1932

Abstract

Neural stem and progenitor cells have a central role in the development and evolution of the mammalian neocortex. In this review, we first provide a set of criteria to classify the various types of cortical stem and progenitor cells. We then discuss the issue of cell polarity, as well as specific subcellular features of these cells that are relevant for their modes of division and daughter cell fate. In addition, cortical stem and progenitor cell behavior is placed into a tissue context, with consideration of extracellular signals and cell-cell interactions. Finally, the differences across species regarding cortical stem and progenitor cells are dissected to gain insight into key developmental and evolutionary mechanisms underlying neocortex expansion.

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2014-10-06
2024-03-28
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Literature Cited

  1. Aaku-Saraste E, Hellwig A, Huttner WB. 1996. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure—remodeling of the neuroepithelium prior to neurogenesis. Dev. Biol. 180:664–79 [Google Scholar]
  2. Aguilar A, Meunier A, Strehl L, Martinovic J, Bonniere M. et al. 2012. Analysis of human samples reveals impaired SHH-dependent cerebellar development in Joubert syndrome/Meckel syndrome. Proc. Natl. Acad. Sci. USA 109:16951–56 [Google Scholar]
  3. Antony JM, Paquin A, Nutt SL, Kaplan DR, Miller FD. 2011. Endogenous microglia regulate development of embryonic cortical precursor cells. J. Neurosci. Res. 89:286–98 [Google Scholar]
  4. Arai Y, Funatsu N, Numayama-Tsuruta K, Nomura T, Nakamura S, Osumi N. 2005. Role of Fabp7, a downstream gene of Pax6, in the maintenance of neuroepithelial cells during early embryonic development of the rat cortex. J. Neurosci. 25:9752–61 [Google Scholar]
  5. Arai Y, Pulvers JN, Haffner C, Schilling B, Nusslein I. et al. 2011. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2:154 [Google Scholar]
  6. Asami M, Pilz GA, Ninkovic J, Godinho L, Schroeder T. et al. 2011. The role of Pax6 in regulating the orientation and mode of cell division of progenitors in the mouse cerebral cortex. Development 138:5067–78 [Google Scholar]
  7. Attardo A, Calegari F, Haubensak W, Wilsch-Bräuninger M, Huttner WB. 2008. Live imaging at the onset of cortical neurogenesis reveals differential appearance of the neuronal phenotype in apical versus basal progenitor progeny. PLOS One 3:e2388 [Google Scholar]
  8. Bae BI, Tietjen I, Atabay KD, Evrony GD, Johnson MB. et al. 2014. Evolutionarily dynamic alternative splicing of GPR56 regulates regional cerebral cortical patterning. Science 343:764–68 [Google Scholar]
  9. Bahi-Buisson N, Guerrini R. 2013. Diffuse malformations of cortical development. Handb. Clin. Neurol. 111:653–65 [Google Scholar]
  10. Bar I, Lambert de Rouvroit C, Goffinet AM. 2000. The Reelin signaling pathway in mouse cortical development. Eur. J. Morphol. 38:321–25 [Google Scholar]
  11. Baye LM, Link BA. 2007. Interkinetic nuclear migration and the selection of neurogenic cell divisions during vertebrate retinogenesis. J. Neurosci. 27:10143–52 [Google Scholar]
  12. Baye LM, Link BA. 2008. Nuclear migration during retinal development. Brain Res. 1192:29–36 [Google Scholar]
  13. Bentivoglio M, Mazzarello P. 1999. The history of radial glia. Brain Res. Bull. 49:305–15 [Google Scholar]
  14. Betizeau M, Cortay V, Patti D, Pfister S, Gautier E. et al. 2013. Precursor diversity and complexity of lineage relationships in the outer subventricular zone (OSVZ) of the primate. Neuron 80:442–57 [Google Scholar]
  15. Bettencourt-Dias M, Hildebrandt F, Pellman D, Woods G, Godinho SA. 2011. Centrosomes and cilia in human disease. Trends Genet. 27:307–15 [Google Scholar]
  16. Bittman K, Owens DF, Kriegstein AR, LoTurco JJ. 1997. Cell coupling and uncoupling in the ventricular zone of developing neocortex. J. Neurosci. 17:7037–44 [Google Scholar]
  17. Bond J, Roberts E, Mochida GH, Hampshire DJ, Scott S. et al. 2002. ASPM is a major determinant of cerebral cortical size. Nat. Genet. 32:316–20 [Google Scholar]
  18. Bond J, Roberts E, Springell K, Lizarraga S, Scott S. et al. 2005. A centrosomal mechanism involving CDK5RAP2 and CENPJ controls brain size. Nat. Genet. 37:353–55 [Google Scholar]
  19. Bond J, Scott S, Hampshire DJ, Springell K, Corry P. et al. 2003. Protein-truncating mutations in ASPM cause variable reduction in brain size. Am. J. Hum. Genet. 73:1170–77 [Google Scholar]
  20. Bond J, Woods CG. 2005. Cytoskeletal genes regulating brain size. Curr. Opin. Cell Biol. 18:95–101 [Google Scholar]
  21. Borrell V, Cardenas A, Ciceri G, Galceran J, Flames N. et al. 2012. Slit/Robo signaling modulates the proliferation of central nervous system progenitors. Neuron 76:338–52 [Google Scholar]
  22. Borrell V, Götz M. 2014. . Role of radial glial cells in cerebral cortex folding. Curr. Opin. Neurobiol. 27:39–46 [Google Scholar]
  23. Borrell V, Marín O. 2006. Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling. Nat. Neurosci. 9:1284–93 [Google Scholar]
  24. Borrell V, Reillo I. 2012. Emerging roles of neural stem cells in cerebral cortex development and evolution. Dev. Neurobiol. 72:955–71 [Google Scholar]
  25. Buchman JJ, Tseng HC, Zhou Y, Frank CL, Xie Z, Tsai LH. 2010. Cdk5rap2 interacts with pericentrin to maintain the neural progenitor pool in the developing neocortex. Neuron 66:386–402 [Google Scholar]
  26. Bultje RS, Castaneda-Castellanos DR, Jan LY, Jan YN, Kriegstein AR, Shi SH. 2009. Mammalian Par3 regulates progenitor cell asymmetric division via Notch signaling in the developing neocortex. Neuron 63:189–202 [Google Scholar]
  27. Calegari F, Haubensak W, Haffner C, Huttner WB. 2005. Selective lengthening of the cell cycle in the neurogenic subpopulation of neural progenitor cells during mouse brain development. J. Neurosci. 25:6533–38 [Google Scholar]
