Skip to main content

Reelin and Cyclin-Dependent Kinase 5

  • Chapter
Reelin Glycoprotein
  • 663 Accesses

Reelin, an extracellular signaling molecule, and cyclin-dependent kinase 5 (Cdk5), a cytoplasmic kinase, are key regulators of normal brain development, including establishment of the complex brain structure. Recent studies have indicated that both Reelin signaling and Cdk5 are also involved in synaptic plasticity and neurodegeneration. In this chapter, I shall describe the functions of Cdk5 in neuronal migration during brain development and present an overview of the relationship of Cdk5 with Reelin signaling based on analyses of mutant mouse models. I shall also refer to the functions of Reelin signaling and Cdk5 in dendrite development, synaptic plasticity, and neurodegeneration.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Arnaud, L., Ballif, B. A., and Cooper, J. A. (2003). Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol. Cell. Biol. 23:9293-9302.

    Article  PubMed  Google Scholar 

  • Assadi, A. H., Zhang, G., Beffert, U., McNeil, R. S., Renfro, A. L., Niu, S., Quattrocchi, C. C., Antalffy, B. A., Sheldon, M., Armstrong, D. D., Wynshaw-Boris, A., Herz, J., D’Arcangelo, G.., and Clark G.. D. (2003). Interaction of reelin signaling and Lis1 in brain development. Nature Genet. 35:270-276.

    Article  PubMed  Google Scholar 

  • Baumann, K., Mandelkow, E. M., Biernat, J., Piwnica-Worms, H., and Mandelkow, E. (1993). Abnormal Alzheimer-like phosphorylation of Tau-protein by cyclin-dependent kinases Cdk2 and Cdk5. FEBS Lett. 336:417-424.

    Article  PubMed  Google Scholar 

  • Beffert, U., Morfini, G., Bock H. H., Reyna, H., Brady, S. T., and Herz, J. (2002). Reelin-mediated signaling locally regulates protein kinase B/Akt and glycogen synthase kinase 3. J. Biol. Chem. 277:49958-49964.

    Article  PubMed  Google Scholar 

  • Beffert, U., Weeber E. J., Morfini, G., Ko, J., Brady, S. T., Tsai, L.H., Sweatt, D., and Herz J. (2004). Reelin and cyclin-dependent kinase 5-dependent signals cooperate in regulating neu-ronal migration and synaptic transmission. J. Neurosci. 24:1897-1906.

    Article  PubMed  Google Scholar 

  • Bibb, J. A., Snyder, G. L., Nishi, A., Zhen, Y., Meijer, L., Fienberg, A. A., Tsai, L. H., Kwon, Y. T., Girault, J. A., Czernik, A. J., Huganir, R. L., Hemmings, H. C., Jr., Nairn, A. C., and Greengard, P. (1999). Protein kinase and phosphatase control by distinct phosphorylation sites within a single regulatory protein. Nature 402:669-671.

    Article  PubMed  Google Scholar 

  • Borrell, V., Del Rio, J. A., Alcantara, S., Derer, M., Martinez, A., D’Arcangelo, G., Nakajima, K., Mikoshiba, K., Derer, P., Curran, T., and Soriano, E. (1999). Reelin regulates the development and synaptogenesis of the layer-specific entorhino-hippocampal connections. J. Neurosci. 19:1345-1358.

    PubMed  Google Scholar 

  • Brich, J., Shie, F. S., Howell, B. W., Li, R., Tus, K., Wakeland, E. K., Jin, L. W., Mumby, M., Churchill, G., Herz, J., and Cooper, J. A. (2003). Genetic modulation of phosphorylation in the mouse. J. Neurosci. 23:187-192.

    PubMed  Google Scholar 

  • Caviness, V. S. (1982). Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H] thymidine autoradiography. Brain Res. 256:293-302.

    PubMed  Google Scholar 

  • Chae, T., Kwon, Y. T., Bronson, R., Dikkes, P., 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.

    Article  PubMed  Google Scholar 

  • Delalle, I., Bhide, P. G., Caviness, V. S. J., and Tsai, L. H. (1997). Temporal and spatial patterns of expression of p35, a regulatory subunit of cyclin-dependent kinase 5, in the nervous system of the mouse. J. Neurocytol. 26:283-296.

    Article  PubMed  Google Scholar 

  • Del Rio, J. A., Heimrich, B., Borrell, V., Forster, E., Drakew, A., Alcantara, S., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., Derer, P., Frotscher, M., and Soriano, E. (1997). A role for Cajal-Retzius cells and reelin in the development of hippocampal connections. Nature 385:70-74.

