Cell size and polarization determine cytokinesis furrow ingression dynamics in mouse embryos

Significance

The final step of cell division, termed cytokinesis, comprises the constriction of a furrow that divides the cytoplasm to form two daughter cells. Although cytokinesis is well studied in traditional cell systems, how cytokinesis is regulated in complex multicellular settings and during cell-fate decisions is less well understood. Here, using live imaging and physical and molecular interventions, we find that the emergence of cell polarity during mouse embryo morphogenesis dramatically impacts cytokinesis mechanisms. Specifically, the assembly of the apical domain in outer cells locally inhibits the cytokinetic machinery, leading to an unexpected laterally biased cytokinesis.

Abstract

Cytokinesis is the final step of cell division during which a contractile ring forms a furrow that partitions the cytoplasm in two. How furrow ingression is spatiotemporally regulated and how it is adapted to complex cellular environments and developmental transitions remain poorly understood. Here, we examine furrow ingression dynamics in the context of the early mouse embryo and find that cell size is a powerful determinant of furrow ingression speed during reductive cell divisions. In addition, the emergence of cell polarity and the assembly of the apical domain in outer cells locally inhibits the recruitment of cytokinesis components and thereby negatively regulates furrow ingression specifically on one side of the furrow. We show that this biasing of cytokinesis is not dependent upon cell–cell adhesion or shape but rather is cell intrinsic and is caused by a paucity of cytokinetic machinery in the apical domain. The results thus reveal that in the mouse embryo cell polarity directly regulates the recruitment of cytokinetic machinery in a cell-autonomous manner and that subcellular organization can instigate differential force generation and constriction speed in different zones of the cytokinetic furrow.