Lissencephaly and the molecular basis of neuronal migration

Human Molecular Genetics

Volumn 12, Issue REV. ISS. 1, 2003, Pages

  Kato, Mitsuhiro ^a,b   Dobyns, William B ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b YAMAGATA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; PROTEIN ARX; PROTEIN DCX; PROTEIN LIS1; PROTEIN RELN; UNCLASSIFIED DRUG;

AGYRIA; BRAIN CORTEX; BRAIN DEVELOPMENT; BRAIN MALFORMATION; BRAIN NERVE CELL; BRAIN VENTRICLE; CELL MIGRATION; CHROMOSOME 17P; CHROMOSOME DELETION; CLINICAL FEATURE; DISEASE CLASSIFICATION; DISEASE SEVERITY; EMBRYO DEVELOPMENT; GENE MUTATION; GENOTYPE; HUMAN; IMAGING; MILLER DIEKER SYNDROME; MITOSIS; MOLECULAR GENETICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; 14-3-3 PROTEINS; BRAIN; BRAIN DISEASES; CELL ADHESION MOLECULES, NEURONAL; CELL MOVEMENT; CEREBRAL CORTEX; CHROMOSOMES, HUMAN, PAIR 17; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENE DELETION; GENOTYPE; HOMEODOMAIN PROTEINS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MITOSIS; MODELS, GENETIC; NERVE TISSUE PROTEINS; NERVOUS SYSTEM MALFORMATIONS; NEURONS; NEUROPEPTIDES; PHENOTYPE; SERINE ENDOPEPTIDASES; SYNDROME; TRANSCRIPTION FACTORS; TYROSINE 3-MONOOXYGENASE;

ACRONICTA LEPORINA;

EID: 0037390829     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (94)

1. Crome, L. (1956) Pachygyria. J. Pathol. Bacteriol., 71, 335-352.
2. Friede, R.L. (1989) Developmental Neuropathology, 2nd edn. Springer, Berlin.
3. Dobyns, W.B., Andermann, E., Andermann, F., Czapansky-Beilman, D., Dubeau, F., Dulac, O., Guerrini, R., Hirsch, B., Ledbetter, D.H., Lee, N.S. et al. (1996) X-linked malformations of neuronal migration. Neurology, 47, 331-339.
4. Barkovich, A.J., Guerrini, R., Battaglia, G., Kalifa, G., N'Guyen, T., Parmeggiani, A., Santucci, M., Giovanardi-Rossi, P., Granata, T. and D'Incerti, L. (1994) Band heterotopia: correlation of outcome with magnetic resonance imaging parameters. Ann. Neurol., 36, 609-617.
5. Dobyns, W.B., Berry-Kravis, E., Havernick, N.J., Holden, K.R. and Viskochil, D. (1999) X-linked lissencephaly with absent corpus callosum and ambiguous genitalia. Am. J. Med. Genet., 86, 331-337.
6. Ross, M.F., Swanson, K. and Dobyns, W.B. (2001) Lissencephaly with cerebellar hypoplasia (LCH): a heterogeneous group of cortical malformations. Neuropediatrics, 32, 256-263.
7. Sheen, V.L., Dixon, P.H., Fox, J.W, Hong, S.E., Kinton, L., Sisodiya, S.M., Duncan, J.S., Dubeau, F., Scheffer, I.E., Schachter, S.C. et al. (2001) Mutations in the X-linked filamin 1 gene cause periventricular nodular heterotopia in males as well as in females. Hum. Mol. Genet., 10, 1775-1783.
8. Ross, M.E. and Walsh, C.A. (2001) Human brain malformations and their lessons for neuronal migration. A. Rev. Neurosci., 24, 1041-1070.
9. Herz, J. and Bock, H.H. (2002) Lipoprotein receptors in the nervous system. A. Rev. Biochem., 71, 405-434.
10. Gupta, A., Tsai, L.H. and Wynshaw-Boris, A. (2002) Life is a journey: a genetic look at neocortical development. Nat. Rev. Genet., 3, 342-355.
