IC261 induces cell cycle arrest and apoptosis of human cancer cells via CK1δ/ε and Wnt/Β-catenin independent inhibition of mitotic spindle formation

Oncogene

Volumn 30, Issue 22, 2011, Pages 2558-2569

  Cheong, J K ^a   Hung, N T ^a   Wang, H ^a   Tan, P ^a   Voorhoeve, P M ^a,b   Lee, S H ^a   Virshup, D M ^a,b  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

cancer; casein kinase 1; IC261; mitotic spindle; synthetic lethal; Wnt

Indexed keywords

ANTINEOPLASTIC AGENT; BETA CATENIN; CASEIN KINASE IDELTA; CASEIN KINASE IEPSILON; COLCHICINE; IC 261; PF 4800567; PF 670462; PROTEIN P53; PROTEIN SERINE THREONINE KINASE INHIBITOR; RAS PROTEIN; SMALL INTERFERING RNA; TUBULIN; UNCLASSIFIED DRUG; WNT PROTEIN;

APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; BINDING AFFINITY; CANCER CELL CULTURE; CANCER INHIBITION; CELL CYCLE ARREST; CELL DEATH; CELL KILLING; CELL PROLIFERATION; CELL VIABILITY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; MICROTUBULE ASSEMBLY; MITOSIS SPINDLE; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS; BETA CATENIN; CASEIN KINASE IDELTA; CASEIN KINASE IEPSILON; CELL CYCLE; CELL LINE, TUMOR; HUMANS; INDOLES; MITOTIC SPINDLE APPARATUS; NEOPLASMS; PHLOROGLUCINOL; PHOSPHOPROTEINS; PHOSPHORYLATION; PYRAZOLES; PYRIMIDINES; RNA, SMALL INTERFERING; WNT PROTEINS;

EID: 79957908556     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.627     Document Type: Article

References (47)

