Identification of Potential miRNA-mRNA Regulatory Network Associated with Regulating Immunity and Metabolism in Pigs Induced by ASFV Infection

African swine fever (ASF) is a devastating infectious disease in domestic pigs caused by African swine fever virus (ASFV) with a mortality rate of about 100%. However, the understanding of the interaction between ASFV and host is still not clear. In this study, the expression differences and functio...

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Main Authors: Zhongbao Pang, Shiyu Chen, Shuai Cui, Wenzhu Zhai, Ying Huang, Xintao Gao, Yang Wang, Fei Jiang, Xiaoyu Guo, Yuxin Hao, Wencai Li, Lei Wang, Hongfei Zhu, Jiajun Wu, Hong Jia
Format: Article
Language:English
Published: MDPI AG 2023-04-01
Series:Animals
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Online Access:https://www.mdpi.com/2076-2615/13/7/1246
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author Zhongbao Pang
Shiyu Chen
Shuai Cui
Wenzhu Zhai
Ying Huang
Xintao Gao
Yang Wang
Fei Jiang
Xiaoyu Guo
Yuxin Hao
Wencai Li
Lei Wang
Hongfei Zhu
Jiajun Wu
Hong Jia
author_facet Zhongbao Pang
Shiyu Chen
Shuai Cui
Wenzhu Zhai
Ying Huang
Xintao Gao
Yang Wang
Fei Jiang
Xiaoyu Guo
Yuxin Hao
Wencai Li
Lei Wang
Hongfei Zhu
Jiajun Wu
Hong Jia
author_sort Zhongbao Pang
collection DOAJ
description African swine fever (ASF) is a devastating infectious disease in domestic pigs caused by African swine fever virus (ASFV) with a mortality rate of about 100%. However, the understanding of the interaction between ASFV and host is still not clear. In this study, the expression differences and functional analysis of microRNA (miRNA) in porcine peripheral blood lymphocytes of ASFV infected pigs and healthy pigs were compared based on Illumina high-throughput sequencing, then the GO and KEGG signal pathways were analyzed. The miRNA related to immunity and inflammation were screened, and the regulatory network of miRNA-mRNA was drawn. A total of 70 differentially expressed miRNAs were found (<i>p</i> ≤ 0.05). Of these, 45 were upregulated and 25 were downregulated in ASFV-infected pigs vs. healthy pigs. A total of 8179 mRNA genes targeted by these 70 differentially expressed miRNA were predicted, of which 1447 mRNA genes were targeted by ssc-miR-2320-5p. Five differentially expressed miRNA were validated by RT-qPCR, which were consistent with the RNA-Seq results. The GO analysis revealed that a total of 30 gene functions were significantly enriched, including 7 molecular functions (MF), 13 cellular components (CC), and 10 biological processes (BP). The KEGG enrichment analysis revealed that the differentially expressed genes were significantly enriched in pathways related to immunity, inflammation, and various metabolic processes, in which a total of two downregulated miRNAs after infection and eight upregulated miRNAs related to immunity and inflammation were screened in ASFV-infected pigs vs. healthy pigs. The network of miRNA-mRNA showed that the mRNA target genes were strongly regulated by ssc-miR-214, ssc-miR-199b-3p, and ssc-miR-199a-3p. The mRNA target genes were enriched into the MAPK signaling pathway, Toll-like receptor signaling pathway, TNF signaling pathway, and IL-17 signaling pathway by using a KEGG enrichment analysis. Therefore, ASFV could regulate immunity and metabolism-related pathways in infected pigs by inducing differential expression of miRNAs. These results provided a new basis for further elucidating the interactions between ASFV and the host as well as the immunity regulation mechanisms of ASFV, which will be conducive to better controlling ASF.
