Casein kinase I epsilon interacts with mitochondrial proteins for the growth and survival of human ovarian cancer cells

EMBO Molecular Medicine

Volumn 4, Issue 9, 2012, Pages 952-963

  Rodriguez, Noah ^a,d   Yang, Junzheng ^a   Hasselblatt, Kathleen ^a   Liu, Shubai ^a   Zhou, Yilan ^a   Rauh Hain, Jose A ^a   Ng, Shu Kay ^b   Choi, Pui Wah ^c   Fong, Wing Ping ^c   Agar, Nathalie Y R ^a   Welch, William R ^a   Berkowitz, Ross S ^a   Ng, Shu Wing ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b GRIFFITH UNIVERSITY   (Australia)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d LOMA LINDA UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Casein kinase I epsilon; Mitochondria; Ovarian cancer; Therapeutic target; Wnt signalling

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; ADENINE NUCLEOTIDE TRANSLOCASE 2; BETA CATENIN; CASEIN KINASE IEPSILON; MITOCHONDRIAL PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; WNT PROTEIN;

ARTICLE; CANCER CELL CULTURE; CELL GROWTH; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; IN VITRO STUDY; OVARY CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

EID: 84865776628     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201101094     Document Type: Article

References (47)

1. Bacher S, Achatz G, Schmitz ML, Lamers MC (2002) Prohibitin and prohibitone are contained in high-molecular weight complexes and interact with alpha-actinin and annexin A2. Biochimie 84: 1207-1220.
2. Barath P, Luciakova K, Hodny Z, Li R, Nelson BD (1999) The growth-dependent expression of the adenine nucleotide translocase-2 (ANT2) gene is regulated at the level of transcription and is a marker of cell proliferation. Exp Cell Res 248: 583-588.
3. Bast RC, Jr, Urban N, Shridhar V, Smith D, Zhang Z, Skates S, Lu K, Liu J, Fishman D, Mills G (2002) Early detection of ovarian cancer: promise and reality. Cancer Treat Res 107: 61-97.
4. Behrend L, Milne DM, Stoter M, Deppert W, Campbell LE, Meek DW, Knippschild U (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.
5. Brockschmidt C, Hirner H, Huber N, Eismann T, Hillenbrand A, Giamas G, Radunsky B, Ammerpohl O, Bohm B, Henne-Bruns D, et al (2008) Anti-apoptotic and growth-stimulatory functions of CK1 delta and epsilon in ductal adenocarcinoma of the pancreas are inhibited by IC261 in vitro and in vivo. Gut 57: 799-806.
6. Cheong JK, Nguyen TH, Wang H, Tan P, Voorhoeve PM, Lee SH, Virshup DM (2011) IC261 induces cell cycle arrest and apoptosis of human cancer cells via CK1delta/varepsilon and Wnt/beta-catenin independent inhibition of mitotic spindle formation. Oncogene 30: 2558-2569.
7. Dolezal T, Kucerova K, Neuhold J, Bryant PJ (2010) Casein kinase I epsilon somatic mutations found in breast cancer cause overgrowth in Drosophila. Int J Dev Biol 54: 1419-1424.
8. Dorner A, Schultheiss HP (2007) Adenine nucleotide translocase in the focus of cardiovascular diseases. Trends Cardiovasc Med 17: 284-290.
9. Dorner A, Schulze K, Rauch U, Schultheiss HP (1997) Adenine nucleotide translocator in dilated cardiomyopathy: pathophysiological alterations in expression and function. Mol Cell Biochem 174: 261-269.
10. Firestein R, Bass AJ, Kim SY, Dunn IF, Silver SJ, Guney I, Freed E, Ligon AH, Vena N, Ogino S, et al (2008) CDK8 is a colorectal cancer oncogene that regulates beta-catenin activity. Nature 455: 547-551.
