Writhing of Cytokinetic Contractile Rings Reveals that the Contractile Ring is an Elastoporous Cable

Abstract

We report extraordinary writhing dynamics of isolated fission yeast contractile rings, revealing basic material properties of the actomyosin ring normally hidden under physiological circumstances. Contractile rings exhibited cable-like writhing and coiling, with repeated twisting of the rings leading to multiple coils, similar to the twisting of a telephone cable. Our results suggest the twisting torque is produced by myosin-II in the ring that twisted around anchored actin filaments. Image analysis revealed twisting rates (0.3 rev per micron) very close to those previously reported for myosin II-actin twisting from in vitro gliding assays (0.25 - 2 rev per micron, Nishizaka et al., 1993; Beausang et al., 2008). We show the twisting is quantitatively as would be predicted for a solid cable, and from the measured writhe versus ring length we extracted the effective ratio of ring twisting and bending moduli. A mathematical model quantitatively reproduced the cable-like twisting, based on continuum treatment of the contractile ring as an elastoporous solid, similar to an emerging view of the cell cytoplasm (Moeendarbary et al., 2013). The model predicts that after a transient the ring deforms affinely, with constant twisting rate like a solid cable whose mechanical rigidity is set by its twisted actin filaments. Thus the contractile ring, considered as a whole, is a highly anisotropic elastoporous cable of actin filaments embedded in an effective fluid of myosin-II. We observed these writhing rings in fission yeast cell ghosts, obtained by cell wall digestion and membrane permeabilization that releases cytoplasm (Mishra et al., 2013). Writhing was triggered by sections of contractile rings unanchoring from the weakened membrane, then shortening and writhing due to an apparent twisting torque at the anchored end points. Repeated rotation produced multiple coils in the rings.