Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain
Anti-disease breeding is becoming the most promising solution to cyprinid herpesvirus-3 (CyHV-3) infection, the major threat to common carp aquaculture. Virus challenging studies suggested that a breeding strain of common carp developed resistance to CyHV-3 infection. This study illustrates the immu...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-07-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2021.687151/full |
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| author | Zhiying Jia Zhiying Jia Zhiying Jia Nan Wu Nan Wu Xiaona Jiang Xiaona Jiang Heng Li Heng Li Jiaxin Sun Jiaxin Sun Mijuan Shi Chitao Li Chitao Li Yanlong Ge Yanlong Ge Xuesong Hu Xuesong Hu Weidong Ye Weidong Ye Ying Tang Junwei Shan Junwei Shan Yingyin Cheng Xiao-Qin Xia Xiao-Qin Xia Xiao-Qin Xia Lianyu Shi Lianyu Shi |
| author_facet | Zhiying Jia Zhiying Jia Zhiying Jia Nan Wu Nan Wu Xiaona Jiang Xiaona Jiang Heng Li Heng Li Jiaxin Sun Jiaxin Sun Mijuan Shi Chitao Li Chitao Li Yanlong Ge Yanlong Ge Xuesong Hu Xuesong Hu Weidong Ye Weidong Ye Ying Tang Junwei Shan Junwei Shan Yingyin Cheng Xiao-Qin Xia Xiao-Qin Xia Xiao-Qin Xia Lianyu Shi Lianyu Shi |
| author_sort | Zhiying Jia |
| collection | DOAJ |
| description | Anti-disease breeding is becoming the most promising solution to cyprinid herpesvirus-3 (CyHV-3) infection, the major threat to common carp aquaculture. Virus challenging studies suggested that a breeding strain of common carp developed resistance to CyHV-3 infection. This study illustrates the immune mechanisms involved in both sensitivity and anti-virus ability for CyHV3 infection in fish. An integrative analysis of the protein-coding genes and long non-coding RNAs (lncRNAs) using transcriptomic data was performed. Tissues from the head kidney of common carp were extracted at days 0 (the healthy control) and 7 after CyHV-3 infection (the survivors) and used to analyze the transcriptome through both Illumina and PacBio sequencing. Following analysis of the GO terms and KEGG pathways involved, the immune-related terms and pathways were merged. To dig out details on the immune aspect, the DEGs were filtered using the current common carp immune gene library. Immune gene categories and their corresponding genes in different comparison groups were revealed. Also, the immunological Gene Ontology terms for lncRNA modulation were retained. The weighted gene co-expression network analysis was used to reveal the regulation of immune genes by lncRNA. The results demonstrated that the breeding carp strain develops a marked resistance to CyHV-3 infection through a specific innate immune mechanism. The featured biological processes were autophagy, phagocytosis, cytotoxicity, and virus blockage by lectins and MUC3. Moreover, the immune-suppressive signals, such as suppression of IL21R on STAT3, PI3K mediated inhibition of inflammation by dopamine upon infection, as well as the inhibition of NLRC3 on STING during a steady state. Possible susceptible factors for CyHV-3, such as ITGB1, TLR18, and CCL4, were also revealed from the non-breeding strain. The results of this study also suggested that Nramp and PAI regulated by LncRNA could facilitate virus infection and proliferation for infected cells respectively, while T cell leukemia homeobox 3 (TLX3), as well as galectin 3 function by lncRNA, may play a role in the resistance mechanism. Therefore, immune factors that are immunogenetically insensitive or susceptible to CyHV-3 infection have been revealed. |
| first_indexed | 2024-12-17T03:23:18Z |
| format | Article |
| id | doaj.art-ba61b774b40343e2815327997d39ca81 |
| institution | Directory Open Access Journal |
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| language | English |
| last_indexed | 2024-12-17T03:23:18Z |
| publishDate | 2021-07-01 |
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| series | Frontiers in Immunology |
| spelling | doaj.art-ba61b774b40343e2815327997d39ca812022-12-21T22:05:28ZengFrontiers Media S.A.Frontiers in Immunology1664-32242021-07-011210.3389/fimmu.2021.687151687151Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp StrainZhiying Jia0Zhiying Jia1Zhiying Jia2Nan Wu3Nan Wu4Xiaona Jiang5Xiaona Jiang6Heng Li7Heng Li8Jiaxin Sun9Jiaxin Sun10Mijuan Shi11Chitao Li12Chitao Li13Yanlong Ge14Yanlong Ge15Xuesong Hu16Xuesong Hu17Weidong Ye18Weidong Ye19Ying Tang20Junwei Shan21Junwei Shan22Yingyin Cheng23Xiao-Qin Xia24Xiao-Qin Xia25Xiao-Qin Xia26Lianyu Shi27Lianyu Shi28Heilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin, ChinaNational and Local Joint Engineering Laboratory for Freshwater Fish Breeding, Harbin, ChinaKey Laboratory of Aquatic Genomics, Ministry of