Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin

Pigment patterns and skin appendages are prominent features of vertebrate skin. In zebrafish, regularly patterned pigment stripes and an array of calcified scales form simultaneously in the skin during post-embryonic development. Understanding the mechanisms that regulate stripe patterning and scale...

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Main Authors: Andrew J Aman, Lauren M Saunders, August A Carr, Sanjay Srivatasan, Colten Eberhard, Blake Carrington, Dawn Watkins-Chow, William J Pavan, Cole Trapnell, David M Parichy
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/86670
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author Andrew J Aman
Lauren M Saunders
August A Carr
Sanjay Srivatasan
Colten Eberhard
Blake Carrington
Dawn Watkins-Chow
William J Pavan
Cole Trapnell
David M Parichy
author_facet Andrew J Aman
Lauren M Saunders
August A Carr
Sanjay Srivatasan
Colten Eberhard
Blake Carrington
Dawn Watkins-Chow
William J Pavan
Cole Trapnell
David M Parichy
author_sort Andrew J Aman
collection DOAJ
description Pigment patterns and skin appendages are prominent features of vertebrate skin. In zebrafish, regularly patterned pigment stripes and an array of calcified scales form simultaneously in the skin during post-embryonic development. Understanding the mechanisms that regulate stripe patterning and scale morphogenesis may lead to the discovery of fundamental mechanisms that govern the development of animal form. To learn about cell types and signaling interactions that govern skin patterning and morphogenesis, we generated and analyzed single-cell transcriptomes of skin from wild-type fish as well as fish having genetic or transgenically induced defects in squamation or pigmentation. These data reveal a previously undescribed population of epidermal cells that express transcripts encoding enamel matrix proteins, suggest hormonal control of epithelial–mesenchymal signaling, clarify the signaling network that governs scale papillae development, and identify a critical role for the hypodermis in supporting pigment cell development. Additionally, these comprehensive single-cell transcriptomic data representing skin phenotypes of biomedical relevance should provide a useful resource for accelerating the discovery of mechanisms that govern skin development and homeostasis.
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spelling doaj.art-0404da2852a442729dc8e111e624a00c2023-11-08T10:26:03ZengeLife Sciences Publications LtdeLife2050-084X2023-09-011210.7554/eLife.86670Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skinAndrew J Aman0https://orcid.org/0009-0003-3311-4661Lauren M Saunders1https://orcid.org/0000-0003-4377-4252August A Carr2Sanjay Srivatasan3Colten Eberhard4https://orcid.org/0000-0001-7292-7313Blake Carrington5Dawn Watkins-Chow6William J Pavan7Cole Trapnell8David M Parichy9https://orcid.org/0000-0003-2771-6095Department of Biology, University of Virginia, Charlottesville, United StatesDepartment of Genome Sciences, University of Washington, Seattle, United StatesDepartment of Biology, University of Virginia, Charlottesville, United StatesDepartment of Genome Sciences, University of Washington, Seattle, United StatesNational Human Genome Research Institute, National Institutes of Health, Bethesda, United StatesNational Human Genome Research Institute, National Institutes of Health, Bethesda, United StatesNational Human Genome Research Institute, National Institutes of Health, Bethesda, United StatesNational Human Genome Research Institute, National Institutes of Health, Bethesda, 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 StatesPigment patterns and skin appendages are prominent features of vertebrate skin. In zebrafish, regularly patterned pigment stripes and an array of calcified scales form simultaneously in the skin during post-embryonic development. Understanding the mechanisms that regulate stripe patterning and scale morphogenesis may lead to the discovery of fundamental mechanisms that govern the development of animal form. To learn about cell types and signaling interactions that govern skin patterning and morphogenesis, we generated and analyzed single-cell transcriptomes of skin from wild-type fish as well as fish having genetic or transgenically induced defects in squamation or pigmentation. These data reveal a previously undescribed population of epidermal cells that express transcripts encoding enamel matrix proteins, suggest hormonal control of epithelial–mesenchymal signaling, clarify the signaling network that governs scale papillae development, and identify a critical role for the hypodermis in supporting pigment cell development. Additionally, these comprehensive single-cell transcriptomic data representing skin phenotypes of biomedical relevance should provide a useful resource for accelerating the discovery of mechanisms that govern skin development and homeostasis.https://elifesciences.org/articles/86670squamationskinpigmentmorphogenesisadult formdifferentiation
spellingShingle Andrew J Aman
Lauren M Saunders
August A Carr
Sanjay Srivatasan
Colten Eberhard
Blake Carrington
Dawn Watkins-Chow
William J Pavan
Cole Trapnell
David M Parichy
Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin
eLife
squamation
skin
pigment
morphogenesis
adult form
differentiation
title Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin
title_full Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin
title_fullStr Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin
title_full_unstemmed Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin
title_short Transcriptomic profiling of tissue environments critical for post-embryonic patterning and morphogenesis of zebrafish skin
title_sort transcriptomic profiling of tissue environments critical for post embryonic patterning and morphogenesis of zebrafish skin
topic squamation
skin
pigment
morphogenesis
adult form
differentiation
url https://elifesciences.org/articles/86670
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