Hierarchical stem cell topography splits growth and homeostatic functions in the fish gill

  1. Julian Stolper
  2. Elizabeth Mayela Ambrosio
  3. Diana-Patricia Danciu
  4. Lorena Bono
  5. David A Elliott
  6. Kiyoshi Naruse
  7. Juan R Martínez-Morales
  8. Anna Marciniak-Czochra
  9. Lazaro Centanin  Is a corresponding author
  1. Centre for Organismal Studies, Heidelberg University, Germany
  2. Heidelberg University, Germany
  3. Centro Andaluz de Biología del Desarrollo, Universidad Pablo de Olavide, Spain
  4. Murdoch Children's Research Institute, Royal Children's Hospital, Australia
  5. National Institute for Basic Biology, National Institutes of Natural Sciences, Japan

Abstract

While lower vertebrates contain adult stem cells (aSCs) that maintain homeostasis and drive un-exhaustive organismal growth, mammalian aSCs display mainly the homeostatic function. Here we use lineage analysis in the fish gill to address aSCs and report separate stem cell populations for homeostasis and growth. These aSCs are fate-restricted during the entire post-embryonic life and even during re-generation paradigms. We use chimeric animals to demonstrate that p53 mediates growth coordination among fate-restricted aSCs, suggesting a hierarchical organisation among lineages in composite organs like the fish gill. Homeostatic and growth aSCs are clonal but differ in their topology; modifications in tissue architecture can convert the homeostatic zone into a growth zone, indicating a leading role for the physical niche defining stem cell output. We hypothesise that physical niches are main players to restrict aSCs to a homeostatic function in animals with fixed adult size.

Data availability

All data analysed for this study is included in the manuscript and supporting files. Raw sequencing data have been deposited in GEO under accession code GSE130939

The following data sets were generated

Article and author information

Author details

  1. Julian Stolper

    Animal Physiology and Development, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Elizabeth Mayela Ambrosio

    Animal Physiology and Development, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7227-7744
  3. Diana-Patricia Danciu

    Institute of Applied Mathematics, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8683-3956
  4. Lorena Bono

    Gene Regulation and Morphogenesis, Centro Andaluz de Biología del Desarrollo, Universidad Pablo de Olavide, Seville, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. David A Elliott

    Cell Biology, Murdoch Children's Research Institute, Royal Children's Hospital, Parkville, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1052-7407
  6. Kiyoshi Naruse

    Laboratory of Bioresources, National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  7. Juan R Martínez-Morales

    Gene Regulation and Morphogenesis, Centro Andaluz de Biología del Desarrollo, Universidad Pablo de Olavide, Seville, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4650-4293
  8. Anna Marciniak-Czochra

    Institute of Applied Mathematics, Heidelberg University, Heidelberg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5831-6505
  9. Lazaro Centanin

    Animal Physiology and Development, Centre for Organismal Studies, Heidelberg University, Heidelberg, Germany
    For correspondence
    lazaro.centanin@cos.uni-heidelberg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3889-4524

Funding

Deutsche Forschungsgemeinschaft (SFB873/A11)

  • Lazaro Centanin

Deutsche Forschungsgemeinschaft (SFB873/B08)

  • Anna Marciniak-Czochra

University of Melbourne (Melbourne Research Fellowship / Graduate Student Fellowship)

  • Julian Stopler

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

Reviewing Editor

  1. Alejandro Sánchez Alvarado, Stowers Institute for Medical Research, United States

Ethics

Animal experimentation: Experimental procedures with fish were performed in accordance with the German animal welfare law and approved by the local government (Tierschutzgesetz {section sign}11, Abs. 1, Nr. 1, husbandry permit number AZ 35-9185.64/BH; line generation permit number AZ 35-9185.81/G-145-15), and with the approval from the Institutional Animal Care and Use Committees of the National Institute for Basic Biology, Japan.

Version history

  1. Received: November 19, 2018
  2. Accepted: May 14, 2019
  3. Accepted Manuscript published: May 15, 2019 (version 1)
  4. Accepted Manuscript updated: May 16, 2019 (version 2)
  5. Version of Record published: May 24, 2019 (version 3)

Copyright

© 2019, Stolper 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. Julian Stolper
  2. Elizabeth Mayela Ambrosio
  3. Diana-Patricia Danciu
  4. Lorena Bono
  5. David A Elliott
  6. Kiyoshi Naruse
  7. Juan R Martínez-Morales
  8. Anna Marciniak-Czochra
  9. Lazaro Centanin
(2019)
Hierarchical stem cell topography splits growth and homeostatic functions in the fish gill
eLife 8:e43747.
https://doi.org/10.7554/eLife.43747

Share this article

https://doi.org/10.7554/eLife.43747

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