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 rearrange-ment 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 junc-tions 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 re-arrangement. 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 be-tween 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.

Automated summary

Epithelial cells undergo cell rearrangement by remodeling cell adhesion and changing their neighbors to shape a tissue. This process involves junction shrinkage, exchange, and elongation, which are facilitated by the formation of myosin-II cables around cell vertices. The detachment of myosin-II from the cell cortex is regulated by the proteins Jub and M6. The interplay between Jub and M6, dependent on junction length, orchestrates the detachment of myosin-II cables and the shrinkage/elongation of junctions during cell rearrangement. A mechanical model based on wetting theory explains how the physical properties of myosin-II cables and junction geometry contribute to the exchange of junctions in a unidirectional manner.