Molecular components and polarity of radial glial cells during cerebral cortex development
- 687 Downloads
- 1 Citations
Abstract
Originating from ectodermal epithelium, radial glial cells (RGCs) retain apico-basolateral polarity and comprise a pseudostratified epithelial layer in the developing cerebral cortex. The apical endfeet of the RGCs faces the fluid-filled ventricles, while the basal processes extend across the entire cortical span towards the pial surface. RGC functions are largely dependent on this polarized structure and the molecular components that define it. In this review, we will dissect existing molecular evidence on RGC polarity establishment and during cerebral cortex development and provide our perspective on the remaining key questions.
Keywords
Radial glia Embryonic neural stem cell Cerebral cortex development Neurogenesis Epithelial polarity Pseudostratified epitheliumNotes
Acknowledgements
This work is supported by Children’s Mercy-Kansas City Children’s Research Institute. The authors would also like to acknowledge the editing services of the Medical Writing Center at Children’s Mercy-Kansas City for reviewing the manuscript.
References
- 1.Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149–184PubMedPubMedCentralCrossRefGoogle Scholar
- 2.Paridaen JTML, Huttner WB (2014) Neurogenesis during development of the vertebrate central nervous system. EMBO Rep 15:351–364PubMedPubMedCentralCrossRefGoogle Scholar
- 3.Rodriguez-Boulan E, Macara IG (2014) Organization and execution of the epithelial polarity programme. Nat Rev Mol Cell Biol 15:225–242PubMedPubMedCentralCrossRefGoogle Scholar
- 4.O’Brien LE, Jou TS, Pollack AL et al (2001) Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat Cell Biol 3:831–838PubMedCrossRefGoogle Scholar
- 5.Yu W, Datta A, Leroy P et al (2005) β1-integrin orients epithelial polarity via Rac1 and laminin. Mol Biol Cell 16:433–445PubMedPubMedCentralCrossRefGoogle Scholar
- 6.Fernandes VM, McCormack K, Lewellyn L, Verheyen EM (2014) Integrins regulate apical constriction via microtubule stabilization in the drosophila eye disc epithelium. Cell Rep 9:2043–2055PubMedCrossRefGoogle Scholar
- 7.Martin AC, Kaschube M, Wieschaus EF (2009) Pulsed contractions of an actin–myosin network drive apical constriction. Nature 457:495PubMedCrossRefGoogle Scholar
- 8.Sawyer JM, Harrell JR, Shemer G et al (2010) Apical constriction: a cell shape change that can drive morphogenesis. Dev Biol 341:5–19PubMedCrossRefGoogle Scholar
- 9.Campanale JP, Sun TY, Montell DJ (2017) Development and dynamics of cell polarity at a glance. J Cell Sci 130:1201–1207PubMedCrossRefGoogle Scholar
- 10.Assémat E, Bazellières E, Pallesi-Pocachard E et al (2008) Polarity complex proteins. Biochim et Biophys Acta (BBA) Biomembr 1778:614–630CrossRefGoogle Scholar
- 11.Bulgakova NA, Knust E (2009) The Crumbs complex: from epithelial-cell polarity to retinal degeneration. J Cell Sci 122:2587–2596PubMedCrossRefGoogle Scholar
- 12.Su W-H, Mruk DD, Wong EWP et al (2012) Polarity protein complex scribble/Lgl/Dlg and epithelial cell barriers. Adv Exp Med Biol 763:149–170PubMedPubMedCentralGoogle Scholar
- 13.Gassama-Diagne A, Yu W, ter Beest M et al (2006) Phosphatidylinositol-3, 4, 5-trisphosphate regulates the formation of the basolateral plasma membrane in epithelial cells. Nat Cell Biol 8:963–970PubMedCrossRefGoogle Scholar
- 14.Martin-Belmonte F, Gassama A, Datta A et al (2007) PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128:383–397PubMedPubMedCentralCrossRefGoogle Scholar
