How does Reelin control neuronal migration and layer formation in the developing mammalian neocortex?

Neuroscience Research

Volumn 86, Issue , 2014, Pages 50-58

  Sekine, Katsutoshi ^a   Kubo, Ken Ichiro ^a   Nakajima, Kazunori ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cell adhesion molecules; Dab1; Inside out; Primitive cortical zone; Reelin; Terminal translocation

Indexed keywords

AFADIN; CULLIN5; DAB1 PROTEIN; NECTIN; NERVE CELL ADHESION MOLECULE; PROTEIN; RBX2 PROTEIN; REELIN; SOCS7 PROTEIN; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5; NERVE PROTEIN; REELIN PROTEIN; SCLEROPROTEIN; SERINE PROTEINASE;

BIRTH; BRAIN CORTEX; BRAIN NERVE CELL; CELL ADHESION; CELL AGGREGATION; CELL MIGRATION; CELL POLARITY; GENE EXPRESSION REGULATION; HUMAN; LOCOMOTION; NEOCORTEX; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SIGNAL TRANSDUCTION; ANATOMY AND HISTOLOGY; ANIMAL; CELL MOTION; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; MAMMAL; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL MOVEMENT; EXTRACELLULAR MATRIX PROTEINS; HUMANS; MAMMALS; NEOCORTEX; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION;

EID: 84912535199     PISSN: 01680102     EISSN: 18728111     Source Type: Journal    
DOI: 10.1016/j.neures.2014.06.004     Document Type: Review

References (60)

