Transcriptome Analysis Identifies Strategies Targeting Immune Response-Related Pathways to Control Enterotoxigenic Escherichia coli Infection in Porcine Intestinal Epithelial Cells

Enterotoxigenic Escherichia coli (ETEC) is an important cause of post-weaning diarrhea (PWD) worldwide, resulting in huge economic losses to the swine industry worldwide. In this study, to understand the pathogenesis, the transcriptomic analysis was performed to explore the biological processes (BP)...

Full description

Bibliographic Details
Main Authors: Qiong Wu, Defeng Cui, Xinyu Chao, Peng Chen, Jiaxuan Liu, Yiding Wang, Tongjian Su, Meng Li, Ruyu Xu, Yaohong Zhu, Yonghong Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-08-01
Series:Frontiers in Veterinary Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fvets.2021.677897/full
_version_ 1819146057656827904
author Qiong Wu
Qiong Wu
Defeng Cui
Defeng Cui
Xinyu Chao
Peng Chen
Jiaxuan Liu
Yiding Wang
Tongjian Su
Meng Li
Ruyu Xu
Yaohong Zhu
Yonghong Zhang
Yonghong Zhang
author_facet Qiong Wu
Qiong Wu
Defeng Cui
Defeng Cui
Xinyu Chao
Peng Chen
Jiaxuan Liu
Yiding Wang
Tongjian Su
Meng Li
Ruyu Xu
Yaohong Zhu
Yonghong Zhang
Yonghong Zhang
author_sort Qiong Wu
collection DOAJ
description Enterotoxigenic Escherichia coli (ETEC) is an important cause of post-weaning diarrhea (PWD) worldwide, resulting in huge economic losses to the swine industry worldwide. In this study, to understand the pathogenesis, the transcriptomic analysis was performed to explore the biological processes (BP) in porcine intestinal epithelial J2 cells infected with an emerging ETEC strain isolated from weaned pigs with diarrhea. Under the criteria of |fold change| (FC) ≥ 2 and P < 0.05 with false discovery rate < 0.05, a total of 131 referenced and 19 novel differentially expressed genes (DEGs) were identified after ETEC infection, including 96 upregulated DEGs and 54 downregulated DEGs. The Gene Ontology (GO) analysis of DEGs showed that ETEC evoked BP specifically involved in response to lipopolysaccharide (LPS) and negative regulation of intracellular signal transduction. The Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis revealed that immune response-related pathways were mainly enriched in J2 cells after ETEC infection, in which tumor necrosis factor (TNF), interleukin 17, and mitogen-activated protein kinase (MAPK) signaling pathways possessed the highest rich factor, followed by nucleotide-binding and oligomerization domain-like receptor (NLRs), C-type lectin receptor (CLR), cytokine–cytokine receptor interaction, and Toll-like receptor (TLR), and nuclear factor kappa-B (NF-κB) signaling pathways. Furthermore, 30 of 131 referenced DEGs, especially the nuclear transcription factor AP-1 and NF-κB, participate in the immune response to infection through an integral signal cascade and can be target molecules for prevention and control of enteric ETEC infection by probiotic Lactobacillus reuteri. Our data provide a comprehensive insight into the immune response of porcine intestinal epithelial cells (IECs) to ETEC infection and advance the identification of targets for prevention and control of ETEC-related PWD.
first_indexed 2024-12-22T13:07:52Z
format Article
id doaj.art-a62cafccf7334fc68a1f21620149d4eb
institution Directory Open Access Journal
issn 2297-1769
language English
last_indexed 2024-12-22T13:07:52Z
publishDate 2021-08-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Veterinary Science
spelling doaj.art-a62cafccf7334fc68a1f21620149d4eb2022-12-21T18:24:49ZengFrontiers Media S.A.Frontiers in Veterinary Science2297-17692021-08-01810.3389/fvets.2021.677897677897Transcriptome Analysis Identifies Strategies Targeting Immune Response-Related Pathways to Control Enterotoxigenic Escherichia coli Infection in Porcine Intestinal Epithelial CellsQiong Wu0Qiong Wu1Defeng Cui2Defeng Cui3Xinyu Chao4Peng Chen5Jiaxuan Liu6Yiding Wang7Tongjian Su8Meng Li9Ruyu Xu10Yaohong Zhu11Yonghong Zhang12Yonghong Zhang13Department of Animal Medicine, College of Animal Science and Technology, Beijing University of Agriculture, Beijing, ChinaBeijing Key Laboratory of Traditional Chinese Veterinary Medicine, Beijing University of Agriculture, Beijing, ChinaDepartment of Animal Medicine, College of Animal Science and Technology, Beijing University of Agriculture, Beijing, ChinaBeijing Key Laboratory of Traditional Chinese Veterinary Medicine, Beijing University of Agriculture, Beijing, ChinaDepartment of Animal Medicine, College of Animal Science and Technology, Beijing University of Agriculture, Beijing, ChinaDepartment of Animal Medicine, College of Animal Science and Technology, Beijing University of Agriculture, Beijing, ChinaDepartment of Animal Medicine, College of Animal Science and Technology, Beijing University of Agriculture, Beijing, ChinaDepartment of Animal Medicine, College of Animal Science and Technology, Beijing University of Agriculture, Beijing, ChinaDepartment of Animal Medicine, College of Animal Science and Technology, Beijing University of Agriculture, Beijing, ChinaDepartment of Animal Medicine, College of Animal Science and Technology, Beijing University of Agriculture, Beijing, ChinaDepartment of Animal Medicine, College of Animal Science and Technology, Beijing University of Agriculture, Beijing, ChinaDepartment of Clinical Veterinary