Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development

  1. Felipe Mora-Bermúdez
  2. Farhath Badsha
  3. Sabina Kanton
  4. J Gray Camp
  5. Benjamin Vernot
  6. Kathrin Köhler
  7. Birger Voigt
  8. Keisuke Okita
  9. Tomislav Maricic
  10. Zhisong He
  11. Robert Lachmann
  12. Svante Pääbo  Is a corresponding author
  13. Barbara Treutlein  Is a corresponding author
  14. Wieland B Huttner  Is a corresponding author
  1. Max Planck Institute of Molecular Cell Biology and Genetics, Germany
  2. Max Planck Institute for Evolutionary Anthropology, Germany
  3. Kyoto University, Japan
  4. CAS-MPG Partner Institute for Computational Biology, China
  5. Technische Universität Dresden, Germany

Abstract

Human neocortex expansion likely contributed to the remarkable cognitive abilities of humans. This expansion is thought to primarily reflect differences in proliferation versus differentiation of neural progenitors during cortical development. Here, we have searched for such differences by analysing cerebral organoids from human and chimpanzees using immunohistochemistry, live imaging, and single-cell transcriptomics. We find that the cytoarchitecture, cell type composition, and neurogenic gene expression programs of humans and chimpanzees are remarkably similar. Notably, however, live imaging of apical progenitor mitosis uncovered a lengthening of prometaphase-metaphase in humans compared to chimpanzees that is specific to proliferating progenitors and not observed in non-neural cells. Consistent with this, the small set of genes more highly expressed in human apical progenitors points to increased proliferative capacity, and the proportion of neurogenic basal progenitors is lower in humans. These subtle differences in cortical progenitors between humans and chimpanzees may have consequences for human neocortex evolution.

Article and author information

Author details

  1. Felipe Mora-Bermúdez

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Farhath Badsha

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

    Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. J Gray Camp

    Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Benjamin Vernot

    Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Kathrin Köhler

    Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Birger Voigt

    Institute of Laboratory Animals, Graduate School of Medicine, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Keisuke Okita

    Department of Reprogramming Science, Center for iPS Cell Research and Application, Kyoto University, Kyoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  9. Tomislav Maricic

    Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Zhisong He

    CAS-MPG Partner Institute for Computational Biology, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  11. Robert Lachmann

    Technische Universität Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  12. Svante Pääbo

    Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
    For correspondence
    paabo@eva.mpg.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
  13. Barbara Treutlein

    Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
    For correspondence
    barbara_treutlein@eva.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
  14. 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

Boehringer Ingelheim Fonds

  • Sabina Kanton

Paul G. Allen Family Foundation

  • Svante Pääbo

Deutsche Forschungsgemeinschaft (DFG, SFB 655, A2)

  • Wieland B Huttner

European Research Council (ERC, 250197)

  • Wieland B Huttner

DFG-Funded Center for Regenerative Therapies Dresden

  • Wieland B Huttner

Fonds der Chemischen Industrie

  • Wieland B Huttner

Max Planck Society

  • Svante Pääbo
  • Barbara Treutlein
  • Wieland B Huttner

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

Ethics

Animal experimentation: Mice were kept pathogen-free at the Biomedical Services Facility of the MPI-CBG. All experiments using mice were performed according to the German Animal Welfare Legislation. In addition, research was approved by the Institutional Review Board of the Max Planck Institute of Molecular Cell Biology and Genetics.

Human subjects: Human fetal brain tissue (11-13 weeks post conception (wpc)) was obtained with informed written maternal consent followed by elective pregnancy termination. Research involving human tissue was approved by the Ethical Review Committee of the Universitaetsklinikum Carl Gustav Carus of the Technische Universitaet Dresden. In addition, research was approved by the Institutional Review Board of the Max Planck Institute of Molecular Cell Biology and Genetics.

Reviewing Editor

  1. Andrea Musacchio, Max Planck Institute of Molecular Physiology, Germany

Publication history

  1. Received: June 9, 2016
  2. Accepted: September 22, 2016
  3. Accepted Manuscript published: September 26, 2016 (version 1)
  4. Accepted Manuscript updated: September 26, 2016 (version 2)
  5. Version of Record published: November 15, 2016 (version 3)

Copyright

© 2016, Mora-Bermúdez 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. Felipe Mora-Bermúdez
  2. Farhath Badsha
  3. Sabina Kanton
  4. J Gray Camp
  5. Benjamin Vernot
  6. Kathrin Köhler
  7. Birger Voigt
  8. Keisuke Okita
  9. Tomislav Maricic
  10. Zhisong He
  11. Robert Lachmann
  12. Svante Pääbo
  13. Barbara Treutlein
  14. Wieland B Huttner
(2016)
Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development
eLife 5:e18683.
https://doi.org/10.7554/eLife.18683
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