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Cited by 27Neurogenesis and neuroplasticity mechanismsDevelopmental Biology and Gene RegulationFetal and Pediatric Neurological Disorders

Progenitor-Based Cell Biological Aspects of Neocortex Development and Evolution

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Vaid, Samir, Huttner, Wieland B.·2022·Frontiers in Cell and Developmental Biology
DOI 10.3389/fcell.2022.892922PMC PMC9119302
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Abstract

During development, the decision of stem and progenitor cells to switch from proliferation to differentiation is of critical importance for the overall size of an organ. Too early a switch will deplete the stem/progenitor cell pool, and too late a switch will not generate the required differentiated cell types. With a focus on the developing neocortex, a six-layered structure constituting the major part of the cerebral cortex in mammals, we discuss here the cell biological features that are crucial to ensure the appropriate proliferation vs. differentiation decision in the neural progenitor cells. In the last two decades, the neural progenitor cells giving rise to the diverse types of neurons that function in the neocortex have been intensely investigated for their role in cortical expansion and gyrification. In this review, we will first describe these different progenitor types and their diversity. We will then review the various cell biological features associated with the cell fate decisions of these progenitor cells, with emphasis on the role of the radial processes emanating from these progenitor cells. We will also discuss the species-specific differences in these cell biological features that have allowed for the evolutionary expansion of the neocortex in humans. Finally, we will discuss the emerging role of cell cycle parameters in neocortical expansion.

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  • Differences in cortical development between mice and humans limit the ability of mouse models to define mechanisms relevant to the human DS phenotype.

    “The field has typically relied on mouse models to gain understanding of the impact of T21, but differences in cortical development between mice and humans — including the complexity of progenitor types or the formation of a lissencephalic rather than gyrencephalic brain153–155 — limit their ability to define mechanisms relevant to the human phenotype.”

    From Consequences of trisomy 21 for brain development in Down syndrome (2024) · cites this paper as [153]

    Section 2 (page unavailable) describes the mouse neocortex as lissencephalic and reports differences in progenitor populations between mice and species with expanded neocortices. The paper does not address Down syndrome or state that these differences limit mouse models’ ability to define mechanisms of the human DS phenotype. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

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References 121 · Cited by 27

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  1. Aaku-Saraste E. Hellwig A. Huttner W. B. (1996). Loss of Occludin and Functional Tight Junctions, but not ZO-1, during Neural Tube Closure-Remodeling of the Neuroepithelium Prior to Neurogenesis. Develop. Biol. 180, 664– 679. 10.1006/dbio.1996.0336 8954735 · DOI
  2. Adams R. J. (1996). Metaphase Spindles Rotate in the Neuroepithelium of Rat Cerebral Cortex. J. Neurosci. 16, 7610– 7618. 10.1523/jneurosci.16-23-07610.1996 8922417 PMC6579107 · DOI
  3. Anderson C. T. Stearns T. (2009). Centriole Age Underlies Asynchronous Primary Cilium Growth in Mammalian Cells. Curr. Biol. 19, 1498– 1502. 10.1016/j.cub.2009.07.034 19682908 PMC3312602 · DOI
