1. Computational and Systems Biology
  2. Developmental Biology

A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses

  1. Mohamad Ibrahim Cheikh
  2. Joel Tchoufag
  3. Miriam Osterfield
  4. Kevin M Dean
  5. Swayamdipta Bhaduri
  6. Chuzhong Zhang
  7. Kranthi Kiran Mandadapu
  8. Konstantin Doubrovinski  Is a corresponding author
  1. The University of Texas Southwestern Medical Center, United States
  2. University of California, Berkeley, United States
  3. The University of Texas at Arlington, United States
https://doi.org/10.7554/eLife.85569
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Cite this article
  1. Mohamad Ibrahim Cheikh
  2. Joel Tchoufag
  3. Miriam Osterfield
  4. Kevin M Dean
  5. Swayamdipta Bhaduri
  6. Chuzhong Zhang
  7. Kranthi Kiran Mandadapu
  8. Konstantin Doubrovinski
(2023)
A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses
eLife 12:e85569.
https://doi.org/10.7554/eLife.85569
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Abstract

In order to understand morphogenesis, it is necessary to know the material properties or forces shaping the living tissue. In spite of this need, very few in vivo measurements are currently available. Here, using the early Drosophila embryo as a model, we describe a novel cantilever-based technique which allows for the simultaneous quantification of applied force and tissue displacement in a living embryo. By analyzing data from a series of experiments in which embryonic epithelium is subjected to developmentally relevant perturbations, we conclude that the response to applied force is adiabatic and is dominated by elastic forces and geometric constraints, or system size effects. Crucially, computational modeling of the experimental data indicated that the apical surface of the epithelium must be softer than the basal surface, a result which we confirmed experimentally. Further, we used the combination of experimental data and comprehensive computational model to estimate the elastic modulus of the apical surface and set a lower bound on the elastic modulus of the basal surface. More generally, our investigations revealed important general features that we believe should be more widely addressed when quantitatively modeling tissue mechanics in any system. Specifically, different compartments of the same cell can have very different mechanical properties; when they do, they can contribute differently to different mechanical stimuli and cannot be merely averaged together. Additionally, tissue geometry can play a substantial role in mechanical response, and cannot be neglected.

Data availability

All simulation code used in the study is publicly available under https://github.com/doubrovinskilab/cantilever_embryo_rheology

Article and author information

Author details

  1. Mohamad Ibrahim Cheikh

    Department of Biophysics, The University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Joel Tchoufag

    Department of Chemical and Biomolecular Engineering, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Miriam Osterfield

    Department of Biophysics, The University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8907-852X

  4. Kevin M Dean

    Department of Bioinformatics, The University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0839-2320

  5. Swayamdipta Bhaduri

    Department of Biophysics, The University of Texas Southwestern Medical Center, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Chuzhong Zhang

    Department of Material Science and Engineering, The University of Texas at Arlington, Arlington, United States
    Competing interests
    The authors declare that no competing interests exist.

  7. Kranthi Kiran Mandadapu

    Department of Chemical and Biomolecular Engineering, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  8. Konstantin Doubrovinski

    Department of Biophysics, The University of Texas Southwestern Medical Center, Dallas, United States
    For correspondence
    Konstantin.Doubrovinski@UTSouthwestern.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4403-948X

Funding

National Institute of General Medical Sciences (1R01GM134207)

  • Mohamad Ibrahim Cheikh
  • Joel Tchoufag
  • Miriam Osterfield
  • Swayamdipta Bhaduri
  • Konstantin Doubrovinski

National Institute for Child Health and Human Development (1R21HD105189)

  • Mohamad Ibrahim Cheikh
  • Joel Tchoufag
  • Miriam Osterfield
  • Swayamdipta Bhaduri
  • Konstantin Doubrovinski

Robert A. Welch Foundation (I-1950-20180324)

  • Mohamad Ibrahim Cheikh
  • Joel Tchoufag
  • Miriam Osterfield
  • Swayamdipta Bhaduri
  • Konstantin Doubrovinski

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

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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  1. Mohamad Ibrahim Cheikh
  2. Joel Tchoufag
  3. Miriam Osterfield
  4. Kevin M Dean
  5. Swayamdipta Bhaduri
  6. Chuzhong Zhang
  7. Kranthi Kiran Mandadapu
  8. Konstantin Doubrovinski
(2023)
A comprehensive model of Drosophila epithelium reveals the role of embryo geometry and cell topology in mechanical responses
eLife 12:e85569.
https://doi.org/10.7554/eLife.85569

Share this article

https://doi.org/10.7554/eLife.85569

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