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

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.