Rupture and Contraction of Crosslinked Actin Networks by Myosin Motor Activity

Abstract

Self-organized contractile arrays of actin filaments and myosin motors drive cell division, migration, and tissue morphogenesis. Biophysical studies have provided detailed mechanistic insights into the mechanisms of force production by individual motor molecule. However, it is not well understood how motors and actin filaments collectively self-organize into force-generating arrays. It is for instance poorly understood how network connectivity (or crosslinking) influences active contractility. We addressed this problem by reconstituting cell-free model systems from purified actin, myosin, and actin crosslinking proteins. By studying motor-driven activity over a broad range of network connectivities, we discovered that myosin motors contract actin networks into clusters that exhibit a scale-free distribution of sizes, characteristic of a critical state. Surprisingly, this critical behavior occurs over a broad range of network connectivities. To explain this robustness, we performed simulations of contractile networks taking into account network restructuring: motors reduce connectivity by promoting crosslink unbinding. We demonstrate that this coupling between activity and connectivity drives initially well-connected networks to a critically connected state. This model provides new avenues to understand contraction and rupture phenomena occurring during cell and tissue morphogenesis.