Abstract
The internalization of the central nervous system, termed neurulation in vertebrates, is a critical step in embryogenesis. Open questions remain regarding how force propels coordinated tissue movement during the process, and little is known as to how internalization happens in invertebrates. We show that in C. elegans morphogenesis, apical constriction in the retracting pharynx drives involution of the adjacent neuroectoderm. HMR-1/cadherin mediates this process via inter-tissue attachment, as well as cohesion within the neuroectoderm. Our results demonstrate that HMR-1 is capable of mediating embryo-wide reorganization driven by a centrally located force generator, and indicate a non-canonical use of cadherin on the basal side of an epithelium that may apply to vertebrate neurulation. Additionally, we highlight shared morphology and gene expression in tissues driving involution, which suggests that neuroectoderm involution in C. elegans is potentially homologous with vertebrate neurulation and thus may help elucidate the evolutionary origin of the brain.
Highlights
Neurulation is the process which establishes the centralized position of the developing nervous system in vertebrates via involution of the neuroectoderm, with failure resulting in the Neural Tube Defect category of diseases (Gilbert 2000)
We connect the morphogenesis of the pharynx and skin to the internalizing movement of the neurons. We show that this movement involves the involution of a cohesive neuroectoderm layer driven by attachment to the retracting pharynx in a pattern with striking similarity to vertebrate neurulation, and we characterize the role of HMR-1 in establishing inter-tissue attachment and maintaining intra-tissue cohesion over the course of head formation
In order to characterize the process by which the nervous system internalizes in C. elegans, we examine head morphogenesis during the 60-minute time window between the terminal division of the neurons and initial axon outgrowth
Summary
Neurulation is the process which establishes the centralized position of the developing nervous system in vertebrates via involution of the neuroectoderm, with failure resulting in the Neural Tube Defect category of diseases (Gilbert 2000). The neuroectoderm layer bends inwards at its center until it is fully internalized. This physical change is part of a coordinated tissue movement, which requires interaction between the neuroectoderm and adjacent tissues. The floor plate, which generates the pulling force and is required for involution, is derived from a separate tissue despite ending up in the same epithelial layer as the neuroectoderm (Smith 1997). Which factors regulate the interaction between adjacent tissues is a understudied aspect of neurulation
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