Molecular regulation of neuronal migration during neocortical development

Molecular and Cellular Neuroscience

Volumn 42, Issue 1, 2009, Pages 11-22

  Huang, Zhen ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

Cajal Retzius cell; Cerebral cortex; Chemokine Cxcl12; Cxcr4; Cyclin dependent kinase 5; Dlx1 2; G protein coupled receptor; Interneuron; Lissencephaly; Locomotion; Neuregulin; Neuronal migration; Nkx2 1; Notch; Nuclear centrosome coupling; Radial glia; Reelin; Semaphorin; Somal translocation; Tangential migration; X linked lissencephaly with abnormal genitalia

Indexed keywords

4 AMINOBUTYRIC ACID; APOLIPOPROTEIN E2; CYCLIN DEPENDENT KINASE 5; DOUBLECORTIN; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NOTCH RECEPTOR; REELIN; VERY LOW DENSITY LIPOPROTEIN RECEPTOR;

BRAIN NERVE CELL; CELL MIGRATION; CELL STRUCTURE; COILED BODY; GABAERGIC SYSTEM; HUMAN; INTERNEURON; MOLECULAR MECHANICS; NEOCORTEX; NERVE CELL DIFFERENTIATION; NERVOUS TISSUE; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MODELS, BIOLOGICAL; NEOCORTEX; NERVE TISSUE PROTEINS; NERVOUS SYSTEM DISEASES; NEURONS; SIGNAL TRANSDUCTION;

EID: 67650960626     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2009.06.003     Document Type: Review

References (177)

1. Abrahams B.S., and Geschwind D.H. Advances in autism genetics: on the threshold of a new neurobiology. Nat. Rev. Genet. 9 (2008) 341-355
2. Alcantara S., Ruiz M., D'Arcangelo G., Ezan F., de Lecea L., Curran T., Sotelo C., and Soriano E. Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J. Neurosci. 18 (1998) 7779-7799
3. Anderson S.A., Eisenstat D.D., Shi L., and Rubenstein J.L. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278 (1997) 474-476
4. Ang Jr. E.S., Haydar T.F., Gluncic V., and Rakic P. Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J. Neurosci. 23 (2003) 5805-5815
5. Angevine Jr. J.B., and Sidman R.L. Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192 (1961) 766-768
6. Anthony T.E., Klein C., Fishell G., and Heintz N. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41 (2004) 881-890
7. Anton E.S., Kreidberg J.A., and Rakic P. Distinct functions of alpha3 and alpha(v) integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 22 (1999) 277-289
8. Arnaud L., Ballif B.A., and Cooper J.A. Regulation of protein tyrosine kinase signaling by substrate degradation during brain development. Mol. Cell. Biol. 23 (2003) 9293-9302
9. Asada N., Sanada K., and Fukada Y. LKB1 regulates neuronal migration and neuronal differentiation in the developing neocortex through centrosomal positioning. J. Neurosci. 27 (2007) 11769-11775
10. Assadi A.H., Zhang G., Beffert U., McNeil R.S., Renfro A.L., Niu S., Quattrocchi C.C., Antalffy B.A., Sheldon M., Armstrong D.D., Wynshaw-Boris A., Herz J., D'Arcangelo G., and Clark G.D. Interaction of reelin signaling and Lis1 in brain development. Nat. Genet. 35 (2003) 270-276
11. Ayala R., Shu T., and Tsai L.H. Trekking across the brain: the journey of neuronal migration. Cell 128 (2007) 29-43
12. Bai J., Ramos R.L., Ackman J.B., Thomas A.M., Lee R.V., and LoTurco J.J. RNAi reveals doublecortin is required for radial migration in rat neocortex. Nat. Neurosci. 6 (2003) 1277-1283
13. Ballif B.A., Arnaud L., and Cooper J.A. Tyrosine phosphorylation of Disabled-1 is essential for Reelin-stimulated activation of Akt and Src family kinases. Brain Res. Mol. Brain Res. 117 (2003) 152-159
14. Barnes A.P., Lilley B.N., Pan Y.A., Plummer L.J., Powell A.W., Raines A.N., Sanes J.R., and Polleux F. LKB1 and SAD kinases define a pathway required for the polarization of cortical neurons. Cell 129 (2007) 549-563
15. Beffert U., Weeber E.J., Morfini G., Ko J., Brady S.T., Tsai L.H., Sweatt J.D., and Herz J. Reelin and cyclin-dependent kinase 5-dependent signals cooperate in regulating neuronal migration and synaptic transmission. J. Neurosci. 24 (2004) 1897-1906
16. Beggs H.E., Schahin-Reed D., Zang K., Goebbels S., Nave K.A., Gorski J., Jones K.R., Sretavan D., and Reichardt L.F. FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40 (2003) 501-514
17. Bellion A., Baudoin J.P., Alvarez C., Bornens M., and Metin C. Nucleokinesis in tangentially migrating neurons comprises two alternating phases: forward migration of the Golgi/centrosome associated with centrosome splitting and myosin contraction at the rear. J. Neurosci. 25 (2005) 5691-5699
