Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early C. elegans development

  1. Lokesh G Pimpale
  2. Teije C Middelkoop
  3. Alexander Mietke
  4. Stephan W Grill  Is a corresponding author
  1. Max Planck Institute for Molecular Cell Biology and Genetics, Germany
  2. Massachusetts Institute of Technology, United States

Abstract

Proper positioning of cells is essential for many aspects of development. Daughter cell positions can be specified via orienting the cell division axis during cytokinesis. Rotatory actomyosin flows during division have been implied in specifying and reorienting the cell division axis, but how general such reorientation events are, and how they are controlled, remains unclear. We followed the first nine divisions of Caenorhabditis elegans embryo development and demonstrate that chiral counter-rotating flows arise systematically in early AB lineage, but not in early P/EMS lineage cell divisions. Combining our experiments with thin film active chiral fluid theory we identify a mechanism by which chiral counter-rotating actomyosin flows arise in the AB lineage only, and show that they drive lineage-specific spindle skew and cell reorientation events. In conclusion, our work sheds light on the physical processes that underlie chiral morphogenesis in early development.

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We will provide all the datasets that have been generated in the course of the study.

Article and author information

Author details

  1. Lokesh G Pimpale

    Biophysics, Max Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Teije C Middelkoop

    Biophysics, Max Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Alexander Mietke

    Department of Mathematics, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1170-2406
  4. Stephan W Grill

    Biophysics, Max Planck Institute for Molecular Cell Biology and Genetics, Dresden, Germany
    For correspondence
    grill@mpi-cbg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6145-1516

Funding

European Union's Horizon 2020 research and innovation program - Marie Sklodowska-Curie Grant (641639)

  • Lokesh G Pimpale

EMBO long-term fellowship (ALTF 1033-2015)

  • Teije C Middelkoop

Dutch Research Council Rubicon fellowship (825.15.010)

  • Teije C Middelkoop

ELBE PhD fellowship

  • Alexander Mietke

DFG (SPP 1782,GSC 97,GR 3271/2,GR 624 3271/3,GR 3271/4)

  • Stephan W Grill

European Research Council (281903,742712)

  • Stephan W Grill

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

Copyright

© 2020, Pimpale 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. Lokesh G Pimpale
  2. Teije C Middelkoop
  3. Alexander Mietke
  4. Stephan W Grill
(2020)
Cell lineage-dependent chiral actomyosin flows drive cellular rearrangements in early C. elegans development
eLife 9:e54930.
https://doi.org/10.7554/eLife.54930

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https://doi.org/10.7554/eLife.54930