Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation

Abstract

Epithelial folding mediated by apical constriction converts flat epithelial sheets into multilayered, complex tissue structures and is employed throughout the development in most animals1. Little is known, however, how forces produced near the apical surface of the tissue are transmitted within individual cells to generate the global changes in cell shape that characterize tissue deformation. Here we apply particle tracking velocimetry in gastrulating Drosophila embryos to measure the movement of cytoplasm and plasma membrane during ventral furrow (VF) formation2, 3. We find that cytoplasmic redistribution during the lengthening phase of VF formation can be precisely described by viscous flows that quantitatively match the predictions of hydrodynamics. Cell membranes move with the ambient cytoplasm, with little resistance to or driving force on the flow. Strikingly, apical constriction produces similar flow patterns in mutant embryos that fail to form cells prior to gastrulation (“acellular” embryos), such that the global redistribution of cytoplasm mirrors the summed redistribution occurring in individual cells of wild type embryos. Our results suggest that during the lengthening phase of VF formation, hydrodynamic behavior of the cytoplasm provides the predominant mechanism transmitting apically generated forces deep into the tissue and that cell individualization is dispensable.

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

“…The early inhibitory effect on cell lengthening can be interpreted as secondary to the inhibition of apical constriction, which is thought to generate intracellular hydrodynamic flows resulting in basal displacement of cytoplasmic content and, given the principle of volume conservation, cell lengthening (He et al , 2014). Importantly, inhibition of apical constriction is not due to a lack of apical myosin‐II accumulation, but rather to an incapability of cells to maintain the constricted state.…”

“…Over the course of the last two decades, the internalization of mesodermal cells during Drosophila melanogaster gastrulation, which is usually referred to as ventral furrow formation, has emerged as a powerful system to dissect the mechanisms controlling tissue invagination (Kolsch et al , 2007; Martin et al , 2009; Mason et al , 2013; Chanet et al , 2017). Both experimental and theoretical work point toward a key role of apical constriction in generating the initial forces necessary to drive invagination (Conte et al , 2009; He et al , 2014; Guglielmi et al , 2015). However, the causal relationship between apical constriction and the subsequent cellular and tissue processes associated with further stages of invagination remains poorly understood.…”

Direct laser manipulation reveals the mechanics of cell contacts in vivo

“…These two timescales can be derived analytically; indeed, one is determined by the friction in the cytosol, whereas the other is given by the viscous component of the cortex constitutive equation. Importantly, both these viscoelastic timescales are under 1 min; neither the experiments nor the model deals with the long-term dynamics (minutes to hours), which presumably imply creep and therefore, fluid-like behavior (9,28).…”

Batchelor Prize Lecture Fluid dynamics at the scale of the cell

“…A second area of interest is within the broad field of developmental biology, where the mechanics and dynamics of tissues have come to be recognized as having hydrodynamic aspects (Ranft et al 2010). Examples of systems in which this has begun to be explored include gastrulation in Drosophila (He et al 2014), where large-scale morphological transformations are driven by cell shape changes. Similar issues arise in the mechanics of embryonic inversion of Volvox Höhn et al 2015).…”