Trends in Cell Biology
ReviewA multicellular view of cytokinesis in epithelial tissue
Section snippets
On the challenges of separating daughter cells in an epithelial tissue
Cytokinesis is the final step of cell division and ensures the physical separation of the two daughter cells after chromosome segregation. In animal cells, the partition of the dividing cell relies on the constriction of an actomyosin contractile ring, which assembles at the division plane and drives the invagination of the cell membrane. Contractile ring assembly is mainly controlled by spindle microtubules, which signal to the cell cortex at early anaphase to create a narrow zone of RhoA
Dividing with and against neighbors
A major aspect to be considered when studying cytokinesis in epithelia is the presence of neighbors. Several works have shown that epithelial cells remain polarized during division and maintain their apical adhesion belt 12, 13, 14, 15, 18, 19. The persistence of cell–cell adhesion implies that the dividing cell remains mechanically coupled to its neighbors during cytokinesis and is consequently subjected to the tension exerted by them. Therefore, the cytokinetic apparatus needs not only to
Cytokinesis and mechanotransduction
An essential property of cells is their ability to respond to mechanical inputs through mechanotransduction pathways. Mechanotransduction is mediated by receptors that sense forces and are able to translate them into biochemical pathways that elicit cellular responses [21]. Mechanotransduction is involved in the control of various processes, ranging from cell fate specification and proliferation to tissue morphogenesis (for a review, see [22]). In epithelial tissues, mechanotransduction has
Asymmetric furrowing in epithelial cells: does it matter?
A commonly observed feature of epithelial cytokinesis is that furrowing occurs asymmetrically. Asymmetric furrowing is characterized by unilateral ingression of the cleavage furrow, from the basal to the apical domain of epithelial cells, resulting in apical midbody formation. This has been observed in several epithelial tissues, such as the mouse intestine 18, 34, polarized monolayers of MDCK cells [19], cultured mouse hepatocytes [35], and, more recently, the Drosophila pupal notum 12, 14,
Role of apical midbody positioning in planar tissue architecture and apical–basal polarity propagation
The recent studies performed in Drosophila epithelial tissues highlighted that the apically positioned midbody acts not only as a platform for cytokinetic abscission, but also as a cue to control planar tissue architecture and the propagation of apical–basal polarity upon cytokinesis. 14, 15 (Figure 4).
Concluding remarks
In conclusion, the recent works performed in Drosophila 12, 13, 14, 15 provide novel insights into epithelial cytokinesis. Remarkably, they highlight that, in epithelial tissues, the cytokinetic machinery serves not only to ensure daughter cell separation, but also to control a series of events that are required for the maintenance of epithelial integrity during proliferation. For instance, the tension generated by the contractile ring favors the formation of a new daughter cell adhesive
Acknowledgments
We apologize to all authors whose primary papers could not be cited because of space constraints. Work in Y.B. lab is supported by the ANR-MorphoDro, ARC, ERC-CePoDro grants as well as funds by the CNRS, the INSERM and the Curie Institute.
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Cited by (38)
Pulsatile contractions promote apoptotic cell extrusion in epithelial tissues
2021, Current BiologyDealing with apical–basal polarity and intercellular junctions: a multidimensional challenge for epithelial cell division
2019, Current Opinion in Cell BiologyCitation Excerpt :During cytokinesis a contractile actomyosin ring constricts until a narrow microtubule-rich bridge, termed midbody, forms between the daughter cells [26]. One almost universal feature of epithelial cytokinesis is that the furrow ingresses asymmetrically from the basal to the apical side ([11,27,28••,29–32]; for review [33,34]). This positions the midbody in the vicinity of the apical junctional complexes, where it then propagates tissue organization (see below).
PP1-Mediated Dephosphorylation of Lgl Controls Apical-basal Polarity
2019, Cell ReportsCitation Excerpt :Simultaneous imaging of Lgl-mCherry with aPKC-GFP shows that Lgl starts localizing to the lateral cortex before apical accumulation of aPKC (Figure 4E, kymographs). This likely results from the basal-to-apical ingression of the cytokinetic furrow, described previously in many epithelia (Herszterg et al., 2014; Morais-de-Sá and Sunkel, 2013). Moreover, Lgl accumulation is completed before aPKC reaches maximum apical levels (Figure 4E, kymographs).
Tricellular junctions: a hot corner of epithelial biology
2018, Current Opinion in Cell BiologyAsymmetric Flows in the Intercellular Membrane during Cytokinesis
2017, Biophysical JournalCitation Excerpt :These cells divide via a pinch-off configuration, where the cell-cell contact area diminishes gradually (5). In contrast, in confined environments such as during embryo development (6,7) and in epithelial tissues (8–10), upon cytokinesis, the daughter cells maintain a finite contact area and form a cell-cell interface consisting of two bilayer membranes, each belonging to one daughter cell (11–13). Formation of the contractile ring and the membrane partition require a supply of actin, myosin, and phospholipids.