Non-uniform filament turnover and mechanically-driven contractility and bundle formation in disordered actomyosin networks

Abstract

Bundles of actin filaments with similar positions and orientations commonly occur in cytoskeletal networks. We use mathematical modelling and simulation to investigate how filament turnover and mechanics influence contractility and bundle formation in disordered actomyosin networks. Using a two-dimensional agent-based model for an actomyosin network, we investigate four simplified models for filament turnover: uniform, biased, branching, and treadmilling. With no turnover, over time contractility decreases and bundle formation increases, and networks eventually form stationary patterns that cannot contract. Introducing turnover allows contractility to persist longer compared to the no-turnover scenario. Uniform turnover, where new filaments have random positions and orientations, disrupts bundle formation and enables persistent contractility. In biased turnover, branching, and treadmilling, the positions and orientations of new filaments depend on the existing network. These non-uniform turnover models increase bundle formation compared to uniform turnover, while still allowing long-term contractility. Branching at 70{degrees} disrupts bundle formation to enable prolonged contractility, whereas filament treadmilling disrupts the trade-off between bundle formation and contractility. Biased turnover places new filaments near existing ones, which promotes bundle formation but is less effective at maintaining contractility. We also varied mechanical factors in our simulations, especially filament bending flexibility and protein friction, which enhance bundle formation and contractility, respectively. Our results suggest that variations in turnover and mechanics might allow cells to tune contractility and bundle formation in disordered actomyosin networks.