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Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types

The immune system of vertebrate species consists of many different cell types that have distinct functional roles and are subject to different evolutionary pressures. Here, we first analyzed conservation of genes specific for all major immune cell types in human and mouse. Our results revealed highe...

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Autores principales: Carmona, Santiago J., Teichmann, Sarah A., Ferreira, Lauren, Macaulay, Iain C., Stubbington, Michael J.T., Cvejic, Ana, Gfeller, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5340972/
https://www.ncbi.nlm.nih.gov/pubmed/28087841
http://dx.doi.org/10.1101/gr.207704.116
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author Carmona, Santiago J.
Teichmann, Sarah A.
Ferreira, Lauren
Macaulay, Iain C.
Stubbington, Michael J.T.
Cvejic, Ana
Gfeller, David
author_facet Carmona, Santiago J.
Teichmann, Sarah A.
Ferreira, Lauren
Macaulay, Iain C.
Stubbington, Michael J.T.
Cvejic, Ana
Gfeller, David
author_sort Carmona, Santiago J.
collection PubMed
description The immune system of vertebrate species consists of many different cell types that have distinct functional roles and are subject to different evolutionary pressures. Here, we first analyzed conservation of genes specific for all major immune cell types in human and mouse. Our results revealed higher gene turnover and faster evolution of trans-membrane proteins in NK cells compared with other immune cell types, and especially T cells, but similar conservation of nuclear and cytoplasmic protein coding genes. To validate these findings in a distant vertebrate species, we used single-cell RNA sequencing of lck:GFP cells in zebrafish and obtained the first transcriptome of specific immune cell types in a nonmammalian species. Unsupervised clustering and single-cell TCR locus reconstruction identified three cell populations, T cells, a novel type of NK-like cells, and a smaller population of myeloid-like cells. Differential expression analysis uncovered new immune-cell–specific genes, including novel immunoglobulin-like receptors, and neofunctionalization of recently duplicated paralogs. Evolutionary analyses confirmed the higher gene turnover of trans-membrane proteins in NK cells compared with T cells in fish species, suggesting that this is a general property of immune cell types across all vertebrates.
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spelling pubmed-53409722017-03-20 Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types Carmona, Santiago J. Teichmann, Sarah A. Ferreira, Lauren Macaulay, Iain C. Stubbington, Michael J.T. Cvejic, Ana Gfeller, David Genome Res Research The immune system of vertebrate species consists of many different cell types that have distinct functional roles and are subject to different evolutionary pressures. Here, we first analyzed conservation of genes specific for all major immune cell types in human and mouse. Our results revealed higher gene turnover and faster evolution of trans-membrane proteins in NK cells compared with other immune cell types, and especially T cells, but similar conservation of nuclear and cytoplasmic protein coding genes. To validate these findings in a distant vertebrate species, we used single-cell RNA sequencing of lck:GFP cells in zebrafish and obtained the first transcriptome of specific immune cell types in a nonmammalian species. Unsupervised clustering and single-cell TCR locus reconstruction identified three cell populations, T cells, a novel type of NK-like cells, and a smaller population of myeloid-like cells. Differential expression analysis uncovered new immune-cell–specific genes, including novel immunoglobulin-like receptors, and neofunctionalization of recently duplicated paralogs. Evolutionary analyses confirmed the higher gene turnover of trans-membrane proteins in NK cells compared with T cells in fish species, suggesting that this is a general property of immune cell types across all vertebrates. Cold Spring Harbor Laboratory Press 2017-03 /pmc/articles/PMC5340972/ /pubmed/28087841 http://dx.doi.org/10.1101/gr.207704.116 Text en © 2017 Carmona et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by/4.0/ This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/.
spellingShingle Research
Carmona, Santiago J.
Teichmann, Sarah A.
Ferreira, Lauren
Macaulay, Iain C.
Stubbington, Michael J.T.
Cvejic, Ana
Gfeller, David
Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types
title Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types
title_full Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types
title_fullStr Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types
title_full_unstemmed Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types
title_short Single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types
title_sort single-cell transcriptome analysis of fish immune cells provides insight into the evolution of vertebrate immune cell types
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5340972/
https://www.ncbi.nlm.nih.gov/pubmed/28087841
http://dx.doi.org/10.1101/gr.207704.116
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