PcTrim prevents early infection with white spot syndrome virus by inhibiting AP1-induced endocytosis

Abstract Viruses have evolved various strategies to achieve early infection by initiating transcription of their own early genes via host transcription factors, such as NF-κb, STAT, and AP1. How the host copes with this immune escape has been a topic of interest. Tripartite motif (TRIM) family prote...

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Main Authors: Xiao-Tong Cao, Lian-Jie Wu, Feng-Lin Xu, Xin-Cang Li, Jiang-Feng Lan
Format: Article
Language:English
Published: BMC 2023-05-01
Series:Cell Communication and Signaling
Subjects:
Online Access:https://doi.org/10.1186/s12964-023-01059-7
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author Xiao-Tong Cao
Lian-Jie Wu
Feng-Lin Xu
Xin-Cang Li
Jiang-Feng Lan
author_facet Xiao-Tong Cao
Lian-Jie Wu
Feng-Lin Xu
Xin-Cang Li
Jiang-Feng Lan
author_sort Xiao-Tong Cao
collection DOAJ
description Abstract Viruses have evolved various strategies to achieve early infection by initiating transcription of their own early genes via host transcription factors, such as NF-κb, STAT, and AP1. How the host copes with this immune escape has been a topic of interest. Tripartite motif (TRIM) family proteins with RING-type domains have E3 ubiquitin ligase activity and are known as host restriction factors. Trim has been reported to be associated with phagocytosis and is also believed to be involved in the activation of autophagy. Preventing the virus from entering the host cell may be the most economical way for the host to resist virus infection. The role of TRIM in the early stage of virus infection in host cells remains to be further interpreted. In the current study, a crayfish TRIM with a RING-type domain, designated as PcTrim, was significantly upregulated under white spot syndrome virus (WSSV) infection in the red swamp crayfish (Procambarus clarkii). Recombinant PcTrim significantly inhibited WSSV replication in crayfish. RNAi targeting PcTrim or blocking PcTrim with an antibody promoted WSSV replication in crayfish. Pulldown and co-IP assays showed that PcTrim can interact with the virus protein VP26. PcTrim restricts the expression level of dynamin, which is involved in the regulation of phagocytosis, by inhibiting AP1 entry into the nucleus. AP1-RNAi effectively reduced the expression levels of dynamin and inhibited host cell endocytosis of WSSV in vivo. Our study demonstrated that PcTrim might reduce early WSSV infection by binding to VP26 and then inhibiting AP1 activation, resulting in reduced endocytosis of WSSV in crayfish hemocytes. Video Abstract
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spelling doaj.art-97718cd6063f4bce9ea4f1ea25f78c992023-05-14T11:22:46ZengBMCCell Communication and Signaling1478-811X2023-05-0121111410.1186/s12964-023-01059-7PcTrim prevents early infection with white spot syndrome virus by inhibiting AP1-induced endocytosisXiao-Tong Cao0Lian-Jie Wu1Feng-Lin Xu2Xin-Cang Li3Jiang-Feng Lan4Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural UniversityShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural UniversityShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural UniversityKey Laboratory of East China Sea Fishery Resources Exploitation, East China Sea Fisheries Research Institute, Chinese Academy of Fishery SciencesShandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural UniversityAbstract Viruses have evolved various strategies to achieve early infection by initiating transcription of their own early genes via host transcription factors, such as NF-κb, STAT, and AP1. How the host copes with this immune escape has been a topic of interest. Tripartite motif (TRIM) family proteins with RING-type domains have E3 ubiquitin ligase activity and are known as host restriction factors. Trim has been reported to be associated with phagocytosis and is also believed to be involved in the activation of autophagy. Preventing the virus from entering the host cell may be the most economical way for the host to resist virus infection. The role of TRIM in the early stage of virus infection in host cells remains to be further interpreted. In the current study, a crayfish TRIM with a RING-type domain, designated as PcTrim, was significantly upregulated under white spot syndrome virus (WSSV) infection in the red swamp crayfish (Procambarus clarkii). Recombinant PcTrim significantly inhibited WSSV replication in crayfish. RNAi targeting PcTrim or blocking PcTrim with an antibody promoted WSSV replication in crayfish. Pulldown and co-IP assays showed that PcTrim can interact with the virus protein VP26. PcTrim restricts the expression level of dynamin, which is involved in the regulation of phagocytosis, by inhibiting AP1 entry into the nucleus. AP1-RNAi effectively reduced the expression levels of dynamin and inhibited host cell endocytosis of WSSV in vivo. Our study demonstrated that PcTrim might reduce early WSSV infection by binding to VP26 and then inhibiting AP1 activation, resulting in reduced endocytosis of WSSV in crayfish hemocytes. Video Abstracthttps://doi.org/10.1186/s12964-023-01059-7Tripartite motif (TRIM)AP1White spot syndrome virusEndocytosisDynaminImmediate-early protein (IE1)
spellingShingle Xiao-Tong Cao
Lian-Jie Wu
Feng-Lin Xu
Xin-Cang Li
Jiang-Feng Lan
PcTrim prevents early infection with white spot syndrome virus by inhibiting AP1-induced endocytosis
Cell Communication and Signaling
Tripartite motif (TRIM)
AP1
White spot syndrome virus
Endocytosis
Dynamin
Immediate-early protein (IE1)
title PcTrim prevents early infection with white spot syndrome virus by inhibiting AP1-induced endocytosis
title_full PcTrim prevents early infection with white spot syndrome virus by inhibiting AP1-induced endocytosis
title_fullStr PcTrim prevents early infection with white spot syndrome virus by inhibiting AP1-induced endocytosis
title_full_unstemmed PcTrim prevents early infection with white spot syndrome virus by inhibiting AP1-induced endocytosis
title_short PcTrim prevents early infection with white spot syndrome virus by inhibiting AP1-induced endocytosis
title_sort pctrim prevents early infection with white spot syndrome virus by inhibiting ap1 induced endocytosis
topic Tripartite motif (TRIM)
AP1
White spot syndrome virus
Endocytosis
Dynamin
Immediate-early protein (IE1)
url https://doi.org/10.1186/s12964-023-01059-7
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