  4. Arai Y. Pulvers J. N. Haffner C. Schilling B. Nüsslein I. Calegari F. (2011). Neural Stem and Progenitor Cells Shorten S-phase on Commitment to Neuron Production. Nat. Commun. 2, 154. 10.1038/ncomms1155 21224845 PMC3105305 · DOI
  5. Asami M. Pilz G. A. Ninkovic J. Godinho L. Schroeder T. Huttner W. B. (2011). The Role of Pax6 in Regulating the Orientation and Mode of Cell Division of Progenitors in the Mouse Cerebral Cortex. Development 138, 5067– 5078. 10.1242/dev.074591 22031545 · DOI
  6. Bandler R. C. Vitali I. Delgado R. N. Ho M. C. Dvoretskova E. Ibarra Molinas J. S. (2022). Single-Cell Delineation of Lineage and Genetic Identity in the Mouse Brain. Nature 601, 404– 409. 10.1038/s41586-021-04237-0 34912118 PMC8770128 · DOI
  7. Betizeau M. Cortay V. Patti D. Pfister S. Gautier E. Bellemin-Ménard A. (2013). Precursor Diversity and Complexity of Lineage Relationships in the Outer Subventricular Zone of the Primate. Neuron 80, 442– 457. 10.1016/j.neuron.2013.09.032 24139044 · DOI · Paper page
  8. Borrell V. Reillo I. (2012). Emerging Roles of Neural Stem Cells in Cerebral Cortex Development and Evolution. Devel. Neurobiol. 72, 955– 971. 10.1002/dneu.22013 22684946 · DOI · Paper page
  9. Breslow D. K. Holland A. J. (2019). Mechanism and Regulation of Centriole and Cilium Biogenesis. Annu. Rev. Biochem. 88, 691– 724. 10.1146/annurev-biochem-013118-111153 30601682 PMC6588485 · DOI
  10. Bultje R. S. Castaneda-Castellanos D. R. Jan L. Y. Jan Y.-N. Kriegstein A. R. Shi S.-H. (2009). Mammalian Par3 Regulates Progenitor Cell Asymmetric Division via Notch Signaling in the Developing Neocortex. Neuron 63, 189– 202. 10.1016/j.neuron.2009.07.004 19640478 PMC2736606 · DOI
  11. Calegari F. Huttner W. B. (2003). An Inhibition of Cyclin-dependent Kinases that Lengthens, but Does not Arrest, Neuroepithelial Cell Cycle Induces Premature Neurogenesis. J. Cel Sci. 116, 4947– 4955. 10.1242/jcs.00825 14625388 · DOI
  12. Camargo Ortega G. Falk S. Johansson P. A. Peyre E. Broix L. Sahu S. K. (2019). The Centrosome Protein Akna Regulates Neurogenesis via Microtubule Organization. Nature 567, 113– 117. 10.1038/s41586-019-0962-4 30787442 · DOI
  13. Cappello S. Attardo A. Wu X. Iwasato T. Itohara S. Wilsch-Bräuninger M. (2006). The Rho-GTPase Cdc42 Regulates Neural Progenitor Fate at the Apical Surface. Nat. Neurosci. 9, 1099– 1107. 10.1038/nn1744 16892058 · DOI
  14. Cappello S. Böhringer C. R. J. Bergami M. Conzelmann K.-K. Ghanem A. Tomassy G. S. (2012). A Radial Glia-specific Role of Rhoa in Double Cortex Formation. Neuron 73, 911– 924. 10.1016/j.neuron.2011.12.030 22405202 · DOI
  15. Carminati M. Gallini S. Pirovano L. Alfieri A. Bisi S. Mapelli M. (2016). Concomitant Binding of Afadin to LGN and F-Actin Directs Planar Spindle Orientation. Nat. Struct. Mol. Biol. 23, 155– 163. 10.1038/nsmb.3152 26751642 · DOI
  16. Chenn A. Walsh C. A. (2002). Regulation of Cerebral Cortical Size by Control of Cell Cycle Exit in Neural Precursors. Science 297, 365– 369. 10.1126/science.1074192 12130776 · DOI · Paper page
  17. Corbit K. C. Aanstad P. Singla V. Norman A. R. Stainier D. Y. R. Reiter J. F. (2005). Vertebrate Smoothened Functions at the Primary Cilium. Nature 437, 1018– 1021. 10.1038/nature04117 16136078 · DOI · Paper page
  18. Costa M. R. 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. 10.1242/dev.009951 18032449 · DOI
  19. Das R. M. Storey K. G. (2014). Apical Abscission Alters Cell Polarity and Dismantles the Primary Cilium during Neurogenesis. Science 343, 200– 204. 10.1126/science.1247521 24408437 PMC4066580 · DOI · Paper page
  20. Del Bene F. Wehman A. M. Link B. A. Baier H. (2008). Regulation of Neurogenesis by Interkinetic Nuclear Migration through an Apical-Basal Notch Gradient. Cell 134, 1055– 1065. 10.1016/j.cell.2008.07.017 18805097 PMC2628487 · DOI
