The Interaction of Mandarin Fish DDX41 with STING Evokes type I Interferon Responses Inhibiting Ranavirus Replication
DDX41 is an intracellular DNA sensor that evokes type I interferon (IFN-I) production via the adaptor stimulator of interferon gene (STING), triggering innate immune responses against viral infection. However, the regulatory mechanism of the DDX41-STING pathway in teleost fish remains unclear. The m...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2022-12-01
|
| Series: | Viruses |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1999-4915/15/1/58 |
| _version_ | 1827621313325301760 |
|---|---|
| author | Xiao-Wei Qin Zhi-Yong Luo Wei-Qiang Pan Jian He Zhi-Min Li Yang Yu Chang Liu Shao-Ping Weng Jian-Guo He Chang-Jun Guo |
| author_facet | Xiao-Wei Qin Zhi-Yong Luo Wei-Qiang Pan Jian He Zhi-Min Li Yang Yu Chang Liu Shao-Ping Weng Jian-Guo He Chang-Jun Guo |
| author_sort | Xiao-Wei Qin |
| collection | DOAJ |
| description | DDX41 is an intracellular DNA sensor that evokes type I interferon (IFN-I) production via the adaptor stimulator of interferon gene (STING), triggering innate immune responses against viral infection. However, the regulatory mechanism of the DDX41-STING pathway in teleost fish remains unclear. The mandarin fish (<i>Siniperca chuatsi</i>) is a cultured freshwater fish species that is popular in China because of its high market value. With the development of a high-density cultural mode in mandarin fish, viral diseases have increased and seriously restricted the development of aquaculture, such as ranavirus and rhabdovirus. Herein, the role of mandarin fish DDX41 (<i>sc</i>DDX41) and its DEAD and HELIC domains in the antiviral innate immune response were investigated. The level of <i>sc</i>DDX41 expression was up-regulated following treatment with poly(dA:dT) or Mandarin fish ranavirus (MRV), suggesting that <i>sc</i>DDX41 might be involved in fish innate immunity. The overexpression of <i>sc</i>DDX41 significantly increased the expression levels of IFN-I, ISGs, and pro-inflammatory cytokine genes. Co-immunoprecipitation and pull-down assays showed that the DEAD domain of <i>sc</i>DDX41 recognized the IFN stimulatory DNA and interacted with STING to activate IFN-I signaling pathway. Interestingly, the HELIC domain of <i>sc</i>DDX41 could directly interact with the N-terminal of STING to induce the expression levels of <i>IFN-I</i> and <i>ISGs</i> genes. Furthermore, the <i>sc</i>DDX41 could enhance the <i>sc</i>STING-induced IFN-I immune response and significantly inhibit MRV replication. Our work would be beneficial to understand the roles of teleost fish DDX41 in the antiviral innate immune response. |
| first_indexed | 2024-03-09T11:03:01Z |
| format | Article |
| id | doaj.art-16ae40dc423d4f70ac6c53f0eef4cf70 |
| institution | Directory Open Access Journal |
| issn | 1999-4915 |
| language | English |
| last_indexed | 2024-03-09T11:03:01Z |
| publishDate | 2022-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Viruses |
| spelling | doaj.art-16ae40dc423d4f70ac6c53f0eef4cf702023-12-01T01:07:31ZengMDPI AGViruses1999-49152022-12-011515810.3390/v15010058The Interaction of Mandarin Fish DDX41 with STING Evokes type I Interferon Responses Inhibiting Ranavirus ReplicationXiao-Wei Qin0Zhi-Yong Luo1Wei-Qiang Pan2Jian He3Zhi-Min Li4Yang Yu5Chang Liu6Shao-Ping Weng7Jian-Guo He8Chang-Jun Guo9State Key Laboratory for Biocontrol & Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Marine Sciences, Sun Yat-sen University, 135 Xingang Road West, Guangzhou 510275, ChinaState Key Laboratory for Biocontrol & Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Marine Sciences, Sun Yat-sen University, 135 Xingang Road West, Guangzhou 510275, ChinaState Key Laboratory for Biocontrol & Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Marine Sciences, Sun Yat-sen University, 135 Xingang Road West, Guangzhou 510275, ChinaState Key Laboratory for Biocontrol & Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Marine Sciences, Sun Yat-sen University, 135 Xingang Road West, Guangzhou 510275, ChinaState Key Laboratory for Biocontrol & Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Marine Sciences, Sun Yat-sen University, 135 Xingang Road West, Guangzhou 510275, ChinaState Key Laboratory for Biocontrol & Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Marine Sciences, Sun Yat-sen University, 135 Xingang Road West, Guangzhou 510275, ChinaState Key Laboratory for Biocontrol & Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Marine Sciences, Sun Yat-sen University, 135 Xingang Road West, Guangzhou 510275, ChinaGuangdong Province Key Laboratory for Aquatic Economic Animals, and Guangdong Provincial Key Laboratory of Marine Resources and Coastal Engineering, Sun Yat-sen University, 135 Xingang Road West, Guangzhou 510275, ChinaState Key Laboratory for Biocontrol & Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Marine Sciences, Sun