Force-dependent activation of actin elongation factor mDia1 protects the cytoskeleton from mechanical damage and promotes stress fiber repair

Plasticity of cell mechanics underlies a wide range of cell and tissue behaviors allowing cells to migrate through narrow spaces, resist shear forces, and safeguard against mechanical damage. Such plasticity depends on spatiotemporal regulation of the actomyosin cytoskeleton, but mechanisms of adaptive change in cell mechanics remain elusive. Here, we report a mechanism of mechanically activated actin polymerization at focal adhesions (FAs), specifically requiring the actin elongation factor mDia1. By combining live-cell imaging with mathematical modeling, we show that actin polymerization at FAs exhibits pulsatile dynamics where spikes of mDia1 activity are triggered by contractile forces. The suppression of mDia1-mediated actin polymerization increases tension on stress fibers (SFs) leading to an increased frequency of spontaneous SF damage and decreased efficiency of zyxin-mediated SF repair. We conclude that tension-controlled actin polymerization acts as a safety valve dampening excessive tension on the actin cytoskeleton and safeguarding SFs against mechanical damage.