- 15.Chartier FJ-M, Hardy ÉJ-L, Laprise P (2011) Crumbs controls epithelial integrity by inhibiting Rac1 and PI3K. J Cell Sci 124:3393–3398PubMedCrossRefGoogle Scholar
- 16.Rajasekaran AK, Hojo M, Huima T, Rodriguez-Boulan E (1996) Catenins and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J Cell Biol 132:451–463PubMedCrossRefGoogle Scholar
- 17.Campbell HK, Maiers JL, DeMali KA (2017) Interplay between tight junctions & adherens junctions. Exp Cell Res. doi: 10.1016/j.yexcr.2017.03.061 PubMedGoogle Scholar
- 18.Hansen AH, Duellberg C, Mieck C et al (2017) Cell polarity in cerebral cortex development-cellular architecture shaped by biochemical networks. Front Cell Neurosci 11:176PubMedPubMedCentralCrossRefGoogle Scholar
- 19.Dwyer ND, Chen B, Chou S-J et al (2016) Neural stem cells to cerebral cortex: emerging mechanisms regulating progenitor behavior and productivity. J Neurosci 36:11394–11401PubMedPubMedCentralCrossRefGoogle Scholar
- 20.Den Hollander AI, Ten Brink JB, De Kok YJM et al (1999) Mutations in a human homologue of drosophila crumbs cause retinitis pigmentosa (RP12). Nat Genet 23:217–221CrossRefGoogle Scholar
- 21.den Hollander AI, Heckenlively JR, van den Born LI et al (2001) Leber congenital amaurosis and retinitis pigmentosa with Coats-like exudative vasculopathy are associated with mutations in the crumbs homologue 1 (CRB1) gene. Am J Hum Genet 69:198–203PubMedCentralCrossRefGoogle Scholar
- 22.van de Pavert SA, Kantardzhieva A, Malysheva A et al (2004) Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. J Cell Sci 117:4169–4177PubMedCrossRefGoogle Scholar
- 23.Xiao Z, Patrakka J, Nukui M et al (2011) Deficiency in crumbs homolog 2 (Crb2) affects gastrulation and results in embryonic lethality in mice. Dev Dyn 240:2646–2656PubMedCrossRefGoogle Scholar
- 24.Whiteman EL, Fan S, Harder JL et al (2014) Crumbs3 is essential for proper epithelial development and viability. Mol Cell Biol 34:43–56PubMedPubMedCentralCrossRefGoogle Scholar
- 25.Hsu Y-C, Willoughby JJ, Christensen AK, Jensen AM (2006) Mosaic eyes is a novel component of the crumbs complex and negatively regulates photoreceptor apical size. Development 133:4849–4859PubMedPubMedCentralCrossRefGoogle Scholar
- 26.Boroviak T, Rashbass P (2011) The apical polarity determinant crumbs 2 is a novel regulator of ESC-derived neural progenitors. Stem Cells 29:193–205PubMedCrossRefGoogle Scholar
- 27.Ohata S, Aoki R, Kinoshita S et al (2011) Dual roles of notch in regulation of apically restricted mitosis and apicobasal polarity of neuroepithelial cells. Neuron 69:215–230PubMedCrossRefGoogle Scholar
- 28.Johnson MW, Miyata H, Vinters HV (2002) Ezrin and moesin expression within the developing human cerebrum and tuberous sclerosis-associated cortical tubers. Acta Neuropathol 104:188–196PubMedCrossRefGoogle Scholar
- 29.Kim S, Lehtinen MK, Sessa A et al (2010) The apical complex couples cell fate and cell survival to cerebral cortical development. Neuron 66:69–84PubMedPubMedCentralCrossRefGoogle Scholar
- 30.Graybill C, Wee B, Atwood SX, Prehoda KE (2012) Partitioning-defective protein 6 (Par-6) activates atypical protein kinase C (aPKC) by pseudosubstrate displacement. J Biol Chem 287:21003–21011PubMedPubMedCentralCrossRefGoogle Scholar
- 31.Tobias IS, Newton AC (2016) Protein scaffolds control localized protein kinase Cζ activity. J Biol Chem 291:13809–13822PubMedPubMedCentralCrossRefGoogle Scholar
