1. Developmental Biology
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Segmentation of the zebrafish axial skeleton relies on notochord sheath cells and not on the segmentation clock

  1. Laura LLeras Forero
  2. Rachna Narayanan
  3. Leonie F A Huitema
  4. Maaike VanBergen
  5. Alexander Apschner
  6. Josi Peterson-Maduro
  7. Ive Logister
  8. Guillaume Valentin
  9. Luis G Morelli
  10. Andrew Oates  Is a corresponding author
  11. Stefan Schulte-Merker  Is a corresponding author
  1. University of Münster, Germany
  2. The Francis Crick Institute, United Kingdom
  3. Hubrecht Institute, Netherlands
  4. University College London, United Kingdom
  5. Instituto de Investigación en Biomedicina de Buenos Aires, Argentina
Research Article
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Cite this article as: eLife 2018;7:e33843 doi: 10.7554/eLife.33843

Abstract

Segmentation of the axial skeleton in amniotes depends on the segmentation clock which patterns the paraxial mesoderm and the sclerotome. While the segmentation clock clearly operates in teleosts, the role of the sclerotome in establishing the axial skeleton is unclear. We severely disrupt zebrafish paraxial segmentation, yet observe a largely normal segmentation process of the chordacentra. We demonstrate that axial entpd5+ notochord sheath cells are responsible for chordacentrum mineralization, and serve as a marker for axial segmentation. While autonomous within the notochord sheath, entpd5 expression and centrum formation show some plasticity and can respond to myotome pattern. These observations reveal for the first time the dynamics of notochord segmentation in a teleost, and are consistent with an autonomous patterning mechanism that is influenced, but not determined by adjacent paraxial mesoderm. This behavior is not consistent with a clock-type mechanism in the notochord.

Data availability

Modelling films and images for the virtual time lapse have been uploaded to a public server from the university of Münster.The code in order to reproduce the model has been submitted to E-life directly

Article and author information

Author details

  1. Laura LLeras Forero

    Institute for Cardiovascular Organogenesis and Regeneration, Faculty of Medicine, University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Rachna Narayanan

    The Francis Crick Institute, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Leonie F A Huitema

    Hubrecht Institute, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Maaike VanBergen

    Institute for Cardiovascular Organogenesis and Regeneration, Faculty of Medicine, University of Münster, Münster, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Alexander Apschner

    Hubrecht Institute, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Josi Peterson-Maduro

    Hubrecht Institute, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  7. Ive Logister

    Hubrecht Institute, Utrecht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  8. Guillaume Valentin

    Department of Cell and Developmental Biology, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Luis G Morelli

    Instituto de Investigación en Biomedicina de Buenos Aires, Buenos Aires, Argentina
    Competing interests
    The authors declare that no competing interests exist.
  10. Andrew Oates

    The Francis Crick Institute, London, United Kingdom
    For correspondence
    andrew.oates@epfl.ch
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3015-3978
  11. Stefan Schulte-Merker

    Institute for Cardiovascular Organogenesis and Regeneration, Faculty of Medicine, University of Münster, Münster, Germany
    For correspondence
    Stefan.Schulte-Merker@ukmuenster.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3617-8807

Funding

Cancer Research UK

  • Rachna Narayanan
  • Andrew Oates

Medical Research Council

  • Rachna Narayanan
  • Andrew Oates

Wellcome

  • Guillaume Valentin
  • Andrew Oates

Fondo para la Investigación Científica y Tecnológica

  • Luis G Morelli

Deutsche Forschungsgemeinschaft

  • Laura LLeras Forero
  • Stefan Schulte-Merker

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

Ethics

Animal experimentation: Animal experiments were approved by the Animal Experimentation Committee (DEC) of the Royal Netherlands Academy of Arts and Sciences and by the UK Home Office under PPL 70/7675

Reviewing Editor

  1. Tanya T. Whitfield, University of Sheffield, United Kingdom

Publication history

  1. Received: November 25, 2017
  2. Accepted: April 4, 2018
  3. Accepted Manuscript published: April 6, 2018 (version 1)
  4. Version of Record published: May 21, 2018 (version 2)

Copyright

© 2018, LLeras Forero 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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