Topological properties and shape of proliferative and nonproliferative cell monolayers.

Abstract

During embryonic development, structures with complex geometry can emerge from planar epithelial monolayers; studying these shape transitions is of key importance for revealing the biophysical laws involved in the morphogenesis of biological systems. Here, using the example of normal proliferative monkey kidney (COS) cell monolayers, we investigate global and local topological characteristics of this model system in dependence on its shape. The obtained distributions of cells by their valence demonstrate a difference between the spherical and planar monolayers. In addition, in both spherical and planar monolayers, the probability of observing a pair of neighboring cells with certain valences depends on the topological charge of the pair. The zero topological charge of the cell pair can increase the probability for the cells to be the nearest neighbors. We then test and confirm that analogous relationships take place in a more ordered spherical system with a larger fraction of 6-valent cells, namely, in the nonproliferative epithelium (follicular system) of ascidian species oocytes. However, unlike spherical COS cell monolayers, ascidian monolayers are prone to nonrandom agglomeration of 6-valent cells and have linear topological defects called scars and pleats. The reasons for this difference in morphology are discussed. The morphological peculiarities found are compared with predictions of the widely used vertex model of epithelium.