Structural polymorphism in heterogeneous cytoskeletal networks

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.