18. Beltran-Valero de Bernabe D., Currier S., Steinbrecher A., Celli J., van Beusekom E., van der Zwaag B., Kayserili H., Merlini L., Chitayat D., Dobyns W.B., Cormand B., Lehesjoki A.E., Cruces J., Voit T., Walsh C.A., van Bokhoven H., and Brunner H.G. Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am. J. Hum. Genet. 71 (2002) 1033-1043
19. Belvindrah R., Graus-Porta D., Goebbels S., Nave K.A., and Muller U. Beta1 integrins in radial glia but not in migrating neurons are essential for the formation of cell layers in the cerebral cortex. J. Neurosci. 27 (2007) 13854-13865
20. Bielle F., Griveau A., Narboux-Neme N., Vigneau S., Sigrist M., Arber S., Wassef M., and Pierani A. Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat. Neurosci. 8 (2005) 1002-1012
21. Bock H.H., and Herz J. Reelin activates SRC family tyrosine kinases in neurons. Curr. Biol. 13 (2003) 18-26
22. Borrell V., and Marin O. Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling. Nat. Neurosci. 9 (2006) 1284-1293
23. Borrell V., Kaspar B.K., Gage F.H., and Callaway E.M. In vivo evidence for radial migration of neurons by long-distance somal translocation in the developing ferret visual cortex. Cereb. Cortex. 16 (2006) 1571-1583
24. Botella-Lopez A., Burgaya F., Gavin R., Garcia-Ayllon M.S., Gomez-Tortosa E., Pena-Casanova J., Urena J.M., Del Rio J.A., Blesa R., Soriano E., and Saez-Valero J. Reelin expression and glycosylation patterns are altered in Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 5573-5578
25. Boycott K.M., Flavelle S., Bureau A., Glass H.C., Fujiwara T.M., Wirrell E., Davey K., Chudley A.E., Scott J.N., McLeod D.R., and Parboosingh J.S. Homozygous deletion of the very low density lipoprotein receptor gene causes autosomal recessive cerebellar hypoplasia with cerebral gyral simplification. Am. J. Hum. Genet. 77 (2005) 477-483
26. Breedveld G.J., van Dongen J.W., Danesino C., Guala A., Percy A.K., Dure L.S., Harper P., Lazarou L.P., van der Linde H., Joosse M., Gruters A., MacDonald M.E., de Vries B.B., Arts W.F., Oostra B.A., Krude H., and Heutink P. Mutations in TITF-1 are associated with benign hereditary chorea. Hum. Mol. Genet. 11 (2002) 971-979
27. Butt S.J., Sousa V.H., Fuccillo M.V., Hjerling-Leffler J., Miyoshi G., Kimura S., and Fishell G. The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59 (2008) 722-732
28. Caviness Jr. V.S., and 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. 148 (1973) 141-151
29. Chae T., Kwon Y.T., Bronson R., Dikkes P., Li E., and Tsai L.H. Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, seizures, and adult lethality. Neuron 18 (1997) 29-42
30. Chen K., Ochalski P.G., Tran T.S., Sahir N., Schubert M., Pramatarova A., and Howell B.W. Interaction between Dab1 and CrkII is promoted by Reelin signaling. J. Cell. Sci. 117 (2004) 4527-4536
31. Chen G., Sima J., Jin M., Wang K.Y., Xue X.J., Zheng W., Ding Y.Q., and Yuan X.B. Semaphorin-3A guides radial migration of cortical neurons during development. Nat. Neurosci. 11 (2008) 36-44
32. Chin J., Massaro C.M., Palop J.J., Thwin M.T., Yu G.Q., Bien-Ly N., Bender A., and Mucke L. Reelin depletion in the entorhinal cortex of human amyloid precursor protein transgenic mice and humans with Alzheimer's disease. J. Neurosci. 27 (2007) 2727-2733
33. Cobos I., Borello U., and Rubenstein J.L. Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 54 (2007) 873-888
34. Corbo J.C., Deuel T.A., Long J.M., LaPorte P., Tsai E., Wynshaw-Boris A., and Walsh C.A. Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. J. Neurosci. 22 (2002) 7548-7557
35. Costell M., Gustafsson E., Aszodi A., Morgelin M., Bloch W., Hunziker E., Addicks K., Timpl R., and Fassler R. Perlecan maintains the integrity of cartilage and some basement membranes. J. Cell. Biol. 147 (1999) 1109-1122
36. D'Arcangelo G., Miao G.G., Chen S.C., Soares H.D., Morgan J.I., and Curran T. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature 374 (1995) 719-723
37. D'Arcangelo G., Homayouni R., Keshvara L., Rice D.S., Sheldon M., and Curran T. Reelin is a ligand for lipoprotein receptors. Neuron 24 (1999) 471-479
38. De Arcangelis A., Mark M., Kreidberg J., Sorokin L., and Georges-Labouesse E. Synergistic activities of alpha3 and alpha6 integrins are required during apical ectodermal ridge formation and organogenesis in the mouse. Development 126 (1999) 3957-3968