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spelling doaj.art-1eed5435ba444d259932d6abe4c726052023-11-17T16:14:47ZengMDPI AGAnimals2076-26152023-04-01137124610.3390/ani13071246Identification of Potential miRNA-mRNA Regulatory Network Associated with Regulating Immunity and Metabolism in Pigs Induced by ASFV InfectionZhongbao Pang0Shiyu Chen1Shuai Cui2Wenzhu Zhai3Ying Huang4Xintao Gao5Yang Wang6Fei Jiang7Xiaoyu Guo8Yuxin Hao9Wencai Li10Lei Wang11Hongfei Zhu12Jiajun Wu13Hong Jia14Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaCollege of Animal Medicine, Shandong Vocational Animal Science and Veterinary College, Weifang 261061, ChinaInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaBiotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaChina Animal Disease Control Center, Beijing 100026, ChinaInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaChina Animal Disease Control Center, Beijing 100026, ChinaChina Animal Disease Control Center, Beijing 100026, ChinaChina Animal Disease Control Center, Beijing 100026, ChinaInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaChina Animal Disease Control Center, Beijing 100026, ChinaInstitute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaAfrican swine fever (ASF) is a devastating infectious disease in domestic pigs caused by African swine fever virus (ASFV) with a mortality rate of about 100%. However, the understanding of the interaction between ASFV and host is still not clear. In this study, the expression differences and functional analysis of microRNA (miRNA) in porcine peripheral blood lymphocytes of ASFV infected pigs and healthy pigs were compared based on Illumina high-throughput sequencing, then the GO and KEGG signal pathways were analyzed. The miRNA related to immunity and inflammation were screened, and the regulatory network of miRNA-mRNA was drawn. A total of 70 differentially expressed miRNAs were found (<i>p</i> ≤ 0.05). Of these, 45 were upregulated and 25 were downregulated in ASFV-infected pigs vs. healthy pigs. A total of 8179 mRNA genes targeted by these 70 differentially expressed miRNA were predicted, of which 1447 mRNA genes were targeted by ssc-miR-2320-5p. Five differentially expressed miRNA were validated by RT-qPCR, which were consistent with the RNA-Seq results. The GO analysis revealed that a total of 30 gene functions were significantly enriched, including 7 molecular functions (MF), 13 cellular components (CC), and 10 biological processes (BP). The KEGG enrichment analysis revealed that the differentially expressed genes were significantly enriched in pathways related to immunity, inflammation, and various metabolic processes, in which a total of two downregulated miRNAs after infection and eight upregulated miRNAs related to immunity and inflammation were screened in ASFV-infected pigs vs. healthy pigs. The network of miRNA-mRNA showed that the mRNA target genes were strongly regulated by ssc-miR-214, ssc-miR-199b-3p, and ssc-miR-199a-3p. The mRNA target genes were enriched into the MAPK signaling pathway, Toll-like receptor signaling pathway, TNF signaling pathway, and IL-17 signaling pathway by using a KEGG enrichment analysis. Therefore, ASFV could regulate immunity and metabolism-related pathways in infected pigs by inducing differential expression of miRNAs. These results provided a new basis for further elucidating the interactions between ASFV and the host as well as the immunity regulation mechanisms of ASFV, which will be conducive to better controlling ASF.https://www.mdpi.com/2076-2615/13/7/1246African swine fever virusmiRNAGO function enrichment analysismiRNA-mRNA networkKEGG signal pathway analysis
spellingShingle Zhongbao Pang
Shiyu Chen
Shuai Cui
Wenzhu Zhai
Ying Huang
Xintao Gao
Yang Wang
Fei Jiang
Xiaoyu Guo
Yuxin Hao
Wencai Li
Lei Wang
Hongfei Zhu
Jiajun Wu
Hong Jia
Identification of Potential miRNA-mRNA Regulatory Network Associated with Regulating Immunity and Metabolism in Pigs Induced by ASFV Infection
Animals
African swine fever virus
miRNA
GO function enrichment analysis
miRNA-mRNA network
KEGG signal pathway analysis
title Identification of Potential miRNA-mRNA Regulatory Network Associated with Regulating Immunity and Metabolism in Pigs Induced by ASFV Infection
title_full Identification of Potential miRNA-mRNA Regulatory Network Associated with Regulating Immunity and Metabolism in Pigs Induced by ASFV Infection
title_fullStr Identification of Potential miRNA-mRNA Regulatory Network Associated with Regulating Immunity and Metabolism in Pigs Induced by ASFV Infection
title_full_unstemmed Identification of Potential miRNA-mRNA Regulatory Network Associated with Regulating Immunity and Metabolism in Pigs Induced by ASFV Infection
title_short Identification of Potential miRNA-mRNA Regulatory Network Associated with Regulating Immunity and Metabolism in Pigs Induced by ASFV Infection
title_sort identification of potential mirna mrna regulatory network associated with regulating immunity and metabolism in pigs induced by asfv infection
topic African swine fever virus
miRNA
GO function enrichment analysis
miRNA-mRNA network
KEGG signal pathway analysis
url https://www.mdpi.com/2076-2615/13/7/1246
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