  21. Eggenschwiler J. T. Anderson K. V. (2007). Cilia and Developmental Signaling. Annu. Rev. Cel Dev. Biol. 23, 345– 373. 10.1146/annurev.cellbio.23.090506.123249 PMC2094042 17506691 · DOI
  22. Erickson A. C. Couchman J. R. (2000). Still More Complexity in Mammalian Basement Membranes. J. Histochem. Cytochem. 48, 1291– 1306. 10.1177/002215540004801001 10990484 · DOI
  23. Farkas L. M. Haffner C. Giger T. Khaitovich P. Nowick K. Birchmeier C. (2008). Insulinoma-Associated 1 has A Panneurogenic Role and Promotes the Generation and Expansion of Basal Progenitors in the Developing Mouse Neocortex. Neuron 60, 40– 55. 10.1016/j.neuron.2008.09.020 18940587 · DOI
  24. Feng Y. Walsh C. A. (2004). Mitotic Spindle Regulation by Nde1 Controls Cerebral Cortical Size. Neuron 44, 279– 293. 10.1016/j.neuron.2004.09.023 15473967 · DOI
  25. Fietz S. A. Kelava I. Vogt J. Wilsch-Bräuninger M. Stenzel D. Fish J. L. (2010). Osvz Progenitors of Human and Ferret Neocortex are Epithelial-like and Expand by Integrin Signaling. Nat. Neurosci. 13, 690– 699. 10.1038/nn.2553 20436478 · DOI · Paper page
  26. Fish J. L. Kosodo Y. Enard W. Pääbo S. Huttner W. B. (2006). Aspm Specifically Maintains Symmetric Proliferative Divisions of Neuroepithelial Cells. Proc. Natl. Acad. Sci. U.S.A. 103, 10438– 10443. 10.1073/pnas.0604066103 16798874 PMC1502476 · DOI · Paper page
  27. Frise E. Knoblich J. A. Younger-Shepherd S. Jan L. Y. Jan Y. N. (1996). The Drosophila Numb Protein Inhibits Signaling of the Notch Receptor during Cell-Cell Interaction in Sensory Organ Lineage. Proc. Natl. Acad. Sci. U.S.A. 93, 11925– 11932. 10.1073/pnas.93.21.11925 8876239 PMC38160 · DOI
  28. Gal J. S. Morozov Y. M. Ayoub A. E. Chatterjee M. Rakic P. Haydar T. F. (2006). Molecular and Morphological Heterogeneity of Neural Precursors in the Mouse Neocortical Proliferative Zones. J. Neurosci. 26, 1045– 1056. 10.1523/jneurosci.4499-05.2006 16421324 PMC3249619 · DOI
  29. Garcez P. P. Diaz-Alonso J. Crespo-Enriquez I. Castro D. Bell D. Guillemot F. (2015). Cenpj/CPAP Regulates Progenitor Divisions and Neuronal Migration in the Cerebral Cortex Downstream of Ascl1. Nat. Commun. 6, 6474. 10.1038/ncomms7474 25753651 PMC4366522 · DOI
  30. Gauthier-Fisher A. Lin D. C. Greeve M. Kaplan D. R. Rottapel R. Miller F. D. (2009). Lfc and Tctex-1 Regulate the Genesis of Neurons from Cortical Precursor Cells. Nat. Neurosci. 12, 735– 744. 10.1038/nn.2339 19448628 · DOI
  31. Gerdes J. M. Katsanis N. (2008). Chapter 7 Ciliary Function and Wnt Signal Modulation. Curr. Top. Dev. Biol. 85, 175– 195. 10.1016/s0070-2153(08)00807-7 19147006 · DOI
  32. Gertz C. C. Lui J. H. Lamonica B. E. Wang X. Kriegstein A. R. (2014). Diverse Behaviors of Outer Radial Glia in Developing Ferret and Human Cortex. J. Neurosci. 34, 2559– 2570. 10.1523/jneurosci.2645-13.2014 24523546 PMC3921426 · DOI
  33. Gil-Sanz C. Landeira B. Ramos C. Costa M. R. Muller U. (2014). Proliferative Defects and Formation of a Double Cortex in Mice Lacking Mltt4 and Cdh2 in the Dorsal Telencephalon. J. Neurosci. 34, 10475– 10487. 10.1523/jneurosci.1793-14.2014 25100583 PMC4200106 · DOI
  34. Goetz S. C. Ocbina P. J. R. Anderson K. V. (2009). The Primary Cilium as A Hedgehog Signal Transduction Machine. Methods Cel Biol. 94, 199– 222. 10.1016/s0091-679x(08)94010-3 PMC2867239 20362092 · DOI
  35. Hatakeyama J. Wakamatsu Y. Nagafuchi A. Kageyama R. Shigemoto R. Shimamura K. (2014). Cadherin-Based Adhesions in the Apical Endfoot are Required for Active Notch Signaling to Control Neurogenesis in Vertebrates. Development 141, 1671– 1682. 10.1242/dev.102988 24715457 · DOI
  36. Haubensak W. Attardo A. Denk W. Huttner W. B. (2004). Neurons Arise in the Basal Neuroepithelium of the Early Mammalian Telencephalon: A Major Site of Neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 101, 3196– 3201. 10.1073/pnas.0308600100 14963232 PMC365766 · DOI
