GC content shapes mRNA storage and decay in human cells
mRNA translation and decay appear often intimately linked although the rules of this interplay are poorly understood. In this study, we combined our recent P-body transcriptome with transcriptomes obtained following silencing of broadly acting mRNA decay and repression factors, and with available CL...
| Main Authors: | , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2019-12-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/49708 |
| _version_ | 1811180549231869952 |
|---|---|
| author | Maïté Courel Yves Clément Clémentine Bossevain Dominika Foretek Olivia Vidal Cruchez Zhou Yi Marianne Bénard Marie-Noëlle Benassy Michel Kress Caroline Vindry Michèle Ernoult-Lange Christophe Antoniewski Antonin Morillon Patrick Brest Arnaud Hubstenberger Hugues Roest Crollius Nancy Standart Dominique Weil |
| author_facet | Maïté Courel Yves Clément Clémentine Bossevain Dominika Foretek Olivia Vidal Cruchez Zhou Yi Marianne Bénard Marie-Noëlle Benassy Michel Kress Caroline Vindry Michèle Ernoult-Lange Christophe Antoniewski Antonin Morillon Patrick Brest Arnaud Hubstenberger Hugues Roest Crollius Nancy Standart Dominique Weil |
| author_sort | Maïté Courel |
| collection | DOAJ |
| description | mRNA translation and decay appear often intimately linked although the rules of this interplay are poorly understood. In this study, we combined our recent P-body transcriptome with transcriptomes obtained following silencing of broadly acting mRNA decay and repression factors, and with available CLIP and related data. This revealed the central role of GC content in mRNA fate, in terms of P-body localization, mRNA translation and mRNA stability: P-bodies contain mostly AU-rich mRNAs, which have a particular codon usage associated with a low protein yield; AU-rich and GC-rich transcripts tend to follow distinct decay pathways; and the targets of sequence-specific RBPs and miRNAs are also biased in terms of GC content. Altogether, these results suggest an integrated view of post-transcriptional control in human cells where most translation regulation is dedicated to inefficiently translated AU-rich mRNAs, whereas control at the level of 5’ decay applies to optimally translated GC-rich mRNAs. |
| first_indexed | 2024-04-11T09:05:08Z |
| format | Article |
| id | doaj.art-984956c05d1a4d48923e9135c8f90307 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:05:08Z |
| publishDate | 2019-12-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-984956c05d1a4d48923e9135c8f903072022-12-22T04:32:40ZengeLife Sciences Publications LtdeLife2050-084X2019-12-01810.7554/eLife.49708GC content shapes mRNA storage and decay in human cellsMaïté Courel0Yves Clément1https://orcid.org/0000-0002-5932-9412Clémentine Bossevain2Dominika Foretek3Olivia Vidal Cruchez4Zhou Yi5Marianne Bénard6Marie-Noëlle Benassy7Michel Kress8Caroline Vindry9Michèle Ernoult-Lange10Christophe Antoniewski11https://orcid.org/0000-0001-7709-2116Antonin Morillon12https://orcid.org/0000-0002-0575-5264Patrick Brest13Arnaud Hubstenberger14Hugues Roest Crollius15https://orcid.org/0000-0002-8209-173XNancy Standart16Dominique Weil17https://orcid.org/0000-0001-7630-1772Sorbonne Université, CNRS, Institut de Biologie Paris Seine (IBPS), Laboratoire de Biologie du Développement, Paris, FranceEcole Normale Supérieure, Institut de Biologie de l'ENS, IBENS, Paris, FranceSorbonne Université, CNRS, Institut de Biologie Paris Seine (IBPS), Laboratoire de Biologie du Développement, Paris, FrancencRNA, Epigenetic and Genome Fluidity, Institut Curie, PSL Research University, CNRS UMR 3244, Sorbonne Université, Paris, FranceUniversité Côte d'Azur, CNRS, INSERM, IRCAN, FHU-OncoAge, Nice, FranceUniversité Côte d'Azur, CNRS, INSERM, iBV, Nice, FranceSorbonne Université, CNRS, Institut de Biologie Paris Seine (IBPS), Laboratoire de Biologie du Développement, Paris, FranceSorbonne Université, CNRS, Institut de Biologie Paris Seine (IBPS), Laboratoire de Biologie du Développement, Paris, FranceSorbonne Université, CNRS, Institut de Biologie Paris Seine (IBPS), Laboratoire de Biologie du Développement, Paris, FranceDepartment of Biochemistry, University of Cambridge, Cambridge, United