Dynamic force patterns promote coordinated cell movements during embryonic wound repair

Embryos display an outstanding ability to rapidly repair wounds, in a process driven by collective cell movements. Actin and the motor protein non-muscle myosin II become polarized in the cells adjacent to the wound, forming a supracellular cable that contracts to coordinate the movements that drive tissue repair. We showed that, in Drosophila embryos, the cable is heterogeneous, with regions of high and low actin density. Mutants in which actin is uniform around the wound display slower wound closure. However, the mechanisms by which a non-uniform distribution of actin favors rapid repair are unknown. Using laser ablation, we demonstrated that actomyosin-rich segments of the cable sustain higher contractile forces, indicating that cable contraction is non-uniform. We developed a computer model of wound repair, and we found that a heterogeneous actomyosin distribution was favorable for wound closure when myosin assembly at the wound edge was strain-dependent. To test the model prediction, we used a laser-based method to induce ectopic strain on cell boundaries in vivo, and we found that myosin accumulated in response to deformation. Using pharmacological and genetic treatments, we found that stretch-activated ion channels were necessary for rapid embryonic wound repair. Our results suggest that local heterogeneities in supracellular actomyosin networks promote faster wound closure by generating mechanical signals sensed by stretch-activated channels that facilitate myosin assembly and coordinate cell behaviors.