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. University of Dundee, United States
  4. 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

    nstitute 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 States
    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.

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.

Metrics

  • 1,465
    views
  • 258
    downloads
  • 27
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Physics of Living Systems
    James E Hammond, Ruth E Baker, Berta Verd
    Research Article

    Vertebrates have evolved great diversity in the number of segments dividing the trunk body, however, the developmental origin of the evolvability of this trait is poorly understood. The number of segments is thought to be determined in embryogenesis as a product of morphogenesis of the pre-somitic mesoderm (PSM) and the periodicity of a molecular oscillator active within the PSM known as the segmentation clock. Here, we explore whether the clock and PSM morphogenesis exhibit developmental modularity, as independent evolution of these two processes may explain the high evolvability of segment number. Using a computational model of the clock and PSM parameterised for zebrafish, we find that the clock is broadly robust to variation in morphogenetic processes such as cell ingression, motility, compaction, and cell division. We show that this robustness is in part determined by the length of the PSM and the strength of phase coupling in the clock. As previous studies report no changes to morphogenesis upon perturbing the clock, we suggest that the clock and morphogenesis of the PSM exhibit developmental modularity.

    1. Physics of Living Systems
    Emmanuel Akabuogu, Victor Carneiro da Cunha Martorelli ... Thomas A Waigh
    Research Article

    Bacterial biofilms are communities of bacteria usually attached to solid strata and often differentiated into complex structures. Communication across biofilms has been shown to involve chemical signaling and, more recently, electrical signaling in Gram-positive biofilms. We report for the first time, community-level synchronized membrane potential dynamics in three-dimensional Escherichia coli biofilms. Two hyperpolarization events are observed in response to light stress. The first requires mechanically sensitive ion channels (MscK, MscL, and MscS) and the second needs the Kch-potassium channel. The channels mediated both local spiking of single E. coli biofilms and long-range coordinated electrical signaling in E. coli biofilms. The electrical phenomena are explained using Hodgkin-Huxley and 3D fire-diffuse-fire agent-based models. These data demonstrate that electrical wavefronts based on potassium ions are a mechanism by which signaling occurs in Gram-negative biofilms and as such may represent a conserved mechanism for communication across biofilms.