Emergence of a smooth interface from growth of a dendritic network against a mechanosensitive contractile material

Abstract

Structures and machines require smoothening of raw materials. Self-organized smoothening guides cell and tissue morphogenesis, and is relevant to advanced manufacturing. Across the syncytial Drosophila embryo surface, smooth interfaces form between expanding Arp2/3-based actin caps and surrounding actomyosin networks, demarcating the circumferences of nascent dome-like compartments used for pseudo-cleavage. We found that forming a smooth and circular boundary of the surrounding actomyosin domain requires Arp2/3 in vivo. To dissect the physical basis of this requirement, we reconstituted the interacting networks using node-based models. In simulations of actomyosin networks with local clearances in place of Arp2/3 domains, rough boundaries persisted when myosin contractility was low. With addition of expanding Arp2/3 network domains, myosin domain boundaries failed to smoothen, but accumulated myosin nodes and tension. After incorporating actomyosin mechanosensitivity, Arp2/3 network growth locally induced a surrounding contractile actomyosin ring that smoothened the interface between the cytoskeletal domains, an effect also evident in vivo. In this way, a smooth structure can emerge from the lateral interaction of irregular active materials.

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All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Medha Sharma

    Cell and Systems Biology, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Tao Jiang

    Cell and Systems Biology, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Zi Chen Jiang

    Cell and Systems Biology, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Carlos E Moguel-Lehmer

    Cell and Systems Biology, University of Toronto, Toronto, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Tony Harris

    Cell and Systems Biology, University of Toronto, Toronto, Canada
    For correspondence
    tony.harris@utoronto.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0798-970X

Funding

Natural Sciences and Engineering Research Council of Canada (RGPIN-2016-05617)

  • Tony Harris

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

Copyright

© 2021, Sharma 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. Medha Sharma
  2. Tao Jiang
  3. Zi Chen Jiang
  4. Carlos E Moguel-Lehmer
  5. Tony Harris
(2021)
Emergence of a smooth interface from growth of a dendritic network against a mechanosensitive contractile material
eLife 10:e66929.
https://doi.org/10.7554/eLife.66929

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https://doi.org/10.7554/eLife.66929

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