Filament turnover tunes both force generation and dissipation to control long-range flows in a model actomyosin cortex

PLoS Comput Biol. 2017 Dec 18;13(12):e1005811. doi: 10.1371/journal.pcbi.1005811. eCollection 2017 Dec.

Abstract

Actomyosin-based cortical flow is a fundamental engine for cellular morphogenesis. Cortical flows are generated by cross-linked networks of actin filaments and myosin motors, in which active stress produced by motor activity is opposed by passive resistance to network deformation. Continuous flow requires local remodeling through crosslink unbinding and and/or filament disassembly. But how local remodeling tunes stress production and dissipation, and how this in turn shapes long range flow, remains poorly understood. Here, we study a computational model for a cross-linked network with active motors based on minimal requirements for production and dissipation of contractile stress: Asymmetric filament compliance, spatial heterogeneity of motor activity, reversible cross-links and filament turnover. We characterize how the production and dissipation of network stress depend, individually, on cross-link dynamics and filament turnover, and how these dependencies combine to determine overall rates of cortical flow. Our analysis predicts that filament turnover is required to maintain active stress against external resistance and steady state flow in response to external stress. Steady state stress increases with filament lifetime up to a characteristic time τm, then decreases with lifetime above τm. Effective viscosity increases with filament lifetime up to a characteristic time τc, and then becomes independent of filament lifetime and sharply dependent on crosslink dynamics. These individual dependencies of active stress and effective viscosity define multiple regimes of steady state flow. In particular our model predicts that when filament lifetimes are shorter than both τc and τm, the dependencies of effective viscosity and steady state stress on filament turnover cancel one another, such that flow speed is insensitive to filament turnover, and shows a simple dependence on motor activity and crosslink dynamics. These results provide a framework for understanding how animal cells tune cortical flow through local control of network remodeling.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / chemistry
  • Actin Cytoskeleton / physiology
  • Actomyosin / chemistry
  • Actomyosin / physiology*
  • Animals
  • Biomechanical Phenomena
  • Computational Biology
  • Computer Simulation
  • Cytoskeleton / physiology
  • Models, Biological
  • Molecular Motor Proteins / chemistry
  • Molecular Motor Proteins / physiology
  • Morphogenesis
  • Rheology
  • Stress, Physiological
  • Viscosity

Substances

  • Molecular Motor Proteins
  • Actomyosin