  28. Calegari F, Huttner WB. 2003. An inhibition of cyclin-dependent kinases that lengthens, but does not arrest, neuroepithelial cell cycle induces premature neurogenesis. J. Cell Sci. 116:4947–55 [Google Scholar]
  29. Cappello S. 2013. Small Rho-GTPases and cortical malformations: fine-tuning the cytoskeleton stability. Small GTPases 4:51–56 [Google Scholar]
  30. Cappello S, Attardo A, Wu X, Iwasato T, Itohara S. et al. 2006. The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat. Neurosci. 9:1099–107 [Google Scholar]
  31. Cappello S, Bohringer CR, Bergami M, Conzelmann KK, Ghanem A. et al. 2012. A radial glia-specific role of RhoA in double cortex formation. Neuron 73:911–24 [Google Scholar]
  32. Cappello S, Monzo P, Vallee RB. 2011. NudC is required for interkinetic nuclear migration and neuronal migration during neocortical development. Dev. Biol. 357:326–35 [Google Scholar]
  33. Cayouette M, Raff M. 2002. Asymmetric segregation of Numb: a mechanism for neural specification from Drosophila to mammals. Nat. Neurosci. 5:1265–69 [Google Scholar]
  34. Chae TH, Kim S, Marz KE, Hanson PI, Walsh CA. 2004. The hyh mutation uncovers roles for αSnap in apical protein localization and control of neural cell fate. Nat. Genet. 36:264–70 [Google Scholar]
  35. Chatzi C, Cunningham TJ. 2013. Investigation of retinoic acid function during embryonic brain development using retinaldehyde-rescued Rdh10 knockout mice.. Dev. Dyn. 242:1056–65 [Google Scholar]
  36. Chen F, LoTurco J. 2012. A method for stable transgenesis of radial glia lineage in rat neocortex by piggyBac mediated transposition. J. Neurosci. Methods 207:172–80 [Google Scholar]
  37. Chenn A, Walsh CA. 2002. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365–69 [Google Scholar]
  38. Chenn A, Walsh CA. 2003. Increased neuronal production, enlarged forebrains and cytoarchitectural distortions in β-catenin overexpressing transgenic mice. Cereb. Cortex 13:599–606 [Google Scholar]
  39. Cheung AFP, Kondo S, Abdel-Mannan O, Chodroff RA, Sirey TM. et al. 2010. The subventricular zone is the developmental milestone of a 6-layered neocortex: comparisons in metatherian and eutherian mammals. Cereb. Cortex 20:1071–81 [Google Scholar]
  40. Corbeil D, Marzesco AM, Wilsch-Brauninger M, Huttner WB. 2010. The intriguing links between prominin-1 (CD133), cholesterol-based membrane microdomains, remodeling of apical plasma membrane protrusions, extracellular membrane particles, and (neuro)epithelial cell differentiation. FEBS Lett. 584:1659–64 [Google Scholar]
  41. Costa MR, Wen G, Lepier A, Schroeder T, Götz M. 2008. Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development 135:11–22 [Google Scholar]
  42. Cremisi F. 2013. MicroRNAs and cell fate in cortical and retinal development. Front. Cell. Neurosci. 7:141 [Google Scholar]
  43. Cunningham CL, Martínez-Cerdeño V, Noctor SC. 2013. Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J. Neurosci. 33:4216–33 [Google Scholar]
  44. Dehay C, Kennedy H. 2007. Cell-cycle control and cortical development. Nat. Rev. Neurosci. 8:438–50 [Google Scholar]
  45. Del Bene F, Wehman AM, Link BA, Baier H. 2008. Regulation of neurogenesis by interkinetic nuclear migration through an apical-basal notch gradient. Cell 134:1055–65 [Google Scholar]
  46. Dubreuil V, Marzesco AM, Corbeil D, Huttner WB, Wilsch-Brauninger M. 2007. Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J. Cell Biol. 176:483–95 [Google Scholar]
  47. Dziegielewska KM, Ek J, Habgood MD, Saunders NR. 2001. Development of the choroid plexus. Microsc. Res. Tech. 52:5–20 [Google Scholar]
  48. Elias LA, Kriegstein AR. 2008. Gap junctions: multifaceted regulators of embryonic cortical development. Trends Neurosci. 31:243–50 [Google Scholar]
  49. Elias LA, Wang DD, Kriegstein AR. 2007. Gap junction adhesion is necessary for radial migration in the neocortex. Nature 448:901–7 [Google Scholar]
  50. Ettinger AW, Wilsch-Brauninger M, Marzesco AM, Bickle M, Lohmann A. et al. 2011. Proliferating versus differentiating stem and cancer cells exhibit distinct midbody-release behaviour. Nat. Commun. 2:503 [Google Scholar]
  51. Fang WQ, Chen WW, Fu AK, Ip NY. 2013. Axin directs the amplification and differentiation of intermediate progenitors in the developing cerebral cortex. Neuron 79:665–79 [Google Scholar]
  52. Faulkner NE, Dujardin DL, Tai CY, Vaughan KT, O'Connell CB. et al. 2000. A role for the lissencephaly gene LIS1 in mitosis and cytoplasmic dynein function. Nat. Cell Biol. 2:784–91 [Google Scholar]
  53. Fei JF, Haffner C, Huttner WB. 2014. 3′ UTR-dependent, miR-92-mediated restriction of Tis21 expression maintains asymmetric neural stem cell division to ensure proper neocortex size. Cell Rep. 7:398–411 [Google Scholar]
  54. Fernandez C, Tatard VM, Bertrand N, Dahmane N. 2010. Differential modulation of Sonic-hedgehog-induced cerebellar granule cell precursor proliferation by the IGF signaling network. Dev. Neurosci. 32:59–70 [Google Scholar]
  55. Fietz SA, Huttner WB. 2011. Cortical progenitor expansion, self-renewal and neurogenesis—a polarized perspective. Curr. Opin. Neurobiol. 21:23–35 [Google Scholar]
  56. Fietz SA, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D. et al. 2010. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci. 13:690–99 [Google Scholar]
  57. Fietz SA, Lachmann R, Brandl H, Kircher M, Samusik N. et al. 2012. Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal. Proc. Natl. Acad. Sci. USA 109:11836–41 [Google Scholar]
  58. Fish JL, Kennedy H, Dehay C, Huttner WB. 2008. Making bigger brains—the evolution of neural-progenitor-cell division. J. Cell Sci. 121:2783–93 [Google Scholar]
  59. Fish JL, Kosodo Y, Enard W, Paabo S, Huttner WB. 2006. Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc. Natl. Acad. Sci. USA 103:10438–43 [Google Scholar]