  37. 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– 3254. 10.1242/dev.02486 16873583 · DOI
  38. Haydar T. F. Ang E. Jr. Rakic P. (2003). Mitotic Spindle Rotation and Mode of Cell Division in the Developing Telencephalon. Proc. Natl. Acad. Sci. U.S.A. 100, 2890– 2895. 10.1073/pnas.0437969100 12589023 PMC151436 · DOI
  39. Itoh M. Nagafuchi A. Yonemura S. Kitani-Yasuda T. Tsukita S. Tsukita S. (1993). The 220-kD Protein Colocalizing with Cadherins in Non-epithelial Cells Is Identical to ZO-1, a Tight junction-associated Protein in Epithelial Cells: cDNA Cloning and Immunoelectron Microscopy. J. Cel Biol. 121, 491– 502. 10.1083/jcb.121.3.491 PMC2119563 8486731 · DOI
  40. Itoh Y. Moriyama Y. Hasegawa T. Endo T. A. Toyoda T. Gotoh Y. (2013). Scratch Regulates Neuronal Migration Onset via an Epithelial-Mesenchymal Transition-like Mechanism. Nat. Neurosci. 16, 416– 425. 10.1038/nn.3336 23434913 · DOI
  41. Jeong S. J. Luo R. Singer K. Giera S. Kreidberg J. Kiyozumi D. (2013). GPR56 Functions Together with α3β1 Integrin in Regulating Cerebral Cortical Development. Plos One 8, E68781. 10.1371/journal.pone.0068781 23874761 PMC3706371 · DOI
  42. Jossin Y. Lee M. Klezovitch O. Kon E. Cossard A. Lien W.-H. (2017). Llgl1 Connects Cell Polarity with Cell-Cell Adhesion in Embryonic Neural Stem Cells. Develop. Cel 41, 481– 495. 10.1016/j.devcel.2017.05.002 PMC5519327 28552558 · DOI
  43. Kadowaki M. Nakamura S. Machon O. Krauss S. Radice G. L. Takeichi M. (2007). N-cadherin Mediates Cortical Organization in the Mouse Brain. Develop. Biol. 304, 22– 33. 10.1016/j.ydbio.2006.12.014 17222817 · DOI
  44. Kalebic N. Huttner W. B. (2020). Basal Progenitor Morphology and Neocortex Evolution. Trends Neurosci. 43, 843– 853. 10.1016/j.tins.2020.07.009 32828546 · DOI
  45. Kalebic N. Gilardi C. Stepien B. Wilsch-Bräuninger M. Long K. R. Namba T. (2019). Neocortical Expansion Due to Increased Proliferation of Basal Progenitors Is Linked to Changes in Their Morphology. Cell Stem Cell 24, 535– 550. 10.1016/j.stem.2019.02.017 30905618 · DOI
  46. Katayama K.-i. Melendez J. Baumann J. M. Leslie J. R. Chauhan B. K. Nemkul N. (2011). Loss of Rhoa in Neural Progenitor Cells Causes the Disruption of Adherens Junctions and Hyperproliferation. Proc. Natl. Acad. Sci. U.S.A. 108, 7607– 7612. 10.1073/pnas.1101347108 21502507 PMC3088619 · DOI
  47. Kawaue T. Shitamukai A. Nagasaka A. Tsunekawa Y. Shinoda T. Saito K. (2019). Lzts1 Controls Both Neuronal Delamination and Outer Radial Glial-like Cell Generation during Mammalian Cerebral Development. Nat. Commun. 10, 2780. 10.1038/s41467-019-10730-y 31239441 PMC6592889 · DOI
  48. Kazanis I. Ffrench-Constant C. (2011). Extracellular Matrix and the Neural Stem Cell Niche. Devel Neurobiol. 71, 1006– 1017. 10.1002/dneu.20970 21898854 PMC4557210 · DOI
  49. Kelava I. Reillo I. Murayama A. Y. Kalinka A. T. Stenzel D. Tomancak P. (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– 481. 10.1093/cercor/bhr301 22114084 PMC3256412 · DOI
  50. Kim S. Lehtinen M. K. Sessa A. Zappaterra M. W. Cho S.-H. Gonzalez D. (2010). The Apical Complex Couples Cell Fate and Cell Survival to Cerebral Cortical Development. Neuron 66, 69– 84. 10.1016/j.neuron.2010.03.019 20399730 PMC2872122 · DOI
  51. Kobayashi T. Kim S. Lin Y.-C. Inoue T. Dynlacht B. D. (2014). The Cp110-Interacting Proteins Talpid3 and Cep290 Play Overlapping and Distinct Roles in Cilia Assembly. J. Cel Biol. 204, 215– 229. 10.1083/jcb.201304153 PMC3897186 24421332 · DOI
  52. Konno D. Shioi G. Shitamukai A. Mori A. Kiyonari H. Miyata T. (2008). Neuroepithelial Progenitors Undergo LGN-dependent Planar Divisions to Maintain Self-Renewability during Mammalian Neurogenesis. Nat. Cel Biol. 10, 93– 101. 10.1038/ncb1673 18084280 · DOI
