Towards a cellular and molecular understanding of neurulation

Abstract

Neurulation occurs during the early embryogenesis of chordates, and it results in the formation of the neural tube, a dorsal hollow nerve cord that constitutes the rudiment of the entire adult central nervous system. The goal of studies on neurulation is to understand its tissue, cellular and molecular basis, as well as how neurulation is perturbed during the formation of neural tube defects. The tissue basis of neurulation consists of a series of coordinated morphogenetic movements within the primitive streak (e.g., regression of Hensen's node) and nascent primary germ layers formed during gastrulation. Signaling occurs between Hensen's node and the nascent ectoderm, initiating neurulation by inducing the neural plate (i.e., actually, by suppressing development of the epidermal ectoderm). Tissue movements subsequently result in shaping and bending of the neural plate and closure of the neural groove. The cellular basis of the tissue movements of neurulation consists of changes in the behavior of the constituent cells; namely, changes in cell number, position, shape, size and adhesion. Neurulation, like any morphogenetic event, occurs within the milieu of generic biophysical determinants of form present in all living tissues. Such forces govern and to some degree control morphogenesis in a tissue-autonomous manner. The molecular basis of neurulation remains largely unknown, but we suggest that neurulation genes have evolved to work in concert with such determinants, so that appropriate changes occur in the behaviors of the correct populations of cells at the correct time, maximizing the efficiency of neurulation and leading to heritable speciesand axial-differences in this process. In this article, we review the tissue and cellular basis of neurulation and provide strategies to determine its molecular basis. We expect that such strategies will lead to the identification in the near future of critical neurulation genes, genes that when mutated perturb neurulation in a highly specific and predictable fashion and cause neurulation defects, thereby contributing to the formation of neural tube defects.

Folate receptor 1 is necessary for neural plate cell apical constriction during Xenopus neural tube formation

“…Neural plate cells are prominently engaged during neurulation and their change in cell morphology is crucial for shaping of the neural plate and closing of the tube (Colas and Schoenwolf, 2001;Moury and Schoenwolf, 1995;Ossipova et al, 2014;Schoenwolf, 1988;Schoenwolf et al, 1989). We find Folr1 colocalized at the apical membrane of superficial neural plate cells with C-cadherin and β-catenin.…”

Timing and kinetics of E‐ to N‐cadherin switch during neurulation in the avian embryo

“…In the chick, the neural tube is formed by two independent mechanisms involving different morphogenetitc movements and termed primary and secondary neurulations (Colas and Schoenwolf, 2001;Lowery and Sive, 2004). Primary neurulation occurs in the head and upper trunk by rolling of the neural plate and formation of neural folds that then fuse dorsally, resulting in the typical hollow shape of the neural tube.…”

“…In this region, the neural tube derives from the tail bud, a mesenchymal population of cells that coalesce into a rod and transform into an epithelium. The lumen is formed secondarily by cavitation to produce a hollow tube (Colas and Schoenwolf, 2001). …”

Sonic Hedgehog Regulates Integrin Activity, Cadherin Contacts, and Cell Polarity to Orchestrate Neural Tube Morphogenesis

“…In vertebrates, neurulation proceeds as a series of steps by which the neural plate is shaped into a tube that extends along the anteroposterior axis (Colas and Schoenwolf, 2001). Cell division transforms the neural plate from a simple cuboidal into a pseudostratified epithelium in which neural epithelial (NE) cells contact both the basal and the luminal sides.…”