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PMID: 16467525 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Impaired neuronal positioning and dendritogenesis in the neocortex after cell-autonomous Dab1 suppression.

The Journal of neuroscience : the official journal of the Society for Neuroscience ·Vol. 26 ·No. 6 ·2006-02-08 ·Pages 1767-75

Olson EC, Kim S, Walsh CA

Abstract

Reelin and Disabled 1 (Dab1) are essential for positioning migrating neurons in the developing neocortex. Cell-autonomous RNA interference-mediated suppression of Dab1 in migrating neurons destined for layer 2/3 shifted the median position of these cells to deeper positions within the cortex. At the time of migration arrest [embryonic day 20 (E20) to E21], Dab1-suppressed cells were underrepresented in the upper approximately 40 microm of the cortex compared with controls, suggesting that Dab1 is essential for somal translocation through the cell-dense cortical plate. Closer examination of the morphology of Dab1-suppressed neurons at E20 revealed simplified leading processes that are less likely to contact the marginal zone (MZ), in which high levels of Reelin are expressed. Examination of Dab1-suppressed cells 3 d later (postnatal day 2) revealed simplified dendrites that are also less likely to contact the MZ. These data reveal a cell-autonomous role of Dab1 in dendritogenesis in the neocortex and suggest that remodeling of the leading process of a migrating neuron into a nascent dendrite by Reelin/Dab1 signaling plays an important role in cell positioning.

