Global siRNA screen identifies human host factors critical for SARS-CoV-2 replication and late stages of infection.

Defining the subset of cellular factors governing SARS-CoV-2 replication can provide critical insights into viral pathogenesis and identify targets for host-directed antiviral therapies. While a number of genetic screens have previously reported SARS-CoV-2 host dependency factors, most of these appr...

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Main Authors: Xin Yin, Yuan Pu, Shuofeng Yuan, Lars Pache, Christopher Churas, Stuart Weston, Laura Riva, Lacy M Simons, William J Cisneros, Thomas Clausen, Grace Biddle, Simon Doss-Gollin, Meagan Deming, Paul D De Jesus, Ha Na Kim, Daniel Fuentes, John M Whitelock, Jeffrey D Esko, Megan S Lord, Ignacio Mena, Adolfo García-Sastre, Judd F Hultquist, Matthew B Frieman, Trey Ideker, Dexter Pratt, Laura Martin-Sancho, Sumit K Chanda
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-06-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3002738
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author Xin Yin
Yuan Pu
Shuofeng Yuan
Lars Pache
Christopher Churas
Stuart Weston
Laura Riva
Lacy M Simons
William J Cisneros
Thomas Clausen
Grace Biddle
Simon Doss-Gollin
Meagan Deming
Paul D De Jesus
Ha Na Kim
Daniel Fuentes
John M Whitelock
Jeffrey D Esko
Megan S Lord
Ignacio Mena
Adolfo García-Sastre
Judd F Hultquist
Matthew B Frieman
Trey Ideker
Dexter Pratt
Laura Martin-Sancho
Sumit K Chanda
author_facet Xin Yin
Yuan Pu
Shuofeng Yuan
Lars Pache
Christopher Churas
Stuart Weston
Laura Riva
Lacy M Simons
William J Cisneros
Thomas Clausen
Grace Biddle
Simon Doss-Gollin
Meagan Deming
Paul D De Jesus
Ha Na Kim
Daniel Fuentes
John M Whitelock
Jeffrey D Esko
Megan S Lord
Ignacio Mena
Adolfo García-Sastre
Judd F Hultquist
Matthew B Frieman
Trey Ideker
Dexter Pratt
Laura Martin-Sancho
Sumit K Chanda
author_sort Xin Yin
collection DOAJ
description Defining the subset of cellular factors governing SARS-CoV-2 replication can provide critical insights into viral pathogenesis and identify targets for host-directed antiviral therapies. While a number of genetic screens have previously reported SARS-CoV-2 host dependency factors, most of these approaches relied on utilizing pooled genome-scale CRISPR libraries, which are biased toward the discovery of host proteins impacting early stages of viral replication. To identify host factors involved throughout the SARS-CoV-2 infectious cycle, we conducted an arrayed genome-scale siRNA screen. Resulting data were integrated with published functional screens and proteomics data to reveal (i) common pathways that were identified in all OMICs datasets-including regulation of Wnt signaling and gap junctions, (ii) pathways uniquely identified in this screen-including NADH oxidation, or (iii) pathways supported by this screen and proteomics data but not published functional screens-including arachionate production and MAPK signaling. The identified proviral host factors were mapped into the SARS-CoV-2 infectious cycle, including 32 proteins that were determined to impact viral replication and 27 impacting late stages of infection, respectively. Additionally, a subset of proteins was tested across other coronaviruses revealing a subset of proviral factors that were conserved across pandemic SARS-CoV-2, epidemic SARS-CoV-1 and MERS-CoV, and the seasonal coronavirus OC43-CoV. Further studies illuminated a role for the heparan sulfate proteoglycan perlecan in SARS-CoV-2 viral entry and found that inhibition of the non-canonical NF-kB pathway through targeting of BIRC2 restricts SARS-CoV-2 replication both in vitro and in vivo. These studies provide critical insight into the landscape of virus-host interactions driving SARS-CoV-2 replication as well as valuable targets for host-directed antivirals.
