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Scientifica
Volume 2013 (2013), Article ID 393975, 17 pages
http://dx.doi.org/10.1155/2013/393975
Review Article

LIS1 and DCX: Implications for Brain Development and Human Disease in Relation to Microtubules

Department of Molecular Genetics, The Weizmann Institute of Science, 76100 Rehovot, Israel

Received 8 January 2013; Accepted 7 February 2013

Academic Editors: K. Endres and D. Jun

Copyright © 2013 Orly Reiner. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Cajal, “Neurons: size and general morphology,” in Histology of the Nervous System, vol. 1, pp. 46–57, Oxford University Press, New York, NY, USA, 1995.
  2. R. Ayala, T. Shu, and L. H. Tsai, “Trekking across the brain: the journey of neuronal migration,” Cell, vol. 128, no. 1, pp. 29–43, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. M. E. Hatten, “New directions in neuronal migration,” Science, vol. 297, no. 5587, pp. 1660–1663, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. A. R. Kriegstein and S. C. Noctor, “Patterns of neuronal migration in the embryonic cortex,” Trends in Neurosciences, vol. 27, no. 7, pp. 392–399, 2004. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Lambert de Rouvroit and A. M. Goffinet, “Neuronal migration,” Mechanisms of Development, vol. 105, no. 1-2, pp. 47–56, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. B. Nadarajah and J. G. Parnavelas, “Modes of neuronal migration in the developing cerebral cortex,” Nature Reviews Neuroscience, vol. 3, no. 6, pp. 423–432, 2002. View at Scopus
  7. X. H. Jaglin and J. Chelly, “Tubulin-related cortical dysgeneses: microtubule dysfunction underlying neuronal migration defects,” Trends in Genetics, vol. 25, no. 12, pp. 555–566, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. W. B. Dobyns, E. Andermann, F. Andermann et al., “X-linked malformations of neuronal migration,” Neurology, vol. 47, no. 2, pp. 331–339, 1996. View at Scopus
  9. J. W. Fox and C. A. Walsh, “Periventricular heterotopia and the genetics of neuronal migration in the cerebral cortex,” American Journal of Human Genetics, vol. 65, no. 1, pp. 19–24, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. R. Guerrini and T. Filippi, “Neuronal migration disorders, genetics, and epileptogenesis,” Journal of Child Neurology, vol. 20, no. 4, pp. 287–299, 2005. View at Scopus
  11. O. Reiner, A. Cahana, O. Shmueli, A. Leeor, and T. Sapir, “LISI, a gene involved in a neuronal migration disorder: from gene isolation towards analysis of gene function,” Cellular Pharmacology, vol. 3, no. 6, pp. 323–329, 1996.
  12. M. E. Ross and C. A. Walsh, “Human brain malformations and their lessons for neuronal migration,” Annual Review of Neuroscience, vol. 24, pp. 1041–1070, 2001. View at Publisher · View at Google Scholar · View at Scopus
  13. C. A. Walsh, “Genetics of neuronal migration in the cerebral cortex,” Mental Retardation and Developmental Disabilities Research Reviews, vol. 6, no. 1, pp. 34–40, 2000.
  14. M. A. Farrell, M. J. DeRosa, J. G. Curran et al., “Neuropathologic findings in cortical resections (including hemispherectomies) performed for the treatment of intractable childhood epilepsy,” Acta Neuropathologica, vol. 83, no. 3, pp. 246–259, 1992. View at Scopus
  15. J. Aicardi, “The place of neuronal migration abnormalities in child neurology,” Canadian Journal of Neurological Sciences, vol. 21, no. 3, pp. 185–193, 1994. View at Scopus
  16. C. Vaillend, R. Poirier, and S. Laroche, “Genes, plasticity and mental retardation,” Behavioural Brain Research, vol. 192, no. 1, pp. 88–105, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Rakic, K. Hashimoto-Torii, and M. R. Sarkisian, “Genetic determinants of neuronal migration in the cerebral cortex,” Novartis Foundation Symposium, vol. 288, pp. 45–98, 2007. View at Scopus
  18. M. Kuijpers and C. C. Hoogenraad, “Centrosomes, microtubules and neuronal development,” Molecular and Cellular Neuroscience, vol. 48, no. 4, pp. 349–358, 2011.
  19. S. H. Fatemi and T. D. Folsom, “The neurodevelopmental hypothesis of Schizophrenia, revisited,” Schizophrenia Bulletin, vol. 35, no. 3, pp. 528–548, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. B. G. Bunney, S. G. Potkin, and W. E. Bunney, “New morphological and neuropathological findings in schizophrenia: a neurodevelopmental perspective,” Clinical Neuroscience, vol. 3, no. 2, pp. 81–88, 1995. View at Scopus
  21. B. S. Peterson, “Neuroimaging in child and adolescent neuropsychiatric disorders,” Journal of the American Academy of Child and Adolescent Psychiatry, vol. 34, no. 12, pp. 1560–1576, 1995. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Götz and W. B. Huttner, “The cell biology of neurogenesis,” Nature Reviews Molecular Cell Biology, vol. 6, no. 10, pp. 777–788, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. R. F. Hevner, “From radial glia to pyramidal-projection neuron: transcription factor cascades in cerebral cortex development,” Molecular Neurobiology, vol. 33, no. 1, pp. 33–50, 2006. View at Scopus
  24. A. Shitamukai and F. Matsuzaki, “Control of asymmetric cell division of mammalian neural progenitors,” Development, Growth & Differentiation, vol. 54, no. 3, pp. 277–286, 2012.
  25. M. K. Lehtinen and C. A. Walsh, “Neurogenesis at the brain-cerebrospinal fluid interface,” Annual Review of Cell and Developmental Biology, vol. 27, pp. 653–679, 2011.
  26. S. A. Fietz and W. B. Huttner, “Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective,” Current Opinion in Neurobiology, vol. 21, no. 1, pp. 23–35, 2011. View at Publisher · View at Google Scholar · View at Scopus
  27. J. S. Gal, Y. M. Morozov, A. E. Ayoub, M. Chatterjee, P. Rakic, and T. F. Haydar, “Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones,” Journal of Neuroscience, vol. 26, no. 3, pp. 1045–1056, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. E. K. Stancik, I. Navarro-Quiroga, R. Sellke, and T. F. Haydar, “Heterogeneity in ventricular zone neural precursors contributes to neuronal fate diversity in the postnatal neocortex,” Journal of Neuroscience, vol. 30, no. 20, pp. 7028–7036, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. S. C. Noctor, A. C. Flint, T. A. Weissman, R. S. Dammerman, and A. R. Kriegstein, “Neurons derived from radial glial cells establish radial units in neocortex,” Nature, vol. 409, no. 6821, pp. 714–720, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. T. Miyata, A. Kawaguchi, H. Okano, and M. Ogawa, “Asymmetric inheritance of radial glial fibers by cortical neurons,” Neuron, vol. 31, no. 5, pp. 727–741, 2001. View at Publisher · View at Google Scholar · View at Scopus
  31. P. Malatesta, E. Hartfuss, and M. Götz, “Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neural lineage,” Development, vol. 127, no. 24, pp. 5253–5263, 2000. View at Scopus
  32. T. E. Anthony, C. Klein, G. Fishell, and N. Heintz, “Radial glia serve as neuronal progenitors in all regions of the central nervous system,” Neuron, vol. 41, no. 6, pp. 881–890, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. J. M. Frade, “Interkinetic nuclear movement in the vertebrate neuroepithelium: encounters with an old acquaintance,” Progress in Brain Research, vol. 136, pp. 67–71, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. L. M. Baye and B. A. Link, “Interkinetic nuclear migration and the selection of neurogenic cell divisions during vertebrate retinogenesis,” Journal of Neuroscience, vol. 27, no. 38, pp. 10143–10152, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. O. Reiner, T. Sapir, and G. Gerlitz, “Interkinetic nuclear movement in the ventricular zone of the cortex,” Journal of Molecular Neuroscience, vol. 46, no. 3, pp. 516–526, 2012. View at Publisher · View at Google Scholar
  36. Y. Kosodo, K. Röper, W. Haubensak, A. M. Marzesco, D. Corbeil, and W. B. Huttner, “Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mamalian neuroepithelial cells,” EMBO Journal, vol. 23, no. 11, pp. 2314–2324, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. S. C. Noctor, V. Martínez-Cerdeño, and A. R. Kriegstein, “Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis,” Journal of Comparative Neurology, vol. 508, no. 1, pp. 28–44, 2008. View at Publisher · View at Google Scholar · View at Scopus
  38. D. Konno, G. Shioi, A. Shitamukai et al., “Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis,” Nature Cell Biology, vol. 10, no. 1, pp. 93–101, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. P. Alexandre, A. M. Reugels, D. Barker, E. Blanc, and J. D. W. Clarke, “Neurons derive from the more apical daughter in asymmetric divisions in the zebrafish neural tube,” Nature Neuroscience, vol. 13, no. 6, pp. 673–679, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Shitamukai, D. Konno, and F. Matsuzaki, “Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors,” Journal of Neuroscience, vol. 31, no. 10, pp. 3683–3695, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. A. M. Reugels, B. Boggetti, N. Scheer, and J. A. Campos-Ortega, “Asymmetric localization of numb: EGFP in dividing neuroepithelial cells during neurulation in Danio rerio,” Developmental Dynamics, vol. 235, no. 4, pp. 934–948, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. Wakamatsu, N. Nakamura, J. A. Lee, G. J. Cole, and N. Osumi, “Transitin, a nestin-like intermediate filament protein, mediates cortical localization and the lateral transport of Numb in mitotic avian neuroepithelial cells,” Development, vol. 134, no. 13, pp. 2425–2433, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. S. C. Noctor, V. Martinez-Cerdeño, L. Ivic, and A. R. Kriegstein, “Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases,” Nature Neuroscience, vol. 7, no. 2, pp. 136–144, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Takahashi, R. S. Nowakowski, and V. S. Caviness, “The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall,” Journal of Neuroscience, vol. 15, no. 9, pp. 6046–6057, 1995. View at Scopus
  45. F. Calegari, W. Haubensak, C. Haffher, and W. B. Huttner, “Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development,” Journal of Neuroscience, vol. 25, no. 28, pp. 6533–6538, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. F. Calegari and W. B. Huttner, “An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis,” Journal of Cell Science, vol. 116, no. 24, pp. 4947–4955, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. W. Haubensak, A. Attardo, W. Denk, and W. B. Huttner, “Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 9, pp. 3196–3201, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. T. Miyata, A. Kawaguchi, K. Saito, M. Kawano, T. Muto, and M. Ogawa, “Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells,” Development, vol. 131, no. 13, pp. 3133–3145, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. I. H. M. Smart, “Proliferative characteristics of the ependymal layer during the early development of the mouse neocortex: a pilot study based on recording the number, location and plane of cleavage of mitotic figures,” Journal of Anatomy, vol. 116, no. 1, pp. 67–91, 1973. View at Scopus
  50. H. Tabata, S. Yoshinaga, and K. Nakajima, “Cytoarchitecture of mouse and human subventricular zone in developing cerebral neocortex,” Experimental Brain Research Experimentelle Hirnforschung Experimentation Cerebrale, vol. 216, no. 2, pp. 161–168, 2012.
