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WIREs Dev Biol
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The cellular and molecular basis of cnidarian neurogenesis

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Neurogenesis initiates during early development and it continues through later developmental stages and in adult animals to enable expansion, remodeling, and homeostasis of the nervous system. The generation of nerve cells has been analyzed in detail in few bilaterian model organisms, leaving open many questions about the evolution of this process. As the sister group to bilaterians, cnidarians occupy an informative phylogenetic position to address the early evolution of cellular and molecular aspects of neurogenesis and to understand common principles of neural development. Here we review studies in several cnidarian model systems that have revealed significant similarities and interesting differences compared to neurogenesis in bilaterian species, and between different cnidarian taxa. Cnidarian neurogenesis is currently best understood in the sea anemone Nematostella vectensis, where it includes epithelial neural progenitor cells that express transcription factors of the soxB and atonal families. Notch signaling regulates the number of these neural progenitor cells, achaete‐scute and dmrt genes are required for their further development and Wnt and BMP signaling appear to be involved in the patterning of the nervous system. In contrast to many vertebrates and Drosophila, cnidarians have a high capacity to generate neurons throughout their lifetime and during regeneration. Utilizing this feature of cnidarian biology will likely allow gaining new insights into the similarities and differences of embryonic and regenerative neurogenesis. The use of different cnidarian model systems and their expanding experimental toolkits will thus continue to provide a better understanding of evolutionary and developmental aspects of nervous system formation. WIREs Dev Biol 2017, 6:e257. doi: 10.1002/wdev.257 This article is categorized under: Gene Expression and Transcriptional Hierarchies > Cellular Differentiation Signaling Pathways > Cell Fate Signaling Comparative Development and Evolution > Organ System Comparisons Between Species
Position of cnidarians in the animal tree of life and phylogenetic diversity within the phylum, with a selection of experimental models used for developmental biology studies. Photo credits: Nematostella vectensis: Chiara Sinigaglia; Clytia hemisphaerica (medusa): Michaël Manuel; Acropora sp.: www.aquaportail.com; Chlorohydra viridissima and Aurelia aurita: Thomas Condamine; Hydractinia echinata: Uri Frank; C. hemisphaerica (polyps): Muriel Jager.
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Neurogenesis in Nematostella embryos and in adult Hydra. (a) In Nematostella, a pool of dedicated neural progenitor cells (NPCs) gives rise to the three major classes of neural cells (sensory cells, ganglion cells, and nematocytes) during embryogenesis. Individual NPCs may give rise to different classes (upper part) or to only one class of neural cells (lower part). Note that the existence of these two types of NPCs is not mutually exclusive. NPCs might be derived from multipotent stem cells, but experimental evidence for such stem cells is missing. Bars above the figure depict the stages at which the indicated genes act during the progression of neurogenesis, according to functional data described in the text (except for NvNCol3 and NvRFa). Notch signaling has a role in regulating the number of NPCs and likely in the differentiation of nematocytes. (b) In adult Hydra, multipotent interstitial stem cells (i‐cells) give rise to the different classes of neural cells, but also to non‐neural cells. As for Nematostella NPCs, the developmental potential of individual i‐cells in vivo is not clear. The generation of neural cells may involve a dedicated NPC. Except for cnox‐2, there are no functional data for the indicated genes.
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Summary of neural gene expression during embryogenesis. Some of the known neural gene expression patterns for Nematostella vectensis (a), Clytia hemisphaerica (b), and Hydractinia echinata (c) are shown. Developmental time progresses from left to right with depicted stage indicated above each image. In all planulae and polyp stages, the images are oriented with oral pole facing up. The orientation of the Clytia tentacle (b, right side) is proximal up and distal down. Note that the expression patterns of CheSox genes are depicted in a simplified manner. CheNgb, neuroglobin.
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Comparative Development and Evolution > Organ System Comparisons Between Species
Gene Expression and Transcriptional Hierarchies > Cellular Differentiation
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