  53. Kosodo Y. Röper K. Haubensak W. Marzesco A.-M. Corbeil D. Huttner W. B. (2004). Asymmetric Distribution of the Apical Plasma Membrane during Neurogenic Divisions of Mammalian Neuroepithelial Cells. Embo J. 23, 2314– 2324. 10.1038/sj.emboj.7600223 15141162 PMC419905 · DOI
  54. Kosodo Y. Toida K. Dubreuil V. Alexandre P. Schenk J. Kiyokage E. (2008). Cytokinesis of Neuroepithelial Cells Can Divide Their Basal Process before Anaphase. Embo J. 27, 3151– 3163. 10.1038/emboj.2008.227 18971946 PMC2599871 · DOI
  55. Kumar D. Reiter J. (2021). How the Centriole Builds its Cilium: Of Mothers, Daughters, and the Acquisition of Appendages. Curr. Opin. Struct. Biol. 66, 41– 48. 10.1016/j.sbi.2020.09.006 33160100 · DOI
  56. Lamonica B. E. Lui J. H. Hansen D. V. Kriegstein A. R. (2013). Mitotic Spindle Orientation Predicts Outer Radial Glial Cell Generation in Human Neocortex. Nat. Commun. 4, 1665. 10.1038/ncomms2647 23575669 PMC3625970 · DOI
  57. Lange C. Huttner W. B. 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– 331. 10.1016/j.stem.2009.05.026 19733543 · DOI
  58. Lehtinen M. K. Walsh C. A. (2011). Neurogenesis at the Brain-Cerebrospinal Fluid Interface. Annu. Rev. Cel Dev. Biol. 27, 653– 679. 10.1146/annurev-cellbio-092910-154026 PMC3777264 21801012 · DOI
  59. Lewitus E. Kelava I. Huttner W. B. (2013). Conical Expansion of the Outer Subventricular Zone and the Role of Neocortical Folding in Evolution and Development. Front. Hum. Neurosci. 7, 424. 10.3389/fnhum.2013.00424 23914167 PMC3729979 · DOI
  60. Lien W.-H. Klezovitch O. Fernandez T. E. Delrow J. Vasioukhin V. (2006). Αe-Catenin Controls Cerebral Cortical Size by Regulating the Hedgehog Signaling Pathway. Science 311, 1609– 1612. 10.1126/science.1121449 16543460 PMC2556178 · DOI
  61. Louvi A. Grove E. A. (2011). Cilia in the Cns: The Quiet Organelle Claims Center Stage. Neuron 69, 1046– 1060. 10.1016/j.neuron.2011.03.002 21435552 PMC3070490 · DOI
  62. Lukaszewicz A. Savatier P. Cortay V. Giroud P. Huissoud C. Berland M. (2005). G1 Phase Regulation, Area-specific Cell Cycle Control, and Cytoarchitectonics in the Primate Cortex. Neuron 47, 353– 364. 10.1016/j.neuron.2005.06.032 16055060 PMC1890568 · DOI · Paper page
  63. Machon O. Van Den Bout C. J. Backman M. Kemler R. Krauss S. (2003). Role of β-catenin in the Developing Cortical and Hippocampal Neuroepithelium. Neuroscience 122, 129– 143. 10.1016/s0306-4522(03)00519-0 14596855 · DOI
  64. Manabe N. Hirai S.-I. Imai F. Nakanishi H. Takai Y. Ohno S. (2002). Association of ASIP/mPAR-3 with Adherens Junctions of Mouse Neuroepithelial Cells. Dev. Dyn. 225, 61– 69. 10.1002/dvdy.10139 12203721 · DOI
  65. Martínez-Martínez M. Á. De Juan Romero C. Fernández V. Cárdenas A. Götz M. Borrell V. (2016). A Restricted Period for Formation of Outer Subventricular Zone Defined by Cdh1 and Trnp1 Levels. Nat. Commun. 7, 11812. 10.1038/ncomms11812 27264089 PMC4897765 · DOI
  66. Miyata T. Kawaguchi A. Okano H. Ogawa M. (2001). Asymmetric Inheritance of Radial Glial Fibers by Cortical Neurons. Neuron 31, 727– 741. 10.1016/s0896-6273(01)00420-2 11567613 · DOI
  67. 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– 3145. 10.1242/dev.01173 15175243 · DOI
  68. Mora-Bermudez F. Matsuzaki F. Huttner W. B. (2014). Specific Polar Subpopulations of Astral Microtubules Control Spindle Orientation and Symmetric Neural Stem Cell Division. Elife 3, e02875. 10.7554/elife.02875 PMC4112548 24996848 · DOI
  69. Mora-Bermúdez F. Badsha F. Kanton S. Camp J. G. Vernot B. Köhler K. (2016). Differences and Similarities between Human and Chimpanzee Neural Progenitors during Cerebral Cortex Development. Elife 5, e18683. 10.7554/eLife.18683 27669147 PMC5110243 · DOI
  70. Noctor S. C. Flint A. C. Weissman T. A. Dammerman R. S. Kriegstein A. R. (2001). Neurons Derived from Radial Glial Cells Establish Radial Units in Neocortex. Nature 409, 714– 720. 10.1038/35055553 11217860 · DOI · Paper page