1. Agapova LS, Ivanov AV, Sablina AA, Kopnin PB, Sokova OI, Chumakov PM et al. (1999). P53-dependent effects of RAS oncogene on chromosome stability and cell cycle checkpoints. Oncogene 18: 3135-3142. (Pubitemid 29261234)
2. Arora S, Wang XI, Keenan SM, Andaya C, Zhang Q, Peng Y et al. (2009). Novel microtubule polymerization inhibitor with potent antiproliferative and antitumor activity. Cancer Res 69: 1910-1915.
3. Badura L, Swanson T, Adamowicz W, Adams J, Cianfrogna J, Fisher K et al. (2007). An inhibitor of casein kinase I epsilon induces phase delays in circadian rhythms under free-running and entrained conditions. J Pharmacol Exp Ther 322: 730-738. (Pubitemid 47105782)
4. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H et al. (2007). The selectivity of protein kinase inhibitors: a further update. Biochem J408: 297-315.
5. Behrend L, Milne DM, Stoter M, Deppert W, Campbell LE, Meek DW et al. (2000). IC261, a specific inhibitor of the protein kinases casein kinase 1-delta and-epsilon, triggers the mitotic checkpoint and induces p53-dependent postmitotic effects. Oncogene 19: 5303-5313.
6. Brockschmidt C, Hirner H, Huber N, Eismann T, Hillenbrand A, Giamas G et al. (2008). Anti-apoptotic and growth-stimulatory functions ofCK1 delta and epsilon in ductal adenocarcinoma of the pancreas are inhibited by IC261 in vitro and in vivo. Gut 57: 799-806. (Pubitemid 351716974)
7. Bryant CD, Graham ME, Distler MG, Munoz MB, Li D, Vezina P et al. (2009). A role for casein kinase 1 epsilon in the locomotor stimulant response to methamphetamine. Psychopharmacology (Berl) 203: 703-711.
8. Bryja V, Schulte G, Arenas E. (2007). Wnt-3a utilizes a novel low dose and rapid pathway that does not require casein kinase 1-mediated phosphorylation of Dvl to activate beta-catenin. Cell Signal 19: 610-616. (Pubitemid 46107812)
9. Cegielska A, Gietzen KF, Rivers A, Virshup DM. (1998). Autoinhibi-tion of casein kinase I epsilon (CKI epsilon) is relieved by protein phosphatases and limited proteolysis. J Biol Chem 273: 1357-1364. (Pubitemid 28133653)
10. Clokie S, Falconer H, Mackie S, Dubois T, Aitken A. (2009). The interaction between casein kinase Ialpha and 14-3-3 is phosphoryla-tion dependent. FEBS J276: 6971-6984.
11. Coombs GS, Yu J, Canning CA, Veltri CA, Covey TM, Cheong JK et al. (2010). WLS-dependent secretion of WNT3A requires Ser209 acylation and vacuolar acidification. J Cell Sci 123: 3357-3367.
12. Dalton WB, Nandan MO, Moore RT, Yang VW. (2007). Human cancer cells commonly acquire DNA damage during mitotic arrest. Cancer Res 67: 11487-11492.
13. Eide EJ, Woolf MF, Kang H, Woolf P, Hurst W, Camacho F et al. (2005). Control of mammalian circadian rhythm by CKIepsilon-regulated proteasome-mediated PER2 degradation. Mol Cell Biol 25: 2795-2807. (Pubitemid 40381641)
14. Eisen MB, Spellman PT, Brown PO, Botstein D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci 282165703USA 95: 14863-14868. (Pubitemid 29003722)
15. Fedorov O, Marsden B, Pogacic V, Rellos P, Muller S, Bullock AN et al. (2007). A systematic interaction map of validated kinase inhibitors with Ser/Thr kinases. Proc Natl Acad Sci USA 104: 20523-20528.
16. Gao Z-H, Seeling JM, Hill V, Yochum A, Virshup DM. (2002). Casein kinase I phosphorylates and destabilizes the beta-catenin degrada-tion complex. Proc Natl Acad Sci USA 99: 1182-1187. (Pubitemid 34136467)
17. Gascoigne KE, Taylor SS. (2008). Cancer cells display profound intra-and interline variation following prolonged exposure to antimitotic drugs. Cancer Cell 14: 111-122.
18. Gigant B, Cormier A, Dorleans A, Ravelli R, Knossow M. (2009). Microtubule-destabilizing agents: structural and mechanistic in-sights from the interaction of colchicine and vinblastine with tubulin. Top Curr Chem 286: 259-278.
19. Grueneberg DA, Degot S, Pearlberg J, Li W, Davies JE, Baldwin A et al. (2008). Kinase requirements in human cells: I. Comparing kinase requirements across various cell types. Proc Natl Acad Sci USA 105: 16472-16477.
20. Hampton T. (2004). 'Promiscuous' anticancer drugs that hit multiple targets may thwart resistance. JAMA 292: 419-422.
21. Kim SY, Dunn IF, Firestein R, Gupta P, Wardwell L, Repich K et al. (2010). CK1epsilon is required for breast cancers dependent on beta-catenin activity. PLoS One 5: e8979.
22. Kishida M, Si H, Michiue T, Yamamoto H, Kishida S, Fukui A et al. (2001). Synergistic activation of the Wnt signaling pathway by Dvl and casein kinase Iepsilon. J Biol Chem 276: 33147-33155.
23. Kloss B, Price JL, Saez L, Blau J, Rothenfluh A, Wesley CS et al. (1998). The Drosophila clock gene double-time encodes a protein closely related to human casein kinase Iepsilon. Cell 94: 97-107. (Pubitemid 28347473)
