90-kDa heat shock protein inhibition abrogates the topoisomerase i poison-induced G 2/M checkpoint in p53-null tumor cells by depleting Chk1 and Wee1

Molecular Pharmacology

Volumn 75, Issue 1, 2009, Pages 124-133

  Tse, Archie N ^a   Sheikh, Tahir N ^a   Alan, Ho ^a   Chou, Ting Chao ^a   Schwartz, Gary K ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7 ETHYL 10 HYDROXYCAMPTOTHECIN; CHECKPOINT KINASE 1; DNA TOPOISOMERASE; HEAT SHOCK PROTEIN 90; PROTEIN; PROTEIN P21; PROTEIN P53; PROTEIN WEE1; SMALL INTERFERING RNA; TANESPIMYCIN; UNCLASSIFIED DRUG; 17-(ALLYLAMINO)-17-DEMETHOXYGELDANAMYCIN; BENZOQUINONE DERIVATIVE; CAMPTOTHECIN; CELL CYCLE PROTEIN; DRUG DERIVATIVE; IRINOTECAN; MACROCYCLIC LACTAM; NUCLEAR PROTEIN; PROTEIN KINASE; PROTEIN TYROSINE KINASE; WEE1 PROTEIN, HUMAN;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL STRAIN HCT116; CONTROLLED STUDY; DRUG ANTAGONISM; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; APOPTOSIS; CELL CYCLE; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECT; DRUG INTERACTION; GENE EXPRESSION REGULATION; METABOLISM; PHYSIOLOGY; TIME;

APOPTOSIS; BENZOQUINONES; CAMPTOTHECIN; CELL CYCLE; CELL CYCLE PROTEINS; CELL SURVIVAL; DNA TOPOISOMERASES, TYPE I; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; G2 PHASE; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; LACTAMS, MACROCYCLIC; NUCLEAR PROTEINS; PROTEIN KINASES; PROTEIN-TYROSINE KINASES; TIME FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 58849115076     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.108.050807     Document Type: Article

References (50)