  60. Gal JS, Morozov YM, Ayoub AE, Chatterjee M, Rakic P, Haydar TF. 2006. Molecular and morphological heterogeneity of neural precursors in the mouse neocortical proliferative zones. J. Neurosci. 26:1045–56 [Google Scholar]
  61. García-Marqués J, López-Mascaraque L. 2013. Clonal identity determines astrocyte cortical heterogeneity. Cereb. Cortex 23:1463–72 [Google Scholar]
  62. García-Moreno F, Vasistha NA, Trevia N, Bourne JA, Molnár Z. 2012. Compartmentalization of cerebral cortical germinal zones in a lissencephalic primate and gyrencephalic rodent. Cereb. Cortex 22:482–92 [Google Scholar]
  63. Gertz CC, Lui JH, LaMonica BE, Wang X, Kriegstein AR. 2014. Diverse behaviors of outer radial glia in developing ferret and human cortex.. J. Neurosci. 34:2559–70 [Google Scholar]
  64. Gilmore EC, Walsh CA. 2013. Genetic causes of microcephaly and lessons for neuronal development. Wiley Interdiscip. Rev. Dev. Biol. 2:461–78 [Google Scholar]
  65. Götz M, Huttner WB. 2005. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6:777–88 [Google Scholar]
  66. Guerout N, Li X, Barnabe-Heider F. 2014. Cell fate control in the developing central nervous system. Exp. Cell Res. 321:77–83 [Google Scholar]
  67. Hall A. 2005. Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 33:891–95 [Google Scholar]
  68. Hansen DV, Lui JH, Parker PR, Kriegstein AR. 2010. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554–61 [Google Scholar]
  69. Hartfuss E, Forster E, Bock HH, Hack MA, Leprince P. et al. 2003. Reelin signaling directly affects radial glia morphology and biochemical maturation. Development 130:4597–609 [Google Scholar]
  70. Haubensak W, Attardo A, Denk W, Huttner WB. 2004. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl. Acad. Sci. USA 101:3196–201 [Google Scholar]
  71. Haubst N, Georges-Labouesse E, De Arcangelis A, Mayer U, Götz M. 2006. Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes. Development 133:3245–54 [Google Scholar]
  72. Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL. et al. 2002. Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5:308–15 [Google Scholar]
  73. Herzog D, Loetscher P, van Hengel J, Knüsel S, Brakebusch C. et al. 2011. The small GTPase RhoA is required to maintain spinal cord neuroepithelium organization and the neural stem cell pool. J. Neurosci. 31:5120–30 [Google Scholar]
  74. Higginbotham H, Guo J, Yokota Y, Umberger NL, Su CY. et al. 2013. Arl13b-regulated cilia activities are essential for polarized radial glial scaffold formation. Nat. Neurosci. 16:1000–7 [Google Scholar]
  75. Hippenmeyer S. 2014. Molecular pathways controlling the sequential steps of cortical projection neuron migration. Adv. Exp. Med. Biol. 800:1–24 [Google Scholar]
  76. Hirabayashi Y, Gotoh Y. 2010. . Epigenetic control of neural precursor cell fate during development.. Nat. Rev. Neurosci. 11:377–88 [Google Scholar]
  77. Hirabayashi Y, Itoh Y, Tabata H, Nakajima K, Akiyama T. et al. 2004. The Wnt/β-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131:2791–801 [Google Scholar]
  78. Holland JD, Klaus A, Garratt AN, Birchmeier W. 2013. Wnt signaling in stem and cancer stem cells. Curr. Opin. Cell Biol. 25:254–64 [Google Scholar]
  79. Huttner WB, Kosodo Y. 2005. Symmetric versus asymmetric cell division during neurogenesis in the developing vertebrate central nervous system. Curr. Opin. Cell Biol. 17:648–57 [Google Scholar]
  80. Huveneers S, de Rooij J. 2013. Mechanosensitive systems at the cadherin-F-actin interface. J. Cell Sci. 126:403–13 [Google Scholar]
  81. Imayoshi I, Shimojo H, Sakamoto M, Ohtsuka T, Kageyama R. 2013. Genetic visualization of notch signaling in mammalian neurogenesis. Cell. Mol. Life Sci. 70:2045–57 [Google Scholar]
  82. Itoh Y, Moriyama Y, Hasegawa T, Endo TA, Toyoda T, Gotoh Y. 2013a. Scratch regulates neuronal migration onset via an epithelial-mesenchymal transition-like mechanism. Nat. Neurosci. 16:416–25 [Google Scholar]
  83. Itoh Y, Tyssowski K, Gotoh Y. 2013b. Transcriptional coupling of neuronal fate commitment and the onset of migration. Curr. Opin. Neurobiol. 23:957–64 [Google Scholar]
  84. Iwata T, Hevner RF. 2009. Fibroblast growth factor signaling in development of the cerebral cortex. Dev. Growth Differ. 51:299–323 [Google Scholar]
  85. Jackson AP, Eastwood H, Bell SM, Adu J, Toomes C. et al. 2002. Identification of microcephalin, a protein implicated in determining the size of the human brain. Am. J. Hum. Genet. 71:136–42 [Google Scholar]
  86. Jaffe AB, Hall A. 2005. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21:247–69 [Google Scholar]
  87. Javaherian A, Kriegstein A. 2009. A stem cell niche for intermediate progenitor cells of the embryonic cortex. Cereb. Cortex 19:Suppl. 1i70–77 [Google Scholar]
  88. Jeong SJ, Luo R, Singer K, Giera S, Kreidberg J. et al. 2013. GPR56 functions together with α3β1 integrin in regulating cerebral cortical development. PLOS One 8:e68781 [Google Scholar]
  89. Johansson PA, Cappello S, Götz M. 2010. Stem cells niches during development—lessons from the cerebral cortex. Curr. Opin. Neurobiol. 20:400–7 [Google Scholar]
  90. Johansson PA, Dziegielewska KM, Liddelow SA, Saunders NR. 2008. The blood-CSF barrier explained: when development is not immaturity. BioEssays 30:237–48 [Google Scholar]
  91. Johansson PA, Irmler M, Acampora D, Beckers J, Simeone A, Götz M. 2013. The transcription factor Otx2 regulates choroid plexus development and function. Development 140:1055–66 [Google Scholar]
  92. Jung JU, Ko K, Lee DH, Chang KT, Choo YK. 2009. The roles of glycosphingolipids in the proliferation and neural differentiation of mouse embryonic stem cells. Exp. Mol. Med. 41:935–45 [Google Scholar]
