Integrated bioinformatics identifies key mediators in cytokine storm and tissue remodeling during Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco)
IntroductionThe pathogenesis of Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco) remains poorly understood, particularly regarding the impact of infection with the pathogen on primary target organs such as the skin and muscle.MethodsIn this study, we aim to analyze the pathologic...
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1172849/full |
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| author | Yang Feng Jiao Wang Wei Fan Yi Geng Xiaoli Huang Ping Ouyang Defang Chen Hongrui Guo Huidan Deng Weimin Lai Zhicai Zuo |
| author_facet | Yang Feng Jiao Wang Wei Fan Yi Geng Xiaoli Huang Ping Ouyang Defang Chen Hongrui Guo Huidan Deng Weimin Lai Zhicai Zuo |
| author_sort | Yang Feng |
| collection | DOAJ |
| description | IntroductionThe pathogenesis of Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco) remains poorly understood, particularly regarding the impact of infection with the pathogen on primary target organs such as the skin and muscle.MethodsIn this study, we aim to analyze the pathological intricacies of the skin and muscle of yellow catfish after being infected with V. mimicus using a 1/10 LC50 seven-day post-infection model. Furthermore, we have utilized integrated bioinformatics to comprehensively elucidate the regulatory mechanisms and identify the key regulatory genes implicated in this phenomenon.ResultsOur histopathological examination revealed significant pathological changes in the skin and muscle, characterized by necrosis and inflammation. Moreover, tissue remodeling occurred, with perimysium degeneration and lesion invasion into the muscle along the endomysium, accompanied by a transformation of type I collagen into a mixture of type I and type III collagens in the perimysium and muscle bundles. Our eukaryotic transcriptomic and 4D label-free analyses demonstrated a predominantly immune pathway response in both the skin and muscle, with downregulation observed in several cell signaling pathways that focused on focal adhesion-dominated cell signaling pathways. The upregulated genes included interleukins (IL)-1 and -6, chemokines, and matrix metallopeptidases (mmp)-9 and -13, while several genes were significantly downregulated, including col1a and col1a1a. Further analysis revealed that these pathways were differentially regulated, with mmp-9 and mmp-13 acting as the potential core regulators of cytokine and tissue remodeling pathways. Upregulation of NF-κB1 and FOSL-1 induced by IL-17C and Nox 1/2-based NADPH oxidase may have held matrix metallopeptidase and cytokine-related genes. Also, we confirmed these relevant regulatory pathways by qPCR and ELISA in expanded samples.DiscussionOur findings unequivocally illustrate the occurrence of a cytokine storm and tissue remodeling, mediated by interleukins, chemokines, and MMPs, in the surface of yellow catfish infected with V. mimicus. Additionally, we unveil the potential bidirectional regulatory role of MMP-9 and MMP-13. These results provide novel perspectives on the intricate immune response to V. mimicus infection in yellow catfish and highlight potential targets for developing therapies. |
| first_indexed | 2024-03-13T10:10:37Z |
| format | Article |
| id | doaj.art-7cc25d814f114406b0b207601a457026 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-03-13T10:10:37Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Immunology |
| spelling | doaj.art-7cc25d814f114406b0b207601a4570262023-05-22T04:27:47ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-05-011410.3389/fimmu.2023.11728491172849Integrated bioinformatics identifies key mediators in cytokine storm and tissue remodeling during Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco)Yang Feng0Jiao Wang1Wei Fan2Yi Geng3Xiaoli Huang4Ping Ouyang5Defang Chen6Hongrui Guo7Huidan Deng8Weimin Lai9Zhicai Zuo10College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaDepartment of Aquaculture, College of Animal Science & Technology, Sichuan Agricultural University, Chengdu, Sichuan, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaDepartment of Aquaculture, College of Animal Science & Technology, Sichuan Agricultural University, Chengdu, Sichuan, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaCollege of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, ChinaIntroductionThe pathogenesis of Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco) remains poorly understood, particularly regarding the impact of infection with the pathogen on primary target organs such as the skin and muscle.MethodsIn this study, we aim to analyze the pathological intricacies of the skin and muscle of yellow catfish after being infected with V. mimicus using a 1/10 LC50 seven-day post-infection model. Furthermore, we have utilized integrated bioinformatics to comprehensively elucidate the regulatory mechanisms and identify the key regulatory genes implicated in this phenomenon.ResultsOur histopathological examination revealed significant pathological changes in the skin and muscle, characterized by necrosis and inflammation. Moreover, tissue remodeling occurred, with perimysium degeneration and lesion invasion into the muscle along the endomysium, accompanied by a transformation of type I collagen into a mixture of type I and type III collagens in the perimysium and muscle bundles. Our eukaryotic transcriptomic and 4D label-free analyses demonstrated a predominantly immune pathway response in both the skin and muscle, with downregulation observed in several cell signaling pathways that focused on focal adhesion-dominated cell signaling pathways. The upregulated genes included interleukins (IL)-1 and -6, chemokines, and matrix metallopeptidases (mmp)-9 and -13, while several genes were significantly downregulated, including col1a and col1a1a. Further analysis revealed that these pathways were differentially regulated, with mmp-9 and mmp-13 acting as the potential core regulators of cytokine and tissue remodeling pathways. Upregulation of NF-κB1 and FOSL-1 induced by IL-17C and Nox 1/2-based NADPH oxidase may have held matrix metallopeptidase and cytokine-related genes. Also, we confirmed these relevant regulatory pathways by qPCR and ELISA in expanded samples.DiscussionOur findings unequivocally illustrate the occurrence of a cytokine storm and tissue remodeling, mediated by interleukins, chemokines, and MMPs, in the surface of yellow catfish infected with V. mimicus. Additionally, we unveil the potential bidirectional regulatory role of MMP-9 and MMP-13. These results provide novel perspectives on the intricate immune response to V. mimicus infection in yellow catfish and highlight potential targets for developing therapies.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1172849/fullVibrio mimicusYellow catfish (Pelteobagrus fulvidraco)skin and musclehistopathologyintegrated bioinformaticssignaling pathway |
| spellingShingle | Yang Feng Jiao Wang Wei Fan Yi Geng Xiaoli Huang Ping Ouyang Defang Chen Hongrui Guo Huidan Deng Weimin Lai Zhicai Zuo Integrated bioinformatics identifies key mediators in cytokine storm and tissue remodeling during Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco) Frontiers in Immunology Vibrio mimicus Yellow catfish (Pelteobagrus fulvidraco) skin and muscle histopathology integrated bioinformatics signaling pathway |
| title | Integrated bioinformatics identifies key mediators in cytokine storm and tissue remodeling during Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco) |
| title_full | Integrated bioinformatics identifies key mediators in cytokine storm and tissue remodeling during Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco) |
| title_fullStr | Integrated bioinformatics identifies key mediators in cytokine storm and tissue remodeling during Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco) |
| title_full_unstemmed | Integrated bioinformatics identifies key mediators in cytokine storm and tissue remodeling during Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco) |
| title_short | Integrated bioinformatics identifies key mediators in cytokine storm and tissue remodeling during Vibrio mimicus infection in yellow catfish (Pelteobagrus fulvidraco) |
| title_sort | integrated bioinformatics identifies key mediators in cytokine storm and tissue remodeling during vibrio mimicus infection in yellow catfish pelteobagrus fulvidraco |
| topic | Vibrio mimicus Yellow catfish (Pelteobagrus fulvidraco) skin and muscle histopathology integrated bioinformatics signaling pathway |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1172849/full |
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