Journal Mobile Options
Table of Contents
Vol. 30, No. 1-3, 2008
Issue release date: December 2007
Dev Neurosci 2008;30:36–46
(DOI:10.1159/000109850)

Molecular Pathways Regulating Cytoskeletal Organization and Morphological Changes in Migrating Neurons

Kawauchi T. · Hoshino M.
aDepartment of Anatomy, Keio University School of Medicine, bDepartment of Biochemistry and Cellular Biology, National Center of Neurology and Psychiatry (NCNP), Tokyo, and cDepartment of Pathology and Tumor Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan

Individual Users: Register with Karger Login Information

Please create your User ID & Password





Contact Information











I have read the Karger Terms and Conditions and agree.

To view the fulltext, please log in

To view the pdf, please log in

Abstract

Neuronal migration is a pivotal step for architectural and functional brain development. Migrating neurons exhibit various morphological changes, based on cytoskeletal organization. In addition to many genetic studies revealing the involvement of several cytoskeletal and signaling molecules in cortical neuronal migration (e.g. doublecortin, Lis1, Filamin A, cyclin-dependent kinase 5, Reelin and Dab1), cell biological studies and recently developed techniques, including in utero electroporation, have uncovered detailed functions of these molecules as well as novel molecules, such as Rho family GTPases, focal adhesion kinase, c-jun N-terminal kinase and p27kip1. In this review, we introduce the molecular pathways underlying cortical neuronal migration and morphological changes, with particular focus on recent findings for the regulatory mechanisms of actin cytoskeleton and microtubules.



Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

References

  1. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR: Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 2004;7:136–144.
  2. Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M: Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 2004;131:3133–3145.
  3. Haubensak W, Attardo A, Denk W, Huttner WB: Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc Natl Acad Sci USA 2004;101:3196–3201.
  4. Sidman RL, Miale IL, Feder N: Cell proliferation and migration in the primitive ependymal zone: an autoradiographic study of histogenesis in the nervous system. Exp Neurol 1959;1:322–333.
  5. Takahashi T, Nowakowski RS, Caviness VS Jr: The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J Neurosci 1995;15:6046–6057.
  6. Gotz M, Huttner WB: The cell biology of neurogenesis. Nat Rev Mol Cell Biol 2005;6:777–788.
  7. Marin-Padilla M: Cajal-Retzius cells and the development of the neocortex. Trends Neurosci 1998;21:64–71.
  8. Takiguchi-Hayashi K, Sekiguchi M, Ashigaki S, Takamatsu M, Hasegawa H, Suzuki- Migishima R, Yokoyama M, Nakanishi S, Tanabe Y: Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J Neurosci 2004;24:2286–2295.
  9. Bielle F, Griveau A, Narboux-Neme N, Vigneau S, Sigrist M, Arber S, Wassef M, Pierani A: Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci 2005;8:1002–1012.
  10. Hevner RF, Neogi T, Englund C, Daza RA, Fink A: Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin. Brain Res Dev Brain Res 2003;141:39–53.
  11. Takahashi T, Nowakowski RS, Caviness VS Jr: The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J Neurosci 1996;16:6183–6196.
  12. Kriegstein A, Noctor S, Martinez-Cerdeno V: Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 2006;7:883–890.
  13. Rakic P: Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 1972;145:61–83.
  14. Angevine JB, Sidman RL: Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 1961;192:766–768.
  15. Ayala R, Shu T, Tsai LH: Trekking across the brain: the journey of neuronal migration. Cell 2007;128:29–43.
  16. Gleeson JG, Walsh CA: Neuronal migration disorders: from genetic diseases to developmental mechanisms. Trends Neurosci 2000;23:352–359.
  17. Feng Y, Walsh CA: The many faces of filamin: a versatile molecular scaffold for cell motility and signalling. Nat Cell Biol 2004;6:1034–1038.
  18. Forman MS, Squier W, Dobyns WB, Golden JA: Genotypically defined lissencephalies show distinct pathologies. J Neuropathol Exp Neurol 2005;64:847–857.
  19. Reiner O, Carrozzo R, Shen Y, Wehnert M, Faustinella F, Dobyns WB, Caskey CT, Ledbetter DH: Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 1993;364:717–721.
  20. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR: Neurons derived from radial glial cells establish radial units in neocortex. Nature 2001;409:714–720.
  21. Tabata H, Nakajima K: Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 2003;23:9996–10001.
  22. Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL: Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 2001;4:143–150.
  23. Miyata T, Kawaguchi A, Okano H, Ogawa M: Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 2001;31:727–741.
  24. Tamamaki N, Nakamura K, Okamoto K, Kaneko T: Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci Res 2001;41:51–60.
  25. Des Portes V, Pinard JM, Billuart P, Vinet MC, 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.
  26. Gleeson JG, Allen KM, Fox JW, Lamperti ED, Berkovic S, Scheffer I, Cooper EC, Dobyns WB, Minnerath SR, Ross ME, Walsh CA: 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.
  27. Sapir T, Elbaum M, Reiner O: Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit. EMBO J 1997;16:6977–6984.
  28. Gleeson JG, Lin PT, Flanagan LA, Walsh CA: Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 1999;23:257–271.
  29. Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, Chelly J: Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 1999;23:247–256.
