Tension-Sensitive Actin Assembly Supports Contractility at the Epithelial Zonula Adherens

Actomyosin-based contractility acts on cadherin junctions to support tissue integrity and morphogenesis. The actomyosin apparatus of the epithelial zonula adherens (ZA) is built by coordinating junctional actin assembly with Myosin II activation. However, the physical interaction between Myosin and actin filaments that is necessary for contractility can induce actin filament turnover, potentially compromising the contractile apparatus itself. We now identify tension-sensitive actin assembly as one cellular solution to this design paradox. We show that junctional actin assembly is maintained by contractility in established junctions and increases when contractility is stimulated. The underlying mechanism entails the tension-sensitive recruitment of vinculin to the ZA. Vinculin, in turn, directly recruits Mena/VASP proteins to support junctional actin assembly. By combining strategies that uncouple Mena/VASP from vinculin or ectopically target Mena/VASP to junctions, we show that tension-sensitive actin assembly is necessary for junctional integrity and effective contractility at the ZA. We conclude that tension-sensitive regulation of actin assembly represents a mechanism for epithelial cells to resolve potential design contradictions that are inherent in the way that the junctional actomyosin system is assembled. This emphasizes that maintenance and regulation of the actin scaffolds themselves influence how cells generate contractile tension. [Display omitted] •Contractile tension stimulates actin assembly at the epithelial zonula adherens•Vinculin mediates tension-sensitive actin assembly through Mena/VASP proteins•Tension recruits vinculin to promote junctional actin assembly•Tension-sensitive actin assembly is necessary for junctional contractility Leerberg et al. demonstrate that actin assembly at the epithelial zonula adherens responds to contractile tension. Contractility recruits vinculin to apical junctions, where it promotes actin assembly via Mena/VASP proteins. This homeostatic pathway counteracts stress-induced actin filament turnover to preserve effective junctional contractility.