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Protein Kinases and Signaling Pathways that Are Activated by Reelin

  • Jonathan A. Cooper
  • Nathaniel S. Allen
  • Libing Feng

Defects in the cortex, hippocampus, inferior olive, and cerebellum of Reeler mutant mice were first detected many decades ago (Caviness and Rakic, 1978; Rice and Curran, 2001). Recently, a plethora of other developmental and adult phenotypes have been detected in mutant mice, including misplacement of olfactory interneurons (Hack et al., 2002), facial motor neurons (FMNs) (Ohshima et al., 2002; Rössel et al., 2005), sympathetic preganglionic neurons (SPNs) (Yip et al., 2000), and gonadotropin-releasing hormone (GnRH) neurons (Cariboni et al., 2005), reduced dendrite outgrowth in the hippocampus (Niu et al., 2004), and defective long-term potentiation (LTP) and memory (Weeber et al., 2002). In some genetic backgrounds, the Reeler mutation also causes neurodegeneration and early death, but these phenotypes are not detected in other backgrounds and are likely to be indirect (Brich et al., 2003; Goffinet, 1990).How Reelin, the Reeler gene product, creates these different phenotypes is still incompletely understood.

The purpose of this chapter is to briefly review the core components and signaling mechanism of the Reelin pathway, and then to present evidence on possible downstream components. Issues related to the first two questions, the timing and site of Reelin action and the possible changes in cell biology, are left for other chapters.

Keywords

Tyrosine Phosphorylation Lipid Raft Radial Glia Cortical Plate Fred Hutchinson Cancer Research 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Anton, E. S., Kreidberg, J. A., and Rakic, P. (1999). Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 22:277-289.PubMedCrossRefGoogle Scholar
  2. Arnaud, L., Ballif, B. A., and Cooper, J. A. (2003a). Regulation of protein tyrosine kinase signal-ing by substrate degradation during brain development. Mol. Cell. Biol. 23:9293-9302.PubMedCrossRefGoogle Scholar
  3. Arnaud, L., Ballif, B. A., Forster, E., and Cooper, J. A. (2003b). Fyn tyrosine kinase is a critical regulator of disabled-1 during brain development. Curr. Biol. 13:9-17.PubMedCrossRefGoogle Scholar
  4. 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.PubMedCrossRefGoogle Scholar
  5. Ballif, B. A., Arnaud, L., and Cooper, J. A. (2003). Tyrosine phosphorylation of disabled-1 is essential for reelin-stimulated activation of Akt and Src family kinases. Brain Res. Mol. Brain Res. 117:152-159.PubMedCrossRefGoogle Scholar
  6. Ballif, B. A., Arnaud, L., Arthur, W. T., Guris, D., Imamoto, A., and Cooper, J. A. (2004). Activation of a Dab1/CrkL/C3G/Rap1 pathway in reelin-stimulated neurons. Curr. Biol. 14:606-610.PubMedCrossRefGoogle Scholar
  7. Beffert, U., Morfini, G., Bock, H. H., Reyna, H., Brady, S. T., and Herz, J. (2002). Reelin-medi-ated signaling locally regulates protein kinase B/Akt and glycogen synthase kinase 3beta. J. Biol. Chem. 277:49958-49964.PubMedCrossRefGoogle Scholar
  8. Beffert, U., Weeber, E. J., Morfini, G., Ko, J., Brady, S. T., Tsai, L. H., Sweatt, J. 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.PubMedCrossRefGoogle Scholar
  9. Beffert, U., Weeber, E. J., Durudas, A., Qiu, S., Masiulis, I., Sweatt, J. D., Li, W. P., Adelmann, G., Frotscher, M., Hammer, R. E., and Herz, J. (2005). Modulation of synaptic plasticity and memory by reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 47:567-579.PubMedCrossRefGoogle Scholar
  10. Beffert, U., Durudas, A., Weeber, E. J., Stolt, P. C., Giehl, K. M., Sweatt, J. D., Hammer, R. E., and Herz, J. (2006). Functional dissection of Reelin signaling by site-directed disruption of Disabled-1 adaptor binding to apolipoprotein E receptor 2: distinct roles in development and synaptic plasticity. J. Neurosci. 26:2041-2052.PubMedCrossRefGoogle Scholar