39. de Carlos J.A., Lopez-Mascaraque L., and Valverde F. Dynamics of cell migration from the lateral ganglionic eminence in the rat. J. Neurosci. 16 (1996) 6146-6156
40. des Portes V., Pinard J.M., Billuart P., Vinet M.C., Koulakoff A., Carrie A., Gelot A., Dupuis E., Motte J., Berwald-Netter Y., Catala M., Kahn A., Beldjord C., and Chelly J. A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92 (1998) 51-61
41. Deuel T.A., Liu J.S., Corbo J.C., Yoo S.Y., Rorke-Adams L.B., and Walsh C.A. Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 49 (2006) 41-53
42. Dhavan R., and Tsai L.H. A decade of CDK5. Nat. Rev. Mol. Cell. Biol. 2 (2001) 749-759
43. Dulabon L., Olson E.C., Taglienti M.G., Eisenhuth S., McGrath B., Walsh C.A., Kreidberg J.A., and Anton E.S. Reelin binds alpha3beta1 integrin and inhibits neuronal migration. Neuron 27 (2000) 33-44
44. Du T., Xu Q., Ocbina P.J., and Anderson S.A. NKX2.1 specifies cortical interneuron fate by activating Lhx6. Development 135 (2008) 1559-1567
45. Efimov V.P., and Morris N.R. The LIS1-related NUDF protein of Aspergillus nidulans interacts with the coiled-coil domain of the NUDE/RO11 protein. J. Cell. Biol. 150 (2000) 681-688
46. Elias L.A., Wang D.D., and Kriegstein A.R. Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448 (2007) 901-907
47. Feng L., Allen N.S., Simo S., and Cooper J.A. Cullin 5 regulates Dab1 protein levels and neuron positioning during cortical development. Genes. Dev. 21 (2007) 2717-2730
48. Feng Y., Olson E.C., Stukenberg P.T., Flanagan L.A., Kirschner M.W., and Walsh C.A. LIS1 regulates CNS lamination by interacting with mNudE, a central component of the centrosome. Neuron 28 (2000) 665-679
49. Flames N., Long J.E., Garratt A.N., Fischer T.M., Gassmann M., Birchmeier C., Lai C., Rubenstein J.L., and Marin O. Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44 (2004) 251-261
50. Francis F., Koulakoff A., Boucher D., Chafey P., Schaar B., Vinet M.C., Friocourt G., McDonnell N., Reiner O., Kahn A., McConnell S.K., Berwald-Netter Y., Denoulet P., and Chelly J. Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23 (1999) 247-256
51. Friocourt G., Liu J.S., Antypa M., Rakic S., Walsh C.A., and Parnavelas J.G. Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J. Neurosci. 27 (2007) 3875-3883
52. Fushiki S., Perez Velazquez J.L., Zhang L., Bechberger J.F., Carlen P.L., and Naus C.C. Changes in neuronal migration in neocortex of connexin43 null mutant mice. J. Neuropathol. Exp. Neurol. 62 (2003) 304-314
53. Gambello M.J., Darling D.L., Yingling J., Tanaka T., Gleeson J.G., and Wynshaw-Boris A. Multiple dose-dependent effects of Lis1 on cerebral cortical development. J. Neurosci. 23 (2003) 1719-1729
54. Garcia-Moreno F., Lopez-Mascaraque L., and De Carlos J.A. Origins and migratory routes of murine Cajal-Retzius cells. J. Comp. Neurol. 500 (2007) 419-432
55. Georges-Labouesse E., Mark M., Messaddeq N., and Gansmuller A. Essential role of alpha 6 integrins in cortical and retinal lamination. Curr. Biol. 8 (1998) 983-986
56. Gilmore E.C., and Herrup K. Neocortical cell migration: GABAergic neurons and cells in layers I and VI move in a cyclin-dependent kinase 5-independent manner. J. Neurosci. 21 (2001) 9690-9700
57. Gilmore E.C., Ohshima T., Goffinet A.M., Kulkarni A.B., and Herrup K. Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in cerebral cortex. J. Neurosci. 18 (1998) 6370-6377
58. Gleeson J.G., Allen K.M., Fox J.W., Lamperti E.D., Berkovic S., Scheffer I., Cooper E.C., Dobyns W.B., Minnerath S.R., Ross M.E., and Walsh C.A. Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell 92 (1998) 63-72
59. Gleeson J.G., Lin P.T., Flanagan L.A., and Walsh C.A. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23 (1999) 257-271
60. Gongidi V., Ring C., Moody M., Brekken R., Sage E.H., Rakic P., and Anton E.S. SPARC-like 1 regulates the terminal phase of radial glia-guided migration in the cerebral cortex. Neuron 41 (2004) 57-69
61. Graus-Porta D., Blaess S., Senften M., Littlewood-Evans A., Damsky C., Huang Z., Orban P., Klein R., Schittny J.C., and Muller U. Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31 (2001) 367-379
62. Grunewald M., Avraham I., Dor Y., Bachar-Lustig E., Itin A., Jung S., Chimenti S., Landsman L., Abramovitch R., and Keshet E. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124 (2006) 175-189
