. Choi J, Appella E, Donehower L. (2000). The structure and expression of the murine wildtype p53-induced phosphatase 1 (Wip1) gene. Genomics 64: 298-306.
12. Chuman Y, Yagi H, Fukuda T, Nomura T, Matsukizono M, Shimohigashi Y. et al. (2008). Characterization of the active site and a unique uncompetitive inhibitor of PPM1-type protein phosphatase PPM1D. Protein Pept Lett 15: 938-948.
13. Damia G, Filiberti L, Vikhanskaya F, Carrassa L, Taya Y, D'incalci M. et al. (2001). Cisplatinum and taxol induce different patterns of p53 phosphorylation. Neoplasia 3: 10-16.
14. Fraser M, Bai T, Tsang BK. (2008). Akt promotes cisplatin resistance in human ovarian cancer cells through inhibition of p53 phosphorylation and nuclear function. Int J Cancer 22: 534-546.
15. Graves PR, Yu L, Schwarz JK, Gales J, Sausville EA, O'Connor PM. et al. (2000). The Chk1 protein kinase and the Cdc25C regulatory pathways are targets of the anticancer agent UCN-01. J Biol Chem 275: 5600-5605.
16. Hirasawa A, Saito-Ohara F, Inoue J, Aoki D, Susumu N, Yokoyama T. et al. (2003). 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: 1995-2004.
17. Honda R, Tanaka H, Yasuda H. (1997). Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 420: 25-27.
18. Jekunen AP, Hom DK, Alcaraz JE, Eastman A, Howell SB. (1994). Cellular pharmacology of dichloro(ethylenediamine)platinum (II) in cisplatin-sensitive and resistant human ovarian carcinoma cells. Cancer Res 54: 2680-2687.
19. Jiang K, Pereira E, Maxfield M, Russell B, Goudelock DM, Sanchez Y. (2003). Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J Biol Chem 278: 25207-25217.
20. Jurvansuu J, Fragkos M, Ingemarsdotter C, Beard P. (2007). Chk1 instability is coupled to mitotic cell death of p53-deficient cells in response to virus-induced DNA damage signaling. J Mol Biol 372: 397-406.
21. Ko LJ, Prives C. (1996). p53: puzzle and paradigm. Genes Dev 10: 1054-1072.
22. Lakin ND, Jackson SP. (1999). Regulation of p53 in response to DNA damage. Oncogene 18: 7644-7655.
23. Levine AJ. (1997). p53, the cellular gatekeeper for growth and division. Cell 88: 323-331.
24. Lu X, Ma O, Nguyen TA, Jones SN, Oren M, Donehower A. (2007). The Wip1 phosphatase acts as a gatekeeper in the p53-Mdm2 autoregulatory loop. Cancer Cell 12: 342-354.
25. Lu X, Nguyen T, Donehower L. (2005). Reversal of the ATM/ATRmediated DNA damage response by the oncogenic phosphatase PPM1D. Cell Cycle 4: 1060-1064.
26. Lu X, Nguyen T, Moon S, Darlington Y, Sommer M, Donehower L. (2008). The type 2C phosphatase Wip1: an oncogenic regulator of tumor suppressor and DNA damage response pathways. Cancer Metastasis Rev 27: 123-135.
27. Lu X, Nguyen TA, Appella E, Donehower LA. (2004). Homeostatic regulation of base excision repair by a p53-induced phosphatase. Cell Cycle 3: 1363-1366.
28. Mistry P, Kelland LR, Loh SW, Abel G, Murrer BA, Harrap KR. (1992). Comparison of cellular accumulation and cytotoxicity of cisplatin with that of tetraplatin and amminedibutyratodichloro(- cyclohexylamine)platinum(IV) (JM221) in human ovarian carcinoma cell lines. Cancer Res 52: 6188-6193.
29. Ouyang G, Yao L, Ruan K, Song G, Mao Y, Bao S. (2009). Genistein induces G2/M cell cycle arrest and apoptosis of human ovarian cancer cells via activation of DNA damage checkpoint pathways. Cell Biol Int 33: 1237-1244.
30. Pan Y, Ren KH, He HW, Shao RG. (2009). Knockdown of Chk1sensitizes human colon carcinoma HCT116 cells in a p53- dependent manner to lidamycin through abrogation of a G2/M checkpoint and induction of apoptosis. Cancer Biol Ther 8: 1559-1566.
31. Perego P, Gatti L, Righetti SC, Beretta GL, Carenini N, Corna E. et al. (2003). Development of resistance to a trinuclear platinum complex in ovarian carcinoma cells. Int J Cancer 105: 617-624.
32. Perego P, Giarola M, Righetti SC, Supino R, Caserini C, Delia D. et al. (1996). Association between cisplatin resistance and mutation of p53 gene and reduced Bax expression in ovarian carcinoma cell systems. Cancer Res 56: 556-562.
33. Playle LC, Hicks DJ, Qualtrough D, Paraskeva C. (2002). Abrogation of the radiation-induced G2 checkpoint by the staurosporine derivative UCN-01 is associated with radiosensitisation in a subset of colorectal tumour cell lines. Br J Cancer 87: 352-358.
