Cyclin-dependent kinase 5 is required for normal cerebellar development

Molecular and Cellular Neuroscience

Volumn 52, Issue , 2013, Pages 97-105

  Kumazawa, A ^a   Mita, N ^a   Hirasawa, M ^b   Adachi, T ^c   Suzuki, H ^c   Shafeghat, N ^a   Kulkarni, A B ^b   Mikoshiba, K ^c   Inoue, T ^a   Ohshima, T ^a,b  

^a WASEDA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Cdk5; Conditional KO; Dendrite; Midbrain hindbrain; Neuronal migration

Indexed keywords

CYCLIN DEPENDENT KINASE 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL MIGRATION; CEREBELLUM; CONTROLLED STUDY; GRANULE CELL; HISTOLOGY; KNOCKOUT MOUSE; LETHALITY; MESENCEPHALON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RHOMBENCEPHALON;

ANIMALS; BLOTTING, WESTERN; CELL MOVEMENT; CEREBELLUM; CYCLIN-DEPENDENT KINASE 5; DENDRITES; IN SITU HYBRIDIZATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGENESIS;

MUS;

EID: 84870350420     PISSN: 10447431     EISSN: 10959327     Source Type: Journal    
DOI: 10.1016/j.mcn.2012.10.007     Document Type: Article

References (41)