  51. T. Takahashi, R. S. Nowakowski, and V. S. Caviness, “Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse,” Journal of Neuroscience, vol. 13, no. 2, pp. 820–833, 1993. View at Scopus
  52. R. S. E. Carney, I. Bystron, G. López-Bendito, and Z. Molnár, “Comparative analysis of extra-ventricular mitoses at early stages of cortical development in rat and human,” Brain Structure and Function, vol. 212, no. 1, pp. 37–54, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. I. H. M. Smart, C. Dehay, P. Giroud, M. Berland, and H. Kennedy, “Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey,” Cerebral Cortex, vol. 12, no. 1, pp. 37–53, 2002. View at Scopus
  54. N. Zecevic, Y. Chen, and R. Filipovic, “Contributions of cortical subventricular zone to the development of the human cerebral cortex,” Journal of Comparative Neurology, vol. 491, no. 2, pp. 109–122, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. J. L. Fish, C. Dehay, H. Kennedy, and W. B. Huttner, “Making bigger brains—the evolution of neural-progenitor-cell division,” Journal of Cell Science, vol. 121, no. 17, pp. 2783–2793, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. P. Rakic, “Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition,” Science, vol. 183, no. 4123, pp. 425–427, 1974. View at Scopus
  57. A. Lukaszewicz, P. Savatier, V. Cortay et al., “G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex,” Neuron, vol. 47, no. 3, pp. 353–364, 2005. View at Publisher · View at Google Scholar · View at Scopus
  58. D. V. Hansen, J. H. Lui, P. R. L. Parker, and A. R. Kriegstein, “Neurogenic radial glia in the outer subventricular zone of human neocortex,” Nature, vol. 464, no. 7288, pp. 554–561, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. S. A. Fietz, I. Kelava, J. Vogt et al., “OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling,” Nature Neuroscience, vol. 13, no. 6, pp. 690–699, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. X. Wang, J. W. Tsai, B. Lamonica, and A. R. Kriegstein, “A new subtype of progenitor cell in the mouse embryonic neocortex,” Nature Neuroscience, vol. 14, no. 5, pp. 555–561, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. S. A. Anderson, D. D. Eisenstat, L. Shi, and J. L. R. Rubenstein, “Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes,” Science, vol. 278, no. 5337, pp. 474–476, 1997. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Wonders and S. A. Anderson, “Cortical interneurons and their origins,” Neuroscientist, vol. 11, no. 3, pp. 199–205, 2005. View at Publisher · View at Google Scholar · View at Scopus
  63. D. M. Gelman and O. Marín, “Generation of interneuron diversity in the mouse cerebral cortex,” European Journal of Neuroscience, vol. 31, no. 12, pp. 2136–2141, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. C. P. Wonders and S. A. Anderson, “The origin and specification of cortical interneurons,” Nature Reviews Neuroscience, vol. 7, no. 9, pp. 687–696, 2006. View at Publisher · View at Google Scholar · View at Scopus
  65. Q. Xu, I. Cobos, E. D. De La Cruz, J. L. Rubenstein, and S. A. Anderson, “Origins of cortical interneuron subtypes,” Journal of Neuroscience, vol. 24, no. 11, pp. 2612–2622, 2004. View at Publisher · View at Google Scholar · View at Scopus
  66. D. Jiménez, L. M. López-Mascaraque, F. Valverde, and J. A. De Carlos, “Tangential migration in neocortical development,” Developmental Biology, vol. 244, no. 1, pp. 155–169, 2002. View at Publisher · View at Google Scholar · View at Scopus
  67. P. Taglialatela, J. M. Soria, V. Caironi, A. Moiana, and S. Bertuzzi, “Compromised generation of GABAergic interneurons in the brains of Vax1-/- mice,” Development, vol. 131, no. 17, pp. 4239–4249, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. D. M. Gelman, F. J. Martini, S. Nóbrega-Pereira, A. Pierani, N. Kessaris, and O. Marín, “The embryonic preoptic area is a novel source of cortical GABAergic interneurons,” Journal of Neuroscience, vol. 29, no. 29, pp. 9380–9389, 2009. View at Publisher · View at Google Scholar · View at Scopus
  69. X. Tan and S. H. Shi, “Neocortical neurogenesis and neuronal migration,” Wiley Interdisciplinary Reviews, 2012. View at Publisher · View at Google Scholar
  70. T. Mori, A. Buffo, and M. Götz, “The novel roles of glial cells revisited: the contribution of radial glia and astrocytes to neurogenesis,” Current Topics in Developmental Biology, vol. 69, pp. 67–99, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. K. Campbell and M. Götz, “Radial glia: multi-purpose cells for vertebrate brain development,” Trends in Neurosciences, vol. 25, no. 5, pp. 235–238, 2002. View at Publisher · View at Google Scholar · View at Scopus
  72. K. N. Brown, S. Chen, Z. Han et al., “Clonal production and organization of inhibitory interneurons in the neocortex,” Science, vol. 334, no. 6055, pp. 480–486, 2011.
  73. K. Yun, S. Potter, and J. L. R. Rubenstein, “Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon,” Development, vol. 128, no. 2, pp. 193–205, 2001. View at Scopus
  74. C. Englund, A. Fink, C. Lau et al., “Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex,” Journal of Neuroscience, vol. 25, no. 1, pp. 247–251, 2005. View at Publisher · View at Google Scholar · View at Scopus
  75. L. Muzio, B. DiBenedetto, A. Stoykova, E. Boncinelli, P. Gruss, and A. Mallamaci, “Conversion of cerebral cortex into basal ganglia in Emx2-/- Pax6Sey/Sey double-mutant mice,” Nature Neuroscience, vol. 5, no. 8, pp. 737–745, 2002. View at Publisher · View at Google Scholar · View at Scopus
  76. P. Malatesta, M. A. Hack, E. Hartfuss et al., “Neuronal or glial progeny: regional differences in radial glia fate,” Neuron, vol. 37, no. 5, pp. 751–764, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. H. Toresson, S. S. Potter, and K. Campbell, “Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2,” Development, vol. 127, no. 20, pp. 4361–4371, 2000. View at Scopus
  78. A. N. Sheth and P. G. Bhide, “Concurrent cellular output from two proliferative populations in the early embryonic mouse corpus striatum,” The Journal of Comparative Neurology, vol. 383, no. 2, pp. 220–230, 1997.
  79. O. Marín and J. L. R. Rubenstein, “Cell migration in the forebrain,” Annual Review of Neuroscience, vol. 26, pp. 441–483, 2003. View at Publisher · View at Google Scholar · View at Scopus
  80. O. Marín and J. L. R. Rubenstein, “A long, remarkable journey: tangential migration in the telencephalon,” Nature Reviews Neuroscience, vol. 2, no. 11, pp. 780–790, 2001. View at Publisher · View at Google Scholar · View at Scopus
  81. L. H. Tsai and J. G. Gleeson, “Nucleokinesis in neuronal migration,” Neuron, vol. 46, no. 3, pp. 383–388, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. O. Reiner and G. Gerlitz, “Nucleokinesis,” in Developmental Neuroscience: A Comprehensive Reference, J. R. Rubinstein and O. Marin, Eds., vol. 1, pp. 1–15, Elsevier, Oxford, UK, 2013.