  30. Horesh D, Sapir T, Francis F, Wolf SG, Caspi M, Elbaum M, Chelly J, Reiner O: Doublecortin, a stabilizer of microtubules. Hum Mol Genet 1999;8:1599–1610.
  31. Fox JW, Lamperti ED, Eksioglu YZ, Hong SE, Feng Y, Graham DA, Scheffer IE, Dobyns WB, Hirsch BA, Radtke RA, Berkovic SF, Huttenlocher PR, Walsh CA: Mutations in filamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron 1998;21:1315–1325.
  32. Nikolic M: The molecular mystery of neuronal migration: FAK and Cdk5. Trends Cell Biol 2004;14:1–5.
  33. Marin O, Valdeolmillos M, Moya F: Neurons in motion: same principles for different shapes? Trends Neurosci 2006;29:655–661.
  34. Xie Z, Sanada K, Samuels BA, Shih H, Tsai LH: Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 2003;114:469–482.
  35. Kawauchi T, Chihama K, Nabeshima Y, Hoshino M: The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration. EMBO J 2003;22:4190–4201.
  36. Kawauchi T, Chihama K, Nabeshima Y, Hoshino M: Cdk5 phosphorylates and stabilizes p27kip1 contributing to actin organization and cortical neuronal migration. Nat Cell Biol 2006;8:17–26.
  37. Ridley AJ: Rho GTPases and cell migration. J Cell Sci 2001;114:2713–2722.
  38. Rivas RJ, Hatten ME: Motility and cytoskeletal organization of migrating cerebellar granule neurons. J Neurosci 1995;15:981–989.
  39. Goh KL, Cai L, Cepko CL, Gertler FB: Ena/VASP proteins regulate cortical neuronal positioning. Curr Biol 2002;12:565–569.
  40. Krause M, Dent EW, Bear JE, Loureiro JJ, Gertler FB: Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration. Annu Rev Cell Dev Biol 2003;19:541–564.
  41. Yoshizawa M, Kawauchi T, Sone M, Nishimura YV, Terao M, Chihama K, Nabeshima Y, Hoshino M: Involvement of a Rac activator, P-Rex1, in neurotrophin-derived signaling and neuronal migration. J Neurosci 2005;25:4406–4419.
  42. Chen L, Liao G, Waclaw RR, Burns KA, Linquist D, Campbell K, Zheng Y, Kuan CY: Rac1 controls the formation of midline commissures and the competency of tangential migration in ventral telencephalic neurons. J Neurosci 2007;27:3884–3893.
  43. Koizumi H, Tanaka T, Gleeson JG: Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 2006;49:55–66.
  44. Deuel TA, Liu JS, Corbo JC, Yoo SY, Rorke-Adams LB, Walsh CA: Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 2006;49:41–53.
  45. Bai J, Ramos RL, Ackman JB, Thomas AM, Lee RV, LoTurco JJ: RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat Neurosci 2003;6:1277–1283.
  46. Itoh Y, Masuyama N, Nakayama K, Nakayama KI, Gotoh Y: The cyclin-dependent kinase inhibitors p57 and p27 regulate neuronal migration in the developing mouse neocortex. J Biol Chem 2007;282:390–396.
  47. Nguyen L, Besson A, Heng JI, Schuurmans C, Teboul L, Parras C, Philpott A, Roberts JM, Guillemot F: p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev 2006;20:1511–1524.
  48. Konno D, Yoshimura S, Hori K, Maruoka H, Sobue K: Involvement of the phosphatidylinositol 3-kinase/rac1 and cdc42 pathways in radial migration of cortical neurons. J Biol Chem 2005;280:5082–5088.
  49. Kholmanskikh SS, Koeller HB, Wynshaw-Boris A, Gomez T, Letourneau PC, Ross ME: Calcium-dependent interaction of Lis1 with IQGAP1 and Cdc42 promotes neuronal motility. Nat Neurosci 2006;9:50–57.
  50. Hand R, Bortone D, Mattar P, Nguyen L, Heng JI, Guerrier S, Boutt E, Peters E, Barnes AP, Parras C, Schuurmans C, Guillemot F, Polleux F: Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 2005;48:45–62.
  51. Ge W, He F, Kim KJ, Blanchi B, Coskun V, Nguyen L, Wu X, Zhao J, Heng JI, Martinowich K, Tao J, Wu H, Castro D, Sobeih MM, Corfas G, Gleeson JG, Greenberg ME, Guillemot F, Sun YE: Coupling of cell migration with neurogenesis by proneural bHLH factors. Proc Natl Acad Sci USA 2006;103:1319–1324.
  52. Kholmanskikh SS, Dobrin JS, Wynshaw-Boris A, Letourneau PC, Ross ME: Disregulated RhoGTPases and actin cytoskeleton contribute to the migration defect in Lis1-deficient neurons. J Neurosci 2003;23:8673–8681.
