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The Reelin-Signaling Pathway and Mouse Cortical Development

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Mouse Brain Development

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 30))

Abstract

Reelin (Rein) is an extracellular matrix protein that plays a pivotal role in the patterning of the brain, as shown by the analysis of the Reln-null phenotype, the so-called reeler mouse. During the last 2 years, Reln has been shown to act on target cells together with partners that include Dabl, VLDLR and ApoER2, thus defining a Re1n-signaling pathway. Although Reln and its partners act all over the central nervous system, it is at the level of the cerebral cortex, hippocampus and cerebellum that their action is best studied and the present discussion will focus on cortical development. A more detailed discussion of the reeler phenotype is provided in a recent review (Lambert de Rouvroit and Goffinet 1998a).

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References

  • Alcantara S, Ruiz M, D’Arcangelo G, Ezan F, de Lecea L, Curran T, Sotelo C, Soriano E (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18: 7779–7799

    PubMed  CAS  Google Scholar 

  • Anderson SA, Eisenstat DD, Shi L, Rubenstein JL (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278: 474–476

    Article  PubMed  CAS  Google Scholar 

  • Angevine JB, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192: 766–768

    Article  PubMed  Google Scholar 

  • Bar I, Goffinet AM (1999) Decoding the reelin signal. Nature 399: 645–646

    Article  PubMed  CAS  Google Scholar 

  • Bar I, Lambert de Rouvroit C, Krizman DB, Royaux I, Dernoncourt C, Ruelle D, Beckers MC, Goffinet AM (1995) A YAC contig containing the reeler locus with preliminary characterization of candidate gene fragments. Genomics 26: 543–549

    Article  PubMed  CAS  Google Scholar 

  • Boulder Committee (1969) Embryonic vertebrate central nervous system: revised terminology. Anat Rec 166: 257–262

    Google Scholar 

  • Caviness VJ Jr (1982) Neocortical histogenesis in normal and reeler mice: a developmental study based upon 3H-thymidine autoradiography. Dev Brain Res 4: 297–326

    Article  Google Scholar 

  • Caviness VS Jr (1976) Patterns of cell and fiber distribution in the neocortex of the reeler mutant mouse. J Comp Neurol 170: 435–448

    Article  PubMed  Google Scholar 

  • Caviness VS, Frost DO, Hayes NL (1976) Barrels in somatosensory cortex of normal and reeler mutant mice. Neurosci Lett 3: 7–14

    Article  PubMed  Google Scholar 

  • Chae T, Kwon YT, Bronson R, Dikkes P, Li E, 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  CAS  Google Scholar 

  • Cooper JA, Howell BW (1999) Lipoprotein receptors: signaling functions in the brain? Cell 97: 671–674

    Article  PubMed  CAS  Google Scholar 

  • D’Arcangelo G, Miao GG, Chen SC, Soares HD, Morgan JI, Curran T (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374: 719–723

    Article  PubMed  Google Scholar 

  • D’Arcangelo G, Nakajima K, Miyata T, Ogawa M, Mikoshiba K, Curran T (1997) Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J Neurosci 17: 23–31

    PubMed  Google Scholar 

  • de Bergeyck V, Naerhuyzen B, Goffinet AM, Lambert de Rouvroit C (1998) A panel of monoclonal antibodies against reelin, the extracellular matrix protein defective in reeler mutant mice. J Neurosci Meth 82: 17–24

    Article  Google Scholar 

  • DeCarlos JA, O’Leary DDM (1992) Growth and targeting of subplate axons and establishment of major cortical pathways. J Neurosci 1194–1211

    Google Scholar 

  • Del Rio JA, Heimrich B, Borrell V, Forster E, Drakew A, Alcantara S, Nakajima K, Miyata T,Ogawa M, Mikoshiba K, Derer P, Frotscher M, 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 

  • Derer P (1979) Evidence for the occurrence of early modifications in the ‘glia limitans’ layer of the neocortex of the reeler mutant mouse. Neurosci Lett 13: 195–202