24. Knippschild U, Wolff S, Giamas G, Brockschmidt C, Wittau M, Wurl PU et al. (2005). The role of the casein kinase 1 (CK1) family in different signaling pathways linked to cancer development. Onkologie 28: 508-514. (Pubitemid 41420848)
25. Kuo CC, Hsieh HP, Pan WY, Chen CP, Liou JP, Lee SJ et al. (2004). BPR0L075, a novel synthetic indole compound with antimitotic activity in human cancer cells, exerts effective antitumoral activity in vivo. Cancer Res 64: 4621-4628.
26. Lee E, Salic A, Kirschner MW. (2001). Physiological regulation of [beta]-catenin stability by Tcf3 and CK1epsilon. J Cell Biol 154: 983-993. (Pubitemid 34286178)
27. Mashhoon N, DeMaggio AJ, Tereshko V, Bergmeier SC, Egli M, Hoekstra MF et al. (2000). Crystal structure of a conformation-selective casein kinase-1 inhibitor. J Biol Chem 275: 20052-20060. (Pubitemid 30441614)
28. McCright B, Virshup DM. (1995). Identification of a new family of protein phosphatase 2A regulatory subunits. J Biol Chem 270: 26123-26128.
29. Meng Q-J, Logunova L, Maywood ES, Gallego M, Lebiecki J, Brown TM et al. (2008). Setting clock speed in mammals: the CK1 epsilon tau mutation in mice accelerates circadian pacemakers by selectively destabilizing PERIOD proteins. Neuron 58: 78-88. (Pubitemid 351467026)
30. Nakayama GR, Caton MC, Nova MP, Parandoosh Z. (1997). Assessment of the Alamar Blue assay for cellular growth and viability in vitro. J Immunol Methods 204: 205-208. (Pubitemid 27262014)
31. Peters JM, McKay RM, McKay JP, Graff JM. (1999). Casein kinase I transduces Wnt signals. Nature 401: 345-350. (Pubitemid 29454951)
32. Price JL, Blau J, Rothenfluh A, Abodeely M, Kloss B, Young MW. (1998). double-time is a novel Drosophila clock gene that regulates PERIOD protein accumulation. Cell 94: 83-95. (Pubitemid 28347472)
33. Price MA. (2006). CKI, there's more than one: casein kinase I family members in Wnt and Hedgehog signaling. Genes Dev 20: 399-410.
34. Rangarajan A, Hong SJ, Gifford A, Weinberg RA. (2004). Species-and cell type-specific requirements for cellular transformation. Cancer Cell 6: 171-183. (Pubitemid 39485689)
35. Rivers A, Gietzen KF, Vielhaber E, Virshup DM. (1998). Regulation of casein kinase I epsilon and casein kinase I delta by an in vivo futile phosphorylation cycle. J Biol Chem 273: 15980-15984. (Pubitemid 28311363)
36. Sakanaka C, Leong P, Xu L, Harrison SD, Williams LT. (1999). Casein kinase iepsilon in the wnt pathway: regulation of beta-catenin function. Proc Natl Acad Sci USA 96: 12548-12552. (Pubitemid 29513539)
37. Sprouse J, Reynolds L, Swanson TA, Engwall M. (2009). Inhibition of casein kinase I epsilon/delta produces phase shifts in the circadian rhythms of Cynomolgus monkeys. Psychopharmacology (Berl) 204: 735-742.
38. Stoter M, Bamberger A-M, Aslan B, Kurth M, Speidel D, Loning T et al. (2005). Inhibition of casein kinase I delta alters mitotic spindle formation and induces apoptosis in trophoblast cells. Oncogene 24: 7964-7975. (Pubitemid 41746740)
39. Toh KL, Jones CR, He Y, Eide EJ, Hinz WA, Virshup DM et al. (2001). An hPer2 phosphorylation site mutation in familial advanced sleep phase syndrome. Science 291: 1040-1043. (Pubitemid 32157412)
40. Tusher VG, Tibshirani R, Chu G (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci 282165720 USA 98: 5116-5121. (Pubitemid 32397092)
41. Vielhaber E, Virshup DM. (2001). Casein kinase I: from obscurity to center stage. IUBMB Life 51: 73-78. (Pubitemid 32651761)
42. Virshup DM, Eide EJ, Forger DB, Gallego M, Harnish EV. (2007). Reversible protein phosphorylation regulates circadian rhythms. Cold Spring Harb Symp Quant Biol 72: 413-420.
43. Voorhoeve PM, Agami R. (2003). The tumor-suppressive functions of the human INK4A locus. Cancer Cell 4: 311-319. (Pubitemid 37329795)
44. Walton K, Fisher K, Rubitski D, Marconi M, Meng Q, Sladek M et al. (2009). Selective inhibition of casein kinase 1 epsilon minimally alters circadian clock period. J Pharmacol Exp Ther 330: 430-439.
45. Weaver BA, Cleveland DW. (2005). Decoding the links between mitosis, cancer, and chemotherapy: the mitotic checkpoint, adapta-tion, and cell death. Cancer Cell 8: 7-12. (Pubitemid 40991810)
46. Yang WS, Stockwell BR. (2008). Inhibition of casein kinase 1-epsilon induces cancer-cell-selective, PERIOD2-dependent growth arrest. Genome Biol 9: R92.
47. Yu W, Zheng H, Price JL, Hardin PE. (2009). DOUBLETIME plays a noncatalytic role to mediate CLOCK phosphorylation and repress CLOCK-dependent transcription within the Drosophila circadian clock. Mol Cell Biol 29: 1452-1458.