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Neurogenic radial glia in the outer subventricular zone of human neocortex

Author

Listed:
  • David V. Hansen

    (Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research,
    Department of Neurology,)

  • Jan H. Lui

    (Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research,
    Department of Neurology,
    Biomedical Sciences Graduate Program,)

  • Philip R. L. Parker

    (Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research,
    Department of Neurology,
    Neuroscience Graduate Program, University of California San Francisco, 513 Parnassus Avenue, San Francisco, California 94143, USA)

  • Arnold R. Kriegstein

    (Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research,
    Department of Neurology,)

Abstract

Neurons in the developing rodent cortex are generated from radial glial cells that function as neural stem cells. These epithelial cells line the cerebral ventricles and generate intermediate progenitor cells that migrate into the subventricular zone (SVZ) and proliferate to increase neuronal number. The developing human SVZ has a massively expanded outer region (OSVZ) thought to contribute to cortical size and complexity. However, OSVZ progenitor cell types and their contribution to neurogenesis are not well understood. Here we show that large numbers of radial glia-like cells and intermediate progenitor cells populate the human OSVZ. We find that OSVZ radial glia-like cells have a long basal process but, surprisingly, are non-epithelial as they lack contact with the ventricular surface. Using real-time imaging and clonal analysis, we demonstrate that these cells can undergo proliferative divisions and self-renewing asymmetric divisions to generate neuronal progenitor cells that can proliferate further. We also show that inhibition of Notch signalling in OSVZ progenitor cells induces their neuronal differentiation. The establishment of non-ventricular radial glia-like cells may have been a critical evolutionary advance underlying increased cortical size and complexity in the human brain.

Suggested Citation

  • David V. Hansen & Jan H. Lui & Philip R. L. Parker & Arnold R. Kriegstein, 2010. "Neurogenic radial glia in the outer subventricular zone of human neocortex," Nature, Nature, vol. 464(7288), pages 554-561, March.
    • Handle: RePEc:nat:nature:v:464:y:2010:i:7288:d:10.1038_nature08845
    DOI: 10.1038/nature08845
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    Cited by:

    1. Annalisa Paolino & Elizabeth H. Haines & Evan J. Bailey & Dylan A. Black & Ching Moey & Fernando García-Moreno & Linda J. Richards & Rodrigo Suárez & Laura R. Fenlon, 2023. "Non-uniform temporal scaling of developmental processes in the mammalian cortex," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Christina Kyrousi & Adam C. O’Neill & Agnieska Brazovskaja & Zhisong He & Pavel Kielkowski & Laure Coquand & Rossella Giaimo & Pierpaolo D’ Andrea & Alexander Belka & Andrea Forero Echeverry & Davide , 2021. "Extracellular LGALS3BP regulates neural progenitor position and relates to human cortical complexity," Nature Communications, Nature, vol. 12(1), pages 1-22, December.
    3. G. Ball & S. Oldham & V. Kyriakopoulou & L. Z. J. Williams & V. Karolis & A. Price & J. Hutter & M. L. Seal & A. Alexander-Bloch & J. V. Hajnal & A. D. Edwards & E. C. Robinson & J. Seidlitz, 2024. "Molecular signatures of cortical expansion in the human foetal brain," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    4. Delfina M. Romero & Karine Poirier & Richard Belvindrah & Imane Moutkine & Anne Houllier & Anne-Gaëlle LeMoing & Florence Petit & Anne Boland & Stephan C. Collins & Mariano Soiza-Reilly & Binnaz Yalci, 2022. "Novel role of the synaptic scaffold protein Dlgap4 in ventricular surface integrity and neuronal migration during cortical development," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    5. Norman L. Lehman & Nathalie Spassky & Müge Sak & Amy Webb & Cory T. Zumbar & Aisulu Usubalieva & Khaled J. Alkhateeb & Joseph P. McElroy & Kirsteen H. Maclean & Paolo Fadda & Tom Liu & Vineela Gangala, 2022. "Astroblastomas exhibit radial glia stem cell lineages and differential expression of imprinted and X-inactivation escape genes," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    6. Soraia Barão & Yijun Xu & José P. Llongueras & Rachel Vistein & Loyal Goff & Kristina J. Nielsen & Byoung-Il Bae & Richard S. Smith & Christopher A. Walsh & Genevieve Stein-O’Brien & Ulrich Müller, 2024. "Conserved transcriptional regulation by BRN1 and BRN2 in neocortical progenitors drives mammalian neural specification and neocortical expansion," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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