Acute hypoxia stress mediates HIF-1α-Yki-Cactus axis to facilitate the infection of Vibrio parahaemolyticus in Litopenaeus vannamei
IntroductionHypoxia stress renders aquatic animals more susceptible to bacterial disease, yet the underlying mechanism remains elusive.MethodsWe conducted an acute hypoxia stress experiment to investigate the impact of stress on the immune response of Litopenaeus vannamei via transcriptome analysis,...
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Frontiers Media S.A.
2024-11-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1476309/full |
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| author | Honghui He Honghui He Honghui He Honghui He Shaoqing Huang Ningze Geng Ningze Geng Shaoping Weng Shaoping Weng Shaoping Weng Shaoping Weng Jianguo He Jianguo He Jianguo He Jianguo He Chaozheng Li Chaozheng Li Chaozheng Li Chaozheng Li |
| author_facet | Honghui He Honghui He Honghui He Honghui He Shaoqing Huang Ningze Geng Ningze Geng Shaoping Weng Shaoping Weng Shaoping Weng Shaoping Weng Jianguo He Jianguo He Jianguo He Jianguo He Chaozheng Li Chaozheng Li Chaozheng Li Chaozheng Li |
| author_sort | Honghui He |
| collection | DOAJ |
| description | IntroductionHypoxia stress renders aquatic animals more susceptible to bacterial disease, yet the underlying mechanism remains elusive.MethodsWe conducted an acute hypoxia stress experiment to investigate the impact of stress on the immune response of Litopenaeus vannamei via transcriptome analysis, RT-qPCR and Western blot.ResultsOur results showed that acute hypoxia stress disrupted the tissue architecture, and significantly changed the gene expression profiles in the hepatopancreas of shrimp. More importantly, acute hypoxia stress significantly changed the expression levels of immune-related genes. Ladderlectin, GBP 1, Caspase-1, CLEC4F, MR1 and GBP 2 were significantly down-regulated, but HIF-1α, Cactus, TIPE, Akirin-2, Ivns1abp and TLR3 were significantly up-regulated. We further demonstrated that acute hypoxia activated Yki via HIF-1α to enhance expression level of Cactus, and then Cactus inhibited the phosphorylation of Dorsal and its nuclear translocation, thereby suppressing antibacterial immunity. Subsequently, the challenge experiment following stress revealed that exposure to acute hypoxia stress amplified the infectivity and lethality of Vibrio parahaemolyticus to shrimp. The mechanism of HIF-1α-Yki-Cautus axis provided an explanation for this phenomenon.DiscussionThis study offered new insights into interactions among environmental hypoxia stress, host immunity and pathogens, thereby providing practical guidelines for optimizing shrimp culture practices. |
| format | Article |
| id | doaj-art-838494d31b3b4787ba292a229e0ffe02 |
| institution | OA Journals |
| issn | 1664-3224 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Immunology |
| spelling | doaj-art-838494d31b3b4787ba292a229e0ffe022025-08-20T02:28:32ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-11-011510.3389/fimmu.2024.14763091476309Acute hypoxia stress mediates HIF-1α-Yki-Cactus axis to facilitate the infection of Vibrio parahaemolyticus in Litopenaeus vannameiHonghui He0Honghui He1Honghui He2Honghui He3Shaoqing Huang4Ningze Geng5Ningze Geng6Shaoping Weng7Shaoping Weng8Shaoping Weng9Shaoping Weng10Jianguo He11Jianguo He12Jianguo He13Jianguo He14Chaozheng Li15Chaozheng Li16Chaozheng Li17Chaozheng Li18State Key Laboratory of Biocontrol/School of Marine Sciences, Sun Yat-sen University, Guangzhou, ChinaSouthern Marine Sciences and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaChina-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangzhou, ChinaCollege of Marine Sciences, Beibu Gulf University, Qinzhou, ChinaState Key Laboratory of Biocontrol/School of Marine Sciences, Sun Yat-sen University, Guangzhou, ChinaSouthern Marine Sciences and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, ChinaState Key Laboratory of Biocontrol/School of Marine