1. Baquet Z.C., Bickford P.C., Jones K.R. Brain-derived neurotrophic factors is required for the establishment of the proper number of dopaminergic neurons in the substantia nigra pars compacta. J. Neurosci. 2005, 29:6251-6259.
2. Causeret F., Terao M., Jacobs T., Nishimura Y.V., Yanagawa Y., Obata K., Hoshino M., Nikolic M. The p21-activated kinase is required for neuronal migration in the cerebral cortex. Cereb. Cortex 2009, 19:861-875.
3. Chae T., Kwon Y.T., Bronson R., Dikkes P., Li E., Tsai L.H. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures and adult lethality. Neuron 1997, 18:29-42.
4. Chai Y., Jiang X., Ito Y., Bringas P., Han J., Rowitch D.H., Soriano P., McMahon A.P., Sucov H.M. Fate of the mammalian cranial neural Crest during tooth and mandibular morphogenesis. Development 2000, 127:1671-1679.
5. Cheung Z.H., Chin W.H., Chen Y., Ng Y.P., Ip N.Y. Cdk5 is involved in BDNF-stimulated dendritic growth in hippocampal neurons. PLoS Biol 2007, 5. (e).
6. Cicero S., Heruup K. Cyclin-dependent kinase 5 is essential for neuronal cell cycle arrest and differentiation. J. Neurosci. 2005, 25:9659-9668.
7. Dahmane N., Ruiz-i-Altaba A. Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 1999, 126:3089-3100.
8. Danielian P.S., Muccino D., Rowich D.H., Michael S.K., McMahon A.P. Modification of gene activity in mouse embryos in utero by a tamoxifen-inducible form of Cre recombinase. Curr. Biol. 1998, 8:1323-1326.
9. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995, 374:719-723.
10. Des Portes V., Pinard J.M., Billuart P., Vinet M.C., Koulakoff A., Carrie A., Gelot A., Dupuis E., Motte J., Berwald-Netter Y., Catala M., Kahn A., Beldjord C., Chelly J. A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 1998, 92:51-61.
11. Dhavan R., Tsai L.H. A decade of Cdk5. Nat. Rev. Mol. Cell Biol. 2001, 2:749-759.
12. Furuya S., Makino A., Hirabayashi Y. An improved method for culturing cerebellar Purkinje cells with differentiated dendrites under a mixed monolayer setting. Brain Res. Brain Res. Protoc. 1998, 3:192-198.
13. Gan W.B., Grutzendler J., Wong R.O., Lichtman J.W. Ballistic delivery of dyes for structural and functional studies of the nervous system. Cold Spring Harb. Protoc. 2009, (pdb.prot5202).
14. Gilmore E.C., Ohshima T., Goffinet A.M., Kulkarni A.B., Herrup K. Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in the cerebral cortex. J. Neurosci. 1998, 18:6370-6377.
15. Gleeson J.G., Allen K.M., Fox J.W., Lamperti E.D., Berkovic S., Scheffer I., Cooper E.C., Dobyns W.B., Minnerath S.R., Ross M.E., Walsh C.A. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 1998, 92:63-72.
16. Hirasawa M., Ohshima T., Takahashi S., Longenecker G., Honjo Y., Veeranna, Pant H.C., Mikoshiba K., Brady R.O., Kulkarni A.B. Perinatal abrogation of Cdk5 expression in brain results in neuronal migration defects. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6249-6254.
17. Hisatsune C., Kuroda Y., Akagi T., Torashima T., Hirai H., Hashikawa T., Inoue T., Mikoshiba K. Inositol 1,4,5-trisphosphate receptor type 1 in granule cells, not in Purkinje cells, regulates the dendritic morphology of Purkinje cells through brain-derived neurotrophic factor production. J. Neurosci. 2006, 26:10916-10924.
18. Ip J.P., Shi L., Chen Y., Itoh Y., Fu W.Y., Betz A., Yung W.H., Gotoh Y., Fu A.K., Ip N.Y. α2-Chimaerin controls neuronal migration and functioning of the cerebral cortex through CRMP-2. Nat. Neurosci. 2011, 15:39-47.
19. Iwasato T., Nomura R., Ando R., Ikeda T., Tanaka M., Itohara S. Dorsal telencephalon-specific expression of Cre recombinase in PAC transgenic mice. Genesis 2004, 38:130-138.
20. Karagogeos D., Morton S.B., Casano F., Dodd J., Jessell T.M. Developmental expression of the axonal glycoprotein TAG-1: differential regulation by central and peripheral neurons in vitro. Development 1991, 112:51-67.
21. Ko J., Humbert S., Brorson T., Takahashi S., Kulkarni A.B., Li E., Tsai L.H. p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. J. Neurosci. 2001, 21:6758-6771.
22. Lewis P.M., Gritil-Linde A., Smeyne R., Kottmann A., McMahon A.P. Sonic hedgehog signaling required for expansion of granule neuron precursors and patterning of the mouse cerebellum. Dev. Biol. 2004, 270:393-410.
23. Maeda N., Niinobe M., Mikoshiba K. A cerebellar the Purkinje cell marker P400 protein is an inositol 1,2,5-triphosphate (InsP3) receptor protein. Purification and characterization of InsP3 receptor complex. EMBO J. 1990, 9:61-67.
24. Nikolic M., Dudek H., Kwon Y.T., Ramos Y.F., Tsai L.H. The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genet Dev. 1996, 10:816-825.
25. Nikolic M., Chou M.M., Lu W., Mayer B.J., Tsai L.H. The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 1998, 395:194-198.
26. Ohshima T., Mikoshiba K. Reelin signaling and Cdk5 in the control of neuronal positioning. Mol. Neurobiol. 2002, 26:153-166.
27. Ohshima T., Ward J.M., Huh C.G., Longnecker G., Veeranna, Pant H.C., Brady R.O., Martin L.J., Kulkarni A.B. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:11173-11178.
28. Ohshima T., Gilmore E.C., Longenecker G., Jacobowitz D.M., Brady R.O., Herrup K., Kulkarni A.B. Migration defects of cdk5(-/-) neurons in the developing cerebellum is cell autonomous. J. Neurosci. 1999, 19:6017-6026.
29. Ohshima T., Ogawa M., Veeranna, Hirasawa M., Longenecker G., Ishiguro K., Pant H.C., Brady R.O., Kulkarni A.B., Mikoshiba K. Synergistic contribution of Cdk5/p35 and Reelin/Dab1 to the positioning of cortical neurons in the developing mouse brain. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:2764-2769.
30. Ohshima T., Ogawa M., Takeuchi K., Takahashi S., Kulkarni A.B., Mikoshiba K. Cdk5/p35 contributes synergistically with Reelin/Dab1 to the positioning of facial branchiomotor and inferior olive neurons in the developing mouse hindbrain. J. Neurosci. 2002, 22:4036-4044.
31. -/- mice. J. Neurochem. 2005, 94:917-925.
32. Ohshima T., Hirasawa M., Tabata H., Mutoh T., Adachi T., Suzuki H., Saruta K., Iwasato T., Itohara S., Hashimoto M., Nakajima K., Ogawa M., Kulkarni A.B., Mikoshiba K. Cdk5 is required for multipolar-to-bipolar transition during radial neuronal migration and proper dendrite development of pyramidal neurons in the cerebral cortex. Development 2007, 134:2273-2282.
33. Rashid T., Banerjee M., Nikolic M. Phosphorylation of Pak1 by the p35/Cdk5 kinase affects neuronal morphology. J. Biol. Chem. 2001, 276:49043-49052.
34. Rico B., Xu B., Reichardt L.F. TrkB receptor signaling is required for establishment of GABAergic synapses in the cerebellum. Nat. Neurosci. 2002, 5:225-233.
35. Sakai K., Miyazaki J. A transgenic mouse line that retains Cre recombinase activity in mature oocytes irrespective of the Cre transgenic transmission. Biochem. Biophys. Res. Commun. 1997, 237:318-324.
36. Tanaka T., Serneo F.F., Tseng H.C., Kulkarni A.B., Tsai L.H., Gleeson J.G. Cdk5 phosphorylation of doublecortin ser 297 regulates its effect on neuronal migration. Neuron 2004, 41:215-227.
37. Tissir F., Goffinet A.M. Reelin and brain development. Nat. Rev. Neurosci. 2003, 4:496-505.
38. Uchida Y., Ohshima T., Sasaki Y., Suzuki H., Yanai S., Yamashita N., Nakamura F., Takei K., Ihara Y., Mikoshiba K., Kolattukudy P., Honnorat J., Goshima Y. Semaphorin-3A signaling is mediated via sequential Cdk5-GSK3β phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer's disease. Genes Cells 2005, 10:165-179.
39. Wechsler-Reya R.J., Scott M.P. Control of neuronal precursor proliferation in the cerebellum by Sonic hedgehog. Neuron 1999, 22:103-114.
40. Weyer A., Schilling K. Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. J. Neurosci. Res. 2003, 73:400-409.
41. Xie Z., Sanada K., Samuels B.A., Shih H., Tsai L.H. Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 2003, 114:469-482.