Cortical flow aligns actin filaments to form a furrow

  1. Anne-Cecile Reymann
  2. Fabio Staniscia
  3. Anna Erzberger
  4. Guillaume Salbreux  Is a corresponding author
  5. Stephan W Grill  Is a corresponding author
  1. Technical University Dresden, Germany
  2. Max Planck Institute for the Physics of Complex Systems, Germany
  3. Technische Universität, Germany

Abstract

Cytokinesis in eukaryotic cells is often accompanied by actomyosin cortical flow. Over 30 years ago, Borisy and White proposed that cortical flow converging upon the cell equator compresses the actomyosin network to mechanically align actin filaments. However, actin filaments also align via search-and-capture, and to what extent compression by flow or active alignment drive furrow formation remains unclear. Here we quantify the dynamical organization of actin filaments at the onset of ring assembly in the C. elegans zygote, and provide a framework for determining emergent actomyosin material parameters by use of active nematic gel theory. We characterize flow-alignment coupling, and verify at a quantitative level that compression by flow drives ring formation. Finally, we find that active alignment enhances, but is not required for ring formation. Our work characterizes the physical mechanisms of actomyosin ring formation and highlights the role of flow as a central organizer of actomyosin network architecture.

Article and author information

Author details

  1. Anne-Cecile Reymann

    Biotechnology Center, Technical University Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0517-5083
  2. Fabio Staniscia

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Anna Erzberger

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Guillaume Salbreux

    Max Planck Institute for the Physics of Complex Systems, Dresden, Germany
    For correspondence
    guillaume.salbreux@crick.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  5. Stephan W Grill

    Biotechnology Center, Technische Universität, Dresden, Germany
    For correspondence
    stephan.grill@biotec.tu-dresden.de
    Competing interests
    The authors declare that no competing interests exist.

Funding

Human Frontier Science Program (LT000926/ 2012)

  • Anne-Cecile Reymann

Human Frontier Science Program (RGP0023/2014)

  • Stephan W Grill

European Research Council (281903)

  • Stephan W Grill

Deutsche Forschungsgemeinschaft (SPP 1782, GR 3271/2-1)

  • Stephan W Grill

Deutsche Forschungsgemeinschaft (DFG-GSC 97/3)

  • Anna Erzberger

Max-Planck-Gesellschaft

  • Guillaume Salbreux
  • Stephan W Grill

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

Reviewing Editor

  1. Pekka Lappalainen, University of Helsinki, Finland

Version history

  1. Received: May 13, 2016
  2. Accepted: October 7, 2016
  3. Accepted Manuscript published: October 10, 2016 (version 1)
  4. Version of Record published: November 21, 2016 (version 2)
  5. Version of Record updated: November 22, 2016 (version 3)

Copyright

© 2016, Reymann 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.

Metrics

  • 10,410
    views
  • 1,342
    downloads
  • 148
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Anne-Cecile Reymann
  2. Fabio Staniscia
  3. Anna Erzberger
  4. Guillaume Salbreux
  5. Stephan W Grill
(2016)
Cortical flow aligns actin filaments to form a furrow
eLife 5:e17807.
https://doi.org/10.7554/eLife.17807

Share this article

https://doi.org/10.7554/eLife.17807

Further reading

    1. Cell Biology
    2. Physics of Living Systems
    Qin Ni, Sean X Sun
    Insight

    An influx of water molecules can help immune cells called neutrophils to move to where they are needed in the body.

    1. Cell Biology
    2. Physics of Living Systems
    Tamas L Nagy, Evelyn Strickland, Orion D Weiner
    Research Article

    While the involvement of actin polymerization in cell migration is well-established, much less is known about the role of transmembrane water flow in cell motility. Here, we investigate the role of water influx in a prototypical migrating cell, the neutrophil, which undergoes rapid, directed movement to sites of injury, and infection. Chemoattractant exposure both increases cell volume and potentiates migration, but the causal link between these processes are not known. We combine single-cell volume measurements and a genome-wide CRISPR screen to identify the regulators of chemoattractant-induced neutrophil swelling, including NHE1, AE2, PI3K-gamma, and CA2. Through NHE1 inhibition in primary human neutrophils, we show that cell swelling is both necessary and sufficient for the potentiation of migration following chemoattractant stimulation. Our data demonstrate that chemoattractant-driven cell swelling complements cytoskeletal rearrangements to enhance migration speed.