1. Ajioka I., Nakajima K. Birth-date-dependent segregation of the mouse cerebral cortical neurons in reaggregation cultures. Eur. J. Neurosci. 2005, 22(2):331-342.
2. Arnaud L., Ballif B.A., Cooper J.A. Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol. Cell. Biol. 2003, 23(24):9293-9302.
3. Ayala R., Shu T., Tsai L.H. Trekking across the brain: the journey of neuronal migration. Cell 2007, 128(1):29-43.
4. Ballif B.A., Arnaud L., Arthur W.T., Guris D., Imamoto A., Cooper J.A. Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Curr. Biol. 2004, 14(7):606-610.
5. Britto J.M., Tait K.J., Johnston L.A., Hammond V.E., Kalloniatis M., Tan S.S. Altered speeds and trajectories of neurons migrating in the ventricular and subventricular zones of the reeler neocortex. Cereb. Cortex 2011, 21:1018-1027.
6. Caviness V.S., Rakic P. Mechanisms of cortical development: a view from mutations in mice. Annu. Rev. Neurosci. 1978, 1:297-326.
7. Caviness V.S., Sidman R.L. Time of origin or corresponding cell classes in the cerebral cortex of normal and reeler mutant mice: an autoradiographic analysis. J. Comp. Neurol. 1973, 148(2):141-151.
8. Chai X., Forster E., Zhao S., Bock H.H., Frotscher M. Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n-cofilin phosphorylation at serine3. J. Neurosci. 2009, 29(1):288-299.
9. D'Arcangelo G., Homayouni R., Keshvara L., Rice D.S., Sheldon M., Curran T. Reelin is a ligand for lipoprotein receptors. Neuron 1999, 24(2):471-479.
10. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 1995, 374(6524):719-723.
11. Dulabon L., Olson E.C., Taglienti M.G., Eisenhuth S., McGrath B., Walsh C.A., Kreidberg J.A., Anton E.S. Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron 2000, 27(1):33-44.
12. Feng L., Allen N.S., Simo S., Cooper J.A. Cullin 5 regulates Dab1 protein levels and neuron positioning during cortical development. Genes Dev. 2007, 21(21):2717-2730.
13. Franco S.J., Martinez-Garay I., Gil-Sanz C., Harkins-Perry S.R., Muller U. Reelin regulates cadherin function via Dab1/Rap1 to control neuronal migration and lamination in the neocortex. Neuron 2011, 69(3):482-497.
14. Gil-Sanz C., Franco S.J., Martinez-Garay I., Espinosa A., Harkins-Perry S., Muller U. Cajal-Retzius cells instruct neuronal migration by coincidence signaling between secreted and contact-dependent guidance cues. Neuron 2013, 79:461-477.
15. Hack I., Hellwig S., Junghans D., Brunne B., Bock H.H., Zhao S., Frotscher M. Divergent roles of ApoER2 and Vldlr in the migration of cortical neurons. Development 2007, 134(21):3883-3891.
16. Hiesberger T., Trommsdorff M., Howell B.W., Goffinet A., Mumby M.C., Cooper J.A., Herz J. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 1999, 24(2):481-489.
17. Hong S.E., Shugart Y.Y., Huang D.T., Shahwan S.A., Grant P.E., Hourihane J.O., Martin N.D., Walsh C.A. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat. Genet. 2000, 26(1):93-96.
18. Howell B.W., Hawkes R., Soriano P., Cooper J.A. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 1997, 389(6652):733-737.
19. Jossin Y., Cooper J.A. Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat. Neurosci. 2011, 14(6):697-703.
20. Jossin Y., Ignatova N., Hiesberger T., Herz J., Lambert de Rouvroit C., Goffinet A.M. The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J. Neurosci. 2004, 24(2):514-521.
21. Kawauchi T., Sekine K., Shikanai M., Chihama K., Tomita K., Kubo K., Nakajima K., Nabeshima Y., Hoshino M. Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron 2010, 67(4):588-602.
22. Kojima T., Nakajima K., Mikoshiba K. The disabled 1 gene is disrupted by a replacement with L1 fragment in yotari mice. Brain Res. Mol. Brain Res. 2000, 75(1):121-127.
23. Kubo K., Honda T., Tomita K., Sekine K., Ishii K., Uto A., Kobayashi K., Tabata H., Nakajima K. Ectopic Reelin induces neuronal aggregation with a normal birthdate-dependent "inside-out" alignment in the developing neocortex. J. Neurosci. 2010, 30(33):10953-10966.
24. Kuo G., Arnaud L., Kronstad-O'Brien P., Cooper J.A. Absence of Fyn and Src causes a reeler-like phenotype. J. Neurosci. 2005, 25(37):8578-8586.
25. Luque J.M., Morante-Oria J., Fairen A. 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, 140(2):195-203.
26. Maeda T.T., Ajioka I., Nakajima K. Computational cell model based on autonomous cell movement regulated by cell-cell signalling successfully recapitulates the "inside and outside" pattern of cell sorting. BMC Syst. Biol. 2007, 1:43.
27. Magdaleno S., Keshvara L., Curran T. Rescue of ataxia and preplate splitting by ectopic expression of Reelin in reeler mice. Neuron 2002, 33(4):573-586.
28. Marin O., Valiente M., Ge X., Tsai L.H. Guiding neuronal cell migrations. Cold Spring Harb. Perspect. Biol. 2010, 2(2):a001834.
29. Meyer G., Soria J.M., Martinez-Galan J.R., Martin-Clemente B., Fairen A. Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex. J. Comp. Neurol. 1998, 397(4):493-518.
30. Molnar Z., Metin C., Stoykova A., Tarabykin V., Price D.J., Francis F., Meyer G., Dehay C., Kennedy H. Comparative aspects of cerebral cortical development. Eur. J. Neurosci. 2006, 23(4):921-934.
