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A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian
Neurogenesis is the generation of neurons from stem cells, a process that is regulated by SoxB transcription factors (TFs) in many animals. Although the roles of these TFs are well understood in bilaterians, how their neural function evolved is unclear. Here, we use Hydractinia symbiolongicarpus, a...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9173746/ https://www.ncbi.nlm.nih.gov/pubmed/35608899 http://dx.doi.org/10.7554/eLife.78793 |
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author | Chrysostomou, Eleni Flici, Hakima Gornik, Sebastian G Salinas-Saavedra, Miguel Gahan, James M McMahon, Emma T Thompson, Kerry Hanley, Shirley Kilcoyne, Michelle Schnitzler, Christine E Gonzalez, Paul Baxevanis, Andreas D Frank, Uri |
author_facet | Chrysostomou, Eleni Flici, Hakima Gornik, Sebastian G Salinas-Saavedra, Miguel Gahan, James M McMahon, Emma T Thompson, Kerry Hanley, Shirley Kilcoyne, Michelle Schnitzler, Christine E Gonzalez, Paul Baxevanis, Andreas D Frank, Uri |
author_sort | Chrysostomou, Eleni |
collection | PubMed |
description | Neurogenesis is the generation of neurons from stem cells, a process that is regulated by SoxB transcription factors (TFs) in many animals. Although the roles of these TFs are well understood in bilaterians, how their neural function evolved is unclear. Here, we use Hydractinia symbiolongicarpus, a member of the early-branching phylum Cnidaria, to provide insight into this question. Using a combination of mRNA in situ hybridization, transgenesis, gene knockdown, transcriptomics, and in vivo imaging, we provide a comprehensive molecular and cellular analysis of neurogenesis during embryogenesis, homeostasis, and regeneration in this animal. We show that SoxB genes act sequentially at least in some cases. Stem cells expressing Piwi1 and Soxb1, which have broad developmental potential, become neural progenitors that express Soxb2 before differentiating into mature neural cells. Knockdown of SoxB genes resulted in complex defects in embryonic neurogenesis. Hydractinia neural cells differentiate while migrating from the aboral to the oral end of the animal, but it is unclear whether migration per se or exposure to different microenvironments is the main driver of their fate determination. Our data constitute a rich resource for studies aiming at addressing this question, which is at the heart of understanding the origin and development of animal nervous systems. |
format | Online Article Text |
id | pubmed-9173746 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-91737462022-06-08 A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian Chrysostomou, Eleni Flici, Hakima Gornik, Sebastian G Salinas-Saavedra, Miguel Gahan, James M McMahon, Emma T Thompson, Kerry Hanley, Shirley Kilcoyne, Michelle Schnitzler, Christine E Gonzalez, Paul Baxevanis, Andreas D Frank, Uri eLife Developmental Biology Neurogenesis is the generation of neurons from stem cells, a process that is regulated by SoxB transcription factors (TFs) in many animals. Although the roles of these TFs are well understood in bilaterians, how their neural function evolved is unclear. Here, we use Hydractinia symbiolongicarpus, a member of the early-branching phylum Cnidaria, to provide insight into this question. Using a combination of mRNA in situ hybridization, transgenesis, gene knockdown, transcriptomics, and in vivo imaging, we provide a comprehensive molecular and cellular analysis of neurogenesis during embryogenesis, homeostasis, and regeneration in this animal. We show that SoxB genes act sequentially at least in some cases. Stem cells expressing Piwi1 and Soxb1, which have broad developmental potential, become neural progenitors that express Soxb2 before differentiating into mature neural cells. Knockdown of SoxB genes resulted in complex defects in embryonic neurogenesis. Hydractinia neural cells differentiate while migrating from the aboral to the oral end of the animal, but it is unclear whether migration per se or exposure to different microenvironments is the main driver of their fate determination. Our data constitute a rich resource for studies aiming at addressing this question, which is at the heart of understanding the origin and development of animal nervous systems. eLife Sciences Publications, Ltd 2022-05-24 /pmc/articles/PMC9173746/ /pubmed/35608899 http://dx.doi.org/10.7554/eLife.78793 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication (https://creativecommons.org/publicdomain/zero/1.0/) . |
spellingShingle | Developmental Biology Chrysostomou, Eleni Flici, Hakima Gornik, Sebastian G Salinas-Saavedra, Miguel Gahan, James M McMahon, Emma T Thompson, Kerry Hanley, Shirley Kilcoyne, Michelle Schnitzler, Christine E Gonzalez, Paul Baxevanis, Andreas D Frank, Uri A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian |
title | A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian |
title_full | A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian |
title_fullStr | A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian |
title_full_unstemmed | A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian |
title_short | A cellular and molecular analysis of SoxB-driven neurogenesis in a cnidarian |
title_sort | cellular and molecular analysis of soxb-driven neurogenesis in a cnidarian |
topic | Developmental Biology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9173746/ https://www.ncbi.nlm.nih.gov/pubmed/35608899 http://dx.doi.org/10.7554/eLife.78793 |
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