Role for Reelin in stabilizing cortical architecture

Trends in Neurosciences

Volumn 33, Issue 9, 2010, Pages 407-414

  Frotscher, Michael ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; COFILIN; NOTCH RECEPTOR; REELIN;

BRAIN DEVELOPMENT; CYTOSKELETON; EPILEPSY; HUMAN; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REVIEW; SCHIZOPHRENIA;

ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL MOVEMENT; CEREBRAL CORTEX; CYTOSKELETON; EPILEPSY; EXTRACELLULAR MATRIX PROTEINS; HUMANS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEURONS; RECEPTORS, NOTCH; SCHIZOPHRENIA; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 77956010349     PISSN: 01662236     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tins.2010.06.001     Document Type: Review

References (91)

1. D'Arcangelo G., et al. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995, 374:719-723.
2. Rakic P., Caviness V.S. Cortical development: view from neurological mutants two decades later. Neuron 1995, 14:1101-1104.
3. Rice D.S., Curran T. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 2001, 24:1005-1039.
4. Tissir F., Goffinet A.M. Reelin and brain development. Nat. Rev. Neurosci. 2003, 4:496-505.
5. Soriano E., Del Rio J.A. The cells of Cajal-Retzius: still a mystery one century after. Neuron 2005, 46:389-394.
6. Förster E., et al. Laminating the hippocampus. Nat. Rev. Neurosci. 2006, 7:259-267.
7. Cooper J.A. A mechanism for inside-out lamination in the neocortex. Trends Neurosci. 2008, 31:113-119.
8. Yip J.W., et al. Reelin controls position of autonomic neurons in the spinal cord. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:8612-8616.
9. Förster E., et al. Emerging topics in Reelin function. Eur. J. Neurosci. 2010, 31:1511-1518.
10. Falconer D.S. Two new mutants " Trembler" and " Reeler" , with neurological actions in the house mouse (Mus Musculus L.). J. Genet. 1951, 50:192-201.
11. Caviness V.S., Rakic P. Mechanisms of cortical development: a view from mutations in mice. Annu. Rev. Neurosci. 1978, 1:297-326.
12. Stanfield B.B., Cowan W.M. The morphology of the hippocampus and dentate gyrus in normal and reeler mice. J. Comp. Neurol. 1979, 185:393-422.
13. Curran T., D'Arcangelo G. Role of reelin in the control of brain development. Brain Res. Brain Res. Rev. 1998, 26:285-294.
14. Drakew A., et al. Dentate granule cells in reeler mutants and VLDLR and ApoER2 knockout mice. Exp. Neurol. 2002, 176:12-24.
15. D'Arcangelo G., et al. Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody. J. Neurosci. 1997, 17:23-31.
16. Frotscher M. Dual role of Cajal-Retzius cells and reelin in cortical development. Cell Tissue Res. 1997, 290:315-322.
17. Frotscher M. Cajal-Retzius cells, Reelin, and the formation of layers. Curr. Opin. Neurobiol. 1998, 8:570-575.
18. Angevine J.B., Sidman R.L. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 1961, 192:766-768.
19. Berry M., Rogers A.W. The migration of neuroblasts in the developing cerebral cortex. J. Anat. 1965, 99:691-709.
20. Nadarajah B., et al. Two modes of radial migration in early development of the cerebral cortex. Nat. Neurosci. 2001, 4:143-150.
21. Nadarajah B., Parnavelas J. Modes of neuronal migration in the developing cerebral cortex. Nat. Rev. Neurosci. 2002, 3:423-432.
22. Miyata T., Ogawa M. Twisting of neocortical progenitor cells underlies a spring-like mechanism for daughter-cell migration. Curr. Biol. 2007, 17:146-151.
23. Olson E.C., et al. Impaired neuronal positioning and dendritogenesis in the neocortex after cell-autonomous Dab1 suppression. J. Neurosci. 2006, 26:1767-1775.
24. Landrieu P., Goffinet A. Inverted pyramidal neurons and their axons in the neocortex of reeler mutant mice. Cell Tissue Res. 1981, 218:293-301.
25. Terashima T., et al. Distribution and morphology of callosal commissural neurons within the motor cortex of normal and reeler mice. J. Comp. Neurol. 1985, 232:83-98.
26. Terashima T., et al. Dendritic arborization of large pyramidal neurons in the motor cortex of normal and reeler mutant mouse. Okajimas Folia Anat. Jpn. 1992, 68:351-363.
