Optical tweezers and DDM characterize time-varying strain fields in kinesin-driven cytoskeleton composites.

Abstract

The cytoskeleton continuously self-generates forces and reconfigures itself - in part by motor proteins pushing and pulling on the comprising filaments - to enable diverse mechanical responses to local stresses and strains. We previously showed that kinesin-microtubule interactions lead to dynamics ranging from uncorrelated isotropic fluctuations, to mesoscale restructuring, to bulk flow of actin-microtubule composites. These non-equilibrium dynamics mediate varying degrees of de-mixing, clustering and bundling of originally interpenetrating networks of actin and microtubules. Here, we combine optical tweezers microrheology and fluorescence microscopy to visualize the dynamical response and strain field of composites subject to cyclic mesoscale straining. To characterize the time-varying filament deformations and stress propagation we use space- and time-resolved differential dynamic microscopy (DDM) for quantifying the strain alignment, speed, periodicity, and dissipation of the network dynamics. We show that intermediate concentrations of kinesin motors lead to the most pronounced strain alignment and stress propagation while both low and high motor concentrations lead to more rapidly decaying response. Composite dynamics also exhibit similar emergent non-monotonic dependences on strain speed owing to the different relaxation mechanisms available to structurally-evolving composites.