63. Gupta A., Sanada K., Miyamoto D.T., Rovelstad S., Nadarajah B., Pearlman A.L., Brunstrom J., and Tsai L.H. Layering defect in p35 deficiency is linked to improper neuronal-glial interaction in radial migration. Nat. Neurosci. 6 (2003) 1284-1291
64. Hack I., Bancila M., Loulier K., Carroll P., and Cremer H. Reelin is a detachment signal in tangential chain-migration during postnatal neurogenesis. Nat. Neurosci. 5 (2002) 939-945
65. Hack I., Hellwig S., Junghans D., Brunne B., Bock H.H., Zhao S., and Frotscher M. Divergent roles of ApoER2 and Vldlr in the migration of cortical neurons. Development 134 (2007) 3883-3891
66. Halfter W., Dong S., Yip Y.P., Willem M., and Mayer U. A critical function of the pial basement membrane in cortical histogenesis. J. Neurosci. 22 (2002) 6029-6040
67. Hammond V., Tsai L.H., and Tan S.S. Control of cortical neuron migration and layering: cell and non cell-autonomous effects of p35. J. Neurosci. 24 (2004) 576-587
68. Hammond V., So E., Gunnersen J., Valcanis H., Kalloniatis M., and Tan S.S. Layer positioning of late-born cortical interneurons is dependent on Reelin but not p35 signaling. J. Neurosci. 26 (2006) 1646-1655
69. Hashimoto-Torii K., Torii M., Sarkisian M.R., Bartley C.M., Shen J., Radtke F., Gridley T., Sestan N., and Rakic P. Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 60 (2008) 273-284
70. Hasling T.A., Gierdalski M., Jablonska B., and Juliano S.L. A radialization factor in normal cortical plate restores disorganized radial glia and disrupted migration in a model of cortical dysplasia. Eur. J. Neurosci. 17 (2003) 467-480
71. Hattori M., Adachi H., Tsujimoto M., Arai H., and Inoue K. Miller-Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor acetylhydrolase [corrected]. Nature 370 (1994) 216-218
72. Haubst N., Georges-Labouesse E., De Arcangelis A., Mayer U., and Gotz M. Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes. Development 133 (2006) 3245-3254
73. Herms J., Anliker B., Heber S., Ring S., Fuhrmann M., Kretzschmar H., Sisodia S., and Muller U. Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members. EMBO J. 23 (2004) 4106-4115
74. Hiesberger T., Trommsdorff M., Howell B.W., Goffinet A., Mumby M.C., Cooper J.A., and Herz J. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron 24 (1999) 481-489
75. Hirotsune S., Fleck M.W., Gambello M.J., Bix G.J., Chen A., Clark G.D., Ledbetter D.H., McBain C.J., and Wynshaw-Boris A. Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat. Genet. 19 (1998) 333-339
76. Hong S.E., Shugart Y.Y., Huang D.T., Shahwan S.A., Grant P.E., Hourihane J.O., Martin N.D., and Walsh C.A. Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat. Genet. 26 (2000) 93-96
77. Howell B.W., Hawkes R., Soriano P., and Cooper J.A. Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389 (1997) 733-737
78. Howell B.W., Herrick T.M., and Cooper J.A. Reelin-induced tyrosine [corrected] phosphorylation of disabled 1 during neuronal positioning. Genes Dev. 13 (1999) 643-648
79. Huang Y., Magdaleno S., Hopkins R., Slaughter C., Curran T., and Keshvara L. Tyrosine phosphorylated Disabled 1 recruits Crk family adapter proteins. Biochem. Biophys. Res. Commun. 318 (2004) 204-212
80. Huang Z., Shimazu K., Woo N.H., Zang K., Muller U., Lu B., and Reichardt L.F. Distinct roles of the beta 1-class integrins at the developing and the mature hippocampal excitatory synapse. J. Neurosci. 26 (2006) 11208-11219
81. Jossin Y., and Goffinet A.M. Reelin signals through phosphatidylinositol 3-kinase and Akt to control cortical development and through mTor to regulate dendritic growth. Mol. Cell. Biol. 27 (2007) 7113-7124
82. Jossin Y., Ogawa M., Metin C., Tissir F., and Goffinet A.M. Inhibition of SRC family kinases and non-classical protein kinases C induce a reeler-like malformation of cortical plate development. J. Neurosci. 23 (2003) 9953-9959
83. Kalil K., and Dent E.W. Touch and go: guidance cues signal to the growth cone cytoskeleton. Curr. Opin. Neurobiol. 15 (2005) 521-526
84. Kamiya A., Kubo K., Tomoda T., Takaki M., Youn R., Ozeki Y., Sawamura N., Park U., Kudo C., Okawa M., Ross C.A., Hatten M.E., Nakajima K., and Sawa A. A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat. Cell. Biol. 7 (2005) 1167-1178
85. Kappeler C., Saillour Y., Baudoin J.P., Tuy F.P., Alvarez C., Houbron C., Gaspar P., Hamard G., Chelly J., Metin C., and Francis F. Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice. Hum. Mol. Genet. 15 (2006) 1387-1400
