Role of radial glial cells in cerebral cortex folding

Radial glial cells play key roles during cerebral cortex development, as primary stem and progenitor cells giving rise-directly or indirectly-to neurons and glia, but also acting as scaffold for the cerebral cortex architecture and migrating neurons. Recent work led to the discovery of novel types of radial glial cells with key roles in gyrification, the folding of the mammalian cerebral cortex in phylogeny and ontogeny. Here we summarize the cellular and molecular basis of this fascinating process allowing the expansion of the mammalian cerebral cortex with all its functional consequences.

[1]  M. Götz,et al.  The cell biology of neurogenesis , 2006, International Journal of Developmental Neuroscience.

[2]  F. Vaccarino,et al.  Cortical Gyrification Induced by Fibroblast Growth Factor 2 in the Mouse Brain , 2013, The Journal of Neuroscience.

[3]  V. Borrell,et al.  Germinal zones in the developing cerebral cortex of ferret: ontogeny, cell cycle kinetics, and diversity of progenitors. , 2012, Cerebral cortex.

[4]  J. Chun,et al.  Non-proliferative effects of lysophosphatidic acid enhance cortical growth and folding , 2003, Nature Neuroscience.

[5]  Anjen Chenn,et al.  Regulation of Cerebral Cortical Size by Control of Cell Cycle Exit in Neural Precursors , 2002, Science.

[6]  A. Peterson,et al.  Retinoic Acid from the Meninges Regulates Cortical Neuron Generation , 2009, Cell.

[7]  Magdalena Götz,et al.  Trnp1 Regulates Expansion and Folding of the Mammalian Cerebral Cortex by Control of Radial Glial Fate , 2013, Cell.

[8]  Hiroshi Kiyonari,et al.  Neuroepithelial progenitors undergo LGN-dependent planar divisions to maintain self-renewability during mammalian neurogenesis , 2008, Nature Cell Biology.

[9]  F. Matsuzaki,et al.  Oblique Radial Glial Divisions in the Developing Mouse Neocortex Induce Self-Renewing Progenitors outside the Germinal Zone That Resemble Primate Outer Subventricular Zone Progenitors , 2011, The Journal of Neuroscience.

[10]  S. Itohara,et al.  The Rho-GTPase cdc42 regulates neural progenitor fate at the apical surface , 2006, Nature Neuroscience.

[11]  Isabel Reillo,et al.  Emerging roles of neural stem cells in cerebral cortex development and evolution , 2012, Developmental neurobiology.

[12]  Federico Calegari,et al.  Regulation of cerebral cortex size and folding by expansion of basal progenitors , 2013, The EMBO journal.

[13]  P. Rakic A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution , 1995, Trends in Neurosciences.

[14]  Henry Kennedy,et al.  Precursor Diversity and Complexity of Lineage Relationships in the Outer Subventricular Zone of the Primate , 2013, Neuron.

[15]  V. Martínez‐Cerdeño,et al.  Comparative Analysis of the Subventricular Zone in Rat, Ferret and Macaque: Evidence for an Outer Subventricular Zone in Rodents , 2012, PloS one.

[16]  A. Kriegstein,et al.  A new subtype of progenitor cell in the mouse embryonic neocortex , 2011, Nature Neuroscience.

[17]  A. Kriegstein,et al.  The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. , 2006, Cerebral cortex.

[18]  Alex T. Kalinka,et al.  Abundant Occurrence of Basal Radial Glia in the Subventricular Zone of Embryonic Neocortex of a Lissencephalic Primate, the Common Marmoset Callithrix jacchus , 2011, Cerebral cortex.

[19]  A. Kriegstein,et al.  Mitotic spindle orientation predicts outer radial glial cell generation in human neocortex , 2013, Nature Communications.

[20]  Y. Gotoh,et al.  Scratch regulates neuronal migration onset via an epithelial-mesenchymal transition–like mechanism , 2013, Nature Neuroscience.

[21]  N. Zečević,et al.  Multiple origins of human neocortical interneurons are supported by distinct expression of transcription factors. , 2011, Cerebral cortex.

[22]  Katrin Amunts,et al.  Development of cortical folding during evolution and ontogeny , 2013, Trends in Neurosciences.

[23]  L. Lum,et al.  Hedgehog Signaling Pathway , 2007, Science's STKE.