Agriculture, Chinese Academy of Fishery Sciences, Beijing, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin, ChinaNational and Local Joint Engineering Laboratory for Freshwater Fish Breeding, Harbin, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin, ChinaNational and Local Joint Engineering Laboratory for Freshwater Fish Breeding, Harbin, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin, ChinaNational and Local Joint Engineering Laboratory for Freshwater Fish Breeding, Harbin, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin, ChinaNational and Local Joint Engineering Laboratory for Freshwater Fish Breeding, Harbin, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin, ChinaNational and Local Joint Engineering Laboratory for Freshwater Fish Breeding, Harbin, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaThe Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, ChinaHeilongjiang River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Harbin, ChinaNational and Local Joint Engineering Laboratory for Freshwater Fish Breeding, Harbin, ChinaAnti-disease breeding is becoming the most promising solution to cyprinid herpesvirus-3 (CyHV-3) infection, the major threat to common carp aquaculture. Virus challenging studies suggested that a breeding strain of common carp developed resistance to CyHV-3 infection. This study illustrates the immune mechanisms involved in both sensitivity and anti-virus ability for CyHV3 infection in fish. An integrative analysis of the protein-coding genes and long non-coding RNAs (lncRNAs) using transcriptomic data was performed. Tissues from the head kidney of common carp were extracted at days 0 (the healthy control) and 7 after CyHV-3 infection (the survivors) and used to analyze the transcriptome through both Illumina and PacBio sequencing. Following analysis of the GO terms and KEGG pathways involved, the immune-related terms and pathways were merged. To dig out details on the immune aspect, the DEGs were filtered using the current common carp immune gene library. Immune gene categories and their corresponding genes in different comparison groups were revealed. Also, the immunological Gene Ontology terms for lncRNA modulation were retained. The weighted gene co-expression network analysis was used to reveal the regulation of immune genes by lncRNA. The results demonstrated that the breeding carp strain develops a marked resistance to CyHV-3 infection through a specific innate immune mechanism. The featured biological processes were autophagy, phagocytosis, cytotoxicity, and virus blockage by lectins and MUC3. Moreover, the immune-suppressive signals, such as suppression of IL21R on STAT3, PI3K mediated inhibition of inflammation by dopamine upon infection, as well as the inhibition of NLRC3 on STING during a steady state. Possible susceptible factors for CyHV-3, such as ITGB1, TLR18, and CCL4, were also revealed from the non-breeding strain. The results of this study also suggested that Nramp and PAI regulated by LncRNA could facilitate virus infection and proliferation for infected cells respectively, while T cell leukemia homeobox 3 (TLX3), as well as galectin 3 function by lncRNA, may play a role in the resistance mechanism. Therefore, immune factors that are immunogenetically insensitive or susceptible to CyHV-3 infection have been revealed.https://www.frontiersin.org/articles/10.3389/fimmu.2021.687151/fulltranscriptomelncRNACyHV-3resistant immune mechanismcommon carp |
| spellingShingle | Zhiying Jia Zhiying Jia Zhiying Jia Nan Wu Nan Wu Xiaona Jiang Xiaona Jiang Heng Li Heng Li Jiaxin Sun Jiaxin Sun Mijuan Shi Chitao Li Chitao Li Yanlong Ge Yanlong Ge Xuesong Hu Xuesong Hu Weidong Ye Weidong Ye Ying Tang Junwei Shan Junwei Shan Yingyin Cheng Xiao-Qin Xia Xiao-Qin Xia Xiao-Qin Xia Lianyu Shi Lianyu Shi Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain Frontiers in Immunology transcriptome lncRNA CyHV-3 resistant immune mechanism common carp |
| title | Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain |
| title_full | Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain |
| title_fullStr | Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain |
| title_full_unstemmed | Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain |
| title_short | Integrative Transcriptomic Analysis Reveals the Immune Mechanism for a CyHV-3-Resistant Common Carp Strain |
| title_sort | integrative transcriptomic analysis reveals the immune mechanism for a cyhv 3 resistant common carp strain |
| topic | transcriptome lncRNA CyHV-3 resistant immune mechanism common carp |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2021.687151/full |
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