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Epithelial Tissues as Active Solids: From Nonlinear Contraction Pulses to Rupture Resistance

View ORCID ProfileShahaf Armon, Matthew S. Bull, View ORCID ProfileAvraham Moriel, View ORCID ProfileHillel Aharoni, View ORCID ProfileManu Prakash
doi: https://doi.org/10.1101/2020.06.15.153163
Shahaf Armon
1Department of Physics of Complex Systems, Weizmann Institute of Science, Rehovot, Israel
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  • For correspondence: shahaf.armon@weizmann.ac.il
Matthew S. Bull
2Department of Applied Physics, Stanford University, California, USA
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Avraham Moriel
3Department of Chemical and Biological Physics, Weizmann Institute of Science, Rehovot, Israel
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Hillel Aharoni
1Department of Physics of Complex Systems, Weizmann Institute of Science, Rehovot, Israel
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Manu Prakash
4Department of Bio-Engineering, Stanford University, California, USA
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Abstract

Epithelial tissues in many contexts can be viewed as soft active solids. Their active nature is manifested in the ability of individual cells within the tissue to contract and/or remodel their mechanical properties in response to various conditions. Little is known about the emergent properties of such materials. Specifically, how an individual cellular activity gives rise to collective spatiotemporal patterns is not fully understood. Recently we reported the observation of ultrafast contraction pulses in the dorsal epithelium of T.adhaerens in vivo [1] and speculated these propagate via mechanical fields. Other accumulating evidence suggest mechanics is involved in similar contractile patterns in embryonic development in vivo and in cellular monolayers in vitro. Here we show that a widespread cellular response – activation of contraction in response to stretch – is sufficient to give rise to nonlinear propagating contraction pulses. Using a minimal numerical model and theoretical considerations we show how such mechanical pulses emerge and propagate, spontaneously or in response to external stretch. The model – whose mathematical structure resembles that of reaction-diffusion systems – explains observed phenomena in T. adhaerens (e.g. excitable or spontaneous pulses, pulse interaction) and predicts other phenomena (e.g. symmetric strain profile, “spike trains”). Finally, we show that such an active two-dimensional sheet dynamically distributes external loads across its surface, facilitating tissue resistance to rupture due to cellular strain. Adding a cellular softening-threshold further enhances the tissue resistance to rupture at cell-cell junctions. As cohesion is at the heart of epithelial physiology, our model may be relevant to many other epithelial systems, even if manifested at different time/length scales.

Significance Our work demonstrates that many observed dynamical phenomena in epithelial tissues can be explained merely by mechanical cell-cell interactions, and do not require chemical diffusion or transport between cells (though chemical activity may participate in relevant intracellular processes). Specifically, we show that single cell extension-induced-contraction (EIC) is sufficient to generate propagating contraction pulses, which also increase the tissue’s resistance to rupture, an essential function of epithelia. Our results may shed light on how epithelial tissues function under challenging physiological conditions, e.g. in lung, gut, vasculature and other biomedical contexts. Our results may also be relevant in the study of early evolution of multicellularity and the nervous-muscular systems. Finally, the work offers guidelines for designing soft synthetic solids with improved mechanical properties.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted June 16, 2020.
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Epithelial Tissues as Active Solids: From Nonlinear Contraction Pulses to Rupture Resistance
Shahaf Armon, Matthew S. Bull, Avraham Moriel, Hillel Aharoni, Manu Prakash
bioRxiv 2020.06.15.153163; doi: https://doi.org/10.1101/2020.06.15.153163
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Epithelial Tissues as Active Solids: From Nonlinear Contraction Pulses to Rupture Resistance
Shahaf Armon, Matthew S. Bull, Avraham Moriel, Hillel Aharoni, Manu Prakash
bioRxiv 2020.06.15.153163; doi: https://doi.org/10.1101/2020.06.15.153163

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