Skin immune response to Aeromonas hydrophila infection in crucian carp Carassius auratus revealed by multi-omics analysis

Li, Xiaowei; Hu, Xiucai; Lü, Aijun; Guan, Zhenguo

doi:10.1016/j.fsi.2022.07.036

Cited by 19 publications

(7 citation statements)

References 56 publications

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“…Propionic acid may be produced by Proteobacteria, which could act as an HDAC inhibitor and thereby promote the release of the anti-inflammatory factor TGF-β , which plays an important role in the regulation of intestinal inflammation ( 80 , 81 ). Previously, the isobaric tags for relative and absolute quantitation (iTRAQ) analysis of differentially expressed proteins of crucian carp infected with Aeromonas hydrophila was performed by our group, and enrichment analysis obtained TLR, TGF-beta, and NF-κB signaling pathways ( 20 , 28 ). However, the functional validation and analysis of target gene proteins were of great significance in fish immunology.…”

Section: Discussionmentioning

confidence: 99%

“…Very recently, the integration of miRNA and mRNA analyses revealed the potential roles of the identified known miRNAs that are involved in the regulation of glycometabolism-related pathways in common carp Cyprinus carpio ( 26 ). Previous studies revealed that mucosal immune responses in crucian carp include the TLR, NOD-like receptor (NLR), and complement and coagulation pathways ( 20 , 27 , 28 ). However, there are few transcriptome analyses of miRNAs (e.g., miR-17, miR-26a, miR-144, and miR-146a) related to the involvement in the mucosal immune response of miRNA and the intestinal microflora regulation function in crucian carp ( 20 ).…”

Section: Introductionmentioning

confidence: 99%

“…In previous studies by our group, a new pathogenic R. aquatilis KCL-5 strain was isolated from diseased crucian carp ( 27 , 30 – 32 ). Subsequently, we detailedly studied the mucosal immunity (skin and gill) response of bacterial septicemia of crucian carp through multi-omics analysis ( 20 , 28 , 41 ). However, the molecular mechanism of the intestinal microflora, inflammation, and immune response-mediated miRNA–target gene axis in the mucosal immune regulation infected with R. aquatilis is still unclear.…”

Section: Introductionmentioning

confidence: 99%

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Multi-omics analysis of miRNA-mediated intestinal microflora changes in crucian carp Carassius auratus infected with Rahnella aquatilis

Huo,

Li,

et al. 2024

Front. Immunol.

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Infection by an emerging bacterial pathogen Rahnella aquatilis caused enteritis and septicemia in fish. However, the molecular pathogenesis of enteritis induced by R. aquatilis infection and its interacting mechanism of the intestinal microflora associated with microRNA (miRNA) immune regulation in crucian carp Carassius auratus are still unclear. In this study, C. auratus intraperitoneally injected with R. aquatilis KCL-5 was used as an experimental animal model, and the intestinal pathological changes, microflora, and differentially expressed miRNAs (DEMs) were investigated by multi-omics analysis. The significant changes in histopathological features, apoptotic cells, and enzyme activities (e.g., lysozyme (LYS), alkaline phosphatase (AKP), alanine aminotransferase (ALT), aspartate transaminase (AST), and glutathione peroxidase (GSH-Px)) in the intestine were examined after infection. Diversity and composition analysis of the intestinal microflora clearly demonstrated four dominant bacteria: Proteobacteria, Fusobacteria, Bacteroidetes, and Firmicutes. A total of 87 DEMs were significantly screened, and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses revealed that the potential target genes were mainly involved in the regulation of lipid, glutathione, cytosine, and purine metabolism, which participated in the local immune response through the intestinal immune network for IgA production, lysosome, and Toll-like receptor (TLR) pathways. Moreover, the expression levels of 11 target genes (e.g., TLR3, MyD88, NF-κB, TGF-β, TNF-α, MHC II, IL-22, LysC, F2, F5, and C3) related to inflammation and immunity were verified by qRT-PCR detection. The correlation analysis indicated that the abundance of intestinal Firmicutes and Proteobacteria was significantly associated with the high local expression of miR-203/NF-κB, miR-129/TNF-α, and miR-205/TGF-β. These findings will help to elucidate the molecular regulation mechanism of the intestinal microflora, inflammation, and immune response-mediated miRNA–target gene axis in cyprinid fish.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Multi-omics analysis of miRNA-mediated intestinal microflora changes in crucian carp Carassius auratus infected with Rahnella aquatilis

Huo,

Li,

et al. 2024

Front. Immunol.

