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....
Main Authors: | , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
eLife Sciences Publications Ltd
2019-05-01
|
Series: | eLife |
Subjects: | |
Online Access: | https://elifesciences.org/articles/45181 |
_version_ | 1818024057216434176 |
---|---|
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. |
first_indexed | 2024-12-10T03:54:09Z |
format | Article |
id | doaj.art-d802aca4e8474f9799616ec7022d2e47 |
institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-12-10T03:54:09Z |
publishDate | 2019-05-01 |
publisher | eLife Sciences Publications Ltd |
record_format | Article |
series | eLife |
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 |
work_keys_str_mv | AT laurenmsaunders thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages AT abhishekkmishra thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages AT andrewjaman thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages AT victormlewis thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages AT matthewbtoomey thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages AT jonathanspacker thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages AT xiaojieqiu thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages AT joselmcfalinefigueroa thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages AT josephccorbo thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages AT coletrapnell thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages AT davidmparichy thyroidhormoneregulatesdistinctpathstomaturationinpigmentcelllineages |