  11. Benhayon, D., Magdaleno, S., and Curran, T. (2003). Binding of purified reelin to ApoER2 and VLDLR mediates tyrosine phosphorylation of disabled-1. Brain Res. Mol. Brain Res. 112:33-45.PubMedCrossRefGoogle Scholar
  12. Bladt, F., Aippersbach, E., Gelkop, S., Strasser, G. A., Nash, P., Tafuri, A., Gertler, F. B., and Pawson, T. (2003). The murine Nck SH2/SH3 adaptors are important for the development of mesoderm-derived embryonic structures and for regulating the cellular actin network. Mol. Cell. Biol. 23:4586-4597.PubMedCrossRefGoogle Scholar
  13. Bock, H. H., and Herz, J. (2003). Reelin activates SRC family tyrosine kinases in neurons. Curr. Biol. 13:18-26.PubMedCrossRefGoogle Scholar
  14. Bock, H. H., Jossin, Y., Liu, P., Forster, E., May, P., Goffinet, A. M., and Herz, J. (2003). Phosphatidylinositol 3-kinase interacts with the adaptor protein Dab1 in response to reelin signaling and is required for normal cortical lamination. J. Biol. Chem. 278:38772-38779.PubMedCrossRefGoogle Scholar
  15. Bock, H. H., Jossin, Y., May, P., Bergner, O., and Herz, J. (2004). Apolipoprotein E receptors are required for reelin-induced proteasomal degradation of the neuronal adaptor protein disabled1. J. Biol. Chem. 279:33471-33479.PubMedCrossRefGoogle Scholar
  16. 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 tau phosphorylation in the mouse. J. Neurosci. 23:187-192.PubMedGoogle Scholar
  17. Calderwood, D. A., Fujioka, Y., de Pereda, J. M., Garcia-Alvarez, B., Nakamoto, T., Margolis, B., McGlade, C. J., Liddington, R. C., and Ginsberg, M. H. (2003). Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diver-sity in integrin signaling. Proc. Natl. Acad. Sci. USA 100:2272-2277.PubMedCrossRefGoogle Scholar
  18. Cariboni, A., Rakic, S., Liapi, A., Maggi, R., Goffinet, A., and Parnavelas, J. G. (2005). Reelin provides an inhibitory signal in the migration of gonadotropin-releasing hormone neurons. Development 132:4709-4718.PubMedCrossRefGoogle Scholar
  19. Caviness, V. S., Jr., and Rakic, P. (1978). Mechanisms of cortical development: a view from muta-tions in mice. Annu. Rev. Neurosci. 1:297-326.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. Chen, K., Ochalski, P. G., Tran, T. S., Sahir, N., Schubert, M., Pramatarova, A., and Howell, B.W. (2004). Interaction between Dab1 and CrkII is promoted by reelin signaling. J. Cell Sci. 117:4527-4536.PubMedCrossRefGoogle Scholar
  22. Chen, M., She, H., Kim, A., Woodley, D. T., and Li, W. (2000). Nckbeta adapter regulates actin polymerization in NIH 3T3 fibroblasts in response to platelet-derived growth factor bb. Mol. Cell. Biol. 20:7867-7880.PubMedCrossRefGoogle Scholar
  23. Chen, Y., Beffert, U., Ertunc, M., Tang, T. S., Kavalali, E. T., Bezprozvanny, I., and Herz, J. (2005). Reelin modulates NMDA receptor activity in cortical neurons. J. Neurosci. 25:8209-8216.PubMedCrossRefGoogle Scholar
  24. Cowan, C. A., and Henkemeyer, M. (2001). The SH2/SH3 adaptor Grb4 transduces B-ephrin reverse signals. Nature 413:174-179.PubMedCrossRefGoogle Scholar
  25. D’Arcangelo, G., Miao, G. G., Chen, S. C., Soares, H. D., Morgan, J. I., and Curran, T. (1995). A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature (London) 374:719-723.CrossRefGoogle Scholar
  26. D’Arcangelo, G., Homayouni, R., Keshvara, L., Rice, D. S., Sheldon, M., and Curran, T. (1999). Reelin is a ligand for lipoprotein receptors. Neuron 24:471-479.PubMedCrossRefGoogle Scholar
  27. de Jong, R., van Wijk, A., Heisterkamp, N., and Groffen, J. (1998). C3G is tyrosine-phosphor-ylated after integrin-mediated cell adhesion in normal but not in Bcr/Abl expressing cells. Oncogene 17:2805-2810.PubMedCrossRefGoogle Scholar
  28. DeLong, G. R., and Sidman, R. L. (1970). Alignment defect of reaggregating cells in cultures of developing brains of reeler mutant mice. Dev. Biol. 22:584-600.CrossRefGoogle Scholar
  29. Dulabon, L., Olson, E. C., Taglienti, M. G., Eisenhuth, S., McGrath, B., Walsh, C. A., Kreidberg, J. A., and Anton, E. S. (2000). Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron 27:33-44.PubMedCrossRefGoogle Scholar