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publisher Public Library of Science (PLoS)
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spelling doaj-art-1ab0ff39590944df975161f024ece3aa2025-08-20T02:36:20ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852025-06-01236e300273810.1371/journal.pbio.3002738Global siRNA screen identifies human host factors critical for SARS-CoV-2 replication and late stages of infection.Xin YinYuan PuShuofeng YuanLars PacheChristopher ChurasStuart WestonLaura RivaLacy M SimonsWilliam J CisnerosThomas ClausenGrace BiddleSimon Doss-GollinMeagan DemingPaul D De JesusHa Na KimDaniel FuentesJohn M WhitelockJeffrey D EskoMegan S LordIgnacio MenaAdolfo García-SastreJudd F HultquistMatthew B FriemanTrey IdekerDexter PrattLaura Martin-SanchoSumit K ChandaDefining the subset of cellular factors governing SARS-CoV-2 replication can provide critical insights into viral pathogenesis and identify targets for host-directed antiviral therapies. While a number of genetic screens have previously reported SARS-CoV-2 host dependency factors, most of these approaches relied on utilizing pooled genome-scale CRISPR libraries, which are biased toward the discovery of host proteins impacting early stages of viral replication. To identify host factors involved throughout the SARS-CoV-2 infectious cycle, we conducted an arrayed genome-scale siRNA screen. Resulting data were integrated with published functional screens and proteomics data to reveal (i) common pathways that were identified in all OMICs datasets-including regulation of Wnt signaling and gap junctions, (ii) pathways uniquely identified in this screen-including NADH oxidation, or (iii) pathways supported by this screen and proteomics data but not published functional screens-including arachionate production and MAPK signaling. The identified proviral host factors were mapped into the SARS-CoV-2 infectious cycle, including 32 proteins that were determined to impact viral replication and 27 impacting late stages of infection, respectively. Additionally, a subset of proteins was tested across other coronaviruses revealing a subset of proviral factors that were conserved across pandemic SARS-CoV-2, epidemic SARS-CoV-1 and MERS-CoV, and the seasonal coronavirus OC43-CoV. Further studies illuminated a role for the heparan sulfate proteoglycan perlecan in SARS-CoV-2 viral entry and found that inhibition of the non-canonical NF-kB pathway through targeting of BIRC2 restricts SARS-CoV-2 replication both in vitro and in vivo. These studies provide critical insight into the landscape of virus-host interactions driving SARS-CoV-2 replication as well as valuable targets for host-directed antivirals.https://doi.org/10.1371/journal.pbio.3002738
spellingShingle Xin Yin
Yuan Pu
Shuofeng Yuan
Lars Pache
Christopher Churas
Stuart Weston
Laura Riva
Lacy M Simons
William J Cisneros
Thomas Clausen
Grace Biddle
Simon Doss-Gollin
Meagan Deming
Paul D De Jesus
Ha Na Kim
Daniel Fuentes
John M Whitelock
Jeffrey D Esko
Megan S Lord
Ignacio Mena
Adolfo García-Sastre
Judd F Hultquist
Matthew B Frieman
Trey Ideker
Dexter Pratt
Laura Martin-Sancho
Sumit K Chanda
Global siRNA screen identifies human host factors critical for SARS-CoV-2 replication and late stages of infection.
PLoS Biology
title Global siRNA screen identifies human host factors critical for SARS-CoV-2 replication and late stages of infection.
title_full Global siRNA screen identifies human host factors critical for SARS-CoV-2 replication and late stages of infection.
title_fullStr Global siRNA screen identifies human host factors critical for SARS-CoV-2 replication and late stages of infection.
title_full_unstemmed Global siRNA screen identifies human host factors critical for SARS-CoV-2 replication and late stages of infection.
title_short Global siRNA screen identifies human host factors critical for SARS-CoV-2 replication and late stages of infection.
title_sort global sirna screen identifies human host factors critical for sars cov 2 replication and late stages of infection
url https://doi.org/10.1371/journal.pbio.3002738
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