Abstract
BackgroundMorphogenesis of the zebrafish neural tube requires the coordinated movement of many cells in both time and space. A good example of this is the movement of the cells in the zebrafish neural plate as they converge towards the dorsal midline before internalizing to form a neural keel. How these cells are regulated to ensure that they move together as a coherent tissue is unknown. Previous work in other systems has suggested that the underlying mesoderm may play a role in this process but this has not been shown directly in vivo.ResultsHere we analyze the roles of subjacent mesoderm in the coordination of neural cell movements during convergence of the zebrafish neural plate and neural keel formation. Live imaging demonstrates that the normal highly coordinated movements of neural plate cells are lost in the absence of underlying mesoderm and the movements of internalization and neural tube formation are severely disrupted. Despite this, neuroepithelial polarity develops in the abnormal neural primordium but the resulting tissue architecture is very disorganized.ConclusionsWe show that the movements of cells in the zebrafish neural plate are highly coordinated during the convergence and internalization movements of neurulation. Our results demonstrate that the underlying mesoderm is required for these coordinated cell movements in the zebrafish neural plate in vivo.
Highlights
Morphogenesis of the zebrafish neural tube requires the coordinated movement of many cells in both time and space
The later stages of neurulation in teleost embryos are different to other vertebrates in that the neural tube is not formed by folding an epithelial neural plate, rather the teleost neural tube is built by generating a lumen at the center of a solid neural rod primordium
maternal-zygotic one-eyed pinhead (MZoep) embryos have severe defects in neural tube morphogenesis To assess the role of the mesoderm during neural tube formation, we directly compared neuroepithelial organization between wild-type and MZoep embryos, which lack Nodal signaling and mesoderm derivatives in the head [20,21]
Summary
Morphogenesis of the zebrafish neural tube requires the coordinated movement of many cells in both time and space. A good example of this is the movement of the cells in the zebrafish neural plate as they converge towards the dorsal midline before internalizing to form a neural keel How these cells are regulated to ensure that they move together as a coherent tissue is unknown. Morphogenesis of the vertebrate neural tube from the neural plate is a fundamental early step in building the brain and spinal cord This complex process is likely to be coordinated by a combination of mechanisms both intrinsic and extrinsic to the neural tissue itself. One important intrinsic mechanism is the non-canonical Wnt/planar cell polarity (PCP) pathway that regulates the movements of convergent extension to shape the neural plate This pathway is thought to act through cell-cell interactions within the neural plate itself and appears to be a prerequisite for efficient neural tube closure and morphogenesis in all vertebrates (reviewed by Ueno and Greene [1]). A possible role for mesoderm in zebrafish neurulation is suggested by the anterior brain defects in maternal-zygotic one-eyed pinhead (MZoep) mutant embryos, which lack Nodal signaling and anterior mesoderm [19], but a detailed analysis of neural morphogenesis in these mutants is lacking
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