Reconstructing 3D deformation dynamics for curved epithelial sheet morphogenesis from positional data of sparsely-labeled cells

Ken-Ichi Hironaka,Yoshihiro Morishita,Daisuke Ohtsuka,Takashi Jin,Sang-Woo Lee

doi:10.1038/s41467-017-00023-7

Ken-Ichi Hironaka, Yoshihiro Morishita + Show 3 more

Open Access

https://doi.org/10.1038/s41467-017-00023-7

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Abstract

Quantifying global tissue deformation patterns is essential for understanding how organ-specific morphology is generated during development and regeneration. However, due to imaging difficulties and complex morphology, little is known about deformation dynamics for most vertebrate organs such as the brain and heart. To better understand these dynamics, we propose a method to precisely reconstruct global deformation patterns for three-dimensional morphogenesis of curved epithelial sheets using positional data from labeled cells representing only 1–10% of the entire tissue with limited resolution. By combining differential-geometrical and Bayesian frameworks, the method is applicable to any morphology described with arbitrary coordinates, and ensures the feasibility of analyzing many vertebrate organs. Application to data from chick forebrain morphogenesis demonstrates that our method provides not only a quantitative description of tissue deformation dynamics but also predictions of the mechanisms that determine organ-specific morphology, which could form the basis for the multi-scale understanding of organ morphogenesis.

Highlights

Quantifying global tissue deformation patterns is essential for understanding how organspecific morphology is generated during development and regeneration
As an actual biological target, we apply this method to morphogenesis during early development of the chick forebrain from somite stage (SS) 5 to SS13; SS5 corresponds to the very beginning of optic vesicle (OV) formation from a simple neural tube and at SS13 a fully evaginated OV and overall more complex morphology is present (Fig. 1)
In the case of forebrain morphogenesis, the neuroepithelial sheet maintains a single layer of columnar cells of almost uniform height throughout each developmental stage from SS5 to SS13 (Fig. 1e and Supplementary Fig. 7C, and see Supplementary Fig. 7A, B for methods on measuring cell height or tissue thickness)

Summary

Introduction

Quantifying global tissue deformation patterns is essential for understanding how organspecific morphology is generated during development and regeneration. Due to imaging difficulties and complex morphology, little is known about deformation dynamics for most vertebrate organs such as the brain and heart To better understand these dynamics, we propose a method to precisely reconstruct global deformation patterns for three-dimensional morphogenesis of curved epithelial sheets using positional data from labeled cells representing only 1–10% of the entire tissue with limited resolution. As will be described below, the 2D coordinate system and metric is, in general, different at each developmental time point with differing morphology, making it difficult to perform ordinary velocimetric analysis Against this background, we propose a method to reconstruct tissue deformation dynamics for 3D morphogenesis of curved epithelial sheets from a small set of positional cellular data with limited resolution. Our analysis provides quantitative descriptions of tissue deformation dynamics and enables the prediction or narrowing of mechanisms that determine organ-specific morphology, which could form the basis for multi-scale understanding of organ morphogenesis

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Conclusion