P53 deficiency enhances mitotic arrest and slippage induced by pharmacological inhibition of Aurora kinases

Oncogene

Volumn 33, Issue 27, 2014, Pages 3550-3560

  Marxer, M ^a   Ma, H T ^a   Man, W Y ^a   Poon, R Y C ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

mitosis; mitotic catastrophe; mitotic slippage

Indexed keywords

ALISERTIB; ANTINEOPLASTIC AGENT; AURORA KINASE INHIBITOR; BARASERTIB; MK 5108; N [4 [6 METHOXY 7 (3 MORPHOLINOPROPOXY) 4 QUINAZOLINYLAMINO]PHENYL]BENZAMIDE; NOCODAZOLE; PROTEIN P53; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE ARREST; CELL DEATH; CELL FATE; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINESIS; CYTOTOXICITY ASSAY; DNA SYNTHESIS; DRUG MECHANISM; DRUG SENSITIVITY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE DISRUPTION; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; MITOSIS; MITOSIS INHIBITION; MITOTIC SLIPPAGE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEPLETION;

AURORA KINASE A; AURORA KINASE B; AZEPINES; CELL LINE, TUMOR; GENE DUPLICATION; HUMANS; M PHASE CELL CYCLE CHECKPOINTS; MITOSIS; PROTEIN KINASE INHIBITORS; PYRIMIDINES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84903903290     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.325     Document Type: Article

References (36)