- 32.Lin D, Edwards AS, Fawcett JP et al (2000) A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol 2:540–547PubMedCrossRefGoogle Scholar
- 33.Plant PJ, Fawcett JP, Lin DCC et al (2003) A polarity complex of mPar-6 and atypical PKC binds, phosphorylates and regulates mammalian Lgl. Nat Cell Biol 5:301–308PubMedCrossRefGoogle Scholar
- 34.Bultje RS, Castaneda-Castellanos DR, Jan LY et al (2009) Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63:189–202PubMedPubMedCentralCrossRefGoogle Scholar
- 35.Cappello S, Attardo A, Wu X et al (2006) The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface. Nat Neurosci 9:1099–1107PubMedCrossRefGoogle Scholar
- 36.Chen L, Liao G, Yang L et al (2006) Cdc42 deficiency causes Sonic hedgehog-independent holoprosencephaly. Proc Natl Acad Sci USA 103:16520–16525PubMedPubMedCentralCrossRefGoogle Scholar
- 37.Hartsock A, Nelson WJ (2008) Adherens and tight junctions: structure, function and connections to the actin cytoskeleton. Biochim Biophys Acta 1778:660–669PubMedCrossRefGoogle Scholar
- 38.Classen A-K, Anderson KI, Marois E, Eaton S (2005) Hexagonal packing of drosophila wing epithelial cells by the planar cell polarity pathway. Dev Cell 9:805–817PubMedCrossRefGoogle Scholar
- 39.Desclozeaux M, Venturato J, Wylie FG et al (2008) Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis. Am J Physiol Cell Physiol 295:C545–C556PubMedCrossRefGoogle Scholar
- 40.Sato K, Watanabe T, Wang S et al (2011) Numb controls E-cadherin endocytosis through p120 catenin with aPKC. Mol Biol Cell 22:3103–3119PubMedPubMedCentralCrossRefGoogle Scholar
- 41.Brüser L, Bogdan S (2017) Adherens Junctions on the move-membrane trafficking of E-Cadherin. Cold Spring Harb Perspect Biol. doi: 10.1101/cshperspect.a029140 PubMedGoogle Scholar
- 42.Stocker AM, Chenn A (2015) The role of adherens junctions in the developing neocortex. Cell Adh Migr 9:167–174PubMedPubMedCentralCrossRefGoogle Scholar
- 43.Malatesta P, Appolloni I, Calzolari F (2008) Radial glia and neural stem cells. Cell Tissue Res 331:165–178PubMedCrossRefGoogle Scholar
- 44.Gänzler-Odenthal SI, Redies C (1998) Blocking N-cadherin function disrupts the epithelial structure of differentiating neural tissue in the embryonic chicken brain. J Neurosci 18:5415–5425PubMedGoogle Scholar
- 45.Kadowaki M, Nakamura S, Machon O et al (2007) N-cadherin mediates cortical organization in the mouse brain. Dev Biol 304:22–33PubMedCrossRefGoogle Scholar
- 46.Zhang J, Woodhead GJ, Swaminathan SK et al (2010) Cortical neural precursors inhibit their own differentiation via N-cadherin maintenance of β-catenin signaling. Dev Cell 18:472–479PubMedPubMedCentralCrossRefGoogle Scholar
- 47.Woodhead GJ, Mutch CA, Olson EC, Chenn A (2006) Cell-autonomous beta-catenin signaling regulates cortical precursor proliferation. J Neurosci 26:12620–12630PubMedPubMedCentralCrossRefGoogle Scholar
- 48.Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365–369PubMedCrossRefGoogle Scholar
- 49.Lien W-H, Klezovitch O, Fernandez TE et al (2006) alphaE-catenin controls cerebral cortical size by regulating the hedgehog signaling pathway. Science 311:1609–1612PubMedPubMedCentralCrossRefGoogle Scholar
- 50.Schmid M-T, Weinandy F, Wilsch-Bräuninger M et al (2014) The role of α-E-catenin in cerebral cortex development: radial glia specific effect on neuronal migration. Front Cell Neurosci 8:215PubMedPubMedCentralCrossRefGoogle Scholar