Medicine, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaDepartment of Animal Medicine, College of Animal Science and Technology, Beijing University of Agriculture, Beijing, ChinaBeijing Key Laboratory of Traditional Chinese Veterinary Medicine, Beijing University of Agriculture, Beijing, ChinaEnterotoxigenic Escherichia coli (ETEC) is an important cause of post-weaning diarrhea (PWD) worldwide, resulting in huge economic losses to the swine industry worldwide. In this study, to understand the pathogenesis, the transcriptomic analysis was performed to explore the biological processes (BP) in porcine intestinal epithelial J2 cells infected with an emerging ETEC strain isolated from weaned pigs with diarrhea. Under the criteria of |fold change| (FC) ≥ 2 and P < 0.05 with false discovery rate < 0.05, a total of 131 referenced and 19 novel differentially expressed genes (DEGs) were identified after ETEC infection, including 96 upregulated DEGs and 54 downregulated DEGs. The Gene Ontology (GO) analysis of DEGs showed that ETEC evoked BP specifically involved in response to lipopolysaccharide (LPS) and negative regulation of intracellular signal transduction. The Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway analysis revealed that immune response-related pathways were mainly enriched in J2 cells after ETEC infection, in which tumor necrosis factor (TNF), interleukin 17, and mitogen-activated protein kinase (MAPK) signaling pathways possessed the highest rich factor, followed by nucleotide-binding and oligomerization domain-like receptor (NLRs), C-type lectin receptor (CLR), cytokine–cytokine receptor interaction, and Toll-like receptor (TLR), and nuclear factor kappa-B (NF-κB) signaling pathways. Furthermore, 30 of 131 referenced DEGs, especially the nuclear transcription factor AP-1 and NF-κB, participate in the immune response to infection through an integral signal cascade and can be target molecules for prevention and control of enteric ETEC infection by probiotic Lactobacillus reuteri. Our data provide a comprehensive insight into the immune response of porcine intestinal epithelial cells (IECs) to ETEC infection and advance the identification of targets for prevention and control of ETEC-related PWD.https://www.frontiersin.org/articles/10.3389/fvets.2021.677897/fulltranscriptome (RNA-seq)intestinal epithelia cellimmune responseEscherichia coliporcineenrichment analysis
spellingShingle Qiong Wu
Qiong Wu
Defeng Cui
Defeng Cui
Xinyu Chao
Peng Chen
Jiaxuan Liu
Yiding Wang
Tongjian Su
Meng Li
Ruyu Xu
Yaohong Zhu
Yonghong Zhang
Yonghong Zhang
Transcriptome Analysis Identifies Strategies Targeting Immune Response-Related Pathways to Control Enterotoxigenic Escherichia coli Infection in Porcine Intestinal Epithelial Cells
Frontiers in Veterinary Science
transcriptome (RNA-seq)
intestinal epithelia cell
immune response
Escherichia coli
porcine
enrichment analysis
title Transcriptome Analysis Identifies Strategies Targeting Immune Response-Related Pathways to Control Enterotoxigenic Escherichia coli Infection in Porcine Intestinal Epithelial Cells
title_full Transcriptome Analysis Identifies Strategies Targeting Immune Response-Related Pathways to Control Enterotoxigenic Escherichia coli Infection in Porcine Intestinal Epithelial Cells
title_fullStr Transcriptome Analysis Identifies Strategies Targeting Immune Response-Related Pathways to Control Enterotoxigenic Escherichia coli Infection in Porcine Intestinal Epithelial Cells
title_full_unstemmed Transcriptome Analysis Identifies Strategies Targeting Immune Response-Related Pathways to Control Enterotoxigenic Escherichia coli Infection in Porcine Intestinal Epithelial Cells
title_short Transcriptome Analysis Identifies Strategies Targeting Immune Response-Related Pathways to Control Enterotoxigenic Escherichia coli Infection in Porcine Intestinal Epithelial Cells
title_sort transcriptome analysis identifies strategies targeting immune response related pathways to control enterotoxigenic escherichia coli infection in porcine intestinal epithelial cells
topic transcriptome (RNA-seq)
intestinal epithelia cell
immune response
Escherichia coli
porcine
enrichment analysis
url https://www.frontiersin.org/articles/10.3389/fvets.2021.677897/full
work_keys_str_mv AT qiongwu transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT qiongwu transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT defengcui transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT defengcui transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT xinyuchao transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT pengchen transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT jiaxuanliu transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT yidingwang transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT tongjiansu transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT mengli transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT ruyuxu transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT yaohongzhu transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT yonghongzhang transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells
AT yonghongzhang transcriptomeanalysisidentifiesstrategiestargetingimmuneresponserelatedpathwaystocontrolenterotoxigenicescherichiacoliinfectioninporcineintestinalepithelialcells