11. Ross, M.E. (2002) Full circle to cobbled brain. Nature, 418, 376-377.
12. Reiner, O., Carrozzo, R., Shen, Y., Wehnert, M., Faustinella, F., Dobyns, W.B., Caskey, C.T. and Ledbetter, D.H. (1993) Isolation of a Miller-Dieker lissencephaly gene containing G protein beta-subunit-like repeats. Nature, 364, 717-721.
13. Hattori, M., Adachi, H., Tsujimoto, M., Arai, H. and Inoue, K. (1994) Miller-Dieker lissencephaly gene encodes a subunit of brain platelet-activating factor acetylhydrolase. Nature, 370, 216-218.
14. Mizuguchi, M., Takashima, S., Kakita, A., Yamada, M. and Ikeda, K. (1995) Lissencephaly gene product. Localization in the central nervous system and loss of immunoreactivity in Miller-Dieker syndrome. Am. J. Pathol., 147, 1142-1151.
15. Sapir, T., Elbaum, M. and Reiner, O. (1997) Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit. EMBO J., 16, 6977-6984.
16. Xiang, X., Osmani, A.H., Osmani, S.A., Xin, M. and Morris, N.R. (1995) NudF, a nuclear migration gene in Aspergillus nidulans, is similar to the human LIS-1 gene required for neuronal migration. Mol. Biol. Cell, 6, 297-310.
17. Smith, D.S., Niethammer, M., Ayala, R., Zhou, Y., Gambello, M.J., Wynshaw-Boris, A. and Tsai, L.H. (2000) Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian Lis1. Nat. Cell Biol., 2, 767-775.
18. Faulkner, N.E., Dujardin, D.L., Tai, C.Y., Vaughan, K.T., O'Connell, C.B., Wang, Y. and Vallee, R.B. (2000) A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell Biol., 2, 784-791.
19. Sasaki, S., Shionoya, A., Ishida, M., Gambello, M.J., Yingling, J., Wynshaw-Boris, A. and Hirotsune, S. (2000) A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron, 28, 681-696.
20. Sweeney, K.J., Prokscha, A. and Eichele, G. (2001) NudE-L, a novel Lis1-interacting protein, belongs to a family of vertebrate coiled-coil proteins. Mech. Dev, 101, 21-33.
21. Hoffmann, B., Zuo, W., Liu, A. and Morris, N.R. (2001) The LIS1-related protein NUDF of Aspergillus nidulans and its interaction partner NUDE bind directly to specific subunits of dynein and dynactin and to alpha- and gamma-tubulin. J. Biol. Chem., 276, 38877-38884.
22. Feng, Y., Olson, E.C., Stukenberg, P.T., Flanagan, L.A., Kirschner, M.W. and Walsh, C.A. (2000) LIS1 regulates CNS lamination by interacting with mNudE, a central component of the centrosome. Neuron, 28, 665-679.
23. Efimov, V.P. and Morris, N.R. (2000) The LIS1-related NUDF protein of Aspergillus nidulans interacts with the coiled-coil domain of the NUDE/RO11 protein. J. Cell Biol., 150, 681-688.
24. Kitagawa, M., Umezu, M., Aoki, J., Koizumi, H., Arai, H. and Inoue, K. (2000) Direct association of LIS1, the lissencephaly gene product, with a mammalian homologue of a fungal nuclear distribution protein, rNUDE. FEBS Lett., 479, 57-62.
25. Tai, C.Y., Dujardin, D.L., Faulkner, N.E. and Vallee, R.B. (2002) Role of dynein, dynactin, and CLIP-170 interactions in LIS1 kinetochore function. J. Cell Biol., 156, 959-968.
26. Coquelle, F.M., Caspi, M., Cordelieres, F.P., Dompierre, J.P., Dujardin, D.L., Koifman, C., Martin, P., Hoogenraad, C.C., Akhmanova, A., Galjart, N. et al. (2002) LIS1, CLIP-170's key to the dynein/dynactin pathway. Mol. Cell Biol., 22, 3089-3102.
27. Yaffe, M.B. and Elia, A.E. (2001) Phosphoserine/threonine-binding domains. Curr. Opin. Cell Biol., 13, 131-138.
28. Tzivion, G. and Avruch, J. (2002) 14-3-3 proteins: active cofactors in cellular regulation by serine/threonine phosphorylation.J. Biol. Chem., 277, 3061-3064.