34. Qu YH, Chung PH, Sun TP, Shieh SY. (2005). p53 C-terminal phosphorylation by CHK1 and CHK2 participates in the regulation of DNA-damage-induced C-terminal acetylation. Mol Biol Cell 16: 1684-1695.
35. Rauta J, Alarmo EL, Kauraniemi P, Karhu R, Kuukasjarvi T, Kallioniemi A. (2006). The serine-threonine protein phosphatase PPM1D is frequently activated through amplification in aggressive primary breast tumours. Breast Cancer Res Treat 95: 257-263.
36. Reinhardt HC, Aslanian AS, Lees JA, Yaffe MB. (2007). p53-deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell 11: 175-189.
37. Rong JJ, Hu R, Song XM, Ha J, Lu N, Qi Q. et al. (2010). Gambogic acid triggers DNA damage signaling that induces p53/p21(Waf1/ CIP1) activation through the ATR-Chk1 pathway. Cancer Lett 296: 55-64.
38. Sasaki H, Sheng Y, Kotsuji F, Tsang BK. (2000). Down-regulation of Xlinked inhibitor of apoptosis protein induces apoptosis in chemoresistant human ovarian cancer cells. Cancer Res 60: 5659-5666.
39. Abrogation of an S-phase checkpoint and potentiation of camptothecin cytotoxicity by 7-hydroxystaurosporine (UCN-01) in human cancer cell lines, possibly influenced by p53 function. Cancer Res 57: 4029-4035.
40. Shaw TJ, Senterman MK, Dawson K, Crane CA, Vanderhyden BC. (2004). Characterization of intraperitoneal, orthotopic and metastatic xenografts models of human ovarian cancer. Mol Ther 10: 1032-1042.
41. Shieh SY, Ahn J, Tamai K, Taya Y, Prives C. (2000). The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev 14: 289-300. Erratum in: Genes Dev (2000) 14(6): 750.
42. Shieh SY, Ikeda M, Taya Y, Prives C. (1997). DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91: 325-334.
43. Shieh SY, Taya Y, Prives C. (1999). DNA damage-inducible phosphorylation of p53 at N-terminal sites including a novel site, Ser20, requires tetramerization. EMBO J 18: 1815-1823.
44. Sugiyama K, Shimizu M, Akiyama T, Tamaoki T, Yamaguchi K, Takahashi R. et al. (2000). UCN-01 selectively enhances mitomycin C cytotoxicity in p53 defective cells which is mediated through S and/or G2 checkpoint abrogation. Int J Cancer 85: 703-709.
45. Tan DS, Lambros MB, Rayter S, Natrajan R, Vatcheva R, Gao Q. et al. (2009). PPM1D is a potential therapeutic target in ovarian clear cell carcinomas. Clin Cancer Res 15: 2269-2280.
46. Traven A, Heierhorst J. (2005). SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damageresponse proteins. Bioassays 27: 397-407.
47. Wagner JM, Karnitz LM. (2009). Cisplatin-induced DNA damage activates replication checkpoint signaling components that differentially affect tumor cell survival. Mol Pharmacol 76: 208-214.
48. Wilsker D, Petermann E, Helleday T, Bunz F. (2008). Essential function of Chk1 can be uncoupled from DNA damage checkpoint and replication control. Proc Natl Acad Sci USA 105: 20752-20757.
49. Yamaguchi H, Durell SR, Chatterjee DK, Anderson CW, Apella E. (2007). The Wip1 phosphatase PPM1D dephosphorylates SQ/TQ motifs in checkpoint substrates phosphorylated by PI3K-like kinases. Biochemistry 46: 12594-12603.
50. Yang X, Fraser M, Abedini MR, Bai T, Tsang BK. (2008). Regulation of apoptosis-inducing factor-mediated, cisplatin-induced apoptosis by Akt. Br J Cancer 98: 803-808.
51. Yang X, Fraser M, Moll UM, Basak A, Tsang BK. (2006). Aktmediated cisplatin resistance in ovarian cancer: modulation of p53 action on caspase-dependent mitochondrial death pathway. Cancer Res 66: 3126-3136.
52. Yazlovitskaya EM, Persons DL. (2003). Inhibition of cisplatin-induced ATR activity and enhanced sensitivity to cisplatin. Anticancer Res 23(3B): 2275-2279.
53. Zhang WH, Poh A, Fanous AA, Eastman A. (2008). DNA damageinduced S phase arrest in human breast cancer depends on Chk1, but G2 arrest can occur independently of Chk1, Chk2, or MAPKAPK2. Cell Cycle 7: 1668-1677.
54. Zhang X, Lin L, Guo H, Yang J, Jones SN, Jochemsen A. et al. (2009). Phosphorylation and degradation of MdmX is inhibited by Wip1 phosphatase in the DNA damage response. Cancer Res 69: 7960-7968.
55. Zhao H, Piwnica-Worms H. (2001). ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Mol Cell Biol 21: 4129-4139.