  30. Eden, S., Rohatgi, R., Podtelejnikov, A. V., Mann, M., and Kirschner, M. W. (2002). Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 418:790-793.PubMedCrossRefGoogle Scholar
  31. Feller, S. M. (2001). Crk family adaptors—signalling complex formation and biological roles.Oncogene 20:6348-6371.PubMedCrossRefGoogle Scholar
  32. Feng, Y., and Walsh, C. A. (2001). Protein-protein interactions, cytoskeletal regulation and neuro-nal migration. Nature Rev. Neurosci. 2:408-416.Google Scholar
  33. Feng, Y., and Walsh, C. A. (2004). Mitotic spindle regulation by Nde1 controls cerebral cortical size. Neuron 44:279-293.PubMedCrossRefGoogle Scholar
  34. Forster, E., Tielsch, A., Saum, B., Weiss, K. H., Johanssen, C., Graus-Porta, D., Muller, U., and Frotscher, M. (2002). Reelin, disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc. Natl. Acad. Sci. USA 99:13178-13183.PubMedCrossRefGoogle Scholar
  35. Frese, S., Schubert, W. D., Findeis, A. C., Marquardt, T., Roske, Y. S., Stradal, T. E., and Heinz, D. W. (2006). The phosphotyrosine peptide binding specificity of Nck1 and Nck2 Src homology 2 domains. J. Biol. Chem. 281:18236-18245.PubMedCrossRefGoogle Scholar
  36. Garrity, P. A., Rao, Y., Salecker, I., McGlade, J., Pawson, T., and Zipursky, S. L. (1996). Drosophila photoreceptor axon guidance and targeting requires the dreadlocks SH2/SH3 adapter protein. Cell 85:639-650.PubMedCrossRefGoogle Scholar
  37. Goffinet, A. M. (1990). Cerebellar phenotype of two alleles of the ‘reeler’ mutation on similar backgrounds. Brain Res. 519:355-357.PubMedCrossRefGoogle Scholar
  38. Gotthardt, M., Trommsdorff, M., Nevitt, M. F., Shelton, J., Richardson, J. A., Stockinger, W., Nimpf, J., and Herz, J. (2000). Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J. Biol. Chem. 275:25616-25624.PubMedCrossRefGoogle Scholar
  39. Grant, S. G., O’Dell, T. J., Karl, K. A., Stein, P. L., Soriano, P., and Kandel, E. R. (1992). Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258:1903-1910.PubMedCrossRefGoogle Scholar
  40. Graus-Porta, D., Blaess, S., Senften, M., Littlewood-Evans, A., Damsky, C., Huang, Z., Orban, P., Klein, R., Schittny, J. C., and Muller, U. (2001). Beta1-class integrins regulate the develop-ment of laminae and folia in the cerebral and cerebellar cortex. Neuron 31:367-379.PubMedCrossRefGoogle Scholar
  41. Gupta, A., Tsai, L. H., and Wynshaw-Boris, A. (2002). Life is a journey: a genetic look at neocor-tical development. Nature Rev. Genet. 3:342-355.Google Scholar
  42. Guris, D. L., Fantes, J., Tara, D., Druker, B. J., and Imamoto, A. (2001). Mice lacking the homo-logue of the human 22q11.2 gene CRKL phenocopy neurocristopathies of DiGeorge syn-drome. Nature Genet. 27:293-298.PubMedCrossRefGoogle Scholar
  43. Hack, I., Bancila, M., Loulier, K., Carroll, P., and Cremer, H. (2002). Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nature Neurosci. 5:939-945.PubMedCrossRefGoogle Scholar
  44. Hammond, V., Howell, B., Godinho, L., and Tan, S. S. (2001). disabled-1 functions cell autonomously during radial migration and cortical layering of pyramidal neurons. J. Neurosci. 21:8798-8808.PubMedGoogle Scholar
  45. Hartfuss, E., Forster, E., Bock, H. H., Hack, M. A., Leprince, P., Luque, J. M., Herz, J., Frotscher, M., and Gotz, M. (2003). Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130:4597-4609.PubMedCrossRefGoogle Scholar
  46. Hasegawa, H., Kiyokawa, E., Tanaka, S., Nagashima, K., Gotoh, N., Shibuya, M., Kurata, T., and Matsuda, M. (1996). DOCK180, a major CRK-binding protein, alters cell morphology upon translocation to the cell membrane. Mol. Cell. Biol. 16:1770-1776.PubMedGoogle Scholar
  47. Hemmeryckx, B., Reichert, A., Watanabe, M., Kaartinen, V., de Jong, R., Pattengale, P. K., Groffen, J., and Heisterkamp, N. (2002). BCR/ABL P190 transgenic mice develop leukemia in the absence of Crkl. Oncogene 21:3225-3231.PubMedCrossRefGoogle Scholar
