Structural polymorphism in heterogeneous cytoskeletal networks

Abstract

The viscoelastic response of living cells is largely determined by heterogenous networks of cross-linked and bundled actin filaments. The quantitative impact of such local network heterogeneities is studied best in well-defined in vitro model systems by employing microscopic and micromechanical techniques. In this study, we show that reconstituted α-actinin/actin networks exhibit a structural polymorphism, which is dictated by two types of mesoscopic heterogeneities: a composite bundle phase at intermediate α-actinin concentrations and clusters of actin bundles at high α-actinin concentrations. We demonstrate the influence of these structural heterogeneities on the mechanical properties of cross-linked and bundled actin networks. First, locally embedding stiff bundles into the network strengthens the macroscopic network response. Second, the formation of fractal, star-like bundle clusters drastically concentrates material in localized spots and weakens the network elasticity. Such bundle cluster networks exhibit kinetically trapped and thus metastable network configurations—which is contrary to the commonly accepted belief of equilibrated network formations.