Coordination of Septate Junctions Assembly and Completion of Cytokinesis in Proliferative Epithelial Tissues

How permeability barrier function is maintained when epithelial cells divide is largely unknown. Here, we have investigated how the bi (BSJ) and tricellular (TSJ) septate junctions are remodeled throughout completion of cytokinesis in Drosophila epithelia. We report that, following cytokinetic ring constriction, the midbody assembles, matures within SJ and is displaced basally in two phases. In a first slow phase, the neighboring cells remain connected to the dividing cells by means of SJ-containing membrane protrusions pointing to the maturing midbody. Fluorescence recovery after photobleaching (FRAP) experiments revealed that SJ present within the membrane protrusions correspond to the old SJ present prior to cytokinesis. In contrast, new SJ are assembled below the adherens junctions and spread basally to build a new belt of SJ, in a manner analogous to a conveyor belt. Loss-of-function of a core BSJ component, the Na/K-ATPase pump Nervana2 subunit, revealed that the apical-to-basal spread of BSJ drives the basal displacement of the midbody. In contrast, loss of the TSJ protein Bark beetle indicated that remodeling of TSJ is rate limiting, and slowed down midbody migration. In the second phase, once the belt of SJ is assembled, the basal displacement of the midbody is accelerated and ultimately leads to abscission. This last step is temporally uncoupled from the remodeling of SJ. We propose that cytokinesis in epithelia involves the coordinated polarized assembly and remodeling of SJ both in the dividing cell and its neighbors to ensure the maintenance of permeability barrier integrity in proliferative epithelia.