1. Ma HT, Poon RY. How protein kinases co-ordinate mitosis in animal cells. Biochem J 2011; 435: 17-31.
2. Karthigeyan D, Prasad SB, Shandilya J, Agrawal S, Kundu TK. Biology of Aurora A kinase: implications in cancer manifestation and therapy. Med Res Rev 2010; 31: 757-793.
3. Ruchaud S, Carmena M, Earnshaw WC. Chromosomal passengers: conducting cell division. Nat Rev Mol Cell Biol 2007; 8: 798-812.
4. Kimura M, Matsuda Y, Yoshioka T, Okano Y. Cell cycle-dependent expression and centrosome localization of a third human aurora/Ipl1-related protein kinase, AIK3. J Biol Chem 1999; 274: 7334-7340.
5. Scutt PJ, Chu ML, Sloane DA, Cherry M, Bignell CR, Williams DH et al. Discovery and exploitation of inhibitor-resistant aurora and polo kinase mutants for the analysis of mitotic networks. J Biol Chem 2009; 284: 15880-15893.
6. Yasui Y, Urano T, Kawajiri A, Nagata K, Tatsuka M, Saya H et al. Autophos-phorylation of a newly identified site of Aurora-B is indispensable for cytokinesis. J Biol Chem 2004; 279: 12997-13003.
7. Gautschi O, Heighway J, Mack PC, Purnell PR, Lara PNJ, Gandara DR. Aurora kinases as anticancer drug targets. Clin Cancer Res 2008; 14: 1639-1648.
8. Green MR, Woolery JE, Mahadevan D. Update on Aurora kinase targeted therapeutics in oncology. Expert Opin Drug Discov 2011; 6: 291-307.
9. Keen N, Taylor S. Aurora-kinase inhibitors as anticancer agents. Nat Rev Cancer 2004; 4: 927-936.
10. Liu Q, Kaneko S, Yang L, Feldman RI, Nicosia SV, Chen J et al. Aurora-A abrogation of p53 DNA binding and transactivation activity by phosphorylation of serine 215. J Biol Chem 2004; 279: 52175-52182.
11. Katayama H, Sasai K, Kawai H, Yuan ZM, Bondaruk J, Suzuki F et al. Phospho-rylation by aurora kinase A induces Mdm2-mediated destabilization and inhibition of p53. Nat Genet 2004; 36: 55-62.
12. Manfredi MG, Ecsedy JA, Chakravarty A, Silverman L, Zhang M, Hoar KM et al. Characterization of Alisertib (MLN8237), an investigational small-molecule inhibitor of aurora A kinase using novel in vivo pharmacodynamic assays. Clin Cancer Res 2011; 17: 7614-7624.
13. Ditchfield C, Johnson VL, Tighe A, Ellston R, Haworth C, Johnson T et al. Aurora B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J Cell Biol 2003; 161: 267-280.
14. Yang J, Ikezoe T, Nishioka C, Tasaka T, Taniguchi A, Kuwayama Y et al. AZD1152, a novel and selective aurora B kinase inhibitor, induces growth arrest, apoptosis, and sensitization for tubulin depolymerizing agent or topoisomerase II inhibitor in human acute leukemia cells in vitro and in vivo. Blood 2007; 110: 2034-2040.
15. Shimomura T, Hasako S, Nakatsuru Y, Mita T, Ichikawa K, Kodera T et al. MK-5108, a highly selective Aurora-A kinase inhibitor, shows antitumor activity alone and in combination with docetaxel. Mol Cancer Ther 2010; 9: 157-166.
16. Harrington EA, Bebbington D, Moore J, Rasmussen RK, Ajose-Adeogun AO, Nakayama T et al. VX-680, a potent and selective small-molecule inhibitor of the Aurora kinases, suppresses tumor growth in vivo. Nat Med 2004; 10: 262-267.
17. Girdler F, Gascoigne KE, Eyers PA, Hartmuth S, Crafter C, Foote KM et al. Validating Aurora B as an anti-cancer drug target. J Cell Sci 2006; 119: 3664-3675.
18. Hegarat N, Smith E, Nayak G, Takeda S, Eyers PA, Hochegger H. Aurora A and Aurora B jointly coordinate chromosome segregation and anaphase microtubule dynamics. J Cell Biol 2011; 195: 1103-1113.
19. Andreassen PR, Lohez OD, Lacroix FB, Margolis RL. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol Biol Cell 2001; 12: 1315-1328.
20. Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 2005; 437: 1043-1047.
21. Uetake Y, Sluder G. Cell cycle progression after cleavage failure: mammalian somatic cells do not possess a "tetraploidy checkpoint". J Cell Biol 2004; 165: 609-615.
22. Wong C, Stearns T. Mammalian cells lack checkpoints for tetraploidy, aberrant centrosome number, and cytokinesis failure. BMC Cell Biol 2005; 6: 6.
23. Storchova Z, Kuffer C. The consequences of tetraploidy and aneuploidy. J Cell Sci 2008; 121: 3859-3866.
24. Dar AA, Belkhiri A, Ecsedy J, Zaika A, El-Rifai W. Aurora kinase A inhibition leads to p73-dependent apoptosis in p53-deficient cancer cells. Cancer Res 2008; 68: 8998-9004.
25. Shao S, Wang Y, Jin S, Song Y, Wang X, Fan W et al. Gadd45a interacts with aurora-A and inhibits its kinase activity. J Biol Chem 2006; 281: 28943-28950.
26. Tao Y, Zhang P, Girdler F, Frascogna V, Castedo M, Bourhis J et al. Enhancement of radiation response in p53-deficient cancer cells by the Aurora-B kinase inhibitor AZD1152. Oncogene 2008; 27: 3244-3255.
27. Gizatullin F, Yao Y, Kung V, Harding MW, Loda M, Shapiro GI. The Aurora kinase inhibitor VX-680 induces endoreduplication and apoptosis preferentially in cells with compromised p53-dependent postmitotic checkpoint function. Cancer Res 2006; 66: 7668-7677.
28. Curry J, Angove H, Fazal L, Lyons J, Reule M, Thompson N et al. Aurora B kinase inhibition in mitosis: strategies for optimising the use of aurora kinase inhibitors such as AT9283. Cell Cycle 2009; 8: 1921-1929.
29. Yam CH, Siu WY, Lau A, Poon RY. Degradation of cyclin A does not require its phosphorylation by CDC2 and cyclin-dependent kinase 2. J Biol Chem 2000; 275: 3158-3167.
30. Chan YW, Ma HT, Wong W, Ho CC, On KF, Poon RY. CDK1 inhibitors antagonize the immediate apoptosis triggered by spindle disruption but promote apoptosis following the subsequent rereplication and abnormal mitosis. Cell Cycle 2008; 7: 1449-1461.
31. On KF, Chen Y, Ma HT, Chow JP, Poon RY. Determinants of mitotic catastrophe on abrogation of the G2 DNA damage checkpoint by UCN-01. Mol Cancer Ther 2011; 10: 784-794.
32. Ma HT, Poon RY. Synchronization of HeLa cells. Methods Mol Biol 2011; 761: 151-161.
33. Poon RY, Toyoshima H, Hunter T. Redistribution of the CDK inhibitor p27 between different cyclin.CDK complexes in the mouse fibroblast cell cycle and in cells arrested with lovastatin or ultraviolet irradiation. Mol Biol Cell 1995; 6: 1197-1213.
34. Siu WY, Arooz T, Poon RY. Differential responses of proliferating versus quiescent cells to adriamycin. Exp Cell Res 1999; 250: 131-141.
35. Chan YW, On KF, Chan WM, Wong W, Siu HO, Hau PM et al. The kinetics of p53 activation versus cyclin E accumulation underlies the relationship between the spindle-assembly checkpoint and the postmitotic checkpoint. J Biol Chem 2008; 283: 15716-15723.
36. Siu WY, Lau A, Arooz T, Chow JP, Ho HT, Poon RY. Topoisomerase poisons differentially activate DNA damage checkpoints through ataxia-telangiectasia mutated-dependent and-independent mechanisms. Mol Cancer Ther 2004; 3: 621-632.