Cargando…

The translational landscape of SARS-CoV-2 and infected cells

SARS-CoV-2 utilizes a number of strategies to modulate viral and host mRNA translation. Here, we used ribosome profiling in SARS-CoV-2 infected model cell lines and primary airway cells grown at the air-liquid interface to gain a deeper understanding of the translationally regulated events in respon...

Descripción completa

Detalles Bibliográficos
Autores principales: Puray-Chavez, Maritza, Lee, Nakyung, Tenneti, Kasyap, Wang, Yiqing, Vuong, Hung R., Liu, Yating, Horani, Amjad, Huang, Tao, Gunsten, Sean P., Case, James B., Yang, Wei, Diamond, Michael S., Brody, Steven L., Dougherty, Joseph, Kutluay, Sebla B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7654850/
https://www.ncbi.nlm.nih.gov/pubmed/33173862
http://dx.doi.org/10.1101/2020.11.03.367516
_version_ 1783608131207561216
author Puray-Chavez, Maritza
Lee, Nakyung
Tenneti, Kasyap
Wang, Yiqing
Vuong, Hung R.
Liu, Yating
Horani, Amjad
Huang, Tao
Gunsten, Sean P.
Case, James B.
Yang, Wei
Diamond, Michael S.
Brody, Steven L.
Dougherty, Joseph
Kutluay, Sebla B.
author_facet Puray-Chavez, Maritza
Lee, Nakyung
Tenneti, Kasyap
Wang, Yiqing
Vuong, Hung R.
Liu, Yating
Horani, Amjad
Huang, Tao
Gunsten, Sean P.
Case, James B.
Yang, Wei
Diamond, Michael S.
Brody, Steven L.
Dougherty, Joseph
Kutluay, Sebla B.
author_sort Puray-Chavez, Maritza
collection PubMed
description SARS-CoV-2 utilizes a number of strategies to modulate viral and host mRNA translation. Here, we used ribosome profiling in SARS-CoV-2 infected model cell lines and primary airway cells grown at the air-liquid interface to gain a deeper understanding of the translationally regulated events in response to virus replication. We find that SARS-CoV-2 mRNAs dominate the cellular mRNA pool but are not more efficiently translated than cellular mRNAs. SARS-CoV-2 utilized a highly efficient ribosomal frameshifting strategy in comparison to HIV-1, suggesting utilization of distinct structural elements. In the highly permissive cell models, although SARS-CoV-2 infection induced the transcriptional upregulation of numerous chemokines, cytokines and interferon stimulated genes, many of these mRNAs were not translated efficiently. Impact of SARS-CoV-2 on host mRNA translation was more subtle in primary cells, with marked transcriptional and translational upregulation of inflammatory and innate immune responses and downregulation of processes involved in ciliated cell function. Together, these data reveal the key role of mRNA translation in SARS-CoV-2 replication and highlight unique mechanisms for therapeutic development.
format Online
Article
Text
id pubmed-7654850
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-76548502020-11-11 The translational landscape of SARS-CoV-2 and infected cells Puray-Chavez, Maritza Lee, Nakyung Tenneti, Kasyap Wang, Yiqing Vuong, Hung R. Liu, Yating Horani, Amjad Huang, Tao Gunsten, Sean P. Case, James B. Yang, Wei Diamond, Michael S. Brody, Steven L. Dougherty, Joseph Kutluay, Sebla B. bioRxiv Article SARS-CoV-2 utilizes a number of strategies to modulate viral and host mRNA translation. Here, we used ribosome profiling in SARS-CoV-2 infected model cell lines and primary airway cells grown at the air-liquid interface to gain a deeper understanding of the translationally regulated events in response to virus replication. We find that SARS-CoV-2 mRNAs dominate the cellular mRNA pool but are not more efficiently translated than cellular mRNAs. SARS-CoV-2 utilized a highly efficient ribosomal frameshifting strategy in comparison to HIV-1, suggesting utilization of distinct structural elements. In the