29. Shaw, A. (2000) The 14-3-3 proteins. Curr. Biol., 10, R400.
30. Muslin, A.J. and Xing, H. (2000) 14-3-3 proteins: regulation of subcellular localization by molecular interference. Cell. Signal., 12, 703-709.
31. Fu, H., Subramanian, R.R. and Masters, S.C. (2000) 14-3-3 proteins: structure, function, and regulation. A. Rev. Pharmac. Toxicol., 40, 617-647.
32. des Portes, V., Pinard, J.M., Billuart, P., Vinet, M.C., Koulakoff, A., Carrie, A., Gelot, A., Dupuis, E., Motte, J., Berwald-Netter, Y. et al. (1998) A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell, 92, 51-61.
33. 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. et al. (1998) Doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell, 92, 63-72.
34. Horesh, D., Sapir, T., Francis, F., Wolf, S.G., Caspi, M., Elbaum, M., Chelly, J. and Reiner, O. (1999) Doublecortin, a stabilizer of microtubules. Hum. Mol. Genet., 8, 1599-1610.
35. Gleeson, J.G., Lin, P.T., Flanagan, L.A. and Walsh, C.A. (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron, 23, 257-271.
36. Sapir, T., Horesh, D., Caspi, M., Atlas, R., Burgess, H.A., Wolf, S.G., Francis, F., Chelly, J., Elbaum, M., Pietrokovski, S. et al. (2000) Doublecortin mutations cluster in evolutionarily conserved functional domains. Hum. Mol. Genet., 9, 703-712.
37. Taylor, K.R., Holzer, A.K., Bazan, J.F., Walsh, C.A. and Gleeson, J.G. (2000) Patient mutations in doublecortin define a repeated tubulin-binding domain. J. Biol. Chem., 275, 34442-34450.
38. Caspi, M., Atlas, R., Kantor, A., Sapir, T. and Reiner, O. (2000) Interaction between LIS1 and doublecortin, two lissencephaly gene products. Hum. Mol. Genet., 9, 2205-2213.
39. D'Arcangelo, G., Miao, G.G., Chen, S.C., Soares, H.D., Morgan, J.I. and Curran, T. (1995) A protein related to extracellular matrix proteins deleted in the mouse mutant reeler. Nature, 374, 719-723.
40. Hirotsune, S., Takahara, T., Sasaki, N., Hirose, K., Yoshiki, A., Ohashi, T., Kusakabe, M., Murakami, Y., Muramatsu, M., Watanabe, S. et al. (1995) The reeler gene encodes a protein with an EGF-like motif expressed by pioneer neurons. Nat. Genet., 10, 77-83.
41. Ogawa, M., Miyata, T., Nakajima, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H. and Mikoshiba, K. (1995) The reeler gene-associated antigen on Caja1-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron, 14, 899-912.
42. DeSilva, U., D'Arcangelo, G., Braden, V.V., Chen, J., Miao, G.G., Curran, T. and Green, E.D. (1997) The human reelin gene: isolation, sequencing, and mapping on chromosome 7. Genome Res., 7, 157-164.
43. Hiesberger, T., Trommsdorff, M., Howell, B.W., Goffinet, A., Mumby, M.C., Cooper, J.A. and Herz, J. (1999) Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation. Neuron, 24, 481-489.
44. Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R.E., Richardson, J.A. and Herz, J. (1999) Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell, 97, 689-701.
45. Rice, D.S., Sheldon, M., D'Arcangelo, G., Nakajima, K., Goldowitz, D. and Curran, T. (1998) Disabled-1 acts downstream of Reelin in a signaling pathway that controls laminar organization in the mammalian brain. Development, 125, 3719-3729.
46. Howell, B.W., Herrick, T.M. and Cooper, J.A. (1999) Reelin-induced tryosine phosphorylation of disabled 1 during neuronal positioning. Genes Dev., 13, 643-648.
47. 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. (1997) Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature, 389, 730-733.
