Physical limits of flow sensing in the left-right organizer

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Cite as: eLife 2017;6:e25078 doi: 10.7554/eLife.25078

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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.

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Author details

Rita R Ferreira

Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France

Competing interests
No competing interests declared.
Andrej Vilfan

J. Stefan Institute, Ljubljana, Slovenia

For correspondence
andrej.vilfan@ijs.si

Competing interests
No competing interests declared.

0000-0001-8985-6072
Frank Jülicher

Max-Planck-Institute for the Physics of Complex Systems, Dresden, Germany

Competing interests
Frank Jülicher, Reviewing editor, eLife.

0000-0003-4731-9185
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.

0000-0002-4562-9166
Julien Vermot

Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France

For correspondence
julien@igbmc.fr

Competing interests
No competing interests declared.

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

Richard M Berry, University of Oxford, United Kingdom

Publication history

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

Copyright

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.