[24]  N. Zečević,et al.  Is Pax6 critical for neurogenesis in the human fetal brain? , 2008, Cerebral cortex.

[25]  J. Fish,et al.  OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling , 2010, Nature Neuroscience.

[26]  O. Marín,et al.  Slit/Robo Signaling Modulates the Proliferation of Central Nervous System Progenitors , 2012, Neuron.

[27]  H. Kennedy,et al.  G1 Phase Regulation, Area-Specific Cell Cycle Control, and Cytoarchitectonics in the Primate Cortex , 2005, Neuron.

[28]  Donald M. Bell,et al.  Proneural Transcription Factors Regulate Different Steps of Cortical Neuron Migration through Rnd-Mediated Inhibition of RhoA Signaling , 2011, Neuron.

[29]  Federico Calegari,et al.  Live Imaging at the Onset of Cortical Neurogenesis Reveals Differential Appearance of the Neuronal Phenotype in Apical versus Basal Progenitor Progeny , 2008, PloS one.

[30]  Andrea L. Cirranello,et al.  The Placental Mammal Ancestor and the Post–K-Pg Radiation of Placentals , 2013, Science.

[31]  C. Englund,et al.  Intermediate neuronal progenitors (basal progenitors) produce pyramidal-projection neurons for all layers of cerebral cortex. , 2009, Cerebral cortex.

[32]  P. Arlotta,et al.  A Radial Glia-Specific Role of RhoA in Double Cortex Formation , 2012, Neuron.

[33]  Martin Kircher,et al.  Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal , 2012, Proceedings of the National Academy of Sciences.

[34]  M. Götz,et al.  Prospective isolation of functionally distinct radial glial subtypes—Lineage and transcriptome analysis , 2008, Molecular and Cellular Neuroscience.

[35]  O. Klezovitch,et al.  αE-Catenin Controls Cerebral Cortical Size by Regulating the Hedgehog Signaling Pathway , 2006, Science.

[36]  S. Juliano,et al.  Fine-tuning of neurogenesis is essential for the evolutionary expansion of the cerebral cortex. , 2015, Cerebral cortex.

[37]  A. Kriegstein,et al.  Neurogenic radial glia in the outer subventricular zone of human neocortex , 2010, Nature.

[38]  Henry Kennedy,et al.  Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. , 2002, Cerebral cortex.

[39]  A. Kriegstein,et al.  Development and Evolution of the Human Neocortex , 2011, Cell.

[40]  M. A. García-Cabezas,et al.  A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. , 2011, Cerebral cortex.

[41]  J. Kleinman,et al.  Spatiotemporal transcriptome of the human brain , 2011, Nature.

[42]  B. Finlay,et al.  Linked regularities in the development and evolution of mammalian brains. , 1995, Science.

[43]  Z. Molnár,et al.  Compartmentalization of cerebral cortical germinal zones in a lissencephalic primate and gyrencephalic rodent. , 2012, Cerebral cortex.

[44]  Xavier Morin,et al.  Control of planar divisions by the G-protein regulator LGN maintains progenitors in the chick neuroepithelium , 2007, Nature Neuroscience.

[45]  P. Rakic,et al.  The role of cell death in regulating the size and shape of the mammalian forebrain. , 1999, Cerebral cortex.

[46]  G. Clowry,et al.  A Molecular Neuroanatomical Study of the Developing Human Neocortex from 8 to 17 Postconceptional Weeks Revealing the Early Differentiation of the Subplate and Subventricular Zone , 2007, Cerebral cortex.

[47]  J. Clarke,et al.  Neurons derive from the more apical daughter in asymmetric divisions in the zebrafish neural tube , 2010, Nature Neuroscience.

[48]  H. Kennedy,et al.  Modulation of the cell cycle contributes to the parcellation of the primate visual cortex , 1993, Nature.

[49]  A. Kriegstein,et al.  Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion , 2006, Nature Reviews Neuroscience.

[50]  H. Kennedy,et al.  Making bigger brains–the evolution of neural-progenitor-cell division , 2008, Journal of Cell Science.

[51]  Allan R. Jones,et al.  Transcriptional Architecture of the Primate Neocortex , 2012, Neuron.

[52]  H. Clevers,et al.  Amplification of progenitors in the mammalian telencephalon includes a new radial glial cell type , 2013, Nature Communications.