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Critical Roles of G3BP1 in Red-Spotted Grouper Nervous Necrosis Virus-Induced Stress Granule Formation and Viral Replication in Orange-Spotted Grouper (Epinephelus coioides)

Viral infection causes changes in the internal environment of host cells, and a series of stress responses are generated to respond to these changes and help the cell survive. Stress granule (SG) formation is a type of cellular stress response that inhibits viral replication. However, the relationsh...

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Autores principales: Sun, Mengshi, Wu, Siting, Kang, Shaozhu, Liao, Jiaming, Zhang, Luhao, Xu, Zhuqing, Chen, Hong, Xu, Linting, Zhang, Xin, Qin, Qiwei, Wei, Jingguang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9354888/
https://www.ncbi.nlm.nih.gov/pubmed/35935992
http://dx.doi.org/10.3389/fimmu.2022.931534
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author Sun, Mengshi
Wu, Siting
Kang, Shaozhu
Liao, Jiaming
Zhang, Luhao
Xu, Zhuqing
Chen, Hong
Xu, Linting
Zhang, Xin
Qin, Qiwei
Wei, Jingguang
author_facet Sun, Mengshi
Wu, Siting
Kang, Shaozhu
Liao, Jiaming
Zhang, Luhao
Xu, Zhuqing
Chen, Hong
Xu, Linting
Zhang, Xin
Qin, Qiwei
Wei, Jingguang
author_sort Sun, Mengshi
collection PubMed
description Viral infection causes changes in the internal environment of host cells, and a series of stress responses are generated to respond to these changes and help the cell survive. Stress granule (SG) formation is a type of cellular stress response that inhibits viral replication. However, the relationship between red-spotted grouper nervous necrosis virus (RGNNV) infection and SGs, and the roles of the SG marker protein RAS GTPase-activating protein (SH3 domain)-binding protein 1 (G3BP1) in viral infection remain unclear. In this study, RGNNV infection induced grouper spleen (GS) cells to produce SGs. The SGs particles co-located with the classic SG marker protein eIF3η, and some SGs depolymerized under treatment with the translation inhibitor, cycloheximide (CHX). In addition, when the four kinases of the eukaryotic translation initiation factor 2α (eIF2α)-dependent pathway were inhibited, knockdown of HRI and GCN2 with small interfering RNAs and inhibition of PKR with 2-aminopurine had little effect on the formation of SGs, but the PERK inhibitor significantly inhibited the formation of SGs and decreased the phosphorylation of eIF2α. G3BP1 of Epinephelus coioides (named as EcG3BP1) encodes 495 amino acids with a predicted molecular weight of 54.12 kDa and 65.9% homology with humans. Overexpression of EcG3BP1 inhibited the replication of RGNNV in vitro by up-regulating the interferon and inflammatory response, whereas knockdown of EcG3BP1 promoted the replication of RGNNV. These results provide a better understanding of the relationship between SGs and viral infection in fish.
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spelling pubmed-93548882022-08-06 Critical Roles of G3BP1 in Red-Spotted Grouper Nervous Necrosis Virus-Induced Stress Granule Formation and Viral Replication in Orange-Spotted Grouper (Epinephelus coioides) Sun, Mengshi Wu, Siting Kang, Shaozhu Liao, Jiaming Zhang, Luhao Xu, Zhuqing Chen, Hong Xu, Linting Zhang, Xin Qin, Qiwei Wei, Jingguang Front Immunol Immunology Viral infection causes changes in the internal environment of host cells, and a series of stress responses are generated to respond to these changes and help the cell survive. Stress granule (SG) formation is a type of cellular stress response that inhibits viral replication. However, the relationship between red-spotted grouper nervous necrosis virus (RGNNV) infection and SGs, and the roles of the SG marker protein RAS GTPase-activating protein (SH3 domain)-binding protein 1 (G3BP1) in viral infection remain unclear. In this study, RGNNV infection induced grouper spleen (GS) cells to produce SGs. The SGs particles co-located with the classic SG marker protein eIF3η, and some SGs depolymerized under treatment with the translation inhibitor, cycloheximide (CHX). In addition, when the four kinases of the eukaryotic translation initiation factor 2α (eIF2α)-dependent pathway were inhibited, knockdown of HRI and GCN2 with small interfering RNAs and inhibition of PKR with 2-aminopurine had little effect on the formation of SGs, but the PERK inhibitor significantly inhibited the formation of SGs and decreased the phosphorylation of eIF2α. G3BP1 of Epinephelus coioides (named as EcG3BP1) encodes 495 amino acids with a predicted molecular weight of 54.12 kDa and 65.9% homology with humans. Overexpression of EcG3BP1 inhibited the replication of RGNNV in vitro by up-regulating the interferon and inflammatory response, whereas knockdown of EcG3BP1 promoted the replication of RGNNV. These results provide a better understanding of the relationship between SGs and viral infection in fish. Frontiers Media S.A. 2022-07-22 /pmc/articles/PMC9354888/ /pubmed/35935992 http://dx.doi.org/10.3389/fimmu.2022.931534 Text en Copyright © 2022 Sun, Wu, Kang, Liao, Zhang, Xu, Chen, Xu, Zhang, Qin and Wei https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Sun, Mengshi
Wu, Siting
Kang, Shaozhu
Liao, Jiaming
Zhang, Luhao
Xu, Zhuqing
Chen, Hong
Xu, Linting
Zhang, Xin
Qin, Qiwei
Wei, Jingguang
Critical Roles of G3BP1 in Red-Spotted Grouper Nervous Necrosis Virus-Induced Stress Granule Formation and Viral Replication in Orange-Spotted Grouper (Epinephelus coioides)
title Critical Roles of G3BP1 in Red-Spotted Grouper Nervous Necrosis Virus-Induced Stress Granule Formation and Viral Replication in Orange-Spotted Grouper (Epinephelus coioides)
title_full Critical Roles of G3BP1 in Red-Spotted Grouper Nervous Necrosis Virus-Induced Stress Granule Formation and Viral Replication in Orange-Spotted Grouper (Epinephelus coioides)
title_fullStr Critical Roles of G3BP1 in Red-Spotted Grouper Nervous Necrosis Virus-Induced Stress Granule Formation and Viral Replication in Orange-Spotted Grouper (Epinephelus coioides)
title_full_unstemmed Critical Roles of G3BP1 in Red-Spotted Grouper Nervous Necrosis Virus-Induced Stress Granule Formation and Viral Replication in Orange-Spotted Grouper (Epinephelus coioides)
title_short Critical Roles of G3BP1 in Red-Spotted Grouper Nervous Necrosis Virus-Induced Stress Granule Formation and Viral Replication in Orange-Spotted Grouper (Epinephelus coioides)
title_sort critical roles of g3bp1 in red-spotted grouper nervous necrosis virus-induced stress granule formation and viral replication in orange-spotted grouper (epinephelus coioides)
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9354888/
https://www.ncbi.nlm.nih.gov/pubmed/35935992
http://dx.doi.org/10.3389/fimmu.2022.931534
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