Comparative Proteomics Reveals Strain-Specific β-TrCP Degradation via Rotavirus NSP1 Hijacking a Host Cullin-3-Rbx1 Complex.

Rotaviruses (RVs) are the leading cause of severe gastroenteritis in young children, accounting for half a million deaths annually worldwide. RV encodes non-structural protein 1 (NSP1), a well-characterized interferon (IFN) antagonist, which facilitates virus replication by mediating the degradation...

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Main Authors: Siyuan Ding, Nancie Mooney, Bin Li, Marcus R Kelly, Ningguo Feng, Alexander V Loktev, Adrish Sen, John T Patton, Peter K Jackson, Harry B Greenberg
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2016-10-01
Series:PLoS Pathogens
Online Access:https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1005929&type=printable
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author Siyuan Ding
Nancie Mooney
Bin Li
Marcus R Kelly
Ningguo Feng
Alexander V Loktev
Adrish Sen
John T Patton
Peter K Jackson
Harry B Greenberg
author_facet Siyuan Ding
Nancie Mooney
Bin Li
Marcus R Kelly
Ningguo Feng
Alexander V Loktev
Adrish Sen
John T Patton
Peter K Jackson
Harry B Greenberg
author_sort Siyuan Ding
collection DOAJ
description Rotaviruses (RVs) are the leading cause of severe gastroenteritis in young children, accounting for half a million deaths annually worldwide. RV encodes non-structural protein 1 (NSP1), a well-characterized interferon (IFN) antagonist, which facilitates virus replication by mediating the degradation of host antiviral factors including IRF3 and β-TrCP. Here, we utilized six human and animal RV NSP1s as baits and performed tandem-affinity purification coupled with high-resolution mass spectrometry to comprehensively characterize NSP1-host protein interaction network. Multiple Cullin-RING ubiquitin ligase (CRL) complexes were identified. Importantly, inhibition of cullin-3 (Cul3) or RING-box protein 1 (Rbx1), by siRNA silencing or chemical perturbation, significantly impairs strain-specific NSP1-mediated β-TrCP degradation. Mechanistically, we demonstrate that NSP1 localizes to the Golgi with the host Cul3-Rbx1 CRL complex, which targets β-TrCP and NSP1 for co-destruction at the proteasome. Our study uncovers a novel mechanism that RV employs to promote β-TrCP turnover and provides molecular insights into virus-mediated innate immunity inhibition.
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institution DOAJ
issn 1553-7366
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language English
publishDate 2016-10-01
publisher Public Library of Science (PLoS)
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spelling doaj-art-1a4783667f544669ba3c3d44d78db0762025-08-20T03:04:53ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742016-10-011210e100592910.1371/journal.ppat.1005929Comparative Proteomics Reveals Strain-Specific β-TrCP Degradation via Rotavirus NSP1 Hijacking a Host Cullin-3-Rbx1 Complex.Siyuan DingNancie MooneyBin LiMarcus R KellyNingguo FengAlexander V LoktevAdrish SenJohn T PattonPeter K JacksonHarry B GreenbergRotaviruses (RVs) are the leading cause of severe gastroenteritis in young children, accounting for half a million deaths annually worldwide. RV encodes non-structural protein 1 (NSP1), a well-characterized interferon (IFN) antagonist, which facilitates virus replication by mediating the degradation of host antiviral factors including IRF3 and β-TrCP. Here, we utilized six human and animal RV NSP1s as baits and performed tandem-affinity purification coupled with high-resolution mass spectrometry to comprehensively characterize NSP1-host protein interaction network. Multiple Cullin-RING ubiquitin ligase (CRL) complexes were identified. Importantly, inhibition of cullin-3 (Cul3) or RING-box protein 1 (Rbx1), by siRNA silencing or chemical perturbation, significantly impairs strain-specific NSP1-mediated β-TrCP degradation. Mechanistically, we demonstrate that NSP1 localizes to the Golgi with the host Cul3-Rbx1 CRL complex, which targets β-TrCP and NSP1 for co-destruction at the proteasome. Our study uncovers a novel mechanism that RV employs to promote β-TrCP turnover and provides molecular insights into virus-mediated innate immunity inhibition.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1005929&type=printable
spellingShingle Siyuan Ding
Nancie Mooney
Bin Li
Marcus R Kelly
Ningguo Feng
Alexander V Loktev
Adrish Sen
John T Patton
Peter K Jackson
Harry B Greenberg
Comparative Proteomics Reveals Strain-Specific β-TrCP Degradation via Rotavirus NSP1 Hijacking a Host Cullin-3-Rbx1 Complex.
PLoS Pathogens
title Comparative Proteomics Reveals Strain-Specific β-TrCP Degradation via Rotavirus NSP1 Hijacking a Host Cullin-3-Rbx1 Complex.
title_full Comparative Proteomics Reveals Strain-Specific β-TrCP Degradation via Rotavirus NSP1 Hijacking a Host Cullin-3-Rbx1 Complex.
title_fullStr Comparative Proteomics Reveals Strain-Specific β-TrCP Degradation via Rotavirus NSP1 Hijacking a Host Cullin-3-Rbx1 Complex.
title_full_unstemmed Comparative Proteomics Reveals Strain-Specific β-TrCP Degradation via Rotavirus NSP1 Hijacking a Host Cullin-3-Rbx1 Complex.
title_short Comparative Proteomics Reveals Strain-Specific β-TrCP Degradation via Rotavirus NSP1 Hijacking a Host Cullin-3-Rbx1 Complex.
title_sort comparative proteomics reveals strain specific β trcp degradation via rotavirus nsp1 hijacking a host cullin 3 rbx1 complex
url https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1005929&type=printable
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