1. Ahn J, Urist M, and Prives C (2003) Questioning the role of checkpoint kinase 2 in the p53 DNA damage response. JBiol Chem 278:20480- 20489.
2. Aligue R, Akhavan-Niak H, and Russell P (1994) A role for Hsp90 in cell cycle control: Wee1 tyrosine kinase activity requires interaction with Hsp90. EMBO J 13:6099-6106.
3. Arlander SJ, Eapen AK, Vroman BT, McDonald RJ, Toft DO, and Karnitz LM (2003) Hsp90 inhibition depletes Chk1 and sensitizes tumor cells to replication stress. J Biol Chem 278:52572-52577.
4. Arlander SJ, Felts SJ, Wagner JM, Stensgard B, Toft DO, and Karnitz LM (2006) Chaperoning checkpoint kinase 1 (Chk1), an Hsp90 client, with purified chaperones. J Biol Chem 281:2989-2998.
5. Blagosklonny MV, Toretsky J, Bohen S, and Neckers L (1996) Mutant conformation of p53 translated in vitro or in vivo requires functional HSP90. Proc Natl Acad Sci USA93:8379 -8383.
6. Blagosklonny MV, Toretsky J, and Neckers L (1995) Geldanamycin selectively destabilizes and conformationally alters mutated p53. Oncogene 11:933-939.
7. Booher RN, Holman PS, and Fattaey A (1997) Human Myt1 is a cell cycle-regulated kinase that inhibits Cdc2 but not Cdk2 activity. J Biol Chem 272:22300-22306.
8. Bunch RT and Eastman A(1996) Enhancement of cisplatin-induced cytotoxicityby 7-hydroxystaurosporine (UCN-01), a new G2-checkpoint inhibitor. Clin Cancer Res 2:791-797.
9. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, Sedivy JM, Kinzler KW, and Vogelstein B (1998) Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282:1497-1501.
10. 1 by stabilizing p53. Genes Dev 14:278-288.
11. Chou TC (2006) Theoretical basis, experimental design, and computerized simulation of synergism and antagonism in drug combination studies. Pharmacol Rev 58:621-681.
12. Chou TC and Martin NM (2005) CompuSyn for Drug Combinations: PC Software and User's Guide: A Computer Program for Quantitation of Synergism and Antagonism in Drug Combinations, and the Determination of IC50 and ED50 and LD50 Values. ComboSyn, Paramus, NJ.
13. de Cárcer G (2004) Heat shock protein 90 regulates the metaphase-anaphase transition in a polo-like kinase-dependent manner. Cancer Res 64:5106-5112.
14. Goes FS and Martin J (2001) Hsp90 chaperone complexes are required for the activity and stability of yeast protein kinases Mik1, Wee1 and Swe1. Eur J Biochem 268:2281-2289.
15. Graves PR, Yu L, Schwarz JK, Gales J, Sausville EA, O'Connor PM, and Piwnica- Worms H (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. Jallepalli PV, Lengauer C, Vogelstein B, and Bunz F (2003) The Chk2 tumor suppressor is not required for p53 responses in human cancer cells. J Biol Chem 278:20475-20479.
17. Jin J, Ang XL, Ye X, Livingstone M, and Harper JW (2008) Differential roles for checkpoint kinases in DNAdamage-dependent degradation of the Cdc25Aprotein phosphatase. J Biol Chem 283:19322-19328.
18. Lee J, Kumagai A, and Dunphy WG (2001) Positive regulation ofWee1 by Chk1 and 14-3-3 proteins. Mol Biol Cell 12:551-563.
19. 2/M DNA damage checkpoint. Genes Dev 14:1448-1459.
20. Mailand N, Falck J, Lukas C, Syljuâsen RG, Welcker M, Bartek J, and Lukas J (2000) Rapid destruction of human Cdc25A in response to DNA damage. Science 288:1425-1429.
21. Manke IA, Nguyen A, Lim D, Stewart MQ, Elia AE, and Yaffe MB (2005) MAPKAP kinase-2 is a cell cycle checkpoint kinase that regulates the G2/M transition and S phase progression in response to UV irradiation. Mol Cell 17:37-48.
22. Matsuda S, Suzuki-Fujimoto T, Minowa A, Ueno H, Katamura K, and Koyasu S (1999) Temperature-sensitive ZAP70 mutants degrading through a proteasome- independent pathway. Restoration of a kinase domain mutant by Cdc37. J Biol Chem 274:34515-34518.
23. Moran DM, Gawlak G, Jayaprakash MS, Mayar S, and Maki CG (2008) Geldanamycin promotes premature mitotic entry and micronucleation in irradiated p53/ p21 deficient colon carcinoma cells. Oncogene 27:5567-5577.
24. Motwani M, Delohery TM, and Schwartz GK (1999) Sequential dependent enhancement of caspase activation and apoptosis by flavopiridol on paclitaxel-treated human gastric and breast cancer cells. Clin Cancer Res 5:1876-1883.
25. Motwani M, Jung C, Sirotnak FM, She Y, Shah MA, Gonen M, and Schwartz GK (2001) Augmentation of apoptosis and tumor regression by flavopiridol in the presence of CPT-11 in Hct116 colon cancer monolayers and xenografts. Clin Cancer Res 7:4209-4219.
