Kinesin-driven de-mixing of cytoskeleton composites drives emergent mechanical properties

TL;DR

This study combines experiments and modeling to reveal how kinesin motors induce de-mixing in cytoskeleton composites, leading to emergent mechanical behaviors like stiffness and resistance, depending on motor concentration and strain rate.

Contribution

It demonstrates that kinesin-driven de-mixing of actin and microtubules causes novel mechanical properties, providing new insights into cytoskeletal mechanics and active composite behavior.

Findings

Composites show elastic, yielding, and stiffening responses.

Mechanical properties are tuned by motor concentration and strain rate.

De-mixing correlates with increased stiffness and resistance.

Abstract

The cytoskeleton is an active composite of filamentous proteins that dictates diverse mechanical properties and processes in eukaryotic cells by generating forces and autonomously restructuring itself. Enzymatic motors that act on the comprising filaments play key roles in this activity, driving spatiotemporally heterogeneous mechanical responses that are critical to cellular multifunctionality, but also render mechanical characterization challenging. Here, we couple optical tweezers microrheology and fluorescence microscopy with simulations and mathematical modeling to robustly characterize the mechanics of active composites of actin filaments and microtubules restructured by kinesin motors. We discover that composites exhibit a rich ensemble of force response behaviors, elastic, yielding, and stiffening, with their propensity and properties tuned by motor concentration and strain rate. Moreover, intermediate kinesin concentrations elicit emergent mechanical stiffness and resistance while higher and lower concentrations exhibit softer, more viscous dissipation. We further show that composites transition from well-mixed interpenetrating double-networks of actin and microtubules to de-mixed states of microtubule-rich aggregates surrounded by relatively undisturbed actin phases. It is this de-mixing that leads to the emergent mechanical response, offering an alternate route that composites can leverage to achieve enhanced stiffness through coupling of structure and mechanics.