Sliding Filament and Fixed Filament Mechanisms Contribute to Tension of the Fission Yeast Cytokinetic Ring

Abstract

A fundamental challenge in cell biology is understanding how cells generate contractile force from actomyosin machineries. The contractile ring is a vital actomyosin machine that generates tension and constricts and divides the cell during cytokinesis. Following discovery of the contractile ring decades ago, a sliding filament mechanism for ring tension was proposed similar to that in muscle (Schroeder, 1972). However, contractile rings lack the highly ordered periodic sarcomeric architecture of muscle, and it remains unknown how tension emerges from the disordered ring organization. Here, we developed a highly coarse-grained continuum model of the fission yeast cytokinetic ring, severely constrained by experimentally measured component amounts. The model incorporates the two myosin-II isoforms, Myo2 in membrane-anchored protein complexes called nodes, and Myp2 clusters assumed unanchored. We found that the model does indeed predict a sliding filament mechanism, but somewhat different to that envisaged by the pioneering studies of Schroeder and others. The sliding filament mechanism is a spatially and temporally homogeneous version of that in muscle: pairs of oppositely oriented actin filaments are made tense as they are pulled toward one another by myosin-II clusters through which they slide. The mechanism relies on anchoring of actin filament barbed ends to the plasma membrane, which enables filaments to become tense when pulled. A second fixed filament component is generated by chains of like-oriented actin filaments encircling the ring, independent of lateral anchoring. Cellular actomyosin contractile machines are intrinsically vulnerable to contractile instabilities. We also studied how such instabilities are controlled. We find that tension loss due to runaway catastrophic aggregation of the contractile components Myo2 and Myp2 is prevented by fast turnover and sufficiently low myosin cluster mobilities, enforced by lateral anchoring and crowding.