  71. Noctor S. C. Martínez-Cerdeño V. Ivic L. Kriegstein A. R. (2004). Cortical Neurons Arise in Symmetric and Asymmetric Division Zones and Migrate through Specific Phases. Nat. Neurosci. 7, 136– 144. 10.1038/nn1172 14703572 · DOI · Paper page
  72. Noctor S. C. Martínez-Cerdeño V. Kriegstein A. R. (2008). Distinct Behaviors of Neural Stem and Progenitor Cells Underlie Cortical Neurogenesis. J. Comp. Neurol. 508, 28– 44. 10.1002/cne.21669 18288691 PMC2635107 · DOI
  73. Nowakowski T. J. Pollen A. A. Sandoval-Espinosa C. Kriegstein A. R. (2016). Transformation of the Radial Glia Scaffold Demarcates Two Stages of Human Cerebral Cortex Development. Neuron 91, 1219– 1227. 10.1016/j.neuron.2016.09.005 27657449 PMC5087333 · DOI
  74. Ohata S. Aoki R. Kinoshita S. Yamaguchi M. Tsuruoka-Kinoshita S. Tanaka H. (2011). Dual Roles of Notch in Regulation of Apically Restricted Mitosis and Apicobasal Polarity of Neuroepithelial Cells. Neuron 69, 215– 230. 10.1016/j.neuron.2010.12.026 21262462 · DOI
  75. O'leary C. J. Nourse C. C. Lee N. K. White A. Langford M. Sempert K. (2017). Neogenin Recruitment of the Wave Regulatory Complex to Ependymal and Radial Progenitor Adherens Junctions Prevents Hydrocephalus. Cell Rep. 20, 370– 383. 10.1016/j.celrep.2017.06.051 28700939 · DOI
  76. Ostrem B. E. L. Lui J. H. Gertz C. C. Kriegstein A. R. (2014). Control of Outer Radial Glial Stem Cell Mitosis in the Human Brain. Cel Rep. 8, 656– 664. 10.1016/j.celrep.2014.06.058 PMC4127493 25088420 · DOI
  77. Paridaen J. T. M. L. Wilsch-Bräuninger M. Huttner W. B. (2013). Asymmetric Inheritance of Centrosome-Associated Primary Cilium Membrane Directs Ciliogenesis after Cell Division. Cell 155, 333– 344. 10.1016/j.cell.2013.08.060 24120134 · DOI
  78. Pilaz L.-J. Lennox A. L. Rouanet J. P. Silver D. L. (2016). Dynamic Mrna Transport and Local Translation in Radial Glial Progenitors of the Developing Brain. Curr. Biol. 26, 3383– 3392. 10.1016/j.cub.2016.10.040 27916527 PMC5203927 · DOI
  79. Pilz G.-A. Shitamukai A. Reillo I. Pacary E. Schwausch J. Stahl R. (2013). Amplification of Progenitors in the Mammalian Telencephalon Includes a New Radial Glial Cell Type. Nat. Commun. 4, 2125. 10.1038/ncomms3125 23839311 PMC3717501 · DOI
  80. Piotrowska-Nitsche K. Caspary T. (2012). Live Imaging of Individual Cell Divisions in Mouse Neuroepithelium Shows Asymmetry in Cilium Formation and Sonic Hedgehog Response. Cilia 1, 6. 10.1186/2046-2530-1-6 23145349 PMC3491994 · DOI
  81. Rakic P. (1972). Mode of Cell Migration to the Superficial Layers of Fetal Monkey Neocortex. J. Comp. Neurol. 145, 61– 83. 10.1002/cne.901450105 4624784 · DOI · Paper page
  82. Rakotomamonjy J. Brunner M. Jüschke C. Zang K. Huang E. J. Reichardt L. F. (2017). Afadin Controls Cell Polarization and Mitotic Spindle Orientation in Developing Cortical Radial Glia. Neural Dev. 12, 7. 10.1186/s13064-017-0085-2 28482867 PMC5422985 · DOI
  83. Rasin M. R. Gazula V. R. Breunig J. J. Kwan K. Y. Johnson M. B. Liu-Chen S. (2007). Numb and Numbl are Required for Maintenance of Cadherin-Based Adhesion and Polarity of Neural Progenitors. Nat. Neurosci. 10, 819– 827. 10.1038/nn1924 17589506 · DOI
  84. Reillo I. De Juan Romero C. García-Cabezas M. Á. Borrell V. (2011). A Role for Intermediate Radial Glia in the Tangential Expansion of the Mammalian Cerebral Cortex. Cereb. Cortex 21, 1674– 1694. 10.1093/cercor/bhq238 21127018 · DOI
  85. Rohatgi R. Scott M. P. (2007). Patching the Gaps in Hedgehog Signalling. Nat. Cel Biol. 9, 1005– 1009. 10.1038/ncb435 17762891 · DOI
  86. Ruan X. Kang B. Qi C. Lin W. Wang J. Zhang X. (2021). Progenitor Cell Diversity in the Developing Mouse Neocortex. Proc. Natl. Acad. Sci. U S A 118, e2018866118. 10.1073/pnas.2018866118 33649223 PMC7958455 · DOI