    Article  PubMed  Google Scholar 

  • 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., and Chelly, J. (1998). A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92:51-61.

    Article  PubMed  Google Scholar 

  • Drakew, A., Deller, T., Heimrich, B., Gebhardt, C., Del Turco, D., Tielsch, A., Forster, E., Herz, J., and Frotscher, M. (2002). Dentate granule cells in reeler mutants and VLDLR and ApoER2 knockout mice. Exp. Neurol. 176:12-24.

    Article  PubMed  Google Scholar 

  • Fox, J. W., Lamperti, E. D., Eksioglu, Y. Z., Hong, S. E., Feng, Y., Graham, D. A., Scheffer, I.E., Dobyns, W. B., Hirsch, B. A., Radtke, R. A., Berkovic, S. F., Huttenlocher, P. R., and Walsh, C. A. (1998). Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron 21:1315-1325.

    Article  PubMed  Google Scholar 

  • Gilmore, E. C., Ohshima, T., Goffinet, A. M., Kulkarni, A. B., and Herrup, K. (1998). Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in cerebral cortex. J. Neurosci. 18:6370-6377.

    PubMed  Google Scholar 

  • 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., and Walsh, C. A. (1998). Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92:63-72.

    Article  PubMed  Google Scholar 

  • Goffinet, A. M. (1984). Events governing organization of postmigratory neurons: studies on brain development in normal and reeler mice. Brain Res. Rev. 7:261-296.

    Google Scholar 

  • Hellmich, M. R., Pant, H. C., Wada, E., and Battey, J. F. (1992). Neuronal cdc2-like kinase: a CDC2-related protein kinase with predominantly neuronal expression. Proc. Natl. Acad. Sci. USA 89:10867-10871.

    Article  PubMed  Google Scholar 

  • Hiesberger, T., Trommsdorff, M., Howell, B. W., Goffinet, A., Mumby, M. C., Cooper, J. A., and Herz, J. (1999). Direct binding of reelin to VLDL receptor and ApoE receptor 2 induces tyro-sine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24:481-489.

    Article  PubMed  Google Scholar 

  • Hoe, H. S., Tran, T. S., Matsuoka, Y., Howell, B. W., and Rebeck, G. W. (2006). Dab1 and reelin effects on APP and ApoEr2 trafficking and processing. J. Biol. Chem. 281:35176-35185.

    Article  PubMed  Google Scholar 

  • Homayouni, R., Rice, D. S., Sheldon, M., and Curran, T. (1999). Disabled-1 binds to the cytoplas-mic domain of amyloid precursor-like protein 1. J. Neurosci. 19:7507-7515.

    PubMed  Google Scholar 

  • Howell, B. W., Herrick, T. M., and Cooper, J. A. (1999). Reelin-induced tyrosine phosphorylation of disabled 1 during neuronal positioning. Genes Dev. 13:643-648.

    Article  PubMed  Google Scholar 

  • Iijima, K., Ando, K., Takeda, S., Satoh, Y., Seki, T., Itohara, S., Greengard, P., Kirino, Y., Nairn, A. C., and Suzuki, T. (2000). Neuron-specific phosphorylation of Alzheimer’s -amyloid pre-cursor protein by cyclin-dependent kinase 5. J. Neurochem. 75:1085-1091.

    Article  PubMed  Google Scholar 

  • Keshvara, L., Magdaleno, S., Benhayon, D., and Curran, T. (2002). Cyclin-dependent kinase 5 phosphorylates disabled 1 independently of reelin signaling. J. Neurosci. 22:4869-4877.

    PubMed  Google Scholar 

  • Ko, J., Humbert, S., Brorson, T., Takahashi, S., Kulkarni, A. B., Li, E., and Tsai, L. H. (2001). p35 and p39 are essential for Cdk5 function during neurodevelopment. J. Neurosci. 21:6758-6771.

    PubMed  Google Scholar 

  • Kobayashi, S., Ishiguro, K., Omori, A., Takamatsu, M., Arioka, M., Imahori, K., and Uchida, T. (1993). Cdc2-related kinase PSSALRE/Cdk5 is homologous with the 30 kDa subunit of tau protein kinase II, a proline-directed protein kinase associated with microtubule. FEBS Lett. 335:171-175.

    Article  PubMed  Google Scholar 

  • Kwon, Y. T., Gupta, A., Zhou, Y., Nikolic, M., and Tsai, L. H. (2000). Regulation of the N-cad-herin-mediated adhesion by the p35/Cdk5 kinase. Curr. Biol. 10:363-372.

