Generating active T1 transitions through mechanochemical feedback

  1. Rastko Sknepnek  Is a corresponding author
  2. Ilyas Djafer-Cherif
  3. Manli Chuai
  4. Cornelis Weijer  Is a corresponding author
  5. Silke Henkes  Is a corresponding author
  1. University of Dundee, United Kingdom
  2. Polish Academy of Sciences, Poland
  3. Leiden University, Netherlands

Abstract

Convergence-extension in embryos is controlled by chemical and mechanical signalling. A key cellular process is the exchange of neighbours via T1 transitions. We propose and analyse a model with positive feedback between recruitment of myosin motors and mechanical tension in cell junctions. The model produces active T1 events, which act to elongate the tissue perpendicular to the main direction of tissue stress. Using an idealized tissue patch comprising several active cells embedded in a matrix of passive hexagonal cells we identified an optimal range of mechanical stresses to trigger an active T1 event. We show that directed stresses also generate tension chains in a realistic patch made entirely of active cells of random shapes, and leads to convergence-extension over a range of parameters. Our findings show that active intercalations can generate stress that activates T1 events in neighbouring cells resulting in tension dependent tissue reorganisation, in qualitative agreement with experiments on gastrulation in chick embryos.

Data availability

The current manuscript is primarily a computational study, so no data have been generated for this manuscript. Modelling code is publically (GNU public license v 2.0) available on GitHub at: https://github.com/sknepneklab/ActiveJunctionModelThe experimental data presented in Figure 8 and Figure 8 - figure supplement 1 has been generated as described in the methods section.

Article and author information

Author details

  1. Rastko Sknepnek

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    For correspondence
    r.sknepnek@dundee.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0144-9921
  2. Ilyas Djafer-Cherif

    Institute of Physical Chemistry, Polish Academy of Sciences, Warsaw, Poland
    Competing interests
    The authors declare that no competing interests exist.
  3. Manli Chuai

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Cornelis Weijer

    School of Life Sciences, University of Dundee, Dundee, United Kingdom
    For correspondence
    c.j.weijer@dundee.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2192-8150
  5. Silke Henkes

    Leiden Institute of Physics, Leiden University, Leiden, Netherlands
    For correspondence
    shenkes@lorentz.leidenuniv.nl
    Competing interests
    The authors declare that no competing interests exist.

Funding

Biotechnology and Biological Sciences Research Council (BB/N009789/1)

  • Rastko Sknepnek
  • Manli Chuai
  • Cornelis Weijer

Biotechnology and Biological Sciences Research Council (BB/N009150/1-2)

  • Ilyas Djafer-Cherif
  • Silke Henkes

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

Reviewing Editor

  1. Karsten Kruse, University of Geneva, Switzerland

Version history

  1. Preprint posted: June 23, 2021 (view preprint)
  2. Received: April 29, 2022
  3. Accepted: April 9, 2023
  4. Accepted Manuscript published: April 11, 2023 (version 1)
  5. Accepted Manuscript updated: April 24, 2023 (version 2)
  6. Version of Record published: May 3, 2023 (version 3)
  7. Version of Record updated: May 4, 2023 (version 4)

Copyright

© 2023, Sknepnek 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. Rastko Sknepnek
  2. Ilyas Djafer-Cherif
  3. Manli Chuai
  4. Cornelis Weijer
  5. Silke Henkes
(2023)
Generating active T1 transitions through mechanochemical feedback
eLife 12:e79862.
https://doi.org/10.7554/eLife.79862

Share this article

https://doi.org/10.7554/eLife.79862

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