Salt-inducible kinase 3 is a novel mitotic regulator and a target for enhancing antimitotic therapeutic-mediated cell death

Cell Death and Disease

Volumn 5, Issue 4, 2014, Pages

  Chen, H ^a,b   Huang, S ^a   Han, X ^a   Zhang, J ^a   Shan, C ^a   Tsang, Y H ^a   Ma, H T ^a   Poon, R Y C ^a  

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

^b PEKING UNIVERSITY CANCER HOSPITAL AND INSTITUTE   (China)

Author keywords

Antimitotic drugs; Aurora kinase; Eg5; Mitosis; PLK1; QSK

Indexed keywords

ANTIMITOTIC AGENT; AURORA A KINASE; AURORA B KINASE; HISTONE H2B; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; KINESIN; KINESIN EG5; POLO LIKE KINASE 1; SALT INDUCIBLE KINASE 3; UNCLASSIFIED DRUG; HISTONE DEACETYLASE; KIAA0999 PROTEIN, HUMAN; PROTEIN KINASE; PROTEIN KINASE INHIBITOR; PROTEIN SERINE THREONINE KINASE; SIK3 PROTEIN, MOUSE; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL DEATH; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; DOWN REGULATION; DRUG TARGETING; FIBROBLAST; HELA CELL LINE; M PHASE CELL CYCLE CHECKPOINT; MITOSIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; 3T3 CELL LINE; ANIMAL; CYTOLOGY; DRUG EFFECTS; DRUG RESISTANCE; ENZYMOLOGY; GENE DELETION; HUMAN; METABOLISM; MITOSIS; SPINDLE APPARATUS;

ANIMALS; ANTIMITOTIC AGENTS; CELL DEATH; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FIBROBLASTS; GENE DELETION; HELA CELLS; HISTONE DEACETYLASES; HUMANS; MICE; MITOSIS; NIH 3T3 CELLS; PROTEIN KINASE INHIBITORS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; SPINDLE APPARATUS;

EID: 84901041806     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.154     Document Type: Article

References (44)

