Human-specific ARHGAP11B induces hallmarks of neocortical expansion in developing ferret neocortex

  1. Nereo Kalebic
  2. Carlotta Gilardi
  3. Mareike Albert
  4. Takashi Namba
  5. Katherine R Long
  6. Milos Kostic
  7. Barbara Langen
  8. Wieland B Huttner  Is a corresponding author
  1. Max Planck Institute of Molecular Cell Biology and Genetics, Germany

Abstract

The evolutionary increase in size and complexity of the primate neocortex is thought to underlie the higher cognitive abilities of humans. ARHGAP11B is a human-specific gene that, based on its expression pattern in fetal human neocortex and progenitor effects in embryonic mouse neocortex, has been proposed to have a key function in the evolutionary expansion of the neocortex. Here, we study the effects of ARHGAP11B expression in the developing neocortex of the gyrencephalic ferret. In contrast to its effects in mouse, ARHGAP11B markedly increases proliferative basal radial glia, a progenitor cell type thought to be instrumental for neocortical expansion, and results in extension of the neurogenic period and an increase in upper-layer neurons. Consequently, the postnatal ferret neocortex exhibits increased neuron density in the upper cortical layers and expands in both the radial and tangential dimensions. Thus, human-specific ARHGAP11B can elicit hallmarks of neocortical expansion in the developing ferret neocortex.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Nereo Kalebic

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8445-2906
  2. Carlotta Gilardi

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Mareike Albert

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9855-9344
  4. Takashi Namba

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Katherine R Long

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0660-2486
  6. Milos Kostic

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Barbara Langen

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Wieland B Huttner

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    For correspondence
    huttner@mpi-cbg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4143-7201

Funding

European Molecular Biology Organization (ALTF 861-2013)

  • Nereo Kalebic

Deutsche Forschungsgemeinschaft (SFB 655 A2)

  • Wieland B Huttner

European Research Council (250197)

  • Wieland B Huttner

Max-Planck-Gesellschaft

  • Wieland B Huttner

Christiane-Nüsslein-Volhard Foundation

  • Mareike Albert

Erasmus+ traineeship program

  • Carlotta Gilardi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experimental procedures were conducted in agreement with the German Animal Welfare Legislation after approval by the Landesdirektion Sachsen (licences TVV 2/2015 and TVV 21/2017).

Reviewing Editor

  1. Paola Arlotta, Harvard University, United States

Publication history

  1. Received: August 19, 2018
  2. Accepted: November 23, 2018
  3. Accepted Manuscript published: November 28, 2018 (version 1)
  4. Version of Record published: December 21, 2018 (version 2)

Copyright

© 2018, Kalebic et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Nereo Kalebic
  2. Carlotta Gilardi
  3. Mareike Albert
  4. Takashi Namba
  5. Katherine R Long
  6. Milos Kostic
  7. Barbara Langen
  8. Wieland B Huttner
(2018)
Human-specific ARHGAP11B induces hallmarks of neocortical expansion in developing ferret neocortex
eLife 7:e41241.
https://doi.org/10.7554/eLife.41241

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