  53. Tsukada M, Prokscha A, Ungewickell E, Eichele G: Doublecortin association with actin filaments is regulated by neurabin II. J Biol Chem 2005;280:11361–11368.
  54. Nagano T, Morikubo S, Sato M: Filamin A and FILIP (Filamin A-interacting protein) regulate cell polarity and motility in neocortical subventricular and intermediate zones during radial migration. J Neurosci 2004;24:9648–9657.
  55. Stossel TP, Condeelis J, Cooley L, Hartwig JH, Noegel A, Schleicher M, Shapiro SS: Filamins as integrators of cell mechanics and signalling. Nat Rev Mol Cell Biol 2001;2:138–145.
  56. Schaar BT, McConnell SK: Cytoskeletal coordination during neuronal migration. Proc Natl Acad Sci USA 2005;102:13652–13657.
  57. Moores CA, Perderiset M, Kappeler C, Kain S, Drummond D, Perkins SJ, Chelly J, Cross R, Houdusse A, Francis F: Distinct roles of doublecortin modulating the microtubule cytoskeleton. EMBO J 2006;25:4448–4457.
  58. Keays DA, Tian G, Poirier K, Huang GJ, Siebold C, Cleak J, Oliver PL, Fray M, Harvey RJ, Molnar Z, Pinon MC, Dear N, Valdar W, Brown SD, Davies KE, Rawlins JN, Cowan NJ, Nolan P, Chelly J, Flint J: Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 2007;128:45–57.
  59. Rakic P, Knyihar-Csillik E, Csillik B: Polarity of microtubule assemblies during neuronal cell migration. Proc Natl Acad Sci USA 1996;93:9218–9222.
  60. Shea TB: Selective stabilization of microtubules within the proximal region of developing axonal neurites. Brain Res Bull 1999;48:255–261.
  61. Goold RG, Owen R, Gordon-Weeks PR: Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J Cell Sci 1999;112:3373–3384.
  62. Kawauchi T, Chihama K, Nishimura YV, Nabeshima Y, Hoshino M: MAP1B phosphorylation is differentially regulated by Cdk5/p35, Cdk5/p25, and JNK. Biochem Biophys Res Commun 2005;331:50–55.
  63. Gonzalez-Billault C, Del Rio JA, Urena JM, Jimenez-Mateos EM, Barallobre MJ, Pascual M, Pujadas L, Simo S, Torre AL, Gavin R, Wandosell F, Soriano E, Avila J: A role of MAP1B in Reelin-dependent neuronal migration. Cereb Cortex 2005;15:1134–1145.
  64. Hirotsune S, Fleck MW, Gambello MJ, Bix GJ, Chen A, Clark GD, Ledbetter DH, McBain CJ, Wynshaw-Boris A: Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat Genet 1998;19:333–339.
  65. Tsai JW, Chen Y, Kriegstein AR, Vallee RB: LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J Cell Biol 2005;170:935–945.
  66. Faulkner NE, Dujardin DL, Tai CY, Vaughan KT, O’Connell CB, Wang Y, Vallee RB: A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat Cell Biol 2000;2:784–791.
  67. Smith DS, Niethammer M, Ayala R, Zhou Y, Gambello MJ, Wynshaw-Boris A, Tsai LH: Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian Lis1. Nat Cell Biol 2000;2:767–775.
  68. Sasaki S, Shionoya A, Ishida M, Gambello MJ, Yingling J, Wynshaw-Boris A, Hirotsune S: A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 2000;28:681–696.
  69. Tai CY, Dujardin DL, Faulkner NE, Vallee RB: Role of dynein, dynactin, and CLIP-170 interactions in LIS1 kinetochore function. J Cell Biol 2002;156:959–968.
  70. Feng Y, Olson EC, Stukenberg PT, Flanagan LA, Kirschner MW, Walsh CA: LIS1 regulates CNS lamination by interacting with mNudE, a central component of the centrosome. Neuron 2000;28:665–679.
  71. Niethammer M, Smith DS, Ayala R, Peng J, Ko J, Lee MS, Morabito M, Tsai LH: NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 2000;28:697–711.
  72. Coquelle FM, Caspi M, Cordelieres FP, Dompierre JP, Dujardin DL, Koifman C, Martin P, Hoogenraad CC, Akhmanova A, Galjart N, De Mey JR, Reiner O: LIS1, CLIP-170’s key to the dynein/dynactin pathway. Mol Cell Biol 2002;22:3089–3102.
  73. Mesngon MT, Tarricone C, Hebbar S, Guillotte AM, Schmitt EW, Lanier L, Musacchio A, King SJ, Smith DS: Regulation of cytoplasmic dynein ATPase by Lis1. J Neurosci 2006;26:2132–2139.
  74. Shu T, Ayala R, Nguyen MD, Xie Z, Gleeson JG, Tsai LH: Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning. Neuron 2004;44:263–277.