highly permissive cell models, although SARS-CoV-2 infection induced the transcriptional upregulation of numerous chemokines, cytokines and interferon stimulated genes, many of these mRNAs were not translated efficiently. Impact of SARS-CoV-2 on host mRNA translation was more subtle in primary cells, with marked transcriptional and translational upregulation of inflammatory and innate immune responses and downregulation of processes involved in ciliated cell function. Together, these data reveal the key role of mRNA translation in SARS-CoV-2 replication and highlight unique mechanisms for therapeutic development. Cold Spring Harbor Laboratory 2021-10-07 /pmc/articles/PMC7654850/ /pubmed/33173862 http://dx.doi.org/10.1101/2020.11.03.367516 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Puray-Chavez, Maritza
Lee, Nakyung
Tenneti, Kasyap
Wang, Yiqing
Vuong, Hung R.
Liu, Yating
Horani, Amjad
Huang, Tao
Gunsten, Sean P.
Case, James B.
Yang, Wei
Diamond, Michael S.
Brody, Steven L.
Dougherty, Joseph
Kutluay, Sebla B.
The translational landscape of SARS-CoV-2 and infected cells
title The translational landscape of SARS-CoV-2 and infected cells
title_full The translational landscape of SARS-CoV-2 and infected cells
title_fullStr The translational landscape of SARS-CoV-2 and infected cells
title_full_unstemmed The translational landscape of SARS-CoV-2 and infected cells
title_short The translational landscape of SARS-CoV-2 and infected cells
title_sort translational landscape of sars-cov-2 and infected cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7654850/
https://www.ncbi.nlm.nih.gov/pubmed/33173862
http://dx.doi.org/10.1101/2020.11.03.367516
work_keys_str_mv AT puraychavezmaritza thetranslationallandscapeofsarscov2andinfectedcells
AT leenakyung thetranslationallandscapeofsarscov2andinfectedcells
AT tennetikasyap thetranslationallandscapeofsarscov2andinfectedcells
AT wangyiqing thetranslationallandscapeofsarscov2andinfectedcells
AT vuonghungr thetranslationallandscapeofsarscov2andinfectedcells
AT liuyating thetranslationallandscapeofsarscov2andinfectedcells
AT horaniamjad thetranslationallandscapeofsarscov2andinfectedcells
AT huangtao thetranslationallandscapeofsarscov2andinfectedcells
AT gunstenseanp thetranslationallandscapeofsarscov2andinfectedcells
AT casejamesb thetranslationallandscapeofsarscov2andinfectedcells
AT yangwei thetranslationallandscapeofsarscov2andinfectedcells
AT diamondmichaels thetranslationallandscapeofsarscov2andinfectedcells
AT brodystevenl thetranslationallandscapeofsarscov2andinfectedcells
AT doughertyjoseph thetranslationallandscapeofsarscov2andinfectedcells
AT kutluayseblab thetranslationallandscapeofsarscov2andinfectedcells
AT puraychavezmaritza translationallandscapeofsarscov2andinfectedcells
AT leenakyung translationallandscapeofsarscov2andinfectedcells
AT tennetikasyap translationallandscapeofsarscov2andinfectedcells
AT wangyiqing translationallandscapeofsarscov2andinfectedcells
AT vuonghungr translationallandscapeofsarscov2andinfectedcells
AT liuyating translationallandscapeofsarscov2andinfectedcells
AT horaniamjad translationallandscapeofsarscov2andinfectedcells
AT huangtao translationallandscapeofsarscov2andinfectedcells
AT gunstenseanp translationallandscapeofsarscov2andinfectedcells
AT casejamesb translationallandscapeofsarscov2andinfectedcells
AT yangwei translationallandscapeofsarscov2andinfectedcells
AT diamondmichaels translationallandscapeofsarscov2andinfectedcells
AT brodystevenl translationallandscapeofsarscov2andinfectedcells
AT doughertyjoseph translationallandscapeofsarscov2andinfectedcells
AT kutluayseblab translationallandscapeofsarscov2andinfectedcells