26. Muñoz MJ, Bejarano ER, Daga RR, and Jimenez J (1999) The identification of Wos2, a p23 homologue that interacts with Wee1 and Cdc2 in the mitotic control offission yeasts. Genetics 153:1561-1572.
27. O'Connell MJ, Raleigh JM, Verkade HM, and Nurse P (1997) Chk1 is a wee1 kinase in the G2 DNA damage checkpoint inhibiting cdc2 by Y15 phosphorylation. EMBO J 16:545-554.
28. Parker LL and Piwnica-Worms H (1992) Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science 257:1955-1957.
29. Picard D (2006) Chaperoning steroid hormone action. Trends Endocrinol Metab 17:229-235.
30. PowellSN, DeFrankJS, ConnellP,EoganM, PrefferF, DombkowskiD, TangW,and Friend S (1995) Differential sensitivity of p53( -) and p53( + ) cells to caffeine- induced radiosensitization and override of G2 delay. Cancer Res 55:1643-1648.
31. Reinhardt HC, Aslanian AS, Lees JA, andYaffe MB (2007)p53- deficientcellsrelyon ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell 11:175-189.
32. Rothblum-Oviatt CJ, Ryan CE, and Piwnica-Worms H (2001) 14-3-3 binding regulates catalytic activity of human Wee1 kinase. Cell Growth Differ 12:581-589.
33. Russell KJ, Wiens LW, Demers GW, Galloway DA, Plon SE, and Groudine M (1995) Abrogation of the G2 checkpoint results in differential radiosensitization of G1 checkpoint-deficient and G1 checkpoint-competent cells. Cancer Res 55:1639-1642.
34. Solit DB and Rosen N (2006) Hsp90: a novel target for cancer therapy. Curr Top Med Chem 6:1205-1214.
35. Sørensen CS, Syljuåsen RG, Falck J, Schroeder T, Rönnstrand L, Khanna KK, Zhou BB, Bartek J, and Lukas J (2003) Chk1 regulates the S phase checkpoint by coupling the physiological turnover and ionizing radiation-induced accelerated proteolysis of Cdc25A. Cancer Cell 3:247-258.
36. Srethapakdi M, Liu F, Tavorath R, and Rosen N (2000) Inhibition ofHsp90 function by ansamycins causes retinoblastoma gene product-dependent G1 arrest. Cancer Res 60:3940-3946.
37. Sugimoto K, Sasaki M, Isobe Y, Tsutsui M, Suto H, Ando J, Tamayose K, Ando M, and Oshimi K (2008) Hsp90-inhibitor geldanamycin abrogates G2 arrest in p53- negative leukemia cell lines through the depletion of Chk1. Oncogene 27:3091-3101.
38. Taylor WR and Stark GR(2001)Regulation of the G2/M transition by p53. Oncogene 20:1803-1815.
39. Tse AN, Carvajal R, and Schwartz GK (2007a) Targeting checkpoint kinase 1 in cancer therapeutics. Clin Cancer Res 13:1955-1960.
40. Tse AN, Rendahl KG, Sheikh T, Cheema H, Aardalen K, Embry M, Ma S, Moler EJ, Ni ZJ, Lopes de Menezes DE, et al. (2007b) CHIR-124, a novel potent inhibitor of Chk1, potentiates the cytotoxicity of topoisomerase I poisons in vitro and in vivo. Clin Cancer Res 13:591-602.
41. Tse AN and Schwartz GK (2004) Potentiation of cytotoxicity of topoisomerase I poison by concurrent and sequential treatment with the checkpoint inhibitor 7-hydroxystaurosporine involves disparate mechanisms resulting in either p53- independent clonogenic suppression or p53-dependent mitotic catastrophe. Cancer Res 64:6635-6644.
42. Wang Q, Fan S, Eastman A, Worland PJ, Sausville EA, and O'Connor PM (1996) UCN-01: a potent abrogator of G2 checkpoint function in cancer cells with disrupted p53. J Natl Cancer Inst 88:956-965.
43. Watanabe N, Arai H, Nishihara Y, Taniguchi M, Watanabe N, Hunter T, and Osada H (2004) M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFβ-TrCP. Proc Natl Acad Sci USA 101:4419-4424.
44. Watanabe N, Broome M, and Hunter T (1995) Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J14:1878-1891.
45. Workman P (2004) Combinatorial attack on multistep oncogenesis by inhibiting the Hsp90 molecular chaperone. Cancer Lett 206:149 -157.
46. Xiao Z, Chen Z, Gunasekera AH, Sowin TJ, Rosenberg SH, Fesik S, and Zhang H (2003) Chk1 mediates S and G2 arrests through Cdc25A degradation in response to DNA-damaging agents. J Biol Chem 278:21767-21773.
47. Zachos G, Rainey MD, and Gillespie DA (2003) Chk1-deficient tumour cells are viable but exhibit multiple checkpoint and survival defects. EMBO J 22:713-723.
48. Zhang WH, Poh A, Fanous AA, and Eastman A (2008) DNA damage-induced 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.
49. Zhao H, Watkins JL, and Piwnica-Worms H (2002) Disruption of the checkpoint kinase 1/cell division cycle 25A pathway abrogates ionizing radiation-induced S and G2 checkpoints. Proc Natl Acad Sci USA 99:14795-14800.
50. Zhou BB and Bartek J (2004) Targeting the checkpoint kinases: chemosensitization versus chemoprotection. Nat Rev Cancer 4:216-225.