  75. Sasaki S, Mori D, Toyo-Oka K, Chen A, Garrett-Beal L, Muramatsu M, Miyagawa S, Hiraiwa N, Yoshiki A, Wynshaw-Boris A, Hirotsune S: Complete loss of Ndel1 results in neuronal migration defects and early embryonic lethality. Mol Cell Biol 2005;25:7812–7827.
  76. Jimenez-Mateos EM, Wandosell F, Reiner O, Avila J, Gonzalez-Billault C: Binding of microtubule-associated protein 1B to LIS1 affects the interaction between dynein and LIS1. Biochem J 2005;389:333–341.
  77. LoTurco J: Doublecortin and a tale of two serines. Neuron 2004;41:175–177.
  78. Corbo JC, Deuel TA, Long JM, LaPorte P, Tsai E, Wynshaw-Boris A, Walsh CA: Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J Neurosci 2002;22:7548–7557.
  79. Koizumi H, Higginbotham H, Poon T, Tanaka T, Brinkman BC, Gleeson JG: Doublecortin maintains bipolar shape and nuclear translocation during migration in the adult forebrain. Nat Neurosci 2006;9:779–786.
  80. Caspi M, Atlas R, Kantor A, Sapir T, Reiner O: Interaction between LIS1 and doublecortin, two lissencephaly gene products. Hum Mol Genet 2000;9:2205–2213.
  81. Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG: Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J Cell Biol 2004;165:709–721.
  82. Solecki DJ, Model L, Gaetz J, Kapoor TM, Hatten ME: Par6alpha signaling controls glial-guided neuronal migration. Nat Neurosci 2004;7:1195–1203.
  83. Sapir T, Cahana A, Seger R, Nekhai S, Reiner O: LIS1 is a microtubule-associated phosphoprotein. Eur J Biochem 1999;265:181–188.
  84. Gordon-Weeks PR, Fischer I: MAP1B expression and microtubule stability in growing and regenerating axons. Microsc Res Tech 2000;48:63–74.
  85. Gilmore EC, Ohshima T, Goffinet AM, Kulkarni AB, Herrup K: Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in cerebral cortex. J Neurosci 1998;18:6370–6377.
  86. Chae T, Kwon YT, Bronson R, Dikkes P, Li E, Tsai LH: Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 1997;18:29–42.
  87. Gupta A, Sanada K, Miyamoto DT, Rovelstad S, Nadarajah B, Pearlman AL, Brunstrom J, Tsai LH: Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat Neurosci 2003;6:1284–1291.
  88. Tanaka T, Serneo FF, Tseng HC, Kulkarni AB, Tsai LH, Gleeson JG: Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 2004;41:215–227.
  89. Toyo-Oka K, Shionoya A, Gambello MJ, Cardoso C, Leventer R, Ward HL, Ayala R, Tsai LH, Dobyns W, Ledbetter D, Hirotsune S, Wynshaw-Boris A: 14-3-3epsilon is important for neuronal migration by binding to NUDEL: a molecular explanation for Miller-Dieker syndrome. Nat Genet 2003;34:274–285.
  90. Toyo-Oka K, Sasaki S, Yano Y, Mori D, Kobayashi T, Toyoshima YY, Tokuoka SM, Ishii S, Shimizu T, Muramatsu M, Hiraiwa N, Yoshiki A, Wynshaw-Boris A, Hirotsune S: Recruitment of katanin p60 by phosphorylated NDEL1, an LIS1 interacting protein, is essential for mitotic cell division and neuronal migration. Hum Mol Genet 2005;14:3113–3128.
  91. Gdalyahu A, Ghosh I, Levy T, Sapir T, Sapoznik S, Fishler Y, Azoulai D, Reiner O: DCX, a new mediator of the JNK pathway. EMBO J 2004;23:823–832.
  92. Schaar BT, Kinoshita K, McConnell SK: Doublecortin microtubule affinity is regulated by a balance of kinase and phosphatase activity at the leading edge of migrating neurons. Neuron 2004;41:203–213.
  93. Coquelle FM, Levy T, Bergmann S, Wolf SG, Bar-El D, Sapir T, Brody Y, Orr I, Barkai N, Eichele G, Reiner O: Common and divergent roles for members of the mouse DCX superfamily. Cell Cycle 2006;5:976–983.
  94. Tsukada M, Prokscha A, Eichele G: Neurabin II mediates doublecortin-dephosphorylation on actin filaments. Biochem Biophys Res Commun 2006;343:839–847.
  95. Shmueli A, Gdalyahu A, Sapoznik S, Sapir T, Tsukada M, Reiner O: Site-specific dephosphorylation of doublecortin (DCX) by protein phosphatase 1 (PP1). Mol Cell Neurosci 2006;32:15–26.
  96. Hirai SI, Feng Cui D, Miyata T, Ogawa M, Kiyonari H, Suda Y, Aizawa S, Banba Y, Ohno S: The c-Jun N-Terminal kinase activator dual leucine zipper kinase regulates axon growth and neuronal migration in the developing cerebral cortex. J Neurosci 2006;26:11992–12002.