11. Fish KJ, Cegielska A, Getman ME, Landes GM, Virshup DM (1995) Isolation and characterization of human casein kinase I epsilon (CKI), a novel member of the CKI gene family. J Biol Chem 270: 14875-14883.
12. Foldynova-Trantirkova S, Sekyrova P, Tmejova K, Brumovska E, Bernatik O, Blankenfeldt W, Krejci P, Kozubik A, Dolezal T, Trantirek L, et al (2010) Breast cancer-specific mutations in CK1epsilon inhibit Wnt/beta-catenin and activate the Wnt/Rac1/JNK and NFAT pathways to decrease cell adhesion and promote cell migration. Breast Cancer Res 12: R30.
13. Frezza C, Cipolat S, Scorrano L (2007) Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat Protoc 2: 287-295.
14. Frierson HF, Jr, El-Naggar AK, Welsh JB, Sapinoso LM, Su AI, Cheng J, Saku T, Moskaluk CA, Hampton GM (2002) Large scale molecular analysis identifies genes with altered expression in salivary adenoid cystic carcinoma. Am J Pathol 161: 1315-1323.
15. Fuja TJ, Lin F, Osann KE, Bryant PJ (2004) Somatic mutations and altered expression of the candidate tumor suppressors CSNK1 epsilon, DLG1, and EDD/hHYD in mammary ductal carcinoma. Cancer Res 64: 942-951.
16. Fulda S, Galluzzi L, Kroemer G (2010) Targeting mitochondria for cancer therapy. Nat Rev Drug Discov 9: 447-464.
17. Galluzzi L, Larochette N, Zamzami N, Kroemer G (2006) Mitochondria as therapeutic targets for cancer chemotherapy. Oncogene 25: 4812-4830.
18. Gao ZH, Seeling JM, Hill V, Yochum A, Virshup DM (2002) Casein kinase I phosphorylates and destabilizes the beta-catenin degradation complex. Proc Natl Acad Sci USA 99: 1182-1187.
19. Houldsworth J, Attardi G (1988) Two distinct genes for ADP/ATP translocase are expressed at the mRNA level in adult human liver. Proc Natl Acad Sci USA 85: 377-381.
20. Huang KC, Park DC, Ng SK, Lee JY, Ni X, Ng WC, Bandera CA, Welch WR, Berkowitz RS, Mok SC, et al (2006) Selenium binding protein 1 in ovarian cancer. Int J Cancer 118: 2433-2440.
21. Jang JY, Choi Y, Jeon YK, Kim CW (2008) Suppression of adenine nucleotide translocase-2 by vector-based siRNA in human breast cancer cells induces apoptosis and inhibits tumor growth in vitro and in vivo. Breast Cancer Res 10: R11.
22. Jemal A, Siegel R, Xu J, Ward E (2010) Cancer statistics, 2010. CA Cancer J Clin 60: 277-300.
23. Kang MH, Reynolds CP (2009) Bcl-2 inhibitors: targeting mitochondrial apoptotic pathways in cancer therapy. Clin Cancer Res 15: 1126-1132.
24. Kim SY, Dunn IF, Firestein R, Gupta P, Wardwell L, Repich K, Schinzel AC, Wittner B, Silver SJ, Root DE, et al (2010) CK1epsilon is required for breast cancers dependent on beta-catenin activity. PLoS One 5: e8979.
25. Kishida M, Hino S, Michiue T, Yamamoto H, Kishida S, Fukui A, Asashima M, Kikuchi A (2001) Synergistic activation of the Wnt signaling pathway by Dvl and casein kinase Iepsilon. J Biol Chem 276: 33147-33155.
26. Knippschild U, Gocht A, Wolff S, Huber N, Lohler J, Stoter M (2005) The casein kinase 1 family: participation in multiple cellular processes in eukaryotes. Cell Signal 17: 675-689.
27. Ko HW, Jiang J, Edery I (2002) Role for Slimb in the degradation of Drosophila period protein phosphorylated by doubletime. Nature 420: 673-678.
28. Kosary C (2008) SEER Survival Monograph. National Cancer Institute: 133-142.
