IL-10 upregulates SOCS3 to inhibit type I interferon signaling to promote PoRVA replication in intestinal epithelial cells

IF 2.4 2区 农林科学 Q3 MICROBIOLOGY Veterinary microbiology Pub Date : 2024-09-23 DOI:10.1016/j.vetmic.2024.110259
Haixin Liu , Yongpan Zhao , Huimin Du , Pengcheng Hao , Haolun Tian , Kun Wang , Yudong Qiu , Haiying Dong , Qian Du , Dewen Tong , Yong Huang
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Abstract

Porcine group A rotavirus (PoRVA) is one of the common enteric viruses causing severe diarrhea in piglets. Although PoRVA infection has been identified to promote IL-10 production, the role of IL-10 during viral infection remains unclear. In this study, we found that elevated IL-10 levels during PoRVA infection promote viral replication by inhibiting type I interferon production and response. IL-10 treatment upregulated the expression of SOCS3 in PoRVA-infected IPEC-J2 cells, which inhibited IFN-I production by preventing the degradation of IκB and nuclear translocation of NF-κB, thereby significantly promoting PoRVA replication. Furthermore, we determined that SOCS3 also inhibited type Ⅰ interferon signaling pathway, which led to a significantly reduced ISGs after IFN-α stimulation. In PoRVA-infected cells, overexpression of SOCS3 significantly inhibits phosphorylation and heterodimerization of STAT1, thereby promoting viral replication. Finally, we demonstrated the effect of IL-10 on PoRVA replication in vivo by murine models of PoRVA infection. PoRVA replication levels were lower in the ileum of IL-10 knockout (IL-10-/-) mice than that in PoRVA-infected wild-type mice, but PoRVA replication levels were higher in the ileum of IFNAR knockout (IFNAR-/-) mice than that in PoRVA-infected wild-type mice. Taken together, our findings provide information to understand the strategies of PoRVA to evade host innate antiviral immunity.
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IL-10 上调 SOCS3,抑制 I 型干扰素信号,促进肠上皮细胞中 PoRVA 的复制
猪 A 组轮状病毒(PoRVA)是导致仔猪严重腹泻的常见肠道病毒之一。虽然已发现 PoRVA 感染会促进 IL-10 的产生,但 IL-10 在病毒感染过程中的作用仍不清楚。在这项研究中,我们发现 PoRVA 感染期间 IL-10 水平升高会抑制 I 型干扰素的产生和反应,从而促进病毒复制。IL-10处理可上调SOCS3在感染PoRVA的IPEC-J2细胞中的表达,SOCS3通过阻止IκB降解和NF-κB核转位来抑制IFN-I的产生,从而显著促进PoRVA的复制。此外,我们还发现 SOCS3 还能抑制Ⅰ型干扰素信号通路,从而使 IFN-α 刺激后的 ISGs 显著减少。在 PoRVA 感染的细胞中,过表达 SOCS3 能明显抑制 STAT1 的磷酸化和异二聚化,从而促进病毒复制。最后,我们通过小鼠 PoRVA 感染模型证明了 IL-10 对 PoRVA 在体内复制的影响。IL-10基因敲除(IL-10-/-)小鼠回肠中的PoRVA复制水平低于感染PoRVA的野生型小鼠,但IFNAR基因敲除(IFNAR-/-)小鼠回肠中的PoRVA复制水平高于感染PoRVA的野生型小鼠。综上所述,我们的研究结果为了解 PoRVA 逃避宿主先天性抗病毒免疫的策略提供了信息。
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来源期刊
Veterinary microbiology
Veterinary microbiology 农林科学-兽医学
CiteScore
5.90
自引率
6.10%
发文量
221
审稿时长
52 days
期刊介绍: Veterinary Microbiology is concerned with microbial (bacterial, fungal, viral) diseases of domesticated vertebrate animals (livestock, companion animals, fur-bearing animals, game, poultry, fish) that supply food, other useful products or companionship. In addition, Microbial diseases of wild animals living in captivity, or as members of the feral fauna will also be considered if the infections are of interest because of their interrelation with humans (zoonoses) and/or domestic animals. Studies of antimicrobial resistance are also included, provided that the results represent a substantial advance in knowledge. Authors are strongly encouraged to read - prior to submission - the Editorials (''Scope or cope'' and ''Scope or cope II'') published previously in the journal. The Editors reserve the right to suggest submission to another journal for those papers which they feel would be more appropriate for consideration by that journal. Original research papers of high quality and novelty on aspects of control, host response, molecular biology, pathogenesis, prevention, and treatment of microbial diseases of animals are published. Papers dealing primarily with immunology, epidemiology, molecular biology and antiviral or microbial agents will only be considered if they demonstrate a clear impact on a disease. Papers focusing solely on diagnostic techniques (such as another PCR protocol or ELISA) will not be published - focus should be on a microorganism and not on a particular technique. Papers only reporting microbial sequences, transcriptomics data, or proteomics data will not be considered unless the results represent a substantial advance in knowledge. Drug trial papers will be considered if they have general application or significance. Papers on the identification of microorganisms will also be considered, but detailed taxonomic studies do not fall within the scope of the journal. Case reports will not be published, unless they have general application or contain novel aspects. Papers of geographically limited interest, which repeat what had been established elsewhere will not be considered. The readership of the journal is global.
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