Molecules and mechanisms that regulate multipolar migration in the intermediate zone

Frontiers in Cellular Neuroscience

Volumn 8, Issue November, 2014, Pages

  Cooper, Jonathan A ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Axonogenesis; Cortical lamination; Mini columns; Multipolar migration; Neocortex development; Neuron locomotion; Neuron migration; Radial migration

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CELL SURFACE RECEPTOR; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; CYCLIN DEPENDENT KINASE 5; CYTOSKELETON PROTEIN; FIBROBLAST GROWTH FACTOR; GUANOSINE TRIPHOSPHATASE; KINESIN; NERVE CELL ADHESION MOLECULE; NEUROGENIN 2; PROTEIN KINASE; RAB PROTEIN; RAC1 PROTEIN; REELIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SEMAPHORIN 3A; SEROTONIN 6 RECEPTOR; STRESS ACTIVATED PROTEIN KINASE;

BRAIN DEVELOPMENT; CELL MIGRATION; CELLULAR STRESS SIGNAL; ENDOCYTOSIS; GENE OVEREXPRESSION; GENE SILENCING; GENETIC MANIPULATION; GOLGI COMPLEX; HUMAN; MULTIPOLAR MIGRATION; NEOCORTEX; NERVE FIBER GROWTH; NERVE PROJECTION; NEURON MIGRATION; POLARIZATION; PROTEIN EXPRESSION; RADIAL MIGRATION; REVIEW; SUBVENTRICULAR ZONE;

EID: 84910155103     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00386     Document Type: Review

References (101)

1. Asada, N., and Sanada, K. (2010). LKB1-mediated spatial control of GSK3beta and adenomatous polyposis coli contributes to centrosomal forward movement and neuronal migration in the developing neocortex. J. Neurosci. 30, 8852-8865. doi: 10.1523/jneurosci.6140-09.2010.
2. Asada, N., Sanada, K., and Fukada, Y. (2007). LKB1 regulates neuronal migration and neuronal differentiation in the developing neocortex through centrosomal positioning. J. Neurosci. 27, 11769-11775. doi: 10.1523/jneurosci.1938-07.2007.
3. Ayala, R., Shu, T., and Tsai, L. H. (2007). Trekking across the brain: the journey of neuronal migration. Cell 128, 29-43. doi: 10.1016/j.cell.2006.12.021.
4. Azzarelli, R., Pacary, E., Garg, R., Garcez, P., Van Den Berg, D., Riou, P., et al. (2014). An antagonistic interaction between PlexinB2 and Rnd3 controls RhoA activity and cortical neuron migration. Nat. Commun. 5:3405. doi: 10.1038/ncomms4405.
5. Barnes, A. P., Lilley, B. N., Pan, Y. A., Plummer, L. J., Powell, A. W., Raines, A. N., et al. (2007). LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129, 549-563. doi: 10.1016/j.cell.2007.03.025.
6. Barnes, A. P., and Polleux, F. (2009). Establishment of axon-dendrite polarity in developing neurons. Annu. Rev. Neurosci. 32, 347-381. doi: 10.1146/annurev.neuro.31.060407.125536.
7. Besson, A., Dowdy, S. F., and Roberts, J. M. (2008). CDK inhibitors: cell cycle regulators and beyond. Dev. Cell 14, 159-169. doi: 10.1016/j.devcel.2008.01.013.
8. Besson, A., Gurian-West, M., Schmidt, A., Hall, A., and Roberts, J. M. (2004). p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 18, 862-876. doi: 10.1101/gad.1185504.
9. Bielas, S., Higginbotham, H., Koizumi, H., Tanaka, T., and Gleeson, J. G. (2004). Cortical neuronal migration mutants suggest separate but intersecting pathways. Annu. Rev. Cell Dev. Biol. 20, 593-618. doi: 10.1146/annurev.cellbio.20.082503.103047.
10. Chen, G., Sima, J., Jin, M., Wang, K. Y., Xue, X. J., Zheng, W., et al. (2008). Semaphorin-3A guides radial migration of cortical neurons during development. Nat. Neurosci. 11, 36-44. doi: 10.1038/nn2018.