- 51.Martínez-Martínez MÁ, De Juan Romero C, Fernández V et al (2016) A restricted period for formation of outer subventricular zone defined by Cdh1 and Trnp1 levels. Nat Commun 7:11812PubMedPubMedCentralCrossRefGoogle Scholar
- 52.Petersen PH, Zou K, Hwang JK et al (2002) Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature 419:929–934PubMedCrossRefGoogle Scholar
- 53.Li HS, Wang D, Shen Q et al (2003) Inactivation of Numb and Numblike in embryonic dorsal forebrain impairs neurogenesis and disrupts cortical morphogenesis. Neuron 40:1105–1118PubMedCrossRefGoogle Scholar
- 54.Rašin M-R, Gazula V-R, Breunig JJ et al (2007) Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat Neurosci 10:819–827PubMedCrossRefGoogle Scholar
- 55.Wang P-S, Chou F-S, Ramachandran S et al (2016) Crucial roles of the Arp2/3 complex during mammalian corticogenesis. Development 143:2741–2752PubMedPubMedCentralCrossRefGoogle Scholar
- 56.Chou F-S, Wang P-S (2016) The Arp2/3 complex is essential at multiple stages of neural development. Neurogenesis 3:e1261653PubMedPubMedCentralCrossRefGoogle Scholar
- 57.Shah B, Lutter D, Tsytsyura Y et al (2016) Rap1 GTPases are master regulators of neural cell polarity in the developing neocortex. Cereb Cortex. doi: 10.1093/cercor/bhv341 Google Scholar
- 58.Maeta K, Edamatsu H, Nishihara K et al (2016) Crucial role of Rapgef2 and Rapgef6, a family of guanine nucleotide exchange factors for Rap1 small GTPase, in formation of apical surface adherens junctions and neural progenitor development in the mouse cerebral cortex. eNeuro. doi: 10.1523/ENEURO.0142-16.2016 PubMedPubMedCentralGoogle Scholar
- 59.Marthiens V, ffrench-Constant C (2009) Adherens junction domains are split by asymmetric division of embryonic neural stem cells. EMBO Rep 10:515–520PubMedPubMedCentralCrossRefGoogle Scholar
- 60.Pedersen LB, Veland IR, Schrøder JM, Christensen ST (2008) Assembly of primary cilia. Dev Dyn 237:1993–2006PubMedCrossRefGoogle Scholar
- 61.Wong SY, Reiter JF (2008) The primary cilium at the crossroads of mammalian hedgehog signaling. Curr Top Dev Biol 85:225–260PubMedPubMedCentralCrossRefGoogle Scholar
- 62.Mariani LE, Bijlsma MF, Ivanova AI et al (2016) Arl13b regulates Shh signaling from both inside and outside the cilium. Mol Biol Cell. doi: 10.1091/mbc.E16-03-0189 PubMedPubMedCentralGoogle Scholar
- 63.Bhattacharyya S, Rainey MA, Arya P et al (2016) Endocytic recycling protein EHD1 regulates primary cilia morphogenesis and SHH signaling during neural tube development. Sci Rep 6:20727PubMedPubMedCentralCrossRefGoogle Scholar
- 64.Choi H, Shin JH, Kim ES et al (2016) Primary cilia negatively regulate melanogenesis in melanocytes and pigmentation in a human skin model. PLoS One 11:e0168025PubMedPubMedCentralCrossRefGoogle Scholar
- 65.Kaku M, Komatsu Y (2017) Functional diversity of ciliary proteins in bone development and disease. Curr Osteoporos Rep. doi: 10.1007/s11914-017-0351-6 PubMedGoogle Scholar
- 66.Snedeker J, Schock EN, Struve JN et al (2017) Unique spatiotemporal requirements for intraflagellar transport genes during forebrain development. PLoS One 12:e0173258PubMedPubMedCentralCrossRefGoogle Scholar
- 67.Millington G, Elliott KH, Chang Y-T et al (2017) Cilia-dependent GLI processing in neural crest cells is required for tongue development. Dev Biol. doi: 10.1016/j.ydbio.2017.02.021 PubMedGoogle Scholar
- 68.Wheatley DN (2005) Landmarks in the first hundred years of primary (9 + 0) cilium research. Cell Biol Int 29:333–339PubMedCrossRefGoogle Scholar