    Article  PubMed  Google Scholar 

  • Lee, M. S., Kao, S. C., Lemere, C. A., Xia, W., Tseng, H. C., Zhou, Y., Neve, R., Ahlijanian, M. K., and Tsai, L. H. (2003). APP processing is regulated by cytoplasmic phosphorylation. J. Cell. Biol. 163:83-95.

    Article  PubMed  Google Scholar 

  • Lew, J., Huang, Q. Q., Qi, Z., Winkfein, R. J., Aebersold, R., Hunt, T., and Wang J. H. (1994). Neuronal cdc2-like kinase is a complex of cyclin-dependent kinase 5 and a novel brain-specific regulatory subunit. Nature 371:423-425.

    Article  PubMed  Google Scholar 

  • Li, B. S., Sun, M. K., Zhang, L., Takahashi, S., Ma, W., Vinade, L., Kulkarni, A. B., Brady, R.O., and Pant, H. C. (2001). Regulation of NMDA receptors by cyclin-dependent kinase-5.Proc. Natl. Acad. Sci. USA 98:12742-12747.

    Article  Google Scholar 

  • Mariani, J., Crepel, F., Mikoshiba, K., Changeux, J. P., and Sotelo, C. (1977). Anatomical, physi-ological and biochemical studies of the cerebellum from Reeler mutant mouse. Philos. Trans. R. Soc. London Ser. B Biol. Sci. 281:1-28.

    Article  Google Scholar 

  • Matsubara, M., Kusubata, M., Ishiguro, K., Uchida, T., Titani, K., and Taniguchi, H. (1996). Site-specific phosphorylation of synapsin I by mitogen-activated protein kinase and Cdk5 and its effects on physiological functions. J. Biol. Chem. 271:21108-21113.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Morabito, M. A., Sheng, M., and Tsai, L. H. (2004). Cyclin-dependent kinase 5 phosphorylates the N-terminal domain of the postsynaptic density protein PSD-95 in neurons. J. Neurosci. 24:865-876.

    Article  PubMed  Google Scholar 

  • Morfini, G., Szebenyim, G., Brown, H., Pant, H. C., Pigino, G., DeBoer, S., Beffert, U., and Brady, S. T. (2004). A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons. EMBO J. 23:2235-2245.

    Article  PubMed  Google Scholar 

  • 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 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28:697-711.

    Article  PubMed  Google Scholar 

  • Nikolic, M., Dudek, H., Kwon, Y. T., Ramos, Y. F. M., and Tsai, L. H. (1996). The Cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev. 10:816-825.

    Article  PubMed  Google Scholar 

  • Nikolic, M., Chou, M. M., Lu, W., Mayer, B. J., and Tsai, L. H. (1998). The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 395:194-198.

    Article  PubMed  Google Scholar 

  • Niu, S., Renfro, A., Quattrocchi, C. C., Sheldon, M., and D’Arcangelo, G. (2004). Reelin pro-motes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41:71-84.

    Article  PubMed  Google Scholar 

  • Ohshima, T., and Mikoshiba, K. (2002). Reelin signaling and Cdk5 in the control of neuronal positioning. Mol. Neurobiol. 26:153-166.

    Article  PubMed  Google Scholar 

  • Ohshima, T., Ward, J. M., Huh, C. G., Longenecker, G., Veeranna, Pant, H. C., Brady, R. O., Martin, L. J., and Kulkarni, A. B. (1996). 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.

    Article  PubMed  Google Scholar 

  • Ohshima, T., Gilmore, E. C., Longenecker, G., Jacobowitz, D. M., Brady, R. O., Herrup, K., and Kulkarni, A. B. (1999). Migration defects of Cdk5(-/-) neurons in the developing cerebellum is cell autonomous. J. Neurosci. 19:6017-6026.

    PubMed  Google Scholar 

  • Ohshima, T., Ogawa, M., Veeranna, Hirasawa, M., Longenecker, G., Ishiguro, K., Pant, H. C., Brady, R. O., Kulkarni, A. B., and Mikoshiba, K. (2001). Synergistic contributions of cyclin-dependent kinase 5/p35 and reelin/Dab1 to the positioning of cortical neurons in the develop-ing mouse brain. Proc. Natl. Acad. Sci. USA 98:2764-2769.

    Article  PubMed  Google Scholar 

  • 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 developing mouse hindbrain. J. Neurosci. 22:4036-4044.

    PubMed  Google Scholar 

  • Ohshima, T., Ogura, H., Tomizawa, K., Hayashi, K., Suzuki, H., Saito, T., Kamei, H., Nishi, A., Bibb, J. A., Hisanaga, S., Matsui, H., and Mikoshiba, K. (2005). Impairment of hippocampal long-term depression and defective spatial learning and memory in p35-/- mice. J. Neurochem. 94:917-925.