KingdomSorbonne Université, CNRS, Institut de Biologie Paris Seine (IBPS), Laboratoire de Biologie du Développement, Paris, FranceSorbonne Université, CNRS, Institut de Biologie Paris Seine (IBPS), ARTbio Bioinformatics Analysis Facility, Paris, FrancencRNA, Epigenetic and Genome Fluidity, Institut Curie, PSL Research University, CNRS UMR 3244, Sorbonne Université, Paris, FranceUniversité Côte d'Azur, CNRS, INSERM, IRCAN, FHU-OncoAge, Nice, FranceUniversité Côte d'Azur, CNRS, INSERM, iBV, Nice, FranceEcole Normale Supérieure, Institut de Biologie de l'ENS, IBENS, Paris, FranceDepartment of Biochemistry, University of Cambridge, Cambridge, United KingdomSorbonne Université, CNRS, Institut de Biologie Paris Seine (IBPS), Laboratoire de Biologie du Développement, Paris, FrancemRNA translation and decay appear often intimately linked although the rules of this interplay are poorly understood. In this study, we combined our recent P-body transcriptome with transcriptomes obtained following silencing of broadly acting mRNA decay and repression factors, and with available CLIP and related data. This revealed the central role of GC content in mRNA fate, in terms of P-body localization, mRNA translation and mRNA stability: P-bodies contain mostly AU-rich mRNAs, which have a particular codon usage associated with a low protein yield; AU-rich and GC-rich transcripts tend to follow distinct decay pathways; and the targets of sequence-specific RBPs and miRNAs are also biased in terms of GC content. Altogether, these results suggest an integrated view of post-transcriptional control in human cells where most translation regulation is dedicated to inefficiently translated AU-rich mRNAs, whereas control at the level of 5’ decay applies to optimally translated GC-rich mRNAs.https://elifesciences.org/articles/49708P-bodiespost-transcriptional regulationmRNA storagemRNA decaycodon usageGC content |
| spellingShingle | Maïté Courel Yves Clément Clémentine Bossevain Dominika Foretek Olivia Vidal Cruchez Zhou Yi Marianne Bénard Marie-Noëlle Benassy Michel Kress Caroline Vindry Michèle Ernoult-Lange Christophe Antoniewski Antonin Morillon Patrick Brest Arnaud Hubstenberger Hugues Roest Crollius Nancy Standart Dominique Weil GC content shapes mRNA storage and decay in human cells eLife P-bodies post-transcriptional regulation mRNA storage mRNA decay codon usage GC content |
| title | GC content shapes mRNA storage and decay in human cells |
| title_full | GC content shapes mRNA storage and decay in human cells |
| title_fullStr | GC content shapes mRNA storage and decay in human cells |
| title_full_unstemmed | GC content shapes mRNA storage and decay in human cells |
| title_short | GC content shapes mRNA storage and decay in human cells |
| title_sort | gc content shapes mrna storage and decay in human cells |
| topic | P-bodies post-transcriptional regulation mRNA storage mRNA decay codon usage GC content |
| url | https://elifesciences.org/articles/49708 |
| work_keys_str_mv | AT maitecourel gccontentshapesmrnastorageanddecayinhumancells AT yvesclement gccontentshapesmrnastorageanddecayinhumancells AT clementinebossevain gccontentshapesmrnastorageanddecayinhumancells AT dominikaforetek gccontentshapesmrnastorageanddecayinhumancells AT oliviavidalcruchez gccontentshapesmrnastorageanddecayinhumancells AT zhouyi gccontentshapesmrnastorageanddecayinhumancells AT mariannebenard gccontentshapesmrnastorageanddecayinhumancells AT marienoellebenassy gccontentshapesmrnastorageanddecayinhumancells AT michelkress gccontentshapesmrnastorageanddecayinhumancells AT carolinevindry gccontentshapesmrnastorageanddecayinhumancells AT micheleernoultlange gccontentshapesmrnastorageanddecayinhumancells AT christopheantoniewski gccontentshapesmrnastorageanddecayinhumancells AT antoninmorillon gccontentshapesmrnastorageanddecayinhumancells AT patrickbrest gccontentshapesmrnastorageanddecayinhumancells AT arnaudhubstenberger gccontentshapesmrnastorageanddecayinhumancells AT huguesroestcrollius gccontentshapesmrnastorageanddecayinhumancells AT nancystandart gccontentshapesmrnastorageanddecayinhumancells AT dominiqueweil gccontentshapesmrnastorageanddecayinhumancells |