Transcriptome Analysis of miRNA and mRNA in Porcine Skeletal Muscle following <i>Glaesserella parasuis</i> Challenge

<i>Glaesserella parasuis</i> (<i>G. parasuis</i>) causes systemic infection in pigs, but its effects on skeletal muscle and underlying mechanisms are poorly understood. We investigated <i>G. parasuis</i> infection in colostrum-deprived piglets, observing decreased...

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Main Authors: Huanhuan Zhou, Xuexue Chen, Xiangwei Deng, Xiaoyu Zhang, Xinqi Zeng, Ke Xu, Hongbo Chen
Format: Article
Language:English
Published: MDPI AG 2024-03-01
Series:Genes
Subjects:
Online Access:https://www.mdpi.com/2073-4425/15/3/359
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author Huanhuan Zhou
Xuexue Chen
Xiangwei Deng
Xiaoyu Zhang
Xinqi Zeng
Ke Xu
Hongbo Chen
author_facet Huanhuan Zhou
Xuexue Chen
Xiangwei Deng
Xiaoyu Zhang
Xinqi Zeng
Ke Xu
Hongbo Chen
author_sort Huanhuan Zhou
collection DOAJ
description <i>Glaesserella parasuis</i> (<i>G. parasuis</i>) causes systemic infection in pigs, but its effects on skeletal muscle and underlying mechanisms are poorly understood. We investigated <i>G. parasuis</i> infection in colostrum-deprived piglets, observing decreased daily weight gain and upregulation of inflammatory factors in skeletal muscle. Muscle fiber area and diameter were significantly reduced in the treated group (<i>n</i> = 3) compared to the control group (<i>n</i> = 3), accompanied by increased expression of <i>FOXO1</i>, <i>FBXO32</i>, <i>TRIM63</i>, <i>CTSL</i>, and <i>BNIP3</i>. Based on mRNA and microRNA (miRNA) sequencing, we identified 1642 differentially expressed (DE) mRNAs and 19 known DE miRNAs in skeletal muscle tissues between the two groups. We predicted target genes with opposite expression patterns to the 19 miRNAs and found significant enrichment and activation of the FoxO signaling pathway. We found that the upregulated core effectors <i>FOXO1</i> and <i>FOXO4</i> were targeted by downregulated ssc-miR-486, ssc-miR-370, ssc-miR-615, and ssc-miR-224. Further investigation showed that their downstream upregulated genes involved in protein degradation were also targeted by the downregulated ssc-miR-370, ssc-miR-615, ssc-miR-194a-5p, and ssc-miR-194b-5p. These findings suggest that <i>G. parasuis</i> infection causes skeletal muscle atrophy in piglets through accelerated protein degradation mediated by the “miRNAs-<i>FOXO1/4</i>” axis, while further research is necessary to validate the regulatory relationships. Our results provide new insights into the understanding of systemic inflammation growth mechanisms caused by <i>G. parasuis</i> and the role of miRNAs in bacterial infection pathogenesis.
