Two White Spot Syndrome Virus MicroRNAs Target the Dorsal Gene To Promote Virus Infection in Marsupenaeus japonicus Shrimp

Abstract

In eukaryotes, microRNAs (miRNAs) serve as regulators of many biological processes, including virus infection. An miRNA can generally target diverse genes during virus-host interactions. However, the regulation of gene expression by multiple miRNAs has not yet been extensively explored during virus infection. This study found that the Spaztle (Spz)-Toll-Dorsal-antilipopolysaccharide factor (ALF) signaling pathway plays a very important role in antiviral immunity against invasion of white spot syndrome virus (WSSV) in shrimp (Marsupenaeus japonicus). Dorsal, the central gene in the Toll pathway, was targeted by two viral miRNAs (WSSV-miR-N13 and WSSV-miR-N23) during WSSV infection. The regulation of Dorsal expression by viral miRNAs suppressed the Spz-Toll-Dorsal-ALF signaling pathway in shrimp in vivo, leading to virus infection. Our study contributes novel insights into the viral miRNAmediated Toll signaling pathway during the virus-host interaction.IMPORTANCE An miRNA can target diverse genes during virus-host interactions. However, the regulation of gene expression by multiple miRNAs during virus infection has not yet been extensively explored. The results of this study indicated that the shrimp Dorsal gene, the central gene in the Toll pathway, was targeted by two viral miRNAs during infection with white spot syndrome virus. Regulation of Dorsal expression by viral miRNAs suppressed the Spz-Toll-Dorsal-ALF signaling pathway in shrimp in vivo, leading to virus infection. Our study provides new insight into the viral miRNA-mediated Toll signaling pathway in virus-host interactions.

RNAi screening identifies a new Toll from shrimp that restricts WSSV infection through activating Dorsal to induce antimicrobial peptides

“…By RNAi method, we observe that shrimps with knockdown of Dorsal have elevated viral loads than those of the GFP control group, suggesting that Dorsal is important for host to limit viral replication. Besides, the report of WSSV encoding two MicroRNAs with the ability to suppress shrimp Dorsal also supports that Dorsal is a key restrict factor against viral infection (56). However, knockdown of Dorsal results in lower viral loads than those of MyD88, Tube and Pelle silenced groups, which may be explained by that Dorsal locates the lower levels at MyD88/Tube/Pelle cascade of the canonical Toll pathway.…”

Cyprinid Herpesvirus 2 miR-C12 Attenuates Virus-Mediated Apoptosis and Promotes Virus Propagation by Targeting Caspase 8

“…Firstly, miRNA was found to have a profound effect on the expression pattern of several hundred mRNAs (Reddy, 2015). One miRNA may target and regulate multiple genes, and one gene can be regulated by multiple miRNA (Qian et al, 2017). For example, several miRNAs in EBV cluster 1 have been identified to show both pro-apoptotic and anti-apoptotic effects (Vereide et al, 2014).…”

“…Several reports have shown that virus-encoded miRNAs influence virus replication and propagation. Viral miRNAs are expressed during infection, suggesting that viral miRNA might participate in virus propagation and survival (Qian et al, 2017). For example, WSSV-miR-N24 inhibits cell apoptosis through increase in caspase 8 expression, leading to an increase in WSSV copy number (Huang et al, 2014).…”

Role of DCP1-DCP2 complex regulated by viral and host microRNAs in DNA virus infection

“…In the present investigation, the results showed that the host and viral miRNAs could inhibit the expressions of DCP1 and DCP2 during DNA virus infection. MiRNAs, a large class of small noncoding RNAs in diverse eukaryotic organisms, are sequentially processed by two RNase III proteins, Drosha and Dicer from the stem regions of long hairpin transcripts (28, 37). The mature miRNA strand is liberated from the miRNA:miRNA* duplex and integrated into the RNA induced silencing complex (RISC), and inhibits the expression of cognate mRNA through degradation or translation repression in the RISC (18).…”