  97. Sarkisian MR, Bartley CM, Chi H, Nakamura F, Hashimoto-Torii K, Torii M, Flavell RA, Rakic P: MEKK4 signaling regulates filamin expression and neuronal migration. Neuron 2006;52:789–801.
  98. Chang L, Jones Y, Ellisman MH, Goldstein LS, Karin M: JNK1 is required for maintenance of neuronal microtubules and controls phosphorylation of microtubule-associated proteins. Dev Cell 2003;4:521–533.
  99. Trivedi N, Marsh P, Goold RG, Wood-Kaczmar A, Gordon-Weeks PR: Glycogen synthase kinase-3beta phosphorylation of MAP1B at Ser1260 and Thr1265 is spatially restricted to growing axons. J Cell Sci 2005;118:993–1005.
  100. Del Rio JA, Gonzalez-Billault C, Urena JM, Jimenez EM, Barallobre MJ, Pascual M, Pujadas L, Simo S, La Torre A, Wandosell F, Avila J, Soriano E: MAP1B is required for Netrin 1 signaling in neuronal migration and axonal guidance. Curr Biol 2004;14:840–850.
  101. Oliva AA Jr, Atkins CM, Copenagle L, Banker GA: Activated c-Jun N-terminal kinase is required for axon formation. J Neurosci 2006;26:9462–9470.
  102. Huang C, Jacobson K, Schaller MD: MAP kinases and cell migration. J Cell Sci 2004;117:4619–4628.
  103. Nikolic M, Chou MM, Lu W, Mayer BJ, Tsai LH: The p35/Cdk5 kinase is a neuron-specific Rac effector that inhibits Pak1 activity. Nature 1998;395:194–198.
  104. Tarui T, Takahashi T, Nowakowski RS, Hayes NL, Bhide PG, Caviness VS: Overexpression of p27 Kip 1, probability of cell cycle exit, and laminar destination of neocortical neurons. Cereb Cortex 2005;15:1343–1355.
  105. Zindy F, Cunningham JJ, Sherr CJ, Jogal S, Smeyne RJ, Roussel MF: Postnatal neuronal proliferation in mice lacking Ink4d and Kip1 inhibitors of cyclin-dependent kinases. Proc Natl Acad Sci USA 1999;96:13462–13467.
  106. Guillemot F, Molnar Z, Tarabykin V, Stoykova A: Molecular mechanisms of cortical differentiation. Eur J Neurosci 2006;23:857–868.
  107. Cicero S, Herrup K: Cyclin-dependent kinase 5 is essential for neuronal cell cycle arrest and differentiation. J Neurosci 2005;25:9658–9668.
  108. Ferguson KL, Vanderluit JL, Hebert JM, McIntosh WC, Tibbo E, MacLaurin JG, Park DS, Wallace VA, Vooijs M, McConnell SK, Slack RS: Telencephalon-specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development. EMBO J 2002;21:3337–3346.
  109. Ferguson KL, McClellan KA, Vanderluit JL, McIntosh WC, Schuurmans C, Polleux F, Slack RS: A cell-autonomous requirement for the cell cycle regulatory protein, Rb, in neuronal migration. EMBO J 2005;24:4381–4391.
  110. McClellan KA, Slack RS: Novel functions for cell cycle genes in nervous system development. Cell Cycle 2006;5:1506–1513.
  111. Nagano T, Yoneda T, Hatanaka Y, Kubota C, Murakami F, Sato M: Filamin A-interacting protein (FILIP) regulates cortical cell migration out of the ventricular zone. Nat Cell Biol 2002;4:495–501.
  112. Komuro H, Kumada T: Ca2+ transients control CNS neuronal migration. Cell Calcium 2005;37:387–393.
  113. Rice DS, Curran T: Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 2001;24:1005–1039.
  114. Tissir F, Goffinet AM: Reelin and brain development. Nat Rev Neurosci 2003;4:496–505.
  115. Hong SE, Shugart YY, Huang DT, Shahwan SA, Grant PE, Hourihane JO, Martin ND, Walsh CA: Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat Genet 2000;26:93–96.
  116. Bock HH, Herz J: Reelin activates SRC family tyrosine kinases in neurons. Curr Biol 2003;13:18–26.
  117. Arnaud L, Ballif BA, Forster E, Cooper JA: Fyn tyrosine kinase is a critical regulator of disabled-1 during brain development. Curr Biol 2003;13:9–17.
  118. Beffert U, Morfini G, Bock HH, Reyna H, Brady ST, Herz J: Reelin-mediated signaling locally regulates protein kinase B/Akt and glycogen synthase kinase 3beta. J Biol Chem 2002;277:49958–49964.
  119. Bock HH, Jossin Y, Liu P, Forster E, May P, Goffinet AM, Herz J: Phosphatidylinositol 3-kinase interacts with the adaptor protein Dab1 in response to Reelin signaling and is required for normal cortical lamination. J Biol Chem 2003;278:38772–38779.
