Inhibition of coronavirus HCoV-OC43 by targeting the eIF4F complex

The translation initiation complex 4F (eIF4F) is a rate-limiting factor in protein synthesis. Alterations in eIF4F activity are linked to several diseases, including cancer and infectious diseases. To this end, coronaviruses require eIF4F complex activity to produce proteins essential for their life...

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Main Authors: Yongmei Feng, Stefan Grotegut, Predrag Jovanovic, Valentina Gandin, Steven H. Olson, Rabi Murad, Anne Beall, Sharon Colayco, Paul De-Jesus, Sumit Chanda, Brian P. English, Robert H. Singer, Michael Jackson, Ivan Topisirovic, Ze’ev A. Ronai
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Pharmacology
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Online Access:https://www.frontiersin.org/articles/10.3389/fphar.2022.1029093/full
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author Yongmei Feng
Stefan Grotegut
Predrag Jovanovic
Valentina Gandin
Steven H. Olson
Rabi Murad
Anne Beall
Sharon Colayco
Paul De-Jesus
Sumit Chanda
Brian P. English
Robert H. Singer
Michael Jackson
Ivan Topisirovic
Ze’ev A. Ronai
author_facet Yongmei Feng
Stefan Grotegut
Predrag Jovanovic
Valentina Gandin
Steven H. Olson
Rabi Murad
Anne Beall
Sharon Colayco
Paul De-Jesus
Sumit Chanda
Brian P. English
Robert H. Singer
Michael Jackson
Ivan Topisirovic
Ze’ev A. Ronai
author_sort Yongmei Feng
collection DOAJ
description The translation initiation complex 4F (eIF4F) is a rate-limiting factor in protein synthesis. Alterations in eIF4F activity are linked to several diseases, including cancer and infectious diseases. To this end, coronaviruses require eIF4F complex activity to produce proteins essential for their life cycle. Efforts to target coronaviruses by abrogating translation have been largely limited to repurposing existing eIF4F complex inhibitors. Here, we report the results of a high throughput screen to identify small molecules that disrupt eIF4F complex formation and inhibit coronavirus RNA and protein levels. Of 338,000 small molecules screened for inhibition of the eIF4F-driven, CAP-dependent translation, we identified SBI-1232 and two structurally related analogs, SBI-5844 and SBI-0498, that inhibit human coronavirus OC43 (HCoV-OC43; OC43) with minimal cell toxicity. Notably, gene expression changes after OC43 infection of Vero E6 or A549 cells were effectively reverted upon treatment with SBI-5844 or SBI-0498. Moreover, SBI-5844 or SBI-0498 treatment effectively impeded the eIF4F complex assembly, with concomitant inhibition of newly synthesized OC43 nucleocapsid protein and OC43 RNA and protein levels. Overall, we identify SBI-5844 and SBI-0498 as small molecules targeting the eIF4F complex that may limit coronavirus transcripts and proteins, thereby representing a basis for developing novel therapeutic modalities against coronaviruses.
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spelling doaj-art-3f5893fb1bab4b94b39dab0daec386242024-12-19T09:07:16ZengFrontiers Media S.A.Frontiers in Pharmacology1663-98122022-12-011310.3389/fphar.2022.10290931029093Inhibition of coronavirus HCoV-OC43 by targeting the eIF4F complexYongmei Feng0Stefan Grotegut1Predrag Jovanovic2Valentina Gandin3Steven H. Olson4Rabi Murad5Anne Beall6Sharon Colayco7Paul De-Jesus8Sumit Chanda9Brian P. English10Robert H. Singer11Michael Jackson12Ivan Topisirovic13Ze’ev A. Ronai14Cancer Center at Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesConrad Prebys Center for Chemical Genomics at Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesLady Davis Institute, SMBD Jewish General Hospital, Gerald Bronfman Department of Oncology and Division of Experimental Medicine, McGill University, Montreal, QC, CanadaJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, United StatesConrad Prebys Center for Chemical Genomics at Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesCancer Center at Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesImmunology and Infectious Disease Center at Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesImmunology and Infectious Disease Center at Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesImmunology and Infectious Disease Center at Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesImmunology and Infectious Disease Center at Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, United StatesJanelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, United StatesConrad Prebys Center for Chemical Genomics at Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesLady Davis Institute, SMBD Jewish General Hospital, Gerald Bronfman Department of Oncology and Division of Experimental Medicine, McGill University, Montreal, QC, CanadaCancer Center at Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA, United StatesThe translation initiation complex 4F (eIF4F) is a rate-limiting factor in protein synthesis. Alterations in eIF4F activity are linked to several diseases, including cancer and infectious diseases. To this end, coronaviruses require eIF4F complex activity to produce proteins essential for their life cycle. Efforts to target coronaviruses by abrogating translation have been largely limited to repurposing existing eIF4F complex inhibitors. Here, we report the results of a high throughput screen to identify small molecules that disrupt eIF4F complex formation and inhibit coronavirus RNA and protein levels. Of 338,000 small molecules screened for inhibition of the eIF4F-driven, CAP-dependent translation, we identified SBI-1232 and two structurally related analogs, SBI-5844 and SBI-0498, that inhibit human coronavirus OC43 (HCoV-OC43; OC43) with minimal cell toxicity. Notably, gene expression changes after OC43 infection of Vero E6 or A549 cells were effectively reverted upon treatment with SBI-5844 or SBI-0498. Moreover, SBI-5844 or SBI-0498 treatment effectively impeded the eIF4F complex assembly, with concomitant inhibition of newly synthesized OC43 nucleocapsid protein and OC43 RNA and protein levels. Overall, we identify SBI-5844 and SBI-0498 as small molecules targeting the eIF4F complex that may limit coronavirus transcripts and proteins, thereby representing a basis for developing novel therapeutic modalities against coronaviruses.https://www.frontiersin.org/articles/10.3389/fphar.2022.1029093/fullCOVID-19OC43SARS-CoV-2coronaviruseIF4Ftranslation initiation complex
spellingShingle Yongmei Feng
Stefan Grotegut
Predrag Jovanovic
Valentina Gandin
Steven H. Olson
Rabi Murad
Anne Beall
Sharon Colayco
Paul De-Jesus
Sumit Chanda
Brian P. English
Robert H. Singer
Michael Jackson
Ivan Topisirovic
Ze’ev A. Ronai
Inhibition of coronavirus HCoV-OC43 by targeting the eIF4F complex
Frontiers in Pharmacology
COVID-19
OC43
SARS-CoV-2
coronavirus
eIF4F
translation initiation complex
title Inhibition of coronavirus HCoV-OC43 by targeting the eIF4F complex
title_full Inhibition of coronavirus HCoV-OC43 by targeting the eIF4F complex
title_fullStr Inhibition of coronavirus HCoV-OC43 by targeting the eIF4F complex
title_full_unstemmed Inhibition of coronavirus HCoV-OC43 by targeting the eIF4F complex
title_short Inhibition of coronavirus HCoV-OC43 by targeting the eIF4F complex
title_sort inhibition of coronavirus hcov oc43 by targeting the eif4f complex
topic COVID-19
OC43
SARS-CoV-2
coronavirus
eIF4F
translation initiation complex
url https://www.frontiersin.org/articles/10.3389/fphar.2022.1029093/full
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