Physical limits of flow sensing in the left-right organizer

  1. Rita R Ferreira
  2. Andrej Vilfan  Is a corresponding author
  3. Frank Jülicher
  4. Willy Supatto  Is a corresponding author
  5. Julien Vermot  Is a corresponding author
  1. Institut de Génétique et de Biologie Moléculaire et Cellulaire, France
  2. J. Stefan Institute, Slovenia
  3. Max-Planck-Institute for the Physics of Complex Systems, Germany
  4. Ecole Polytechnique, Centre National de la Recherche Scientifique (UMR7645), France

Abstract

Fluid flows generated by motile cilia are guiding the establishment of the left-right asymmetry of the body in the vertebrate left-right organizer. Competing hypotheses have been proposed: the direction of flow is sensed either through mechanosensation, or via the detection of chemical signals transported in the flow. We investigated the physical limits of flow detection in order to clarify which mechanisms could be reliably used for symmetry breaking. We integrated parameters describing cilia distribution and orientation obtained in vivo in zebrafish into a multiscale physical study of flow generation and detection. Our results show that the number of immotile cilia is too small to ensure robust left and right determination by mechanosensing, given the large spatial variability of the flow. However, motile cilia could sense their own motion by a yet unknown mechanism. Finally, transport of chemical signals by the flow can provide a simple and reliable mechanism of asymmetry establishment.

Article and author information

Author details

  1. Rita R Ferreira

    Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
    Competing interests
    No competing interests declared.
  2. Andrej Vilfan

    J. Stefan Institute, Ljubljana, Slovenia
    For correspondence
    andrej.vilfan@ijs.si
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8985-6072
  3. Frank Jülicher

    Max-Planck-Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    Frank Jülicher, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4731-9185
  4. Willy Supatto

    Laboratory for Optics and Biosciences, Ecole Polytechnique, Centre National de la Recherche Scientifique (UMR7645), Palaiseau, France
    For correspondence
    willy.supatto@polytechnique.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4562-9166
  5. Julien Vermot

    Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France
    For correspondence
    julien@igbmc.fr
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8924-732X

Funding

Human Frontier Science Program (CDA00032/2010-C)

  • Julien Vermot

Labex (ANR-10-LABX-0030-INRT)

  • Rita R Ferreira
  • Julien Vermot

Agence Nationale de la Recherche (ANR-13-BSV1-0016)

  • Julien Vermot

Agence Nationale de la Recherche (ANR- 12-ISV2-0001)

  • Julien Vermot

Agence Nationale de la Recherche (ANR-2010-JCJC-1510-01​)

  • Willy Supatto

Agence Nationale de la Recherche (ANR-11-EQPX-0029​)

  • Willy Supatto

Javna Agencija za Raziskovalno Dejavnost RS (grant J1-5437)

  • Andrej Vilfan

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 of the Institutional Review Board of the IGBMC.

Reviewing Editor

  1. Richard M Berry, University of Oxford, United Kingdom

Publication history

  1. Received: January 19, 2017
  2. Accepted: June 13, 2017
  3. Accepted Manuscript published: June 14, 2017 (version 1)
  4. Version of Record published: August 4, 2017 (version 2)

Copyright

© 2017, Ferreira 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. Rita R Ferreira
  2. Andrej Vilfan
  3. Frank Jülicher
  4. Willy Supatto
  5. Julien Vermot
(2017)
Physical limits of flow sensing in the left-right organizer
eLife 6:e25078.
https://doi.org/10.7554/eLife.25078

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