- 69.Satir P, Christensen ST (2007) Overview of structure and function of mammalian cilia. Annu Rev Physiol 69:377–400PubMedCrossRefGoogle Scholar
- 70.Wong MY, McCaughan GW, Strasser SI (2017) An update on the pathophysiology and management of polycystic liver disease. Expert Rev Gastroenterol Hepatol. doi: 10.1080/17474124.2017.1309280 PubMedGoogle Scholar
- 71.Ma M, Gallagher A-R, Somlo S (2017) Ciliary mechanisms of cyst formation in polycystic kidney disease. Cold Spring Harb Perspect Biol. doi: 10.1101/cshperspect.a028209 PubMedGoogle Scholar
- 72.Goetz SC, Bangs F, Barrington CL et al (2017) The Meckel syndrome—associated protein MKS1 functionally interacts with components of the BBSome and IFT complexes to mediate ciliary trafficking and hedgehog signaling. PLoS One 12:e0173399PubMedPubMedCentralCrossRefGoogle Scholar
- 73.Lehtinen MK, Zappaterra MW, Chen X et al (2011) The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron 69:893–905PubMedPubMedCentralCrossRefGoogle Scholar
- 74.Paridaen JTML, Wilsch-Bräuninger M, Huttner WB (2013) Asymmetric inheritance of centrosome-associated primary cilium membrane directs ciliogenesis after cell division. Cell 155:333–344PubMedCrossRefGoogle Scholar
- 75.Wilsch-Bräuninger M, Florio M, Huttner WB (2016) Neocortex expansion in development and evolution—from cell biology to single genes. Curr Opin Neurobiol 39:122–132PubMedCrossRefGoogle Scholar
- 76.Huangfu D, Liu A, Rakeman AS et al (2003) Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 426:83–87PubMedCrossRefGoogle Scholar
- 77.Corbit KC, Aanstad P, Singla V et al (2005) Vertebrate smoothened functions at the primary cilium. Nature 437:1018–1021PubMedCrossRefGoogle Scholar
- 78.Haycraft CJ, Banizs B, Aydin-Son Y et al (2005) Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet 1:e53PubMedPubMedCentralCrossRefGoogle Scholar
- 79.Ma Y, Erkner A, Gong R et al (2002) Hedgehog-mediated patterning of the mammalian embryo requires transporter-like function of dispatched. Cell 111:63–75PubMedCrossRefGoogle Scholar
- 80.Higginbotham H, Guo J, Yokota Y et al (2013) Arl13b-regulated cilia activities are essential for polarized radial glial scaffold formation. Nat Neurosci 16:1000–1007PubMedPubMedCentralCrossRefGoogle Scholar
- 81.Ezratty EJ, Stokes N, Chai S et al (2011) A role for the primary cilium in notch signaling and epidermal differentiation during skin development. Cell 145:1129–1141PubMedPubMedCentralCrossRefGoogle Scholar
- 82.Bergstralh DT, Haack T, St Johnston D (2013) Epithelial polarity and spindle orientation: intersecting pathways. Philos Trans R Soc Lond B Biol Sci 368:20130291PubMedPubMedCentralCrossRefGoogle Scholar
- 83.Vorhagen S, Niessen CM (2014) Mammalian aPKC/Par polarity complex mediated regulation of epithelial division orientation and cell fate. Exp Cell Res 328:296–302PubMedCrossRefGoogle Scholar
- 84.Durgan J, Kaji N, Jin D, Hall A (2011) Par6B and atypical PKC regulate mitotic spindle orientation during epithelial morphogenesis. J Biol Chem 286:12461–12474PubMedPubMedCentralCrossRefGoogle Scholar
- 85.Carvalho CA, Moreira S, Ventura G et al (2015) Aurora A triggers Lgl cortical release during symmetric division to control planar spindle orientation. Curr Biol 25:53–60PubMedCrossRefGoogle Scholar
- 86.Lancaster MA, Knoblich JA (2012) Spindle orientation in mammalian cerebral cortical development. Curr Opin Neurobiol 22:737–746PubMedPubMedCentralCrossRefGoogle Scholar