  48. Herrick, T. M., and Cooper, J. A. (2002). A hypomorphic allele of dab1 reveals regional differ-ences in reelin-Dab1 signaling during brain development. Development 129:787-796.PubMedGoogle Scholar
  49. 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 tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24:481-489.PubMedCrossRefGoogle Scholar
  50. 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.PubMedGoogle Scholar
  51. Homayouni, R., Magdaleno, S., Keshvara, L., Rice, D. S., and Curran, T. (2003). Interaction of disabled-1 and the GTPase activating protein Dab2IP in mouse brain. Brain Res. Mol. Brain Res. 115:121-129.PubMedCrossRefGoogle Scholar
  52. Howell, B. W., Gertler, F. B., and Cooper, J. A. (1997a). Mouse disabled (mDab1): a Src binding protein implicated in neuronal development. EMBO J. 16:121-132.PubMedCrossRefGoogle Scholar
  53. Howell, B. W., Hawkes, R., Soriano, P., and Cooper, J. A. (1997b). Neuronal position in the devel-oping brain is regulated by mouse disabled-1. Nature (London) 389:733-737.CrossRefGoogle Scholar
  54. Howell, B. W., Herrick, T. M., and Cooper, J. A. (1999a). Reelin-induced tyrosine phosphoryla-tion of disabled 1 during neuronal positioning. Genes Dev. 13:643-648.PubMedCrossRefGoogle Scholar
  55. Howell, B. W., Lanier, L. M., Frank, R., Gertler, F. B., and Cooper, J. A. (1999b). The disabled 1 phosphotyrosine-binding domain binds to the internalization signals of transmembrane glyco-proteins and to phospholipids. Mol. Cell. Biol. 19:5179-5188.PubMedGoogle Scholar
  56. Howell, B. W., Herrick, T. M., Hildebrand, J. D., Zhang, Y., and Cooper, J. A. (2000). Dab1 tyro-sine phosphorylation sites relay positional signals during mouse brain development. Curr. Biol. 10:877-885.PubMedCrossRefGoogle Scholar
  57. Huang, Y., Magdaleno, S., Hopkins, R., Slaughter, C., Curran, T., and Keshvara, L. (2004). Tyrosine phosphorylated disabled 1 recruits Crk family adapter proteins. Biochem. Biophys. Res. Commun. 318:204-212.PubMedCrossRefGoogle Scholar
  58. Huang, Y., Shah, V., Liu, T., and Keshvara, L. (2005). Signaling through disabled 1 requires phos-phoinositide binding. Biochem. Biophys. Res. Commun. 331:1460-1468.PubMedCrossRefGoogle Scholar
  59. Hunter-Schaedle, K. E. (1997). Radial glial cell development and transformation are disturbed in reeler forebrain. J. Neurobiol. 33:459-472.PubMedCrossRefGoogle Scholar
  60. Ichiba, T., Hashimoto, Y., Nakaya, M., Kuraishi, Y., Tanaka, S., Kurata, T., Mochizuki, N., and Matsuda, M. (1999). Activation of C3G guanine nucleotide exchange factor for Rap1 by phos-phorylation of tyrosine 504. J. Biol. Chem. 274:14376-14381.PubMedCrossRefGoogle Scholar
  61. Jones, N., Blasutig, I. M., Eremina, V., Ruston, J. M., Bladt, F., Li, H., Huang, H., Larose, L., Li, S. S., Takano, T., Quaggin, S. E., and Pawson, T. (2006). Nck adaptor proteins link nephrin to the actin cytoskeleton of kidney podocytes. Nature 440:818-823.PubMedCrossRefGoogle Scholar
  62. Jossin, Y. (2004). Neuronal migration and the role of reelin during early development of the cere-bral cortex. Mol. Neurobiol. 30:225-251.PubMedCrossRefGoogle Scholar
  63. Jossin, Y., Bar, I., Ignatova, N., Tissir, F., Lambert de Rouvroit, C., and Goffinet, A. M. (2003a). The reelin signaling pathway: some recent developments. Cereb. Cortex 13:627-633.PubMedCrossRefGoogle Scholar
  64. Jossin, Y., Ogawa, M., Metin, C., Tissir, F., and Goffinet, A. M. (2003b). Inhibition of SRC family kinases and non-classical protein kinases C induce a reeler-like malformation of cortical plate development. J. Neurosci. 23:9953-9959.PubMedGoogle Scholar
  65. Jossin, Y., Ignatova, N., Hiesberger, T., Herz, J., Lambert de Rouvroit, C., and Goffinet, A. M. (2004). The central fragment of reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J. Neurosci. 24:514-521.PubMedCrossRefGoogle Scholar
  66. Katyal, S., and Godbout, R. (2004). Alternative splicing modulates disabled-1 (Dab1) function in the developing chick retina. EMBO J. 23:1878-1888.PubMedCrossRefGoogle Scholar
