Passive Mechanical Forces Control Cell-Shape Change during Drosophila Ventral Furrow Formation

Abstract

During Drosophila gastrulation, the ventral mesodermal cells constrict their apices, undergo a series of coordinated cell-shape changes to form a ventral furrow (VF) and are subsequently internalized. Although it has been well documented that apical constriction is necessary for VF formation, the mechanism by which apical constriction transmits forces throughout the bulk tissue of the cell remains poorly understood. In this work, we develop a computational vertex model to investigate the role of the passive mechanical properties of the cellular blastoderm during gastrulation. We introduce to our knowledge novel data that confirm that the volume of apically constricting cells is conserved throughout the entire course of invagination. We show that maintenance of this constant volume is sufficient to generate invagination as a passive response to apical constriction when it is combined with region-specific elasticities in the membranes surrounding individual cells. We find that the specific sequence of cell-shape changes during VF formation is critically controlled by the stiffness of the lateral and basal membrane surfaces. In particular, our model demonstrates that a transition in basal rigidity is sufficient to drive VF formation along the same sequence of cell-shape change that we observed in the actual embryo, with no active force generation required other than apical constriction.

Downregulation of basal myosin‐ II is required for cell shape changes and tissue invagination

“…The later effects of basal myosin‐II up‐regulation on cell shortening can also be interpreted in the context of volume conservation and are consistent with the cell shape changes predicted by the region elasticity theory of cell membranes (Polyakov et al , 2014). According to this model, the elastic energy that accumulates during cell lengthening in the lateral membrane is released during basal relaxation causing cell shortening and invagination.…”

“…These stereotypic changes in cell morphology might reflect complex intracellular regulations, for example, of membrane and microtubule dynamics, or alternatively, passive response to apical constriction, as suggested by a recent computer simulation study (Polyakov et al , 2014). According to this model, which is based on region‐specific elasticity of cell membranes, during the initial stages of ventral furrow invagination, apical constriction causes viscous hydrodynamic flows of the cytoplasm and movement of nuclei toward the base.…”

Actomyosin-based tissue folding requires a multicellular myosin gradient

“…This is not the case in vivo, where apical constriction initially results in cells lengthening along their apicalbasal axis, followed by shortening along same axis (Sweeton et al, 1991). This final shortening step is associated with the generation of the highest curvature (Polyakov et al, 2014). Given that our model successfully predicts several experimental observations, the concept that a given magnitude of apical contractility generates a local preferred curvature of the surface of a shell provides a useful framework with which to understand tissue folding.…”

“…Our mechanical model differs from previous models of Drosophila gastrulation. It represents the first 3D continuum model of ventral furrow formation in which apical constriction is the only active force input into the system (Conte et al, 2009;Conte et al, 2008;Odell et al, 1981;Polyakov et al, 2014;Spahn and Reuter, 2013). In particular, our theoretical analysis implies the role of active myosin gradients in tissue bending.…”

Optogenetic control of morphogenesis goes 3D

“…Just such a disassembly of basal contractile actomyosin has been visualised during ventral furrow formation (Sweeton et al , 1991; Dawes‐Hoang et al , 2005). However, whether basal relaxation is truly necessary for folding remained unclear, as some models point to basal relaxation as a passive consequence of apical constriction (Polyakov et al , 2014). …”