  83. J. B. Angevine and R. L. Sidman, “Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse,” Nature, vol. 192, no. 4804, pp. 766–768, 1961. View at Publisher · View at Google Scholar · View at Scopus
  84. S. K. McConnell, “The generation of neuronal diversity in the central nervous system,” Annual Review of Neuroscience, vol. 14, pp. 269–300, 1991. View at Scopus
  85. S. Nery, G. Fishell, and J. G. Corbin, “The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations,” Nature Neuroscience, vol. 5, no. 12, pp. 1279–1287, 2002. View at Publisher · View at Google Scholar · View at Scopus
  86. M. W. Miller, “Cogeneration of retrogradely labeled corticocortical projection and GABA-immunoreactive local circuit neurons in cerebral cortex,” Brain Research, vol. 355, no. 2, pp. 187–192, 1985. View at Scopus
  87. A. Fairen, A. Cobas, and M. Fonseca, “Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex,” Journal of Comparative Neurology, vol. 251, no. 1, pp. 67–83, 1986. View at Scopus
  88. H. Valcanis and S. S. Tan, “Layer specification of transplanted interneurons in developing mouse neocortex,” The Journal of Neuroscience, vol. 23, no. 12, pp. 5113–5122, 2003. View at Scopus
  89. P. Rakic, “Mode of cell migration to the superficial layers of fetal monkey neocortex,” Journal of Comparative Neurology, vol. 145, no. 1, pp. 61–83, 1972. View at Scopus
  90. M. E. Hatten, “Central nervous system neuronal migration,” Annual Review of Neuroscience, vol. 22, pp. 511–539, 1999. View at Publisher · View at Google Scholar · View at Scopus
  91. A. A. Lavdas, M. Grigoriou, V. Pachnis, and J. G. Parnavelas, “The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex,” The Journal of Neuroscience, vol. 19, no. 18, pp. 7881–7888, 1999. View at Scopus
  92. J. A. De Carlos, L. López-Mascaraque, and F. Valverde, “Dynamics of cell migration from the lateral ganglionic eminence in the rat,” The Journal of Neuroscience, vol. 16, no. 19, pp. 6146–6156, 1996. View at Scopus
  93. S. S. Tan, M. Kalloniatis, K. Sturm, P. P. L. Tam, B. E. Reese, and B. Faulkner-Jones, “Separate progenitors for radial and tangential cell dispersion during development of the cerebral neocortex,” Neuron, vol. 21, no. 2, pp. 295–304, 1998. View at Scopus
  94. M. L. Ware, S. F. Tavazoie, C. B. Reid, and C. A. Walsh, “Coexistence of widespread clones and large radial clones in early embryonic ferret cortex,” Cerebral Cortex, vol. 9, no. 6, pp. 636–645, 1999. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Anderson, M. Mione, K. Yun, and J. L. R. Rubenstein, “Differential origins of neocortical projection and local circuit neurons: role of Dlx genes in neocortical interneuronogenesis,” Cerebral Cortex, vol. 9, no. 6, pp. 646–654, 1999. View at Publisher · View at Google Scholar · View at Scopus
  96. S. A. Anderson, O. Marín, C. Horn, K. Jennings, and J. L. R. Rubenstein, “Distinct cortical migrations from the medial and lateral ganglionic eminences,” Development, vol. 128, no. 3, pp. 353–363, 2001. View at Scopus
  97. F. Polleux, K. L. Whitford, P. A. Dijkhuizen, T. Vitalis, and A. Ghosh, “Control of cortical interneuron migration by neurotrophins and PI3-kinase signaling,” Development, vol. 129, no. 13, pp. 3147–3160, 2002. View at Scopus
  98. H. Wichterle, D. H. Turnbull, S. Nery, G. Fishell, and A. Alvarez-Buylla, “In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain,” Development, vol. 128, no. 19, pp. 3759–3771, 2001. View at Scopus
  99. M. Yozu, H. Tabata, and K. Nakajima, “The Caudal migratory stream: a novel migratory stream of interneurons derived from the caudal ganglionic eminence in the developing mouse forebrain,” The Journal of Neuroscience, vol. 25, no. 31, pp. 7268–7277, 2005. View at Publisher · View at Google Scholar · View at Scopus
  100. G. Miyoshi, J. Hjerling-Leffler, T. Karayannis et al., “Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons,” The Journal of Neuroscience, vol. 30, no. 5, pp. 1582–1594, 2010. View at Publisher · View at Google Scholar · View at Scopus
  101. W. Ochiai, S. Minobe, M. Ogawa, and T. Miyata, “Transformation of pin-like ventricular zone cells into cortical neurons,” Neuroscience Research, vol. 57, no. 2, pp. 326–329, 2007. View at Publisher · View at Google Scholar · View at Scopus
  102. H. Tabata and K. Nakajima, “Multipolar migration: the third mode of radial neuronal migration in the developing cerebral cortex,” The Journal of Neuroscience, vol. 23, no. 31, pp. 9996–10001, 2003. View at Scopus
  103. S. C. Noctor, A. C. Flint, T. A. Weissman, W. S. Wong, B. K. Clinton, and A. R. Kriegstein, “Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia,” The Journal of Neuroscience, vol. 22, no. 8, pp. 3161–3173, 2002. View at Scopus
  104. J. J. LoTurco and J. Bai, “The multipolar stage and disruptions in neuronal migration,” Trends in Neurosciences, vol. 29, no. 7, pp. 407–413, 2006. View at Publisher · View at Google Scholar · View at Scopus
  105. O. Reiner and T. Sapir, “Polarity regulation in migrating neurons in the cortex,” Molecular Neurobiology, vol. 40, no. 1, pp. 1–14, 2009. View at Publisher · View at Google Scholar · View at Scopus
  106. A. Sakakibara, T. Sato, R. Ando, N. Noguchi, M. Masaoka, and T. Miyata, “Dynamics of centrosome translocation and microtubule organization in neocortical neurons during distinct modes of polarization,” Cerebral Cortex, 2013. View at Publisher · View at Google Scholar
  107. J. W. Tsai, K. H. Bremner, and R. B. Vallee, “Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue,” Nature Neuroscience, vol. 10, no. 8, pp. 970–979, 2007. View at Publisher · View at Google Scholar · View at Scopus
  108. J. W. Tsai, Y. Chen, A. R. Kriegstein, and R. B. Vallee, “LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages,” Journal of Cell Biology, vol. 170, no. 6, pp. 935–945, 2005. View at Publisher · View at Google Scholar · View at Scopus
  109. T. Sapir, S. Sapoznik, T. Levy et al., “Accurate balance of the polarity kinase MARK2/Par-1 is required for proper cortical neuronal migration,” The Journal of Neuroscience, vol. 28, no. 22, pp. 5710–5720, 2008. View at Publisher · View at Google Scholar · View at Scopus
  110. T. Sapir, A. Shmueli, T. Levy et al., “Antagonistic effects of doublecortin and MARK2/Par-1 in the developing cerebral cortex,” The Journal of Neuroscience, vol. 28, no. 48, pp. 13008–13013, 2008. View at Publisher · View at Google Scholar · View at Scopus
  111. T. Horio and H. Hotani, “Visualization of the dynamic instability of individual microtubules by dark-field microscopy,” Nature, vol. 321, no. 6070, pp. 605–607, 1986. View at Scopus
  112. T. Mitchinson and M. Kirschner, “Dynamic instability of microtubule growth,” Nature, vol. 312, no. 5991, pp. 237–242, 1984. View at Scopus
  113. P. J. Sammak and G. G. Borisy, “Direct observation of microtubule dynamics in living cells,” Nature, vol. 332, no. 6166, pp. 724–726, 1988. View at Scopus
  114. E. Schulze and M. Kirschner, “New features of microtubule behaviour observed in vivo,” Nature, vol. 334, no. 6180, pp. 356–359, 1988. View at Scopus
  115. L. Cassimeris, N. K. Pryer, and E. D. Salmon, “Real-time observations of microtubule dynamic instability in living cells,” Journal of Cell Biology, vol. 107, no. 6, pp. 2223–2231, 1988. View at Scopus
  116. P. W. Baas, “Microtubules and neuronal polarity: lessons from mitosis,” Neuron, vol. 22, no. 1, pp. 23–31, 1999. View at Publisher · View at Google Scholar · View at Scopus
  117. M. Stiess and F. Bradke, “Neuronal polarization: the cytoskeleton leads the way,” Developmental Neurobiology, vol. 71, no. 6, pp. 430–444, 2011. View at Publisher · View at Google Scholar · View at Scopus
  118. H. R. Higginbotham and J. G. Gleeson, “The centrosome in neuronal development,” Trends in Neurosciences, vol. 30, no. 6, pp. 276–283, 2007. View at Publisher · View at Google Scholar · View at Scopus
  119. F. C. De Anda, G. Pollarolo, J. S. Da Silva, P. G. Camoletto, F. Feiguin, and C. G. Dotti, “Centrosome localization determines neuronal polarity,” Nature, vol. 436, no. 7051, pp. 704–708, 2005. View at Publisher · View at Google Scholar · View at Scopus
  120. F. C. De Anda, K. Meletis, X. Ge, D. Rei, and L. H. Tsai, “Centrosome motility is essential for initial axon formation in the neocortex,” The Journal of Neuroscience, vol. 30, no. 31, pp. 10391–10406, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. M. Distel, J. C. Hocking, K. Volkmann, and R. W. Köster, “The centrosome neither persistently leads migration nor determines the site of axonogenesis in migrating neurons in vivo,” Journal of Cell Biology, vol. 191, no. 7, article 1413, 2010. View at Publisher · View at Google Scholar · View at Scopus
  122. A. Gartner, E. F. Fornasiero, S. Munck et al., “N-cadherin specifies first asymmetry in developing neurons,” The EMBO Journal, vol. 31, no. 8, pp. 1893–1903, 2012.