  93. Kageyama R, Ohtsuka T, Shimojo H, Imayoshi I. 2009. Dynamic regulation of Notch signaling in neural progenitor cells. Curr. Opin. Cell Biol. 21:733–40 [Google Scholar]
  94. Katayama K, Melendez J, Baumann JM, Leslie JR, Chauhan BK. et al. 2011. Loss of RhoA in neural progenitor cells causes the disruption of adherens junctions and hyperproliferation. Proc. Natl. Acad. Sci. USA 108:7607–12 [Google Scholar]
  95. Kelava I, Reillo I, Murayama AY, Kalinka AT, Stenzel D. et al. 2012. Abundant occurrence of basal radial glia in the subventricular zone of embryonic neocortex of a lissencephalic primate, the common marmoset Callithrix jacchus. Cereb. Cortex 22:469–81 [Google Scholar]
  96. Kim J, Krishnaswami SR, Gleeson JG. 2008. CEP290 interacts with the centriolar satellite component PCM-1 and is required for Rab8 localization to the primary cilium. Hum. Mol. Genet. 17:3796–805 [Google Scholar]
  97. Kim S, Lehtinen MK, Sessa A, Zappaterra MW, Cho SH. et al. 2010. The apical complex couples cell fate and cell survival to cerebral cortical development. Neuron 66:69–84 [Google Scholar]
  98. Kim S, Walsh CA. 2007. Numb, neurogenesis and epithelial polarity. Nat. Neurosci. 10:812–13 [Google Scholar]
  99. Kim W, Kim M, Jho EH. 2013. Wnt/β-catenin signalling: from plasma membrane to nucleus. Biochem. J. 450:9–21 [Google Scholar]
  100. Kim WY, Wang X, Wu Y, Doble BW, Patel S. et al. 2009. GSK-3 is a master regulator of neural progenitor homeostasis. Nat. Neurosci. 12:1390–97 [Google Scholar]
  101. Knoblich JA. 2001. Asymmetric cell division during animal development. Nat. Rev. Mol. Cell Biol. 2:11–20 [Google Scholar]
  102. Kobielak A, Fuchs E. 2004. α-Catenin: at the junction of intercellular adhesion and actin dynamics. Nat. Rev. Mol. Cell Biol. 5:614–25 [Google Scholar]
  103. Komada M, Saitsu H, Kinboshi M, Miura T, Shiota K, Ishibashi M. 2008. Hedgehog signaling is involved in development of the neocortex. Development 135:2717–27 [Google Scholar]
  104. Komuro H, Rakic P. 1998. Distinct modes of neuronal migration in different domains of developing cerebellar cortex. J. Neurosci. 18:1478–90 [Google Scholar]
  105. Konno D, Shioi G, Shitamukai A, Mori A, Kiyonari H. et al. 2008. Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat. Cell Biol. 10:93–101 [Google Scholar]
  106. Kosodo Y, Huttner WB. 2009. Basal process and cell divisions of neural progenitors in the developing brain. Dev. Growth Differ. 51:251–61 [Google Scholar]
  107. Kosodo Y, Kimura A, Suetsugu T, Baba SA, Matsuzaki F. 2009. Comprehensive analysis of interkinetic nuclear migration in developing mouse brain. Mech. Dev. 126:S84 [Google Scholar]
  108. Kosodo Y, Röper K, Haubensak W, Marzesco A-M, Corbeil D, Huttner WB. 2004. Asymmetric distribution of the apical plasma membrane during neurogenic divisions of mammalian neuroepithelial cells. EMBO J. 23:2314–24 [Google Scholar]
  109. Kosodo Y, Suetsugu T, Suda M, Mimori-Kiyosue Y, Toida K. et al. 2011. Regulation of interkinetic nuclear migration by cell cycle-coupled active and passive mechanisms in the developing brain. EMBO J. 30:1690–704 [Google Scholar]
  110. Kosodo Y, Toida K, Dubreuil V, Alexandre P, Schenk J. et al. 2008. Cytokinesis of neuroepithelial cells can divide their basal process before anaphase. EMBO J. 27:3151–63 [Google Scholar]
  111. Kurabayashi N, Nguyen MD, Sanada K. 2013. The G protein-coupled receptor GPRC5B contributes to neurogenesis in the developing mouse neocortex. Development 140:4335–46 [Google Scholar]
  112. Kriegstein A, Noctor S, Martínez-Cerdeño V. 2006. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat. Rev. Neurosci. 7:883–90 [Google Scholar]
  113. Kriegstein AR, Götz M. 2003. Radial glia diversity: a matter of cell fate. Glia 43:37–43 [Google Scholar]
  114. Kriegstein AR, Noctor SC. 2004. Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 27:392–99 [Google Scholar]
  115. Kuwahara A, Hirabayashi Y, Knoepfler PS, Taketo MM, Sakai J. et al. 2010. Wnt signaling and its downstream target N-myc regulate basal progenitors in the developing neocortex. Development 137:1035–44 [Google Scholar]
  116. Lakomá J, Garcia-Alonso L, Luque JM. 2011. Reelin sets the pace of neocortical neurogenesis. Development 138:5223–34 [Google Scholar]
  117. LaMonica BE, Lui JH, Hansen DV, Kriegstein AR. 2013. Mitotic spindle orientation predicts outer radial glial cell generation in human neocortex. Nat. Commun. 4:1665 [Google Scholar]
  118. LaMonica BE, Lui JH, Wang X, Kriegstein AR. 2012. OSVZ progenitors in the human cortex: an updated perspective on neurodevelopmental disease. Curr. Opin. Neurobiol. 22:747–53 [Google Scholar]
  119. Lancaster MA, Gleeson JG. 2009. The primary cilium as a cellular signaling center: lessons from disease. Curr. Opin. Genet. Dev. 19:220–29 [Google Scholar]
  120. Lancaster MA, Gopal DJ, Kim J, Saleem SN, Silhavy JL. et al. 2011. Defective Wnt-dependent cerebellar midline fusion in a mouse model of Joubert syndrome. Nat. Med. 17:726–31 [Google Scholar]
  121. Lancaster MA, Knoblich JA. 2012. Spindle orientation in mammalian cerebral cortical development. Curr. Opin. Neurobiol. 22:737–46 [Google Scholar]
  122. Lancaster MA, Renner M, Martin CA, Wenzel D, Bicknell LS. et al. 2013. Cerebral organoids model human brain development and microcephaly. Nature 501:373–79 [Google Scholar]
  123. Lange C, Huttner WB, Calegari F. 2009. Cdk4/CyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5:320–31 [Google Scholar]
  124. Lee HO, Norden C. 2013. Mechanisms controlling arrangements and movements of nuclei in pseudostratified epithelia. Trends Cell Biol. 23:141–50 [Google Scholar]
  125. Lehtinen MK, Bjornsson CS, Dymecki SM, Gilbertson RJ, Holtzman DM, Monuki ES. 2013. The choroid plexus and cerebrospinal fluid: emerging roles in development, disease, and therapy. J. Neurosci. 33:17553–59 [Google Scholar]
