Scutoids: Understanding the 3D Packing of Curved Epithelia

Abstract

During development metazoa are shaped into complex 3D structures. This process is achieved using epithelial cells as building blocks. Thus, driven by internal/external stimuli, epithelial cells adopt a variety of shapes that affect their packing and the properties of the tissue and its morphology. In this context, the accepted view was that when tissues bend, cells change theirs shape from columnar (prism) to a “bottle shape” (frustum) hence assuming that the 3D packing properties remain unchanged along the apicobasal axis. In order to characterize and investigate the 3D packing and the shapes of cells in curved epithelia we mimicked computationally the architecture of tissues using computational geometry methods (Voronoi tessellation). To confirm the predictions of our model, we have investigated by microscopy means the 3D packing of the salivary gland of Drosophila (a model extensively used for tubulogenesis) as well as other tissues in different organisms. Finally, we have also developed a theoretical model based on energetic considerations to understand the biophysical origin of the 3D cellular organization. Our computational model predicts, and our experiments confirm, that, as the curvature of the tissue increases, prisms and frusta are not the only cell shapes that develop and reveals a previously undescribed geometrical shape: the scutoid. As a consequence, the apical and basal surfaces may have different packing topologies showing a neighbor interchange between cells along their apicobasal. Our energetics analysis reveals that scutoids allow tissues to minimize the packing energy and we propose that such geometrical shape is nature's solution to epithelial bending. 1) Scutoids are a geometrical solution to three-dimensional packing of epithelia, P. Gómez-G〈lvez et al., Nature Communications 9, 2960 (2018). 2) A 3D cell shape that enables tube formation, G. Blanchard, Nature 561, 182 (2018)