Abstract
Organs are sculpted by extracellular as well as cell-intrinsic forces, but how collective cell dynamics are orchestrated in response to environmental cues is poorly understood. Here we apply advanced image analysis to reveal extracellular matrix-responsive cell behaviors that drive elongation of the Drosophila follicle, a model system in which basement membrane stiffness instructs three-dimensional tissue morphogenesis. Through in toto morphometric analyses of wild type and round egg mutants, we find that neither changes in average cell shape nor oriented cell division are required for appropriate organ shape. Instead, a major element is the reorientation of elongated cells at the follicle anterior. Polarized reorientation is regulated by mechanical cues from the basement membrane, which are transduced by the Src tyrosine kinase to alter junctional E-cadherin trafficking. This mechanosensitive cellular behavior represents a conserved mechanism that can elongate edgeless tubular epithelia in a process distinct from those that elongate bounded, planar epithelia.
Highlights
Organs are sculpted by extracellular as well as cell-intrinsic forces, but how collective cell dynamics are orchestrated in response to environmental cues is poorly understood
Because morphometric measurements can be altered by mounting preparation and by artifacts of imaging plane (e.g. XY slices of cells that have Z orientation in the epithelial plane), complete XYZ images of follicles within a depression slide were captured on a confocal microscope, and analyzed using advanced software including the recently described package ImSAnE7,10 (Fig. 1a–c). lmSAnE detects the surfaces of 3D objects and projects them onto 2D planes to facilitate quantitative analysis and visualization
Mechanical regulation of animal tissues is a current frontier of biology, as quantitative tools and model systems allow interrogation of unappreciated phenomena[32,33,34,35]
Summary
Organs are sculpted by extracellular as well as cell-intrinsic forces, but how collective cell dynamics are orchestrated in response to environmental cues is poorly understood. This degree of elongation is similar to that in paradigmatic morphogenetic systems such as the amphibian neural plate and mesoderm, or the Drosophila germband In the latter tissues, the main cellular behavior that drives elongation is convergent extension, as cells intercalate mediolaterally toward a specific landmark that is defined anatomically and/or molecularly. A gradient of matrix stiffness that is low at the poles and peaks in the organ center provides differential resistance to luminal expansion, leading to tissue elongation Construction of this pattern relies in part on a collective migration of cells around the follicle equatorial axis, leading to global tissue rotation[9]. How the cells of the epithelium respond to stiffness cues and engage in the dynamics that elongate the organ along the anterior-posterior (A–P) axis remains unexplored
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