11. Cooper, J. A., Allen, N. S., and Feng, L. (2008). "Protein kinases and signaling pathways that are activated by Reelin," in Reelin Glycoprotein: Structure, Biology and Roles in Health and Disease, ed S. H. Fatemi (New York, NY: Springer), 193-216.
12. de Anda, F. C., Meletis, K., Ge, X., Rei, D., and Tsai, L. H. (2010). Centrosome motility is essential for initial axon formation in the neocortex. J. Neurosci. 30, 10391-10406. doi: 10.1523/jneurosci.0381-10.2010.
13. Dimidschstein, J., Passante, L., Dufour, A., Van Den Ameele, J., Tiberi, L., Hrechdakian, T., et al. (2013). Ephrin-B1 controls the columnar distribution of cortical pyramidal neurons by restricting their tangential migration. Neuron 79, 1123-1135. doi: 10.1016/j.neuron.2013.07.015.
14. Elias, L. A., Wang, D. D., and Kriegstein, A. R. (2007). Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448, 901-907. doi: 10.1038/nature06063.
15. Fagotto, F. (2014). The cellular basis of tissue separation. Development 141, 3303-3318. doi: 10.1242/dev.090332.
16. Falnikar, A., Tole, S., Liu, M., Liu, J. S., and Baas, P. W. (2013). Polarity in migrating neurons is related to a mechanism analogous to cytokinesis. Curr. Biol. 23, 1215-1220. doi: 10.1016/j.cub.2013.05.027.
17. Fang, W. Q., Ip, J. P., Li, R., Ng, Y. P., Lin, S. C., Chen, Y., et al. (2011). Cdk5-mediated phosphorylation of Axin directs axon formation during cerebral cortex development. J. Neurosci. 31, 13613-13624. doi: 10.1523/jneurosci.3120-11.2011.
18. Feng, L., and Cooper, J. A. (2009). Dual functions of Dab1 during brain development. Mol. Cell. Biol. 29, 324-332. doi: 10.1128/mcb.00663-08.
19. Fishell, G., and Hanashima, C. (2008). Pyramidal neurons grow up and change their mind. Neuron 57, 333-338. doi: 10.1016/j.neuron.2008.01.018.
20. Franco, S. J., Martinez-Garay, I., Gil-Sanz, C., Harkins-Perry, S. R., and Müller, U. (2011). Reelin regulates cadherin function via Dab1/Rap1 to control neuronal migration and lamination in the neocortex. Neuron 69, 482-497. doi: 10.1016/j.neuron.2011.01.003.
21. Fukuda, T., Kawano, H., Ohyama, K., Li, H. P., Takeda, Y., Oohira, A., et al. (1997). Immunohistochemical localization of neurocan and L1 in the formation of thalamocortical pathway of developing rats. J. Comp. Neurol. 382, 141-152. doi: 10.1002/(sici)1096-9861(19970602)382:2<141::aid-cne1>3.3.co;2-9.
22. Fukumitsu, H., Ohtsuka, M., Murai, R., Nakamura, H., Itoh, K., and Furukawa, S. (2006). Brain-derived neurotrophic factor participates in determination of neuronal laminar fate in the developing mouse cerebral cortex. J. Neurosci. 26, 13218-13230. doi: 10.1523/jneurosci.4251-06.2006.
23. Gao, P., Sultan, K. T., Zhang, X. J., and Shi, S. H. (2013). Lineage-dependent circuit assembly in the neocortex. Development 140, 2645-2655. doi: 10.1242/dev.087668.
24. Gil-Sanz, C., Franco, S. J., Martinez-Garay, I., Espinosa, A., Harkins-Perry, S., and Müller, U. (2013). Cajal-Retzius cells instruct neuronal migration by coincidence signaling between secreted and contact-dependent guidance cues. Neuron 79, 461-477. doi: 10.1016/j.neuron.2013.06.040.
25. Godin, J. D., Thomas, N., Laguesse, S., Malinouskaya, L., Close, P., Malaise, O., et al. (2012). p27(Kip1) is a microtubule-associated protein that promotes microtubule polymerization during neuron migration. Dev. Cell 23, 729-744. doi: 10.1016/j.devcel.2012.08.006.
