Knockdown of cyclin-dependent kinase 10 (cdk10) gene impairs neural progenitor survival via modulation of raf1a gene expression

Journal of Biological Chemistry

Volumn 288, Issue 39, 2013, Pages 27927-27939

  Yeh, Chi Wei ^a   Kao, Shoa Hsuan ^a   Cheng, Yi Chuan ^b   Hsu, Li Sung ^a,c  

^a CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c CHUNG SHAN MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEVELOPMENT; CYCLIN-DEPENDENT KINASE; NEURAL PROGENITOR CELLS; NEUROGENESIS; ZEBRAFISH;

CELL DEATH; CELL PROLIFERATION; GENE EXPRESSION;

MODULATION;

CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 10; HISTONE H1; MESSENGER RNA; MORPHOLINO OLIGONUCLEOTIDE; PROTEIN; RAF1A PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETS2; TUBULIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENE FUNCTION; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NONHUMAN; ORTHOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAF1A GENE; RETINA GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSORY NERVE CELL; SPINAL CORD; TELENCEPHALON; ZEBRA FISH;

APOPTOSIS; CDK (CYCLIN-DEPENDENT KINASE); CDK10; DEVELOPMENT; NEURONS; ZEBRAFISH;

AMINO ACID SEQUENCE; ANIMALS; CYCLIN-DEPENDENT KINASES; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEK293 CELLS; HISTONES; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NEUROGENESIS; NEURONS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-RAF; RETINAL GANGLION CELLS; SEQUENCE HOMOLOGY, AMINO ACID; STEM CELLS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84884734639     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.420265     Document Type: Article

References (47)

