Neuronal differentiation influences progenitor arrangement in the vertebrate neuroepithelium.

Pilar Guerrero,Ruben Perez-Carrasco,Karen M Page,James Briscoe,Marcin Zagorski,Anna Kicheva,David Page

doi:10.1242/dev.176297

Abstract

ABSTRACTCell division, movement and differentiation contribute to pattern formation in developing tissues. This is the case in the vertebrate neural tube, in which neurons differentiate in a characteristic pattern from a highly dynamic proliferating pseudostratified epithelium. To investigate how progenitor proliferation and differentiation affect cell arrangement and growth of the neural tube, we used experimental measurements to develop a mechanical model of the apical surface of the neuroepithelium that incorporates the effect of interkinetic nuclear movement and spatially varying rates of neuronal differentiation. Simulations predict that tissue growth and the shape of lineage-related clones of cells differ with the rate of differentiation. Growth is isotropic in regions of high differentiation, but dorsoventrally biased in regions of low differentiation. This is consistent with experimental observations. The absence of directional signalling in the simulations indicates that global mechanical constraints are sufficient to explain the observed differences in anisotropy. This provides insight into how the tissue growth rate affects cell dynamics and growth anisotropy and opens up possibilities to study the coupling between mechanics, pattern formation and growth in the neural tube.

Highlights

The mechanisms that control the arrangement of cells in developing tissues involve both molecular and mechanical processes that spatially and temporally coordinate the division, shape, displacement and differentiation of cells
Cell geometry in the mouse neuroepithelium To construct a mechanical model of neural tube growth we first measured key features of neural progenitor organisation in the mouse embryonic neural tube
There were some differences in the mean and variance of cell areas and perimeters in the samples (Fig. 1C), which were most noticeable at E10.5, when the rate of neuronal differentiation is highest in the pMN (Kicheva et al, 2014)

Summary

Introduction

The mechanisms that control the arrangement of cells in developing tissues involve both molecular and mechanical processes that spatially and temporally coordinate the division, shape, displacement and differentiation of cells. In the Drosophila wing imaginal disc a combination of experimental observations, quantitative image analysis and computational modelling have revealed the global patterns of mechanical tension that affect the final size and shape of the wing These patterns result from spatial differences in proliferation, cell shape, division orientation and exchange of neighbouring cells (Shraiman, 2005; Aegerter-Wilmsen et al, 2010; Aigouy et al, 2010; LeGoff et al, 2013; Mao et al, 2013; Guirao et al, 2015; Kursawe et al, 2015; Dye et al, 2017), as well as external mechanical constraints, such as the attachment of the wing blade to the contracting wing hinge (Aigouy et al, 2010; Sugimura and Ishihara, 2013; Etournay et al, 2015; Ray et al, 2015). Wing morphogenesis is influenced by planar-polarity signalling, which influences the apical geometry of cells and the orientation of cell division (Aigouy et al, 2010; Mao et al, 2011)

Objectives

Methods

Results

Conclusion