29. Le Bras M, Borgne-Sanchez A, Touat Z, El Dein OS, Deniaud A, Maillier E, Lecellier G, Rebouillat D, Lemaire C, Kroemer G, et al (2006) Chemosensitization by knockdown of adenine nucleotide translocase-2. Cancer Res 66: 9143-9152.
30. Lee H, Chen R, Lee Y, Yoo S, Lee C (2009) Essential roles of CKIdelta and CKIepsilon in the mammalian circadian clock. Proc Natl Acad Sci USA 106: 21359-21364.
31. Luo J, Manning BD, Cantley LC (2003) Targeting the PI3K-Akt pathway in human cancer: rationale and promise. Cancer Cell 4: 257-262.
32. McCormick F (1999) Signalling networks that cause cancer. Trends Cell Biol 9: M53- M56.
33. McGuire WP, Hoskins WJ, Brady MF, Kucera PR, Partridge EE, Look KY, Clarke-Pearson DL, Davidson M (1996) Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. N Engl J Med 334: 1-6.
34. Meng QJ, Maywood ES, Bechtold DA, Lu WQ, Li J, Gibbs JE, Dupre SM, Chesham JE, Rajamohan F, Knafels J, et al (2010) Entrainment of disrupted circadian behavior through inhibition of casein kinase 1 (CK1) enzymes. Proc Natl Acad Sci USA 107: 15240-15245.
35. Neckelmann N, Li K, Wade RP, Shuster R, Wallace DC (1987) cDNA sequence of a human skeletal muscle ADP/ATP translocator: lack of a leader peptide, divergence from a fibroblast translocator cDNA, and coevolution with mitochondrial DNA genes. Proc Natl Acad Sci USA 84: 7580-7584.
36. Ng SW, Eder JP, Schnipper LE, Chan VT (1995) Molecular cloning and characterization of the promoter for the Chinese hamster DNA topoisomerase II alpha gene. J Biol Chem 270: 25850-25858.
37. Ozols RF, Bundy BN, Greer BE, Fowler JM, Clarke-Pearson D, Burger RA, Mannel RS, DeGeest K, Hartenbach EM, Baergen R (2003) Phase III trial of carboplatin and paclitaxel compared with cisplatin and paclitaxel in patients with optimally resected stage III ovarian cancer: a Gynecologic Oncology Group study. J Clin Oncol 21: 3194-3200.
38. Patel N, Chatterjee SK, Vrbanac V, Chung I, Mu CJ, Olsen RR, Waghorne C, Zetter BR (2010) Rescue of paclitaxel sensitivity by repression of Prohibitin1 in drug-resistant cancer cells. Proc Natl Acad Sci USA 107: 2503-2508.
39. Peters JM, McKay RM, McKay JP, Graff JM (1999) Casein kinase I transduces Wnt signals. Nature 401: 345-350.
40. Polakis P (2007) The many ways of Wnt in cancer. Curr Opin Genet Dev 17: 45-51.
41. Price MA (2006) CKI, there's more than one: casein kinase I family members in Wnt and Hedgehog signaling. Genes Dev 20: 399-410.
42. Rodriguez-Viciana P, Sabatier C, McCormick F (2004) Signaling specificity by Ras family GTPases is determined by the full spectrum of effectors they regulate. Mol Cell Biol 24: 4943-4954.
43. Seifert JR, Mlodzik M (2007) Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat Rev Genet 8: 126-138.
44. Tang L, Yang J, Ng SK, Rodriguez N, Choi PW, Vitonis A, Wang K, McLachlan GJ, Caiazzo RJ, Jr, Liu BC, et al (2010) Autoantibody profiling to identify biomarkers of key pathogenic pathways in mucinous ovarian cancer. Eur J Cancer 46: 170-179.
45. Tsai IC, Amack JD, Gao ZH, Band V, Yost HJ, Virshup DM (2007) A Wnt-CKIvarepsilon-Rap1 pathway regulates gastrulation by modulating SIPA1L1, a Rap GTPase activating protein. Dev Cell 12: 335-347.
46. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124: 471-484.
47. Yang WS, Stockwell BR (2008) Inhibition of casein kinase 1-epsilon induces cancer-cell-selective, PERIOD2-dependent growth arrest. Genome Biol 9: R92.