1. Ma HT, Poon RY. How protein kinases co-ordinate mitosis in animal cells. Biochem J 2011; 435: 17-31.
2. Bettencourt-Dias M, Giet R, Sinka R, Mazumdar A, Lock WG, Balloux F, Zafiropoulos PJ, Yamaguchi S, Winter S, Carthew RW, Cooper M, Jones D, Frenz L, Glover DM. Genomewide survey of protein kinases required for cell cycle progression. Nature 2004; 432: 980-987.
3. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S. The protein kinase complement of the human genome. Science 2002; 298: 1912-1934.
4. Wang Z, Takemori H, Halder SK, Nonaka Y, Okamoto M. Cloning of a novel kinase (SIK) of the SNF1/AMPK family from high salt diet-treated rat adrenal. FEBS Lett 1999; 453: 135-139.
5. Lizcano JM, Goransson O, Toth R, Deak M, Morrice NA, Boudeau J, Hawley SA, Udd L, Makela TP, Hardie DG, Alessi DR. LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J 2004; 23: 833-843.
6. Al-Hakim AK, Goransson O, Deak M, Toth R, Campbell DG, Morrice NA, Prescott AR, Alessi DR. 14-3-3 cooperates with LKB1 to regulate the activity and localization of QSK and SIK. J Cell Sci 2005; 118: 5661-5673.
7. Walkinshaw DR, Weist R, Kim GW, You L, Xiao L, Nie J, Li CS, Zhao S, Xu M, Yang XJ. The tumor suppressor kinase LKB1 activates the downstream kinases SIK2 and SIK3 to stimulate nuclear export of class IIa histone deacetylases. J Biol Chem 2013; 288: 9345-9362.
8. Wang B, Moya N, Niessen S, Hoover H, Mihaylova MM, Shaw RJ, Yates JRr, Fischer WH, Thomas JB, Montminy M. A hormone-dependent module regulating energy balance. Cell 2011; 145: 596-606.
9. Uebi T, Itoh Y, Hatano O, Kumagai A, Sanosaka M, Sasaki T, Sasagawa S, Doi J, Tatsumi K, Mitamura K, Morii E, Aozasa K, Kawamura T, Okumura M, Nakae J, Takikawa H, Fukusato T, Koura M, Nish M, Hamsten A, Silveira A, Bertorello AM, Kitagawa K, Nagaoka Y, Kawahara H, Tomonaga T, Naka T, Ikegawa S, Tsumaki N, Matsuda J, Takemori H. Involvement of SIK3 in glucose and lipid homeostasis in mice. PLoS One 2012; 7: e37803.
10. Sasagawa S, Takemori H, Uebi T, Ikegami D, Hiramatsu K, Ikegawa S, Yoshikawa H, Tsumaki N. SIK3 is essential for chondrocyte hypertrophy during skeletal development in mice. Development 2012; 139: 1153-1163.
11. Wehr MC, Holder MV, Gailite I, Saunders RE, Maile TM, Ciirdaeva E, Instrell R, Jiang M, Howell M, Rossner MJ, Tapon N. Salt-inducible kinases regulate growth through the Hippo signalling pathway in Drosophila. Nat Cell Biol 2013; 15: 61-71.
12. Charoenfuprasert S, Yang YY, Lee YC, Chao KC, Chu PY, Lai CR, Hsu KF, Chang KC, Chen YC, Chen LT, Chang JY, Leu SJ, Shih NY. Identification of salt-inducible kinase 3 as a novel tumor antigen associated with tumorigenesis of ovarian cancer. Oncogene 2011; 30: 3570-3584.
13. Manfredi MG, Ecsedy JA, Chakravarty A, Silverman L, Zhang M, Hoar KM, Stroud SG, Chen W, Shinde V, Huck JJ,Wysong DR, Janowick DA, Hyer ML, Leroy PJ, Gershman RE, Silva MD, Germanos MS, Bolen JB, Claiborne CF, Sells TB. 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.
14. Marxer M, Ma HT, Man WY, Poon RYC. p53 deficiency enhances mitotic arrest and slippage induced by pharmacological inhibition of Aurora kinases. Oncogene 2013; e-pub ahead of print 19 August 2013; doi:10.1038/onc.2013.325.
15. Shimomura T, Hasako S, Nakatsuru Y, Mita T, Ichikawa K, Kodera T, Sakai T, Nambu T, Miyamoto M, Takahashi I, Miki S, Kawanishi N, Ohkubo M, Kotani H, Iwasawa Y. 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. Yang J, Ikezoe T, Nishioka C, Tasaka T, Taniguchi A, Kuwayama Y, Komatsu N, Bandobashi K, Togitani K, Koeffler HP, Taguchi H, Yokoyama A. 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.
17. Steegmaier M, Hoffmann M, Baum A, Lenart P, Petronczki M, Krssak M, Gurtler U, Garin-Chesa P, Lieb S, Quant J, Grauert M, Adolf GR, Kraut N, Peters JM, Rettig WJ. BI 2536, a potent and selective inhibitor of polo-like kinase 1, inhibits tumor growth in vivo. Curr Biol 2007; 17: 316-322.
18. Sakowicz R, Finer JT, Beraud C, Crompton A, Lewis E, Fritsch A, Lee Y, Mak J, Moody R, Turincio R, Chabala JC, Gonzales P, Roth S, Weitman S, Wood KW. Antitumor activity of a kinesin inhibitor. Cancer Res 2004; 64: 3276-3280.