  126. Lehtinen MK, Walsh CA. 2011. Neurogenesis at the brain-cerebrospinal fluid interface. Annu. Rev. Cell Dev. Biol. 27:653–79 [Google Scholar]
  127. Lehtinen MK, Zappaterra MW, Chen X, Yang YJ, Hill AD. et al. 2011. The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 69:893–905 [Google Scholar]
  128. Leung L, Klopper AV, Grill SW, Harris WA, Norden C. 2011. Apical migration of nuclei during G2 is a prerequisite for all nuclear motion in zebrafish neuroepithelia. Development 138:5003–13 [Google Scholar]
  129. Liu X, Hashimoto-Torii K, Torii M, Ding C, Rakic P. 2010. Gap junctions/hemichannels modulate interkinetic nuclear migration in the forebrain precursors. J. Neurosci. 30:4197–209 [Google Scholar]
  130. Liu X, Hashimoto-Torii K, Torii M, Haydar TF, Rakic P. 2008. The role of ATP signaling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone. Proc. Natl. Acad. Sci. USA 105:11802–7 [Google Scholar]
  131. Lizarraga SB, Margossian SP, Harris MH, Campagna DR, Han AP. et al. 2010. Cdk5rap2 regulates centrosome function and chromosome segregation in neuronal progenitors. Development 137:1907–17 [Google Scholar]
  132. LoTurco J, Kriegstein A. 1991. Clusters of coupled neuroblasts in embryonic neocortex. Science 252:563–66 [Google Scholar]
  133. Loulier K, Barry R, Mahou P, Le Franc Y, Supatto W. et al. 2014. Multiplex cell and lineage tracking with combinatorial labels. Neuron 81:505–20 [Google Scholar]
  134. Loulier K, Lathia JD, Marthiens V, Relucio J, Mughal MR. et al. 2009. β1 Integrin maintains integrity of the embryonic neocortical stem cell niche. PLOS Biol 7:e1000176 [Google Scholar]
  135. Louvi A, Grove EA. 2011. Cilia in the CNS: The quiet organelle claims center stage. Neuron 69:1046–60 [Google Scholar]
  136. Lui JH, Hansen DV, Kriegstein AR. 2011. Development and evolution of the human neocortex. Cell 146:18–36 [Google Scholar]
  137. Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C. et al. 2005. G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47:353–64 [Google Scholar]
  138. Ma S, Kwon HJ, Johng H, Zang K, Huang Z. 2013. Radial glial neural progenitors regulate nascent brain vascular network stabilization via inhibition of Wnt signaling. PLOS Biol. 11:e1001469 [Google Scholar]
  139. Malatesta P, Hartfuss E, Götz M. 2000. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127:5253–63 [Google Scholar]
  140. Marthiens V, Ffrench-Constant C. 2009. Adherens junction domains are split by asymmetric division of embryonic neural stem cells. EMBO Rep. 10:515–20 [Google Scholar]
  141. Marthiens V, Kazanis I, Moss L, Long K, Ffrench-Constant C. 2010. Adhesion molecules in the stem cell niche—more than just staying in shape?. J. Cell Sci. 123:1613–22 [Google Scholar]
  142. Marthiens V, Rujano MA, Pennetier C, Tessier S, Paul-Gilloteaux P, Basto R. 2013. Centrosome amplification causes microcephaly. Nat. Cell Biol. 15:731–40 [Google Scholar]
  143. Martin-Belmonte F, Gassama A, Datta A, Yu W, Rescher U. et al. 2007. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128:383–97 [Google Scholar]
  144. Marzesco A-M, Janich P, Wilsch-Brauninger M, Dubreuil V, Langenfeld K. et al. 2005. Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J. Cell Sci. 118:2849–58 [Google Scholar]
  145. Marzesco A-M, Wilsch-Bräuninger M, Dubreuil V, Janich P, Langenfeld K. et al. 2009. Release of extracellular membrane vesicles from microvilli of epithelial cells is enhanced by depleting membrane cholesterol. FEBS Lett. 583:897–902 [Google Scholar]
  146. McCarthy RA, Argraves WS. 2003. Megalin and the neurodevelopmental biology of sonic hedgehog and retinol. J. Cell Sci. 116:955–60 [Google Scholar]
  147. McCarthy RA, Barth JL, Chintalapudi MR, Knaak C, Argraves WS. 2002. Megalin functions as an endocytic sonic hedgehog receptor. J. Biol. Chem. 277:25660–67 [Google Scholar]
  148. Megraw TL, Sharkey JT, Nowakowski RS. 2011. Cdk5rap2 exposes the centrosomal root of microcephaly syndromes. Trends Cell Biol. 21:470–80 [Google Scholar]
  149. Meigs TE, Fields TA, McKee DD, Casey PJ. 2001. Interaction of Gα12 and Gα13 with the cytoplasmic domain of cadherin provides a mechanism for β-catenin release. Proc. Natl. Acad. Sci. USA 98:519–24 [Google Scholar]
  150. Miyata T, Kawaguchi A, Okano H, Ogawa M. 2001. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727–41 [Google Scholar]
  151. Miyata T, Kawaguchi A, Saito K, Kawano M, Muto T, Ogawa M. 2004. Asymmetric production of surface-dividing and non-surface-dividing cortical progenitor cells. Development 131:3133–45 [Google Scholar]
  152. Molnar Z. 2011. Evolution of cerebral cortical development. Brain Behav. Evol. 78:94–107 [Google Scholar]
  153. Moon HM, Wynshaw-Boris A. 2013. Cytoskeleton in action: lissencephaly, a neuronal migration disorder. Wiley Interdiscip. Rev. Dev. Biol. 2:229–45 [Google Scholar]
  154. Mora-Bermúdez F, García M, Huttner W. 2013. Stem cells: neural stem cells in cerebral cortex development. Neuroscience in the 21st Century D Pfaff 137–59 New York: Springer [Google Scholar]
  155. Morin X, Jaouen F, Durbec P. 2007. Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium. Nat. Neurosci. 10:1440–48 [Google Scholar]
  156. Morris NR, Efimov VP, Xiang X. 1998a. Nuclear migration, nucleokinesis and lissencephaly. Trends Cell Biol. 8:467–70 [Google Scholar]
  157. Morris SM, Albrecht U, Reiner O, Eichele G, Yu-Lee LY. 1998b. The lissencephaly gene product Lis1, a protein involved in neuronal migration, interacts with a nuclear movement protein, NudC. Curr. Biol. 8:603–6 [Google Scholar]
  158. Murciano A, Zamora J, López-Sánchez J, Frade JM. 2002. Interkinetic nuclear movement may provide spatial clues to the regulation of neurogenesis. Mol. Cell. Neurosci. 21:285–300 [Google Scholar]
  159. Neugebauer JM, Amack JD, Peterson AG, Bisgrove BW, Yost HJ. 2009. FGF signalling during embryo development regulates cilia length in diverse epithelia. Nature 458:651–54 [Google Scholar]