  67. Keshvara, L., Benhayon, D., Magdaleno, S., and Curran, T. (2001). Identification of reelin-induced sites of tyrosyl phosphorylation on disabled 1. J. Biol. Chem. 276:16008-16014.PubMedCrossRefGoogle Scholar
  68. 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.PubMedGoogle Scholar
  69. Ko, J., Humbert, S., Bronson, R. T., Takahashi, S., Kulkarni, A. B., Li, E., and Tsai, L. H. (2001). p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. J. Neurosci. 21:6758-6771.PubMedGoogle Scholar
  70. Kuo, G., Arnaud, L., Kronstad-O’Brien, P., and Cooper, J. A. (2005). Absence of Fyn and Src causes a reeler-like phenotype. J. Neurosci. 25:8578-8586.PubMedCrossRefGoogle Scholar
  71. Kwon, Y. T., and Tsai, L. H. (1998). A novel disruption of cortical development in p35(-/-) mice distinct from reeler. J. Comp. Neurol. 395:510-522.PubMedCrossRefGoogle Scholar
  72. Lambert de Rouvroit, C., and Goffinet, A. M. (2001). Neuronal migration. Mech. Dev. 105:47-56.PubMedCrossRefGoogle Scholar
  73. Li, W., Fan, J., and Woodley, D. T. (2001). Nck/Dock: an adapter between cell surface receptors and the actin cytoskeleton. Oncogene 20:6403-6417.PubMedCrossRefGoogle Scholar
  74. Mayer, H., Duit, S., Hauser, C., Schneider, W. J., and Nimpf, J. (2006). Reconstitution of the reelin signaling pathway in fibroblasts demonstrates that Dab1 phosphorylation is independent of receptor localization in lipid rafts. Mol. Cell. Biol. 26:19-27.PubMedCrossRefGoogle Scholar
  75. Morimura, T., Hattori, M., Ogawa, M., and Mikoshiba, K. (2005). Disabled1 regulates the intrac-ellular trafficking of reelin receptors. J. Biol. Chem. 280:16901-16908.PubMedCrossRefGoogle Scholar
  76. Mukherjee, A., Arnaud, L., and Cooper, J. A. (2003). Lipid-dependent recruitment of NSrc to lipid rafts in the brain. J. Biol. Chem. 278:40806-40814.PubMedCrossRefGoogle Scholar
  77. 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.PubMedCrossRefGoogle Scholar
  78. Ogawa, M., Miyata, T., Nakajima, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H., and Mikoshiba, K. (1995). The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14:899-912.PubMedCrossRefGoogle Scholar
  79. Ohba, Y., Ikuta, K., Ogura, A., Matsuda, J., Mochizuki, N., Nagashima, K., Kurokawa, K., Mayer, B. J., Maki, K., Miyazaki, J., and Matsuda, M. (2001). Requirement for C3G-dependent Rap1 activation for cell adhesion and embryogenesis. EMBO J. 20:3333-3341.PubMedCrossRefGoogle Scholar
  80. Ohkubo, N., Lee, Y. D., Morishima, A., Terashima, T., Kikkawa, S., Tohyama, M., Sakanaka, M., Tanaka, J., Maeda, N., Vitek, M. P., and Mitsuda, N. (2003). Apolipoprotein E and reelin lig-ands modulate tau phosphorylation through an apolipoprotein E receptor/disabled-1/glycogen synthase kinase-3beta cascade. FASEB J. 17:295-297.PubMedGoogle Scholar
  81. 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.PubMedCrossRefGoogle Scholar
  82. 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.PubMedCrossRefGoogle Scholar
  83. 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.PubMedGoogle Scholar
  84. 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.PubMedCrossRefGoogle Scholar
  85. Olson, E. C., Kim, S., and Walsh, C. A. (2006). Impaired neuronal positioning and dendritogene-sis in the neocortex after cell-autonomous Dab1 suppression. J. Neurosci. 26:1767-1775.PubMedCrossRefGoogle Scholar
  86. O’Sullivan, E., Kinnon, C., and Brickell, P. (1999). Wiskott-Aldrich syndrome protein, WASP. Int. J. Biochem. Cell Biol. 31:383-387.CrossRefGoogle Scholar
  87. Park, T. J., Boyd, K., and Curran, T. (2006). Cardiovascular and craniofacial defects in Crk-null mice. Mol. Cell. Biol. 26:6272-6282.PubMedCrossRefGoogle Scholar
  88. Pawson, T. (1995). Protein modules and signalling networks. Nature (London) 373:573-580.CrossRefGoogle Scholar
