Review
A multicellular view of cytokinesis in epithelial tissue

https://doi.org/10.1016/j.tcb.2013.11.009Get rights and content

Highlights

  • Cytokinesis in epithelial tissues needs to counteract the tension imposed by surrounding epithelial cells.

  • Cytokinetic ring constriction is sensed by neighboring cells and acts as a mechanical signal to remodel AJs.

  • Apical midbody formation on asymmetric or symmetric furrowing regulates the planar and apical–basal organization of epithelia.

  • Cytokinesis in epithelia is a multicellular process.

The study of cytokinesis in single-cell systems provided a wealth of knowledge on the molecular and biophysical mechanisms controlling daughter cell separation. In this review, we outline recent advances in the understanding of cytokinesis in epithelial tissues. These findings provide evidence for how the cytokinetic machinery adapts to a multicellular context and how the cytokinetic machinery is itself exploited by the tissue for the preservation of tissue function and architecture during proliferation. We propose that cytokinesis in epithelia should be viewed as a multicellular process, whereby the biochemical and mechanical interactions between the dividing cell and its neighbors are essential for successful daughter cell separation while defining epithelial tissue organization and preserving tissue integrity.

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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