  120. Ballif BA, Arnaud L, Arthur WT, Guris D, Imamoto A, Cooper JA: Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Curr Biol 2004;14:606–610.
  121. Chen K, Ochalski PG, Tran TS, Sahir N, Schubert M, Pramatarova A, Howell BW: Interaction between Dab1 and CrkII is promoted by Reelin signaling. J Cell Sci 2004;117:4527–4536.
  122. Huang Y, Magdaleno S, Hopkins R, Slaughter C, Curran T, Keshvara L: Tyrosine phosphorylated Disabled 1 recruits Crk family adapter proteins. Biochem Biophys Res Commun 2004;318:204–212.
  123. Suetsugu S, Tezuka T, Morimura T, Hattori M, Mikoshiba K, Yamamoto T, Takenawa T: Regulation of actin cytoskeleton by mDab1 through N-WASP and ubiquitination of mDab1. Biochem J 2004;384:1–8.
  124. Assadi AH, Zhang G, Beffert U, McNeil RS, Renfro AL, Niu S, Quattrocchi CC, Antalffy BA, Sheldon M, Armstrong DD, Wynshaw-Boris A, Herz J, D’Arcangelo G, Clark GD: Interaction of reelin signaling and Lis1 in brain development. Nat Genet 2003;35:270–276.
  125. Ohshima T, Ogawa M, Veeranna, Hirasawa M, Longenecker G, Ishiguro K, Pant HC, Brady RO, Kulkarni AB, Mikoshiba K: Synergistic contributions of cyclin-dependent kinase 5/p35 and Reelin/Dab1 to the positioning of cortical neurons in the developing mouse brain. Proc Natl Acad Sci USA 2001;98:2764–2769.
  126. Tabata H, Nakajima K: Neurons tend to stop migration and differentiate along the cortical internal plexiform zones in the Reelin signal-deficient mice. J Neurosci Res 2002;69:723–730.
  127. Olson EC, Kim S, Walsh CA: Impaired neuronal positioning and dendritogenesis in the neocortex after cell-autonomous Dab1 suppression. J Neurosci 2006;26:1767–1775.
  128. Hartfuss E, Forster E, Bock HH, Hack MA, Leprince P, Luque JM, Herz J, Frotscher M, Gotz M: Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 2003;130:4597–4609.
  129. Caric D, Raphael H, Viti J, Feathers A, Wancio D, Lillien L: EGFRs mediate chemotactic migration in the developing telencephalon. Development 2001;128:4203–4216.
  130. Medina DL, Sciarretta C, Calella AM, Von Bohlen Und Halbach O, Unsicker K, Minichiello L: TrkB regulates neocortex formation through the Shc/PLCgamma-mediated control of neuronal migration. EMBO J 2004;23:3803–3814.
  131. Dulabon L, Olson EC, Taglienti MG, Eisenhuth S, McGrath B, Walsh CA, Kreidberg JA, Anton ES: Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron 2000;27:33–44.
  132. Sanada K, Gupta A, Tsai LH: Disabled-1-regulated adhesion of migrating neurons to radial glial fiber contributes to neuronal positioning during early corticogenesis. Neuron 2004;42:197–211.
  133. Kamiya A, Kubo K, Tomoda T, Takaki M, Youn R, Ozeki Y, Sawamura N, Park U, Kudo C, Okawa M, Ross CA, Hatten ME, Nakajima K, Sawa A: A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat Cell Biol 2005;7:1167–1178.
  134. Galaburda AM, Loturco J, Ramus F, Fitch RH, Rosen GD: From genes to behavior in developmental dyslexia. Nat Neurosci 2006;9:1213–1217.
  135. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH: Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999;402:615–622.
  136. Cruz JC, Tsai LH: Cdk5 deregulation in the pathogenesis of Alzheimer’s disease. Trends Mol Med 2004;10:452–458.
  137. Metin C, Baudoin JP, Rakic S, Parnavelas JG: Cell and molecular mechanisms involved in the migration of cortical interneurons. Eur J Neurosci 2006;23:894–900.
  138. Hoshino M, Nakamura S, Mori K, Kawauchi T, Terao M, Nishimura YV, Fukuda A, Fuse T, Matsuo N, Sone M, Watanabe M, Bito H, Terashima T, Wright CV, Kawaguchi Y, Nakao K, Nabeshima Y: Ptf1a, a bHLH transcriptional gene, defines GABAergic neuronal fates in cerebellum. Neuron 2005;47:201–213.


Pay-per-View Options
Direct payment This item at the regular price: USD 9.00
Payment from account With a Karger Pay-per-View account (down payment USD 150) you profit from a special rate for this and other single items.
This item at the discounted price: USD 8.00