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Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation
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Journal Article
Apical constriction drives tissue-scale hydrodynamic flow to mediate cell elongation
2014
Overview
The lengthening phase of ventral furrow formation in
Drosophila
gastrulation is driven by cytoplasmic flows triggered by apical constriction of mesoderm cells independent of the mechanical inputs from the basolateral membranes.
A role for viscosity on cellular morphogenesis
Using
Drosophila
gastrulation as a model, Eric Wieschaus and colleagues have studied the respective contributions of cortical cellular forces and cytoplasmic viscous forces to the generation of complex three-dimensional morphogenetic processes. They found that the lengthening phase in furrow formation is driven by cytoplasmic flows triggered by apical constriction of mesoderm cells, and that cell individualization is dispensable. These findings favour a viscous component in morphogenesis, rather than one based solely on mechanical inputs from cell membranes.
Epithelial folding mediated by apical constriction converts flat epithelial sheets into multilayered, complex tissue structures and is used throughout development in most animals
1
. Little is known, however, about 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 formation
2
,
3
. We find that cytoplasmic redistribution during the lengthening phase of ventral furrow 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 before gastrulation (‘acellular’ embryos), such that the global redistribution of cytoplasm mirrors the summed redistribution occurring in individual cells of wild-type embryos. Our results indicate that during the lengthening phase of ventral furrow formation, hydrodynamic behaviour of the cytoplasm provides the predominant mechanism transmitting apically generated forces deep into the tissue and that cell individualization is dispensable.
Publisher
Nature Publishing Group UK,Nature Publishing Group
