Singapore grouper iridovirus infection counteracts poly I:C induced antiviral immune response in vitro

Wenji Wang; Ya Zhang; Xixi Guo; Weihua Xu; Qiwei Qin; Youhua Huang; Xiaohong Huang

doi:10.1016/j.fsi.2023.108685

Singapore grouper iridovirus infection counteracts poly I:C induced antiviral immune response in vitro

Fish Shellfish Immunol. 2023 Apr:135:108685. doi: 10.1016/j.fsi.2023.108685. Epub 2023 Mar 13.

Authors

Wenji Wang¹, Ya Zhang¹, Xixi Guo¹, Weihua Xu¹, Qiwei Qin², Youhua Huang³, Xiaohong Huang⁴

Affiliations

¹ Lingnan Guangdong Laboratory of Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou, 510642, China.
² Lingnan Guangdong Laboratory of Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou, 510642, China; Southern Marine Science and Engineering Guangdong Laboratory, Zhuhai, 519082, China; Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266000, China.
³ Lingnan Guangdong Laboratory of Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou, 510642, China. Electronic address: huangyh@scau.edu.cn.
⁴ Lingnan Guangdong Laboratory of Modern Agriculture, College of Marine Sciences, South China Agricultural University, Guangzhou, 510642, China. Electronic address: huangxh@scau.edu.cn.

PMID: 36921879
DOI: 10.1016/j.fsi.2023.108685

Abstract

Groupers are important mariculture fish in South China and Southeast Asian countries. However, the increasing frequency of infectious disease outbreaks has caused great economic losses in the grouper industry. Among these pathogens, Singapore grouper iridovirus (SGIV) infection causes high mortality in larval and juvenile stages of grouper. However, the mechanism underlying the action of viral manipulation on cellular immune response still remained largely uncertain. Here, using RNA-seq technology, we investigated the regulatory roles of SGIV infection on synthetic RNA duplex poly I:C induced immune response in vitro. Using reporter gene assays, we found that SGIV infection decreased poly I:C induced interferon promoter activation. Transcriptomic analysis showed that the mRNA expression levels of 2238 genes were up-regulated, while 1247 genes were down-regulated in poly I:C transfected grouper spleen (GS) cells. Interestingly, SGIV infection decreased the expression of 1479 up-regulated genes and increased the expression of 297 down-regulated genes in poly I:C transfected cells. The differentially expressed genes (DEGs) down-regulated by SGIV were directly related to immune, inflammation and viral infection, and JUN, STAT1, NFKB1, MAPK14A, TGFB1 and MX were the 6 top hub genes in the down-regulated DEGs' protein-protein interaction (PPI) network. Furthermore, quantitative real-time PCR (qPCR) analysis confirmed that the interferon signaling and inflammatory-related genes, including cGAS, STING, TBK1, MAVS, TNF, IRAK4 and NOD2 were up-regulated by poly I:C stimulation, but all significantly down-regulated after SGIV infection. Thus, we speculated that SGIV infection counteracted poly I:C induced antiviral immune response and this ability helped itself to escape host immune surveillance. Together, our data will contribute greatly to understanding the potential immune evasion mechanism of iridovirus infection in vitro.

Keywords: Immune evasion; Immune response; Inflammatory response; Poly I:C; SGIV.

MeSH terms

Animals
Antiviral Agents
Bass*
Cloning, Molecular
DNA Virus Infections*
Fish Diseases*
Fish Proteins
Immunity, Innate / genetics
Interferons / genetics
Iridovirus* / physiology
Poly I-C / pharmacology
Ranavirus* / physiology
Singapore

Substances

Antiviral Agents
Poly I-C
Interferons
Fish Proteins