19. Cadot B, Brunetti M, Coppari S, Fedeli S, de Rinaldis E, Dello Russo C, Gallinari P, De Francesco R, Steinkuhler C, Filocamo G. Loss of histone deacetylase 4 causes segregation defects during mitosis of p53-deficient human tumor cells. Cancer Res 2009; 69: 6074-6082.
20. Eot-Houllier G, Fulcrand G, Magnaghi-Jaulin L, Jaulin C. Histone deacetylase inhibitors and genomic instability. Cancer Lett 2009; 274: 169-176.
21. Richon VM, Webb Y, Merger R, Sheppard T, Jursic B, Ngo L, Civoli F, Breslow R, Rifkind RA, Marks PA. Second generation hybrid polar compounds are potent inducers of transformed cell differentiation. Proc Natl Acad Sci USA 1996; 93: 5705-5708.
22. Caenepeel S, Charydczak G, Sudarsanam S, Hunter T, Manning G. The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc Natl Acad Sci USA 2004; 101: 11707-11712.
23. Wang Q, Greene MI. EGFR enhances Survivin expression through the phosphoinositide 3 (PI-3) kinase signaling pathway. Exp Mol Pathol 2005; 79: 100-107.
24. Tao W, Zhang S, Turenchalk GS, Stewart RA St, John MA, Chen W, Xu T. Human homologue of the Drosophila melanogaster lats tumour suppressor modulates CDC2 activity. Nat Genet 1999; 21: 177-181.
25. Bachmann M, Hennemann H, Xing PX, Hoffmann I, Moroy T. The oncogenic serine/ threonine kinase Pim-1 phosphorylates and inhibits the activity of Cdc25C-associated kinase 1 (C-TAK1): a novel role for Pim-1 at the G2/M cell cycle checkpoint. J Biol Chem 2004; 279: 48319-48328.
26. Kato M, Yano K, Morotomi-Yano K, Saito H, Miki Y. Identification and characterization of the human protein kinase-like gene NTKL: mitosis-specific centrosomal localization of an alternatively spliced isoform. Genomics 2002; 79: 760-767.
27. Hergovich A, Stegert MR, Schmitz D, Hemmings BA. NDR kinases regulate essential cell processes from yeast to humans. Nat Rev Mol Cell Biol 2006; 7: 253-264.
28. Ma HT, Tsang YH, Marxer M, Poon RY. Cyclin A2-cyclin-dependent kinase 2 cooperates with the PLK1-SCFbeta-TrCP1-EMI1-anaphase-promoting complex/cyclosome axis to promote genome reduplication in the absence of mitosis. Mol Cell Biol 2009; 29: 6500-6514.
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. Cheung ST, Huang DP, Hui AB, Lo KW, Ko CW, Tsang YS, Wong N, Whitney BM, Lee JC. Nasopharyngeal carcinoma cell line (C666-1) consistently harbouring Epstein-Barr virus. Int J Cancer 1999; 83: 121-126.
31. Sizhong Z, Xiukung G, Yi Z. Cytogenetic studies on an epithelial cell line derived from poorly differentiated nasopharyngeal carcinoma. Int J Cancer 1983; 31: 587-590.
32. Glaser R, Zhang HY, Yao KT, Zhu HC, Wang FX, Li GY, Wen DS, Li YP. Two epithelial tumor cell lines (HNE-1 and HONE-1) latently infected with Epstein-Barr virus that were derived from nasopharyngeal carcinomas. Proc Natl Acad Sci USA 1989; 86: 9524-9528.
33. Li HM, Man C, Jin Y, Deng W, Yip YL, Feng HC, Cheung YC, Lo KW, Meltzer PS, Wu ZG, Kwong YL, Yuen AP, Tsao SW. Molecular and cytogenetic changes involved in the immortalization of nasopharyngeal epithelial cells by telomerase. Int J Cancer 2006; 119: 1567-1576.
34. 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.
35. 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.
36. Ma HT, Chan YY, Chen X, On KF, Poon RY. Depletion of p31comet protein promotes sensitivity to antimitotic drugs. J Biol Chem 2012; 287: 21561-21569.
37. Ma HT, Poon RY. Synchronization of HeLa cells. Methods Mol Biol 2011; 761: 151-161.
38. 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.
39. Siu WY, Arooz T, Poon RY. Differential responses of proliferating versus quiescent cells to adriamycin. Exp Cell Res 1999; 250: 131-141.
40. Chow JP, Siu WY, Ho HT, Ma KH, Ho CC, Poon RY. Differential contribution of inhibitory phosphorylation of CDC2 and CDK2 for unperturbed cell cycle control and DNA integrity checkpoints. J Biol Chem 2003; 278: 40815-40828.
41. Chan YW, On KF, Chan WM, Wong W, Siu HO, Hau PM, Poon RY. 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.
42. 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.
43. Fung TK, Siu WY, Yam CH, Lau A, Poon RY. Cyclin F is degraded during G2-M by mechanisms fundamentally different from other cyclins. J Biol Chem 2002; 277: 35140-35149.
44. Harlow E, Lane DP. Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press: New York, USA, 1988.