31. Morimura T., Ogawa M. Relative importance of the tyrosine phosphorylation sites of Disabled-1 to the transmission of Reelin signaling. Brain Res. 2009, 1304:26-37.
32. Nadarajah B., Brunstrom J.E., Grutzendler J., Wong R.O., Pearlman A.L. Two modes of radial migration in early development of the cerebral cortex. Nat. Neurosci. 2001, 4(2):143-150.
33. Nomura T., Takahashi M., Hara Y., Osumi N. Patterns of neurogenesis and amplitude of Reelin expression are essential for making a mammalian-type cortex. PLoS ONE 2008, 3(1):e1454.
34. Ogawa M., Miyata T., Nakajima K., Yagyu K., Seike M., Ikenaka K., Yamamoto H., Mikoshiba K. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 1995, 14(5):899-912.
35. Olson E.C., Kim S., Walsh C.A. Impaired neuronal positioning and dendritogenesis in the neocortex after cell-autonomous Dab1 suppression. J. Neurosci. 2006, 26(6):1767-1775.
36. Park T.J., Curran T. Crk and Crk-like play essential overlapping roles downstream of disabled-1 in the Reelin pathway. J. Neurosci. 2008, 28(50):13551-13562.
37. Rakic P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 1972, 145(1):61-83.
38. Rakic P. Evolution of the neocortex: a perspective from developmental biology. Nat. Rev. Neurosci. 2009, 10(10):724-735.
39. Rice D.S., Curran T. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 2001, 24:1005-1039.
40. Sanada K., Gupta A., Tsai L.H. Disabled-1-regulated adhesion of migrating neurons to radial glial fiber contributes to neuronal positioning during early corticogenesis. Neuron 2004, 42(2):197-211.
41. Sekine K., Honda T., Kawauchi T., Kubo K., Nakajima K. The outermost region of the developing cortical plate is crucial for both the switch of the radial migration mode and the dab1-dependent "inside-out" lamination in the neocortex. J. Neurosci. 2011, 31(25):9426-9439.
42. Sekine K., Kawauchi T., Kubo K., Honda T., Herz J., Hattori M., Kinashi T., Nakajima K. Reelin controls neuronal positioning by promoting cell-matrix adhesion via inside-out activation of Integrin alpha 5 beta 1. Neuron 2012, 76:353-369.
43. Sheldon M., Rice D.S., D'Arcangelo G., Yoneshima H., Nakajima K., Mikoshiba K., Howell B.W., Cooper J.A., Goldowitz D., Curran T. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 1997, 389(6652):730-733.
44. Simo S., Cooper J.A. Rbx2 regulates neuronal migration through different Cullin 5-RING ligase adaptors. Dev. Cell 2013, 27(4):399-411.
45. Simo S., Jossin Y., Cooper J.A. Cullin 5 regulates cortical layering by modulating the speed and duration of Dab1-dependent neuronal migration. J. Neurosci. 2010, 30(16):5668-5676.
46. Tabata H., Kanatani S., Nakajima K. Differences of migratory behavior between direct progeny of apical progenitors and basal progenitors in the developing cerebral cortex. Cereb. Cortex 2009, 19(9):2092-2105.
47. Tabata H., Nakajima K. 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):865-872.
48. 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(6):723-730.
49. Tabata H., Nakajima K. Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J. Neurosci. 2003, 23(31):9996-10001.
50. Tachikawa K., Sasaki S., Maeda T., Nakajima K. Identification of molecules preferentially expressed beneath the marginal zone in the developing cerebral cortex. Neurosci. Res. 2008, 60(2):135-146.
51. Tissir F., Goffinet A.M. Reelin and brain development. Nat. Rev. Neurosci. 2003, 4(6):496-505.
52. Torii M., Hashimoto-Torii K., Levitt P., Rakic P. Integration of neuronal clones in the radial cortical columns by EphA and ephrin-A signalling. Nature 2009, 461(7263):524-528.
53. Trommsdorff M., Gotthardt M., Hiesberger T., Shelton J., Stockinger W., Nimpf J., Hammer R.E., Richardson J.A., Herz J. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 1999, 97(6):689-701.
54. Uchida T., Baba A., Perez-Martinez F.J., Hibi T., Miyata T., Luque J.M., Nakajima K., Hattori M. Downregulation of functional Reelin receptors in projection neurons implies that primary Reelin action occurs at early/premigratory stages. J. Neurosci. 2009, 29(34):10653-10662.
55. Voss A.K., Britto J.M., Dixon M.P., Sheikh B.N., Collin C., Tan S.S., Thomas T. C3G regulates cortical neuron migration, preplate splitting and radial glial cell attachment. Development 2008, 135(12):2139-2149.
56. Ware M.L., Fox J.W., Gonzalez J.L., Davis N.M., Lambert de Rouvroit C., Russo C.J., Chua S.C., Goffinet A.M., Walsh C.A. Aberrant splicing of a mouse disabled homolog, mdab1, in the scrambler mouse. Neuron 1997, 19(2):239-249.
57. Weber G.F., Bjerke M.A., DeSimone D.W. Integrins and cadherins join forces to form adhesive networks. J. Cell Sci. 2011, 124:1183-1193.
58. Yano M., Hayakawa-Yano Y., Mele A., Darnell R.B. Nova2 regulates neuronal migration through an RNA switch in disabled-1 signaling. Neuron 2010, 66(6):848-858.
59. Yoneshima H., Nagata E., Matsumoto M., Yamada M., Nakajima K., Miyata T., Ogawa M., Mikoshiba K. A novel neurological mutant mouse, yotari, which exhibits reeler-like phenotype but expresses CR-50 antigen/reelin. Neurosci. Res. 1997, 29(3):217-223.
60. Yoshida M., Assimacopoulos S., Jones K.R., Grove E.A. Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 2006, 133(3):537-545.