    Article  PubMed  CAS  Google Scholar 

  • Frotscher M (1997) Dual role of Cajal-Retzius cells and reelin in cortical development. Cell Tissue Res 290: 315–322

    Article  PubMed  CAS  Google Scholar 

  • Gallagher E, Howell BW, Soriano P, Cooper JA, Hawkes R (1998) Cerebellar abnormalities in the disabled (mdabl-1) mouse. J Comp Neurol 402: 238–251

    Article  PubMed  CAS  Google Scholar 

  • Ghosh A (1997) Axons follow Reelin routes. Nature 385: 23–24

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Goffinet AM (1997) Unscrambling a disabled brain. Nature 389: 668–669

    Article  PubMed  CAS  Google Scholar 

  • Goldowitz D, Cushing RC, Laywell E, D’Arcangelo G, Sheldon M, Sweet HO, Davisson M, Steindler D, Curran T (1997) Cerebellar disorganization characteristic of reeler in scrambler mutant mice despite presence of reelin. J Neurosci 17: 8767–8776

    PubMed  CAS  Google Scholar 

  • Gonzales JL, Russo CJ, Goldowitz D, Sweet HO, Davisson MT, Walsh CA (1997) Birthdata and cell marker analysis of scrambler: a novel mutation affecting cortical development with a reeler-like phenotype. J Neurosci 17: 9204–9211

    Google Scholar 

  • Hiesberger T, Trommsdorff M, Howell BW, Goffinet A, Mumby MC, Cooper JA, 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

    Article  PubMed  CAS  Google Scholar 

  • Homayouni R, Rice DS, Sheldon M, Curran T (1999) Disabled-1 binds to the cytoplasmic domain of amyloid precursor-like protein 1. J Neurosci 19: 7507–7515

    PubMed  CAS  Google Scholar 

  • Howell BW, Gertler FB, Cooper JA (1997a) Mouse disabled (mDab1): a Src binding protein implicated in neuronal development. EMBO J 16: 121–132

    Article  PubMed  CAS  Google Scholar 

  • Howell BW, Hawkes R, Soriano P, Cooper JA (1997b) Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389: 733–737

    Article  PubMed  CAS  Google Scholar 

  • Howell BW, Herrick TM, Cooper JA (1999a) Reelin-induced tyrosine phosphorylation of disabled 1 during neuronal positioning. Genes Dev 13: 643–648

    Article  PubMed  CAS  Google Scholar 

  • Howell BW, Lanier LM, Frank R, Gertler FB, Cooper JA (1999b) The Disabled 1 PTB domain binds to the internalization signals of transmembrane glycoproteins and to phospholipids. Mol Cell Biol 19: 5179–5188

    PubMed  CAS  Google Scholar 

  • Hunter-Schaedle KE (1997) Radial glial cell development and transformation are disturbed in reeler forebrain. J Neurobiol 33: 459–472

    Article  PubMed  CAS  Google Scholar 

  • Klar A, Baldassare M, Jessell T (1992) F-spondin: a gene expressed at high levels in the floor plate encodes a secreted protein that promotes neural cell adhesion and neurite extension. Cell 69: 95–110

    Article  PubMed  CAS  Google Scholar 

  • Lambert de Rouvroit C, Goffinet AM (1998a) The reeler mouse as a model of brain development. Adv Anat Embryol Cell Biol 150: 1–108

    Article  Google Scholar 

  • Lambert de Rouvroit C, Goffinet AM (1998b) Cloning of human DAB1 and mapping to chromosome 1p31-p32. Genomics 53: 246–247

    Article  Google Scholar 

  • Lambert de Rouvroit C, de Bergeyck V, Cortvrindt C, Bar I, Eeckhout Y, Goffinet AM (1999a) Reelin, the extracellular matrix protein deficient in reeler mutant mice, is processed by a metalloproteinase. Exp Neurol 156: 214–217