27. Trommsdorff M., et al. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 1999, 97:689-701.
28. Hiesberger T., et al. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 1999, 24:481-489.
29. Howell B.W., et al. Reelin-induced tyrosine phosphorylation of disabled 1 during neuronal positioning. Genes Dev. 1999, 13:643-648.
30. Bock H.H., et al. 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.
31. Beffert U., et al. Reelin-mediated signaling locally regulates protein kinase B/Akt and glycogen synthase kinase 3beta. J. Biol. Chem. 2002, 277:49958-49964.
32. Howell B.W., et al. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 1997, 389:733-737.
33. Sheldon M., et al. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 1997, 389:730-733.
34. Ware M.L., et al. Aberrant splicing of a mouse disabled homolog, mdab1, in the scrambler mouse. Neuron 1997, 19:239-249.
35. Lambert de Rouvroit C., Goffinet A.M. The reeler mouse as a model of brain development. Adv. Anat. Embryol. Cell Biol. 1998, 150:1-106.
36. Hong S.E., et al. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat. Genet. 2000, 26:93-96.
37. Zaki M., et al. Identification of a novel recessive RELN mutation using a homozygous balanced reciprocal translocation. Am. J. Med. Genet. A 2007, 143A:939-944.
38. Impagnatiello F., et al. A decrease of reelin expression as a putative vulnerability factor in schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:15718-15723.
39. Fatemi S.H. The role of reelin in pathology of autism. Mol. Psychiatry 2002, 7:919-920.
40. Fatemi S.H., et al. Reduction in reelin immunoreactivity in hippocampus of subjects with schizophrenia, bipolar disorder and major depression. Mol. Psychiatry 2000, 5:654-663.
41. Botella-Lopez A., et al. Reelin expression and glycosylation patterns are altered in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5573-5578.
42. Beffert U., et al. Modulation of synaptic plasticity and memory by Reelin involves differential splicing of the lipoprotein receptor Apoer2. Neuron 2005, 47:567-579.
43. Durakoglugil M.S., et al. Reelin signaling antagonizes beta-amyloid at the synapse. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:15938-15943.
44. Drakew A., et al. Developmental distribution of a reeler gene-related antigen in the rat hippocampal formation visualized by CR-50 immunocytochemistry. Neuroscience 1998, 82:1079-1086.
45. Pesold C., et al. Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:3221-3226.
46. Alcantara S., et al. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci. 1998, 18:7779-7799.
47. Ramos-Moreno T., et al. Extracellular matrix molecules and synaptic plasticity: immunomapping of intracellular and secreted Reelin in the adult rat brain. Eur. J. Neurosci. 2006, 23:401-422.
48. Hack I., et al. Divergent roles of ApoER2 and Vldlr in the migration of cortical neurons. Development 2007, 134:3883-3891.
49. Bamburg J.R. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 1999, 15:185-230.
50. Heng J.I., et al. Molecular layers underlying cytoskeletal remodelling during cortical development. Trends Neurosci. 2010, 33:38-47.
51. Arber S., et al. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 1998, 393:805-809.
52. Yang N., et al. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 1998, 393:809-812.
53. Chai X., et al. Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n-cofilin phosphorylation at serine3. J. Neurosci. 2009, 29:288-299.
54. Bock H.H., Herz J. Reelin activates SRC family tyrosine kinases in neurons. Curr. Biol. 2003, 13:18-26.
55. Dulabon L., et al. Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron 2000, 27:33-44.
56. Sanada K., et al. Disabled-1-regulated adhesion of migrating neurons to radial glial fiber contributes to neuronal positioning during early corticogenesis. Neuron 2004, 42:197-211.
57. Feng L., et al. Cullin 5 regulates Dab1 protein levels and neuron positioning during cortical development. Genes Dev. 2007, 21:2717-2730.
58. Causeret F., et al. The p21-activated kinase is required for neuronal migration in the cerebral cortex. Cerebral Cortex 2009, 19:861-875.
