Comprehensive profiling of lncRNAs in the immune response of largemouth bass to Nocardia Seriolae infection

Long noncoding RNAs (lncRNAs) are crucial regulators of various biological processes. However, it remains unclear how lncRNAs can be involved in the immune response to Nocardia seriolae invasion in largemouth bass (Micropterus salmoides). Here we leveraged the whole transcriptome RNA-seq technique t...

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Main Authors: Xiaona Fu, Longsheng Zhang, Keqi Li, Zhigang Liu, Jikui Wu, Junling Zhang
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Comparative Immunology Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2950311624000326
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author Xiaona Fu
Longsheng Zhang
Keqi Li
Zhigang Liu
Jikui Wu
Junling Zhang
author_facet Xiaona Fu
Longsheng Zhang
Keqi Li
Zhigang Liu
Jikui Wu
Junling Zhang
author_sort Xiaona Fu
collection DOAJ
description Long noncoding RNAs (lncRNAs) are crucial regulators of various biological processes. However, it remains unclear how lncRNAs can be involved in the immune response to Nocardia seriolae invasion in largemouth bass (Micropterus salmoides). Here we leveraged the whole transcriptome RNA-seq technique to screen lncRNAs associated with the head kidney infected with Nocardia seriolae. A total of 5,661 lncRNAs were identified, comprising 2,427 known lncRNAs and 3,234 novel lncRNAs. Among these, 531 lncRNAs were found to be differentially expressed, with 213 showing increased expression and 318 showing reduced expression. In these differentially expressed lncRNAs, 176 lncRNAs may have cis-regulatory relationships with 243 protein-coding genes. For example, MSTRG.17818.1, MSTRG.10160.1 target mapk1 and rela, respectively, thereby regulating gene expression. We then exploited Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) to analyze the enrichment of target genes of lncRNAs. These target genes were found to be significantly enriched in immune signaling pathways, including RIG-I-like receptor signaling and Toll-like receptor signaling. Furthermore, we harnessed a total of 12 mRNAs, 33 miRNAs, and 167 lncRNAs to construct two lncRNA-miRNA-mRNA network maps. CeRNA maps revealed that some lncRNAs can competitively bind to the same miRNA and affect the expression of immune-related genes. For instance, MSTRG.13668.1 and MSTRG.5180.1 can simultaneously bind to mir-155–5p to increase irak4 expression. These findings suggest that lncRNAs may participate in the immune response process of infected largemouth bass with Nocardia seriolae. Overall, this work presents a thorough lncRNAs expression profile of Nocardia seriolae-infected largemouth bass and offers insights into the ceRNA regulatory processes that influence fish's immune response to bacterial infections.
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series Comparative Immunology Reports
spelling doaj-art-ad94e06c4a9e44109bade2a66b603e552024-12-18T08:56:02ZengElsevierComparative Immunology Reports2950-31162024-12-017200165Comprehensive profiling of lncRNAs in the immune response of largemouth bass to Nocardia Seriolae infectionXiaona Fu0Longsheng Zhang1Keqi Li2Zhigang Liu3Jikui Wu4Junling Zhang5Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai Engineering Research Center of Aquaculture, Shanghai 201306, PR ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai Engineering Research Center of Aquaculture, Shanghai 201306, PR ChinaKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai Engineering Research Center of Aquaculture, Shanghai 201306, PR ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, Guangzhou 510380, PR ChinaLaboratory of Quality and Safety Risk Assessment for Aquatic Product on Storage and Preservation, Ministry of Agriculture, Shanghai Ocean University, Shanghai 201306, PR China; Corresponding authors.Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai Engineering Research Center of Aquaculture, Shanghai 201306, PR China; Corresponding authors.Long noncoding RNAs (lncRNAs) are crucial regulators of various biological processes. However, it remains unclear how lncRNAs can be involved in the immune response to Nocardia seriolae invasion in largemouth bass (Micropterus salmoides). Here we leveraged the whole transcriptome RNA-seq technique to screen lncRNAs associated with the head kidney infected with Nocardia seriolae. A total of 5,661 lncRNAs were identified, comprising 2,427 known lncRNAs and 3,234 novel lncRNAs. Among these, 531 lncRNAs were found to be differentially expressed, with 213 showing increased expression and 318 showing reduced expression. In these differentially expressed lncRNAs, 176 lncRNAs may have cis-regulatory relationships with 243 protein-coding genes. For example, MSTRG.17818.1, MSTRG.10160.1 target mapk1 and rela, respectively, thereby regulating gene expression. We then exploited Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) to analyze the enrichment of target genes of lncRNAs. These target genes were found to be significantly enriched in immune signaling pathways, including RIG-I-like receptor signaling and Toll-like receptor signaling. Furthermore, we harnessed a total of 12 mRNAs, 33 miRNAs, and 167 lncRNAs to construct two lncRNA-miRNA-mRNA network maps. CeRNA maps revealed that some lncRNAs can competitively bind to the same miRNA and affect the expression of immune-related genes. For instance, MSTRG.13668.1 and MSTRG.5180.1 can simultaneously bind to mir-155–5p to increase irak4 expression. These findings suggest that lncRNAs may participate in the immune response process of infected largemouth bass with Nocardia seriolae. Overall, this work presents a thorough lncRNAs expression profile of Nocardia seriolae-infected largemouth bass and offers insights into the ceRNA regulatory processes that influence fish's immune response to bacterial infections.http://www.sciencedirect.com/science/article/pii/S2950311624000326Largemouth bassNocardia seriolaeHead kidneylncRNACERNA, Immune response
spellingShingle Xiaona Fu
Longsheng Zhang
Keqi Li
Zhigang Liu
Jikui Wu
Junling Zhang
Comprehensive profiling of lncRNAs in the immune response of largemouth bass to Nocardia Seriolae infection
Comparative Immunology Reports
Largemouth bass
Nocardia seriolae
Head kidney
lncRNA
CERNA, Immune response
title Comprehensive profiling of lncRNAs in the immune response of largemouth bass to Nocardia Seriolae infection
title_full Comprehensive profiling of lncRNAs in the immune response of largemouth bass to Nocardia Seriolae infection
title_fullStr Comprehensive profiling of lncRNAs in the immune response of largemouth bass to Nocardia Seriolae infection
title_full_unstemmed Comprehensive profiling of lncRNAs in the immune response of largemouth bass to Nocardia Seriolae infection
title_short Comprehensive profiling of lncRNAs in the immune response of largemouth bass to Nocardia Seriolae infection
title_sort comprehensive profiling of lncrnas in the immune response of largemouth bass to nocardia seriolae infection
topic Largemouth bass
Nocardia seriolae
Head kidney
lncRNA
CERNA, Immune response
url http://www.sciencedirect.com/science/article/pii/S2950311624000326
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