26. Guerrier, S., Coutinho-Budd, J., Sassa, T., Gresset, A., Jordan, N. V., Chen, K., et al. (2009). The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. Cell 138, 990-1004. doi: 10.1016/j.cell.2009.06.047.
27. Guijarro, P., Wang, Y., Ying, Y., Yao, Y., Jieyi, X., and Yuan, X. (2013). In vivo knockdown of cKit impairs neuronal migration and axonal extension in the cerebral cortex. Dev. Neurobiol. 73, 871-887. doi: 10.1002/dneu.22107.
28. Gupta, A., Sanada, K., Miyamoto, D. T., Rovelstad, S., Nadarajah, B., Pearlman, A. L., et al. (2003). Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat. Neurosci. 6, 1284-1291. doi: 10.1038/nn1151.
29. Hand, R., Bortone, D., Mattar, P., Nguyen, L., Heng, J. I., Guerrier, S., et al. (2005). Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 48, 45-62. doi: 10.1016/j.neuron.2005.08.032.
30. Hatanaka, Y., Hisanaga, S., Heizmann, C. W., and Murakami, F. (2004). Distinct migratory behavior of early-and late-born neurons derived from the cortical ventricular zone. J. Comp. Neurol. 479, 1-14. doi: 10.1002/cne.20256.
31. Hatanaka, Y., Matsumoto, T., Yanagawa, Y., Fujisawa, H., Murakami, F., and Masu, M. (2009). Distinct roles of neuropilin 1 signaling for radial and tangential extension of callosal axons. J. Comp. Neurol. 514, 215-225. doi: 10.1002/cne.22021.
32. Hatanaka, Y., and Murakami, F. (2002). In vitro analysis of the origin, migratory behavior and maturation of cortical pyramidal cells. J. Comp. Neurol. 454, 1-14. doi: 10.1002/cne.10421.
33. Hatanaka, Y., and Yamauchi, K. (2013). Excitatory cortical neurons with multipolar shape establish neuronal polarity by forming a tangentially oriented axon in the intermediate zone. Cereb. Cortex 23, 105-113. doi: 10.1093/cercor/bhr383.
34. Hatten, M. E. (2002). New directions in neuronal migration. Science 297, 1660-1663. doi: 10.1126/science.1074572.
35. Heng, J. I., Nguyen, L., Castro, D. S., Zimmer, C., Wildner, H., Armant, O., et al. (2008). Neurogenin 2 controls cortical neuron migration through regulation of Rnd2. Nature 455, 114-118. doi: 10.1038/nature07198.
36. Hirai, S., Cui De, F., Miyata, T., Ogawa, M., Kiyonari, H., Suda, Y., et al. (2006). The c-Jun N-terminal kinase activator dual leucine zipper kinase regulates axon growth and neuronal migration in the developing cerebral cortex. J. Neurosci. 26, 11992-12002. doi: 10.1523/jneurosci.2272-06.2006.
37. Hirai, S., Kawaguchi, A., Hirasawa, R., Baba, M., Ohnishi, T., and Ohno, S. (2002). MAPK-upstream protein kinase (MUK) regulates the radial migration of immature neurons in telencephalon of mouse embryo. Development 129, 4483-4495.
38. Honda, T., Kobayashi, K., Mikoshiba, K., and Nakajima, K. (2011). Regulation of cortical neuron migration by the Reelin signaling pathway. Neurochem. Res. 36, 1270-1279. doi: 10.1007/s11064-011-0407-4.
39. Hur, E. M., and Zhou, F. Q. (2010). GSK3 signalling in neural development. Nat. Rev. Neurosci. 11, 539-551. doi: 10.1038/nrn2870.
40. Ip, J. P., Shi, L., Chen, Y., Itoh, Y., Fu, W. Y., Betz, A., et al. (2012). α2-chimaerin controls neuronal migration and functioning of the cerebral cortex through CRMP-2. Nat. Neurosci. 15, 39-47. doi: 10.1038/nn.2972.