    Article  Google Scholar 

  • Lambert de Rouvroit C, Bernier B, Royaux I, de Bergeyck V, Goffinet AM (1999b) Evolutionarily

    Google Scholar 

  • conserved, alternative splicing of reelin during brain development. Exp Neurol 156: 229–238 Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons

    Google Scholar 

  • derived from the forebrain subventricular zone. Neuron 11:173–189

    Google Scholar 

  • McConnell SK, Gosh A, Shatz CJ (1989) Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245: 978–982

    Article  PubMed  CAS  Google Scholar 

  • Meyer G, Goffinet AM (1998) Prenatal development of reelin-immunoreactive neurons in the human neocortex. J Comp Neurol 397: 29–40

    Article  PubMed  CAS  Google Scholar 

  • Meyer G, Soria JM, Martinez-Galan JR, Martin-Clemente B, Fairen A (1998) Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J Comp Neurol 397: 493–518

    Article  PubMed  CAS  Google Scholar 

  • Miale I, Sidman RL (1961) An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol 4: 277–296

    Article  PubMed  CAS  Google Scholar 

  • Misson JP, Austin CP, Takahashi T, Cepko CL, Caviness VS (1991) The alignment of migrating

    Google Scholar 

  • neural cells in relation to the murine neopallial radial glial fiber system. Cereb Cortex 1: 221–229 Miyata T, Nakajima K, Mikoshiba K, Ogawa M (1997) Regulation of Purkinje cell alignment by

    Google Scholar 

  • reelin as revealed with CR-50 antibody. J Neurosci 17:3599–3609

    Google Scholar 

  • Molnar Z (1998) Development of thalamocortical connections. Neuroscience intelligence unit series, RG Landes Bioscience Publishers, Austin, Texas

    Google Scholar 

  • Molnar Z, Blakemore C (1995) How do thalamic axons find their way to the cortex? Trends Neurosci 18: 389–397

    Article  PubMed  CAS  Google Scholar 

  • Molnar Z, Adams R, Goffinet AM, Blakemore C (1998) The role of the first postmitotic cortical cells in the development of thalamocortical innervation in the reeler mouse. J Neurosci 18: 5746–5765

    PubMed  CAS  Google Scholar 

  • Nakajima K, Mikoshiba K, Miyata T, Kudo C, Ogawa M (1997) Disruption of hippocampal development in vivo by CR-50 mAb against reelin. Proc Natl Acad Sci USA 94: 8196–8201

    Article  PubMed  CAS  Google Scholar 

  • Nowakowski R, Rakic P (1981) The site of origin and route and rate of migration of neurons to the hippocampal region of the rhesus monkey. J Comp Neurol 196: 129–154

    Article  PubMed  CAS  Google Scholar 

  • Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, Yamamoto H, 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

    Article  PubMed  CAS  Google Scholar 

  • Pesold C, Liu WS, Guidotti A, Costa E, Caruncho HJ (1999) Cortical bitufted, horizontal, and Martinotti cells preferentially express and secrete reelin into perineuronal nets, nonsynaptically modulating gene expression. Proc Natl Acad Sci USA 96: 3217–3222

    Article  PubMed  CAS  Google Scholar 

  • Pinto-Lord MC, Caviness VS Jr (1979) Determinants of cell shape and orientation: a comparative Golgi analysis of cell-axon interrelationships in the developing neocortex of normal and reeler mice. J Comp Neurol 187: 49–70

    Article  PubMed  CAS  Google Scholar 

  • Rice DS, Sheldon M, D’Arcangelo G, Nakajima K, Goldowitz D, 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

    PubMed  CAS  Google Scholar 

  • Royaux I, Lambert de Rouvroit C, D’Arcangelo G, Demirov D, Goffinet AM (1997) Genomic organization of the mouse reelin gene. Genomics 46: 240–250

