Uridylation prevents 3′ trimming of oligoadenylated mRNAs

Degradation of mRNAs is usually initiated by deadenylation, the shortening of long poly(A) tails to oligo(A) tails of 12–15 As. Deadenylation leads to decapping and to subsequent 5′ to 3′ degradation by XRN proteins, or alternatively 3′ to 5′ degradation by the exosome. Decapping can also be induced...

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Main Authors: Sement, François Michaël, Ferrier, Emilie, Zuber, Hélène, Merret, Rémy, Alioua, Malek, Deragon, Jean-Marc, Bousquet-Antonelli, Cécile, Lange, Heike, Gagliardi, Dominique
Format: Online
Language:English
Published: Oxford University Press 2013
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3737552/
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spelling pubmed-37375522013-08-08 Uridylation prevents 3′ trimming of oligoadenylated mRNAs Sement, François Michaël Ferrier, Emilie Zuber, Hélène Merret, Rémy Alioua, Malek Deragon, Jean-Marc Bousquet-Antonelli, Cécile Lange, Heike Gagliardi, Dominique RNA Degradation of mRNAs is usually initiated by deadenylation, the shortening of long poly(A) tails to oligo(A) tails of 12–15 As. Deadenylation leads to decapping and to subsequent 5′ to 3′ degradation by XRN proteins, or alternatively 3′ to 5′ degradation by the exosome. Decapping can also be induced by uridylation as shown for the non-polyadenylated histone mRNAs in humans and for several mRNAs in Schizosaccharomyces pombe and Aspergillus nidulans. Here we report a novel role for uridylation in preventing 3′ trimming of oligoadenylated mRNAs in Arabidopsis. We show that oligo(A)-tailed mRNAs are uridylated by the cytosolic UTP:RNA uridylyltransferase URT1 and that URT1 has no major impact on mRNA degradation rates. However, in absence of uridylation, oligo(A) tails are trimmed, indicating that uridylation protects oligoadenylated mRNAs from 3′ ribonucleolytic attacks. This conclusion is further supported by an increase in 3′ truncated transcripts detected in urt1 mutants. We propose that preventing 3′ trimming of oligo(A)-tailed mRNAs by uridylation participates in establishing the 5′ to 3′ directionality of mRNA degradation. Importantly, uridylation prevents 3′ shortening of mRNAs associated with polysomes, suggesting that a key biological function of uridylation is to confer 5′ to 3′ polarity in case of co-translational mRNA decay. Oxford University Press 2013-08 2013-06-06 /pmc/articles/PMC3737552/ /pubmed/23748567 http://dx.doi.org/10.1093/nar/gkt465 Text en © The Author(s) 2013. Published by Oxford University Press. http://creativecommons.org/licenses/by-nc/3.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Sement, François Michaël
Ferrier, Emilie
Zuber, Hélène
Merret, Rémy
Alioua, Malek
Deragon, Jean-Marc
Bousquet-Antonelli, Cécile
Lange, Heike
Gagliardi, Dominique
spellingShingle Sement, François Michaël
Ferrier, Emilie
Zuber, Hélène
Merret, Rémy
Alioua, Malek
Deragon, Jean-Marc
Bousquet-Antonelli, Cécile
Lange, Heike
Gagliardi, Dominique
Uridylation prevents 3′ trimming of oligoadenylated mRNAs
author_facet Sement, François Michaël
Ferrier, Emilie
Zuber, Hélène
Merret, Rémy
Alioua, Malek
Deragon, Jean-Marc
Bousquet-Antonelli, Cécile
Lange, Heike
Gagliardi, Dominique
author_sort Sement, François Michaël
title Uridylation prevents 3′ trimming of oligoadenylated mRNAs
title_short Uridylation prevents 3′ trimming of oligoadenylated mRNAs
title_full Uridylation prevents 3′ trimming of oligoadenylated mRNAs
title_fullStr Uridylation prevents 3′ trimming of oligoadenylated mRNAs
title_full_unstemmed Uridylation prevents 3′ trimming of oligoadenylated mRNAs
title_sort uridylation prevents 3′ trimming of oligoadenylated mrnas
description Degradation of mRNAs is usually initiated by deadenylation, the shortening of long poly(A) tails to oligo(A) tails of 12–15 As. Deadenylation leads to decapping and to subsequent 5′ to 3′ degradation by XRN proteins, or alternatively 3′ to 5′ degradation by the exosome. Decapping can also be induced by uridylation as shown for the non-polyadenylated histone mRNAs in humans and for several mRNAs in Schizosaccharomyces pombe and Aspergillus nidulans. Here we report a novel role for uridylation in preventing 3′ trimming of oligoadenylated mRNAs in Arabidopsis. We show that oligo(A)-tailed mRNAs are uridylated by the cytosolic UTP:RNA uridylyltransferase URT1 and that URT1 has no major impact on mRNA degradation rates. However, in absence of uridylation, oligo(A) tails are trimmed, indicating that uridylation protects oligoadenylated mRNAs from 3′ ribonucleolytic attacks. This conclusion is further supported by an increase in 3′ truncated transcripts detected in urt1 mutants. We propose that preventing 3′ trimming of oligo(A)-tailed mRNAs by uridylation participates in establishing the 5′ to 3′ directionality of mRNA degradation. Importantly, uridylation prevents 3′ shortening of mRNAs associated with polysomes, suggesting that a key biological function of uridylation is to confer 5′ to 3′ polarity in case of co-translational mRNA decay.
publisher Oxford University Press
publishDate 2013
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3737552/
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