RNA 3′end tailing safeguards cells against products of pervasive transcription termination

Abstract Premature transcription termination yields a wealth of unadenylated (pA−) RNA. Although this can be targeted for degradation by the Nuclear EXosome Targeting (NEXT) complex, possible backup pathways remain poorly understood. Here, we find increased levels of 3′ end uridylated and adenylated...

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Main Authors: Guifen Wu, Jérôme O. Rouvière, Manfred Schmid, Torben Heick Jensen
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54834-6
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author Guifen Wu
Jérôme O. Rouvière
Manfred Schmid
Torben Heick Jensen
author_facet Guifen Wu
Jérôme O. Rouvière
Manfred Schmid
Torben Heick Jensen
author_sort Guifen Wu
collection DOAJ
description Abstract Premature transcription termination yields a wealth of unadenylated (pA−) RNA. Although this can be targeted for degradation by the Nuclear EXosome Targeting (NEXT) complex, possible backup pathways remain poorly understood. Here, we find increased levels of 3′ end uridylated and adenylated RNAs upon NEXT inactivation. U-tailed RNAs are mostly short and modified by the cytoplasmic tailing enzymes, TUT4/7, following their PHAX-dependent nuclear export and prior to their degradation by the cytoplasmic exosome or the exoribonuclease DIS3L2. Longer RNAs are instead adenylated redundantly by enzymes TENT2, PAPOLA and PAPOLG. These transcripts are either degraded via the nuclear Poly(A) tail eXosome Targeting (PAXT) connection or exported and removed by the cytoplasmic exosome in a translation-dependent manner. Failure to do so decreases global translation and induces cell death. We conclude that post-transcriptional 3′ end modification and removal of excess pA− RNA is achieved by tailing enzymes and export factors shared with productive RNA pathways.
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spelling doaj-art-e99415ed4c0741c4b7b9e0390f6ee14b2025-08-20T02:49:17ZengNature PortfolioNature Communications2041-17232024-12-0115111410.1038/s41467-024-54834-6RNA 3′end tailing safeguards cells against products of pervasive transcription terminationGuifen Wu0Jérôme O. Rouvière1Manfred Schmid2Torben Heick Jensen3Department of Molecular Biology and Genetics, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityDepartment of Molecular Biology and Genetics, Aarhus UniversityAbstract Premature transcription termination yields a wealth of unadenylated (pA−) RNA. Although this can be targeted for degradation by the Nuclear EXosome Targeting (NEXT) complex, possible backup pathways remain poorly understood. Here, we find increased levels of 3′ end uridylated and adenylated RNAs upon NEXT inactivation. U-tailed RNAs are mostly short and modified by the cytoplasmic tailing enzymes, TUT4/7, following their PHAX-dependent nuclear export and prior to their degradation by the cytoplasmic exosome or the exoribonuclease DIS3L2. Longer RNAs are instead adenylated redundantly by enzymes TENT2, PAPOLA and PAPOLG. These transcripts are either degraded via the nuclear Poly(A) tail eXosome Targeting (PAXT) connection or exported and removed by the cytoplasmic exosome in a translation-dependent manner. Failure to do so decreases global translation and induces cell death. We conclude that post-transcriptional 3′ end modification and removal of excess pA− RNA is achieved by tailing enzymes and export factors shared with productive RNA pathways.https://doi.org/10.1038/s41467-024-54834-6
spellingShingle Guifen Wu
Jérôme O. Rouvière
Manfred Schmid
Torben Heick Jensen
RNA 3′end tailing safeguards cells against products of pervasive transcription termination
Nature Communications
title RNA 3′end tailing safeguards cells against products of pervasive transcription termination
title_full RNA 3′end tailing safeguards cells against products of pervasive transcription termination
title_fullStr RNA 3′end tailing safeguards cells against products of pervasive transcription termination
title_full_unstemmed RNA 3′end tailing safeguards cells against products of pervasive transcription termination
title_short RNA 3′end tailing safeguards cells against products of pervasive transcription termination
title_sort rna 3 end tailing safeguards cells against products of pervasive transcription termination
url https://doi.org/10.1038/s41467-024-54834-6
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