Wnt/β-catenin regulates an ancient signaling network during zebrafish scale development

  1. Andrew J Aman
  2. Alexis N Fulbright
  3. David M Parichy  Is a corresponding author
  1. University of Virginia, United States
  2. Huntsman Cancer Institute, United States

Abstract

Understanding how patterning influences cell behaviors to generate three dimensional morphologies is a central goal of developmental biology. Additionally, comparing these regulatory mechanisms among morphologically diverse tissues allows for rigorous testing of evolutionary hypotheses. Zebrafish skin is endowed with a coat of precisely patterned bony scales. We use in-toto live imaging during scale development and manipulations of cell signaling activity to elucidate core features of scale patterning and morphogenesis. These analyses show that scale development requires the concerted activity of Wnt/β-catenin, Ectodysplasin (Eda) and Fibroblast growth factor (Fgf) signaling. This regulatory module coordinates Hedgehog (HH) dependent collective cell migration during epidermal invagination, a cell behavior not previously implicated in skin appendage morphogenesis. Our analyses demonstrate the utility of zebrafish scale development as a tractable system in which to elucidate mechanisms of developmental patterning and morphogenesis, and suggest a single, ancient origin of skin appendage patterning mechanisms in vertebrates.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Specialized materials including transgenic and mutant lines are available upon request.

Article and author information

Author details

  1. Andrew J Aman

    Department of Biology and Department of Cell Biology, University of Virginia, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Alexis N Fulbright

    University of Utah, Huntsman Cancer Institute, Salt Lake Cite, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5634-4094
  3. David M Parichy

    Department of Biology and Department of Cell Biology, University of Virginia, Charlottesville, United States
    For correspondence
    dparichy@virginia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2771-6095

Funding

National Institutes of Health (R35 GM122471)

  • David M Parichy

Royalty Research Fund (A112414)

  • David M Parichy

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

Reviewing Editor

  1. Richard M White, Memorial Sloan Kettering Cancer Center, United States

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved Animal Care and Use Committee (ACUC) protocols (#4170) of the University of Virginia. All imaging and regeneration experiments were performed under MS222 anesthesi , and every effort was made to minimize suffering.

Version history

  1. Received: March 26, 2018
  2. Accepted: June 21, 2018
  3. Accepted Manuscript published: July 17, 2018 (version 1)
  4. Version of Record published: August 2, 2018 (version 2)

Copyright

© 2018, Aman 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. Andrew J Aman
  2. Alexis N Fulbright
  3. David M Parichy
(2018)
Wnt/β-catenin regulates an ancient signaling network during zebrafish scale development
eLife 7:e37001.
https://doi.org/10.7554/eLife.37001

Share this article

https://doi.org/10.7554/eLife.37001

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