Integrative profiling of gene expression and chromatin accessibility elucidates specific transcriptional networks in porcine neutrophils

Neutrophils are vital components of the immune system for limiting the invasion and proliferation of pathogens in the body. Surprisingly, the functional annotation of porcine neutrophils is still limited. The transcriptomic and epigenetic assessment of porcine neutrophils from healthy pigs was perfo...

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Main Authors: Juber Herrera-Uribe, Kyu-Sang Lim, Kristen A. Byrne, Lance Daharsh, Haibo Liu, Ryan J. Corbett, Gianna Marco, Martine Schroyen, James E. Koltes, Crystal L. Loving, Christopher K. Tuggle
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Genetics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fgene.2023.1107462/full
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author Juber Herrera-Uribe
Kyu-Sang Lim
Kyu-Sang Lim
Kristen A. Byrne
Lance Daharsh
Haibo Liu
Ryan J. Corbett
Gianna Marco
Martine Schroyen
James E. Koltes
Crystal L. Loving
Christopher K. Tuggle
author_facet Juber Herrera-Uribe
Kyu-Sang Lim
Kyu-Sang Lim
Kristen A. Byrne
Lance Daharsh
Haibo Liu
Ryan J. Corbett
Gianna Marco
Martine Schroyen
James E. Koltes
Crystal L. Loving
Christopher K. Tuggle
author_sort Juber Herrera-Uribe
collection DOAJ
description Neutrophils are vital components of the immune system for limiting the invasion and proliferation of pathogens in the body. Surprisingly, the functional annotation of porcine neutrophils is still limited. The transcriptomic and epigenetic assessment of porcine neutrophils from healthy pigs was performed by bulk RNA sequencing and transposase accessible chromatin sequencing (ATAC-seq). First, we sequenced and compared the transcriptome of porcine neutrophils with eight other immune cell transcriptomes to identify a neutrophil-enriched gene list within a detected neutrophil co-expression module. Second, we used ATAC-seq analysis to report for the first time the genome-wide chromatin accessible regions of porcine neutrophils. A combined analysis using both transcriptomic and chromatin accessibility data further defined the neutrophil co-expression network controlled by transcription factors likely important for neutrophil lineage commitment and function. We identified chromatin accessible regions around promoters of neutrophil-specific genes that were predicted to be bound by neutrophil-specific transcription factors. Additionally, published DNA methylation data from porcine immune cells including neutrophils were used to link low DNA methylation patterns to accessible chromatin regions and genes with highly enriched expression in porcine neutrophils. In summary, our data provides the first integrative analysis of the accessible chromatin regions and transcriptional status of porcine neutrophils, contributing to the Functional Annotation of Animal Genomes (FAANG) project, and demonstrates the utility of chromatin accessible regions to identify and enrich our understanding of transcriptional networks in a cell type such as neutrophils.
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spelling doaj.art-cedb7edc21234d88b20d51e19310d1be2023-05-23T05:17:51ZengFrontiers Media S.A.Frontiers in Genetics1664-80212023-05-011410.3389/fgene.2023.11074621107462Integrative profiling of gene expression and chromatin accessibility elucidates specific transcriptional networks in porcine neutrophilsJuber Herrera-Uribe0Kyu-Sang Lim1Kyu-Sang Lim2Kristen A. Byrne3Lance Daharsh4Haibo Liu5Ryan J. Corbett6Gianna Marco7Martine Schroyen8James E. Koltes9Crystal L. Loving10Christopher K. Tuggle11Department of Animal Science, Iowa State University, Ames, IA, United StatesDepartment of Animal Science, Iowa State University, Ames, IA, United StatesDepartment of Animal Resource Science, Kongju National University, Yesan, Republic of KoreaUSDA-Agriculture Research Service, National Animal Disease Center, Food Safety and Enteric Pathogens Research Unit, Ames, IA, United StatesDepartment of Animal Science, Iowa State University, Ames, IA, United StatesDepartment of Animal Science, Iowa State University, Ames, IA, United StatesDepartment of Animal Science, Iowa State University, Ames, IA, United StatesDepartment of Animal Science, Iowa State University, Ames, IA, United StatesDepartment of Animal Science, Iowa State University, Ames, IA, United StatesDepartment of Animal Science, Iowa State University, Ames, IA, United StatesUSDA-Agriculture Research Service, National Animal Disease Center, Food Safety and Enteric Pathogens Research Unit, Ames, IA, United StatesDepartment of Animal Science, Iowa State University, Ames, IA, United StatesNeutrophils are vital components of the immune system for limiting the invasion and proliferation of pathogens in the body. Surprisingly, the functional annotation of porcine neutrophils is still limited. The transcriptomic and epigenetic assessment of porcine neutrophils from healthy pigs was performed by bulk RNA sequencing and transposase accessible chromatin sequencing (ATAC-seq). First, we sequenced and compared the transcriptome of porcine neutrophils with eight other immune cell transcriptomes to identify a neutrophil-enriched gene list within a detected neutrophil co-expression module. Second, we used ATAC-seq analysis to report for the first time the genome-wide chromatin accessible regions of porcine neutrophils. A combined analysis using both transcriptomic and chromatin accessibility data further defined the neutrophil co-expression network controlled by transcription factors likely important for neutrophil lineage commitment and function. We identified chromatin accessible regions around promoters of neutrophil-specific genes that were predicted to be bound by neutrophil-specific transcription factors. Additionally, published DNA methylation data from porcine immune cells including neutrophils were used to link low DNA methylation patterns to accessible chromatin regions and genes with highly enriched expression in porcine neutrophils. In summary, our data provides the first integrative analysis of the accessible chromatin regions and transcriptional status of porcine neutrophils, contributing to the Functional Annotation of Animal Genomes (FAANG) project, and demonstrates the utility of chromatin accessible regions to identify and enrich our understanding of transcriptional networks in a cell type such as neutrophils.https://www.frontiersin.org/articles/10.3389/fgene.2023.1107462/fullpigtranscriptomebulk-RNA-seqco-expressed genestranscription factor (TF)gene regulation
spellingShingle Juber Herrera-Uribe
Kyu-Sang Lim
Kyu-Sang Lim
Kristen A. Byrne
Lance Daharsh
Haibo Liu
Ryan J. Corbett
Gianna Marco
Martine Schroyen
James E. Koltes
Crystal L. Loving
Christopher K. Tuggle
Integrative profiling of gene expression and chromatin accessibility elucidates specific transcriptional networks in porcine neutrophils
Frontiers in Genetics
pig
transcriptome
bulk-RNA-seq
co-expressed genes
transcription factor (TF)
gene regulation
title Integrative profiling of gene expression and chromatin accessibility elucidates specific transcriptional networks in porcine neutrophils
title_full Integrative profiling of gene expression and chromatin accessibility elucidates specific transcriptional networks in porcine neutrophils
title_fullStr Integrative profiling of gene expression and chromatin accessibility elucidates specific transcriptional networks in porcine neutrophils
title_full_unstemmed Integrative profiling of gene expression and chromatin accessibility elucidates specific transcriptional networks in porcine neutrophils
title_short Integrative profiling of gene expression and chromatin accessibility elucidates specific transcriptional networks in porcine neutrophils
title_sort integrative profiling of gene expression and chromatin accessibility elucidates specific transcriptional networks in porcine neutrophils
topic pig
transcriptome
bulk-RNA-seq
co-expressed genes
transcription factor (TF)
gene regulation
url https://www.frontiersin.org/articles/10.3389/fgene.2023.1107462/full
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