86. Keays D.A., Tian G., Poirier K., Huang G.J., Siebold C., Cleak J., Oliver P.L., Fray M., Harvey R.J., Molnar Z., Pinon M.C., Dear N., Valdar W., Brown S.D., Davies K.E., Rawlins J.N., Cowan N.J., Nolan P., Chelly J., and Flint J. Mutations in alpha-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans. Cell 128 (2007) 45-57
87. Keshvara L., Magdaleno S., Benhayon D., and Curran T. Cyclin-dependent kinase 5 phosphorylates disabled 1 independently of Reelin signaling. J. Neurosci. 22 (2002) 4869-4877
88. Kitamura K., Yanazawa M., Sugiyama N., Miura H., Iizuka-Kogo A., Kusaka M., Omichi K., Suzuki R., Kato-Fukui Y., Kamiirisa K., Matsuo M., Kamijo S., Kasahara M., Yoshioka H., Ogata T., Fukuda T., Kondo I., Kato M., Dobyns W.B., Yokoyama M., and Morohashi K. Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans. Nat. Genet. 32 (2002) 359-369
89. Kleiner-Fisman G., and Lang A.E. Benign hereditary chorea revisited: a journey to understanding. Mov. Disord. 22 (2007) 2297-2305 quiz 2452
90. Kobayashi K., Nakahori Y., Miyake M., Matsumura K., Kondo-Iida E., Nomura Y., Segawa M., Yoshioka M., Saito K., Osawa M., Hamano K., Sakakihara Y., Nonaka I., Nakagome Y., Kanazawa I., Nakamura Y., Tokunaga K., and Toda T. An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature 394 (1998) 388-392
91. Koizumi H., Tanaka T., and Gleeson J.G. Doublecortin-like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron 49 (2006) 55-66
92. Ko J., Humbert S., Bronson R.T., Takahashi S., Kulkarni A.B., Li E., and Tsai L.H. p35 and p39 are essential for cyclin-dependent kinase 5 function during neurodevelopment. J. Neurosci. 21 (2001) 6758-6771
93. Krude H., Schutz B., Biebermann H., von Moers A., Schnabel D., Neitzel H., Tonnies H., Weise D., Lafferty A., Schwarz S., DeFelice M., von Deimling A., van Landeghem F., DiLauro R., and Gruters A. Choreoathetosis, hypothyroidism, and pulmonary alterations due to human NKX2-1 haploinsufficiency. J. Clin. Invest. 109 (2002) 475-480
94. Kuo G., Arnaud L., Kronstad-O'Brien P., and Cooper J.A. Absence of Fyn and Src causes a reeler-like phenotype. J. Neurosci. 25 (2005) 8578-8586
95. Kwon Y.T., and Tsai L.H. A novel disruption of cortical development in p35(-/-) mice distinct from reeler. J. Comp. Neurol. 395 (1998) 510-522
96. Letinic K., Zoncu R., and Rakic P. Origin of GABAergic neurons in the human neocortex. Nature 417 (2002) 645-649
97. Li G., Adesnik H., Li J., Long J., Nicoll R.A., Rubenstein J.L., and Pleasure S.J. Regional distribution of cortical interneurons and development of inhibitory tone are regulated by Cxcl12/Cxcr4 signaling. J. Neurosci. 28 (2008) 1085-1098
98. Li S., Jin Z., Koirala S., Bu L., Xu L., Hynes R.O., Walsh C.A., Corfas G., and Piao X. GPR56 regulates pial basement membrane integrity and cortical lamination. J. Neurosci. 28 (2008) 5817-5826
99. Lopez-Bendito G., Sanchez-Alcaniz J.A., Pla R., Borrell V., Pico E., Valdeolmillos M., and Marin O. Chemokine signaling controls intracortical migration and final distribution of GABAergic interneurons. J. Neurosci. 28 (2008) 1613-1624
100. Malatesta P., Hartfuss E., and Gotz M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127 (2000) 5253-5263
101. Manent J.B., Wang Y., Chang Y., Paramasivam M., and LoTurco J.J. Dcx reexpression reduces subcortical band heterotopia and seizure threshold in an animal model of neuronal migration disorder. Nat. Med. 15 (2009) 84-90
102. Marin O., and Rubenstein J.L. Cell migration in the forebrain. Annu. Rev. Neurosci. 26 (2003) 441-483
103. Marin O., Yaron A., Bagri A., Tessier-Lavigne M., and Rubenstein J.L. Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science 293 (2001) 872-875
104. Martini F.J., Valiente M., Lopez Bendito G., Szabo G., Moya F., Valdeolmillos M., and Marin O. Biased selection of leading process branches mediates chemotaxis during tangential neuronal migration. Development 136 (2009) 41-50
105. McManus M.F., Nasrallah I.M., Pancoast M.M., Wynshaw-Boris A., and Golden J.A. Lis1 is necessary for normal non-radial migration of inhibitory interneurons. Am. J. Pathol. 165 (2004) 775-784
106. Metin C., Baudoin J.P., Rakic S., and Parnavelas J.G. Cell and molecular mechanisms involved in the migration of cortical interneurons. Eur. J. Neurosci. 23 (2006) 894-900
