Cdk5 is required for multipolar-to-bipolar transition during neuronal migration and proper dendrite development of pyramidal neurons in the cerebral cortex

Development

Volumn 134, Issue 12, 2007, Pages 2273-2282

  Ohshima, Toshio ^a   Hirasawa, Motoyuki ^b   Tabata, Hidenori ^c   Mutoh, Tetsuji ^a   Adachi, Tomoko ^a   Suzuki, Hiromi ^a   Saruta, Keiko ^a   Iwasato, Takuji ^a   Itohara, Shigeyoshi ^a   Hashimoto, Mistuhiro ^a   Nakajima, Kazunori ^c,d   Ogawa, Masaharu ^a   Kulkarni, Ashok B ^b   Mikoshiba, Katsuhiko ^a,e  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

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

^c KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cdk5; Cerebral cortex; Map2 (Mtap2); Mouse; Neuronal migration

Indexed keywords

CYCLIN DEPENDENT KINASE 5; GREEN FLUORESCENT PROTEIN; NERVE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX LESION; BRAIN NERVE CELL; CELL MIGRATION; CELL POLARITY; CELL SHAPE; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; ELECTROPORATION; EMBRYO; GLIA CELL; KNOCKOUT MOUSE; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SUBVENTRICULAR ZONE; WILD TYPE;

ANIMALS; CELL MOVEMENT; CELLS, CULTURED; CEREBRAL CORTEX; CYCLIN-DEPENDENT KINASE 5; DENDRITES; ELECTROPORATION; IN SITU HYBRIDIZATION; MICE; MICE, INBRED ICR; MICE, KNOCKOUT; MICE, NEUROLOGIC MUTANTS; NEURONS; PYRAMIDAL CELLS;

MAMMALIA; MUS;

EID: 34347355521     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02854     Document Type: Article

References (47)

