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Coupled protein quality control during nonsense-mediated mRNA decay

Translation of mRNAs containing premature termination codons (PTCs) results in truncated protein products with deleterious effects. Nonsense-mediated decay (NMD) is a surveillance pathway responsible for detecting PTC containing transcripts. Although the molecular mechanisms governing mRNA degradati...

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Autores principales: Inglis, Alison J., Guna, Alina, Gálvez-Merchán, Ángel, Pal, Akshaye, Esantsi, Theodore K., Keys, Heather R., Frenkel, Evgeni M., Oania, Robert, Weissman, Jonathan S., Voorhees, Rebecca M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10234110/
https://www.ncbi.nlm.nih.gov/pubmed/37218462
http://dx.doi.org/10.1242/jcs.261216
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author Inglis, Alison J.
Guna, Alina
Gálvez-Merchán, Ángel
Pal, Akshaye
Esantsi, Theodore K.
Keys, Heather R.
Frenkel, Evgeni M.
Oania, Robert
Weissman, Jonathan S.
Voorhees, Rebecca M.
author_facet Inglis, Alison J.
Guna, Alina
Gálvez-Merchán, Ángel
Pal, Akshaye
Esantsi, Theodore K.
Keys, Heather R.
Frenkel, Evgeni M.
Oania, Robert
Weissman, Jonathan S.
Voorhees, Rebecca M.
author_sort Inglis, Alison J.
collection PubMed
description Translation of mRNAs containing premature termination codons (PTCs) results in truncated protein products with deleterious effects. Nonsense-mediated decay (NMD) is a surveillance pathway responsible for detecting PTC containing transcripts. Although the molecular mechanisms governing mRNA degradation have been extensively studied, the fate of the nascent protein product remains largely uncharacterized. Here, we use a fluorescent reporter system in mammalian cells to reveal a selective degradation pathway specifically targeting the protein product of an NMD mRNA. We show that this process is post-translational and dependent on the ubiquitin proteasome system. To systematically uncover factors involved in NMD-linked protein quality control, we conducted genome-wide flow cytometry-based screens. Our screens recovered known NMD factors but suggested that protein degradation did not depend on the canonical ribosome-quality control (RQC) pathway. A subsequent arrayed screen demonstrated that protein and mRNA branches of NMD rely on a shared recognition event. Our results establish the existence of a targeted pathway for nascent protein degradation from PTC containing mRNAs, and provide a reference for the field to identify and characterize required factors.
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spelling pubmed-102341102023-06-02 Coupled protein quality control during nonsense-mediated mRNA decay Inglis, Alison J. Guna, Alina Gálvez-Merchán, Ángel Pal, Akshaye Esantsi, Theodore K. Keys, Heather R. Frenkel, Evgeni M. Oania, Robert Weissman, Jonathan S. Voorhees, Rebecca M. J Cell Sci Research Article Translation of mRNAs containing premature termination codons (PTCs) results in truncated protein products with deleterious effects. Nonsense-mediated decay (NMD) is a surveillance pathway responsible for detecting PTC containing transcripts. Although the molecular mechanisms governing mRNA degradation have been extensively studied, the fate of the nascent protein product remains largely uncharacterized. Here, we use a fluorescent reporter system in mammalian cells to reveal a selective degradation pathway specifically targeting the protein product of an NMD mRNA. We show that this process is post-translational and dependent on the ubiquitin proteasome system. To systematically uncover factors involved in NMD-linked protein quality control, we conducted genome-wide flow cytometry-based screens. Our screens recovered known NMD factors but suggested that protein degradation did not depend on the canonical ribosome-quality control (RQC) pathway. A subsequent arrayed screen demonstrated that protein and mRNA branches of NMD rely on a shared recognition event. Our results establish the existence of a targeted pathway for nascent protein degradation from PTC containing mRNAs, and provide a reference for the field to identify and characterize required factors. The Company of Biologists Ltd 2023-05-23 /pmc/articles/PMC10234110/ /pubmed/37218462 http://dx.doi.org/10.1242/jcs.261216 Text en © 2023. Published by The Company of Biologists Ltd https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Inglis, Alison J.
Guna, Alina
Gálvez-Merchán, Ángel
Pal, Akshaye
Esantsi, Theodore K.
Keys, Heather R.
Frenkel, Evgeni M.
Oania, Robert
Weissman, Jonathan S.
Voorhees, Rebecca M.
Coupled protein quality control during nonsense-mediated mRNA decay
title Coupled protein quality control during nonsense-mediated mRNA decay
title_full Coupled protein quality control during nonsense-mediated mRNA decay
title_fullStr Coupled protein quality control during nonsense-mediated mRNA decay
title_full_unstemmed Coupled protein quality control during nonsense-mediated mRNA decay
title_short Coupled protein quality control during nonsense-mediated mRNA decay
title_sort coupled protein quality control during nonsense-mediated mrna decay
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10234110/
https://www.ncbi.nlm.nih.gov/pubmed/37218462
http://dx.doi.org/10.1242/jcs.261216
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