Yat-sen University, 135 Xingang Road West, Guangzhou 510275, ChinaState Key Laboratory for Biocontrol & Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), School of Marine Sciences, Sun Yat-sen University, 135 Xingang Road West, Guangzhou 510275, ChinaDDX41 is an intracellular DNA sensor that evokes type I interferon (IFN-I) production via the adaptor stimulator of interferon gene (STING), triggering innate immune responses against viral infection. However, the regulatory mechanism of the DDX41-STING pathway in teleost fish remains unclear. The mandarin fish (<i>Siniperca chuatsi</i>) is a cultured freshwater fish species that is popular in China because of its high market value. With the development of a high-density cultural mode in mandarin fish, viral diseases have increased and seriously restricted the development of aquaculture, such as ranavirus and rhabdovirus. Herein, the role of mandarin fish DDX41 (<i>sc</i>DDX41) and its DEAD and HELIC domains in the antiviral innate immune response were investigated. The level of <i>sc</i>DDX41 expression was up-regulated following treatment with poly(dA:dT) or Mandarin fish ranavirus (MRV), suggesting that <i>sc</i>DDX41 might be involved in fish innate immunity. The overexpression of <i>sc</i>DDX41 significantly increased the expression levels of IFN-I, ISGs, and pro-inflammatory cytokine genes. Co-immunoprecipitation and pull-down assays showed that the DEAD domain of <i>sc</i>DDX41 recognized the IFN stimulatory DNA and interacted with STING to activate IFN-I signaling pathway. Interestingly, the HELIC domain of <i>sc</i>DDX41 could directly interact with the N-terminal of STING to induce the expression levels of <i>IFN-I</i> and <i>ISGs</i> genes. Furthermore, the <i>sc</i>DDX41 could enhance the <i>sc</i>STING-induced IFN-I immune response and significantly inhibit MRV replication. Our work would be beneficial to understand the roles of teleost fish DDX41 in the antiviral innate immune response.https://www.mdpi.com/1999-4915/15/1/58DDX41STINGranavirusinterferoninnate immunemandarin fish |
| spellingShingle | Xiao-Wei Qin Zhi-Yong Luo Wei-Qiang Pan Jian He Zhi-Min Li Yang Yu Chang Liu Shao-Ping Weng Jian-Guo He Chang-Jun Guo The Interaction of Mandarin Fish DDX41 with STING Evokes type I Interferon Responses Inhibiting Ranavirus Replication Viruses DDX41 STING ranavirus interferon innate immune mandarin fish |
| title | The Interaction of Mandarin Fish DDX41 with STING Evokes type I Interferon Responses Inhibiting Ranavirus Replication |
| title_full | The Interaction of Mandarin Fish DDX41 with STING Evokes type I Interferon Responses Inhibiting Ranavirus Replication |
| title_fullStr | The Interaction of Mandarin Fish DDX41 with STING Evokes type I Interferon Responses Inhibiting Ranavirus Replication |
| title_full_unstemmed | The Interaction of Mandarin Fish DDX41 with STING Evokes type I Interferon Responses Inhibiting Ranavirus Replication |
| title_short | The Interaction of Mandarin Fish DDX41 with STING Evokes type I Interferon Responses Inhibiting Ranavirus Replication |
| title_sort | interaction of mandarin fish ddx41 with sting evokes type i interferon responses inhibiting ranavirus replication |
| topic | DDX41 STING ranavirus interferon innate immune mandarin fish |
| url | https://www.mdpi.com/1999-4915/15/1/58 |
| work_keys_str_mv | AT xiaoweiqin theinteractionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT zhiyongluo theinteractionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT weiqiangpan theinteractionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT jianhe theinteractionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT zhiminli theinteractionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT yangyu theinteractionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT changliu theinteractionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT shaopingweng theinteractionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT jianguohe theinteractionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT changjunguo theinteractionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT xiaoweiqin interactionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT zhiyongluo interactionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT weiqiangpan interactionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT jianhe interactionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT zhiminli interactionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT yangyu interactionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT changliu interactionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT shaopingweng interactionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT jianguohe interactionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication AT changjunguo interactionofmandarinfishddx41withstingevokestypeiinterferonresponsesinhibitingranavirusreplication |