    Article  PubMed  Google Scholar 

  • Ohshima, T., Suzuki, H., Morimura, T., Ogawa, M., and Mikoshiba, K. (2007). Modulation of reelin signaling by cyclin-dependent kinase 5. Brain Res. 1140:84-95.

    Article  PubMed  Google Scholar 

  • Olson, E C., Kim, S., and Walsh, C. A. (2006). Impaired neuronal positioning and dendritogenesis in the neocortex after cell-autonomous Dab1 suppression. J. Neurosci. 26:1767-1775.

    Article  PubMed  Google Scholar 

  • Paglini, G., Pigino, G., Kunda, P., Morfini, G., Maccioni, R., Quiroga, S., Ferreira, A., and Caceres, A. (1998). Evidence for the participation of the neuron-specific CDK5 activator P35 during laminin-enhanced axonal growth. J. Neurosci. 18:9858-9869.

    PubMed  Google Scholar 

  • Patrick, G. N., Zukerberg, L., Nikolic, M., de la Monte, S., Dikkes, P., and Tsai, L. H. (1999). Conversion of p35 to p25 de-regulates Cdk5 activity and promotes neurodegeneration. Nature 402:615-622.

    Article  PubMed  Google Scholar 

  • Paudel, H. K., Lew, J., Ali, Z., and Wang, J. H. (1993). Brain proline-directed protein kinase phosphorylates tau on sites that are abnormally phosphorylated in tau associated with Alzheimer’s paired helical filaments. J. Biol. Chem. 268:23512-23518.

    PubMed  Google Scholar 

  • Rashid, T., Banerjee, M., and Nikolic, M. (2001). Phosphorylation of Pak1 by the p35/Cdk5 kinase affects neuronal morphology. J. Biol. Chem. 276:49043-49052.

    Article  PubMed  Google Scholar 

  • Reiner, O., Carrozzo, R., Shen, Y., Wehnert, M., Faustinella, F., Dobyns, W. B., Caskey, C. T., and Ledbetter, D. H. (1993). Isolation of a Miller-Dieker lissencephaly gene containing G-protein-subunit-like repeats. Nature 364:717-721.

    Article  PubMed  Google Scholar 

  • 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 devel-oping and adult nervous system. Neuron 28:681-696.

    Article  PubMed  Google Scholar 

  • Sheppard, A. M., and Pearlman, A. L. (1997). Abnormal reorganization of preplate neurons and their associated extracellular matrix: an early manifestation of altered neocortical development in the reeler mutant mouse. J. Comp. Neurol. 378:173-179.

    Article  PubMed  Google Scholar 

  • Shuang, R., Zhang, L., Fletcher, A., Groblewski, G. E., Pevsner, J., and Stuenkel, E. L. (1998). Regulation of Munc18/syntaxin 1A interaction by cyclin-dependent kinase 5 in nerve endings. J. Biol. Chem. 273:4957-4966.

    Article  PubMed  Google Scholar 

  • Stanfield, B. B., and Cowan, W. M. (1979). The morphology of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 185:393-422.

    Article  PubMed  Google Scholar 

  • Takahashi, S., Saito, T., Hisanaga, S., Pant, H. C., and Kulkarni, A. B. (2003). Tau phosphoryla-tion by cyclin-dependent kinase 5/p39 during brain development reduces its affinity for micro-tubules. J. Biol. Chem. 278:10506-10515.

    Article  PubMed  Google Scholar 

  • Takashima, A., Murayama, M., Yasutake, K., Takahashi, H., Yokoyama, M., and Ishiguro, K. (2001). Involvement of cyclin dependent kinase 5 activator p25 on tau phosphorylation in mouse brain. Neurosci. Lett. 306:37-40.

    Article  PubMed  Google Scholar 

  • Tan, T. C., Valova, V. A., Malladi, C. S., Graham, M. E., Berven, L. A., Jupp, O. J., Hansra, G., McClure, S. J., Sarcevic, B., Boadle, R. A., Larsen, M. R., Cousin, M. A., and Robinson, P. J. (2003). Cdk5 is essential for synaptic vesicle endocytosis. Nature Cell Biol. 5:701-710.

    Article  PubMed  Google Scholar 

  • Tanaka, T., Serneo, F. F., Tseng, H. C., Kulkarni, A. B., Tsai, L. H., and Gleeson, J. G. (2004). Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 41:215-227.

