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

Journal of Neuroscience

Volumn 31, Issue 25, 2011, Pages 9426-9439

  Sekine, Katsutoshi ^a   Honda, Takao ^a   Kawauchi, Takeshi ^a,b   Kubo, Ken ichiro ^a   Nakajima, Kazunori ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DISABLED HOMOLOG 1; GLYCOPROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL MIGRATION; CELL TRANSPORT; CONTROLLED STUDY; EMBRYO; FEMALE; MALE; MOUSE; NEOCORTEX; NONHUMAN; PRIMITIVE CORTICAL ZONE; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; CELL MOVEMENT; MICE; MICE, INBRED ICR; MORPHOGENESIS; NEOCORTEX; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS;

EID: 79959675087     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0650-11.2011     Document Type: Article

References (58)

1. Ajioka I, Nakajima K (2005) Birth-date-dependent segregation of the mouse cerebral cortical neurons in reaggregation cultures. Eur J Neurosci 22:331-342.
2. Bar I, Lambert de Rouvroit C, Goffinet AM (2000) The evolution of cortical development. An hypothesis based on the role of the Reelin signaling pathway. Trends Neurosci 23:633-638.
3. Caviness VS Jr, Rakic P (1978) Mechanisms of cortical development: a view from mutations in mice. Annu Rev Neurosci 1:297-326.
4. Caviness VS Jr, Sidman RL (1973) Time of origin or corresponding cell classes in the cerebral cortex of normal and reeler mutant mice: an autoradiographic analysis. J Comp Neurol 148:141-151.
5. Chai X, Förster E, Zhao S, Bock HH, Frotscher M (2009) Reelin stabilizes the actin cytoskeleton of neuronal processes by inducing n-cofilin phosphorylation at serine3. J Neurosci 29:288-299.
6. Cooper JA (2008) A mechanism for inside-out lamination in the neocortex. Trends Neurosci 31:113-119.
7. 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.
8. Feng L, Cooper JA (2009) Dual functions of Dab1 during brain development. Mol Cell Biol 29:324-332.
9. Feng L, Allen NS, Simo S, Cooper JA (2007) Cullin 5 regulates Dab1 protein levels and neuron positioning during cortical development. Genes Dev 21:2717-2730.
10. Franco SJ, Martinez-Garay I, Gil-Sanz C, Harkins-Perry SR, Müller U (2011) Reelin regulates cadherin function via Dab1/Rap1 to control neuronal migration and lamination in the neocortex. Neuron 69:482-497.
11. Gal JS, Morozov YM, Ayoub AE, Chatterjee M, Rakic P, Haydar TF (2006) Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J Neurosci 26:1045-1056.
12. Gloster A, Wu W, Speelman A, Weiss S, Causing C, Pozniak C, Reynolds B, Chang E, Toma JG, Miller FD (1994) The Tα1α-tubulin promoter specifies gene expression as a function of neuronal growth and regeneration in transgenic mice. J Neurosci 14:7319-7330.
13. Goffinet AM (1979) An early development defect in the cerebral cortex of the reeler mouse. A morphological study leading to a hypothesis concerning the action of the mutant gene. Anat Embryol (Berl) 157:205-216.
14. Hammond V, Howell B, Godinho L, Tan SS (2001) disabled-1 functions cell autonomously during radial migration and cortical layering of pyramidal neurons. J Neurosci 21:8798-8808.
15. Hartfuss E, Förster E, Bock HH, Hack MA, Leprince P, Luque JM, Herz J, Frotscher M, Götz M (2003) Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130:4597-4609.
16. Hashimoto-Torii K, Torii M, Sarkisian MR, Bartley CM, Shen J, Radtke F, Gridley T, Sestan N, Rakic P (2008) Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 60:273-284.
17. Hatanaka Y, Hisanaga S, Heizmann CW, Murakami F (2004) Distinct migratory behavior of early- and late-born neurons derived from the cortical ventricular zone. J Comp Neurol 479:1-14.
18. Honda T, Nakajima K (2006) Mouse Disabled1 (DAB1) is a nucleocytoplasmic shuttling protein. J Biol Chem 281:38951-38965.
19. Howell BW, Hawkes R, Soriano P, Cooper JA (1997) Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389:733-737.
20. Kawauchi T, Hoshino M (2008) Molecular pathways regulating cytoskeletal organization and morphological changes in migrating neurons. Dev Neurosci 30:36-46.
21. Kojima T, Nakajima K, Mikoshiba K (2000) The disabled 1 gene is disrupted by a replacement with L1 fragment in yotari mice. Brain Res Mol Brain Res 75:121-127.
22. Kubo K, Honda T, Tomita K, Sekine K, Ishii K, Uto A, Kobayashi K, Tabata H, Nakajima K (2010a) Ectopic Reelin induces neuronal aggregation with a normal birthdate-dependent "inside-out" alignment in the developing neocortex. J Neurosci 30:10953-10966.
23. Kubo K, Tomita K, Uto A, Kuroda K, Seshadri S, Cohen J, Kaibuchi K, Kamiya A, Nakajima K (2010b) Migration defects by DISC1 knockdown in C57BL/6, 129X1/SvJ, and ICR strains via in utero gene transfer and virus-mediated RNAi. Biochem Biophys Res Commun 400:631-637.
24. Luque JM, Morante-Oria J, Fairén A (2003) 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 140:195-203.
25. Marín-Padilla M (1998) Cajal-Retzius cells and the development of the neocortex. Trends Neurosci 21:64-71.
