Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock

  1. Alexis B Webb
  2. Iván M Lengyel
  3. David J Jörg
  4. Guillaume Valentin
  5. Frank Jülicher
  6. Luis G Morelli
  7. Andrew C Oates  Is a corresponding author
  1. The Francis Crick Institute, United Kingdom
  2. CONICET, Argentina
  3. Max Planck Institute for the Physics of Complex Systems, Germany
  4. Genoway, France

Abstract

In vertebrate development, the sequential and rhythmic segmentation of the body axis is regulated by a 'segmentation clock.' This clock is comprised of a population of coordinated oscillating cells that together produce rhythmic gene expression patterns in the embryo. Whether individual cells autonomously maintain oscillations, or whether oscillations depend on signals from neighboring cells is unknown. Using a transgenic zebrafish reporter line for the cyclic transcription factor Her1, we recorded single tailbud cells in vitro. We demonstrate that individual cells can behave as autonomous cellular oscillators. We described the observed variability in cell behavior using a theory of generic oscillators with correlated noise. Single cells have longer periods and lower precision than the tissue, highlighting the role of collective processes in the segmentation clock. Our work reveals a population of cells from the zebrafish segmentation clock that behave as self-sustained, autonomous oscillators with distinctive noisy dynamics.

Article and author information

Author details

  1. Alexis B Webb

    The Francis Crick Institute, London, United Kingdom
    Competing interests
    No competing interests declared.
  2. Iván M Lengyel

    Departamento de Física, FCEyN UBA and IFIBA, CONICET, Buenos Aires, Argentina
    Competing interests
    No competing interests declared.
  3. David J Jörg

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    No competing interests declared.
  4. Guillaume Valentin

    Genoway, Lyon, France
    Competing interests
    No competing interests declared.
  5. Frank Jülicher

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    Frank Jülicher, Reviewing editor, eLife.
  6. Luis G Morelli

    Departamento de Física, FCEyN UBA and IFIBA, CONICET, Buenos Aires, Argentina
    Competing interests
    No competing interests declared.
  7. Andrew C Oates

    Mill Hill Laboratory, The Francis Crick Institute, London, United Kingdom
    For correspondence
    andrew.oates@crick.ac.uk
    Competing interests
    No competing interests declared.

Reviewing Editor

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

Ethics

Animal experimentation: Zebrafish experimentation was carried out in strict accordance with the ethics and regulations of the Saxonian Ministry of the Environment and Agriculture in Germany under licence Az. 74-9165.40-9-2001, and the Home Office in the United Kingdom under project licence PPL No. 70/7675.

Version history

  1. Received: July 8, 2015
  2. Accepted: February 11, 2016
  3. Accepted Manuscript published: February 13, 2016 (version 1)
  4. Version of Record published: March 4, 2016 (version 2)

Copyright

© 2016, Webb 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. Alexis B Webb
  2. Iván M Lengyel
  3. David J Jörg
  4. Guillaume Valentin
  5. Frank Jülicher
  6. Luis G Morelli
  7. Andrew C Oates
(2016)
Persistence, period and precision of autonomous cellular oscillators from the zebrafish segmentation clock
eLife 5:e08438.
https://doi.org/10.7554/eLife.08438

Share this article

https://doi.org/10.7554/eLife.08438

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