1. Developmental Biology
  2. Genetics and Genomics
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Thyroid hormone regulates distinct paths to maturation in pigment cell lineages

  1. Lauren M Saunders
  2. Abhishek K Mishra
  3. Andrew J Aman
  4. Victor M Lewis
  5. Matthew B Toomey
  6. Jonathan S Packer
  7. Xiaojie Qiu
  8. Jose L McFaline-Figueroa
  9. Joseph C Corbo
  10. Cole Trapnell  Is a corresponding author
  11. David M Parichy  Is a corresponding author
  1. University of Washington, United States
  2. University of Virginia, United States
  3. Washington University School of Medicine, United States
Research Article
  • Cited 10
  • Views 2,339
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Cite this article as: eLife 2019;8:e45181 doi: 10.7554/eLife.45181

Abstract

Thyroid hormone (TH) regulates diverse developmental events and can drive disparate cellular outcomes. In zebrafish, TH has opposite effects on neural crest derived pigment cells of the adult stripe pattern, limiting melanophore population expansion, yet increasing yellow/orange xanthophore numbers. To learn how TH elicits seemingly opposite responses in cells having a common embryological origin, we analyzed individual transcriptomes from thousands of neural crest derived cells, reconstructed developmental trajectories, identified pigment cell-lineage specific responses to TH, and assessed roles for TH receptors. We show that TH promotes maturation of both cell types but in distinct ways. In melanophores, TH drives terminal differentiation, limiting final cell numbers. In xanthophores, TH promotes accumulation of orange carotenoids, making the cells visible. TH receptors act primarily to repress these programs when TH is limiting. Our findings show how a single endocrine factor integrates very different cellular activities during the generation of adult form.

Article and author information

Author details

  1. Lauren M Saunders

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4377-4252
  2. Abhishek K Mishra

    Department of Biology, University of Virginia, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Andrew J Aman

    Department of Biology, University of Virginia, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Victor M Lewis

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Matthew B Toomey

    Department of Pathology and Immunology, Washington University School of Medicine, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9184-197X
  6. Jonathan S Packer

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Xiaojie Qiu

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Jose L McFaline-Figueroa

    Department of Genome Sciences, University of Washington, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Joseph C Corbo

    Department of Pathology and Immunology, Washington University School of Medicine, St Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9323-7140
  10. Cole Trapnell

    Department of Genome Sciences, University of Washington, Seattle, United States
    For correspondence
    coletrap@uw.edu
    Competing interests
    The authors declare that no competing interests exist.
  11. David M Parichy

    Department of 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 Institute of General Medical Sciences (R35 GM122471)

  • David M Parichy

Eunice Kennedy Shriver National Institute of Child Health and Human Development (DP2 HD088158)

  • Cole Trapnell

National Eye Institute (EY024958)

  • Joseph C Corbo

W. M. Keck Foundation

  • Cole Trapnell

Alfred P. Sloan Foundation

  • Cole Trapnell

Paul G Allen Frontiers Group

  • Cole Trapnell

National Eye Institute (EY025196)

  • Joseph C Corbo

National Eye Institute (EY026672)

  • Joseph C Corbo

National Institute of General Medical Sciences (T32 GM007067)

  • Lauren M Saunders

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

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 institutional animal care and use committee (IACUC) protocols (4170) of the University of Vriginia and (4094-01) of the University of Washington. For imaging and other procedures animals were anesthetized with MS222 or euthanized by overdose of MS222 and every effort was made to minimize suffering.

Reviewing Editor

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

Publication history

  1. Received: January 18, 2019
  2. Accepted: May 24, 2019
  3. Accepted Manuscript published: May 29, 2019 (version 1)
  4. Version of Record published: June 21, 2019 (version 2)

Copyright

© 2019, Saunders 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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