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

• Published in: Current biology Vol. 28; no. 9; pp. 1380 - 1391.e4
• Main Authors: Daniel, Emeline, Daudé, Marion, Kolotuev, Irina, Charish, Kristi, Auld, Vanessa, Le Borgne, Roland
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 07.05.2018; Elsevier
• Subjects: adherens junctions; Cellular Biology; cytokinesis; Drosophila; epithelial cells; Life Sciences; live imaging; paracellular diffusion barrier; scanning face block electron microscopy; septate junctions; Subcellular Processes; transmission electron microscopy; tricellular junctions; live imaging; tricellular junctions; cytokinesis; Drosophila; scanning face block electron microscopy; epithelial cells; paracellular diffusion barrier; transmission electron microscopy; septate junctions; adherens junctions; Paracellular Diffusion Barrier; Scanning Face Block Electron Microscopy; Septate Junctions; Transmission Electron Microscopy Manuscript; Epithelial Cells; Live Imaging; Cytokinesis; Tricellular Junctions
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2018.03.034

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. •Permeability barrier function is preserved throughout epithelial cytokinesis•Dividing cells remains connected to their neighbors at the level of the midbody•Septate junctions (SJs) are assembled de novo apically and outspread basally•Assembly of SJs regulates the basal displacement of the midbody Using live imaging and electron microscopy of Drosophila epithelia, Daniel et al. investigate how septate junctions are remodeled during cytokinesis and show that it is a multicellular process relying on the interplay between dividing cells and their neighbors, thereby ensuring the maintenance of permeability barrier function.