    Article  PubMed  CAS  Google Scholar 

  • Schiffmann SN, Bernier B, Goffinet AM (1997) Reelin mRNA expression during mouse brain development. Eur J Neurosci 9: 1055–1071

    Article  PubMed  CAS  Google Scholar 

  • Sheldon M, Rice DS, D’Arcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell B, Cooper JA, Goldowitz D, Curran T (1997) Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype on mice. Nature 389: 730–733

    Article  PubMed  CAS  Google Scholar 

  • Sheppard AM, Pearlman AL (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  CAS  Google Scholar 

  • Shoukimas GM, Hinds JW (1978) The development of the cerebral cortex in the embryonic mouse: an electron microscopic serial section analysis. J Comp Neurol 179: 795–830

    Article  PubMed  CAS  Google Scholar 

  • Soriano E, Alvarado-Mallart RM, Dumesnil N, Del Rio JA, Sotelo C (1997) Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron 18: 563–577

    Article  PubMed  CAS  Google Scholar 

  • Stockinger W, Hengstschlager-Ottnad E, Novak S, Matus A, Huttinger M, Bauer J, Lassman H, Schneider WJ, Nimpf J (1998) The low density lipoprotein receptor gene family. J Biol Chem 273: 32213–32221

    Article  PubMed  CAS  Google Scholar 

  • Tan SS, Kalloniatis M, Sturm K, Tam PP, Reese BE, Faulkner-Jones B (1998) Separate progenitors for radial and tangential cell dispersion during development of the cerebral neo-cortex. Neuron 21: 295–304

    Article  PubMed  CAS  Google Scholar 

  • Trommsdorff M, Borg JP, Margolis B, Herz J (1998) Interaction of cytosolic adaptor adaptor proteins with neuronal apolipoprotein E receptors and the amyloid precursor protein. J Biol Chem 273: 33556–33560

    CAS  Google Scholar 

  • Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J (1999) Reeler/Disabled 1-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97: 689–701

    Article  PubMed  CAS  Google Scholar 

  • Van Leuven F, Thiry E, Stas L, Nelissen B (1998) Analysis of the human LRPAP1 gene coding for the lipoprotein receptor-associated protein: identification of 22 polymorphisms and one mutation. Genomics 52: 145–151

    Article  PubMed  Google Scholar 

  • Ware ML, Fox JW, Davis NM, Lambert de Rouvroit C, Russo C, Chua SC Jr, Goffinet AM, Walsh CA (1997) Aberrant splicing of a mouse disabled homolog, mDabl, in the scrambler mouse. Neuron 19: 239–249

    Article  PubMed  CAS  Google Scholar 

  • Yuasa S, Kitoh J, Kawamura K (1994) Interactions between growing thalamocortical afferent axons and the neocortical primordium in normal and reeler mutant mice. Anat Embryol 190: 137–154

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Neurobiology Unit, University of Namur School of Medicine, 61, rue de Bruxelles, B5000, Namur, Belgium

    André M. Goffinet

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  1. Isabelle Bar
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  2. Catherine Lambert de Rouvroit
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  3. André M. Goffinet
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Editors and Affiliations

  1. Neurobiology Unit, University of Namur Medical School, 61, rue de Bruxelles, B-5000, Namur, Belgium

    André M. Goffinet

  2. Section of Neurobiology, Yale University School of Medicine, 333, Cedar Street, 06510, New Haven, CT, USA

    Pasko Rakic

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© 2000 Springer-Verlag Berlin Heidelberg

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Bar, I., de Rouvroit, C.L., Goffinet, A.M. (2000). The Reelin-Signaling Pathway and Mouse Cortical Development. In: Goffinet, A.M., Rakic, P. (eds) Mouse Brain Development. Results and Problems in Cell Differentiation, vol 30. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-48002-0_11

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  • DOI: https://doi.org/10.1007/978-3-540-48002-0_11

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-53684-7

  • Online ISBN: 978-3-540-48002-0

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