  123. A. Falnikar and P. W. Baas, “Critical roles for microtubules in axonal development and disease,” Results and Problems in Cell Differentiation, vol. 48, pp. 47–64, 2009. View at Publisher · View at Google Scholar · View at Scopus
  124. M. Stiess, N. Maghelli, L. C. Kapitein et al., “Axon extension occurs independently of centrosomal microtubule nucleation,” Science, vol. 327, no. 5966, pp. 704–707, 2010. View at Publisher · View at Google Scholar · View at Scopus
  125. P. W. Baas, J. S. Deitch, M. M. Black, and G. A. Banker, “Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite,” Proceedings of the National Academy of Sciences of the United States of America, vol. 85, no. 21, pp. 8335–8339, 1988. View at Scopus
  126. T. Stepanova, J. Slemmer, C. C. Hoogenraad et al., “Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein),” The Journal of Neuroscience, vol. 23, no. 7, pp. 2655–2664, 2003. View at Scopus
  127. O. Reiner, “The unfolding story of two lissencephaly genes and brain development,” Molecular Neurobiology, vol. 20, no. 2-3, pp. 143–156, 1999. View at Scopus
  128. A. J. Barkovich, R. I. Kuzniecky, W. B. Dobyns, G. D. Jackson, L. E. Becker, and P. Evrard, “A classification scheme for malformations of cortical development,” Neuropediatrics, vol. 27, no. 2, pp. 59–63, 1996. View at Scopus
  129. G. Kurlemann, G. Schuierer, K. Kuchelmeister, M. Kleine, J. Weglage, and D. G. Palm, “Lissencephaly syndromes: clinical aspects,” Child's Nervous System, vol. 9, no. 7, pp. 380–386, 1993. View at Publisher · View at Google Scholar · View at Scopus
  130. M. Pancoast, W. Dobyns, and J. A. Golden, “Interneuron deficits in patients with the Miller-Dieker syndrome,” Acta Neuropathologica, vol. 109, no. 4, pp. 400–404, 2005. View at Publisher · View at Google Scholar · View at Scopus
  131. K. Shimojima, C. Sugiura, H. Takahashi et al., “Genomic copy number variations at 17p13.3 and epileptogenesis,” Epilepsy Research, vol. 89, no. 2-3, pp. 303–309, 2010. View at Publisher · View at Google Scholar · View at Scopus
  132. O. Reiner, R. Carrozzo, Y. Shen et al., “Isolation of a Miller-Dieker lissencephaly gene containing G protein β- subunit-like repeats,” Nature, vol. 364, no. 6439, pp. 717–721, 1993. View at Publisher · View at Google Scholar · View at Scopus
  133. V. Des Portes, J. M. Pinard, P. Billuart et al., “A novel CNS gene required for neuronal migration and involved in X- linked subcortical laminar heterotopia and lissencephaly syndrome,” Cell, vol. 92, no. 1, pp. 51–61, 1998. View at Publisher · View at Google Scholar · View at Scopus
  134. J. G. Gleeson, K. M. Allen, J. W. Fox et al., “doublecortin, a brain-specific gene mutated in human X-linked lissencephaly and double cortex syndrome, encodes a putative signaling protein,” Cell, vol. 92, no. 1, pp. 63–72, 1998. View at Publisher · View at Google Scholar · View at Scopus
  135. D. A. Keays, G. Tian, K. Poirier et al., “Mutations in α-tubulin cause abnormal neuronal migration in mice and lissencephaly in humans,” Cell, vol. 128, no. 1, pp. 45–57, 2007. View at Publisher · View at Google Scholar · View at Scopus
  136. K. Poirier, D. A. Keays, F. Francis et al., “Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUBA1A),” Human Mutation, vol. 28, no. 11, pp. 1055–1064, 2007. View at Publisher · View at Google Scholar · View at Scopus
  137. A. Mokanszki, I. Korhegyi, N. Szabo et al., “Lissencephaly and band heterotopia: LIS1, TUBA1A, and DCX mutations in hungary,” Journal of Child Neurology, vol. 27, no. 12, pp. 1534–1540, 2012.
  138. W. B. Dobyns, O. Reiner, R. Carrozzo, and D. H. Ledbetter, “Lissencephaly: a human brain malformation associated with deletion of the LIS1 gene located at chromosome 17p13,” Journal of the American Medical Association, vol. 270, no. 23, pp. 2838–2842, 1993. View at Publisher · View at Google Scholar · View at Scopus
  139. D. T. Pilz, N. Matsumoto, S. Minnerath et al., “LIS1 and XLIS (DCX) mutations cause most classical lissencephaly, but different patterns of malformation,” Human Molecular Genetics, vol. 7, no. 13, pp. 2029–2037, 1998. View at Scopus
  140. W. B. Dobyns, C. L. Truwit, M. E. Ross et al., “Differences in the gyral pattern distinguish chromosome 17-linked and X-linked lissencephaly,” Neurology, vol. 53, no. 2, pp. 270–277, 1999. View at Scopus
  141. G. Viot, P. Sonigo, I. Simon et al., “Neocortical neuronal arrangement in LIS1 and DCX lissencephaly may be different,” American Journal of Medical Genetics, vol. 126, no. 2, pp. 123–128, 2004. View at Scopus
  142. F. Sicca, A. Kelemen, P. Genton et al., “Mosaic mutations of the LIS1 gene cause subcortical band heterotopia,” Neurology, vol. 61, no. 8, pp. 1042–1046, 2003. View at Scopus
  143. A. Mineyko, A. Doja, J. Hurteau, W. B. Dobyns, S. Das, and K. M. Boycott, “A novel missense mutation in LIS1 in a child with subcortical band heterotopia and pachygyria inherited from his mildly affected mother with somatic mosaicism,” Journal of Child Neurology, vol. 25, no. 6, pp. 738–741, 2010. View at Publisher · View at Google Scholar · View at Scopus
  144. X. H. Jaglin, K. Poirier, Y. Saillour et al., “Mutations in the β-tubulin gene TUBB2B result in asymmetrical polymicrogyria,” Nature Genetics, vol. 41, no. 6, pp. 746–752, 2009. View at Publisher · View at Google Scholar · View at Scopus
  145. R. Guerrini, W. B. Dobyns, and A. J. Barkovich, “Abnormal development of the human cerebral cortex: genetics, functional consequences and treatment options,” Trends in Neurosciences, vol. 31, no. 3, pp. 154–162, 2008. View at Publisher · View at Google Scholar · View at Scopus
  146. J. P. Lockrow, K. R. Holden, A. Dwivedi, M. G. Matheus, and M. J. Lyons, “LIS1 duplication: expanding the phenotype,” Journal of Child Neurology, vol. 27, no. 6, pp. 791–795, 2012.
  147. B. Harding, “Gray matter heterotopia,” in Dysplasias of Cerebral Cortex and Epilepsy, R. Guerrini, F. Andermann, R. Canapicchi, J. Roger, B. Zilfkin, and P. Pfanner, Eds., pp. 81–88, Lippincott-Raven, Philadelphia, Pa, USA, 1996.
