Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing

Abstract

How tissue shape emerges from the collective mechanical properties and behavior of individual cells is not understood. We combine experiment and theory to study this problem in the developing wing epithelium of Drosophila. At pupal stages, the wing-hinge contraction contributes to anisotropic tissue flows that reshape the wing blade. Here, we quantitatively account for this wing-blade shape change on the basis of cell divisions, cell rearrangements and cell shape changes. We show that cells both generate and respond to epithelial stresses during this process, and that the nature of this interplay specifies the pattern of junctional network remodeling that changes wing shape. We show that patterned constraints exerted on the tissue by the extracellular matrix are key to force the tissue into the right shape. We present a continuum mechanical model that quantitatively describes the relationship between epithelial stresses and cell dynamics, and how their interplay reshapes the wing.

DOI: http://dx.doi.org/10.7554/eLife.07090.001

eLife digest

The individual cells in a developing animal embryo organize themselves into tissues with specific and reproducible shapes, which requires the cells to communicate with one another. Cells in tissues exert forces on their neighbors, and respond to being pushed and pulled by the cells around them.

In the fruit fly Drosophila melanogaster, each wing consists mainly of a framework of proteins and other molecules that is built by epithelial cells. These epithelial cells divide and grow during the life of a fly larva, and then reorganize themselves into the shape of the wing after it forms into a pupa. During this reshaping, epithelial cells in some regions of the wing experience powerful contractions. Previous work had suggested that and these forces produced tension in the rest of the wing to pull it into its final elongated shape. But it wasn't clear what exactly these contractions were pulling against to produce the tension. Nor was it understood exactly how wing epithelial cells responded to tension to reorganize themselves into a different wing shape.

Now, Etournay, Popović, Merkel, Nandi et al. have analyzed the forces acting across the entire wing blade and how these forces shape the wing. All cell divisions, cell neighbor exchanges and changes in cell shape in the developing wing blade were tracked under a microscope; this revealed how each one of them contributed to the change in wing shape. Further experiments revealed that localized contractile forces produce tension in the wing because it is connected around its edge to surrounding structures via an extracellular protein called Dumpy. Releasing these contacts, by severing them with a laser or by mutating Dumpy, caused the wing to develop into abnormal shapes, showing that the tension in the wing blade has an important role in determining wing shape. Furthermore, by tracking cells in wings that had been severed by a laser, or mutated for Dumpy Etournay, Popović, Merkel, Nandi et al. could figure out exactly which cellular processes were guided by epithelial tension.

Etournay Popović, Merkel, Nandi et al. also present a theoretical model that describes how the interplay between active force generation and the response of cells to the resulting tension shapes the wings of fruit flies. They propose that epithelial tension provides a mechanism through which cells can communicate with each other to ensure that together the combined behavior of these cells generates reproducible shapes. Further studies are required to analyze how active force generation is patterned and cells sense and respond to external forces during development.

DOI: http://dx.doi.org/10.7554/eLife.07090.002