  89. Pinto-Lord, M. C., Evrard, P., and Caviness, V. S., Jr. (1982). Obstructed neuronal migration along radial glial fibers in the neocortex of the reeler mouse: a Golgi-EM analysis. Brain Res. 256:379-393.PubMedGoogle Scholar
  90. Ponniah, S., Wang, D. Z., Lim, K. L., and Pallen, C. J. (1999). Targeted disruption of the tyrosine phosphatase PTPalpha leads to constitutive downregulation of the kinases Src and Fyn. Curr. Biol. 9:535-538.PubMedCrossRefGoogle Scholar
  91. Pramatarova, A., Ochalski, P. G., Chen, K., Gropman, A., Myers, S., Min, K. T., and Howell, B. W. (2003). Nck beta interacts with tyrosine-phosphorylated disabled 1 and redistributes in reelin-stimulated neurons. Mol. Cell. Biol. 23:7210-7221.PubMedCrossRefGoogle Scholar
  92. Rakic, S., Davis, C., Molnar, Z., Nikolic, M., and Parnavelas, J. G. (2006). Role of p35/Cdk5 in preplate splitting in the developing cerebral cortex. Cereb. Cortex 16(Suppl. 1):i35-45.PubMedCrossRefGoogle Scholar
  93. Reiner, O. (2000). LIS1. let’s interact sometimes (part 1). Neuron 28:633-636.PubMedCrossRefGoogle Scholar
  94. 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 beta-subunit-like repeats. Nature 364:717-721.PubMedCrossRefGoogle Scholar
  95. Rice, D. S., and Curran, T. (2001). Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 24:1005-1039.PubMedCrossRefGoogle Scholar
  96. Rice, D. S., Sheldon, M., D’Arcangelo, G., Nakajima, K., Goldowitz, D., and Curran, T. (1998). Disabled-1 acts downstream of reelin in a signaling pathway that controls laminar organization in the mammalian brain. Development 125:3719-3729.PubMedGoogle Scholar
  97. Riddell, D. R., Sun, X. M., Stannard, A. K., Soutar, A. K., and Owen, J. S. (2001). Localization of apolipoprotein E receptor 2 to caveolae in the plasma membrane. J. Lipid Res. 42:998-1002.PubMedGoogle Scholar
  98. Rohatgi, R., Nollau, P., Ho, H. Y., Kirschner, M. W., and Mayer, B. J. (2001). Nck and phosphati-dylinositol 4,5-bisphosphate synergistically activate actin polymerization through the N-WASP-Arp2/3 pathway. J. Biol. Chem. 276:26448-26452.PubMedCrossRefGoogle Scholar
  99. Rossel, M., Loulier, K., Feuillet, C., Alonso, S., and Carroll, P. (2005). Reelin signaling is neces-sary for a specific step in the migration of hindbrain efferent neurons. Development 132:1175-1185.PubMedCrossRefGoogle Scholar
  100. Sanada, K., Gupta, A., and Tsai, L. H. (2004). Disabled-1-regulated adhesion of migrating neu-rons to radial glial fiber contributes to neuronal positioning during early corticogenesis. Neuron 42:197-211.PubMedCrossRefGoogle Scholar
  101. Sasaki, Y., Cheng, C., Uchida, Y., Nakajima, O., Ohshima, T., Yagi, T., Taniguchi, M., Nakayama, T., Kishida, R., Kudo, Y., Ohno, S., Nakamura, F., and Goshima, Y. (2002). Fyn and Cdk5 mediate semaphorin-3A signaling, which is involved in regulation of dendrite orientation in cerebral cortex. Neuron 35:907-920.PubMedCrossRefGoogle Scholar
  102. Schmid, R. S., Shelton, S., Stanco, A., Yokota, Y., Kreidberg, J. A., and Anton, E. S. (2004). alpha3beta1 integrin modulates neuronal migration and placement during early stages of cere-bral cortical development. Development 131:6023-6031.PubMedCrossRefGoogle Scholar
  103. Schmid, R. S., Jo, R., Shelton, S., Kreidberg, J. A., and Anton, E. S. (2005). Reelin, integrin and Dab1 interactions during embryonic cerebral cortical development. Cereb. Cortex 15:1632-1636.PubMedCrossRefGoogle Scholar
  104. Schmidt, E. K., Fichelson, S., and Feller, S. M. (2004). PI3 kinase is important for Ras, MEK and Erk activation of Epo-stimulated human erythroid progenitors. BMC Biol. 2:7.PubMedCrossRefGoogle Scholar
  105. Sheen, V. L., Ferland, R. J., Harney, M., Hill, R. S., Neal, J., Banham, A. H., Brown, P., Chenn, A., Corbo, J., Hecht, J., Folkerth, R., and Walsh, C. A. (2006). Impaired proliferation and migration in human Miller-Dieker neural precursors. Ann. Neurol. 60:137-144.PubMedCrossRefGoogle Scholar
