Generating active T1 transitions through mechanochemical feedback
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
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
-
- 1,402
- views
-
- 249
- downloads
-
- 25
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
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)
Further reading
-
- Neuroscience
- Physics of Living Systems
Recent experimental studies showed that electrically coupled neural networks like in mammalian inferior olive nucleus generate synchronized rhythmic activity by the subthreshold sinusoidal-like oscillations of the membrane voltage. Understanding the basic mechanism and its implication of such phenomena in the nervous system bears fundamental importance and requires preemptively the connectome information of a given nervous system. Inspired by these necessities of developing a theoretical and computational model to this end and, however, in the absence of connectome information for the inferior olive nucleus, here we investigated interference phenomena of the subthreshold oscillations in the reference system Caenorhabditis elegans for which the structural anatomical connectome was completely known recently. We evaluated how strongly the sinusoidal wave was transmitted between arbitrary two cells in the model network. The region of cell-pairs that are good at transmitting waves changed according to the wavenumber of the wave, for which we named a wavenumber-dependent transmission map. Also, we unraveled that (1) the transmission of all cell-pairs disappeared beyond a threshold wavenumber, (2) long distance and regular patterned transmission existed in the body-wall muscles part of the model network, and (3) major hub cell-pairs of the transmission were identified for many wavenumber conditions. A theoretical and computational model presented in this study provided fundamental insight for understanding how the multi-path constructive/destructive interference of the subthreshold oscillations propagating on electrically coupled neural networks could generate wavenumber-dependent synchronized rhythmic activity.
-
- Physics of Living Systems
The coordinated motion of animal groups through fluids is thought to reduce the cost of locomotion to individuals in the group. However, the connection between the spatial patterns observed in collectively moving animals and the energetic benefits at each position within the group remains unclear. To address this knowledge gap, we study the spontaneous emergence of cohesive formations in groups of fish, modeled as flapping foils, all heading in the same direction. We show in pairwise formations and with increasing group size that (1) in side-by-side arrangements, the reciprocal nature of flow coupling results in an equal distribution of energy requirements among all members, with reduction in cost of locomotion for swimmers flapping inphase but an increase in cost for swimmers flapping antiphase, and (2) in inline arrangements, flow coupling is non-reciprocal for all flapping phase, with energetic savings in favor of trailing swimmers, but only up to a finite number of swimmers, beyond which school cohesion and energetic benefits are lost at once. We explain these findings mechanistically and we provide efficient diagnostic tools for identifying locations in the wake of single and multiple swimmers that offer opportunities for hydrodynamic benefits to aspiring followers. Our results imply a connection between the resources generated by flow physics and social traits that influence greedy and cooperative group behavior.