Actomyosin at the epithelial zonula adherens (ZA) generates junctional tension for tissue integrity and morphogenesis. This requires the RhoA GTPase, which establishes a strikingly stable active zone at the ZA. Mechanisms must then exist to confer robustness on junctional RhoA signalling at the population level. We now identify a feedback network that generates a stable mesoscopic RhoA zone out of dynamic elements. The key is scaffolding of ROCK1 to the ZA by myosin II. ROCK1 protects junctional RhoA by phosphorylating Rnd3 to prevent the cortical recruitment of the Rho suppressor, p190B RhoGAP. Combining predictive modelling and experimentation, we show that this network constitutes a bistable dynamical system that is realized at the population level of the ZA. Thus, stability of the RhoA zone is an emergent consequence of the network of interactions that allow myosin II to feedback to RhoA.

Highlights d Anillin enhances RhoA signaling by countering its labile cortical association d Anillin concentrates PI(4,5)P 2 to retain membrane GTP-RhoA for effector recruitment d Re-binding of RhoA to anillin creates cycles that increase the dwell time of active RhoA d Kinetic scaffolding is sufficient for anillin to support cell contractility

Graphical Abstract Highlights d Acute tensile stress on epithelial monolayer activates RhoA at adherens junctions d Myosin VI is a force sensor responsible for activating RhoA d RhoA signals to stimulate mDia1-mediated F-actin assembly at junctions d Mechanotransduction reinforces the tensile strength of multicellular vertices

Highlights d Caveolae influence contractile tension in epithelial monolayers d Caveolin-1 depletion enhances epithelial tension via PtdIns(4,5)P 2 signaling d Elevated epithelial tension inhibits oncogenic cell extrusion

A mechanosensitive RhoA pathway that protects epithelia against acute tensile stress. AbstractAdherens junctions are tensile structures that couple epithelial cells together.