Regulation of mRNA and miRNA in the response to Salmonella enterica serovar Enteritidis infection in chicken cecum

Abstract Background Salmonella enterica, serovar Enteritidis (SE) is a food-borne pathogen, which can cause great threat to human health through consumption of the contaminated poultry products. Chicken is the main host of SE. The mRNA and microRNA (miRNA) expression profiles were analyzed on cecum...

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Main Authors: Xiuxiu Miao, Lewen Liu, Liying Liu, Geng Hu, Guixian Wu, Yuanmei Wang, Yanan Zhao, Jingchao Yang, Xianyao Li
Format: Article
Language:English
Published: BMC 2022-12-01
Series:BMC Veterinary Research
Subjects:
Online Access:https://doi.org/10.1186/s12917-022-03522-y
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author Xiuxiu Miao
Lewen Liu
Liying Liu
Geng Hu
Guixian Wu
Yuanmei Wang
Yanan Zhao
Jingchao Yang
Xianyao Li
author_facet Xiuxiu Miao
Lewen Liu
Liying Liu
Geng Hu
Guixian Wu
Yuanmei Wang
Yanan Zhao
Jingchao Yang
Xianyao Li
author_sort Xiuxiu Miao
collection DOAJ
description Abstract Background Salmonella enterica, serovar Enteritidis (SE) is a food-borne pathogen, which can cause great threat to human health through consumption of the contaminated poultry products. Chicken is the main host of SE. The mRNA and microRNA (miRNA) expression profiles were analyzed on cecum of Shouguang chicken via next-generation sequencing and bioinformatics approaches. The treated group was inoculated SE, and the control group was inoculated with phosphate buffer saline (PBS). Results There were 1760 differentially expressed mRNAs in the SE-infected group, of which 1046 were up-regulated mRNA, and 714 were down-regulated mRNA. In addition, a total of 821 miRNAs were identified, and 174 miRNAs were differentially expressed, of which 100 were up-regulated and 74 were down-regulated. Functional enrichment of differentially expressed mRNAs was similar to miRNA target genes. The functional analysis results of differentially expressed mRNAs and miRNAs were performed. Immune-related processes and KEGG (Kyoto Encyclopedia of Genes and Genomes) pathways were enriched by up-regulated mRNA. The down-regulated mRNAs were enriched in tissue development and metabolic-related KEGG pathways. The functional analysis of up-regulated miRNA target genes was similar to the down-regulated mRNAs. The down-regulated miRNA target genes were enriched in metabolic-related GO (Gene Ontology) -BP (Biological process) terms and KEGG pathways. The overlap of the up-regulated mRNA and the up-regulated miRNA target genes (class I) was 325, and the overlap of the down-regulated miRNA target genes (class II) was 169. The class I enriched in the immune-related GO-BP terms and KEGG pathways. The class II mainly enriched in metabolic-related GO-BP terms and KEGG pathways. Then we detected the expression of mRNA and miRNA through qRT-PCR. The results shown that the expression of HHIP, PGM1, HTR2B, ITGB5, RELN, SFRP1, TCF7L2, SCNN1A, NEK7, miR-20b-5p, miR-1662, miR-15a, miR-16-1-3p was significantly different between two groups. Dual-luciferase reporter assay was used to detect the relationship between miR-20b-5p and SCNN1A. The result indicated that miR-20b-5p regulate immune or metabolic responses after SE infection in Shouguang chickens by directly targeting SCNN1A. Conclusions The findings here contribute to the further analysis of the mechanism of mRNA and miRNA defense against SE infection, and provide a theoretical foundation for the molecular disease-resistant breeding of chickens.
