Spring Viremia of Carp Virus Infection Induces Carp IL-10 Expression, Both In Vitro and In Vivo
Interleukin-10 (IL-10) is a pleiotropic cytokine with both immune enhancement and immunosuppression activities, but the main role is immunosuppression and anti-inflammatory ability. In order to use the immunosuppressive function of IL-10, many viruses, such as SARS-CoV-2, hepatitis B virus and EB vi...
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| Format: | Article |
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MDPI AG
2023-11-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/11/11/2812 |
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| author | Ping Ouyang Yu Tao Wenyan Wei Qiunan Li Shuya Liu Yongqiang Ren Xiaoli Huang Defang Chen Yi Geng |
| author_facet | Ping Ouyang Yu Tao Wenyan Wei Qiunan Li Shuya Liu Yongqiang Ren Xiaoli Huang Defang Chen Yi Geng |
| author_sort | Ping Ouyang |
| collection | DOAJ |
| description | Interleukin-10 (IL-10) is a pleiotropic cytokine with both immune enhancement and immunosuppression activities, but the main role is immunosuppression and anti-inflammatory ability. In order to use the immunosuppressive function of IL-10, many viruses, such as SARS-CoV-2, hepatitis B virus and EB virus, can evade the host’s immune surveillance and clearance by increasing the expression of host IL-10. However, it has not been reported whether the aquatic animal infection virus can upregulate the expression of host IL-10 and the mechanisms are still unknown. Spring viremia of carp (SVC) is a fatal viral disease for many fish species and is caused by spring viremia of carp virus (SVCV). This disease has caused significant economic losses in the aquaculture industry worldwide. In this study, the expression of carp IL-10 with or without infection of SVCV in epithelioma papulosum cyprinid (EPC) cells, carp head kidney (cHK) primary cells and common carp tissues were analyzed using RT-PCR and ELISA. The results show that SVCV infection induced carp IL-10 mRNA and protein expression, both in vitro and in vivo. However, the upregulation of carp IL-10 by SVCV was hindered by specific inhibitors of the JAK inhibitor (CP-690550), STAT3 inhibitor (STA-21), NF-κB inhibitor (BAY11-7082) and p38 MAPK (mitogen-activated protein kinase) inhibitor (SB202190), but not JNK inhibitor (SP600125). Furthermore, the results demonstrated that JAK1, JAK2, JAK3, TYK2 and STAT5 played important roles in carp IL-10 production induced by SVCV infection. Taken together, SVCV infection significantly induced carp IL-10 expression and the upregulation trigged in JAK-STAT, NF-κB and p38MAPK pathways. To our knowledge, this is the first time that a fish infection virus upregulated the host IL-10 expression through the JAK-STAT, NF-κB and p38MAPK pathways. Altogether, fish viruses may have a similar mechanism as human or other mammalian viruses to escape host immune surveillance and clearance. |
| first_indexed | 2024-03-09T16:35:42Z |
| format | Article |
| id | doaj.art-e44e2904bcf24e0bbed822781a4cf52d |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-09T16:35:42Z |
| publishDate | 2023-11-01 |
| publisher | MDPI AG |
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| series | Microorganisms |
| spelling | doaj.art-e44e2904bcf24e0bbed822781a4cf52d2023-11-24T14:57:21ZengMDPI AGMicroorganisms2076-26072023-11-011111281210.3390/microorganisms11112812Spring Viremia of Carp Virus Infection Induces Carp IL-10 Expression, Both In Vitro and In VivoPing Ouyang0Yu Tao1Wenyan Wei2Qiunan Li3Shuya Liu4Yongqiang Ren5Xiaoli Huang6Defang Chen7Yi Geng8Department of Basic Veterinary, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaChengdu Academy of Agriculture and Forestry Sciences, Chengdu 611130, ChinaDepartment of Basic Veterinary, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Aquaculture, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Aquaculture, College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, ChinaDepartment of Basic Veterinary, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, ChinaInterleukin-10 (IL-10) is a pleiotropic cytokine with both immune enhancement and immunosuppression activities, but the main role is immunosuppression and anti-inflammatory ability. In order to use the immunosuppressive function of IL-10, many viruses, such as SARS-CoV-2, hepatitis B virus and EB virus, can evade the host’s immune surveillance and clearance by increasing the expression of host IL-10. However, it has not been reported whether the aquatic animal infection virus can upregulate the expression of host IL-10 and the mechanisms are still unknown. Spring viremia of carp (SVC) is a fatal viral disease for many fish species and is caused by spring viremia of carp virus (SVCV). This disease has caused significant economic losses in the aquaculture industry worldwide. In this study, the expression of carp IL-10 with or without infection of SVCV in epithelioma papulosum cyprinid (EPC) cells, carp head kidney (cHK) primary cells and common carp tissues were analyzed using RT-PCR and ELISA. The results show that SVCV infection induced carp IL-10 mRNA and protein expression, both in vitro and in vivo. However, the upregulation of carp IL-10 by SVCV was hindered by specific inhibitors of the JAK inhibitor (CP-690550), STAT3 inhibitor (STA-21), NF-κB inhibitor (BAY11-7082) and p38 MAPK (mitogen-activated protein kinase) inhibitor (SB202190), but not JNK inhibitor (SP600125). Furthermore, the results demonstrated that JAK1, JAK2, JAK3, TYK2 and STAT5 played important roles in carp IL-10 production induced by SVCV infection. Taken together, SVCV infection significantly induced carp IL-10 expression and the upregulation trigged in JAK-STAT, NF-κB and p38MAPK pathways. To our knowledge, this is the first time that a fish infection virus upregulated the host IL-10 expression through the JAK-STAT, NF-κB and p38MAPK pathways. Altogether, fish viruses may have a similar mechanism as human or other mammalian viruses to escape host immune surveillance and clearance.https://www.mdpi.com/2076-2607/11/11/2812spring viremia of carp virus (SVCV)interleukin 10 (IL-10)JAK-STATNF-κBp38MAPK |
| spellingShingle | Ping Ouyang Yu Tao Wenyan Wei Qiunan Li Shuya Liu Yongqiang Ren Xiaoli Huang Defang Chen Yi Geng Spring Viremia of Carp Virus Infection Induces Carp IL-10 Expression, Both In Vitro and In Vivo Microorganisms spring viremia of carp virus (SVCV) interleukin 10 (IL-10) JAK-STAT NF-κB p38MAPK |
| title | Spring Viremia of Carp Virus Infection Induces Carp IL-10 Expression, Both In Vitro and In Vivo |
| title_full | Spring Viremia of Carp Virus Infection Induces Carp IL-10 Expression, Both In Vitro and In Vivo |
| title_fullStr | Spring Viremia of Carp Virus Infection Induces Carp IL-10 Expression, Both In Vitro and In Vivo |
| title_full_unstemmed | Spring Viremia of Carp Virus Infection Induces Carp IL-10 Expression, Both In Vitro and In Vivo |
| title_short | Spring Viremia of Carp Virus Infection Induces Carp IL-10 Expression, Both In Vitro and In Vivo |
| title_sort | spring viremia of carp virus infection induces carp il 10 expression both in vitro and in vivo |
| topic | spring viremia of carp virus (SVCV) interleukin 10 (IL-10) JAK-STAT NF-κB p38MAPK |
| url | https://www.mdpi.com/2076-2607/11/11/2812 |
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