Attachment and detachment of cortical myosin regulates cell junction exchange during cell rearrangement in the Drosophila wing epithelium

Epithelial cells remodel cell adhesion and change their neighbors to shape a tissue. This cellular rearrangement proceeds in three steps: the shrinkage of a junction, exchange of junctions, and elongation of the newly generated junction. Herein, by combining live imaging and physical modeling, we showed that the formation of myosin-II (myo-II) cables around the cell vertices underlies the exchange of junctions in the Drosophila wing epithelium. The local and transient detachment of myo-II from the cell cortex is regulated by the LIM domain-containing protein Jub and the tricellular septate junction protein M6. Moreover, we found that M6 shifts to the adherens junction plane on jub RNAi and that Jub is persistently retained at reconnecting junctions in m6 RNAi cells. This interplay between Jub and M6 can depend on the junction length and thereby couples the detachment of cortical myo-II cables and the shrinkage/elongation of the junction during cell rearrangement. Furthermore, we developed a mechanical model based on the wetting theory and clarified how the physical properties of myo-II cables are integrated with the junction geometry to induce the transition between the attached and detached states and support the unidirectionality of cell rearrangement. Collectively, this study elucidates the orchestration of geometry, mechanics, and signaling for exchanging junctions. [Display omitted] •myo-II transiently forms rectangle-shaped cables around the cell vertices•The local and transient detachment of myo-II underlies the cell junction exchange•Jub, M6, and PTEN regulate the detachment of myo-II from the cell cortex•A physical model clarifies conditions for the myo-II detachment/reattachment Ikawa et al. show that the formation of myo-II cables around the cell vertices underlies the exchange of junctions during cell rearrangement. The local and transient detachment of myo-II from the cell cortex is controlled by the junction geometry, the physical properties of myosin-II cables, and an interplay between Jub and M6.