    Article  PubMed  Google Scholar 

  • Tang, D., Yeung, J., Lee, K. Y., Matsushita, M., Matsui, H., Tomizawa, K., Hatase, O., and Wang, J. H. (1995). An isoform of the neuronal cyclin-dependent kinase 5 (cdk5) activator. J. Biol. Chem. 270:26897-26903.

    Article  PubMed  Google Scholar 

  • Tomizawa, K., Ohta, J., Matsushita, M., Moriwaki, A., Li, S. T., Takei, K., and Matsui, H. (2002). Cdk5/p35 regulates neurotransmitter release through phosphorylation and downregulation of P/Q-type voltage-dependent calcium channel activity. J. Neurosci. 22:2590-2597.

    PubMed  Google Scholar 

  • Tomizawa, K., Sunada, S., Lu, Y. F., Oda, Y., Kinuta, M., Ohshima, T., Saito, T., Wei, F. Y., Matsushita, M., Li, S. T., Tsutsui, K., Hisanaga, S., Mikoshiba, K., Takei, K., and Matsui, H. (2003). Cophosphorylation of amphiphysin I and dynamin I by Cdk5 regulates clathrin-medi-ated endocytosis of synaptic vesicles. J. Cell Biol. 163:813-824.

    Article  PubMed  Google Scholar 

  • Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R. E., Richardson, J. A., and Herz, J. (1999). Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97:689-701.

    Article  PubMed  Google Scholar 

  • Tsai, L. H., Takahashi, T., Caviness, V. S., Jr., and Harlow, E. (1993). Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development 119:1029-1040.

    PubMed  Google Scholar 

  • Tsai, L. H., Delalle, I., Caviness, V. S., Jr., Chae, T., and Harlow, E. (1994). p35 is a neural-spe-cific regulatory subunit of cyclin-dependent kinase 5. Nature 371:419-423.

    Article  PubMed  Google Scholar 

  • Uchida, Y., Ohshima, T., Sasaki, Y., Suzuki, H., Yanai, S., Yamashita, N., Nakamura, F., Takei, K., Ihara, Y., Mikoshiba, K., Kolattukudy, P., Honnorat, J., and Goshima, Y. (2005).Semaphorin3A signalling is mediated via sequential Cdk5 and GSK3β phosphorylation of CRMP2: implication of common phosphorylating mechanism underlying axon guidance and Alzheimer’s disease. Genes Cells 10:165-179.

    Article  PubMed  Google Scholar 

  • Weeber, E. J., Beffert, U., Jones, C., Christian, J. M., Forster, E., Sweatt, J. D., and Herz, J. (2002). Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J. Biol. Chem. 277:39944-39952.

    Article  PubMed  Google Scholar 

  • Wenzel, H. J., Robbins, C. A., Tsai, L. H., and Schwartzkroin, P. A. (2001). Abnormal morpho-logical and functional organization of the hippocampus in a p35 mutant model of cortical dys-plasia associated with spontaneous seizure. J. Neurosci. 21:983-998.

    PubMed  Google Scholar 

  • Wu, D. C., Yu, Y. P., Lee, N. T., Yu, A. C., Wang, J. H., and Han, Y. F. (2000). The expression of Cdk5, p35, p39, and Cdk5 kinase activity in developing, adult, and aged rat brains. Neurochem. Res. 25:923-929.

    Article  PubMed  Google Scholar 

  • Xiong, W., Pestell, R., and Rosner, M. R. (1997). Role of cyclins in neuronal differentiation of immortalized hippocampal cells. Mol. Cell. Biol. 17:6585-6597.

    PubMed  Google Scholar 

  • Yamashita, N., Uchida, Y., Ohshima, T., Hirai, S. I., Nakamura, F., Taniguchi, M., Mikoshiba, K., Honnorat, J., Kolattukudy, P., Thomasset, N., Takei, K., Takahashi, T., and Goshima, Y. (2006). CRMP1 mediates reelin signaling in cortical neuronal migration. J. Neurosci. 26:13357-13362.

    Article  PubMed  Google Scholar 

  • Yoo, B. C., and Lubec, G. (2001). p25 protein in neurodegeneration. Nature 30:135-147.

    Google Scholar 

  • Zheng, M., Leung, C. L., and Liem, R. K. (1998). Region-specific expression of cyclin-dependent kinase 5 (Cdk5) and its activators, p35 and p39, in the developing and adult rat central nervous system. J. Neurobiol. 35:141-159.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer

About this chapter

Cite this chapter

Ohshima, T. (2008). Reelin and Cyclin-Dependent Kinase 5. In: Fatemi, S.H. (eds) Reelin Glycoprotein. Springer, New York, NY. https://doi.org/10.1007/978-0-387-76761-1_9

Download citation

Publish with us

Policies and ethics