  148. D. R. Weinberger, “Implications of normal brain development for the pathogenesis of schizophrenia,” Archives of General Psychiatry, vol. 44, no. 7, pp. 660–669, 1987. View at Scopus
  149. O. Reiner, S. Sapoznik, and T. Sapir, “Lissencephaly 1 linking to multiple diseases: mental retardation, neurodegeneration, schizophrenia, male sterility, and more,” NeuroMolecular Medicine, vol. 8, no. 4, pp. 547–566, 2006. View at Publisher · View at Google Scholar · View at Scopus
  150. D. H. Geschwind and P. Levitt, “Autism spectrum disorders: developmental disconnection syndromes,” Current Opinion in Neurobiology, vol. 17, no. 1, pp. 103–111, 2007. View at Publisher · View at Google Scholar · View at Scopus
  151. G. Maussion, J. Carayol, A. M. Lepagnol-bestel et al., “Convergent evidence identifying MAP/microtubule affinity-regulating kinase 1 (MARK1) as a susceptibility gene for autism,” Human Molecular Genetics, vol. 17, no. 16, pp. 2541–2551, 2008. View at Publisher · View at Google Scholar · View at Scopus
  152. J. P. Tassan and X. Le Goff, “An overview of the KIN1/PAR-1/MARK kinase family,” Biology of the Cell, vol. 96, no. 3, pp. 193–199, 2004. View at Publisher · View at Google Scholar · View at Scopus
  153. G. Drewes, A. Ebneth, U. Preuss, E. M. Mandelkow, and E. Mandelkow, “MARK, a novel family of protein kinases that phosphorylate microtubule- associated proteins and trigger microtubule disruption,” Cell, vol. 89, no. 2, pp. 297–308, 1997. View at Scopus
  154. G. Drewes, B. Trinczek, S. Illenberger et al., “Microtubule-associated protein/microtubule affinity-regulating kinase (p110mark). A novel protein kinase that regulates tau-microtubule interactions and dynamic instability by phosphorylation at the Alzheimer-specific site serine 262,” Journal of Biological Chemistry, vol. 270, no. 13, pp. 7679–7688, 1995. View at Publisher · View at Google Scholar · View at Scopus
  155. W. Bi, T. Sapir, O. A. Shchelochkov et al., “Increased LIS1 expression affects human and mouse brain development,” Nature Genetics, vol. 41, no. 2, pp. 168–177, 2009. View at Publisher · View at Google Scholar · View at Scopus
  156. K. Avela, K. Aktan-Collan, N. Horelli-Kuitunen, S. Knuutila, and M. Somer, “A microduplication on chromosome 17p13.1p13.3 including the PAFAH1B1 (LIS1) gene,” American Journal of Medical Genetics A, vol. 155, no. 4, pp. 875–879, 2011. View at Publisher · View at Google Scholar · View at Scopus
  157. D. L. Bruno, B. M. Anderlid, A. Lindstrand et al., “Further molecular and clinical delineation of co-locating 17p13.3 microdeletions and microduplications that show distinctive phenotypes,” Journal of Medical Genetics, vol. 47, no. 5, pp. 299–311, 2010. View at Publisher · View at Google Scholar · View at Scopus
  158. C. Shaw-Smith, A. M. Pittman, L. Willatt et al., “Microdeletion encompassing MAPT at chromosome 17q21.3 is associated with developmental delay and learning disability,” Nature Genetics, vol. 38, no. 9, pp. 1032–1037, 2006. View at Publisher · View at Google Scholar · View at Scopus
  159. A. J. Sharp, S. Hansen, R. R. Selzer et al., “Discovery of previously unidentified genomic disorders from the duplication architecture of the human genome,” Nature Genetics, vol. 38, no. 9, pp. 1038–1042, 2006. View at Publisher · View at Google Scholar · View at Scopus
  160. D. A. Koolen, L. E. L. M. Vissers, R. Pfundt et al., “A new chromosome 17q21.31 microdeletion syndrome associated with a common inversion polymorphism,” Nature Genetics, vol. 38, no. 9, pp. 999–1001, 2006. View at Publisher · View at Google Scholar · View at Scopus
  161. M. C. Varela, A. C. V. Krepischi-Santos, J. A. Paz et al., “A 17q21.31 microdeletion encompassing the MAPT gene in a mentally impaired patient,” Cytogenetic and Genome Research, vol. 114, no. 1, pp. 89–92, 2006. View at Publisher · View at Google Scholar · View at Scopus
  162. D. A. Koolen, A. J. Sharp, J. A. Hurst et al., “Clinical and molecular delineation of the 17q21.31 microdeletion syndrome,” Journal of Medical Genetics, vol. 45, no. 11, pp. 710–720, 2008. View at Publisher · View at Google Scholar · View at Scopus
  163. T. Bullmann, M. Holzer, H. Mori, and T. Arendt, “Pattern of tau isoforms expression during development in vivo,” International Journal of Developmental Neuroscience, vol. 27, no. 6, pp. 591–597, 2009. View at Publisher · View at Google Scholar · View at Scopus
  164. H. Takuma, S. Arawaka, and H. Mori, “Isoforms changes of tau protein during development in various species,” Developmental Brain Research, vol. 142, no. 2, pp. 121–127, 2003. View at Publisher · View at Google Scholar · View at Scopus
  165. M. D. Weingarten, A. H. Lockwood, S. Y. Hwo, and M. W. Kirschner, “A protein factor essential for microtubule assembly,” Proceedings of the National Academy of Sciences of the United States of America, vol. 72, no. 5, pp. 1858–1862, 1975. View at Scopus
  166. D. W. Cleveland, S. Y. Hwo, and M. W. Kirschner, “Purification of tau, a microtubule associated protein that induces assembly of microtubules from purified tubulin,” Journal of Molecular Biology, vol. 116, no. 2, pp. 207–225, 1977. View at Scopus
  167. O. Reiner, A. Shmueli, and T. Sapir, “Neuronal migration and neurodegeneration: 2 sides of the same coin,” Cerebral Cortex, vol. 19, pp. i42–i48, 2009. View at Publisher · View at Google Scholar · View at Scopus
  168. M. L. Billingsley and R. L. Kincaid, “Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration,” Biochemical Journal, vol. 323, no. 3, pp. 577–591, 1997. View at Scopus
  169. C. Ballatore, V. M. Y. Lee, and J. Q. Trojanowski, “Tau-mediated neurodegeneration in Alzheimer's disease and related disorders,” Nature Reviews Neuroscience, vol. 8, no. 9, pp. 663–672, 2007. View at Publisher · View at Google Scholar · View at Scopus
  170. L. Dehmelt and S. Halpain, “Actin and microtubules in neurite initiation: are maps the missing link?” Journal of Neurobiology, vol. 58, no. 1, pp. 18–33, 2004. View at Publisher · View at Google Scholar · View at Scopus
  171. G. B. Stokin and L. S. B. Goldstein, “Axonal transport and Alzheimer's disease,” Annual Review of Biochemistry, vol. 75, pp. 607–627, 2006. View at Publisher · View at Google Scholar · View at Scopus
  172. J. M. Gerdes and N. Katsanis, “Microtubule transport defects in neurological and ciliary disease,” Cellular and Molecular Life Sciences, vol. 62, no. 14, pp. 1556–1570, 2005. View at Publisher · View at Google Scholar · View at Scopus
  173. E. L. F. Holzbaur, “Motor neurons rely on motor proteins,” Trends in Cell Biology, vol. 14, no. 5, pp. 233–240, 2004. View at Publisher · View at Google Scholar · View at Scopus
  174. P. W. Baas and L. Qiang, “Neuronal microtubules: when the MAP is the roadblock,” Trends in Cell Biology, vol. 15, no. 4, pp. 183–187, 2005. View at Publisher · View at Google Scholar · View at Scopus
  175. D. A. Willins, X. Xiang, and N. R. Morris, “An alpha tubulin mutation suppresses nuclear migration mutations in Aspergillus nidulans,” Genetics, vol. 141, no. 4, pp. 1287–1298, 1995. View at Scopus
  176. T. Sapir, M. Elbaum, and O. Reiner, “Reduction of microtubule catastrophe events by LIS1, platelet-activating factor acetylhydrolase subunit,” EMBO Journal, vol. 16, no. 23, pp. 6977–6984, 1997. View at Scopus
  177. D. S. Smith, M. Niethammer, R. Ayala et al., “Regulation of cytoplasmic dynein behaviour and microtubule organization by mammalian Lis1,” Nature Cell Biology, vol. 2, no. 11, pp. 767–775, 2000. View at Publisher · View at Google Scholar · View at Scopus
  178. S. Sasaki, A. Shionoya, M. Ishida et al., “A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system,” Neuron, vol. 28, no. 3, pp. 681–696, 2000. View at Publisher · View at Google Scholar · View at Scopus
  179. K. D. Sumigray, H. Chen, and T. Lechler, “Lis1 is essential for cortical microtubule organization and desmosome stability in the epidermis,” Journal of Cell Biology, vol. 194, no. 4, pp. 631–642, 2011.