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spelling doaj.art-16163d1957b7452da53ebeabb4f07a892024-03-27T13:43:11ZengMDPI AGGenes2073-44252024-03-0115335910.3390/genes15030359Transcriptome Analysis of miRNA and mRNA in Porcine Skeletal Muscle following <i>Glaesserella parasuis</i> ChallengeHuanhuan Zhou0Xuexue Chen1Xiangwei Deng2Xiaoyu Zhang3Xinqi Zeng4Ke Xu5Hongbo Chen6Laboratory of Genetic Breeding, Reproduction and Precision Livestock Farming, School of Animal Science and Nutritional Engineering, Wuhan Polytechnic University, Wuhan 430023, ChinaLaboratory of Genetic Breeding, Reproduction and Precision Livestock Farming, School of Animal Science and Nutritional Engineering, Wuhan Polytechnic University, Wuhan 430023, ChinaLaboratory of Genetic Breeding, Reproduction and Precision Livestock Farming, School of Animal Science and Nutritional Engineering, Wuhan Polytechnic University, Wuhan 430023, ChinaLaboratory of Genetic Breeding, Reproduction and Precision Livestock Farming, School of Animal Science and Nutritional Engineering, Wuhan Polytechnic University, Wuhan 430023, ChinaLaboratory of Genetic Breeding, Reproduction and Precision Livestock Farming, School of Animal Science and Nutritional Engineering, Wuhan Polytechnic University, Wuhan 430023, ChinaLaboratory of Genetic Breeding, Reproduction and Precision Livestock Farming, School of Animal Science and Nutritional Engineering, Wuhan Polytechnic University, Wuhan 430023, ChinaLaboratory of Genetic Breeding, Reproduction and Precision Livestock Farming, School of Animal Science and Nutritional Engineering, Wuhan Polytechnic University, Wuhan 430023, China<i>Glaesserella parasuis</i> (<i>G. parasuis</i>) causes systemic infection in pigs, but its effects on skeletal muscle and underlying mechanisms are poorly understood. We investigated <i>G. parasuis</i> infection in colostrum-deprived piglets, observing decreased daily weight gain and upregulation of inflammatory factors in skeletal muscle. Muscle fiber area and diameter were significantly reduced in the treated group (<i>n</i> = 3) compared to the control group (<i>n</i> = 3), accompanied by increased expression of <i>FOXO1</i>, <i>FBXO32</i>, <i>TRIM63</i>, <i>CTSL</i>, and <i>BNIP3</i>. Based on mRNA and microRNA (miRNA) sequencing, we identified 1642 differentially expressed (DE) mRNAs and 19 known DE miRNAs in skeletal muscle tissues between the two groups. We predicted target genes with opposite expression patterns to the 19 miRNAs and found significant enrichment and activation of the FoxO signaling pathway. We found that the upregulated core effectors <i>FOXO1</i> and <i>FOXO4</i> were targeted by downregulated ssc-miR-486, ssc-miR-370, ssc-miR-615, and ssc-miR-224. Further investigation showed that their downstream upregulated genes involved in protein degradation were also targeted by the downregulated ssc-miR-370, ssc-miR-615, ssc-miR-194a-5p, and ssc-miR-194b-5p. These findings suggest that <i>G. parasuis</i> infection causes skeletal muscle atrophy in piglets through accelerated protein degradation mediated by the “miRNAs-<i>FOXO1/4</i>” axis, while further research is necessary to validate the regulatory relationships. Our results provide new insights into the understanding of systemic inflammation growth mechanisms caused by <i>G. parasuis</i> and the role of miRNAs in bacterial infection pathogenesis.https://www.mdpi.com/2073-4425/15/3/359pig<i>G. parasuis</i>skeletal muscle atrophymiRNAstranscriptome
spellingShingle Huanhuan Zhou
Xuexue Chen
Xiangwei Deng
Xiaoyu Zhang
Xinqi Zeng
Ke Xu
Hongbo Chen
Transcriptome Analysis of miRNA and mRNA in Porcine Skeletal Muscle following <i>Glaesserella parasuis</i> Challenge
Genes
pig
<i>G. parasuis</i>
skeletal muscle atrophy
miRNAs
transcriptome
title Transcriptome Analysis of miRNA and mRNA in Porcine Skeletal Muscle following <i>Glaesserella parasuis</i> Challenge
title_full Transcriptome Analysis of miRNA and mRNA in Porcine Skeletal Muscle following <i>Glaesserella parasuis</i> Challenge
title_fullStr Transcriptome Analysis of miRNA and mRNA in Porcine Skeletal Muscle following <i>Glaesserella parasuis</i> Challenge
title_full_unstemmed Transcriptome Analysis of miRNA and mRNA in Porcine Skeletal Muscle following <i>Glaesserella parasuis</i> Challenge
title_short Transcriptome Analysis of miRNA and mRNA in Porcine Skeletal Muscle following <i>Glaesserella parasuis</i> Challenge
title_sort transcriptome analysis of mirna and mrna in porcine skeletal muscle following i glaesserella parasuis i challenge
topic pig
<i>G. parasuis</i>
skeletal muscle atrophy
miRNAs
transcriptome
url https://www.mdpi.com/2073-4425/15/3/359
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