48. Miura, H., Yanazawa, M., Kato, K. and Kitamura, K. (1997) Expression of a novel aristaless related homeobox gene 'Arx' in the vertebrate telencephalon, diencephalon and floor plate. Mech. Dev, 65, 99-109.
49. Stromme, P., Mangelsdorf, M.E., Shaw, M.A., Lower, K.M., Lewis, S.M., Bruyere, H., Lutcherath, V., Gedeon, A.K., Wallace, R.H., Scheffer, I.E. et al. (2002) Mutations in the human ortholog of Aristaless cause X-linked mental retardation and epilepsy. Nat. Genet., 30, 441-445.
50. Kitamura, K., Yanazawa, M., Sugiyama, N., Miura, H., Iizuka-Kogo, A., Kusaka, M., Omichi, K., Suzuki, R., Kato-Fukui, Y., Kamiirisa, K. et al. (2002) Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans. Nat. Genet., 32, 359-369.
51. Pilz, D.T., Matsumoto, N., Minnerath, S., Mills, P., Gleeson, J.G., Allen, K.M., Walsh, C.A., Barkovich, A.J., Dobyns, W.B., Ledbetter, D.H. et al. (1998) LIS1 and XLIS (DCX) mutations cause most classical lissencephaly, but different patterns of malformation. Hum. Mol. Genet., 7, 2029-2037.
52. Dobyns, W.B., Truwit, C.L., Ross, M.E., Matsumoto, N., Pilz, D.T., Ledbetter, D.H., Gleeson, J.G., Walsh, C.A. and Barkovich, A.J. (1999) Differences in the gyral pattern distinguish chromosome 17-linked and X-linked lissencephaly. Neurology, 53, 270-277.
53. Cardoso, C., Leventer, R.J., Matsumoto, N., Kuc, J.A., Ramocki, M.B., Mewborn, S.K., Dudlicek, L.L., May, L.F., Mills, P.L., Das, S. et al. (2000) The location and type of mutation predict malformation severity in isolated lissencephaly caused by abnormalities within the LIS1 gene. Hum. Mol. Genet., 9, 3019-3028.
54. Pilz, D.T., Kuc, J., Matsumoto, N., Bodurtha, J., Bernadi, B., Tassinari, C.A., Dobyns, W.B. and Ledbetter, D.H. (1999) Subcortical band heterotopia in rare affected males can be caused by missense mutations in DCX (XLIS) or LIS1. Hum. Mol. Genet., 8, 1757-1760.
55. Leventer, R.J., Cardoso, C., Ledbetter, D.H. and Dobyns, W.B. (2001) LIS1 missense mutations cause milder lissencephaly phenotypes including a child with normal IQ. Neurology, 57, 416-422.
56. Sweeney, K.J., Clark, G.D., Prokscha, A., Dobyns, W.B. and Eichele, G. (2000) Lissencephaly associated mutations suggest a requirement for the PAFAH1B heterotrimeric complex in brain development. Mech. Dev., 92, 263-271.
57. Smith, T.F., Gaitatzes, C., Saxena, K. and Neer, E.J. (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci., 24, 181-185.
58. Dobyns, W.B., Stratton, R.F., Parke, J.T., Greenberg, F., Nussbaum, R.L. and Ledbetter, D.H. (1983) Miller-Dieker syndrome: lissencephaly and monosomy 17p. J. Pediatr., 102, 552-558.
59. Dobyns, W.B., Curry, C.J., Hoyme, H.E., Turlington, L. and Ledbetter, D.H. (1991) Clinical and molecular diagnosis of Miller-Dieker syndrome. Am. J. Hum. Genet., 48, 584-594.
60. Chong, S.S., Pack, S.D., Roschke, A.V., Tanigami, A., Carrozzo, R., Smith, A.C., Dobyns, W.B. and Ledbetter, D.H. (1997) A revision of the lissencephaly and Miller-Dieker syndrome critical regions in chromosome 17p13.3. Hum. Mol. Genet., 6, 147-155.