107. Michele D.E., Barresi R., Kanagawa M., Saito F., Cohn R.D., Satz J.S., Dollar J., Nishino I., Kelley R.I., Somer H., Straub V., Mathews K.D., Moore S.A., and Campbell K.P. Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418 (2002) 417-422
108. Miner J.H., Cunningham J., and Sanes J.R. Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. J. Cell. Biol. 143 (1998) 1713-1723
109. Miyata T., and Ogawa M. Twisting of neocortical progenitor cells underlies a spring-like mechanism for daughter-cell migration. Curr. Biol. 17 (2007) 146-151
110. Miyata T., Kawaguchi A., Okano H., and Ogawa M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31 (2001) 727-741
111. Moers A., Nurnberg A., Goebbels S., Wettschureck N., and Offermanns S. Galpha12/Galpha13 deficiency causes localized overmigration of neurons in the developing cerebral and cerebellar cortices. Mol. Cell. Biol. 28 (2008) 1480-1488
112. Moore S.A., Saito F., Chen J., Michele D.E., Henry M.D., Messing A., Cohn R.D., Ross-Barta S.E., Westra S., Williamson R.A., Hoshi T., and Campbell K.P. Deletion of brain dystroglycan recapitulates aspects of congenital muscular dystrophy. Nature 418 (2002) 422-425
113. Nadarajah B., Brunstrom J.E., Grutzendler J., Wong R.O., and Pearlman A.L. Two modes of radial migration in early development of the cerebral cortex. Nat. Neurosci. 4 (2001) 143-150
114. Niethammer M., Smith D.S., Ayala R., Peng J., Ko J., Lee M.S., Morabito M., and Tsai L.H. NUDEL is a novel Cdk5 substrate that associates with LIS1 and cytoplasmic dynein. Neuron 28 (2000) 697-711
115. Niewmierzycka A., Mills J., St-Arnaud R., Dedhar S., and Reichardt L.F. Integrin-linked kinase deletion from mouse cortex results in cortical lamination defects resembling cobblestone lissencephaly. J. Neurosci. 25 (2005) 7022-7031
116. Niu S., Renfro A., Quattrocchi C.C., Sheldon M., and D'Arcangelo G. Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway. Neuron 41 (2004) 71-84
117. Niu S., Yabut O., and D'Arcangelo G. The Reelin signaling pathway promotes dendritic spine development in hippocampal neurons. J. Neurosci. 28 (2008) 10339-10348
118. Nobrega-Pereira S., Kessaris N., Du T., Kimura S., Anderson S.A., and Marin O. Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors. Neuron 59 (2008) 733-745
119. Noctor S.C., Flint A.C., Weissman T.A., Dammerman R.S., and Kriegstein A.R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409 (2001) 714-720
120. Noctor S.C., Martinez-Cerdeno V., Ivic L., and Kriegstein A.R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7 (2004) 136-144
121. Ogawa M., Miyata T., Nakajima K., Yagyu K., Seike M., Ikenaka K., Yamamoto H., and Mikoshiba K. The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14 (1995) 899-912
122. Ohshima T., Ward J.M., Huh C.G., Longenecker G., Veeranna Pant H.C., Brady R.O., Martin L.J., and Kulkarni A.B. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 11173-11178
123. Ohshima T., Ogawa M., Veeranna Hirasawa M., Longenecker G., Ishiguro K., Pant H.C., Brady R.O., Kulkarni A.B., and Mikoshiba K. Synergistic contributions of cyclin-dependant kinase 5/p35 and Reelin/Dab1 to the positioning of cortical neurons in the developing mouse brain. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 2764-2769
124. Ohshima T., Hirasawa M., Tabata H., Mutoh T., Adachi T., Suzuki H., Saruta K., Iwasato T., Itohara S., Hashimoto M., Nakajima K., Ogawa M., Kulkarni A.B., and Mikoshiba K. 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 (2007) 2273-2282
125. Paredes M.F., Li G., Berger O., Baraban S.C., and Pleasure S.J. Stromal-derived factor-1 (CXCL12) regulates laminar position of Cajal-Retzius cells in normal and dysplastic brains. J. Neurosci. 26 (2006) 9404-9412
126. Piao X., Hill R.S., Bodell A., Chang B.S., Basel-Vanagaite L., Straussberg R., Dobyns W.B., Qasrawi B., Winter R.M., Innes A.M., Voit T., Ross M.E., Michaud J.L., Descarie J.C., Barkovich A.J., and Walsh C.A. G protein-coupled receptor-dependent development of human frontal cortex. Science 303 (2004) 2033-2036
127. Pla R., Borrell V., Flames N., and Marin O. Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J. Neurosci. 26 (2006) 6924-6934
128. Polleux F., Morrow T., and Ghosh A. Semaphorin 3A is a chemoattractant for cortical apical dendrites. Nature 404 (2000) 567-573
129. Polleux F., Whitford K.L., Dijkhuizen P.A., Vitalis T., and Ghosh A. Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling. Development 129 (2002) 3147-3160
