3D viscoelastic drag forces contribute to cell shape changes during organogenesis in the zebrafish embryo

The left-right organizer in zebrafish embryos, Kupffer's Vesicle (KV), is a simple organ that undergoes programmed asymmetric cell shape changes that are necessary to establish the left-right axis of the embryo. We use simulations and experiments to investigate whether 3D mechanical drag forces generated by the posteriorly-directed motion of the KV through the tailbud tissue are sufficient to drive such shape changes. We develop a fully 3D vertex-like (Voronoi) model for the tissue architecture, and demonstrate that the tissue can generate drag forces and drive cell shape changes. Furthermore, we find that tailbud tissue presents a shear-thinning, viscoelastic behavior consistent with those observed in published experiments. We then perform live imaging experiments and particle image velocimetry analysis to quantify the precise tissue velocity gradients around KV as a function of developmental time. We observe robust velocity gradients around the KV, indicating that mechanical drag forces must be exerted on the KV by the tailbud tissue. We demonstrate that experimentally observed velocity fields are consistent with the viscoelastic response seen in simulations. This work also suggests that 3D viscoelastic drag forces could be a generic mechanism for cell shape change in other biological processes.

Automated summary

This study investigates whether 3D mechanical drag forces generated by Kupffer's Vesicle motion through the tailbud tissue are sufficient to drive cell shape changes necessary for establishing the left-right axis in zebrafish embryos. Using simulations and experiments, researchers demonstrate that the tailbud tissue can produce drag forces and drive cell shape changes, and observe velocity gradients around Kupffer's Vesicle consistent with a viscoelastic response. This work suggests that 3D viscoelastic drag forces may be a generic mechanism for cell shape change in various biological processes.