Polarity transitions during neurogenesis and germinal zone exit in the developing central nervous system

Shalini Singh,David J Solecki

doi:10.3389/fncel.2015.00062

Shalini Singh, David J Solecki

Open Access

https://doi.org/10.3389/fncel.2015.00062

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Abstract

During neural development, billions of neurons differentiate, polarize, migrate and form synapses in a precisely choreographed sequence. These precise developmental events are accompanied by discreet transitions in cellular polarity. While radial glial neural stem cells are highly polarized, transiently amplifying neural progenitors are less polarized after delaminating from their parental stem cell. Moreover, preceding their radial migration to a final laminar position neural progenitors re-adopt a polarized morphology before they embarking on their journey along a glial guide to the destination where they will fully mature. In this review, we will compare and contrast the key polarity transitions of cells derived from a neuroepithelium to the well-characterized polarity transitions that occur in true epithelia. We will highlight recent advances in the field that shows that neuronal progenitor delamination from germinal zone (GZ) niche shares similarities to an epithelial-mesenchymal transition. Moreover, studies in the cerebellum suggest the acquisition of radial migration and polarity in transiently amplifying neural progenitors share similarities to mesenchymal-epithelial transitions. Where applicable, we will compare and contrast the precise molecular mechanisms used by epithelial cells and neuronal progenitors to control plasticity in cell polarity during their distinct developmental programs.

Highlights

The developing central nervous system, including the spinal cord, retina and brain, occupies a complex developmental landscape wherein neural stem cells are born and proliferate, differentiate and migrate long distances to form intricate networks, all of which ensure proper CNS functioning
Subsequent symmetric and asymmetric division of the neural stem cells imparts a pseudostratified appearance to neuroepithelium, in which the nuclei undergo interkinetic nuclear migration while the apical-basal surfaces of the cells remain anchored through intercellular junctions (Figure 1A; Haubensak et al, 2004; Götz and Huttner, 2005)
Our understanding of key components and signaling cascades, such as the Par polarity complex and its interplay with adhesion molecules such as cadherins, nectins, claudins and junctional adhesion molecules (JAMs), has advanced considerably (Tsukita and Furuse, 1999; Mizoguchi et al, 2002; Costa et al, 2008; Ishiuchi et al, 2009; Famulski et al, 2010), but some key questions remain, including: What are the specific biological processes that precede delamination? What initiates and controls the switch in polarity and how is this linked to adherens junction (AJ) disassembly? Epithelial cells frequently display polar plasticity through processes known as epithelial-to-mesenchymal transition (EMT) and its reverse, mesenchymal-to-epithelial transition (MET), which developing neurons appear to mirror

Summary

CELLULAR NEUROSCIENCE

Billions of neurons differentiate, polarize, migrate and form synapses in a precisely choreographed sequence. These precise developmental events are accompanied by discreet transitions in cellular polarity. While radial glial neural stem cells are highly polarized, transiently amplifying neural progenitors are less polarized after delaminating from their parental stem cell. Studies in the cerebellum suggest the acquisition of radial migration and polarity in transiently amplifying neural progenitors share similarities to mesenchymal-epithelial transitions. We will compare and contrast the precise molecular mechanisms used by epithelial cells and neuronal progenitors to control plasticity in cell polarity during their distinct developmental programs

INTRODUCTION

Neurogenesis and epithelial mesenchymal transitions