Transient Membrane Localization of SPV-1 Drives Cyclical Actomyosin Contractions in the C. elegans Spermatheca

Abstract

Actomyosin contractility is the major cellular force driving changes in cell and tissue shape. A principal regulator of contractility is the small GTPase RhoA. External mechanical forces have been shown to impact RhoA activity and cellular contractility. However, the mechanotransduction pathway from external forces to actomyosin contractility is poorly understood. Here, we show that actomyosin contractility in the C. elegans spermatheca is under control of RHO-1/RhoA, which, in turn, is regulated by the F-BAR and RhoGAP protein SPV-1. In the relaxed spermatheca, SPV-1 localizes through its F-BAR domain to the apical membrane, where it inhibits RHO-1/RhoA activity through its RhoGAP domain. Oocyte entry forces the spermatheca cells to stretch, and subsequently SPV-1 detaches from the membrane, permitting RHO-1 activity to increase. The increase in RHO-1 activity facilitates spermatheca contraction and expulsion of the newly fertilized embryo into the uterus, leading to relaxation of the spermatheca, SPV-1 membrane localization, and initiation of a new cycle. Our results demonstrate how transient membrane localization of a novel F-BAR domain, likely via specific binding to curved membranes, coupled to a RhoGAP domain, can provide feedback between a mechanical signal (membrane stretching) and actomyosin contractility. We anticipate this to be a widely utilized feedback mechanism used to balance actomyosin forces in the face of externally applied forces, as well as intrinsic processes involving cell deformation, from single-cell migration to tissue morphogenesis.