130. Powell E.M., Mars W.M., and Levitt P. Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 30 (2001) 79-89
131. Powell E.M., Campbell D.B., Stanwood G.D., Davis C., Noebels J.L., and Levitt P. Genetic disruption of cortical interneuron development causes region- and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J. Neurosci. 23 (2003) 622-631
132. Pozas E., and Ibanez C.F. GDNF and GFRalpha1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 45 (2005) 701-713
133. Rakic P. Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol. 145 (1972) 61-83
134. Rakic P. Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183 (1974) 425-427
135. Rakic P. The radial edifice of cortical architecture: from neuronal silhouettes to genetic engineering. Brain Res. Rev. 55 (2007) 204-219
136. Rakic S., Yanagawa Y., Obata K., Faux C., Parnavelas J.G., and Nikolic M. Cortical interneurons require p35/Cdk5 for their migration and laminar organization. Cereb. Cortex (2008). http://doi:10.1093/cercor/bhn213 Advance Access published November 26, 2008. doi:10.1093/cercor/bhn213
137. Ramos R.L., Bai J., and LoTurco J.J. Heterotopia formation in rat but not mouse neocortex after RNA interference knockdown of DCX. Cereb. Cortex 16 (2006) 1323-1331
138. Reiner O., Carrozzo R., Shen Y., Wehnert M., Faustinella F., Dobyns W.B., Caskey C.T., and Ledbetter D.H. Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature 364 (1993) 717-721
139. Rice D.S., and Curran T. Role of the reelin signaling pathway in central nervous system development. Annu. Rev. Neurosci. 24 (2001) 1005-1039
140. Rymar V.V., and Sadikot A.F. Laminar fate of cortical GABAergic interneurons is dependent on both birthdate and phenotype. J. Comp. Neurol. 501 (2007) 369-380
141. Sanada K., Gupta A., and Tsai L.H. Disabled-1-regulated adhesion of migrating neurons to radial glial fiber contributes to neuronal positioning during early corticogenesis. Neuron 42 (2004) 197-211
142. Sapir T., Sapoznik S., Levy T., Finkelshtein D., Shmueli A., Timm T., Mandelkow E.M., and Reiner O. Accurate balance of the polarity kinase MARK2/Par-1 is required for proper cortical neuronal migration. J. Neurosci. 28 (2008) 5710-5720
143. Sasaki S., Shionoya A., Ishida M., Gambello M.J., Yingling J., Wynshaw-Boris A., and Hirotsune S. A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28 (2000) 681-696
144. Schaar B.T., Kinoshita K., and McConnell S.K. Doublecortin microtubule affinity is regulated by a balance of kinase and phosphatase activity at the leading edge of migrating neurons. Neuron 41 (2004) 203-213
145. Schmid R.S., Shelton S., Stanco A., Yokota Y., Kreidberg J.A., and Anton E.S. alpha3beta1 integrin modulates neuronal migration and placement during early stages of cerebral cortical development. Development 131 (2004) 6023-6031
146. Senzaki K., Ogawa M., and Yagi T. Proteins of the CNR family are multiple receptors for Reelin. Cell 99 (1999) 635-647
147. Sheldon M., Rice D.S., D'Arcangelo G., Yoneshima H., Nakajima K., Mikoshiba K., Howell B.W., Cooper J.A., Goldowitz D., and Curran T. Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389 (1997) 730-733
148. Shu T., Ayala R., Nguyen M.D., Xie Z., Gleeson J.G., and Tsai L.H. Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning. Neuron 44 (2004) 263-277
149. Solecki D.J., Model L., Gaetz J., Kapoor T.M., and Hatten M.E. Par6alpha signaling controls glial-guided neuronal migration. Nat. Neurosci. 7 (2004) 1195-1203
150. Soriano E., and Del Rio J.A. The cells of Cajal-Retzius: still a mystery one century after. Neuron 46 (2005) 389-394
151. Soriano E., Alvarado-Mallart R.M., Dumesnil N., Del Rio J.A., and Sotelo C. Cajal-Retzius cells regulate the radial glia phenotype in the adult and developing cerebellum and alter granule cell migration. Neuron 18 (1997) 563-577
152. Stumm R.K., Zhou C., Ara T., Lazarini F., Dubois-Dalcq M., Nagasawa T., Hollt V., and Schulz S. CXCR4 regulates interneuron migration in the developing neocortex. J. Neurosci. 23 (2003) 5123-5130
153. Tabata H., and Nakajima K. Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex. J. Neurosci. 23 (2003) 9996-10001
154. Takiguchi-Hayashi K., Sekiguchi M., Ashigaki S., Takamatsu M., Hasegawa H., Suzuki-Migishima R., Yokoyama M., Nakanishi S., and Tanabe Y. Generation of reelin-positive marginal zone cells from the caudomedial wall of telencephalic vesicles. J. Neurosci. 24 (2004) 2286-2295
