Thyroid hormone regulates distinct paths to maturation in pigment cell lineages

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....

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Main Authors: Lauren M Saunders, Abhishek K Mishra, Andrew J Aman, Victor M Lewis, Matthew B Toomey, Jonathan S Packer, Xiaojie Qiu, Jose L McFaline-Figueroa, Joseph C Corbo, Cole Trapnell, David M Parichy
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/45181
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author Lauren M Saunders
Abhishek K Mishra
Andrew J Aman
Victor M Lewis
Matthew B Toomey
Jonathan S Packer
Xiaojie Qiu
Jose L McFaline-Figueroa
Joseph C Corbo
Cole Trapnell
David M Parichy
author_facet Lauren M Saunders
Abhishek K Mishra
Andrew J Aman
Victor M Lewis
Matthew B Toomey
Jonathan S Packer
Xiaojie Qiu
Jose L McFaline-Figueroa
Joseph C Corbo
Cole Trapnell
David M Parichy
author_sort Lauren M Saunders
collection DOAJ
description 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.
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spelling doaj.art-d802aca4e8474f9799616ec7022d2e472022-12-22T02:03:10ZengeLife Sciences Publications LtdeLife2050-084X2019-05-01810.7554/eLife.45181Thyroid hormone regulates distinct paths to maturation in pigment cell lineagesLauren M Saunders0https://orcid.org/0000-0003-4377-4252Abhishek K Mishra1Andrew J Aman2Victor M Lewis3Matthew B Toomey4https://orcid.org/0000-0001-9184-197XJonathan S Packer5Xiaojie Qiu6Jose L McFaline-Figueroa7Joseph C Corbo8https://orcid.org/0000-0002-9323-7140Cole Trapnell9David M Parichy10https://orcid.org/0000-0003-2771-6095Department of Genome Sciences, University of Washington, Seattle, United States; Department of Biology, University of Virginia, Charlottesville, United States; Department of Cell Biology, University of Virginia, Charlottesville, United StatesDepartment of Biology, University of Virginia, Charlottesville, United States; Department of Cell Biology, University of Virginia, Charlottesville, United StatesDepartment of Biology, University of Virginia, Charlottesville, United States; Department of Cell Biology, University of Virginia, Charlottesville, United StatesDepartment of Genome Sciences, University of Washington, Seattle, United States; Department of Biology, University of Virginia, Charlottesville, United States; Department of Cell Biology, University of Virginia, Charlottesville, United StatesDepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, United StatesDepartment of Genome Sciences, University of Washington, Seattle, United StatesDepartment of Genome Sciences, University of Washington, Seattle, United StatesDepartment of Genome Sciences, University of Washington, Seattle, United StatesDepartment of Pathology and Immunology, Washington University School of Medicine, St. Louis, United StatesDepartment of Genome Sciences, University of Washington, Seattle, United StatesDepartment of Biology, University of Virginia, Charlottesville, United States; Department of Cell Biology, University of Virginia, Charlottesville, United StatesThyroid 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.https://elifesciences.org/articles/45181pigmentationneural crestthyroid hormonepost-embryonic developmentmelanophorexanthophore
spellingShingle Lauren M Saunders
Abhishek K Mishra
Andrew J Aman
Victor M Lewis
Matthew B Toomey
Jonathan S Packer
Xiaojie Qiu
Jose L McFaline-Figueroa
Joseph C Corbo
Cole Trapnell
David M Parichy
Thyroid hormone regulates distinct paths to maturation in pigment cell lineages
eLife
pigmentation
neural crest
thyroid hormone
post-embryonic development
melanophore
xanthophore
title Thyroid hormone regulates distinct paths to maturation in pigment cell lineages
title_full Thyroid hormone regulates distinct paths to maturation in pigment cell lineages
title_fullStr Thyroid hormone regulates distinct paths to maturation in pigment cell lineages
title_full_unstemmed Thyroid hormone regulates distinct paths to maturation in pigment cell lineages
title_short Thyroid hormone regulates distinct paths to maturation in pigment cell lineages
title_sort thyroid hormone regulates distinct paths to maturation in pigment cell lineages
topic pigmentation
neural crest
thyroid hormone
post-embryonic development
melanophore
xanthophore
url https://elifesciences.org/articles/45181
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