Both neural crest cells and placodes arose around the same time during evolution, generate some similar cell types sensory neurons , and a portion of these cells possess migratory properties. Furthermore, as described above, these cells in the invertebrate chordate lateral non-neural ectoderm or the neural ectoderm express transcription factors homologous to the neural crest progenitors and pre-placodal domain.
This raises the question of whether basal chordates or early vertebrates possessed a hybrid neural border cell population, a common ancestral cell type to neural crest and pre-placodal progenitors reviewed in Schlosser, Comparative studies across the evolutionary spectrum can also shed light on the role of signaling pathways and transcription factors for cell type-specific development. For example, single cell RNA- and ATAC-sequencing of mammalian hair cells and the ciliated primary sensory cells of the ascidians could compare the transcriptomic and epigenomic regulation of fate specification in the two taxa.
Another unaddressed question that has been debated for several decades is whether neural crest cells and the pre-placodal domain share a common evolutionary origin. Fine signaling pathway or transcription factor misexpressing easily transforms one cell type to another as demonstrated, for example, in tunicate embryos in Horie et al. A detailed review by Schlosser , however, argues against this, since the neural crest cells are specified and migrate from the neural plate border before the placodes, and many cell fates are exclusive to each of the lineages — only neural crest cells make bone and cartilage, while only placodes form specialized mechano- or chemoreceptive sensory cells.
For further evidence for the interplay of these gene regulatory networks, we need a comprehensive comparison of active, repressed, and accessible genome loci across the two neural plate border lineages during late gastrulation and early neurulation stages. The question remains as to what mechanisms localized the proto-neural plate border gene regulatory network to the edge of the neural plate during evolution.
Many such questions remain to be explored in the field of early ectodermal patterning in chordates and with the emergence of novel tools to probe gene expression and regulation at the single cell level, we can continue to piece together the mystery of neural plate border induction, specification, and lineage commitment.
Many questions in the field of neural plate border development remain to be addressed. How do cells segregate from pluripotential epiblast cells to one of four lineages; each remaining multipotent but nonetheless distinct and restricted in their fates from the other lineages?
Do the neural crest progenitors and pre-placodal ectoderm arise from a common pool of cells at the border region in a hybrid stage, or do they come from the neural and non-neural ectoderm respectively? Is the chromatin conformation of the border irreversible at early developmental stages when the first neural crest cell or pre-placodal marker expression is observed, or does it remain plastic?
Do neural crest cells retain some or all aspects of pluripotency? How similar are the cell types that originate in the non-neural ectoderm adjacent to the neural plate in protochordates to those in vertebrates that generate sensory patches and organs? To address these questions, we need to follow the transcriptomic and epigenomic states of cells at the neural plate border in the medial-lateral as well as anterior-posterior axes. Embryonic cellular maps are difficult to construct due to the rapidly changing nature of embryonic tissue, unlike the atlases of adult organs.
Histochemical methods can only reveal spatial expression of certain known genes and proteins in the organism, with further limitations pertaining to lack of cross-species utility of those tools. Introduction of single cell sequencing techniques in the last decade has finally made it possible to observe a more holistic picture of a developing cell and its state at a particular point in embryonic time. Single-cell level transcriptomic, epigenomic, and other sequencing techniques provide the necessary apparatuses to capture the dynamic state of the developing embryo to track lineages, observe fate specification, and study the multipotency of the differentiating cells.
Several recent studies present a comprehensive atlas of different cell types of the developing mouse embryos pre-gastrulation Mohammed et al. Statistical clustering of single cells can be used to discover previously unidentified or non-distinct cell populations as well as observe detailed similarities and differences in the transcriptional states of known cell types.
Molecular maps of cell lineage induction and specification can be gathered by profiling the tissue of interest from multiple ages simultaneously, which can further help to understand the gene regulatory networks involved. For example, Pijuan-Sala et al. A similar analysis in tunicate embryos permitted virtual lineage tracing of the nervous system. This transcriptomic study revealed molecular similarities between the vertebrate telencephalon and the anterior domain of the tunicate embryo palp sensory cells and anterior sensory vesicle supporting the idea that protochordate ectodermal gene regulatory modules must have evolved to expand the vertebrate forebrain Cao et al.
It will be possible to compare the transcriptomic profile of bipolar tail neurons, atrial siphon primordium, oral siphon primordium, and palp organs with vertebrate transcriptomes of crest and placode derivatives to comprehensively explore the parallels between vertebrate and protochordate neural plate border ectoderm development.