- 87.di Pietro F, Echard A, Morin X (2016) Regulation of mitotic spindle orientation: an integrated view. EMBO Rep 17:1106–1130PubMedPubMedCentralCrossRefGoogle Scholar
- 88.Lamouille S, Xu J, Derynck R (2014) Molecular mechanisms of epithelial–mesenchymal transition. Nat Rev Mol Cell Biol 15:178–196PubMedPubMedCentralCrossRefGoogle Scholar
- 89.Wheelock MJ, Shintani Y, Maeda M et al (2008) Cadherin switching. J Cell Sci 121:727–735PubMedCrossRefGoogle Scholar
- 90.Noctor SC, Flint AC, Weissman TA et al (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409:714–720PubMedCrossRefGoogle Scholar
- 91.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 7:136–144PubMedCrossRefGoogle Scholar
- 92.Noctor SC, Martínez-Cerdeño V, Kriegstein AR (2008) Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J Comp Neurol 508:28–44PubMedPubMedCentralCrossRefGoogle Scholar
- 93.Konno D, Shioi G, Shitamukai A et al (2008) Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis. Nat Cell Biol 10:93–101PubMedCrossRefGoogle Scholar
- 94.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 31:3683–3695PubMedCrossRefGoogle Scholar
- 95.Subramanian L, Bershteyn M, Paredes MF, Kriegstein AR (2017) Dynamic behaviour of human neuroepithelial cells in the developing forebrain. Nat Commun 8:14167PubMedPubMedCentralCrossRefGoogle Scholar
- 96.Haydar TF, Ang E Jr, Rakic P (2003) Mitotic spindle rotation and mode of cell division in the developing telencephalon. Proc Natl Acad Sci USA 100:2890–2895PubMedPubMedCentralCrossRefGoogle Scholar
- 97.Yingling J, Youn YH, Darling D et al (2008) Neuroepithelial stem cell proliferation requires LIS1 for precise spindle orientation and symmetric division. Cell 132:474–486PubMedPubMedCentralCrossRefGoogle Scholar
- 98.Falk S, Bugeon S, Ninkovic J et al (2017) Time-specific effects of spindle positioning on embryonic progenitor pool composition and adult neural stem cell seeding. Neuron 93(777–791):e3Google Scholar
- 99.Itoh Y, Moriyama Y, Hasegawa T et al (2013) Scratch regulates neuronal migration onset via an epithelial-mesenchymal transition-like mechanism. Nat Neurosci 16:416–425PubMedCrossRefGoogle Scholar
- 100.Stipursky J, Francis D, Dezonne RS et al (2014) TGF-β1 promotes cerebral cortex radial glia-astrocyte differentiation in vivo. Front Cell Neurosci 8:393PubMedPubMedCentralCrossRefGoogle Scholar
- 101.Klezovitch O, Fernandez TE, Tapscott SJ, Vasioukhin V (2004) Loss of cell polarity causes severe brain dysplasia in Lgl1 knockout mice. Genes Dev 18:559–571PubMedPubMedCentralCrossRefGoogle Scholar
- 102.Jossin Y, Lee M, Klezovitch O et al (2017) Llgl1 connects cell polarity with cell–cell adhesion in embryonic neural stem cells. Dev Cell. doi: 10.1016/j.devcel.2017.05.002 PubMedGoogle Scholar
- 103.Yokota Y, Eom T-Y, Stanco A 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 137:4101–4110PubMedPubMedCentralCrossRefGoogle Scholar
- 104.Miyata T, Ogawa M (2007) Twisting of neocortical progenitor cells underlies a spring-like mechanism for daughter-cell migration. Curr Biol 17:146–151PubMedCrossRefGoogle Scholar
- 105.Siegenthaler JA, Ashique AM, Zarbalis K et al (2009) Retinoic acid from the meninges regulates cortical neuron generation. Cell 139:597–609PubMedPubMedCentralCrossRefGoogle Scholar
- 106.Seuntjens E, Nityanandam A, Miquelajauregui A et al (2009) Sip1 regulates sequential fate decisions by feedback signaling from postmitotic neurons to progenitors. Nat Neurosci 12:1373–1380PubMedCrossRefGoogle Scholar
