The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection
ABSTRACTCSFV (classical swine fever virus) is currently endemic in developing countries in Asia and has recently re-emerged in Japan. Under the pressure of natural selection pressure, CSFV keeps evolving to maintain its ecological niche in nature. CSFV has evolved mechanisms that induce immune depre...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Taylor & Francis Group
2023-12-01
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| Series: | Emerging Microbes and Infections |
| Subjects: | |
| Online Access: | https://www.tandfonline.com/doi/10.1080/22221751.2022.2164217 |
| _version_ | 1797652836754915328 |
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| author | Xiaowen Li Yiwan Song Xinyan Wang Cheng Fu Feifan Zhao Linke Zou Keke Wu Wenxian Chen Zhaoyao Li Jindai Fan Yuwan Li Bingke Li Sen Zeng Xiaodi Liu Mingqiu Zhao Lin Yi Jinding Chen Shuangqi Fan |
| author_facet | Xiaowen Li Yiwan Song Xinyan Wang Cheng Fu Feifan Zhao Linke Zou Keke Wu Wenxian Chen Zhaoyao Li Jindai Fan Yuwan Li Bingke Li Sen Zeng Xiaodi Liu Mingqiu Zhao Lin Yi Jinding Chen Shuangqi Fan |
| author_sort | Xiaowen Li |
| collection | DOAJ |
| description | ABSTRACTCSFV (classical swine fever virus) is currently endemic in developing countries in Asia and has recently re-emerged in Japan. Under the pressure of natural selection pressure, CSFV keeps evolving to maintain its ecological niche in nature. CSFV has evolved mechanisms that induce immune depression, but its pathogenic mechanism is still unclear. In this study, using transcriptomics and metabolomics methods, we found that CSFV infection alters innate host immunity by activating the interferon pathway, inhibiting host inflammation, apoptosis, and remodelling host metabolism in porcine alveolar macrophages. Moreover, we revealed that autophagy could alter innate immunity and metabolism induced by CSFV infection. Enhanced autophagy further inhibited CSFV-induced RIG-I-IRF3 signal transduction axis and JAK-STAT signalling pathway and blocked type I interferon production while reducing autophagy inhibition of the NF-κB signalling pathway and apoptosis in CSFV infection cells. Furthermore, the level of CSFV infection-induced glycolysis and the content of lactate and pyruvate, as well as 3-phosphoglyceraldehyde, a derivative of glycolysis converted to serine, was altered by autophagy. We also found that silencing HK2 (hexokinase 2), the rate-limiting enzyme of glycolytic metabolism, could induce autophagy but reduce the interferon signalling pathway, NF-κB signalling pathway, and inhibition of apoptosis induced by CSFV infection. In addition, inhibited cellular autophagy by silencing ATG5 or using 3-Methyladenine, could backfill the inhibitory effect of silencing HK2 on the cellular interferon signalling pathway, NF-κB signalling pathway, and apoptosis. |
| first_indexed | 2024-03-11T16:35:40Z |
| format | Article |
| id | doaj.art-ec48abeffbd74a4094c17fd46d9c266d |
| institution | Directory Open Access Journal |
| issn | 2222-1751 |
| language | English |
| last_indexed | 2024-03-11T16:35:40Z |
| publishDate | 2023-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Emerging Microbes and Infections |
| spelling | doaj.art-ec48abeffbd74a4094c17fd46d9c266d2023-10-23T17:36:55ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512023-12-0112110.1080/22221751.2022.2164217The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infectionXiaowen Li0Yiwan Song1Xinyan Wang2Cheng Fu3Feifan Zhao4Linke Zou5Keke Wu6Wenxian Chen7Zhaoyao Li8Jindai Fan9Yuwan Li10Bingke Li11Sen Zeng12Xiaodi Liu13Mingqiu Zhao14Lin Yi15Jinding Chen16Shuangqi Fan17College of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Animal Science & Technology, Zhongkai University of Agriculture and EngineeringCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaCollege of Veterinary Medicine, South China Agricultural University, Guangzhou, People’s Republic of ChinaABSTRACTCSFV (classical swine fever virus) is currently endemic in developing countries in Asia and has recently re-emerged in Japan. Under the pressure of natural selection pressure, CSFV keeps evolving to maintain its ecological niche in nature. CSFV has evolved mechanisms that induce immune depression, but its pathogenic mechanism is still unclear. In this study, using transcriptomics and metabolomics methods, we found that CSFV infection alters innate host immunity by activating the interferon pathway, inhibiting host inflammation, apoptosis, and remodelling host metabolism in porcine alveolar macrophages. Moreover, we revealed that autophagy could alter innate immunity and metabolism induced by CSFV infection. Enhanced autophagy further inhibited CSFV-induced RIG-I-IRF3 signal transduction axis and JAK-STAT signalling pathway and blocked type I interferon production while reducing autophagy inhibition of the NF-κB signalling pathway and apoptosis in CSFV infection cells. Furthermore, the level of CSFV infection-induced glycolysis and the content of lactate and pyruvate, as well as 3-phosphoglyceraldehyde, a derivative of glycolysis converted to serine, was altered by autophagy. We also found that silencing HK2 (hexokinase 2), the rate-limiting enzyme of glycolytic metabolism, could induce autophagy but reduce the interferon signalling pathway, NF-κB signalling pathway, and inhibition of apoptosis induced by CSFV infection. In addition, inhibited cellular autophagy by silencing ATG5 or using 3-Methyladenine, could backfill the inhibitory effect of silencing HK2 on the cellular interferon signalling pathway, NF-κB signalling pathway, and apoptosis.https://www.tandfonline.com/doi/10.1080/22221751.2022.2164217CSFVtranscriptomicsmetabolomicsautophagyinnate immunityhexokinase 2 |
| spellingShingle | Xiaowen Li Yiwan Song Xinyan Wang Cheng Fu Feifan Zhao Linke Zou Keke Wu Wenxian Chen Zhaoyao Li Jindai Fan Yuwan Li Bingke Li Sen Zeng Xiaodi Liu Mingqiu Zhao Lin Yi Jinding Chen Shuangqi Fan The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection Emerging Microbes and Infections CSFV transcriptomics metabolomics autophagy innate immunity hexokinase 2 |
| title | The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection |
| title_full | The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection |
| title_fullStr | The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection |
| title_full_unstemmed | The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection |
| title_short | The regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection |
| title_sort | regulation of cell homeostasis and antiviral innate immunity by autophagy during classical swine fever virus infection |
| topic | CSFV transcriptomics metabolomics autophagy innate immunity hexokinase 2 |
| url | https://www.tandfonline.com/doi/10.1080/22221751.2022.2164217 |
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