59. Yoon K., Gaiano N. Notch signaling in the mammalian central nervous system: insights from mouse mutants. Nat. Neurosci. 2005, 8:709-715.
60. Louvi A., Artavanis-Tsakonas S. Notch signalling in vertebrate neural development. Nat. Rev. Neurosci. 2006, 7:93-102.
61. Sestan N., et al. Contact-dependent inhibition of cortical neurite growth mediated by Notch signaling. Science 1999, 286:741-746.
62. Hashimoto-Torii K., et al. Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 2008, 60:273-284.
63. Sibbe M., et al. Reelin and Notch1 cooperate in the development of the dentate gyrus. J. Neurosci. 2009, 29:8578-8585.
64. Houser C.R. Granule cell dispersion in the dentate gyrus of humans with temporal lobe epilepsy. Brain Res. 1990, 535:195-204.
65. Haas C.A., et al. Role for reelin in the development of granule cell dispersion in temporal lobe epilepsy. J. Neurosci. 2002, 22:5797-5802.
66. Bouilleret V., et al. Recurrent seizures and hippocampal sclerosis following intrahippocampal kainate injection in adult mice: electroencephalography, histopathology and synaptic reorganization similar to mesial temporal lobe epilepsy. Neuroscience 1999, 89:717-729.
67. Heinrich C., et al. Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J. Neurosci. 2006, 26:4701-4713.
68. Müller M.C., et al. Exogenous reelin prevents granule cell dispersion in experimental epilepsy. Exp. Neurol. 2009, 216:390-397.
69. Jessell T.M., Kandel E.R. Synaptic transmission: a bidirectional and self-modifiable form of cell-cell communication. Cell 72/Neuron 1993, 10:S1-30.
70. Bailey C.H., Kandel E.R. Structural changes accompanying memory storage. Annu. Rev. Physiol. 1993, 55:397-426.
71. Yuste R., Bonhoeffer T. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 2001, 24:1071-1089.
72. Geinisman Y. Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cerebral Cortex 2000, 10:952-962.
73. Matsuzaki M., et al. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
74. Harris K.M., et al. Structural changes at dendritic spine synapses during long-term potentiation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358:745-748.
75. DeBello W. Micro-rewiring as a substrate for learning. Trends Neurosci. 2008, 31:577-584.
76. Holtmaat A., Svoboda K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 2009, 10:647-658.
77. Hofer S.B., et al. Experience leaves a lasting structural trace in cortical circuits. Nature 2009, 457:313-317.
78. Yang G., et al. Stably maintained dendritic spines are associated with lifelong memories. Nature 2009, 462:920-924.
79. Kobow K., et al. Increased Reelin promoter methylation is associated with granule cell dispersion in human temporal lobe epilepsy. J. Neuropathol. Exp. Neurol. 2009, 68:356-364.
80. Lendvai B., et al. Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 2000, 404:876-881.
81. Trachtenberg J.T., et al. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002, 420:788-794.
82. Zuo Y., et al. Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 2005, 46:181-189.
83. Stettler D.D., et al. Axons and synaptic boutons are highly dynamic in adult visual cortex. Neuron 2006, 49:877-887.
84. Holtmaat A., et al. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 2006, 441:979-983.
85. Meyer-Luehmann M., et al. Rapid appearance and local toxicity of amyloid plaques in a mouse model of Alzheimer's disease. Nature 2008, 451:720-724.
86. Spires T.L., et al. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J. Neurosci. 2005, 25:7278-7287.
87. Yang G., et al. Thinned-skull cranial window technique for long-term imaging of the cortex in live mice. Nat. Protoc. 2010, 5:201-208.
88. Duit S., et al. Differential functions of ApoER2 and very low density lipoprotein receptor in Reelin signaling depend on differential sorting of the receptors. J. Biol. Chem. 2010, 285:4896-4908.
89. Studer D., et al. A new approach for cryofixation by high-pressure freezing. J. Microsc. 2001, 203:285-294.
90. Rostaing P., et al. Analysis of synaptic ultrastructure without fixative using high-pressure freezing and tomography. Eur. J. Neurosci. 2006, 24:3463-3473.
91. Frotscher M., et al. New ways of looking at synapses. Histochem. Cell Biol. 2007, 128:91-96.