1. Aouadi, M., Binetruy, B., Caron, L., Le Marchand-Brustel, Y., and Bost, F. (2006) Role of MAPKs in development and differentiation: lessons from knockout mice. Biochimie 88, 1091-1098
2. Deacon, E. M., Pettitt, T. R., Webb, P., Cross, T., Chahal, H., Wakelam, M. J., and Lord, J. M. (2002) Generation of diacylglycerol molecular species through the cell cycle: a role for 1-stearoyl,2-arachidonyl glycerol in the activation of nuclear protein kinase C-II at G2/M. J. Cell Sci. 115, 983-989
3. Morgan, D. O. (1997) Cyclin-dependent kinases: engines, clocks, and microprocessors. Annu. Rev. Cell Dev. Biol. 13, 261-291
4. Morgan, D. O. (1995) Principles of CDK regulation. Nature 374, 131-134
5. Meyerson, M., Enders, G. H., Wu, C. L., Su, L. K., Gorka, C., Nelson, C., Harlow, E., and Tsai, L. H. (1992) A family of human cdc2-related protein kinases. EMBO J. 11, 2909-2917
6. Bullrich, F., MacLachlan, T. K., Sang, N., Druck, T., Veronese, M. L., Allen, S. L., Chiorazzi, N., Koff, A., Heubner, K., Croce, C. M., and Giordano, A. (1995) Chromosomal mapping of members of the cdc2 family of protein kinases, cdk3, cdk6, PISSLRE, and PITALRE, and a cdk inhibitor, p27Kip1, to regions involved in human cancer. Cancer Res. 55, 1199-1205
7. Kasten, M., and Giordano, A. (2001) Cdk10, a Cdc2-related kinase, associates with the Ets2 transcription factor and modulates its transactivation activity. Oncogene 20, 1832-1838
8. Li, S., MacLachlan, T. K., De Luca, A., Claudio, P. P., Condorelli, G., and Giordano, A. (1995) The cdc-2-related kinase, PISSLRE, is essential for cell growth and acts in G2 phase of the cell cycle. Cancer Res. 55, 3992-3995
9. Li, A., Zhu, X., Brown, B., and Craft, C. M. (2003) Gene expression networks underlying retinoic acid-induced differentiation of human retinoblastoma cells. Invest. Ophthalmol. Vis. Sci. 44, 996-1007
10. Leman, E. S., Magheli, A., Yong, K. M., Netto, G., Hinz, S., and Getzenberg, R. H. (2009) Identification of nuclear structural protein alterations associated with seminomas. J. Cell. Biochem. 108, 1274-1279
11. Husson, H., Carideo, E. G., Neuberg, D., Schultze, J., Munoz, O., Marks, P. W., Donovan, J. W., Chillemi, A. C., O'Connell, P., and Freedman, A. S. (2002) Gene expression profiling of follicular lymphoma and normal germinal center B cells using cDNA arrays. Blood 99, 282-289
12. Iorns, E., Turner, N. C., Elliott, R., Syed, N., Garrone, O., Gasco, M., Tutt, A. N., Crook, T., Lord, C. J., and Ashworth, A. (2008) Identification of CDK10 as an important determinant of resistance to endocrine therapy for breast cancer. Cancer Cell 13, 91-104
13. Chen, E., and Ekker, S. C. (2004) Zebrafish as a genomics research model. Curr. Pharm. Biotechnol. 5, 409-413
14. Liu, Q. Y., Wu, Z. L., Lv, W. J., Yan, Y. C., and Li, Y. P. (2007) Developmental expression of cyclin H and Cdk7 in zebrafish: the essential role of cyclin H during early embryo development. Cell Res. 17, 163-173
15. Kanungo, J., Li, B. S., Zheng, Y., and Pant, H. C. (2006) Cyclin-dependent kinase 5 influences Rohon-Beard neuron survival in zebrafish. J. Neurochem. 99, 251-259
16. Grant, P., Sharma, P., and Pant, H. C. (2001) Cyclin-dependent protein kinase 5 (Cdk5) and the regulation of neurofilament metabolism. Eur. J. Biochem. 268, 1534-1546
17. Kanungo, J., Zheng, Y. L., Amin, N. D., Kaur, S., Ramchandran, R., and Pant, H. C. (2009) Specific inhibition of cyclin-dependent kinase 5 activity induces motor neuron development in vivo. Biochem. Biophys. Res. Commun. 386, 263-267
18. Hsu, L. S., Liang, C. J., Tseng, C. Y., Yeh, C. W., and Tsai, J. N. (2011) Zebrafish Cyclin-dependent protein kinase-like 1 (zcdkl1): identification and functional characterization. Int. J. Mol. Sci. 12, 3606-3617
19. Westerfield, M., Doerry, E., Kirkpatrick, A. E., Driever, W., and Douglas, S. A. (1997) An on-line database for zebrafish development and genetics research. Semin. Cell Dev. Biol. 8, 477-488
20. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., and Schilling, T. F. (1995) Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310
21. Hsu, L. S., and Tseng, C. Y. (2010) Zebrafish calcium/calmodulin- dependent protein kinase II (cam-kii) inhibitors: expression patterns and their roles in zebrafish brain development. Dev. Dyn. 239, 3098-3105
22. Thisse, C., and Thisse, B. (2008) High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protoc. 3, 59-69
23. Robu, M. E., Larson, J. D., Nasevicius, A., Beiraghi, S., Brenner, C., Farber, S. A., and Ekker, S. C. (2007) p53 activation by knockdown technologies. PLoS Genet. 3, e78
24. Fan, Y., and Bergmann, A. (2008) Apoptosis-induced compensatory proliferation. The cell is dead. Long live the cell! Trends Cell Biol. 18, 467-473
25. Graham, V., Khudyakov, J., Ellis, P., and Pevny, L. (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39, 749-765