  87. Schmid M.-T. Weinandy F. Wilsch-Bräuninger M. Huttner W. B. Cappello S. Götz M. (2014). The Role of α-E-Catenin in Cerebral Cortex Development: Radial Glia Specific Effect on Neuronal Migration. Front. Cel. Neurosci. 8, 215. 10.3389/fncel.2014.00215 PMC4124588 25147501 · DOI
  88. 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– 3695. 10.1523/jneurosci.4773-10.2011 21389223 PMC6622781 · DOI
  89. Silva C. G. Peyre E. Nguyen L. (2019). Cell Migration Promotes Dynamic Cellular Interactions to Control Cerebral Cortex Morphogenesis. Nat. Rev. Neurosci. 20, 318– 329. 10.1038/s41583-019-0148-y 30874623 · DOI
  90. Singer K. Luo R. Jeong S.-J. Piao X. (2013). Gpr56 and the Developing Cerebral Cortex: Cells, Matrix, and Neuronal Migration. Mol. Neurobiol. 47, 186– 196. 10.1007/s12035-012-8343-0 23001883 PMC3538897 · DOI
  91. Smart I. H. M. 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. 10.1093/cercor/12.1.37 11734531 PMC1931430 · DOI · Paper page
  92. Spana E. P. Doe C. Q. (1996). Numb Antagonizes Notch Signaling to Specify Sibling Neuron Cell Fates. Neuron 17, 21– 26. 10.1016/s0896-6273(00)80277-9 8755475 · DOI
  93. Stahl R. Walcher T. De Juan Romero C. Pilz G. A. Cappello S. Irmler M. (2013). Trnp1 Regulates Expansion and Folding of the Mammalian Cerebral Cortex by Control of Radial Glial Fate. Cell 153, 535– 549. 10.1016/j.cell.2013.03.027 23622239 · DOI
  94. Stocker A. M. Chenn A. (2015). The Role of Adherens Junctions in the Developing Neocortex. Cell Adhes. Migration 9, 167– 174. 10.1080/19336918.2015.1027478 PMC4594481 25914082 · DOI
  95. Subramanian L. Bershteyn M. Paredes M. F. Kriegstein A. R. (2017). Dynamic Behaviour of Human Neuroepithelial Cells in the Developing Forebrain. Nat. Commun. 8, 14167. 10.1038/ncomms14167 28139695 PMC5290330 · DOI
  96. Takekuni K. Ikeda W. Fujito T. Morimoto K. Takeuchi M. Monden M. (2003). Direct Binding of Cell Polarity Protein Par-3 to Cell-Cell Adhesion Molecule Nectin at Neuroepithelial Cells of Developing Mouse. J. Biol. Chem. 278, 5497– 5500. 10.1074/jbc.c200707200 12515806 · DOI
  97. Tavano S. Taverna E. Kalebic N. Haffner C. Namba T. Dahl A. (2018). Insm1 Induces Neural Progenitor Delamination in Developing Neocortex via Downregulation of the Adherens Junction Belt-Specific Protein Plekha7. Neuron 97, 1299– 1314. 10.1016/j.neuron.2018.01.052 29503187 · DOI
  98. Taverna E. Götz M. Huttner W. B. (2014). The Cell Biology of Neurogenesis: Toward an Understanding of the Development and Evolution of the Neocortex. Annu. Rev. Cel Dev. Biol. 30, 465– 502. 10.1146/annurev-cellbio-101011-155801 25000993 · DOI
  99. Telley L. Agirman G. Prados J. Amberg N. Fièvre S. Oberst P. (2019). Temporal Patterning of Apical Progenitors and Their Daughter Neurons in the Developing Neocortex. Science 364. 10.1126/science.aav2522 31073041 · DOI · Paper page
  100. Tischer J. Carden S. Gergely F. (2021). Accessorizing the Centrosome: New Insights into Centriolar Appendages and Satellites. Curr. Opin. Struct. Biol. 66, 148– 155. 10.1016/j.sbi.2020.10.021 33279729 · DOI
  101. Tsunekawa Y. Britto J. M. Takahashi M. Polleux F. Tan S.-S. Osumi N. (2012). Cyclin D2 in the Basal Process of Neural Progenitors is Linked to Non-equivalent Cell Fates. Embo J. 31, 1879– 1892. 10.1038/emboj.2012.43 22395070 PMC3343330 · DOI
  102. Uzquiano A. Gladwyn‐Ng I. Nguyen L. Reiner O. Götz M. Matsuzaki F. (2018). Cortical Progenitor Biology: Key Features Mediating Proliferation versus Differentiation. J. Neurochem. 146, 500– 525. 10.1111/jnc.14338 29570795 · DOI
  103. Vaid S. Huttner W. B. (2020). Transcriptional Regulators and Human-Specific/Primate-specific Genes in Neocortical Neurogenesis. Int. J. Mol. Sci. 21, 4614. 10.3390/ijms21134614 PMC7369782 32610533 · DOI
