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De novo enteric neurogenesis in post-embryonic zebrafish from Schwann cell precursors rather than resident cell types

El-Nachef, Wael Noor and Bronner, Marianne E. (2020) De novo enteric neurogenesis in post-embryonic zebrafish from Schwann cell precursors rather than resident cell types. Development, 147 (13). Art. No. dev186619. ISSN 0950-1991. PMCID PMC7375481. https://resolver.caltech.edu/CaltechAUTHORS:20200603-132940388

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Abstract

The enteric nervous system (ENS) is essential for normal gastrointestinal function. Although the embryonic origin of enteric neurons from the neural crest is well established, conflicting evidence exists regarding postnatal enteric neurogenesis. Here, we address this by examining the origin of de novo neurogenesis in the post-embryonic zebrafish ENS. Although new neurons are added during growth and after injury, the larval intestine appears to lack resident neurogenic precursors or classical glia marked by sox10, plp1a, gfap or s100. Rather, lineage tracing with lipophilic dye or inducible Sox10-Cre suggests that post-embryonic enteric neurons arise from trunk neural crest-derived Schwann cell precursors that migrate from the spinal cord into the intestine. Furthermore, the 5-HT₄ receptor agonist prucalopride increases enteric neurogenesis in normal development and after injury. Taken together, the results suggest that despite the lack of resident progenitors in the gut, post-embryonic enteric neurogenesis occurs via gut-extrinsic Schwann cell precursors during development and injury, and is promoted by serotonin receptor agonists. The absence of classical glia in the ENS further suggests that neural crest-derived enteric glia might have evolved after the teleost lineage.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1242/dev.186619DOIArticle
https://doi.org/10.1101/2020.06.01.127712DOIDiscussion Paper
https://resolver.caltech.edu/CaltechAUTHORS:20200409-140201559Related ItemConference Abstract
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc7375481/PubMed CentralArticle
ORCID:
AuthorORCID
Bronner, Marianne E.0000-0003-4274-1862
Additional Information:© 2020 Published by The Company of Biologists Ltd. Received November 30, 2019; Accepted June 3, 2020; Published 13 July 2020. We thank the Beckman Institute Biological Imaging Facility of Caltech for technical assistance with microscopy experiments. For generously supplying transgenic fish lines, we thank the Ian Shepherd Lab (Phox2b-kaede), the Jua-Nian Chen Lab (sox10:GAL4-UAS-Cre and ubi:switch) and the Christiane Nüsslein-Volhard Lab (cmlc:GFP-sox10:ERT2-Cre). Special thanks to Megan Martik and Can Li for sharing ISH probes (Sox10, Phox2bb). We also recognize Claire Hu (California Institute of Technology) for assistance with IHC. The authors declare no competing or financial interests. Author contributions: Conceptualization: W.N.E.-N., M.E.B.; Methodology: W.N.E.-N., M.E.B.; Validation: W.N.E.-N.; Formal analysis: W.N.E.-N., M.E.B.; Investigation: W.N.E.-N.; Resources: W.N.E.-N., M.E.B.; Data curation: W.N.E.-N., M.E.B.; Writing - original draft: W.N.E.-N.; Writing - review & editing: W.N.E.-N., M.E.B.; Visualization: W.N.E.-N.; Supervision: M.E.B.; Project administration: M.E.B.; Funding acquisition: M.E.B. This work was supported by the National Institutes of Health (NIH R35NS111564 to M.E.B. and NIH R01NS108500 to M.E.B.). Deposited in PMC for release after 12 months.
Funders:
Funding AgencyGrant Number
NIHR35NS111564
NIHR01NS108500
Subject Keywords:enteric nervous system; neural crest; prucalopride; 5-HT₄
Issue or Number:13
PubMed Central ID:PMC7375481
Record Number:CaltechAUTHORS:20200603-132940388
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200603-132940388
Official Citation:De novo enteric neurogenesis in post-embryonic zebrafish from Schwann cell precursors rather than resident cell types. Wael Noor El-Nachef, Marianne E. Bronner. Development 2020 147: dev186619 doi: 10.1242/dev.186619; Published 13 July 2020
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:103673
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:03 Jun 2020 20:44
Last Modified:31 Jul 2020 15:45

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