Scutoids are a geometrical solution to three-dimensional packing of epithelia

Abstract

As animals develop, tissue bending contributes to shape the organs into complex three-dimensional structures. However, the architecture and packing of curved epithelia remains largely unknown. Here we show by means of mathematical modelling that cells in bent epithelia can undergo intercalations along the apico-basal axis. This phenomenon forces cells to have different neighbours in their basal and apical surfaces. As a consequence, epithelial cells adopt a novel shape that we term “scutoid”. The detailed analysis of diverse tissues confirms that generation of apico-basal intercalations between cells is a common feature during morphogenesis. Using biophysical arguments, we propose that scutoids make possible the minimization of the tissue energy and stabilize three-dimensional packing. Hence, we conclude that scutoids are one of nature's solutions to achieve epithelial bending. Our findings pave the way to understand the three-dimensional organization of epithelial organs.

Minimisation of surface energy drives apical epithelial organisation and gives rise to Lewis’ law

“…We sought to test this prediction by artificially creating epithelia with wider apical cell area distributions. To this end, we induced the expression of an RNAi targeting the growth regulator gigas/TSC2 [20] in cell patches randomly located within Drosophila wing discs. gigas attenuation results in larger cells because cells repeat S phase without entering M phase [20].…”

“…To this end, we induced the expression of an RNAi targeting the growth regulator gigas/TSC2 [20] in cell patches randomly located within Drosophila wing discs. gigas attenuation results in larger cells because cells repeat S phase without entering M phase [20]. Indeed, in mosaic gigas/TCS-RNAi wing discs we observe cells with substantially larger apical areas than in the control, scattered throughout the epithelium (Fig.…”

Self-sustained Planar Intercalations due to Mechanosignaling Feedbacks Lead to Robust Axis Extension during Morphogenesis

“…This over-simplification is standard in the field and can possibly provide a plausible, yet basic, understanding of tissue remodeling. However, recent discoveries about the cellular behavior in 3D environments when tissues are subjected to some level of curvature, point towards an intriguing and important role of spatial T1 transitions [50]. In that regard, to what extent the framework presented here depends on the 3D structure of the cells is an interesting subject for further studies.…”

The topology of vitronectin: A complementary feature for neuroblastoma risk classification based on computer‐aided detection

“…The interplay between different fields of basic science has been revealed as an efficient way to advance in medicine. Physics and mathematics‐related terms like tensegrity, topology and tessellations (see Glossary) are now used to improve understanding of biology and biomedicine . In parallel, a robust and efficient analysis of histopathological images is required due to their increasingly accepted use.…”

“…Physics and mathematics-related terms like tensegrity, topology and tessellations (see Glossary) are now used to improve understanding of biology and biomedicine. [1][2][3] In parallel, a robust and efficient analysis of histopathological images is required due to their increasingly accepted use. Image analysis landscape has enormous potential to improve the quality of histological image interpretation, supporting without overruling pathologists in decision-making.…”