MeSH Terms
Animals Base Sequence Cloning, Molecular DNA Primers Dendrites/physiology Electroporation Gene Expression Regulation Mice Mice, Inbred C3H Mice, Mutant Strains Molecular Sequence Data Neocortex/anatomy & histology,embryology,physiology Nerve Tissue Proteins/deficiency,genetics,physiology Neurons/physiology Polymerase Chain Reaction/methods Recombinant Fusion Proteins/metabolism Reelin Protein Signal Transduction/physiology
Chemicals
DNA Primers Dab1 protein, mouse Nerve Tissue Proteins Recombinant Fusion Proteins Reelin Protein Reln protein, mouse
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Olson Eric C
Howard Hughes Medical Institute, Beth Israel Deaconess Medical Center, Department of Neurology, Program in Neuroscience, Harvard Medical School, Boston, Massachusetts 02115, USA.
Kim Seonhee
Walsh Christopher A
References (44)
44 references, click to expand
  1. Radial glial cell development and transformation are disturbed in reeler forebrain.
    J Neurobiol. 1997 Oct;33(4):459-72 PMID: 9322161
  2. 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. 1979 Sep 1;187(1):49-69 PMID: 489778
  3. Dual origin of the mammalian neocortex and evolution of the cortical plate.
    Anat Embryol (Berl). 1978 Feb 20;152(2):109-26 PMID: 637312
  4. Birthdate and cell marker analysis of scrambler: a novel mutation affecting cortical development with a reeler-like phenotype.
    J Neurosci. 1997 Dec 1;17(23):9204-11 PMID: 9364067
  5. Obstructed neuronal migration along radial glial fibers in the neocortex of the reeler mouse: a Golgi-EM analysis.
    Brain Res. 1982 Aug;256(4):379-93 PMID: 7127145
  6. Localization of ApoER2, VLDLR and Dab1 in radial glia: groundwork for a new model of reelin action during cortical development.
    Brain Res Dev Brain Res. 2003 Feb 16;140(2):195-203 PMID: 12586425
  7. Mouse disabled (mDab1): a Src binding protein implicated in neuronal development.
    EMBO J. 1997 Jan 2;16(1):121-32 PMID: 9009273
  8. Neuronal position in the developing brain is regulated by mouse disabled-1.
    Nature. 1997 Oct 16;389(6652):733-7 PMID: 9338785
  9. disabled-1 functions cell autonomously during radial migration and cortical layering of pyramidal neurons.
    J Neurosci. 2001 Nov 15;21(22):8798-808 PMID: 11698592
  10. Reelin signaling directly affects radial glia morphology and biochemical maturation.
    Development. 2003 Oct;130(19):4597-609 PMID: 12925587
  11. Aberrant splicing of a mouse disabled homolog, mdab1, in the scrambler mouse.
    Neuron. 1997 Aug;19(2):239-49 PMID: 9292716
  12. Identification of major cell classes in the developing mammalian nervous system.
    J Neurosci. 1985 Dec;5(12):3310-28 PMID: 4078630
  13. Scrambler, a new neurological mutation of the mouse with abnormalities of neuronal migration.
    Mamm Genome. 1996 Nov;7(11):798-802 PMID: 8875886
  14. Motility and cytoskeletal organization of migrating cerebellar granule neurons.
    J Neurosci. 1995 Feb;15(2):981-9 PMID: 7869123
  15. Architectonic and hodological organization of the cerebellum in reeler mutant mice.
    Brain Res. 1984 Nov;318(2):263-76 PMID: 6498501
  16. Disruption of neuronal migration and radial glia in the developing cerebral cortex following ablation of Cajal-Retzius cells.
    Cereb Cortex. 2000 Jun;10(6):602-13 PMID: 10859138
  17. Abundant GFP expression and LTP in hippocampal acute slices by in vivo injection of sindbis virus.
    J Neurophysiol. 2001 Aug;86(2):1037-42 PMID: 11495971
  18. Two new mutants, 'trembler' and 'reeler', with neurological actions in the house mouse (Mus musculus L.).
    J Genet. 1951 Jan;50(2):192-201 PMID: 24539699
  19. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2.
    Cell. 1999 Jun 11;97(6):689-701 PMID: 10380922
  20. Reelin binds alpha3beta1 integrin and inhibits neuronal migration.
    Neuron. 2000 Jul;27(1):33-44 PMID: 10939329
  21. Rescue of ataxia and preplate splitting by ectopic expression of Reelin in reeler mice.
    Neuron. 2002 Feb 14;33(4):573-86 PMID: 11856531
  22. Neurons tend to stop migration and differentiate along the cortical internal plexiform zones in the Reelin signal-deficient mice.
    J Neurosci Res. 2002 Sep 15;69(6):723-30 PMID: 12205665
  23. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations.
    Nat Genet. 2000 Sep;26(1):93-6 PMID: 10973257
  24. Electroporation and RNA interference in the rodent retina in vivo and in vitro.
    Proc Natl Acad Sci U S A. 2004 Jan 6;101(1):16-22 PMID: 14603031
  25. Disabled-1-regulated adhesion of migrating neurons to radial glial fiber contributes to neuronal positioning during early corticogenesis.
    Neuron. 2004 Apr 22;42(2):197-211 PMID: 15091337
  26. Three-dimensional structural organization of layer I of the human cerebral cortex: a Golgi study.
    J Comp Neurol. 1990 Sep 1;299(1):89-105 PMID: 2212113
  27. Reelin is a ligand for lipoprotein receptors.
    Neuron. 1999 Oct;24(2):471-9 PMID: 10571240
  28. The cerebral cortex of the reeler mouse embryo. An electron microscopic analysis.
    Anat Embryol (Berl). 1980;159(2):199-210 PMID: 7447037
  29. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation.
    Neuron. 1999 Oct;24(2):481-9 PMID: 10571241
  30. Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway.
    Neuron. 2004 Jan 8;41(1):71-84 PMID: 14715136
  31. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice.
    Nature. 1997 Oct 16;389(6652):730-3 PMID: 9338784
  32. Diverse migratory pathways in the developing cerebral cortex.
    Science. 1992 Oct 9;258(5080):299-302 PMID: 1411527
  33. Time of origin or corresponding cell classes in the cerebral cortex of normal and reeler mutant mice: an autoradiographic analysis.
    J Comp Neurol. 1973 Mar 15;148(2):141-51 PMID: 4700506
  34. Transcriptional regulation of cortical neuron migration by POU domain factors.
    Science. 2002 Feb 22;295(5559):1528-32 PMID: 11859196
  35. Identification of radial glial cells within the developing murine central nervous system: studies based upon a new immunohistochemical marker.
    Brain Res Dev Brain Res. 1988 Nov 1;44(1):95-108 PMID: 3069243
  36. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex.
    J Comp Neurol. 2004 Nov 8;479(2):168-80 PMID: 15452856
  37. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler.
    Nature. 1995 Apr 20;374(6524):719-23 PMID: 7715726
  38. Reelin-induced tyrosine [corrected] phosphorylation of disabled 1 during neuronal positioning.
    Genes Dev. 1999 Mar 15;13(6):643-8 PMID: 10090720
  39. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex.
    Neuroscience. 2001;103(4):865-72 PMID: 11301197
  40. Human CCAAT displacement protein is homologous to the Drosophila homeoprotein, cut.
    Nat Genet. 1992 Apr;1(1):50-5 PMID: 1301999
  41. Two modes of radial migration in early development of the cerebral cortex.
    Nat Neurosci. 2001 Feb;4(2):143-50 PMID: 11175874
  42. Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall.
    J Neurosci. 1999 Dec 1;19(23):10357-71 PMID: 10575033
  43. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons.
    Neuron. 1999 Jun;23(2):257-71 PMID: 10399933
  44. Axonal secretion of Reelin by Cajal-Retzius cells: evidence from comparison of normal and Reln(Orl) mutant mice.
    J Comp Neurol. 2001 Nov 12;440(2):136-43 PMID: 11745613
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
DOI
10.1523/JNEUROSCI.3000-05.2006
Published
2006-02-08
Pages
1767-75
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6793623
Subset
IM
Grants
NINDS NIH HHS · P01 NS40043 · United States
External Links
PubMed source DOI: 10.1523/JNEUROSCI.3000-05.2006 PMC Full Text View journal details
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