26. Marín Padilla M (2001) The evolution of the structure of the neocortex in mammals: a new theory of cytoarchitecture (in Spanish). Rev Neurol 33:843-853.
27. Meyer G, Soria JM, Martínez-Galán JR, Martín-Clemente B, Fairén 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.
28. Molnár Z, Métin C, Stoykova A, Tarabykin V, Price DJ, Francis F, Meyer G, Dehay C, Kennedy H (2006) Comparative aspects of cerebral cortical development. Eur J Neurosci 23:921-934.
29. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8:427-437.
30. Morimura T, Ogawa M (2009) Relative importance of the tyrosine phosphorylation sites of Disabled-1 to the transmission of Reelin signaling. Brain Res 1304:26-37.
31. Mullen RJ, Buck CR, Smith AM (1992) NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
32. Nadarajah B, Brunstrom JE, Grutzendler J, Wong RO, Pearlman AL (2001) Two modes of radial migration in early development of the cerebral cortex. Nat Neurosci 4:143-150.
33. 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 U S A 94:8196-8201.
34. Niwa H, Yamamura K, Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-199.
35. 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.
36. Olson EC, Kim S, Walsh CA (2006) Impaired neuronal positioning and dendritogenesis in the neocortex after cell-autonomous Dab1 suppression. J Neurosci 26:1767-1775.
37. Park TJ, Curran T (2008) Crk and Crk-like play essential overlapping roles downstream of disabled-1 in the Reelin pathway. J Neurosci 28:13551-13562.
38. Pinto-Lord MC, Evrard P, Caviness VS Jr (1982) Obstructed neuronal migration along radial glial fibers in the neocortex of the reeler mouse: a Golgi-EM analysis. Brain Res 256:379-393.
39. Rakic P (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol 145:61-83.
40. Rice DS, Curran T (2001) Role of the reelin signaling pathway in central nervous system development. Annu Rev Neurosci 24:1005-1039.
41. Sanada K, Gupta A, Tsai LH (2004) Disabled-1-regulated adhesion of migrating neurons to radial glial fiber contributes to neuronal positioning during early corticogenesis. Neuron 42:197-211.
42. Sarnat HB, Nochlin D, Born DE (1998) Neuronal nuclear antigen (NeuN): a marker of neuronal maturation in early human fetal nervous system. Brain Dev 20:88-94.
43. Sheldon M, Rice DS, D'Arcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T (1997) Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389:730-733.
44. Simó S, Jossin Y, Cooper JA (2010) Cullin 5 regulates cortical layering by modulating the speed and duration of Dab1-dependent neuronal migration. J Neurosci 30:5668-5676.
45. Tabata H, Nakajima K (2001) Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 103:865-872.
46. Tabata H, Nakajima K (2002) Neurons tend to stop migration and differentiate along the cortical internal plexiform zones in the Reelin signaldeficient mice. J Neurosci Res 69:723-730.
47. Tabata H, Nakajima K (2003) Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J Neurosci 23:9996-10001.
48. Tabata H, Kanatani S, Nakajima K (2009) Differences of migratory behavior between direct progeny of apical progenitors and basal progenitors in the developing cerebral cortex. Cereb Cortex 19:2092-2105.
49. Tachikawa K, Sasaki S, Maeda T, Nakajima K (2008) Identification of molecules preferentially expressed beneath the marginal zone in the developing cerebral cortex. Neurosci Res 60:135-146.
50. Takahashi T, Goto T, Miyama S, Nowakowski RS, Caviness VS Jr (1999) Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 19:10357-10371.
51. Tissir F, Goffinet AM (2003) Reelin and brain development. Nat Rev Neurosci 4:496-505.
52. Uchida T, Baba A, Pérez-Martínez FJ, Hibi T, Miyata T, Luque JM, Nakajima K, Hattori M (2009) Downregulation of functional Reelin receptors in projection neurons implies that primary Reelin action occurs at early/premigratory stages. J Neurosci 29:10653-10662.
53. Voss AK, Britto JM, Dixon MP, Sheikh BN, Collin C, Tan SS, Thomas T (2008) C3G regulates cortical neuron migration, preplate splitting and radial glial cell attachment. Development 135:2139-2149.
54. Ware ML, Fox JW, González JL, Davis NM, Lambert de Rouvroit C, Russo CJ, Chua SC Jr, Goffinet AM, Walsh CA (1997) Aberrant splicing of a mouse disabled homolog, mdab1, in the scrambler mouse. Neuron 19:239-249.
55. Yano M, Hayakawa-Yano Y, Mele A, Darnell RB (2010) Nova2 regulates neuronal migration through an RNA switch in disabled-1 signaling. Neuron 66:848-858.
56. Yoneshima H, Nagata E, Matsumoto M, Yamada M, Nakajima K, Miyata T, Ogawa M, Mikoshiba K (1997) A novel neurological mutant mouse, yotari, which exhibits reeler-like phenotype but expresses CR-50 antigen/reelin. Neurosci Res 29:217-223.
57. Yoshida M, Assimacopoulos S, Jones KR, Grove EA (2006) Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 133:537-545.
58. Zheng L, Baumann U, Reymond JL (2004) An efficient one-step sitedirected and site-saturation mutagenesis protocol. Nucleic Acids Res 32: e115