155. Tamamaki N., Fujimori K.E., and Takauji R. Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J. Neurosci. 17 (1997) 8313-8323
156. Tanaka T., Serneo F.F., Higgins C., Gambello M.J., Wynshaw-Boris A., and Gleeson J.G. Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J. Cell. Biol. 165 (2004) 709-721
157. Tanaka T., Serneo F.F., Tseng H.C., Kulkarni A.B., Tsai L.H., and Gleeson J.G. Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration. Neuron 41 (2004) 215-227
158. Tanaka D.H., Maekawa K., Yanagawa Y., Obata K., and Murakami F. Multidirectional and multizonal tangential migration of GABAergic interneurons in the developing cerebral cortex. Development 133 (2006) 2167-2176
159. Taya S., Shinoda T., Tsuboi D., Asaki J., Nagai K., Hikita T., Kuroda S., Kuroda K., Shimizu M., Hirotsune S., Iwamatsu A., and Kaibuchi K. DISC1 regulates the transport of the NUDEL/LIS1/14-3-3epsilon complex through kinesin-1. J. Neurosci. 27 (2007) 15-26
160. Tissir F., and Goffinet A.M. Reelin and brain development. Nat. Rev. Neurosci. 4 (2003) 496-505
161. Tiveron M.C., Rossel M., Moepps B., Zhang Y.L., Seidenfaden R., Favor J., Konig N., and Cremer H. Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/intermediate zone. J. Neurosci. 26 (2006) 13273-13278
162. Trommsdorff M., Gotthardt M., Hiesberger T., Shelton J., Stockinger W., Nimpf J., Hammer R.E., Richardson J.A., and Herz J. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97 (1999) 689-701
163. Tsai L.H., and Gleeson J.G. Nucleokinesis in neuronal migration. Neuron 46 (2005) 383-388
164. Tsai J.W., Chen Y., Kriegstein A.R., and Vallee R.B. LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J. Cell. Biol. 170 (2005) 935-945
165. Tsai J.W., Bremner K.H., and Vallee R.B. Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat. Neurosci. 10 (2007) 970-979
166. Umeshima H., Hirano T., and Kengaku M. Microtubule-based nuclear movement occurs independently of centrosome positioning in migrating neurons. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 16182-16187
167. van Reeuwijk J., Janssen M., van den Elzen C., Beltran-Valero de Bernabe D., Sabatelli P., Merlini L., Boon M., Scheffer H., Brockington M., Muntoni F., Huynen M.A., Verrips A., Walsh C.A., Barth P.G., Brunner H.G., and van Bokhoven H. POMT2 mutations cause alpha-dystroglycan hypoglycosylation and Walker-Warburg syndrome. J. Med. Genet. 42 (2005) 907-912
168. Voss A.K., Britto J.M., Dixon M.P., Sheikh B.N., Collin C., Tan S.S., and Thomas T. C3G regulates cortical neuron migration, preplate splitting and radial glial cell attachment. Development 135 (2008) 2139-2149
169. Xie Z., Sanada K., Samuels B.A., Shih H., and Tsai L.H. Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 114 (2003) 469-482
170. Yingling J., Youn Y.H., Darling D., Toyo-Oka K., Pramparo T., Hirotsune S., and Wynshaw-Boris A. Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132 (2008) 474-486
171. Yokota Y., Gashghaei H.T., Han C., Watson H., Campbell K.J., and Anton E.S. Radial glial dependent and independent dynamics of interneuronal migration in the developing cerebral cortex. PLoS ONE 2 (2007) e794
172. Yoshida A., Kobayashi K., Manya H., Taniguchi K., Kano H., Mizuno M., Inazu T., Mitsuhashi H., Takahashi S., Takeuchi M., Herrmann R., Straub V., Talim B., Voit T., Topaloglu H., Toda T., and Endo T. Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev. Cell. 1 (2001) 717-724
173. Yoshida M., Assimacopoulos S., Jones K.R., and Grove E.A. Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order. Development 133 (2006) 537-545
174. Young-Pearse T.L., Bai J., Chang R., Zheng J.B., LoTurco J.J., and Selkoe D.J. A critical function for beta-amyloid precursor protein in neuronal migration revealed by in utero RNA interference. J. Neurosci. 27 (2007) 14459-14469
175. Zhang G., Assadi A.H., McNeil R.S., Beffert U., Wynshaw-Boris A., Herz J., Clark G.D., and D'Arcangelo G. The Pafah1b complex interacts with the Reelin receptor VLDLR. PLoS ONE 2 (2007) e252
176. Zhao S., Chai X., Forster E., and Frotscher M. Reelin is a positional signal for the lamination of dentate granule cells. Development 131 (2004) 5117-5125
177. Zhao C., Guan W., and Pleasure S.J. A transgenic marker mouse line labels Cajal-Retzius cells from the cortical hem and thalamocortical axons. Brain Res. 1077 (2006) 48-53