Filament-level mechanical model of symmetry breaking and comet tail propulsion by branched actin networks

Force generated by growing branched actin networks is of great importance for organelle and cell motility. It has been the subject of extensive investigation, including in vitro reconstitution experiments where Arp2/3 complex branching is activated on micron-sized objects, leading to symmetry breaking and formation of a propelling actin comet tail. We simulated branched network growth on surfaces with attached Arp2/3 activators by extending a filament-level computational model in Xu et al. (Sci. Adv. 2024). In comparison to prior work, the model incorporates mechanics and realistic filament sizes in addition to tracking the entire process of shell growth, symmetry breaking, and bead motion. Semiflexible actin filaments are represented as particles connected by springs that actively polymerize at their barbed ends and elongate according to a Brownian-ratchet-type relationship. A friction coefficient incorporates transient connections between filaments and surface. We explore how symmetry breaking, branched network structure, and force depend on experimentally tunable parameters such as concentrations of Arp2/3 complex, capping protein, myosin 1 motors, and surface shape. We characterize filament severing and debranching contributions to symmetry breaking. We reproduce conditions for saltatory motion and quantify the magnitudes of force by polymerization, elastic squeezing, and myosin 1 through time. Overall, our model provides a cohesive framework for dendritic network mechanics.