  106. Sheldon, M., Rice, D. S., D’Arcangelo, G., Yoneshima, H., Nakajima, K., Mikoshiba, K., Howell, B. W., Cooper, J. A., Goldowitz, D., and Curran, T. (1997). Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature (London) 389:730-733.CrossRefGoogle Scholar
  107. Shu, T., Ayala, R., Nguyen, M. D., Xie, Z., Gleeson, J. G., and Tsai, L. H. (2004). Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal posi-tioning. Neuron 44:263-277.PubMedCrossRefGoogle Scholar
  108. Sicheri, F., and Kuriyan, J. (1997). Structures of Src-family tyrosine kinases. Curr. Opin. Struct. Biol. 7:777-785.PubMedCrossRefGoogle Scholar
  109. Simo, S., Pujadas, L., Segura, M. F., La Torre, A., Del Rio, J. A., Urena, J. M., Comella, J. X., and Soriano, E. (2007). Reelin induces the detachment of postnatal subventricular zone cells and the expression of the Egr-1 through Erk1/2 activation. Cereb. Cortex 17:294-303.PubMedCrossRefGoogle Scholar
  110. Sondermann, H., and Kuriyan, J. (2005). C2 can do it, too. Cell 121:158-160.PubMedCrossRefGoogle Scholar
  111. Songyang, Z., Shoelson, S. E., Chaudhuri, M., Gish, G., Pawson, T., Haser, W. G., King, F., Roberts, T., Ratnofsky, S., Lechleider, R. J., Neel, B. G., Birge, R. B., Fajardo, J. E., Chou, M. M., Hanafusa, H., Schaffhausen, B., and Cantley, L. C. (1993). SH2 domains recognize specific phosphopeptide sequences. Cell 72:767-778.PubMedCrossRefGoogle Scholar
  112. Soriano, P., Montgomery, C., Geske, R., and Bradley, A. (1991). Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64:693-702.PubMedCrossRefGoogle Scholar
  113. Stolt, P. C., Jeon, H., Song, H. K., Herz, J., Eck, M. J., and Blacklow, S. C. (2003). Origins of peptide selectivity and phosphoinositide binding revealed by structures of disabled-1 PTB domain complexes. Structure (Camb.) 11:569-579.CrossRefGoogle Scholar
  114. Stolt, P. C., Vardar, D., and Blacklow, S. C. (2004). The dual-function disabled-1 PTB domain exhibits site independence in binding phosphoinositide and peptide ligands. Biochemistry 43:10979-10987.PubMedCrossRefGoogle Scholar
  115. Stolt, P. C., Chen, Y., Liu, P., Bock, H. H., Blacklow, S. C., and Herz, J. (2005). Phosphoinositide binding by the disabled-1 PTB domain is necessary for membrane localization and reelin sig-nal transduction. J. Biol. Chem. 280:9671-9677.PubMedCrossRefGoogle Scholar
  116. Strasser, V., Fasching, D., Hauser, C., Mayer, H., Bock, H. H., Hiesberger, T., Herz, J., Weeber, E. J., Sweatt, J. D., Pramatarova, A., Howell, B., Schneider, W. J., and Nimpf, J. (2004). Receptor clustering is involved in reelin signaling. Mol. Cell. Biol. 24:1378-1386.PubMedCrossRefGoogle Scholar
  117. Su, J., Muranjan, M., and Sap, J. (1999). Receptor protein tyrosine phosphatase alpha activates Src-family kinases and controls integrin-mediated responses in fibroblasts. Curr. Biol. 9:505-511.PubMedCrossRefGoogle Scholar
  118. Suetsugu, S., Tezuka, T., Morimura, T., Hattori, M., Mikoshiba, K., Yamamoto, T., and Takenawa, T. (2004). Regulation of actin cytoskeleton by mDab1 through N-WASP and ubiquitination of mDab1. Biochem. J. 384:1-8.PubMedCrossRefGoogle Scholar
  119. Sweet, H. O., Bronson, R. T., Johnson, K. R., Cook, S. A., and Davisson, M. T. (1996). Scrambler, a new neurological mutation of the mouse with abnormalities of neuronal migration. Mamm. Genome 7:798-802.PubMedCrossRefGoogle Scholar
  120. Tabata, H., and Nakajima, K. (2002). Neurons tend to stop migration and differentiate along the cor-tical internal plexiform zones in the reelin signal-deficient mice. J. Neurosci. Res. 69:723-730.PubMedCrossRefGoogle Scholar
  121. Takeda, H., Matozaki, T., Takada, T., Noguchi, T., Yamao, T., Tsuda, M., Ochi, F., Fukunaga, K., Inagaki, K., and Kasuga, M. (1999). PI 3-kinase gamma and protein kinase C-zeta mediate RAS-independent activation of MAP kinase by a Gi protein-coupled receptor. EMBO J. 18:386-395.PubMedCrossRefGoogle Scholar
