How permeability barrier function is maintained when epithelial cells divide is largely unknown. Here, we have investigated how the bicellular septate junctions (BSJs) and tricellular septate junctions (TSJs) are remodeled throughout completion of cytokinesis in Drosophila epithelia. We report that, following cytokinetic ring constriction, the midbody assembles, matures within SJs, 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 SJs within the membrane protrusions correspond to the old SJs that were present prior to cytokinesis. In contrast, new SJs are assembled below the adherens junctions and spread basally to build a new belt of SJs in a manner analogous to a conveyor belt. Loss of function of a core BSJ component, the Na+/K+-ATPase pump Nervana 2 subunit, revealed that the apical-to-basal spread of BSJs drives the basal displacement of the midbody. In contrast, loss of the TSJ protein Bark beetle indicated that remodeling of TSJs is rate limiting and slowed down midbody migration. In the second phase, once the belt of SJs 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 SJs. We propose that cytokinesis in epithelia involves the coordinated polarized assembly and remodeling of SJs both in the dividing cell and its neighbors to ensure the maintenance of permeability barrier integrity in proliferative epithelia.

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While the molecular mechanisms underlying the abscission of isolated cells are largely decrypted, those of fast-cycling, epithelial progenitors surrounded by epidermal cells (ECs) connected by junctions remain largely unexplored. Here, we investigated the remodeling of the permeability barrier ensured by septate junctions (SJs) during cytokinesis of Drosophila sensory organ precursor (SOP). We report that SOP cytokinesis involves the coordinated polarized assembly and remodeling of SJs in the dividing cell and its neighbors, which remained connected via membrane protrusions pointing toward the SOP midbody. SJs assembly and midbody basal displacement occur more rapidly in SOP than in ECs, leading to a faster disentanglement of the protrusions that precedes midbody release. As reported in isolated cells, the endosomal sorting complex required for transport-III component Shrub/CHMP4B is recruited at the midbody and cell-autonomously regulates abscission. In addition, we found that Shrub is recruited to membrane protrusions, is required for SJ integrity, and that alteration of SJ integrity leads to premature abscission. Our study uncovers cell- intrinsic and -extrinsic functions of Shrub in epithelial abscission to support the coordination of permeability barrier maintenance and abscission in SOPs.