Actomyosin pulsation and symmetry breaking flows in a confined active elastomer subject to affine and nonaffine deformations

TL;DR

This study models the actomyosin cytoskeleton as a confined active elastomer, revealing how its nonlinear dynamics lead to pulsation, flow, and symmetry breaking, with implications for tissue remodeling.

Contribution

It introduces a theoretical framework for actomyosin dynamics incorporating affine and nonaffine deformations, explaining spontaneous oscillations and flows observed in tissues.

Findings

Active elastomer exhibits spontaneous oscillations and waves.

Large contractile stresses induce nonaffine deformations.

Predictions validated in Drosophila embryonic cells.

Abstract

Tissue remodelling in diverse developmental contexts require cell shape changes that have been associated with pulsation and flow of the actomyosin cytoskeleton. Here we describe the dynamics of the actomyosin cytoskeleton as a confined active elastomer embedded in the cytosol and subject to turnover of its components. Under affine deformations (homogeneous deformation over a spatially coarse-grained scale), the active elastomer exhibits spontaneous oscillations, propagating waves, contractile collapse and spatiotemporal chaos. The collective nonlinear dynamics shows nucleation, growth and coalescence of actomyosin-dense regions which, beyond a threshold, spontaneously move as a spatially localized traveling front towards one of the boundaries. However, large myosin-induced contractile stresses, can lead to nonaffine deformations due to actin turnover. This results in a transient actin network, that naturally accommodates intranetwork flows of the actomyosin dense regions as a consequence of filament unbinding and rebinding. Our work suggests that the driving force for the spontaneous movement comes from the actomyosin-dense region itself and not the cell boundary. We verify the many predictions of our study in Drosophila embryonic epithelial cells undergoing neighbour exchange during a collective process of tissue extension called germband extension.