  180. M. Rehberg, J. Kleylein-Sohn, J. Faix, T. H. Ho, I. Schulz, and R. Gräf, “Dictyostelium LIS1 is a centrosomal protein required for microtubule/cell cortex interactions, nucleus/centrosome linkage, and actin dynamics,” Molecular Biology of the Cell, vol. 16, no. 6, pp. 2759–2771, 2005. View at Publisher · View at Google Scholar · View at Scopus
  181. T. Sapir, A. Cahana, R. Seger, S. Nekhai, and O. Reiner, “LIS1 is a microtubule-associated phosphoprotein,” European Journal of Biochemistry, vol. 265, no. 1, pp. 181–188, 1999. View at Publisher · View at Google Scholar · View at Scopus
  182. M. Caspi, R. Atlas, A. Kantor, T. Sapir, and O. Reiner, “Interaction between LIS1 and doublecortin, two lissencephaly gene products,” Human Molecular Genetics, vol. 9, no. 15, pp. 2205–2213, 2000. View at Scopus
  183. F. M. Coquelle, M. Caspi, F. P. Cordelières et al., “LIS1, CLIP-170's key to the dynein/dynactin pathway,” Molecular and Cellular Biology, vol. 22, no. 9, pp. 3089–3102, 2002. View at Publisher · View at Google Scholar · View at Scopus
  184. E. M. Jiménez-Mateos, F. Wandosell, O. Reiner, J. Avila, and C. González-Billault, “Binding of microtubule-associated protein 1B to LIS1 affects the interaction between dynein and LIS1,” Biochemical Journal, vol. 389, no. 2, pp. 333–341, 2005. View at Publisher · View at Google Scholar · View at Scopus
  185. S. S. Kholmanskikh, J. S. Dobrin, A. Wynshaw-Boris, P. C. Letourneau, and M. E. Ross, “Disregulated RhoGTPases and actin cytoskeleton contribute to the migration defect in Lis1-deficient neurons,” The Journal of Neuroscience, vol. 23, no. 25, pp. 8673–8681, 2003. View at Scopus
  186. S. S. Kholmanskikh, H. B. Koeller, A. Wynshaw-Boris, T. Gomez, P. C. Letourneau, and M. E. Ross, “Calcium-dependent interaction of Lis1 with IQGAP1 and Cdc42 promotes neuronal motility,” Nature Neuroscience, vol. 9, no. 1, pp. 50–57, 2006. View at Publisher · View at Google Scholar · View at Scopus
  187. S. M. Beckwith, C. H. Roghi, B. Liu, and N. R. Morris, “The '8-kD' cytoplasmic dynein light chain is required for nuclear migration and for dynein heavy chain localization in Aspergillus nidulans,” Journal of Cell Biology, vol. 143, no. 5, pp. 1239–1247, 1998. View at Publisher · View at Google Scholar · View at Scopus
  188. X. Xiang, S. M. Beckwith, and N. R. Morris, “Cytoplasmic dynein is involved in nuclear migration in Aspergillus nidulans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 6, pp. 2100–2104, 1994. View at Scopus
  189. X. Xiang, G. Han, D. A. Winkelmann, W. Zuo, and N. R. Morris, “Dynamics of cytoplasmic dynein in living cells and the effect of a mutation in the dynactin complex actin-related protein Arp1,” Current Biology, vol. 10, no. 10, pp. 603–606, 2000. View at Publisher · View at Google Scholar · View at Scopus
  190. Z. Liu, T. Xie, and R. Steward, “Lis1, the Drosophila homolog of a human lissencephaly disease gene, is required for germline cell division and oocyte differentiation,” Development, vol. 126, no. 20, pp. 4477–4488, 1999. View at Scopus
  191. A. Swan, T. Nguyen, and B. Suter, “Drosophila Lissencephaly-1 functions with Bic-D and dynein in oocyte determination and nuclear positioning,” Nature Cell Biology, vol. 1, no. 7, pp. 444–449, 1999. View at Scopus
  192. Y. Lei and R. Warrior, “The Drosophila lissencephalyl (DLis1) gene is required for nuclear migration,” Developmental Biology, vol. 226, no. 1, pp. 57–72, 2000. View at Publisher · View at Google Scholar · View at Scopus
  193. T. Fujiwara, K. Tanaka, E. Inoue, M. Kikyo, and Y. Takai, “Bni1p regulates microtubule-dependent nuclear migration through the actin cytoskeleton in Saccharomyces cerevisiae,” Molecular and Cellular Biology, vol. 19, no. 12, pp. 8016–8027, 1999. View at Scopus
  194. W. L. Lee, J. R. Oberle, and J. A. Cooper, “The role of the lissencephaly protein Pac1 during nuclear migration in budding yeast,” Journal of Cell Biology, vol. 160, no. 3, pp. 355–364, 2003. View at Publisher · View at Google Scholar · View at Scopus
  195. N. E. Faulkner, D. L. Dujardin, C. Y. Tai et al., “A role for the lissencephaly gene Lis1 in mitosis and cytoplasmic dynein function,” Nature Cell Biology, vol. 2, no. 11, pp. 784–791, 2000. View at Publisher · View at Google Scholar · View at Scopus
  196. C. Y. Tai, D. L. Dujardin, N. E. Faulkner, and R. B. Vallee, “Role of dynein, dynactin, and CLIP-170 interactions in LIS1 kinetochore function,” Journal of Cell Biology, vol. 156, no. 6, pp. 959–968, 2002. View at Publisher · View at Google Scholar · View at Scopus
  197. Z. Liu, R. Steward, and L. Luo, “Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration and axonal transport,” Nature Cell Biology, vol. 2, no. 11, pp. 776–783, 2000. View at Publisher · View at Google Scholar · View at Scopus
  198. J. P. Pandey and D. S. Smith, “A Cdk5-dependent switch regulates Lis1/Ndel1/dynein-driven organelle transport in adult axons,” The Journal of Neuroscience, vol. 31, no. 47, pp. 17207–17219, 2011.
  199. D. Splinter, D. S. Razafsky, M. A. Schlager et al., “BICD2, dynactin, and LIS1 cooperate in regulating dynein recruitment to cellular structures,” Molecular Biology of the Cell, vol. 23, no. 21, pp. 4226–4241, 2012.
  200. C. Lam, M. A. S. Vergnolle, L. Thorpe, P. G. Woodman, and V. J. Allan, “Functional interplay between LIS1, NDE1 and NDEL1 in dynein-dependent organelle positioning,” Journal of Cell Science, vol. 123, no. 2, pp. 202–212, 2010. View at Publisher · View at Google Scholar · View at Scopus
  201. Y. Liang, W. Yu, Y. Li et al., “Nudel functions in membrane traffic mainly through association with Lis1 and cytoplasmic dynein,” Journal of Cell Biology, vol. 164, no. 4, pp. 557–566, 2004. View at Publisher · View at Google Scholar · View at Scopus
  202. D. Mori, Y. Yano, K. Toyo-Oka et al., “NDEL1 phosphorylation by Aurora-A kinase is essential for centrosomal maturation, separation, and TACC3 recruitment,” Molecular and Cellular Biology, vol. 27, no. 1, pp. 352–367, 2007. View at Publisher · View at Google Scholar · View at Scopus
  203. M. A. S. Vergnolle and S. S. Taylor, “Cenp-F links kinetochores to Ndel1/Nde1/Lis1/dynein microtubule motor complexes,” Current Biology, vol. 17, no. 13, pp. 1173–1179, 2007. View at Publisher · View at Google Scholar · View at Scopus
  204. N. J. Bradshaw, D. C. Soares, B. C. Carlyle et al., “Pka phosphorylation of NDE1 is DISC1/PDE4 dependent and modulates its interaction with LIS1 and NDEL1,” The Journal of Neuroscience, vol. 31, no. 24, pp. 9043–9054, 2011. View at Publisher · View at Google Scholar · View at Scopus
  205. J. Huang, A. J. Roberts, A. E. Leschziner, and S. L. Reck-Peterson, “Lis1 acts as a, “clutch” between the ATPase and microtubule-binding domains of the dynein motor,” Cell, vol. 150, no. 5, pp. 975–986, 2012.
  206. V. J. Allan, “Cytoplasmic dynein,” Biochemical Society Transactions, vol. 39, no. 5, pp. 1169–1178, 2011.
  207. R. J. McKenney, M. Vershinin, A. Kunwar, R. B. Vallee, and S. P. Gross, “LIS1 and NudE induce a persistent dynein force-producing state,” Cell, vol. 141, no. 2, pp. 304–314, 2010. View at Publisher · View at Google Scholar · View at Scopus
  208. R. B. Vallee, R. J. McKenney, and K. M. Ori-McKenney, “Multiple modes of cytoplasmic dynein regulation,” Nature Cell Biology, vol. 14, no. 3, pp. 224–230, 2012.
  209. M. J. Egan, K. Tan, and S. L. Reck-Peterson, “Lis1 is an initiation factor for dynein-driven organelle transport,” Journal of Cell Biology, vol. 197, no. 7, pp. 971–982, 2012.
  210. Y. Zheng, J. Wildonger, B. Ye et al., “Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons,” Nature Cell Biology, vol. 10, no. 10, pp. 1172–1180, 2008. View at Publisher · View at Google Scholar · View at Scopus
  211. S. Taya, T. Shinoda, D. Tsuboi et al., “DISC1 regulates the transport of the NUDEL/LIS1/14-3-3ε complex through Kinesin-1,” The Journal of Neuroscience, vol. 27, no. 1, pp. 15–26, 2007. View at Publisher · View at Google Scholar · View at Scopus
  212. M. Yamada, S. Toba, Y. Yoshida et al., “LIS1 and NDEL1 coordinate the plus-end-directed transport of cytoplasmic dynein,” EMBO Journal, vol. 27, no. 19, pp. 2471–2483, 2008. View at Publisher · View at Google Scholar · View at Scopus
  213. F. Francis, A. Koulakoff, D. Boucher et al., “Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons,” Neuron, vol. 23, no. 2, pp. 247–256, 1999. View at Publisher · View at Google Scholar · View at Scopus
  214. J. G. Gleeson, L. Peter T, L. A. Flanagan, and C. A. Walsh, “Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons,” Neuron, vol. 23, no. 2, pp. 257–271, 1999. View at Publisher · View at Google Scholar · View at Scopus
  215. D. Horesh, T. Sapir, F. Francis et al., “Doublecortin, a stabilizer of microtubules,” Human Molecular Genetics, vol. 8, no. 9, pp. 1599–1610, 1999. View at Publisher · View at Google Scholar · View at Scopus
  216. F. J. Fourniol, C. V. Sindelar, B. Amigues et al., “Template-free 13-protofilament microtubule-MAP assembly visualized at 8 A resolution,” Journal of Cell Biology, vol. 191, no. 3, pp. 463–470, 2010.