  122. Tanaka, S., Morishita, T., Hashimoto, Y., Hattori, S., Nakamura, S., Shibuya, M., Matuoka, K., Takenawa, T., Kurata, T., Nagashima, K., and Matsuda, M. (1994). C3G, a guanine nucleotide-releasing protein expressed ubiquitously, binds to the Src homology 3 domains of CRK and GRB2/ASH proteins. Proc. Natl. Acad. Sci. USA 91:3443-3447.PubMedCrossRefGoogle Scholar
  123. Terashima, T., Inoue, K., Inoue, Y., Yokoyama, M., and Mikoshiba, K. (1986). Observations on the cerebellum of normal-reeler mutant mouse chimera. J. Comp. Neurol. 252:264-278.PubMedCrossRefGoogle Scholar
  124. Tezuka, T., Umemori, H., Akiyama, T., Nakanishi, S., and Yamamoto, T. (1999). PSD-95 promotes Fyn-mediated tyrosine phosphorylation of the N-methyl-D-aspartate receptor subu-nit NR2A. Proc. Natl. Acad. Sci. USA 96:435-440.PubMedCrossRefGoogle Scholar
  125. 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.PubMedCrossRefGoogle Scholar
  126. Vanhaesebroeck, B., and Alessi, D. R. (2000). The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 346(Pt 3):561-576.PubMedCrossRefGoogle Scholar
  127. Ware, M. L., Fox, J. W., Gonzalez, J. L., Davis, N. M., Lambert de Rouvroit, C. L., Russo, C. J., Chua, S. C., Goffinet, A. M., and Walsh, C. A. (1997). Aberrant splicing of a mouse disabled homolog, mdab1, in the scrambler mouse. Neuron 19:239-249.PubMedCrossRefGoogle Scholar
  128. 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. 7:7.Google Scholar
  129. Xu, M., Arnaud, L., and Cooper, J. A. (2005). Both the phosphoinositide and receptor binding activities of Dab1 are required for reelin-stimulated Dab1 tyrosine phosphorylation. Brain Res. Mol. Brain Res. 139:300-305.PubMedCrossRefGoogle Scholar
  130. Yang, H., Jensen, P., and Goldowitz, D. (2002). The community effect and Purkinje cell migration in the cerebellar cortex: analysis of scrambler chimeric mice. J. Neurosci. 22:464-470.PubMedGoogle Scholar
  131. Yip, J. W., Yip, Y. P., Nakajima, K., and Capriotti, C. (2000). Reelin controls position of auto-nomic neurons in the spinal cord. Proc. Natl. Acad. Sci. USA 97:8612-8616.PubMedCrossRefGoogle Scholar
  132. Yoneshima, H., Nagata, E., Matsumoto, M., Yamada, M., Nakajima, K., Miyata, T., Ogawa, M., and Mikoshiba, K. (1997). A novel neurological mutant mouse, yotari, which exhibits reeler-like phenotype but expresses CR-50 antigen/reelin. Neurosci. Res. 29:217-223.PubMedCrossRefGoogle Scholar
  133. York, R. D., Yao, H., Dillon, T., Ellig, C. L., Eckert, S. P., McCleskey, E. W., and Stork, P. J. (1998). Rap1 mediates sustained MAP kinase activation induced by nerve growth factor. Nature 392:622-626.PubMedCrossRefGoogle Scholar
  134. Yoshiki, A., and Kusakabe, M. (1998). Cerebellar histogenesis as seen in identified cells of nor-mal-reeler mouse chimeras. Int. J. Dev. Biol. 42:695-700.PubMedGoogle Scholar
  135. Yu, X. M., Askalan, R., Keil, G. J., 2nd, and Salter, M. W. (1997). NMDA channel regulation by channel-associated protein tyrosine kinase Src. Science 275:674-678.PubMedCrossRefGoogle Scholar
  136. Yuasa, S., Hattori, K., and Yagi, T. (2004). Defective neocortical development in Fyn-tyrosine-kinase-deficient mice. Neuroreport 15:819-822.PubMedCrossRefGoogle Scholar
  137. Yun, M., Keshvara, L., Park, C. G., Zhang, Y. M., Dickerson, J. B., Zheng, J., Rock, C. O., Curran, T., and Park, H. W. (2003). Crystal structures of the dab homology domains of mouse disabled 1 and 2. J. Biol. Chem. 278:36572-36581.PubMedCrossRefGoogle Scholar
  138. Zhao, S., Chai, X., Forster, E., and Frotscher, M. (2004). Reelin is a positional signal for the lami-nation of dentate granule cells. Development 131:5117-5125.PubMedCrossRefGoogle Scholar
  139. Zheng, X. M., Wang, Y., and Pallen, C. J. (1992). Cell transformation and activation of pp60c-src by overexpression of a protein tyrosine phosphatase. Nature 359:336-339.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2008

Authors and Affiliations

  • Jonathan A. Cooper
    • 1
  • Nathaniel S. Allen
    • 1
  • Libing Feng
    • 1
  1. 1.Division of Basic SciencesFred Hutchinson Cancer Research CenterSeattle

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