Proper lamination of the cerebral cortex requires the orchestrated motility of neurons from their place of birth to their final destination. Improper neuronal migration may result in a wide range of diseases, including brain malformations, such as lissencephaly, mental retardation, schizophrenia, and autism. Ours and other studies have implicated that microtubules and microtubule-associated proteins play an important role in the regulation of neuronal polarization and neuronal migration. Here, we will review normal processes of brain development and neuronal migration, describe neuronal migration diseases, and will focus on the microtubule-associated functions of LIS1 and DCX, which participate in the regulation of neuronal migration and are involved in the human developmental brain disease, lissencephaly. 1. Introduction Defined cell polarization is the key for the function of multiple cell types in the body, for example, the gut epithelium and the neuroepithelium, which both display an apicobasal orientation. Neurons, which part of them are generated from neuroepithelial cells, are also highly polarized cells with two distinct main structures that emerge from the cell body: usually a thin single axon, which is the key for signal transmission, and multiple shorter dendrites, which are designed for signal reception. The basic polarity of neurons was first recognized by Ramon y Cajal, who studied and described the morphology of neurons more than one hundred years ago [1]. In the cerebral cortex, two major types of neurons were defined: the excitatory or the glutaminergic neurons which compose the majority of the neurons in the cerebral cortex, and the inhibitory or the GABAergic interneurons composing the minority of the neurons. These two types of neurons are born in physically distinct areas of the brain, therefore, they need to migrate, sometimes very long distances, to reach their final destinations (reviews [2–6]). Genetic mutations, which affect polarity regulation and processes of neuronal migration in the developing brain, result in a wide array of human diseases. The range of diseases includes on the more severe end brain malformations, such as the lissencephaly-pachygyria spectrum, which defines the variety of diseases that cause relative smoothness of the brain surface and includes lissencephaly (smooth brain surface), agyria (no gyri), and pachygyria (broad gyri). In other cases, the brain surface may appear normal, but neurons can be mislocalized, which will be defined as cortical dysplasia. The position and the extent of the heterotropic
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.
[3]
M. E. Hatten, “New directions in neuronal migration,” Science, vol. 297, no. 5587, pp. 1660–1663, 2002.
[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.
[5]
C. Lambert de Rouvroit and A. M. Goffinet, “Neuronal migration,” Mechanisms of Development, vol. 105, no. 1-2, pp. 47–56, 2001.
[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.
[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.
[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.
[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.
[10]
R. Guerrini and T. Filippi, “Neuronal migration disorders, genetics, and epileptogenesis,” Journal of Child Neurology, vol. 20, no. 4, pp. 287–299, 2005.
[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.
[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.
[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.
[16]
C. Vaillend, R. Poirier, and S. Laroche, “Genes, plasticity and mental retardation,” Behavioural Brain Research, vol. 192, no. 1, pp. 88–105, 2008.
[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.
[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.
[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.
[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.
[22]
M. G？tz and W. B. Huttner, “The cell biology of neurogenesis,” Nature Reviews Molecular Cell Biology, vol. 6, no. 10, pp. 777–788, 2005.
[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.
[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.
[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.
[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.
[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.
[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.
[31]
P. Malatesta, E. Hartfuss, and M. G？tz, “Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neural lineage,” Development, vol. 127, no. 24, pp. 5253–5263, 2000.
[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.
[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.
[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.
[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.
[36]
Y. Kosodo, K. R？per, 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.
[37]
S. C. Noctor, V. Martínez-Cerde？o, 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.
[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.
[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.
[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.
[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.
[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.
[43]
S. C. Noctor, V. Martinez-Cerde？o, 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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[62]
C. Wonders and S. A. Anderson, “Cortical interneurons and their origins,” Neuroscientist, vol. 11, no. 3, pp. 199–205, 2005.
[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.
[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.
[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.
[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.
[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.
[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.
[69]
X. Tan and S. H. Shi, “Neocortical neurogenesis and neuronal migration,” Wiley Interdisciplinary Reviews, 2012.
[70]
T. Mori, A. Buffo, and M. G？tz, “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.
[71]
K. Campbell and M. G？tz, “Radial glia: multi-purpose cells for vertebrate brain development,” Trends in Neurosciences, vol. 25, no. 5, pp. 235–238, 2002.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[81]
L. H. Tsai and J. G. Gleeson, “Nucleokinesis in neuronal migration,” Neuron, vol. 46, no. 3, pp. 383–388, 2005.
[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.
[84]
S. K. McConnell, “The generation of neuronal diversity in the central nervous system,” Annual Review of Neuroscience, vol. 14, pp. 269–300, 1991.
[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.
[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.
[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.
[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.
[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.
[90]
M. E. Hatten, “Central nervous system neuronal migration,” Annual Review of Neuroscience, vol. 22, pp. 511–539, 1999.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[105]
O. Reiner and T. Sapir, “Polarity regulation in migrating neurons in the cortex,” Molecular Neurobiology, vol. 40, no. 1, pp. 1–14, 2009.
[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.
[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.
[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.
[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.
[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.
[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.
[112]
T. Mitchinson and M. Kirschner, “Dynamic instability of microtubule growth,” Nature, vol. 312, no. 5991, pp. 237–242, 1984.
[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.
[114]
E. Schulze and M. Kirschner, “New features of microtubule behaviour observed in vivo,” Nature, vol. 334, no. 6180, pp. 356–359, 1988.
[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.
[116]
P. W. Baas, “Microtubules and neuronal polarity: lessons from mitosis,” Neuron, vol. 22, no. 1, pp. 23–31, 1999.
[117]
M. Stiess and F. Bradke, “Neuronal polarization: the cytoskeleton leads the way,” Developmental Neurobiology, vol. 71, no. 6, pp. 430–444, 2011.
[118]
H. R. Higginbotham and J. G. Gleeson, “The centrosome in neuronal development,” Trends in Neurosciences, vol. 30, no. 6, pp. 276–283, 2007.
[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.
[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.
[121]
M. Distel, J. C. Hocking, K. Volkmann, and R. W. K？ster, “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.
[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.
[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.
[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.
[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.
[127]
O. Reiner, “The unfolding story of two lissencephaly genes and brain development,” Molecular Neurobiology, vol. 20, no. 2-3, pp. 143–156, 1999.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[173]
E. L. F. Holzbaur, “Motor neurons rely on motor proteins,” Trends in Cell Biology, vol. 14, no. 5, pp. 233–240, 2004.
[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.
[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.
[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.
[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.
[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.
[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. Gr？f, “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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[220]
O. Reiner, F. M. Coquelle, B. Peter et al., “The evolving doublecortin (DCX) superfamily,” BMC Genomics, vol. 7, article 188, 2006.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[258]
G. Friocourt, J. S. Liu, M. Antypa, S. Raki？, 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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
[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.
