Cellular context specific tuning of actomyosin ring contractility within a common cytoplasm

Abstract

The non-muscle actomyosin cytoskeleton generates contractile force through the dynamic rearrangement of its constituent parts. Actomyosin rings are a specialization of the non-muscle actomyosin cytoskeleton that are associated with a number of cell biological processes. To explore how contractile forces are generated by actomyosin rings, we studied three instances of ring closure within the common cytoplasm of the C. elegans oogenic germline: when germline stem cells (GSCs) divide mitotically, when meiotic compartments undergo apoptosis, and when nascent oocytes cellularize. We found that each of these rings closed with unique kinetics, protein density and abundance dynamics. These measurements suggested that the mechanism of contractile force generation varied across the subcellular contexts. Next, we formulated a physical model that related the forces generated by filament-filament interactions to the material properties of these rings that dictate the kinetics of their closure. Using this framework, we related the density of conserved cytoskeletal proteins anillin and myosin to the kinematics of ring closure. We found that actomyosin ring closure results from the asymmetric distribution of protein along the length of F-actin, which occurs naturally due to differences in crosslinker and NMMII bundle size. Our work predicts that the role of myosin varies across these ring types, due in part to its distribution along F-actin and motoring.