41. Itoh, Y., Moriyama, Y., Hasegawa, T., Endo, T. A., Toyoda, T., and Gotoh, Y. (2013a). Scratch regulates neuronal migration onset via an epithelial-mesenchymal transition-like mechanism. Nat. Neurosci. 16, 416-425. doi: 10.1038/nn.3336.
42. Itoh, Y., Tyssowski, K., and Gotoh, Y. (2013b). Transcriptional coupling of neuronal fate commitment and the onset of migration. Curr. Opin. Neurobiol. 23, 957-964. doi: 10.1016/j.conb.2013.08.003.
43. Iwashita, M., Kataoka, N., Toida, K., and Kosodo, Y. (2014). Systematic profiling of spatiotemporal tissue and cellular stiffness in the developing brain. Development 141, 3793-3798. doi: 10.1242/dev.109637.
44. Jacobshagen, M., Niquille, M., Chaumont-Dubel, S., Marin, P., and Dayer, A. (2014). The serotonin 6 receptor controls neuronal migration during corticogenesis via a ligand-independent Cdk5-dependent mechanism. Development 141, 3370-3377. doi: 10.1242/dev.108043.
45. Jossin, Y., and Cooper, J. A. (2011). Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat. Neurosci. 14, 697-703. doi: 10.1038/nn.2816.
46. Jossin, Y., Gui, L., and Goffinet, A. M. (2007). Processing of Reelin by embryonic neurons is important for function in tissue but not in dissociated cultured neurons. J. Neurosci. 27, 4243-4252. doi: 10.1523/jneurosci.0023-07.2007.
47. Jossin, Y., Ignatova, N., Hiesberger, T., Herz, J., Lambert de Rouvroit, C., and Goffinet, A. M. (2004). The central fragment of Reelin, generated by proteolytic processing in vivo, is critical to its function during cortical plate development. J. Neurosci. 24, 514-521. doi: 10.1523/jneurosci.3408-03.2004.
48. Kawauchi, T., Chihama, K., Nabeshima, Y. I., and Hoshino, M. (2003). The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration. Embo J. 22, 4190-4201. doi: 10.1093/emboj/cdg413.
49. Kawauchi, T., Chihama, K., Nabeshima, Y. I., and Hoshino, M. (2006). Cdk5 phosphorylates and stabilizes p27(kip1) contributing to actin organization and cortical neuronal migration. Nat. Cell Biol. 8, 17-26. doi: 10.1038/ncb1338.
50. Kawauchi, T., Sekine, K., Shikanai, M., Chihama, K., Tomita, K., Kubo, K., et al. (2010). Rab GTPases-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron 67, 588-602. doi: 10.1016/j.neuron.2010.07.007.
51. Konno, D., Yoshimura, S., Hori, K., Maruoka, H., and Sobue, K. (2005). Involvement of the phosphatidylinositol 3-kinase/rac1 and cdc42 pathways in radial migration of cortical neurons. J. Biol. Chem. 280, 5082-5088. doi: 10.1074/jbc.m408251200.
52. Landrieu, P., and Goffinet, A. (1981). Inverted pyramidal neurons and their axons in the neocortex of reeler mutant mice. Cell Tissue Res. 218, 293-301. doi: 10.1007/bf00210345.
53. Lin, S., Liu, M., Mozgova, O. I., Yu, W., and Baas, P. W. (2012). Mitotic motors coregulate microtubule patterns in axons and dendrites. J. Neurosci. 32, 14033-14049. doi: 10.1523/jneurosci.3070-12.2012.
54. Liu, G., Beggs, H., Jürgensen, C., Park, H. T., Tang, H., Gorski, J., et al. (2004). Netrin requires focal adhesion kinase and Src family kinases for axon outgrowth and attraction. Nat. Neurosci. 7, 1222-1232. doi: 10.1038/nn1331.
55. Liu, X., Hashimoto-Torii, K., Torii, M., Ding, C., and Rakic, P. (2010). Gap junctions/hemichannels modulate interkinetic nuclear migration in the forebrain precursors. J. Neurosci. 30, 4197-4209. doi: 10.1523/jneurosci.4187-09.2010.
