Reversible stress softening of actin networks

Abstract

The mechanical properties of cells are governed by a network of interconnected actin filaments. In the past, actin networks in vitro have been studied mainly as collections of randomly organized filaments, and experiments have revealed stiffening of the network on the application of stress. A new study of dendritic actin networks (similar to those in some motile cells) shows that these architectures do undergo stress stiffening, but that it is followed by reversible stress softening at higher loads. These dendritic architectures appear to be geared towards bearing high compressive loads, but the mechanical properties of such networks more generally are the result of a complex interplay of different elastic regimes. The mechanical properties of cells play an essential role in numerous physiological processes. Organized networks of semiflexible actin filaments determine cell stiffness and transmit force during mechanotransduction, cytokinesis, cell motility and other cellular shape changes1,2,3. Although numerous actin-binding proteins have been identified that organize networks, the mechanical properties of actin networks with physiological architectures and concentrations have been difficult to measure quantitatively. Studies of mechanical properties in vitro have found that crosslinked networks of actin filaments formed in solution exhibit stress stiffening arising from the entropic elasticity of individual filaments or crosslinkers resisting extension4,5,6,7,8. Here we report reversible stress-softening behaviour in actin networks reconstituted in vitro that suggests a critical role for filaments resisting compression. Using a modified atomic force microscope to probe dendritic actin networks (like those formed in the lamellipodia of motile cells), we observe stress stiffening followed by a regime of reversible stress softening at higher loads. This softening behaviour can be explained by elastic buckling of individual filaments under compression that avoids catastrophic fracture of the network. The observation of both stress stiffening and softening suggests a complex interplay between entropic and enthalpic elasticity in determining the mechanical properties of actin networks.