  160. Nicholas AK, Khurshid M, Desir J, Carvalho OP, Cox JJ. et al. 2010. WDR62 is associated with the spindle pole and is mutated in human microcephaly. Nat. Genet. 42:1010–14 [Google Scholar]
  161. Ninkovic J, Götz M. 2013. Fate specification in the adult brain—lessons for eliciting neurogenesis from glial cells. BioEssays 35:242–52 [Google Scholar]
  162. Ninkovic J, Steiner-Mezzadri A, Jawerka M, Akinci U, Masserdotti G. et al. 2013. The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic cross-regulatory transcriptional network. Cell Stem Cell 13:403–18 [Google Scholar]
  163. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR. 2001. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714–20 [Google Scholar]
  164. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7:136–44 [Google Scholar]
  165. Noctor SC, Martínez-Cerdeño V, Kriegstein AR. 2007. Neural stem and progenitor cells in cortical development. Novartis Found. Symp. 288:59–73; discussion 73–78, 96–98 [Google Scholar]
  166. Norden C, Young S, Link BA, Harris WA. 2009. Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138:1195–208 [Google Scholar]
  167. Okamoto M, Namba T, Shinoda T, Kondo T, Watanabe T. et al. 2013. TAG-1-assisted progenitor elongation streamlines nuclear migration to optimize subapical crowding. Nat. Neurosci. 16:1556–66 [Google Scholar]
  168. Osumi N, Shinohara H, Numayama-Tsuruta K, Maekawa M. 2008. Concise review: Pax6 transcription factor contributes to both embryonic and adult neurogenesis as a multifunctional regulator. Stem Cells 26:1663–72 [Google Scholar]
  169. Owens DF, Kriegstein AR. 1998. Patterns of intracellular calcium fluctuation in precursor cells of the neocortical ventricular zone. J. Neurosci. 18:5374–88 [Google Scholar]
  170. Paridaen JT, Huttner WB. 2014. Neurogenesis during development of the vertebrate central nervous system. EMBO Rep. 15:351–64 [Google Scholar]
  171. Paridaen JT, Wilsch-Brauninger M, Huttner WB. 2013. Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell 155:333–44 [Google Scholar]
  172. Peyre E, Morin X. 2012. An oblique view on the role of spindle orientation in vertebrate neurogenesis. Dev. Growth Differ. 54:287–305 [Google Scholar]
  173. Pilaz LJ, Patti D, Marcy G, Ollier E, Pfister S. et al. 2009. Forced G1-phase reduction alters mode of division, neuron number, and laminar phenotype in the cerebral cortex. Proc. Natl. Acad. Sci. USA 106:21924–29 [Google Scholar]
  174. Pilz GA, Shitamukai A, Reillo I, Pacary E, Schwausch J. et al. 2013. Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type. Nat. Commun. 4:2125 [Google Scholar]
  175. Pinto L, Götz M. 2007. Radial glial cell heterogeneity—the source of diverse progeny in the CNS. Prog. Neurobiol. 83:2–23 [Google Scholar]
  176. Poduri A, Evrony GD, Cai X, Walsh CA. 2013. Somatic mutation, genomic variation, and neurological disease. Science 341:6141 [Google Scholar]
  177. Poirier K, Lebrun N, Broix L, Tian G, Saillour Y. et al. 2013. Mutations in TUBG1, DYNC1H1, KIF5C and KIF2A cause malformations of cortical development and microcephaly. Nat. Genet. 45:639–47 [Google Scholar]
  178. Qu Q, Sun G, Murai K, Ye P, Li W. et al. 2013. Wnt7a regulates multiple steps of neurogenesis. Mol. Cell. Biol. 33:2551–59 [Google Scholar]
  179. Rakic P. 2000. Radial unit hypothesis of neocortical expansion. Novartis Found. Symp. 228:30–42; discussion 42–52 [Google Scholar]
  180. Rakic P. 2003. Elusive radial glial cells: historical and evolutionary perspective. Glia 43:19–32 [Google Scholar]
  181. Rakic P, Lombroso PJ. 1998. Development of the cerebral cortex: I. Forming the cortical structure. J. Am. Acad. Child Adolesc. Psychiatry 37:116–17 [Google Scholar]
  182. Rao G, Pedone CA, Del Valle L, Reiss K, Holland EC, Fults DW. 2004. Sonic hedgehog and insulin-like growth factor signaling synergize to induce medulloblastoma formation from nestin-expressing neural progenitors in mice. Oncogene 23:6156–62 [Google Scholar]
  183. Rasin MR, Gazula VR, Breunig JJ, Kwan KY, Johnson MB. et al. 2007. Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat. Neurosci. 10:819–27 [Google Scholar]
  184. Reillo I, Borrell V. 2012. Germinal zones in the developing cerebral cortex of ferret: ontogeny, cell cycle kinetics, and diversity of progenitors. Cereb. Cortex 22:2039–54 [Google Scholar]
  185. Reillo I, de Juan Romero C, García-Cabezas MA, Borrell V. 2011. A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb. Cortex 21:1674–94 [Google Scholar]
  186. Reiner O, Sapir T. 2013. LIS1 functions in normal development and disease. Curr. Opin. Neurobiol. 23:951–56 [Google Scholar]
  187. Röper K, Corbeil D, Huttner WB. 2000. Retention of prominin in microvilli reveals distinct cholesterol-based lipid microdomains in the apical plasma membrane. Nat. Cell Biol. 2:582–92 [Google Scholar]
  188. Rowitch DH, Kriegstein AR. 2010. Developmental genetics of vertebrate glial-cell specification. Nature 468:214–22 [Google Scholar]
  189. Rujano MA, Sanchez-Pulido L, Pennetier C, le Dez G, Basto R. 2013. The microcephaly protein Asp regulates neuroepithelium morphogenesis by controlling the spatial distribution of myosin II. Nat. Cell Biol. 15:1294–306 [Google Scholar]
  190. Saarikangas J, Hakanen J, Mattila PK, Grumet M, Salminen M, Lappalainen P. 2008. ABBA regulates plasma-membrane and actin dynamics to promote radial glia extension. J. Cell Sci. 121:1444–54 [Google Scholar]
  191. Saito K, Dubreuil V, Arai Y, Wilsch-Brauninger M, Schwudke D. et al. 2009. Ablation of cholesterol biosynthesis in neural stem cells increases their VEGF expression and angiogenesis but causes neuron apoptosis. Proc. Natl. Acad. Sci. USA 106:8350–55 [Google Scholar]
  192. Salomoni P, Calegari F. 2010. Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol. 20:233–43 [Google Scholar]