56. Liu, X., Sun, L., Torii, M., and Rakic, P. (2012). Connexin 43 controls the multipolar phase of neuronal migration to the cerebral cortex. Proc. Natl. Acad. Sci. U S A 109, 8280-8285. doi: 10.1073/pnas.1205880109.
57. LoTurco, J. J., and Bai, J. (2006). The multipolar stage and disruptions in neuronal migration. Trends Neurosci. 29, 407-413. doi: 10.1016/j.tins.2006.05.006.
58. Magdaleno, S., Keshvara, L., and Curran, T. (2002). Rescue of ataxia and preplate splitting by ectopic expression of Reelin in reeler mice. Neuron 33, 573-586. doi: 10.1016/s0896-6273(02)00582-2.
59. Marín, O., and Rubenstein, J. L. (2003). Cell migration in the forebrain. Annu. Rev. Neurosci. 26, 441-483. doi: 10.1146/annurev.neuro.26.041002.131058.
60. Matsuki, T., Chen, J., and Howell, B. W. (2013). Acute inactivation of the serine-threonine kinase Stk25 disrupts neuronal migration. Neural Dev. 8:21. doi: 10.1186/1749-8104-8-21.
61. Matsuki, T., Matthews, R. T., Cooper, J. A., Van der Brug, M. P., Cookson, M. R., Hardy, J. A., et al. (2010). Reelin and stk25 have opposing roles in neuronal polarization and dendritic Golgi deployment. Cell 143, 826-836. doi: 10.1016/j.cell.2010.10.029.
62. Medina, D. L., Sciarretta, C., Calella, A. M., Von Bohlen Und Halbach, O., Unsicker, K., and Minichiello, L. (2004). TrkB regulates neocortex formation through the Shc/PLCgamma-mediated control of neuronal migration. EMBO J. 23, 3803-3814. doi: 10.1038/sj.emboj.7600399.
63. Miyoshi, G., and Fishell, G. (2012). Dynamic FoxG1 expression coordinates the integration of multipolar pyramidal neuron precursors into the cortical plate. Neuron 74, 1045-1058. doi: 10.1016/j.neuron.2012.04.025.
64. Molyneaux, B. J., Arlotta, P., Menezes, J. R., and Macklis, J. D. (2007). Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437. doi: 10.1038/nrn2151.
65. Morgan-Smith, M., Wu, Y., Zhu, X., Pringle, J., and Snider, W. D. (2014). GSK-3 signaling in developing cortical neurons is essential for radial migration and dendritic orientation. Elife 3:e02663. doi: 10.7554/elife.02663.
66. Nadarajah, B., Brunstrom, J. E., Grutzendler, J., Wong, R. O., and Pearlman, A. L. (2001). Two modes of radial migration in early development of the cerebral cortex. Nat. Neurosci. 4, 143-150. doi: 10.1038/83967.
67. Nakamuta, S., Funahashi, Y., Namba, T., Arimura, N., Picciotto, M. R., Tokumitsu, H., et al. (2011). Local application of neurotrophins specifies axons through inositol 1,4,5-trisphosphate, calcium and Ca2+/calmodulin-dependent protein kinases. Sci. Signal. 4:ra76. doi: 10.1126/scisignal.2002011.
68. Namba, T., Kibe, Y., Funahashi, Y., Nakamuta, S., Takano, T., Ueno, T., et al. (2014). Pioneering axons regulate neuronal polarization in the developing cerebral cortex. Neuron 81, 814-829. doi: 10.1016/j.neuron.2013.12.015.
69. Nguyen, L., Besson, A., Heng, J. I., Schuurmans, C., Teboul, L., Parras, C., et al. (2006). p27kip1 independently promotes neuronal differentiation and migration in the cerebral cortex. Genes Dev. 20, 1511-1524. doi: 10.1101/gad.377106.
70. Nichols, A. J., and Olson, E. C. (2010). Reelin promotes neuronal orientation and dendritogenesis during preplate splitting. Cereb. Cortex 20, 2213-2223. doi: 10.1093/cercor/bhp303.
71. Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S., and Kriegstein, A. R. (2001). Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714-720.
72. Noctor, S. C., Flint, A. C., Weissman, T. A., Wong, W. S., Clinton, B. K., and Kriegstein, A. R. (2002). Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J. Neurosci. 22, 3161-3173.
73. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L., and Kriegstein, A. R. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144. doi: 10.1038/nn1172.
74. Ochiai, W., Minobe, S., Ogawa, M., and Miyata, T. (2007). Transformation of pin-like ventricular zone cells into cortical neurons. Neurosci. Res. 57, 326-329. doi: 10.1016/j.neures.2006.10.015.
75. O'Dell, R. S., Ustine, C. J., Cameron, D. A., Lawless, S. M., Williams, R. R., Zipfel, W. R., et al. (2012). Layer 6 cortical neurons require Reelin-Dab1 signaling for cellular orientation, Golgi deployment and directed neurite growth into the marginal zone. Neural Dev. 7:25. doi: 10.1186/1749-8104-7-25.
76. Ohshima, T., Hirasawa, M., Tabata, H., Mutoh, T., Adachi, T., Suzuki, H., et al. (2007). Cdk5 is required for multipolar-to-bipolar transition during radial neuronal migration and proper dendrite development of pyramidal neurons in the cerebral cortex. Development 134, 2273-2282. doi: 10.1242/dev.02854.
77. Orlova, K. A., Parker, W. E., Heuer, G. G., Tsai, V., Yoon, J., Baybis, M., et al. (2010). STRADalpha deficiency results in aberrant mTORC1 signaling during corticogenesis in humans and mice. J. Clin. Invest. 120, 1591-1602. doi: 10.1172/jci41592.
78. O'Rourke, N. A., Dailey, M. E., Smith, S. J., and Mcconnell, S. K. (1992). Diverse migratory pathways in the developing cerebral cortex. Science 258, 299-302. doi: 10.1126/science.1411527.
79. Park, T. J., and Curran, T. (2008). Crk and Crk-like play essential overlapping roles downstream of disabled-1 in the Reelin pathway. J. Neurosci. 28, 13551-13562. doi: 10.1523/jneurosci.4323-08.2008.
80. Polleux, F., and Ghosh, A. (2002). The slice overlay assay: a versatile tool to study the influence of extracellular signals on neuronal development. Sci. STKE 2002:pl9. doi: 10.1126/scisignal.1362002pl9.
81. Polleux, F., Giger, R. J., Ginty, D. D., Kolodkin, A. L., and Ghosh, A. (1998). Patterning of cortical efferent projections by semaphorin-neuropilin interactions. Science 282, 1904-1906. doi: 10.1126/science.282.5395.1904.
82. Rakic, P. (2000). Radial unit hypothesis of neocortical expansion. Novartis Found. Symp. 228, 30-42; discussion 42-52. doi: 10.1002/0470846631.ch3.
83. Roca-Cusachs, P., Sunyer, R., and Trepat, X. (2013). Mechanical guidance of cell migration: lessons from chemotaxis. Curr. Opin. Cell Biol. 25, 543-549. doi: 10.1016/j.ceb.2013.04.010.
84. Sanada, K., Gupta, A., and Tsai, L. H. (2004). Disabled-1-regulated adhesion of migrating neurons to radial glial fiber contributes to neuronal positioning during early corticogenesis. Neuron 42, 197-211. doi: 10.1016/s0896-6273(04)00222-3.
85. Sasaki, S., Tabata, H., Tachikawa, K., and Nakajima, K. (2008). The cortical subventricular zone-specific molecule Svet1 is part of the nuclear RNA coded by the putative netrin receptor gene Unc5d and is expressed in multipolar migrating cells. Mol. Cell. Neurosci. 38, 474-483. doi: 10.1016/j.mcn.2008.04.002.
86. Schneider, S., Gulacsi, A., and Hatten, M. E. (2011). Lrp12/Mig13a reveals changing patterns of preplate neuronal polarity during corticogenesis that are absent in reeler mutant mice. Cereb. Cortex 21, 134-144. doi: 10.1093/cercor/bhq070.
