Manipulation of the unfolded protein response: A pharmacological strategy against coronavirus infection.

Coronavirus infection induces the unfolded protein response (UPR), a cellular signalling pathway composed of three branches, triggered by unfolded proteins in the endoplasmic reticulum (ER) due to high ER load. We have used RNA sequencing and ribosome profiling to investigate holistically the transc...

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Main Authors: Liliana Echavarría-Consuegra, Georgia M Cook, Idoia Busnadiego, Charlotte Lefèvre, Sarah Keep, Katherine Brown, Nicole Doyle, Giulia Dowgier, Krzysztof Franaszek, Nathan A Moore, Stuart G Siddell, Erica Bickerton, Benjamin G Hale, Andrew E Firth, Ian Brierley, Nerea Irigoyen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-06-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1009644
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author Liliana Echavarría-Consuegra
Georgia M Cook
Idoia Busnadiego
Charlotte Lefèvre
Sarah Keep
Katherine Brown
Nicole Doyle
Giulia Dowgier
Krzysztof Franaszek
Nathan A Moore
Stuart G Siddell
Erica Bickerton
Benjamin G Hale
Andrew E Firth
Ian Brierley
Nerea Irigoyen
author_facet Liliana Echavarría-Consuegra
Georgia M Cook
Idoia Busnadiego
Charlotte Lefèvre
Sarah Keep
Katherine Brown
Nicole Doyle
Giulia Dowgier
Krzysztof Franaszek
Nathan A Moore
Stuart G Siddell
Erica Bickerton
Benjamin G Hale
Andrew E Firth
Ian Brierley
Nerea Irigoyen
author_sort Liliana Echavarría-Consuegra
collection DOAJ
description Coronavirus infection induces the unfolded protein response (UPR), a cellular signalling pathway composed of three branches, triggered by unfolded proteins in the endoplasmic reticulum (ER) due to high ER load. We have used RNA sequencing and ribosome profiling to investigate holistically the transcriptional and translational response to cellular infection by murine hepatitis virus (MHV), often used as a model for the Betacoronavirus genus to which the recently emerged SARS-CoV-2 also belongs. We found the UPR to be amongst the most significantly up-regulated pathways in response to MHV infection. To confirm and extend these observations, we show experimentally the induction of all three branches of the UPR in both MHV- and SARS-CoV-2-infected cells. Over-expression of the SARS-CoV-2 ORF8 or S proteins alone is itself sufficient to induce the UPR. Remarkably, pharmacological inhibition of the UPR greatly reduced the replication of both MHV and SARS-CoV-2, revealing the importance of this pathway for successful coronavirus replication. This was particularly striking when both IRE1α and ATF6 branches of the UPR were inhibited, reducing SARS-CoV-2 virion release (~1,000-fold). Together, these data highlight the UPR as a promising antiviral target to combat coronavirus infection.
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spelling doaj-art-eaf77300e108401e93e7f0b5b3c8dc132025-08-20T02:33:18ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742021-06-01176e100964410.1371/journal.ppat.1009644Manipulation of the unfolded protein response: A pharmacological strategy against coronavirus infection.Liliana Echavarría-ConsuegraGeorgia M CookIdoia BusnadiegoCharlotte LefèvreSarah KeepKatherine BrownNicole DoyleGiulia DowgierKrzysztof FranaszekNathan A MooreStuart G SiddellErica BickertonBenjamin G HaleAndrew E FirthIan BrierleyNerea IrigoyenCoronavirus infection induces the unfolded protein response (UPR), a cellular signalling pathway composed of three branches, triggered by unfolded proteins in the endoplasmic reticulum (ER) due to high ER load. We have used RNA sequencing and ribosome profiling to investigate holistically the transcriptional and translational response to cellular infection by murine hepatitis virus (MHV), often used as a model for the Betacoronavirus genus to which the recently emerged SARS-CoV-2 also belongs. We found the UPR to be amongst the most significantly up-regulated pathways in response to MHV infection. To confirm and extend these observations, we show experimentally the induction of all three branches of the UPR in both MHV- and SARS-CoV-2-infected cells. Over-expression of the SARS-CoV-2 ORF8 or S proteins alone is itself sufficient to induce the UPR. Remarkably, pharmacological inhibition of the UPR greatly reduced the replication of both MHV and SARS-CoV-2, revealing the importance of this pathway for successful coronavirus replication. This was particularly striking when both IRE1α and ATF6 branches of the UPR were inhibited, reducing SARS-CoV-2 virion release (~1,000-fold). Together, these data highlight the UPR as a promising antiviral target to combat coronavirus infection.https://doi.org/10.1371/journal.ppat.1009644
spellingShingle Liliana Echavarría-Consuegra
Georgia M Cook
Idoia Busnadiego
Charlotte Lefèvre
Sarah Keep
Katherine Brown
Nicole Doyle
Giulia Dowgier
Krzysztof Franaszek
Nathan A Moore
Stuart G Siddell
Erica Bickerton
Benjamin G Hale
Andrew E Firth
Ian Brierley
Nerea Irigoyen
Manipulation of the unfolded protein response: A pharmacological strategy against coronavirus infection.
PLoS Pathogens
title Manipulation of the unfolded protein response: A pharmacological strategy against coronavirus infection.
title_full Manipulation of the unfolded protein response: A pharmacological strategy against coronavirus infection.
title_fullStr Manipulation of the unfolded protein response: A pharmacological strategy against coronavirus infection.
title_full_unstemmed Manipulation of the unfolded protein response: A pharmacological strategy against coronavirus infection.
title_short Manipulation of the unfolded protein response: A pharmacological strategy against coronavirus infection.
title_sort manipulation of the unfolded protein response a pharmacological strategy against coronavirus infection
url https://doi.org/10.1371/journal.ppat.1009644
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