Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination

  1. Hanqing Guo
  2. Michael Swan
  3. Bing He  Is a corresponding author
  1. Dartmouth College, United States
  2. Princeton University, United States

Abstract

Apical constriction driven by actin and non-muscle myosin II ('actomyosin') provides a well-conserved mechanism to mediate epithelial folding. It remains unclear how contractile forces near the apical surface of a cell sheet drive out-of-the-plane bending of the sheet and whether myosin contractility is required throughout folding. By optogenetic-mediated acute inhibition of actomyosin, we find that during Drosophila mesoderm invagination, actomyosin contractility is critical to prevent tissue relaxation during the early, 'priming' stage of folding but is dispensable for the actual folding step after the tissue passes through a stereotyped transitional configuration. This binary response suggests that Drosophila mesoderm is mechanically bistable during gastrulation. Computer modeling analysis demonstrates that the binary tissue response to actomyosin inhibition can be recapitulated in the simulated epithelium that undergoes buckling-like deformation jointly mediated by apical constriction in the mesoderm and in-plane compression generated by apicobasal shrinkage of the surrounding ectoderm. Interestingly, comparison between wild type and snail mutants that fail to specify the mesoderm demonstrates that the lateral ectoderm undergoes apicobasal shrinkage during gastrulation independently of mesoderm invagination. We propose that Drosophila mesoderm invagination is achieved through an interplay between local apical constriction and mechanical bistability of the epithelium that facilitates epithelial buckling.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for the codes for the computer models described in this work and the numerical data for Figure 4 - figure supplement 1 and Figure 9.

Article and author information

Author details

  1. Hanqing Guo

    Department of Biological Sciences, Dartmouth College, Hanover, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Michael Swan

    Department of Molecular Biology, Princeton University, Princeton, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Bing He

    Department of Biological Sciences, Dartmouth College, Hanover, United States
    For correspondence
    Bing.He@Dartmouth.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8564-0933

Funding

National Institute of General Medical Sciences (ESI-MIRA R35GM128745)

  • Hanqing Guo
  • Bing He

American Cancer Society (#IRG -82-003-33)

  • Bing He

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

Reviewing Editor

  1. Michel Bagnat, Duke University, United States

Publication history

  1. Preprint posted: March 19, 2021 (view preprint)
  2. Received: April 3, 2021
  3. Accepted: February 22, 2022
  4. Accepted Manuscript published: February 23, 2022 (version 1)
  5. Version of Record published: March 4, 2022 (version 2)

Copyright

© 2022, Guo 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. Hanqing Guo
  2. Michael Swan
  3. Bing He
(2022)
Optogenetic inhibition of actomyosin reveals mechanical bistability of the mesoderm epithelium during Drosophila mesoderm invagination
eLife 11:e69082.
https://doi.org/10.7554/eLife.69082

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