On the force--velocity relationship of a bundle of rigid living filaments

TL;DR

This paper models the force-velocity relationship of a bundle of living filaments, like actin, under load, revealing how their dynamics lead to predictable mechanical behavior in cellular processes.

Contribution

It introduces a stochastic dynamical model for filament bundles under load, analyzing their force-velocity relationship in different experimental setups and conditions.

Findings

The model predicts a stationary velocity under constant load.

Force-velocity curves in optical trap experiments match stationary predictions.

Adiabatic separation explains the similarity of force-velocity curves in different protocols.

Abstract

In various cellular processes, biofilaments like F-actin and F-tubulin are able to exploit chemical energy associated to polymerization to perform mechanical work against an external load. The force-velocity relationship quantitatively summarizes the nature of this process. By a stochastic dynamical model, we give, together with the evolution of a staggered bundle of $N_f$ rigid living filaments facing a loaded wall, the corresponding force--velocity relationship. We compute systematically the simplified evolution of the model in supercritical conditions $\rho_1=U_0/W_0>1$ at $\epsilon=d^2W_0/D=0$, where $d$ is the monomer size, $D$ is the obstacle diffusion coefficient, $U_0$ and $W_0$ are the polymerization and depolymerization rates. Moreover, we see that the solution at $\epsilon=0$ is valid for a good range of small non-zero $\epsilon$ values. We consider two classical protocols: the bundle is opposed either to a constant load or to an optical trap set-up, characterized by a harmonic restoring force. The constant force case leads, for each $F$ value, to a stationary velocity $V^{stat}(F;N_f,\rho_1)$ after a relaxation with characteristic time $\tau_{micro}(F)$. When the bundle (initially taken as an assembly of filament seeds) is subjected to a harmonic restoring force (optical trap load), the bundle elongates and the load increases up to stalling (equilibrium) over a characteristic time $\tau^{OT}$. Extracted from this single experiment, the force-velocity $V^{OT}(F;N_f,\rho_1)$ curve is found to coincide with $V^{stat}(F;N_f,\rho_1)$, except at low loads. We show that this result follows from the adiabatic separation between $\tau_{micro}$ and $\tau^{OT}$, i.e. $\tau_{micro}\ll\tau^{OT}$.