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Zebrafish F-box Protein fbxo3 Negatively Regulates Antiviral Response through Promoting K27-Linked Polyubiquitination of the Transcription Factors irf3 and irf7

Zhi Li, Sijia Fan, Jing Wang, Xiaoyun Chen, Qian Liao, Xing Liu, Gang Ouyang, Hong Cao and Wuhan Xiao
J Immunol October 1, 2020, 205 (7) 1897-1908; DOI: https://doi.org/10.4049/jimmunol.2000305
Zhi Li
*State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
†The Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
‡The Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
§The Innovation Academy of Seed Design, Chinese Academy of Sciences, Wuhan 430072, China; and
¶University of Chinese Academy of Sciences, Beijing 100049, China
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Sijia Fan
*State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
†The Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
‡The Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
§The Innovation Academy of Seed Design, Chinese Academy of Sciences, Wuhan 430072, China; and
¶University of Chinese Academy of Sciences, Beijing 100049, China
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Jing Wang
*State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
†The Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
‡The Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
§The Innovation Academy of Seed Design, Chinese Academy of Sciences, Wuhan 430072, China; and
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  • ORCID record for Jing Wang
Xiaoyun Chen
*State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
†The Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
‡The Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
§The Innovation Academy of Seed Design, Chinese Academy of Sciences, Wuhan 430072, China; and
¶University of Chinese Academy of Sciences, Beijing 100049, China
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Qian Liao
*State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
†The Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
‡The Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
§The Innovation Academy of Seed Design, Chinese Academy of Sciences, Wuhan 430072, China; and
¶University of Chinese Academy of Sciences, Beijing 100049, China
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Xing Liu
*State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
†The Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
‡The Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
§The Innovation Academy of Seed Design, Chinese Academy of Sciences, Wuhan 430072, China; and
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Gang Ouyang
*State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
†The Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
‡The Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
§The Innovation Academy of Seed Design, Chinese Academy of Sciences, Wuhan 430072, China; and
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Hong Cao
*State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
†The Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
‡The Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
§The Innovation Academy of Seed Design, Chinese Academy of Sciences, Wuhan 430072, China; and
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Wuhan Xiao
*State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
†The Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
‡The Key Laboratory of Aquatic Biodiversity and Conservation, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, People’s Republic of China;
§The Innovation Academy of Seed Design, Chinese Academy of Sciences, Wuhan 430072, China; and
¶University of Chinese Academy of Sciences, Beijing 100049, China
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This article has a correction. Please see:

  • Errata - January 01, 2021

Key Points

  • Zebrafish fbxo3 negatively regulates antiviral responses.

  • Zebrafish fbxo3 inhibits expression of antiviral response genes upon SVCV infection.

  • Zebrafish fbxo3 promotes degradation of irf3 and irf7 by catalyzing ubiquitination.

Abstract

FBXO3, belongs to the F-box family of proteins, which has been reported to involve in host autoimmune and inflammatory responses by promoting its substrates for ubiquitylation. However, thus far, its physiological function in antiviral immunity remains elusive. In this study, we report that overexpression of zebrafish fbxo3 suppresses cellular antiviral responses. Moreover, disruption of fbxo3 in zebrafish increases the survival rate upon spring viremia of carp virus exposure. Further assays indicate that fbxo3 interacts with irf3/irf7 and specifically catalyzes K27-linked ubiquitination of irf3 and irf7, resulting in proteasomal degradation of irf3 and irf7. However, the F-box domain of fbxo3 is not required for fbxo3 to interact with irf3/irf7 and to inhibit transactivity of irf3 and irf7. This study provides novel insights into fbxo3 function and the underlying mechanisms. In addition, it sheds new light on the regulation of IFN-I signaling by F-box proteins.

This article is featured in Top Reads, p.1719

Footnotes

  • This work was supported by Strategic Priority Research Program of the Chinese Academy of Sciences Grant XDA24010308, National Natural Science Foundation of China Grants 31830101, 31721005, and 31671315, and National Key Research and Development Program of China Grant 2018YFD0900602.

  • The online version of this article contains supplemental material.

  • Abbreviations used in this article:

    CHX
    cycloheximide
    CPE
    cytopathic effect
    dpf
    day postfertilization
    EPC
    epithelioma papulosum cyprini
    HEK
    human embryonic kidney
    IFN-I
    type I IFN signaling
    IRF
    IFN regulatory factor
    ISRE
    IFN-stimulated response element
    M1
    mutant 1
    M2
    mutant 2
    MAVS
    mitochondrial antiviral signaling protein
    MOI
    multiplicity of infection
    mpf
    month postfertilization
    PTM
    posttranslational modification
    qRT-PCR
    quantitative real-time PCR
    RIG-I
    retinoic acid–inducible gene-I
    RLR
    RIG-I–like receptor
    SCF
    SKP1–Cullin1–F-box
    sgRNA
    single-guide RNA
    SVSC
    spring viremia of carp virus
    TCID50
    50% tissue culture–infective dose
    WT
    wild-type
    ZFL
    zebrafish liver.

  • Received March 20, 2020.
  • Accepted July 29, 2020.
  • Copyright © 2020 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 205 (7)
The Journal of Immunology
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1 Oct 2020
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Zebrafish F-box Protein fbxo3 Negatively Regulates Antiviral Response through Promoting K27-Linked Polyubiquitination of the Transcription Factors irf3 and irf7
Zhi Li, Sijia Fan, Jing Wang, Xiaoyun Chen, Qian Liao, Xing Liu, Gang Ouyang, Hong Cao, Wuhan Xiao
The Journal of Immunology October 1, 2020, 205 (7) 1897-1908; DOI: 10.4049/jimmunol.2000305

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Zebrafish F-box Protein fbxo3 Negatively Regulates Antiviral Response through Promoting K27-Linked Polyubiquitination of the Transcription Factors irf3 and irf7
Zhi Li, Sijia Fan, Jing Wang, Xiaoyun Chen, Qian Liao, Xing Liu, Gang Ouyang, Hong Cao, Wuhan Xiao
The Journal of Immunology October 1, 2020, 205 (7) 1897-1908; DOI: 10.4049/jimmunol.2000305
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