  193. Sattar S, Gleeson JG. 2011. The ciliopathies in neuronal development: a clinical approach to investigation of Joubert syndrome and Joubert syndrome-related disorders. Dev. Med. Child Neurol. 53:793–98 [Google Scholar]
  194. Sauer FC. 1935. Mitosis in the neural tube. J. Comp. Neurol. 62:377–405 [Google Scholar]
  195. Scheidecker S, Etard C, Pierce NW, Geoffroy V, Schaefer E. et al. 2013. Exome sequencing of Bardet-Biedl syndrome patient identifies a null mutation in the BBSome subunit BBIP1 (BBS18). J. Med. Genet. 51:132–36 [Google Scholar]
  196. Schenk J, Wilsch-Brauninger M, Calegari F, Huttner WB. 2009. Myosin II is required for interkinetic nuclear migration of neural progenitors. Proc. Natl. Acad. Sci. USA 106:16487–92 [Google Scholar]
  197. Schuck S, Simons K. 2004. Polarized sorting in epithelial cells: raft clustering and the biogenesis of the apical membrane. J. Cell Sci. 117:5955–64 [Google Scholar]
  198. Segklia A, Seuntjens E, Elkouris M, Tsalavos S, Stappers E. et al. 2012. Bmp7 regulates the survival, proliferation, and neurogenic properties of neural progenitor cells during corticogenesis in the mouse. PLOS One 7:e34088 [Google Scholar]
  199. Sheen VL, Ganesh VS, Topcu M, Sebire G, Bodell A. et al. 2004. Mutations in ARFGEF2 implicate vesicle trafficking in neural progenitor proliferation and migration in the human cerebral cortex. Nat. Genet. 36:69–76 [Google Scholar]
  200. Shewan A, Eastburn DJ, Mostov K. 2011. Phosphoinositides in cell architecture. Cold Spring Harb. Perspect. Biol. 3:a004796 [Google Scholar]
  201. Shitamukai A, Konno D, Matsuzaki F. 2011. Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J. Neurosci. 31:3683–95 [Google Scholar]
  202. Shitamukai A, Matsuzaki F. 2012. Control of asymmetric cell division of mammalian neural progenitors. Dev. Growth Differ. 54:277–86 [Google Scholar]
  203. Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH. et al. 2009. Retinoic acid from the meninges regulates cortical neuron generation. Cell 139:597–609 [Google Scholar]
  204. Simons K, Fuller SD. 1985. Cell surface polarity in epithelia. Annu. Rev. Cell Biol. 1:243–88 [Google Scholar]
  205. Simons K, Toomre D. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31–39 [Google Scholar]
  206. Simons K, van Meer G. 1988. Lipid sorting in epithelial cells. Biochemistry 27:6197–202 [Google Scholar]
  207. Singer K, Luo R, Jeong SJ, Piao X. 2013. GPR56 and the developing cerebral cortex: cells, matrix, and neuronal migration. Mol. Neurobiol. 47:186–96 [Google Scholar]
  208. Smart IH. 1971. Location and orientation of mitotic figures in the developing mouse olfactory epithelium. J. Anat. 109:243–51 [Google Scholar]
  209. Smart IH, Dehay C, Giroud P, Berland M, Kennedy H. 2002. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb. Cortex 12:37–53 [Google Scholar]
  210. Smart IHM. 1972a. Proliferative characteristics of the ependymal layer during the early development of the spinal cord in the mouse. J. Anat. 111:365–80 [Google Scholar]
  211. Smart IHM. 1972b. Proliferative characteristics of the ependymal layer during the early development of the mouse diencephalon, as revealed by recording the number, location, and plane of cleavage of mitotic figures. J. Anat. 113:109–29 [Google Scholar]
  212. Smart IHM. 1973. 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. J. Anat. 116:67–91 [Google Scholar]
  213. Soriano E, del Río JA. 2005. The cells of Cajal-Retzius: still a mystery one century after. Neuron 46:389–94 [Google Scholar]
  214. Spassky N, Han YG, Aguilar A, Strehl L, Besse L. et al. 2008. Primary cilia are required for cerebellar development and Shh-dependent expansion of progenitor pool. Dev. Biol. 317:246–59 [Google Scholar]
  215. Stahl R, Walcher T, De Juan Romero C, Pilz GA, Cappello S. et al. 2013. Trnp1 regulates expansion and folding of the mammalian cerebral cortex by control of radial glial fate. Cell 153:535–49 [Google Scholar]
  216. Stenzel D, Wilsch-Brauninger M, Wong FK, Heuer H, Huttner WB. 2014. Integrin αvβ3 and thyroid hormones promote expansion of progenitors in embryonic neocortex. Development 141:795–806 [Google Scholar]
  217. Stojiljkovic M, Blagojevic T, Vukosavic S, Zvezdina ND, Pekovic S. et al. 1996. Ganglioside GM1 and GM3 in early human brain development: an immunocytochemical study. Int. J. Dev. Neurosci. 14:35–44 [Google Scholar]
  218. Stubbs D, DeProto J, Nie K, Englund C, Mahmud I. et al. 2009. . Neurovascular congruence during cerebral cortical development.. Cereb. Cortex 19:Suppl. 1i32–41 [Google Scholar]
  219. Sun T, Hevner RF. 2014. Growth and folding of the mammalian cerebral cortex: from molecules to malformations. Nat. Rev. Neurosci. 15:217–32 [Google Scholar]
  220. Sutor B, Hagerty T. 2005. Involvement of gap junctions in the development of the neocortex. Biochim. Biophys. Acta 1719:59–68 [Google Scholar]
  221. Suzuki SC, Takeichi M. 2008. Cadherins in neuronal morphogenesis and function. Dev. Growth Differ. 50:Suppl. 1S119–30 [Google Scholar]
  222. Tamai H, Shinohara H, Miyata T, Saito K, Nishizawa Y. et al. 2007. Pax6 transcription factor is required for the interkinetic nuclear movement of neuroepithelial cells. Genes Cells 12:983–96 [Google Scholar]
  223. Tanaka T, Serneo FF, Higgins C, Gambello MJ, Wynshaw-Boris A, Gleeson JG. 2004. Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration. J. Cell Biol. 165:709–21 [Google Scholar]
  224. Taverna E, Haffner C, Pepperkok R, Huttner WB. 2012. A new approach to manipulate the fate of single neural stem cells in tissue. Nat. Neurosci. 15:329–37 [Google Scholar]
  225. Taverna E, Huttner WB. 2010. Neural progenitor nuclei IN motion. Neuron 67:906–14 [Google Scholar]