  217. C. A. Moores, M. Perderiset, F. Francis, J. Chelly, A. Houdusse, and R. A. Milligan, “Mechanism of microtubule stabilization by doublecortin,” Molecular Cell, vol. 14, no. 6, pp. 833–839, 2004. View at Publisher · View at Google Scholar · View at Scopus
  218. S. Bechstedt and G. J. Brouhard, “Doublecortin recognizes the 13-protofilament microtubule cooperatively and tracks microtubule ends,” Developmental Cell, vol. 23, no. 1, pp. 181–192, 2012.
  219. F. M. Coquelle, T. Levy, S. Bergmann et al., “Common and divergent roles for members of the mouse DCX superfamily,” Cell Cycle, vol. 5, no. 9, pp. 976–983, 2006. View at Scopus
  220. O. Reiner, F. M. Coquelle, B. Peter et al., “The evolving doublecortin (DCX) superfamily,” BMC Genomics, vol. 7, article 188, 2006. View at Publisher · View at Google Scholar · View at Scopus
  221. T. Sapir, D. Horesh, M. Caspi et al., “Doublecortin mutations cluster in evolutionarily conserved functional domains,” Human Molecular Genetics, vol. 9, no. 5, pp. 703–712, 2000. View at Scopus
  222. K. R. Taylor, A. K. Holzer, J. F. Bazan, C. A. Walsh, and J. G. Gleeson, “Patient mutations in doublecortin define a repeated tubulin-binding domain,” Journal of Biological Chemistry, vol. 275, no. 44, pp. 34442–34450, 2000. View at Scopus
  223. T. Tanaka, F. F. Serneo, C. Higgins, M. J. Gambello, A. Wynshaw-Boris, and J. G. Gleeson, “Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration,” Journal of Cell Biology, vol. 165, no. 5, pp. 709–721, 2004. View at Publisher · View at Google Scholar · View at Scopus
  224. M. Tsukada, A. Prokscha, and G. Eichele, “Neurabin II mediates doublecortin-dephosphorylation on actin filaments,” Biochemical and Biophysical Research Communications, vol. 343, no. 3, pp. 839–847, 2006. View at Publisher · View at Google Scholar · View at Scopus
  225. M. Tsukada, A. Prokscha, J. Oldekamp, and G. Eichele, “Identification of neurabin II as a novel doublecortin interacting protein,” Mechanisms of Development, vol. 120, no. 9, pp. 1033–1043, 2003. View at Publisher · View at Google Scholar · View at Scopus
  226. M. Tsukada, A. Prokscha, E. Ungewickell, and G. Eichele, “Doublecortin association with actin filaments is regulated by neurabin II,” Journal of Biological Chemistry, vol. 280, no. 12, pp. 11361–11368, 2005. View at Publisher · View at Google Scholar · View at Scopus
  227. G. Friocourt, P. Chafey, P. Billuart et al., “Doublecortin interacts with μ subunits of clathrin adaptor complexes in the developing nervous system,” Molecular and Cellular Neuroscience, vol. 18, no. 3, pp. 307–319, 2001. View at Publisher · View at Google Scholar · View at Scopus
  228. C. C. Yap, M. Vakulenko, K. Kruczek et al., “(DCX) mediates endocytosis of neurofascin independently of microtubule binding,” The Journal of Neuroscience, vol. 32, no. 22, pp. 7439–7453, 2012.
  229. A. Gdalyahu, I. Ghosh, T. Levy et al., “DCX, a new mediator of the JNK pathway,” EMBO Journal, vol. 23, no. 4, pp. 823–832, 2004. View at Publisher · View at Google Scholar · View at Scopus
  230. T. Tanaka, F. F. Serneo, H. C. Tseng, A. B. Kulkarni, L. H. Tsai, and J. G. Gleeson, “Cdk5 phosphorylation of doublecortin ser297 regulates its effect on neuronal migration,” Neuron, vol. 41, no. 2, pp. 215–227, 2004. View at Publisher · View at Google Scholar · View at Scopus
  231. M. E. Graham, P. Ruma-Haynes, A. G. Capes-Davis et al., “Multisite phosphorylation of doublecortin by cyclin-dependent kinase 5,” Biochemical Journal, vol. 381, no. 2, pp. 471–481, 2004. View at Publisher · View at Google Scholar · View at Scopus
  232. B. T. Schaar, K. Kinoshita, and S. K. McConnell, “Doublecortin microtubule affinity is regulated by a balance of kinase and phosphatase activity at the leading edge of migrating neurons,” Neuron, vol. 41, no. 2, pp. 203–213, 2004. View at Publisher · View at Google Scholar · View at Scopus
  233. P. M. Bilimoria, L. De La Torre-Ubieta, Y. Ikeuchi, E. B. E. Becker, O. Reiner, and A. Bonni, “A JIP3-regulated GSK3β/DCX signaling pathway restricts axon branching,” The Journal of Neuroscience, vol. 30, no. 50, pp. 16766–16776, 2010. View at Publisher · View at Google Scholar · View at Scopus
  234. S. L. Bielas, F. F. Serneo, M. Chechlacz et al., “Spinophilin facilitates dephosphorylation of doublecortin by pp1 to mediate microtubule bundling at the axonal wrist,” Cell, vol. 129, no. 3, pp. 579–591, 2007. View at Publisher · View at Google Scholar · View at Scopus
  235. A. Shmueli, A. Gdalyahu, S. Sapoznik, T. Sapir, M. Tsukada, and O. Reiner, “Site-specific dephosphorylation of doublecortin (DCX) by protein phosphatase 1 (PP1),” Molecular and Cellular Neuroscience, vol. 32, no. 1-2, pp. 15–26, 2006. View at Publisher · View at Google Scholar · View at Scopus
  236. I. Tint, D. Jean, P. W. Baas, and M. M. Black, “Doublecortin associates with microtubules preferentially in regions of the axon displaying actin-rich protrusive structures,” The Journal of Neuroscience, vol. 29, no. 35, pp. 10995–11010, 2009. View at Publisher · View at Google Scholar · View at Scopus
  237. D. Cohen, M. Segal, and O. Reiner, “Doublecortin supports the development of dendritic arbors in primary hippocampal neurons,” Developmental Neuroscience, vol. 30, no. 1–3, pp. 187–199, 2007. View at Publisher · View at Google Scholar · View at Scopus
  238. C. A. Moores, M. Perderiset, C. Kappeler et al., “Distinct roles of doublecortin modulating the microtubule cytoskeleton,” EMBO Journal, vol. 25, no. 19, pp. 4448–4457, 2006. View at Publisher · View at Google Scholar · View at Scopus
  239. J. S. Liu, C. R. Schubert, X. Fu et al., “Molecular basis for specific regulation of neuronal kinesin-3 motors by doublecortin family proteins,” Molecular Cell, vol. 47, no. 5, pp. 707–721, 2012.
