Abstract

The presence and identity of neural progenitors in the enteric nervous system (ENS) of vertebrates is a matter of intense debate. Here we demonstrate that the non-neuronal ENS cell compartment of teleosts shares molecular and morphological characteristics with mammalian enteric glia but cannot be identified by the expression of canonical glia markers. However, unlike their mammalian counterparts, which are generally quiescent and do not undergo neuronal differentiation during homeostasis, we show that a relatively high proportion of zebrafish enteric glia proliferate under physiological conditions giving rise to progeny that differentiate into enteric neurons. We also provide evidence that, similar to brain neural stem cells, the activation and neuronal differentiation of enteric glia are regulated by Notch signalling. Our experiments reveal remarkable similarities between enteric glia and brain neural stem cells in teleosts and open new possibilities for use of mammalian enteric glia as a potential source of neurons to restore the activity of intestinal neural circuits compromised by injury or disease.

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High-throughput sequencing data have been deposited in GEO under accession codes GSE145885.

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Article and author information

Author details

  1. Sarah McCallum

    Development and Homeostasis of the Nervous System Lab, The Francis Crick Institute, London, United Kingdom
    Competing interests
    No competing interests declared.
  2. Yuuki Obata

    Development and Homeostasis of the Nervous System Lab, The Francis Crick Institute, London, United Kingdom
    Competing interests
    No competing interests declared.
  3. Evangelia Fourli

    Development and Homeostasis of the Nervous System Lab, The Francis Crick Institute, London, United Kingdom
    Competing interests
    No competing interests declared.
  4. Stefan Boeing

    Bionformatics & Biostatistics Science Technology Platform, The Francis Crick Institute, London, United Kingdom
    Competing interests
    No competing interests declared.
  5. Christopher J Peddie

    Electron Microscopy Science Technology Platform, The Francis Crick Institute, London, United Kingdom
    Competing interests
    No competing interests declared.
  6. Qiling Xu

    Neural Development Laboratory, The Francis Crick Institute, London, United Kingdom
    Competing interests
    No competing interests declared.
  7. Stuart Horswell

    Bionformatics & Biostatistics Science Technology Platform, The Francis Crick Institute, London, United Kingdom
    Competing interests
    No competing interests declared.
  8. Robert Kelsh

    Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
    Competing interests
    No competing interests declared.
  9. Lucy Collinson

    Electron Microscopy Science Technology Platform, The Francis Crick Institute, London, United Kingdom
    Competing interests
    No competing interests declared.
  10. David Wilkinson

    Neural Development Laboratory, The Francis Crick Institute, London, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6757-7080
  11. Carmen Pin

    Clinical and Quantitative Pharmacology, AstraZeneca, Cambridge, United Kingdom
    Competing interests
    Carmen Pin, Carmen Pin is affiliated with AstraZeneca. The author has no financial interests to declare..
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8734-6167
  12. Vassilis Pachnis

    Nervous System Development and Homeostasis Laboratory, The Francis Crick Institute, London, United Kingdom
    For correspondence
    vassilis.pachnis@crick.ac.uk
    Competing interests
    No competing interests declared.
  13. Tiffany A Heanue

    Development and Homeostasis of the Nervous System Lab, The Francis Crick Institute, London, United Kingdom
    For correspondence
    tiffany.heanue@crick.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6678-8246

Funding

The Francis Crick Institute (core funding)

  • Vassilis Pachnis

BBSRC (BB/L022974/1)

  • Vassilis Pachnis

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All animal experiments were carried out in compliance with the Animals (Scientific Procedures) Act 1986 (UK) and in accordance with the regulatory standards of the UK Home Office (Project Licence PCBBB9ABB). Experimental protocols were approved by the local Animal Welfare and Ethical Review Body (AWERB) of the Francis Crick Institute.

Copyright

© 2020, McCallum et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Sarah McCallum
  2. Yuuki Obata
  3. Evangelia Fourli
  4. Stefan Boeing
  5. Christopher J Peddie
  6. Qiling Xu
  7. Stuart Horswell
  8. Robert Kelsh
  9. Lucy Collinson
  10. David Wilkinson
  11. Carmen Pin
  12. Vassilis Pachnis
  13. Tiffany A Heanue
(2020)
Enteric glia as a source of neural progenitors in adult zebrafish
eLife 9:e56086.
https://doi.org/10.7554/eLife.56086

Share this article

https://doi.org/10.7554/eLife.56086

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