As a complement to single cell RNA sequencing, multi-color imaging methods like RNAscope or in situ Hybridization Chain Reaction can be used to record and validate spatial expression of key genetic variations observed in cell clustering Choi et al. The neural plate border region of the chordates is only a few cells thick and techniques like Slide-seq and MERFISH may be able to give higher resolution spatial information of the cellular transcriptome during border development Chen et al.
While the former method transfers single cell thick tissue sections onto a single cell RNA sequencing grid Rodriques et al. Depending on the cellular resolution of these techniques, they may be useful for parsing out the cellular identities at the neural plate border region where the four ectodermal lineages are intermingled over just a few cell diameters. For instance, although WNT, BMP, and FGF signaling are important for neural crest progenitors and pre-placodal domain patterning, far less is known of the fine-tuned signaling levels and subsequent cascade of downstream molecules that specify these cell fates.
Single cell RNA sequencing techniques can elaborate upon the levels of signaling and expression of respective downstream effectors to delve deeper into the signaling pathway interactions at the neural plate border. Advances in transgenic animal models, CRISPR technology, and high-resolution live imaging of fluorescent reporter of cell signaling can help us visualize signaling spatiotemporally.
Ideally, we would want to interrogate the expression levels and cell state of every cell in an embryo at a chosen state of development and be able to track each individual cell through time and space. Although it is enough to cluster the single cells identified, the studies may give an incomplete picture of the transitional states due to insufficient sequencing depth. With the realistic limitations of the technology, integrating databases across published studies can help us trace the lineage of cell clusters along the developmental timeline Tam and Ho, Alternatively, higher sensitivity but lower throughput techniques, such as MATQ-seq and SMARTer-seq, can detect a higher number of genes per cell and are useful for a deeper transcriptomic analysis of single cells Sheng et al.
In addition to the transcriptomic status of the cells at the developing neural plate border region, it remains to be addressed when the cells are fully committed to a lineage. Epigenomic sequencing analysis, such as ATAC-seq, can identify accessible genomic loci available for transcriptional activity. Using this data, we can identify relevant enhancers for lineage specific transcription factors and evaluate plasticity of the cells, whether trans-differentiation is feasible from one ectodermal path to another.
Their data show that FoxD3 binds to cis-regulatory elements for neural crest specifier genes as an activator, and at later stages, represses mesenchymal and migratory programs to prevent premature differentiation Lukoseviciute et al.
Yet another transcription factor, AP2 or TFAP2 has been shown to play a dual role in activating neural crest induction genes Pax , Zic , and Msx and, at a later stage of development, neural crest specification genes FoxD and Sox The ability to interrogate the gene expression, histones, nucleosome availability, and more recently, genome occupancy is finally shedding light on the role of such key transcription factors and signaling cascades for ectodermal patterning to generate and specify distinct lineages.
AT and AG wrote and edited the manuscript together. Both the authors contributed to the article and approved the submitted version. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. We thank our colleagues in the neural crest and placode field for many interesting discussions over the years that spurred ideas in this review, and we apologize for omission of many articles from the review for reasons of space.
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At the cranial end the neural plate is wider and consists of the region where the brain will arise. At the caudal end it is narrower and gives rise to the spinal cord. The neural plate develops in step with the genesis of the notochord, i.
The induction process is very complex, but has its origin in the secretion of inducing factors by axial mesoderm cells. These factors diffuse in the direction of the ectoderm cells that lie above them where they activate genes that are responsible for the differentiation of epithelium that has come from the ectoderm into several rows of prismatic epithelium: the neuroectoblast.
In the course of the 3rd week the edges of the neural plate rise up and become neural folds 9 , enclosing the neural groove 8. The caudal end is narrower; there the spinal cord will form.
The neural folds approach each other after the 25th day and merge to form the neural tube delimitating the future central canal, which is coated with ependymal cells. The closure of the neural tube begins in the cervical area in the middle of the embryo and extends from there in both the cranial and caudal directions.
The anterior neuropore cranial closes itself on the 29th day The posterior neuropore caudal closes a day later The top of the anterior neuropore corresponds to the terminal lamina of the adult brain and the posterior neuropore to the terminal filum at the end of the spinal cord.
If the posterior neuropore does not close, a spina bifida occurs. Edit article. View revision history Report problem with Article. Citation, DOI and article data. Peterson, M. Neural plate. Reference article, Radiopaedia. Central Nervous System. URL of Article. Related pathology Failure of neural tube closure in early pregnancy can result in neural tube defects , one of the commonest and most severe malformations of the fetus and newborn 1,2. Vishram Singh. Textbook of Clinical Embryology.
Gary C. Schoenwolf, Steven B. Bleyl, Philip R. Brauer, Philippa H. Larsen's Human Embryology E-Book. Bruce M.
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