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Nuclear mRNPs are compact particles packaged with a network of proteins promoting RNA–RNA interactions

Messenger RNAs (mRNAs) are at the center of the central dogma of molecular biology. In eukaryotic cells, these long ribonucleic acid polymers do not exist as naked transcripts; rather, they associate with mRNA-binding proteins to form messenger ribonucleoprotein (mRNP) complexes. Recently, global pr...

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Autores principales: Bonneau, Fabien, Basquin, Jérôme, Steigenberger, Barbara, Schäfer, Tillman, Schäfer, Ingmar B., Conti, Elena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10393194/
https://www.ncbi.nlm.nih.gov/pubmed/37399331
http://dx.doi.org/10.1101/gad.350630.123
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author Bonneau, Fabien
Basquin, Jérôme
Steigenberger, Barbara
Schäfer, Tillman
Schäfer, Ingmar B.
Conti, Elena
author_facet Bonneau, Fabien
Basquin, Jérôme
Steigenberger, Barbara
Schäfer, Tillman
Schäfer, Ingmar B.
Conti, Elena
author_sort Bonneau, Fabien
collection PubMed
description Messenger RNAs (mRNAs) are at the center of the central dogma of molecular biology. In eukaryotic cells, these long ribonucleic acid polymers do not exist as naked transcripts; rather, they associate with mRNA-binding proteins to form messenger ribonucleoprotein (mRNP) complexes. Recently, global proteomic and transcriptomic studies have provided comprehensive inventories of mRNP components. However, knowledge of the molecular features of distinct mRNP populations has remained elusive. We purified endogenous nuclear mRNPs from Saccharomyces cerevisiae by harnessing the mRNP biogenesis factors THO and Sub2 in biochemical procedures optimized to preserve the integrity of these transient ribonucleoprotein assemblies. We found that these mRNPs are compact particles that contain multiple copies of Yra1, an essential protein with RNA-annealing properties. To investigate their molecular and architectural organization, we used a combination of proteomics, RNA sequencing, cryo-electron microscopy, cross-linking mass spectrometry, structural models, and biochemical assays. Our findings indicate that yeast nuclear mRNPs are packaged around an intricate network of interconnected proteins capable of promoting RNA–RNA interactions via their positively charged intrinsically disordered regions. The evolutionary conservation of the major mRNA-packaging factor (yeast Yra1 and Aly/REF in metazoans) points toward a general paradigm governing nuclear mRNP packaging.
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spelling pubmed-103931942023-08-02 Nuclear mRNPs are compact particles packaged with a network of proteins promoting RNA–RNA interactions Bonneau, Fabien Basquin, Jérôme Steigenberger, Barbara Schäfer, Tillman Schäfer, Ingmar B. Conti, Elena Genes Dev Research Papers Messenger RNAs (mRNAs) are at the center of the central dogma of molecular biology. In eukaryotic cells, these long ribonucleic acid polymers do not exist as naked transcripts; rather, they associate with mRNA-binding proteins to form messenger ribonucleoprotein (mRNP) complexes. Recently, global proteomic and transcriptomic studies have provided comprehensive inventories of mRNP components. However, knowledge of the molecular features of distinct mRNP populations has remained elusive. We purified endogenous nuclear mRNPs from Saccharomyces cerevisiae by harnessing the mRNP biogenesis factors THO and Sub2 in biochemical procedures optimized to preserve the integrity of these transient ribonucleoprotein assemblies. We found that these mRNPs are compact particles that contain multiple copies of Yra1, an essential protein with RNA-annealing properties. To investigate their molecular and architectural organization, we used a combination of proteomics, RNA sequencing, cryo-electron microscopy, cross-linking mass spectrometry, structural models, and biochemical assays. Our findings indicate that yeast nuclear mRNPs are packaged around an intricate network of interconnected proteins capable of promoting RNA–RNA interactions via their positively charged intrinsically disordered regions. The evolutionary conservation of the major mRNA-packaging factor (yeast Yra1 and Aly/REF in metazoans) points toward a general paradigm governing nuclear mRNP packaging. Cold Spring Harbor Laboratory Press 2023-06-01 /pmc/articles/PMC10393194/ /pubmed/37399331 http://dx.doi.org/10.1101/gad.350630.123 Text en © 2023 Bonneau et al.; Published by Cold Spring Harbor Laboratory Press https://creativecommons.org/licenses/by/4.0/This article, published in Genes & Development, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Papers
Bonneau, Fabien
Basquin, Jérôme
Steigenberger, Barbara
Schäfer, Tillman
Schäfer, Ingmar B.
Conti, Elena
Nuclear mRNPs are compact particles packaged with a network of proteins promoting RNA–RNA interactions
title Nuclear mRNPs are compact particles packaged with a network of proteins promoting RNA–RNA interactions
title_full Nuclear mRNPs are compact particles packaged with a network of proteins promoting RNA–RNA interactions
title_fullStr Nuclear mRNPs are compact particles packaged with a network of proteins promoting RNA–RNA interactions
title_full_unstemmed Nuclear mRNPs are compact particles packaged with a network of proteins promoting RNA–RNA interactions
title_short Nuclear mRNPs are compact particles packaged with a network of proteins promoting RNA–RNA interactions
title_sort nuclear mrnps are compact particles packaged with a network of proteins promoting rna–rna interactions
topic Research Papers
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10393194/
https://www.ncbi.nlm.nih.gov/pubmed/37399331
http://dx.doi.org/10.1101/gad.350630.123
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