Model to Link Cell Shape and Polarity with Organogenesis

Abstract

How do flat sheets of cells form gut and neural tubes? Across systems, several mechanisms are at play: cells wedge, form actomyosin cables, or intercalate. As a result, the cell sheet bends, and the tube elongates. It is unclear to what extent each mechanism can drive tube formation on its own. To address this question, we computationally probe if one mechanism, either cell wedging or intercalation, may suffice for the entire sheet-to-tube transition. Using a physical model with epithelial cells represented by polarized point particles, we show that either cell intercalation or wedging alone can be sufficient and that each can both bend the sheet and extend the tube. When working in parallel, the two mechanisms increase the robustness of the tube formation. The successful simulations of the key features in Drosophila salivary gland budding, sea urchin gastrulation, and mammalian neurulation support the generality of our results.

Polarity Establishment and Maintenance in Ascidian Notochord

“…Polarity plays an important role in coordination of multiple tissue development by controlling tissue mechanical property. For example, when flat cell sheets bundle to form a biological tube, polarity regulates an asymmetry cell wedge or drives cell directional intercalate, leading to the bending movement through the mechanical property change in different parts of the cell flat sheet (Nielsen et al, 2020). Compared with the anatomically complex of vertebrate, Ciona embryonic tail is structurally simple, providing an excellent model to understand how polarity signaling coordinates the multiple tissue development.…”

Mechanisms of vertebrate neural plate internalization

“…Particularly, the recent incorporation of optogenetic technology to control protein activity in time and space appears as an excellent approach to understand the specific biomechanical contribution of CE and AC to neural midline internalization (Krueger et al, 2018). Collectively, the use of extensive live imaging studies as well as the identification of mechanical properties of neural plate cells will result in more compelling computational simulations to model vertebrate neurulation at both cell and tissue levels (Jacobson, 1984;Nielsen et al, 2020).…”

“…excencephaly, Copp et al, 2003). Alternatively, experimental observations and computational modelling has suggested that the interaction of these two collective cell dynamics is both necessary and additive to shape the vertebrate neural plate (Jacobson, 1984;Nielsen et al, 2020). In support of this a recent work in the mouse has shown that both Sroom3 and the PCP pathway (vangl2) genetically interact to enhance vertebrate NTD phenotype (McGreevy et al, 2015).…”

Biophysical models of early mammalian embryogenesis

“…In these models, an implied cell shape can be found as a Voronoi diagram ( Okabe et al., 2009 ). Particle-potential models are typically used for studying cell positioning, or tissue deformation under certain conditions or confinements ( Krupinski et al., 2011 ; Giammona and Campàs, 2021 ; Nielsen et al., 2020 ). Although quick to simulate, these models cannot explicitly represent complex cell deformations ( Tanaka, 2015 ).…”

“…implemented a model where cells are treated as point particles that have a polarity axis. Modifying cell-cell forces to favor a tilt in apical-basal polarities allowed them to mimic cell wedging ( Nielsen et al., 2020 ; Nissen et al., 2018 ).…”