Active Patterning and Contractile Dynamics in Actin Networks Driven by Myosin Motors

Abstract

Self-organized contractile arrays of actin filaments and myosin motors drive cell division, migration, and tissue morphogenesis. Biophysical studies have provided many insights into the mechanisms of force production by individual motor molecule. However, a mechanistic explanation of collective self-assembly into force-generating arrays is still lacking. We studied how the collective activity of myosin motors organizes actin filaments into contractile structures in a simplified model system devoid of biochemical regulation. We showed that myosin organizes actin into contractile arrays by a 3-stage process. First, the actin filaments mediate the formation of dense foci by active motor transport and motor coalescence. The myosin foci then accumulate actin filaments in a disordered cloud around them, and these actomyosin condensates finally merge into superaggregates by contractile coalescence. We propose that the origin of this multistage aggregation is the highly nonlinear load response of actin filaments, which can support large tensions but buckle already under picoNewton-compressive loads. Since the motor generated forces well exceed this buckling threshold, buckling is induced by the elastic resistance of connected actin networks to filament sliding. We furthermore mapped the spatiotemporal characteristics of the motor-induced contractility by tracking embedded particles, and found that myosin induces long-range, but localized, contractile fluctuations. The contractile dynamics and actomyosin superaggregates closely mimic observations in vivo. However, the localization and turnover of actomyosin arrays and directed cortical flows likely require an interplay of collective self-organization and biochemical regulation.