87. Shelly, M., Cancedda, L., Lim, B. K., Popescu, A. T., Cheng, P. L., Gao, H., et al. (2011). Semaphorin3A regulates neuronal polarization by suppressing axon formation and promoting dendrite growth. Neuron 71, 433-446. doi: 10.1016/j.neuron.2011.06.041.
88. Shoukimas, G. M., and Hinds, J. W. (1978). The development of the cerebral cortex in the embryonic mouse: an electron microscopic serial section analysis. J. Comp. Neurol. 179, 795-830. doi: 10.1002/cne.901790407.
89. Sun, Y., Fei, T., Yang, T., Zhang, F., Chen, Y. G., Li, H., et al. (2010). The suppression of CRMP2 expression by bone morphogenetic protein (BMP)-SMAD gradient signaling controls multiple stages of neuronal development. J. Biol. Chem. 285, 39039-39050. doi: 10.1074/jbc.m110.168351.
90. Tabata, H., Kanatani, S., and 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. doi: 10.1093/cercor/bhn227.
91. Tabata, H., and Nakajima, K. (2003). Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J. Neurosci. 23, 9996-10001.
92. Tang, J., Ip, J. P., Ye, T., Ng, Y. P., Yung, W. H., Wu, Z., et al. (2014). Cdk5-dependent Mst3 phosphorylation and activity regulate neuronal migration through RhoA inhibition. J. Neurosci. 34, 7425-7436. doi: 10.1523/jneurosci.5449-13.2014.
93. Toma, K., Kumamoto, T., and Hanashima, C. (2014). The timing of upper-layer neurogenesis is conferred by sequential derepression and negative feedback from deep-layer neurons. J. Neurosci. 34, 13259-13276. doi: 10.1523/jneurosci.2334-14.2014.
94. Torii, M., Hashimoto-Torii, K., Levitt, P., and Rakic, P. (2009). Integration of neuronal clones in the radial cortical columns by EphA and ephrin-A signalling. Nature 461, 524-528. doi: 10.1038/nature08362.
95. Uchida, T., Baba, A., Pérez-Martínez, F. J., Hibi, T., Miyata, T., Luque, J. M., et al. (2009). Downregulation of functional Reelin receptors in projection neurons implies that primary Reelin action occurs at early/premigratory stages. J. Neurosci. 29, 10653-10662. doi: 10.1523/jneurosci.0345-09.2009.
96. Voss, A. K., Britto, J. M., Dixon, M. P., Sheikh, B. N., Collin, C., Tan, S. S., et al. (2008). C3G regulates cortical neuron migration, preplate splitting and radial glial cell attachment. Development 135, 2139-2149. doi: 10.1242/dev.016725.
97. Westerlund, N., Zdrojewska, J., Padzik, A., Komulainen, E., Bjorkblom, B., Rannikko, E., et al. (2011). Phosphorylation of SCG10/stathmin-2 determines multipolar stage exit and neuronal migration rate. Nat. Neurosci. 14, 305-313. doi: 10.1038/nn.2755.
98. Wu, Q. F., Yang, L., Li, S., Wang, Q., Yuan, X. B., Gao, X., et al. (2012). Fibroblast growth factor 13 is a microtubule-stabilizing protein regulating neuronal polarization and migration. Cell 149, 1549-1564. doi: 10.1016/j.cell.2012.04.046.
99. Young-Pearse, T. L., Bai, J., Chang, R., Zheng, J. B., Loturco, J. J., and Selkoe, D. J. (2007). A critical function for beta-amyloid precursor protein in neuronal migration revealed by in utero RNA interference. J. Neurosci. 27, 14459-14469. doi: 10.1523/jneurosci.4701-07.2007.
100. Yu, Y. C., Bultje, R. S., Wang, X., and Shi, S. H. (2009). Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 458, 501-504. doi: 10.1038/nature07722.
101. Yu, Y. C., He, S., Chen, S., Fu, Y., Brown, K. N., Yao, X. H., et al. (2012). Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly. Nature 486, 113-117. doi: 10.1038/nature10958.