26. Ko, C. Y., Tsai, M. Y., Tseng, W. F., Cheng, C. H., Huang, C. R., Wu, J. S., Chung, H. Y., Hsieh, C. S., Sun, C. K., Hwang, S. P., Yuh, C. H., Huang, C. J., Pai, T. W., Tzou, W. S., and Hu, C. H. (2011) Integration of CNS survival and differentiation by HIF2. Cell Death Differ. 18, 1757-1770
27. Kay, J. N., Link, B. A., and Baier, H. (2005) Staggered cell-intrinsic timing of ath5 expression underlies the wave of ganglion cell neurogenesis in the zebrafish retina. Development 132, 2573-2585
28. Liu, W., Mo, Z., and Xiang, M. (2001) The Ath5 proneural genes function upstream of Brn3 POU domain transcription factor genes to promote retinal ganglion cell development. Proc. Natl. Acad. Sci. U.S.A. 98, 1649-1654
29. Yu, J. H., Zhong, X. Y., Zhang, W. G., Wang, Z. D., Dong, Q., Tai, S., Li, H., and Cui, Y. F. (2012) CDK10 functions as a tumor suppressor gene and regulates survivability of biliary tract cancer cells. Oncol. Rep. 27, 1266-1276
30. Zhong, X. Y., Xu, X. X., Yu, J. H., Jiang, G. X., Yu, Y., Tai, S., Wang, Z. D., and Cui, Y. F. (2012) Clinical and biological significance of Cdk10 in hepatocellular carcinoma. Gene 498, 68-74
31. Kanungo, J., Li, B. S., Goswami, M., Zheng, Y. L., Ramchandran, R., and Pant, H. C. (2007) Cloning and characterization of zebrafish (Danio rerio) cyclin-dependent kinase. Neurosci. Lett. 412, 233-238
32. Cole, L. K., and Ross, L. S. (2001) Apoptosis in the developing zebrafish embryo. Dev. Biol. 240, 123-142
33. Tanaka, H., Morimura, R., and Ohshima, T. (2012) Dpysl2 (CRMP2) and Dpysl3 (CRMP4) phosphorylation by Cdk5 and DYRK2 is required for proper positioning of Rohon-Beard neurons and neural crest cells during neurulation in zebrafish. Dev. Biol. 370, 223-236
34. Zhang, L., Li, Y. Y., Chen, T., Xia, W., Zhou, Y., Wan, Y. J., Lv, Z. Q., Li, G. Q., and Xu, S. Q. (2011) Abnormal development of motor neurons in perfluorooctane sulphonate exposed zebrafish embryos. Ecotoxicology 20, 643-652
35. Bagella, L., Giacinti, C., Simone, C., and Giordano, A. (2006) Identification of murine cdk10: association with Ets2 transcription factor and effects on the cell cycle. J. Cell. Biochem. 99, 978-985
36. McLaughlin, T., Torborg, C. L., Feller, M. B., and O'Leary, D. D. (2003) Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 40, 1147-1160
37. Chen, J., Miao, Y., Wang, X. H., and Wang, Z. (2011) Elevation of p-NR2A(S1232) by Cdk5/p35 contributes to retinal ganglion cell apoptosis in a rat experimental glaucoma model. Neurobiol. Dis. 43, 455-464
38. Bermel, C., Tönges, L., Planchamp, V., Gillardon, F., Weishaupt, J. H., Dietz, G. P., Bähr, M., and Lingor, P. (2009) Combined inhibition of Cdk5 and ROCK additively increase cell survival, but not the regenerative response in regenerating retinal ganglion cells. Mol. Cell. Neurosci. 42, 427-437
39. Sakamoto, K., Ohki, K., Saito, M., Nakahara, T., and Ishii, K. (2011) Small molecule cyclin-dependent kinase inhibitors protect against neuronal cell death in the ischemic-reperfused rat retina. J. Ocul. Pharmacol. Ther. 27, 419-425
40. Cheung, Z. H., Gong, K., and Ip, N. Y. (2008) Cyclin-dependent kinase 5 supports neuronal survival through phosphorylation of Bcl-2. J. Neurosci. 28, 4872-4877
41. Hahn, C. M., Kleinholz, H., Koester, M. P., Grieser, S., Thelen, K., and Pollerberg, G. E. (2005) Role of cyclin-dependent kinase 5 and its activator P35 in local axon and growth cone stabilization. Neuroscience 134, 449-465
42. Illanes, O., Anderson, S., Niesman, M., Zwick, L., and Jessen, B. A. (2006) Retinal and peripheral nerve toxicity induced by the administration of a pan-cyclin dependent kinase (cdk) inhibitor in mice. Toxicol. Pathol. 34, 243-248
43. Lesuisse, C., and Martin, L. J. (2002) Immature and mature cortical neurons engage different apoptotic mechanisms involving caspase-3 and the mitogen-activated protein kinase pathway. J. Cereb. Blood Flow Metab. 22, 935-950
44. Chen, J., Rusnak, M., Lombroso, P. J., and Sidhu, A. (2009) Dopamine promotes striatal neuronal apoptotic death via ERK signaling cascades. Eur. J. Neurosci. 29, 287-306
45. Yang, K., Cao, F., Sheikh, A. M., Malik, M., Wen, G., Wei, H., Ted Brown, W., and Li, X. (2013) Up-regulation of Ras/Raf/ERK1/2 signaling impairs cultured neuronal cell migration, neurogenesis, synapse formation, and dendritic spine development. Brain Struct. Funct. 218, 669-682
46. Rössler, O. G., Giehl, K. M., and Thiel, G. (2004) Neuroprotection of immortalized hippocampal neurones by brain-derived neurotrophic factor and Raf-1 protein kinase: role of extracellular signal-regulated protein kinase and phosphatidylinositol 3-kinase. J. Neurochem. 88, 1240-1252
47. Magariños, M., Aburto, M. R., SAnchez-Calderón, H., Muñoz-Agudo, C., Rapp, U. R., and Varela-Nieto, I. (2010) RAF kinase activity regulates neuroepithelial cell proliferation and neuronal progenitor cell differentiation during early inner ear development. PLoS One 5, e14435