61. Cardoso, C., Leventer, R.J., Ward, H.L., Toyo-oka, K., Chung, J., Gross, A., Martin, C.L., Allanson, J., Pilz, D.T., Olney, A.H. et al. (2003) Refinement of a 400 kb critical region allows genotypic differentiation between isolated lissencephaly, Miller-Dicker syndrome and other phenotypes secondary to deletions of 17pl3.3. Am. J. Hum. Genet. (in press).
62. Demelas, L., Serra, G., Conti, M., Achene, A., Mastropaolo, C., Matsumoto, N., Dudlicek, L.L., Mills, P.L., Dobyns, W.B., Ledbetter, D.H. et al. (2001) Incomplete penetrance with normal MRI in a woman with germline mutation of the DCX gene. Neurology, 57, 327-330.
63. Matsumoto, N., Leventer, R.J., Kuc, J.A., Mewborn, S.K., Dudlicek, L.L., Ramocki, M.B., Pilz, D.T., Mills, P.L., Das, S., Ross, M.E. et al. (2001) Mutation analysis of the DCX gene and genotype/phenotype correlation in subcortical band heterotopia. Eur. J. Hum. Genet., 9, 5-12.
64. Gleeson, J.G., Minnerath, S., Kuzniecky, R.I., Dobyns, W.B., Young, I.D., Ross, M.E. and Walsh, C.A. (2000) Somatic and germline mosaic mutations in the doublecortin gene are associated with variable phenotypes. Am. J. Hum. Genet., 67, 574-581.
65. Kato, M., Kanai, M., Soma, O., Takusa, Y., Kimura, T., Numakura, C., Matsuki, T., Nakamura, S. and Hayasaka, K. (2001) Mutation of the doublecortin gene in male patients with double cortex syndrome: somatic mosaicism detected by hair root analysis. Ann. Neurol., 50, 547-551.
66. Poolos, N.P., Das, S., Clark, G.D., Lardizabal, D., Noebels, J.L., Wyllie, E. and Dobyns, W.B. (2002) Males with epilepsy, complete subcortical band heterotopia, and somatic mosaicism for DCX. Neurology, 58, 1559-1562.
67. 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. (2000) Autosomal recessive lissencephaly with cerebellar hypoplasia is associated with human RELN mutations. Nat. Genet., 26, 93-96.
68. Kato, M., Takizawa, N., Yamada, S., Ito, A., Honma, T., Hashimoto, M., Saito, E., Ohta, T., Chikaoka, H. and Hayasaka, K. (1999) Diffuse pachygyria with cerebellar hypoplasia: a milder form of microlissencephaly or a new genetic syndrome? Ann. Neurol., 46, 660-663.
69. Bonneau, D., Toutain, A., Laquerriere, A., Marret, S., Saugier-Veber, P., Barthez, M.A., Radi, S., Biran-Mucignat, V., Rodriguez, D. and Gelot, A. (2002) X-linked lissencephaly with absent corpus callosum and ambiguous genitalia (XLAG): clinical, magnetic resonance imaging, and neuropathological findings. Ann. Neurol., 51, 340-349.
70. Frints, S.G., Froyen, G., Marynen, P., Willekens, D., Legius, E. and Fryns, J.P. (2002) Re-evaluation of MRX36 family after discovery of an ARX gene mutation reveals mild neurological features of Partington syndrome. Am. J. Med. Genet., 112, 427-428.
71. Stromme, P., Mangelsdorf, M.E., Scheffer, I.E. and Gecz, J. (2002) Infantile spasms, dystonia, and other X-linked phenotypes caused by mutations in Aristaless related homeobox gene, ARX. Brain Dev., 24, 266-268.
72. Scheffer, I.E., Wallace, R.H., Phillips, F.L., Hewson, P., Reardon, K., Parasivam, G., Stromme, P., Berkovic, S.F., Gecz, J. and Mulley, J.C. (2002) X-linked myoclonic epilepsy with spasticity and intellectual disability: mutation in the homeobox gene ARX. Neurology, 59, 348-356.
73. Turner, G., Partington, M., Kerr, B., Mangelsdorf, M. and Gecz, J. (2002) Variable expression of mental retardation, autism, seizures, and dystonic hand movements in two families with an identical ARX gene mutation. Am. J. Med. Genet., 112, 405-411.