  226. Teissier A, Waclaw RR, Griveau A, Campbell K, Pierani A. 2011. Tangentially migrating transient glutamatergic neurons control neurogenesis and maintenance of cerebral cortical progenitor pools. Cereb. Cortex 22:403–16 [Google Scholar]
  227. Tepass U. 2012. The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival. Annu. Rev. Cell Dev. Biol. 28:655–85 [Google Scholar]
  228. Thornton GK, Woods CG. 2009. Primary microcephaly: Do all roads lead to Rome?. Trends Genet. 25:501–10 [Google Scholar]
  229. Tsai JW, Chen Y, Kriegstein AR, Vallee RB. 2005. LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J. Cell Biol. 170:935–45 [Google Scholar]
  230. Tsai JW, Lian WN, Kemal S, Kriegstein AR, Vallee RB. 2010. Kinesin 3 and cytoplasmic dynein mediate interkinetic nuclear migration in neural stem cells. Nat. Neurosci. 13:1463–71 [Google Scholar]
  231. Tsunekawa Y, Britto JM, Takahashi M, Polleux F, Tan SS, Osumi N. 2012. Cyclin D2 in the basal process of neural progenitors is linked to non-equivalent cell fates. EMBO J. 31:1879–92 [Google Scholar]
  232. Tsunekawa Y, Osumi N. 2012. How to keep proliferative neural stem/progenitor cells: a critical role of asymmetric inheritance of cyclin D2. Cell Cycle 11:3550–54 [Google Scholar]
  233. Tuoc TC, Pavlakis E, Tylkowski MA, Stoykova A. 2014. Control of cerebral size and thickness. Cell. Mol. Life Sci. In press
  234. Tyler WA, Haydar TF. 2013. Multiplex genetic fate mapping reveals a novel route of neocortical neurogenesis, which is altered in the Ts65Dn mouse model of Down syndrome. J. Neurosci. 33:5106–19 [Google Scholar]
  235. Ueno M, Yamashita T. 2014. Bidirectional tuning of microglia in the developing brain: from neurogenesis to neural circuit formation. Curr. Opin. Neurobiol. 27C:8–15 [Google Scholar]
  236. Valente EM, Rosti RO, Gibbs E, Gleeson JG. 2014. Primary cilia in neurodevelopmental disorders. Nat. Rev. Neurol. 10:27–36 [Google Scholar]
  237. Vallee RB, Tai C, Faulkner NE. 2001. LIS1: cellular function of a disease-causing gene. Trends Cell Biol. 11:155–60 [Google Scholar]
  238. Wang X, Tsai JW, Imai JH, Lian WN, Vallee RB, Shi SH. 2009. Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461:947–55 [Google Scholar]
  239. Wang X, Tsai JW, Lamonica B, Kriegstein AR. 2011. A new subtype of progenitor cell in the mouse embryonic neocortex. Nat. Neurosci. 14:555–61 [Google Scholar]
  240. Wang Z, Wu T, Shi L, Zhang L, Zheng W. et al. 2010. Conserved motif of CDK5RAP2 mediates its localization to centrosomes and the Golgi complex. J. Biol. Chem. 285:22658–65 [Google Scholar]
  241. Wei Q, Zhang Y, Li Y, Zhang Q, Ling K, Hu J. 2012. The BBSome controls IFT assembly and turnaround in cilia. Nat. Cell Biol. 14:950–57 [Google Scholar]
  242. Wicher G, Larsson M, Rask L, Aldskogius H. 2005. Low-density lipoprotein receptor-related protein (LRP)-2/megalin is transiently expressed in a subpopulation of neural progenitors in the embryonic mouse spinal cord. J. Comp. Neurol. 492:123–31 [Google Scholar]
  243. Wilcock AC, Swedlow JR, Storey KG. 2007. Mitotic spindle orientation distinguishes stem cell and terminal modes of neuron production in the early spinal cord. Development 134:1943–54 [Google Scholar]
  244. Willnow TE, Hilpert J, Armstrong SA, Rohlmann A, Hammer RE. et al. 1996. Defective forebrain development in mice lacking gp330/megalin. Proc. Natl. Acad. Sci. USA 93:8460–64 [Google Scholar]
  245. Wilsch-Bräuninger M, Peters J, Paridaen JTML, Huttner WB. 2012. Basolateral rather than apical primary cilia on neuroepithelial cells committed to delamination. Development 139:95–105 [Google Scholar]
  246. Wodarz A, Nusse R. 1998. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14:59–88 [Google Scholar]
  247. Woods CG. 2004. Human microcephaly. Curr. Opin. Neurobiol. 14:112–17 [Google Scholar]
  248. Woods CG, Bond J, Enard W. 2005. Autosomal recessive primary microcephaly (MCPH): a review of clinical, molecular, and evolutionary findings. Am. J. Hum. Genet. 76:717–28 [Google Scholar]
  249. Wynshaw-Boris A, Gambello MJ. 2001. LIS1 and dynein motor function in neuronal migration and development. Genes Dev. 15:639–51 [Google Scholar]
  250. Xuan S, Baptista CA, Balas G, Tao W, Soares VC, Lai E. 1995. Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 14:1141–52 [Google Scholar]
  251. Yamashita M. 2013. From neuroepithelial cells to neurons: changes in the physiological properties of neuroepithelial stem cells. Arch. Biochem. Biophys. 534:64–70 [Google Scholar]
  252. Yeh C, Li A, Chuang JZ, Saito M, Cáceres A, Sung CH. 2013. IGF-1 activates a cilium-localized noncanonical Gβγ signaling pathway that regulates cell-cycle progression. Dev. Cell 26:358–68 [Google Scholar]
  253. Yokota Y, Eom TY, Stanco A, Kim WY, Rao S. et al. 2010. Cdc42 and Gsk3 modulate the dynamics of radial glial growth, inter-radial glial interactions and polarity in the developing cerebral cortex. Development 137:4101–10 [Google Scholar]
  254. Yoon KJ, Koo BK, Im SK, Jeong HW, Ghim J. et al. 2008. Mind bomb 1-expressing intermediate progenitors generate notch signaling to maintain radial glial cells. Neuron 58:519–31 [Google Scholar]
  255. Zhang JN, Woodhead GJ, Swaminathan SK, Noles SR, McQuinn ER. et al. 2010. Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of β-catenin signaling. Dev. Cell 18:472–79 [Google Scholar]
  256. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y. et al. 2009. SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 64:173–87 [Google Scholar]
  257. Zhong W, Feder JN, Jiang MM, Jan LY, Jan YN. 1996. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron 17:43–53 [Google Scholar]
  258. Zhou Y, Atkins JB, Rompani SB, Bancescu DL, Petersen PH. et al. 2007. The mammalian Golgi regulates numb signaling in asymmetric cell division by releasing ACBD3 during mitosis. Cell 129:163–78 [Google Scholar]
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