  104. Vaid S. Camp J. G. Hersemann L. Eugster Oegema C. Heninger A. K. Winkler S (2018). A Novel Population of Hopx-dependent Basal Radial Glial Cells in the Developing Mouse Neocortex. Development 145, dev169276. 10.1242/dev.169276 30266827 · DOI
  105. Veeraval L. O’Leary C. J. Cooper H. M. (2020). Adherens Junctions: Guardians of Cortical Development. Front. Cel Dev. Biol. 8, 6. 10.3389/fcell.2020.00006 PMC7025593 32117958 · DOI
  106. Wade A. Mckinney A. Phillips J. J. (2014). Matrix Regulators in Neural Stem Cell Functions. Biochim. Biophys. Acta Gen. Subjects 1840, 2520– 2525. 10.1016/j.bbagen.2014.01.017 PMC4074566 24447567 · DOI
  107. Wang X. Tsai J.-W. Imai J. H. Lian W.-N. Vallee R. B. Shi S.-H. (2009). Asymmetric Centrosome Inheritance Maintains Neural Progenitors in the Neocortex. Nature 461, 947– 955. 10.1038/nature08435 19829375 PMC2764320 · DOI
  108. Wang J. Li T. Wang J.-L. Xu Z. Meng W. Wu Q.-F. (2020). Talpid3-Mediated Centrosome Integrity Restrains Neural Progenitor Delamination to Sustain Neurogenesis by Stabilizing Adherens Junctions. Cel Rep. 33, 108495. 10.1016/j.celrep.2020.108495 33326788 · DOI
  109. Wilsch-Bräuninger M. Huttner W. B. (2021). Primary Cilia and Centrosomes in Neocortex Development. Front. Neurosci. 15, 755867. 10.3389/fnins.2021.755867 34744618 PMC8566538 · DOI
  110. Wilsch-Bräuninger M. Peters J. Paridaen J. T. Huttner W. B. (2012). Basolateral rather Than Apical Primary Cilia on Neuroepithelial Cells Committed to Delamination. Development 139, 95– 105. 10.1242/dev.069294 22096071 · DOI
  111. Wong F. K. Fei J. F. Mora-Bermúdez F. Taverna E. Haffner C. Fu J. (2015). Sustained Pax6 Expression Generates Primate-like Basal Radial Glia in Developing Mouse Neocortex. Plos Biol. 13, E1002217. 10.1371/journal.pbio.1002217 26252244 PMC4529158 · DOI
  112. Woodhead G. J. Mutch C. A. Olson E. C. Chenn A. (2006). Cell-Autonomous Beta-Catenin Signaling Regulates Cortical Precursor Proliferation. J. Neurosci. 26, 12620– 12630. 10.1523/jneurosci.3180-06.2006 17135424 PMC2867669 · DOI
  113. Yamamoto H. Maruo T. Majima T. Ishizaki H. Tanaka-Okamoto M. Miyoshi J. (2013). Genetic Deletion of Afadin Causes Hydrocephalus by Destruction of Adherens Junctions in Radial Glial and Ependymal Cells in the Midbrain. Plos One 8, E80356. 10.1371/journal.pone.0080356 24236178 PMC3827428 · DOI
  114. Yin Y. Bangs F. Paton I. R. Prescott A. James J. Davey M. G. (2009). The Talpid3 gene (KIAA0586) Encodes a Centrosomal Protein that is Essential for Primary Cilia Formation. Development 136, 655– 664. 10.1242/dev.028464 19144723 PMC2741201 · DOI
  115. Yokota Y. Eom T.-Y. Stanco A. Kim W.-Y. Rao S. Snider W. D. (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– 4110. 10.1242/dev.048637 21062867 PMC2976289 · DOI
  116. Zhang X. Lei K. Yuan X. Wu X. Zhuang Y. Xu T. (2009). SUN1/2 and Syne/Nesprin-1/2 Complexes Connect Centrosome to the Nucleus during Neurogenesis and Neuronal Migration in Mice. Neuron 64, 173– 187. 10.1016/j.neuron.2009.08.018 19874786 PMC2788510 · DOI

Authors
Vaid, S., & Huttner, W. B.
Affiliations
University of Geneva (CH)
Corresponding author
Vaid, Samir
ORCID
Vaid, Samir
Venue
Frontiers in Cell and Developmental Biology
Publisher
Frontiers Media SA
Published
2022-05-02
Volume
10
Pages
892922-892922
ISSN
2296-634X (ISSN-L)
DOI
10.3389/fcell.2022.892922
PMC
PMC9119302
OpenAlex
W4225266567
Cited by
27
References
121
Citations by year
2026: 1 · 2025: 4 · 2024: 9 · 2023: 12 · 2022: 1
FWCI
1.02
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Cell and Developmental Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Topics
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Fetal and Pediatric Neurological Disorders
Keywords
neocortex development, neural progenitor cells, cortical expansion, cortical folding, cell fate determination, species differences, cerebral cortex

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