Sciences, Sun Yat-sen University, Guangzhou, ChinaSouthern Marine Sciences and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaChina-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangzhou, ChinaState Key Laboratory of Biocontrol/School of Marine Sciences, Sun Yat-sen University, Guangzhou, ChinaSouthern Marine Sciences and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaChina-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangzhou, ChinaState Key Laboratory of Biocontrol/School of Marine Sciences, Sun Yat-sen University, Guangzhou, ChinaSouthern Marine Sciences and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, ChinaSchool of Life Sciences, Sun Yat-sen University, Guangzhou, ChinaChina-ASEAN Belt and Road Joint Laboratory on Mariculture Technology, Guangzhou, ChinaIntroductionHypoxia stress renders aquatic animals more susceptible to bacterial disease, yet the underlying mechanism remains elusive.MethodsWe conducted an acute hypoxia stress experiment to investigate the impact of stress on the immune response of Litopenaeus vannamei via transcriptome analysis, RT-qPCR and Western blot.ResultsOur results showed that acute hypoxia stress disrupted the tissue architecture, and significantly changed the gene expression profiles in the hepatopancreas of shrimp. More importantly, acute hypoxia stress significantly changed the expression levels of immune-related genes. Ladderlectin, GBP 1, Caspase-1, CLEC4F, MR1 and GBP 2 were significantly down-regulated, but HIF-1α, Cactus, TIPE, Akirin-2, Ivns1abp and TLR3 were significantly up-regulated. We further demonstrated that acute hypoxia activated Yki via HIF-1α to enhance expression level of Cactus, and then Cactus inhibited the phosphorylation of Dorsal and its nuclear translocation, thereby suppressing antibacterial immunity. Subsequently, the challenge experiment following stress revealed that exposure to acute hypoxia stress amplified the infectivity and lethality of Vibrio parahaemolyticus to shrimp. The mechanism of HIF-1α-Yki-Cautus axis provided an explanation for this phenomenon.DiscussionThis study offered new insights into interactions among environmental hypoxia stress, host immunity and pathogens, thereby providing practical guidelines for optimizing shrimp culture practices.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1476309/fullhypoxiashrimpdiseaseHIF-1α-Yki-CautusVibrio parahaemolyticus |
| spellingShingle | Honghui He Honghui He Honghui He Honghui He Shaoqing Huang Ningze Geng Ningze Geng Shaoping Weng Shaoping Weng Shaoping Weng Shaoping Weng Jianguo He Jianguo He Jianguo He Jianguo He Chaozheng Li Chaozheng Li Chaozheng Li Chaozheng Li Acute hypoxia stress mediates HIF-1α-Yki-Cactus axis to facilitate the infection of Vibrio parahaemolyticus in Litopenaeus vannamei Frontiers in Immunology hypoxia shrimp disease HIF-1α-Yki-Cautus Vibrio parahaemolyticus |
| title | Acute hypoxia stress mediates HIF-1α-Yki-Cactus axis to facilitate the infection of Vibrio parahaemolyticus in Litopenaeus vannamei |
| title_full | Acute hypoxia stress mediates HIF-1α-Yki-Cactus axis to facilitate the infection of Vibrio parahaemolyticus in Litopenaeus vannamei |
| title_fullStr | Acute hypoxia stress mediates HIF-1α-Yki-Cactus axis to facilitate the infection of Vibrio parahaemolyticus in Litopenaeus vannamei |
| title_full_unstemmed | Acute hypoxia stress mediates HIF-1α-Yki-Cactus axis to facilitate the infection of Vibrio parahaemolyticus in Litopenaeus vannamei |
| title_short | Acute hypoxia stress mediates HIF-1α-Yki-Cactus axis to facilitate the infection of Vibrio parahaemolyticus in Litopenaeus vannamei |
| title_sort | acute hypoxia stress mediates hif 1α yki cactus axis to facilitate the infection of vibrio parahaemolyticus in litopenaeus vannamei |
| topic | hypoxia shrimp disease HIF-1α-Yki-Cautus Vibrio parahaemolyticus |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1476309/full |
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