Myosin II does it all: assembly, remodeling, and disassembly of actin networks are governed by myosin II activity

Abstract

Eukaryotic cells rely on their cytoskeleton to carry out coordinated motion, to transport materials within them, and to interact mechanically with their environment. To adapt to the changing requirements, the cell's cytoskeleton constantly remodels through the action of myosin II motor clusters that interact with numerous actin filaments simultaneously. Here we study the various roles of myosin II clusters in the formation and evolution of in vitro actomyosin networks as a model system for the cell's cytoskeleton. In our experiments the motor clusters can vary in size between 14 and 144 myosin II molecules and apply forces ranging from several to tens of piconewtons. During the initial process of network formation the motor clusters become embedded within the network structure, where they act as internal active cross-linkers. Myosin II clusters enhance the nucleation of network filaments/bundles in a concentration dependent manner, in the presence of the passive bundling protein fascin, thus functioning as a ‘network co-nucleator’. As network formation is achieved, myosin II turns into a ‘network reorganizer’, where it takes part in remodeling and coarsening of the overall network structure. As a result of the strong confinement (the motor clusters within the network bundles exhibit high processivity with a fraction of attached motors p_att ≥ 0.15), their effect on the nucleation and reorganization of the actin network is enhanced, rendering even small clusters of 14 myosin II molecules efficient. The stresses building-up in the networks lead to complex dynamics and can drive their contraction and rupture, depending on the motor concentration and cluster size. Above a certain concentration, the severing and disassembly properties of the motors dominate, and they function as ‘network disassembly agents’. Myosin II motors are shown to be unique motors that function as complex machines that can perform a diversity of tasks, thereby regulating the nature of the assembled network and facilitating its formation.