Extensive 5′-surveillance guards against non-canonical NAD-caps of nuclear mRNAs in yeast

The ubiquitous redox coenzyme nicotinamide adenine dinucleotide (NAD) acts as a non-canonical cap structure on prokaryotic and eukaryotic ribonucleic acids. Here we find that in budding yeast, NAD-RNAs are abundant (>1400 species), short (<170 nt), and mostly correspond to mRNA 5′-ends. The mo...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhang, Yaqing, Kuster, David, Schmidt, Tobias, Kirrmaier, Daniel, Nübel, Gabriele, Ibberson, David, Benes, Vladimir, Hombauer, Hans, Knop, Michael, Jäschke, Andres
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7606564/
https://www.ncbi.nlm.nih.gov/pubmed/33139726
http://dx.doi.org/10.1038/s41467-020-19326-3
_version_ 1783604501657157632
author Zhang, Yaqing
Kuster, David
Schmidt, Tobias
Kirrmaier, Daniel
Nübel, Gabriele
Ibberson, David
Benes, Vladimir
Hombauer, Hans
Knop, Michael
Jäschke, Andres
author_facet Zhang, Yaqing
Kuster, David
Schmidt, Tobias
Kirrmaier, Daniel
Nübel, Gabriele
Ibberson, David
Benes, Vladimir
Hombauer, Hans
Knop, Michael
Jäschke, Andres
author_sort Zhang, Yaqing
collection PubMed
description The ubiquitous redox coenzyme nicotinamide adenine dinucleotide (NAD) acts as a non-canonical cap structure on prokaryotic and eukaryotic ribonucleic acids. Here we find that in budding yeast, NAD-RNAs are abundant (>1400 species), short (<170 nt), and mostly correspond to mRNA 5′-ends. The modification percentage of transcripts is low (<5%). NAD incorporation occurs mainly during transcription initiation by RNA polymerase II, which uses distinct promoters with a YAAG core motif for this purpose. Most NAD-RNAs are 3′-truncated. At least three decapping enzymes, Rai1, Dxo1, and Npy1, guard against NAD-RNA at different cellular locations, targeting overlapping transcript populations. NAD-mRNAs are not translatable in vitro. Our work indicates that in budding yeast, most of the NAD incorporation into RNA seems to be disadvantageous to the cell, which has evolved a diverse surveillance machinery to prematurely terminate, decap and reject NAD-RNAs.
format Online
Article
Text
id pubmed-7606564
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-76065642020-11-10 Extensive 5′-surveillance guards against non-canonical NAD-caps of nuclear mRNAs in yeast Zhang, Yaqing Kuster, David Schmidt, Tobias Kirrmaier, Daniel Nübel, Gabriele Ibberson, David Benes, Vladimir Hombauer, Hans Knop, Michael Jäschke, Andres Nat Commun Article The ubiquitous redox coenzyme nicotinamide adenine dinucleotide (NAD) acts as a non-canonical cap structure on prokaryotic and eukaryotic ribonucleic acids. Here we find that in budding yeast, NAD-RNAs are abundant (>1400 species), short (<170 nt), and mostly correspond to mRNA 5′-ends. The modification percentage of transcripts is low (<5%). NAD incorporation occurs mainly during transcription initiation by RNA polymerase II, which uses distinct promoters with a YAAG core motif for this purpose. Most NAD-RNAs are 3′-truncated. At least three decapping enzymes, Rai1, Dxo1, and Npy1, guard against NAD-RNA at different cellular locations, targeting overlapping transcript populations. NAD-mRNAs are not translatable in vitro. Our work indicates that in budding yeast, most of the NAD incorporation into RNA seems to be disadvantageous to the cell, which has evolved a diverse surveillance machinery to prematurely terminate, decap and reject NAD-RNAs. Nature Publishing Group UK 2020-11-02 /pmc/articles/PMC7606564/ /pubmed/33139726 http://dx.doi.org/10.1038/s41467-020-19326-3 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Zhang, Yaqing
Kuster, David
Schmidt, Tobias
Kirrmaier, Daniel
Nübel, Gabriele
Ibberson, David
Benes, Vladimir
Hombauer, Hans
Knop, Michael
Jäschke, Andres
Extensive 5′-surveillance guards against non-canonical NAD-caps of nuclear mRNAs in yeast
title Extensive 5′-surveillance guards against non-canonical NAD-caps of nuclear mRNAs in yeast
title_full Extensive 5′-surveillance guards against non-canonical NAD-caps of nuclear mRNAs in yeast
title_fullStr Extensive 5′-surveillance guards against non-canonical NAD-caps of nuclear mRNAs in yeast
title_full_unstemmed Extensive 5′-surveillance guards against non-canonical NAD-caps of nuclear mRNAs in yeast
title_short Extensive 5′-surveillance guards against non-canonical NAD-caps of nuclear mRNAs in yeast
title_sort extensive 5′-surveillance guards against non-canonical nad-caps of nuclear mrnas in yeast
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7606564/
https://www.ncbi.nlm.nih.gov/pubmed/33139726
http://dx.doi.org/10.1038/s41467-020-19326-3
work_keys_str_mv AT zhangyaqing extensive5surveillanceguardsagainstnoncanonicalnadcapsofnuclearmrnasinyeast
AT kusterdavid extensive5surveillanceguardsagainstnoncanonicalnadcapsofnuclearmrnasinyeast
AT schmidttobias extensive5surveillanceguardsagainstnoncanonicalnadcapsofnuclearmrnasinyeast
AT kirrmaierdaniel extensive5surveillanceguardsagainstnoncanonicalnadcapsofnuclearmrnasinyeast
AT nubelgabriele extensive5surveillanceguardsagainstnoncanonicalnadcapsofnuclearmrnasinyeast
AT ibbersondavid extensive5surveillanceguardsagainstnoncanonicalnadcapsofnuclearmrnasinyeast
AT benesvladimir extensive5surveillanceguardsagainstnoncanonicalnadcapsofnuclearmrnasinyeast
AT hombauerhans extensive5surveillanceguardsagainstnoncanonicalnadcapsofnuclearmrnasinyeast
AT knopmichael extensive5surveillanceguardsagainstnoncanonicalnadcapsofnuclearmrnasinyeast
AT jaschkeandres extensive5surveillanceguardsagainstnoncanonicalnadcapsofnuclearmrnasinyeast