Astral architecture can enhance mechanical strength of cytoskeletal networks by modulating percolation thresholds

Abstract

A repeated pattern in cytoskeletal architecture is the aster, in which a number of F-actin filaments emerge star-shaped from a central node. Aster-based structures occur in cytoplasmic actin, the early stages of the cytokinetic ring in yeast, and in the context of biomimetic materials engineering. In this work, we use computational simulation to show that there is an optimal number of filaments per aster that maximizes rigidity, even at a fixed density of F-actin. This nonlinear dependence holds for both the shear and extensional moduli. At physiological parameters, the maximum corresponds approximately to the same filaments-per-aster observed in recent super-resolution images of cortical F-actin. Furthermore, we find that increasing filaments-per-aster leads to dramatic increases in the sample-to-sample variability in network rigidity. We explain both effects using percolation theory, wherein the probability that a given network is productively connected exhibits a sharp dependence on parameters. The dependence of network rigidity on this nanoscale architectural feature may suggest a mechanism by which cells tune the physical properties of their actin networks locally and rapidly (since no new F-actin must be assembled) and may inform efforts to create adaptive synthetic metamaterials inspired by actin networks.