Development of a New 3D Hybrid Model for Epithelia Morphogenesis

Abstract

Many epithelial developmental processes like cell migration and spreading, cell sorting, or T1 transitions can be described as planar deformations. As such, they can be studied using two-dimensional tools and vertex models that can properly predict collective dynamics. However, many other epithelial shape changes are characterized by out-of-plane mechanics and three-dimensional effects, such as bending, cell extrusion, delamination, or invagination. Furthermore, during planar cell dynamics or tissue repair in monolayers, spatial intercalation between the apical and basal sides has even been detected. Motivated by this lack of symmetry with respect to the midsurface, we here present a 3D hybrid model that allows us to model differential contractility at the apical, basal or lateral sides. We use the model to study the effects on wound closure of solely apical or lateral contractile contributions and show that an apical purse-string can be sufficient for full closure when it is accompanied by volume preservation.

Cell Centred Finite Element Model for Intestinal Organoids Shape Analysis: From tissue architecture to mechanics

“…All together these results confirm the flexibility of our FEM formulation to create complex deformation. This was the case with previous vertex models allowing to create high deformations for morphogenetic events [4,55] or artificial tissues [14,39,56] without using FEM analytic power. FEM interest in biology is not new, FEM was previously used to model morphomecanic at a meso-scale level [57] and FEM was recently implemented on a nice platform for quantifying plant morphogenesis in 2.5D, MorphoGraphX, that can be used for image analysis, and using surface elements [58].…”

The complex three-dimensional organization of epithelial tissues

“…On the other hand, the parametrization and calibration of in silico models must be consistent with those force estimations. Fortunately, recent results seem to suggest that realistic 3D tissue organizational traits, such as the scutoidal shapes, can be reproduced in force-driven models without implementing excessive complexity (Okuda et al, 2019;Ioannou et al, 2020). This will facilitate the exploration of dynamical phenomena in the near future, because apico-basal intercalations also appear to be involved in active cell movements, such as the Drosophila germ band extension, egg chamber rotation or the early morphogenesis of salivary glands (Gómez-Gálvez et al, 2018;Sanchez-Corrales et al, 2018;Sun et al, 2017).…”

“…GFI) with enough complex elements to generate the observed self-organization in tissues containing complex cellular geometries. Some recent promising results have been presented by Ioannou and colleagues, who have proposed a methodology that accounts for the reported asymmetries between apical and basal surfaces, and have applied it to study wound healing (Ioannou et al, 2020).…”

Junctional and cytoplasmic contributions in wound healing

“…Differences in apical and basal progression of closure and reduction of tissue height at the wound front may reveal three-dimensional effects on the mechanisms described here. Although some three-dimensional extensions of the vertex model presented here can be found in [27], with distinct intercalations in the apical and basal surface, this reference does not provide any energy analysis or inspection of the tissue fluidity. Further extension of our study to three-dimensional vertex models is under progress.…”

“…In addition to the absence of detailed experimental measurements of intercalation along the tissue height, this reduction is also motivated by the simplicity of our resulting energy analysis. Some works have attempted to take into account the imbalance between lateral, basal and apical junctions in tissue folding [26] and wound healing [27]. However, they do not inspect the fluidity of the tissue and intercalation rates, which is one of our main purposes in the present work.…”