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“…In addition, the miRNAs interacting with the target genes and proteins were not only associated with immune response ( 7 , 45 ) but also played important roles in regulating the regulators of the immune network ( 28 , 58 ). In M. miiuy infected with Vibrio harveyi , miR-148 targeted and negatively regulated the expression of the MyD88 gene, and overexpression of miR-148 inhibited the inflammatory cytokine production of both IL-6 and IL-1β ( 16 ).…”

Section: Discussionmentioning

confidence: 99%

“…Recently, the characterization of the miRNAs and target genes in the internal organs (e.g., kidney, spleen, and liver) and skin of C. auratus has been performed using deep sequencing analysis ( 5 , 18 ). Moreover, proteomic analyses (e.g., iTRAQ and 2-DE/MS) were performed in zebrafish gills and crucian carp skin after A. hydrophila infection ( 19 , 28 ). However, the miRNA expression and its regulatory mechanism in the gills of C. auratus are still unclear.…”

Section: Introductionmentioning

confidence: 99%

Multiomics analysis revealed miRNAs as potential regulators of the immune response in Carassius auratus gills to Aeromonas hydrophila infection

Huo

Bai

et al. 2023

Front. Immunol.

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The gill of fish is an important immune organ for pathogen defense, but its microRNA (miRNA) expression and regulatory mechanism remain unclear. In this study, we report on the histopathological and immunohistochemical features of the gills of the crucian carp Carassius auratus challenged with Aeromonas hydrophila. Small RNA libraries of the gills were constructed and sequenced on the Illumina HiSeq 2000 platform. A total of 1,165 differentially expressed miRNAs (DEMs) were identified in gills, of which 539 known and 7 unknown DEMs were significantly screened (p < 0.05). Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses revealed that the potential target genes/proteins were primarily involved in 33 immune-related pathways, in which the inflammatory responses were focused on the Toll-like receptor (TLR), mitogen-activated protein kinase (MAPK), and nuclear factor kappa B (NF-κB) signaling pathways. Moreover, the expression levels of 14 key miRNAs (e.g., miR-10, miR-17, miR-26a, miR-144, miR-145, and miR-146a) and their target genes (e.g., TNFα, TLR4, NF-κB, TAB1, PI3K, and IRAK1) were verified. In addition, the protein levels based on isobaric tags for relative and absolute quantification (iTRAQ) were significantly associated with the results of the quantitative real-time PCR (qRT-PCR) analysis (p < 0.01). miR-17/pre-miR-17 were identified in the regulation expression of the NF-κB target gene, and the phylogenetic tree analysis showed that the pre-miR-17 of C. auratus with the closest similarity to the zebrafish Danio rerio is highly conserved in teleosts. This is the first report of the multi-omics analysis of the miRNAs and proteins in the gills of C. auratus infected with A. hydrophila, thus enriching knowledge on the regulation mechanism of the local immune response in Cyprinidae fish.

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Identification of Single-Nucleotide Polymorphisms in Differentially Expressed Genes Favoring Soybean Meal Tolerance in Higher-Growth Zebrafish (Danio rerio)

Ulloa,

Jilberto,

Lam

et al. 2024

Mar Biotechnol

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Skin immune response to Aeromonas hydrophila infection in crucian carp Carassius auratus revealed by multi-omics analysis

Cited by 19 publications

References 56 publications

Multi-omics analysis of miRNA-mediated intestinal microflora changes in crucian carp Carassius auratus infected with Rahnella aquatilis

Multi-omics analysis of miRNA-mediated intestinal microflora changes in crucian carp Carassius auratus infected with Rahnella aquatilis

Multiomics analysis revealed miRNAs as potential regulators of the immune response in Carassius auratus gills to Aeromonas hydrophila infection

Identification of Single-Nucleotide Polymorphisms in Differentially Expressed Genes Favoring Soybean Meal Tolerance in Higher-Growth Zebrafish (Danio rerio)

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