74. Bienvenu, T., Poirier, K., Friocourt, G., Bahi, N., Beaumont, D., Fauchereau, F., Ben Jeema, L., Zemni, R., Vinet, M.C., Francis, F. et al. (2002) ARX, a novel Prd-class-homeobox gene highly expressed in the telencephalon, is mutated in X-linked mental retardation. Hum. Mol. Genet., 11, 981-991.
75. Rakic, P. (1972) Mode of cell migration to the superficial layers of fetal monkey neocortex. J. Comp. Neurol., 145, 61-83.
76. Jellinger, K. and Rett, A. (1976) Agyria-pachygyria (lissencephaly syndrome). Neuropadiatrie, 7, 66-91.
77. Walsh, C. and Cepko, C.L. (1988) Clonally related cortical cells show several migration patterns. Science, 241, 1342-1345.
78. Anderson, S.A., Eisenstat, D.D., Shi, L. and Rubenstein, J.L. (1997) Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science, 278, 474-476.
79. 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.
80. Nadarajah, B. and Parnavelas, J.G. (2002) Modes of neuronal migration in the developing cerebral cortex. Nat. Rev. Neurosci., 3, 423-432.
81. Angevine, J.B. and Sidman, R.L. (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature, 192, 766-768.
82. Denaxa, M., Chan, C.H., Schachner, M., Parnavelas, J.G. and Karagogeos, D. (2001) The adhesion molecule TAG-1 mediates the migration of cortical interneurons from the ganglionic eminence along the corticofugal fiber system. Development, 128, 4635-4644.
83. Parnavelas, J.G. (2000) The origin and migration of cortical neurones: new vistas. Trends Neurosci., 23, 126-131.
84. Marin, O. and Rubenstein, J.L. (2001) A long, remarkable journey: tangential migration in the telencephalon. Nat. Rev. Neurosci., 2, 780-790.
85. Nadarajah, B., Alifragis, P., Wong, R.O. and Parnavelas, J.G. (2002) Ventricle-directed migration in the developing cerebral cortex. Nat. Neurosci., 5, 218-224.
86. Caviness, V.S. Jr (1982) Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res., 256, 293-302.
87. Sheppard, A.M. and Pearlman, A.L. (1997) Abnormal reorganization of preplate neurons and their associated extracellular matrix: an early manifestation of altered neocortical development in the reeler mutant mouse. J. Comp. Neurol., 378, 173-179.
88. Forster, E., Tielsch, A., Saum, B., Weiss, K.H., Johanssen, C., Graus-Porta, D., Muller, U. and Frotscher, M. (2002) Reelin, Disabled 1, and beta 1 integrins are required for the formation of the radial glial scaffold in the hippocampus. Proc. Natl Acad. Sci. USA, 99, 13178-13183.
89. Gambello, M.J., Darling, D.L., Yingling, J., Tanaka, T., Gleeson, J.G. and Wynshaw-Boris, A. (2003) Multiple dose dependent effects of Lis1 on cerebral cortical development. J. Neurosci. (in press).
90. 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. (1998) Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat. Genet., 19, 333-339.
91. Francis, F., Koulakoff, A., Boucher, D., Chafey, P., Schaar, B., Vinet, M.C., Friocourt, G., McDonnell, N., Reiner, O., Kahn, A. et al. (1999) Doublecortin is a developmentally regulated microtubule-associated protein expressed in migrating and differentiating neurons. Neuron, 23, 247-256.
92. Meyer, G., Perez-Garcia, C.G. and Gleeson, J.G. (2002) Selective expression of doublecortin and LIS1 in developing human cortex suggests unique modes of neuronal movement. Cereb. Cortex, 12, 1225-1236.
93. Letinic, K., Zoncu, R. and Rakic, P. (2002) Origin of GABAergic neurons in the human neocortex. Nature, 417, 645-649.
94. Hourihane, J.O., Bennett, C.P., Chaudhuri, R., Robb, S.A. and Martin, N.D. (1993) A sibship with a neuronal migration defect, cerebellar hypoplasia and congenital lymphedema. Neuropediatrics, 24, 43-46.