Nanoscale indentation of plasma membrane establishes a contractile actomyosin scaffold through selective activation of the Amphiphysin-Rho1-Dia/DAAM and Rok pathway

Abstract

Nanoscale bending of plasma membrane increases cell adhesion, induces cell-signalling, triggers F-actin assembly and endocytosis in tissue-cultured cells. The underlying mechanisms are not very well understood. Here, we show that stretching the plasma membrane of somatic cyst cell around rigid spermatid heads generates a stable, tubular endomembrane scaffold supported by contractile actomyosin. The structure resembles an actin-basket covering the bundle of spermatid heads. Genetic analysis suggests that the actomyosin organisation is nucleated exclusively by the Formins, Diaphanous and DAAM, downstream of Rho1, recruited by the Bin-Amphiphysin-Rvs (BAR)-domain protein, Amphiphysin, around the spermatid heads. Actomyosin activity at the actin-basket gathers the spermatid heads into a compact bundle and resists the invasion of the somatic cell by the intruding spermatids. These observations revealed a new response mechanism of nanoscale bending of the plasma membrane, which generates a novel cell adhesion strategy through active clamping. HighlightsO_LIStretching the plasma membrane around a spermatid head recruits Amphiphysin and Rho1. C_LIO_LIRho1 activation triggers F-actin assembly in situ through Diaphanous and DAAM. C_LIO_LIRho1-Rok activation assembles actomyosin scaffold around the folded plasma membrane. C_LIO_LIContractile actomyosin enables plasma membrane to clamp onto the spermatid head. C_LI Author summarySperm released from the somatic enclosure is essential for male fertility. During differentiation, the somatic cell membrane, associated with dense F-actin scaffold, tightly hold each spermatid head before release. Kapoor et al., showed that the bending and stretching of the plasma membrane trigger the assembly of an actomyosin scaffold around the bent membrane, which clamps the spermatids together preventing the premature release and somatic cell penetration. This finding provides new insight into the molecular networks activated by mechanical bending of the plasma membrane.