Thyroid hormone regulates distinct paths to maturation in pigment cell lineages
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.
Data availability
Data deposited in GEO under accession code GSE131136. Additional data are provided as source data files.
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Thyroid hormone regulates distinct paths to maturation in pigment cell lineagesNCBI Gene Expression Omnibus, GSE131136.
Article and author information
Author details
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.
Reviewing Editor
- 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 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.
Version history
- Received: January 18, 2019
- Accepted: May 24, 2019
- Accepted Manuscript published: May 29, 2019 (version 1)
- 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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