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spelling doaj.art-e34449900c0c49de8834c675d04496df2022-12-22T04:23:44ZengBMCBMC Veterinary Research1746-61482022-12-0118111510.1186/s12917-022-03522-yRegulation of mRNA and miRNA in the response to Salmonella enterica serovar Enteritidis infection in chicken cecumXiuxiu Miao0Lewen Liu1Liying Liu2Geng Hu3Guixian Wu4Yuanmei Wang5Yanan Zhao6Jingchao Yang7Xianyao Li8College of Animal Science and Technology, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural UniversityCollege of Animal Science and Technology, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural UniversityCollege of Life Sciences, Shandong Agricultural UniversityCollege of Animal Science and Technology, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural UniversityCollege of Animal Science and Technology, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural UniversityCollege of Animal Science and Technology, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural UniversityCollege of Animal Science and Technology, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural UniversityShandong Animal Husbandry General StationCollege of Animal Science and Technology, Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural UniversityAbstract Background Salmonella enterica, serovar Enteritidis (SE) is a food-borne pathogen, which can cause great threat to human health through consumption of the contaminated poultry products. Chicken is the main host of SE. The mRNA and microRNA (miRNA) expression profiles were analyzed on cecum of Shouguang chicken via next-generation sequencing and bioinformatics approaches. The treated group was inoculated SE, and the control group was inoculated with phosphate buffer saline (PBS). Results There were 1760 differentially expressed mRNAs in the SE-infected group, of which 1046 were up-regulated mRNA, and 714 were down-regulated mRNA. In addition, a total of 821 miRNAs were identified, and 174 miRNAs were differentially expressed, of which 100 were up-regulated and 74 were down-regulated. Functional enrichment of differentially expressed mRNAs was similar to miRNA target genes. The functional analysis results of differentially expressed mRNAs and miRNAs were performed. Immune-related processes and KEGG (Kyoto Encyclopedia of Genes and Genomes) pathways were enriched by up-regulated mRNA. The down-regulated mRNAs were enriched in tissue development and metabolic-related KEGG pathways. The functional analysis of up-regulated miRNA target genes was similar to the down-regulated mRNAs. The down-regulated miRNA target genes were enriched in metabolic-related GO (Gene Ontology) -BP (Biological process) terms and KEGG pathways. The overlap of the up-regulated mRNA and the up-regulated miRNA target genes (class I) was 325, and the overlap of the down-regulated miRNA target genes (class II) was 169. The class I enriched in the immune-related GO-BP terms and KEGG pathways. The class II mainly enriched in metabolic-related GO-BP terms and KEGG pathways. Then we detected the expression of mRNA and miRNA through qRT-PCR. The results shown that the expression of HHIP, PGM1, HTR2B, ITGB5, RELN, SFRP1, TCF7L2, SCNN1A, NEK7, miR-20b-5p, miR-1662, miR-15a, miR-16-1-3p was significantly different between two groups. Dual-luciferase reporter assay was used to detect the relationship between miR-20b-5p and SCNN1A. The result indicated that miR-20b-5p regulate immune or metabolic responses after SE infection in Shouguang chickens by directly targeting SCNN1A. Conclusions The findings here contribute to the further analysis of the mechanism of mRNA and miRNA defense against SE infection, and provide a theoretical foundation for the molecular disease-resistant breeding of chickens.https://doi.org/10.1186/s12917-022-03522-ySalmonella enterica serovar EnteritidisShouguang chickenCecumTranscriptome sequencingmiRNA
spellingShingle Xiuxiu Miao
Lewen Liu
Liying Liu
Geng Hu
Guixian Wu
Yuanmei Wang
Yanan Zhao
Jingchao Yang
Xianyao Li
Regulation of mRNA and miRNA in the response to Salmonella enterica serovar Enteritidis infection in chicken cecum
BMC Veterinary Research
Salmonella enterica serovar Enteritidis
Shouguang chicken
Cecum
Transcriptome sequencing
miRNA
title Regulation of mRNA and miRNA in the response to Salmonella enterica serovar Enteritidis infection in chicken cecum
title_full Regulation of mRNA and miRNA in the response to Salmonella enterica serovar Enteritidis infection in chicken cecum
title_fullStr Regulation of mRNA and miRNA in the response to Salmonella enterica serovar Enteritidis infection in chicken cecum
title_full_unstemmed Regulation of mRNA and miRNA in the response to Salmonella enterica serovar Enteritidis infection in chicken cecum
title_short Regulation of mRNA and miRNA in the response to Salmonella enterica serovar Enteritidis infection in chicken cecum
title_sort regulation of mrna and mirna in the response to salmonella enterica serovar enteritidis infection in chicken cecum
topic Salmonella enterica serovar Enteritidis
Shouguang chicken
Cecum
Transcriptome sequencing
miRNA
url https://doi.org/10.1186/s12917-022-03522-y
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