  240. T. Pramparo, O. Libiger, S. Jain et al., “Global developmental gene expression and pathway analysis of normal brain development and mouse models of human neuronal migration defects,” PLoS Genetics, vol. 7, no. 3, Article ID e1001331, 2011. View at Publisher · View at Google Scholar · View at Scopus
  241. T. Pramparo, Y. H. Youn, J. Yingling, S. Hirotsune, and A. Wynshaw-Boris, “Novel embryonic neuronal migration and proliferation defects in Dcx mutant mice are exacerbated by Lis1 reduction,” The Journal of Neuroscience, vol. 30, no. 8, pp. 3002–3012, 2010. View at Publisher · View at Google Scholar · View at Scopus
  242. M. J. Gambello, D. L. Darling, J. Yingling, T. Tanaka, J. G. Gleeson, and A. Wynshaw-Boris, “Multiple dose-dependent effects of Lis1 on cerebral cortical development,” The Journal of Neuroscience, vol. 23, no. 5, pp. 1719–1729, 2003. View at Scopus
  243. Y. H. Youn, T. Pramparo, S. Hirotsune, and A. Wynshaw-Boris, “Distinct dose-dependent cortical neuronal migration and neurite extension defects in Lis1 and Ndel1 mutant mice,” The Journal of Neuroscience, vol. 29, no. 49, pp. 15520–15530, 2009. View at Publisher · View at Google Scholar · View at Scopus
  244. D. L. Silver, D. E. Watkins-Chow, K. C. Schreck et al., “The exon junction complex component Magoh controls brain size by regulating neural stem cell division,” Nature Neuroscience, vol. 13, no. 5, pp. 551–558, 2010. View at Publisher · View at Google Scholar · View at Scopus
  245. S. Hebbar, M. T. Mesngon, A. M. Guillotte, B. Desai, R. Ayala, and D. S. Smith, “Lis1 and Ndel1 influence the timing of nuclear envelope breakdown in neural stem cells,” Journal of Cell Biology, vol. 182, no. 6, pp. 1063–1071, 2008. View at Publisher · View at Google Scholar · View at Scopus
  246. S. Hippenmeyer, Y. H. Youn, H. M. Moon et al., “Genetic mosaic dissection of Lis1 and Ndel1 in neuronal migration,” Neuron, vol. 68, no. 4, pp. 695–709, 2010. View at Publisher · View at Google Scholar · View at Scopus
  247. J. Yingling, Y. H. Youn, D. Darling et al., “Neuroepithelial stem cell proliferation requires lis1 for precise spindle orientation and symmetric division,” Cell, vol. 132, no. 3, pp. 474–486, 2008. View at Publisher · View at Google Scholar · View at Scopus
  248. A. S. Pawlisz, C. Mutch, A. Wynshaw-Boris, A. Chenn, C. A. Walsh, and Y. Feng, “Lis1-Nde1-dependent neuronal fate control determines cerebral cortical size and lamination,” Human Molecular Genetics, vol. 17, no. 16, pp. 2441–2455, 2008. View at Publisher · View at Google Scholar · View at Scopus
  249. A. Cahana, T. Escamez, R. S. Nowakowski et al., “Targeted mutagenesis of Lis1 disrupts cortical development and LIS1 homodimerization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 11, pp. 6429–6434, 2001. View at Publisher · View at Google Scholar · View at Scopus
  250. S. Hirotsune, M. W. Fleck, M. J. Gambello et al., “Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality,” Nature Genetics, vol. 19, no. 4, pp. 333–339, 1998. View at Publisher · View at Google Scholar · View at Scopus
  251. T. Shu, R. Ayala, M. D. Nguyen, Z. Xie, J. G. Gleeson, and L. H. Tsai, “Ndel1 operates in a common pathway with LIS1 and cytoplasmic dynein to regulate cortical neuronal positioning,” Neuron, vol. 44, no. 2, pp. 263–277, 2004. View at Publisher · View at Google Scholar · View at Scopus
  252. H. Umeshima, T. Hirano, and M. Kengaku, “Microtubule-based nuclear movement occurs independently of centrosome positioning in migrating neurons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 41, pp. 16182–16187, 2007. View at Publisher · View at Google Scholar · View at Scopus
  253. M. F. McManus, I. M. Nasrallah, M. M. Pancoast, A. Wynshaw-Boris, and J. A. Golden, “Lis1 is necessary for normal non-radial migration of inhibitory interneurons,” American Journal of Pathology, vol. 165, no. 3, pp. 775–784, 2004. View at Scopus
  254. K. D. Moore, R. Chen, M. Cilluffo, J. A. Golden, and P. E. Phelps, “Lis1 reduction causes tangential migratory errors in mouse spinal cord,” Journal of Comparative Neurology, vol. 520, no. 6, pp. 1198–1211, 2012.
  255. J. C. Corbo, T. A. Deuel, J. M. Long et al., “Doublecortin is required in mice for lamination of the hippocampus but not the neocortex,” The Journal of Neuroscience, vol. 22, no. 17, pp. 7548–7557, 2002. View at Scopus
  256. O. Reiner, A. Gorelik, and R. Greenman, “Use of RNA interference by in utero electroporation to study cortical development: the example of the doublecortin superfamily,” Genes, vol. 3, no. 4, pp. 759–778, 2012.
  257. C. Kappeler, Y. Saillour, J. P. Baudoin et al., “Branching and nucleokinesis defects in migrating interneurons derived from doublecortin knockout mice,” Human Molecular Genetics, vol. 15, no. 9, pp. 1387–1400, 2006. View at Publisher · View at Google Scholar · View at Scopus
  258. G. Friocourt, J. S. Liu, M. Antypa, S. Rakić, C. A. Walsh, and J. G. Parnavelas, “Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration,” The Journal of Neuroscience, vol. 27, no. 14, pp. 3875–3883, 2007. View at Publisher · View at Google Scholar · View at Scopus
  259. J. Bai, R. L. Ramos, M. Paramasivam, F. Siddiqi, J. B. Ackman, and J. J. LoTurco, “The role of DCX and LIS1 in migration through the lateral cortical stream of developing forebrain,” Developmental Neuroscience, vol. 30, no. 1–3, pp. 144–156, 2008. View at Publisher · View at Google Scholar · View at Scopus
  260. P. J. Ocbina, M. L. V. Dizon, L. Shin, and F. G. Szele, “Doublecortin is necessary for the migration of adult subventricular zone cells from neurospheres,” Molecular and Cellular Neuroscience, vol. 33, no. 2, pp. 126–135, 2006. View at Publisher · View at Google Scholar · View at Scopus
  261. J. S. F. Greenwood, Y. Wang, R. C. Estrada, L. Ackerman, P. T. Ohara, and S. C. Baraban, “Seizures, enhanced excitation, and increased vesicle number in Lis1 mutant mice,” Annals of Neurology, vol. 66, no. 5, pp. 644–653, 2009. View at Publisher · View at Google Scholar · View at Scopus
  262. D. L. Jones and S. C. Baraban, “Inhibitory inputs to hippocampal interneurons are reorganized in Lis1 mutant mice,” Journal of Neurophysiology, vol. 102, no. 2, pp. 648–658, 2009. View at Publisher · View at Google Scholar · View at Scopus
  263. R. F. Hunt, M. T. Dinday, W. Hindle-Katel, and S. C. Baraban, “LIS1 deficiency promotes dysfunctional synaptic integration of granule cells generated in the developing and adult dentate gyrus,” The Journal of Neuroscience, vol. 32, no. 37, pp. 12862–12875, 2012.
  264. L. Valdés-Sánchez, T. Escámez, D. Echevarria et al., “Postnatal alterations of the inhibitory synaptic responses recorded from cortical pyramidal neurons in the Lis1/sLis1 mutant mouse,” Molecular and Cellular Neuroscience, vol. 35, no. 2, pp. 220–229, 2007. View at Publisher · View at Google Scholar · View at Scopus
  265. I. Kawabata, Y. Kashiwagi, K. Obashi et al., “LIS1-dependent retrograde translocation of excitatory synapses in developing interneuron dendrites,” Nature Communications, vol. 3, article 722, 2012.
  266. M. Nosten-Bertrand, C. Kappeler, C. Dinocourt et al., “Epilepsy in Dcx knockout mice associated with discrete lamination defects and enhanced excitability in the hippocampus,” PLoS ONE, vol. 3, no. 6, Article ID e2473, 2008. View at Publisher · View at Google Scholar · View at Scopus
  267. G. Kerjan, H. Koizumi, E. B. Han et al., “Mice lacking doublecortin and doublecortin-like kinase 2 display altered hippocampal neuronal maturation and spontaneous seizures,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 16, pp. 6766–6771, 2009. View at Publisher · View at Google Scholar · View at Scopus
  268. M. Bazelot, J. Simonnet, C. Dinocourt et al., “Cellular anatomy, physiology and epileptiform activity in the CA3 region of Dcx knockout mice: a neuronal lamination defect and its consequences,” European Journal of Neuroscience, vol. 35, no. 2, pp. 244–256, 2012.
  269. J. B. Ackman, L. Aniksztejn, V. Crépel et al., “Abnormal network activity in a targeted genetic model of human double cortex,” The Journal of Neuroscience, vol. 29, no. 2, pp. 313–327, 2009. View at Publisher · View at Google Scholar · View at Scopus
  270. D. Lapray, I. Y. Popova, J. Kindler et al., “Spontaneous epileptic manifestations in a DCX knockdown model of human double cortex,” Cerebral Cortex, vol. 20, no. 11, pp. 2694–2701, 2010. View at Publisher · View at Google Scholar · View at Scopus
  271. M. Yamada, Y. Yoshida, D. Mori et al., “Inhibition of calpain increases LIS1 expression and partially rescues in vivo phenotypes in a mouse model of lissencephaly,” Nature Medicine, vol. 15, no. 10, pp. 1202–1207, 2009. View at Publisher · View at Google Scholar · View at Scopus
  272. M. Yamada, S. Hirotsune, and A. Wynshaw-Boris, “A novel strategy for therapeutic intervention for the genetic disease: preventing proteolytic cleavage using small chemical compound,” International Journal of Biochemistry and Cell Biology, vol. 42, no. 9, pp. 1401–1407, 2010. View at Publisher · View at Google Scholar · View at Scopus
  273. J. B. Manent and J. LoTurco, “Reversing disorders of neuronal migration and differentiation in animal models,” in Jasper's Basic Mechanisms of the Epilepsies, J. L. Noebels, M. Avoli, M. A. Rogawski, and R. W. Olsen, Eds., Delgado-Escueta AV, Bethesda, Md, USA, 4th edition, 2012.
  274. J. Y. Sebe, M. Bershteyn, S. Hirotsune, A. Wynshaw-Boris, and S. C. Baraban, “ALLN rescues an in vitro excitatory synaptic transmission deficit in Lis1 mutant mice,” Journal of Neurophysiology, vol. 109, no. 2, pp. 429–436, 2013. View at Publisher · View at Google Scholar
  275. J. B. Manent, Y. Wang, Y. Chang, M. Paramasivam, and J. J. LoTurco, “Dcx reexpression reduces subcortical band heterotopia and seizure threshold in an animal model of neuronal migration disorder,” Nature Medicine, vol. 15, no. 1, pp. 84–90, 2009. View at Publisher · View at Google Scholar · View at Scopus