- 107.Griveau A, Borello U, Causeret F et al (2010) A novel role for Dbx1-derived Cajal-Retzius cells in early regionalization of the cerebral cortical neuroepithelium. PLoS Biol 8:e1000440PubMedPubMedCentralCrossRefGoogle Scholar
- 108.Miyata T, Kawaguchi A, Okano H, Ogawa M (2001) Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31:727–741PubMedCrossRefGoogle Scholar
- 109.Yokota Y, Kim W-Y, Chen Y et al (2009) The adenomatous polyposis coli protein is an essential regulator of radial glial polarity and construction of the cerebral cortex. Neuron 61:42–56PubMedPubMedCentralCrossRefGoogle Scholar
- 110.Tsunekawa Y, Britto JM, Takahashi M et al (2012) Cyclin D2 in the basal process of neural progenitors is linked to non-equivalent cell fates. EMBO J 31:1879–1892PubMedPubMedCentralCrossRefGoogle Scholar
- 111.Pilaz L-J, Lennox AL, Rouanet JP, Silver DL (2016) Dynamic mRNA transport and local translation in radial glial progenitors of the developing brain. Curr Biol 26:3383–3392PubMedPubMedCentralCrossRefGoogle Scholar
- 112.Taverna E, Huttner WB (2010) Neural progenitor nuclei IN motion. Neuron 67:906–914PubMedCrossRefGoogle Scholar
- 113.Miyata T, Okamoto M, Shinoda T, Kawaguchi A (2014) Interkinetic nuclear migration generates and opposes ventricular-zone crowding: insight into tissue mechanics. Front Cell Neurosci 8:473PubMedGoogle Scholar
- 114.Georges-Labouesse E, Mark M, Messaddeq N, Gansmüller A (1998) Essential role of α6 integrins in cortical and retinal lamination. Curr Biol 8:983–986PubMedCrossRefGoogle Scholar
- 115.Graus-Porta D, Blaess S, Senften M et al (2001) Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31:367–379PubMedCrossRefGoogle Scholar
- 116.Beggs HE, Schahin-Reed D, Zang K et al (2003) FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40:501–514PubMedPubMedCentralCrossRefGoogle Scholar
- 117.Halfter W, Dong S, Yip Y-P et al (2002) A critical function of the pial basement membrane in cortical histogenesis. J Neurosci 22:6029–6040PubMedGoogle Scholar
- 118.Haubst N, Georges-Labouesse E, De Arcangelis A et al (2006) Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes. Development 133:3245–3254PubMedCrossRefGoogle Scholar
- 119.Zarbalis K, Siegenthaler JA, Choe Y et al (2007) Cortical dysplasia and skull defects in mice with a Foxc1 allele reveal the role of meningeal differentiation in regulating cortical development. Proc Natl Acad Sci USA 104:14002–14007PubMedPubMedCentralCrossRefGoogle Scholar
- 120.Zheng C, Heintz N, Hatten ME (1996) CNS gene encoding astrotactin, which supports neuronal migration along glial fibers. Science 272:417–419PubMedCrossRefGoogle Scholar
- 121.Anton ES, Marchionni MA, Lee KF, Rakic P (1997) Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124:3501–3510PubMedGoogle Scholar
- 122.Schmid RS, McGrath B, Berechid BE et al (2003) Neuregulin 1–erbB2 signaling is required for the establishment of radial glia and their transformation into astrocytes in cerebral cortex. Proc Natl Acad Sci 100:4251–4256PubMedPubMedCentralCrossRefGoogle Scholar
- 123.Patten BA, Peyrin JM, Weinmaster G, Corfas G (2003) Sequential signaling through Notch1 and erbB receptors mediates radial glia differentiation. J Neurosci 23:6132–6140PubMedGoogle Scholar
- 124.Anthony TE, Mason HA, Gridley T et al (2005) Brain lipid-binding protein is a direct target of notch signaling in radial glial cells. Genes Dev 19:1028–1033PubMedPubMedCentralCrossRefGoogle Scholar