1. Argevine, J., Jr and Sidman, R. L. (1961). Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192, 766-768.
2. Arber, S., Ladle, D. R., Lin, J. H., Frank, E. and Jessell, T. M. (2000). ETS gene Er81 controls the formation of functional connections between group Ia sensory afferents and motor neurons. Cell 101, 485-498.
3. Bai, J., Raddy, L., Ackman, J. B., Thomas, A. M., Lee, R. V. and LoTurco, J. J. (2003). RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat. Neurosci. 12, 1277-1283.
4. Bellion, A., Baudoin, J. R, Alvarez, C., Bornens, M. and Metin, C. (2005). Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J. Neurosci. 25, 5691-5699.
5. kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 18, 862-876,
6. Cappello, S., Attardo, A., Wu, X., Iwasato, T., Itohara, S., Wilsch-Brauninger, M., Eilken, H. M., Rieger, M. A., Schroeder, T. T., Huttner, W. B. et al. (2006). The Rho-GTPase cdc42 regulates neuronal progenitor fate at the apical face. Nat. Neurosci 9, 1099-1107.
7. Chae, T, Kwon, Y. T., Bronson, R., Dikkes, R, Li, E. and Tsai, L, H. (1997). Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 18, 29-42.
8. Cicero, S. and Herrup, K. (2005). Cyclin-dependent kinase 5 is essential for neuronal cell cycle arrest and differentiation, J. Neurosci 25, 9659-9668.
9. Dhaavan, R. and Tsai, L. H. (2001). A decade of Cdk5. Nat. Rev. Mol. Cell Biol. 2, 749-759.
10. Feng, G., Mellor, R. H., Bernstein, M., Keller-Peck, C., Nguyen, Q. T., Wallace, M., Nerbonne, J. M., Lichtman, J. W. and Sanes, J. R. (2000). Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51.
11. Ferland, R. J., Cherry, T. J., Preware, P. O., Morrisey, E. E. and Walsh, C. A. (2003). Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J. Comp. Neurol. 469, 266-279.
12. Ge, W., He, F., Kim, K. J., Blanchi, B., Coskun, V., Nguyen, L., Wu, X., Zhao, J., Heng, J. I., Martinowich, K. et al. (2006). Coupling of cell migration with neurogenesis by proneural bHLH factors. Proc. Natl. Acad. Sci. USA 103, 1319-1324.
13. Gilmore, E. C., Ohshima, T. Goffinet, A. M., Kulkarni, A. B. and Herrup, K. (1998). Cyclin-dependent kinase 5-deficent mice demonstrate novel developmental arrest in cerebral cortex. J. Neurosci. 18, 6370-6377.
14. Guipta, A., Sanada, K., Miyamoto, D. T., Rovelstad, S., Nadarajah, B., Pearlman, A. L., Brunstrom, J. and Tsai, L. H. (2003). Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat. Neurosci. 6, 1284-1291.
15. Hand, R., Bortone, D., Mattar, P., Nguyen, L., Heng, J. L, Guerrier, S., Boutt, E., ieters, E., Barnes, A. P., Parras, C. et al. (2005). Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48, 45-62.
16. Hashimoto, M. and Mikoshiba, K. (2004). Neuronal birthdate-specific gene transfer with adenoviral vectors. J. Neurosci. 24, 286-296.
17. Hatanaka, Y. and Murakami, F. (2002). In vitro analysis of the origin, migratory behavior, and maturation of cortical pyramidal cells. J. Comp. Neurol. 454, 1-14.
18. Hatanaka, Y., Hisanaga, S.-L, Heizman, C. W. and Murakami, F. (2004). Distinct migratory behavior of early- and late-born neurons derived from the cortical ~entricular zone. J. Comp. Neurol. 479, 1-14.
19. Hayashi, K., Ohshima, T. and Mikoshiba, K. (2002). Pak 1 is involved in dendrite initiation as a downstream effector of Rac1 in cortical neurons. Mol. Cell. Neurosci. 20, 579-594.
20. Hirasawa M., Ohshimi T. Takahashi, S., Longenecker, G., Honjo, Y., Veeranna, Pant H. C., Mikoshiba, K., Brady, R. O. and Kulkarni, A. B. (2004). Perinatal abrogation of Cdk5 expression in brain results in neuronal migration defects. Proc. Natl. Acad. Sci. USA 101, 6249-6254.
21. Iwasato, T., Datwani, A., Wolf, A. M., Nishimura, H., Taguchi, Y., Tonegawa S., Knopfel, T., Erurumlu, R. S. and Itohara, S. (2000). Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406, 726-731.
22. Kawauchi, T, Chilhama, K., Nabashima, Y. and Hoshino, M. (2003). The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration. EMBO J, 22, 4190-4201.
23. kip1 contributing to actin organization and cortical neuronal migration. Nat. Cell Biol. 8, 17-26.
24. Li, B. S., Zhang, L., Takahashi, S., Ma, W., Jaffe, H., Kulkarni, A. B. and Pant, H. C. (2002). Cyclin-dependent kinase 5 prevents neuronal apoptosis by negative regulation of c-Jun N-terminal kinase 3. EMBO J. 21, 324-333.
25. LoTurco, J. J. and Bai, J. (2006). The multipolar stage 4 nd disruptions in neuronal migration. Trends Neurosci 29, 407-413
26. Nedarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R. O. L. and Pearlman, A. L. (2001). Two modes of radial migration in early development of the cerebral cortex. Nat. Neurosci. 4, 143-150.
27. Nagai, T. Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K. and Miyawaki, A. (2002). A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol. 20, 87-90.
28. Nagano, T., Morikubo, S. and Sato, M. (2004). Filamin A and FILIP (Filamin A-Interacting Protein) regulate cell polarity and motility in neocortical subventricular and intermediate zones during radial migration. J. Neurosci. 24, 9648-9657.
29. Niethammer, M., Smith, D. S., Ayala, R., Peng, J., Ko, J., Lee, M.-S., Morabito, M. and Tsai, L H. (2000). NUDEL is a novel Cdk5 su$strate that associates with LIS1 and cytoplasmic dynein. Neuron 28, 697-711.
30. Nieto, M., Monuki, E. S., Tang, H., Imitola, J., Haubst N., Khoury, S. J., Cunningham, J., Gotz, M. and Walsh, C. A. (2004). Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex. J. Comp. Neurol. 479, 168-180.
31. Niwa, H., Yamamura, K. and Miyazaki, J. (1991). Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
32. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L. and Kriegstein, A. R. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144.
33. Ohshima, T., Ward, J. M., Huh, C. G., Longenecker, G., Veeranna, Pant, H. C., Brady, R. O., Martin, L. J. and Kulkarni, A. B. (1995). Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl. Acad. Sci. USA 93, 11173-11178.
34. Ohshima, T., Ogawa, M., Veeranna, Hirasai M., Longenecker, G., Ishiguro, K., Pant, H. C., Brady, R. O., Kulkarni, A. B. and Mikoshiba. K. (2001). Synergistic contribution of Cdk5/p35 and Reelin/Dab1 to the positioning of cortical neurons in the developing mouse brain. Proc. Natl. Acad. Sci. USA 98, 2764-2769.
35. Ohshima, T., Ogawa, M., Takeuchi, K., Takahashi, S., Kulkarni, A. B. and Mikoshiba, K. (2002). Cyclin-dependent kinase 5/p35 contributes synergistically with Reelin/Dab1 to the positioning of facial branchiomotor and inferior olive neurons in the Dev.eloping mouse hindbrain. J. Neurosci. 22, 4036-4044.
36. -/- mice. J. Neurochem. 94, 917-925.
37. Sasaki, S., Shionoya, A., Ishida, M., Gambello, M. J. Yingling, J., Wynshaw-Boris, A. and Hirotsune, S. (2000). A LIS1/NUDEL cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28, 681-696.
38. Schaar, B. T. and McConnell, S. K. (2005). Cytoskeletal coordination during neuronal migration. Proc Natl. Acad. Sci. USA 102, 13652-13657.
39. Tabata, H. and Nakajima, K. (2001). Efficient in utero ene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103, 865-872
40. Tabata, H. and Nakajima, K. (2003). Multipolar mignition: the third mode of radial neuronal migration in the developing cerebral cortex. J. Neurosci. 23, 9996-10001.
41. Tanaka, T., Semeo, F. F, Higgins, C., Gambello, M. J.; Wynshaw-Boris, A. and Gleeson., (2004a). Lisl and cloublecortin functi with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J. Cell Biol. 165, 709-721.
42. Tanaka, T., Serneo, F. F, Tseng, H. C., Kulkarni, A. B., Tsai, L. H. and Gleeson, J. G. (2004b). Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 41, 215-227.
43. Terashima, T., Inoue, K., Inoue, Y., Mikoshiba, K. and Tsukada, Y. (1983). Distribution and morphology of corticospinal tract neorons in reeler mouse cortex by the retrograde HRP method. J. Comp. Neurol. 218, 314-326.
44. The FANTOM Consortium (2005). The transcriptonal landscape of the mammalian genome. Science 309, 1559-1563,
45. Threadgill, R., Bobb, K. and Ghosh, A. (1997). Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 19, 625-634.
46. Tsai, J., Chen, Y., Kriegstein, A. R. and Vallee, R. B. (2005). LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J. Cell Biol. 170, 935-945.
47. Xie, Z., Sanada, K., Samuels, B. A., Shih, H. and Tsai L. H. (2003). Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 114, 469-482.