Epithelial colonies in vitro elongate through collective effects.

Jordi Comelles,S Anvitha,Daniel Riveline,Soumya Ss,Linjie Lu,Emilie Le Maout,Frank Jülicher,Guillaume Salbreux,Mandar M Inamdar

doi:10.7554/elife.57730

Abstract

Epithelial tissues of the developing embryos elongate by different mechanisms, such as neighbor exchange, cell elongation, and oriented cell division. Since autonomous tissue self-organization is influenced by external cues such as morphogen gradients or neighboring tissues, it is difficult to distinguish intrinsic from directed tissue behavior. The mesoscopic processes leading to the different mechanisms remain elusive. Here, we study the spontaneous elongation behavior of spreading circular epithelial colonies in vitro. By quantifying deformation kinematics at multiple scales, we report that global elongation happens primarily due to cell elongations, and its direction correlates with the anisotropy of the average cell elongation. By imposing an external time-periodic stretch, the axis of this global symmetry breaking can be modified and elongation occurs primarily due to orientated neighbor exchange. These different behaviors are confirmed using a vertex model for collective cell behavior, providing a framework for understanding autonomous tissue elongation and its origins.

Highlights

Tissue elongation is a central morphogenetic event occurring in many organisms during development (Lecuit and Lenne, 2007; Guillot and Lecuit, 2013), such as Drosophila orC. elegans
Our results reinforce the idea that cell elongation nematic field, which could only arise from collective interaction between cells, can have an impact on epithelial morphogenesis
Our results show that cell elongation nematic field can have an impact on epithelia morphogenesis

Summary

Introduction

Tissue elongation is a central morphogenetic event occurring in many organisms during development (Lecuit and Lenne, 2007; Guillot and Lecuit, 2013), such as Drosophila orC. elegans. While the phenomenon is known to involve remodeling of adherens junctions (Rauzi, Lenne and Lecuit, 2010) and acto-myosin (He et al, 2010; Rauzi, Lenne and Lecuit, 2010) at the molecular level, mesoscopic mechanisms leading to distinct morphogenesis processes are poorly understood This is partly because inputs from morphogen gradients (Gilmour, Rembold and Leptin, 2017) or from neighboring tissues (Zhang et al, 2011; Etournay et al, 2015) can affect tissue autonomous selforganization in vivo. It appears important to characterize elongation in an in vitro system where the epithelial tissue undergoes shape transition autonomously

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Conclusion