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Splicing-Mediated Autoregulation Modulates Rpl22p Expression in Saccharomyces cerevisiae

In Saccharomyces cerevisiae, splicing is critical for expression of ribosomal protein genes (RPGs), which are among the most highly expressed genes and are tightly regulated according to growth and environmental conditions. However, knowledge of the precise mechanisms by which RPG pre-mRNA splicing...

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Autores principales: Gabunilas, Jason, Chanfreau, Guillaume
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4838235/
https://www.ncbi.nlm.nih.gov/pubmed/27097027
http://dx.doi.org/10.1371/journal.pgen.1005999
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author Gabunilas, Jason
Chanfreau, Guillaume
author_facet Gabunilas, Jason
Chanfreau, Guillaume
author_sort Gabunilas, Jason
collection PubMed
description In Saccharomyces cerevisiae, splicing is critical for expression of ribosomal protein genes (RPGs), which are among the most highly expressed genes and are tightly regulated according to growth and environmental conditions. However, knowledge of the precise mechanisms by which RPG pre-mRNA splicing is regulated on a gene-by-gene basis is lacking. Here we show that Rpl22p has an extraribosomal role in the inhibition of splicing of the RPL22B pre-mRNA transcript. A stem loop secondary structure within the intron is necessary for pre-mRNA binding by Rpl22p in vivo and splicing inhibition in vivo and in vitro and can rescue splicing inhibition in vitro when added in trans to splicing reactions. Splicing inhibition by Rpl22p may be partly attributed to the reduction of co-transcriptional U1 snRNP recruitment to the pre-mRNA at the RPL22B locus. We further demonstrate that the inhibition of RPL22B pre-mRNA splicing contributes to the down-regulation of mature transcript during specific stress conditions, and provide evidence hinting at a regulatory role for this mechanism in conditions of suppressed ribosome biogenesis. These results demonstrate an autoregulatory mechanism that fine-tunes the expression of the Rpl22 protein and by extension Rpl22p paralog composition according to the cellular demands for ribosome biogenesis.
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spelling pubmed-48382352016-04-29 Splicing-Mediated Autoregulation Modulates Rpl22p Expression in Saccharomyces cerevisiae Gabunilas, Jason Chanfreau, Guillaume PLoS Genet Research Article In Saccharomyces cerevisiae, splicing is critical for expression of ribosomal protein genes (RPGs), which are among the most highly expressed genes and are tightly regulated according to growth and environmental conditions. However, knowledge of the precise mechanisms by which RPG pre-mRNA splicing is regulated on a gene-by-gene basis is lacking. Here we show that Rpl22p has an extraribosomal role in the inhibition of splicing of the RPL22B pre-mRNA transcript. A stem loop secondary structure within the intron is necessary for pre-mRNA binding by Rpl22p in vivo and splicing inhibition in vivo and in vitro and can rescue splicing inhibition in vitro when added in trans to splicing reactions. Splicing inhibition by Rpl22p may be partly attributed to the reduction of co-transcriptional U1 snRNP recruitment to the pre-mRNA at the RPL22B locus. We further demonstrate that the inhibition of RPL22B pre-mRNA splicing contributes to the down-regulation of mature transcript during specific stress conditions, and provide evidence hinting at a regulatory role for this mechanism in conditions of suppressed ribosome biogenesis. These results demonstrate an autoregulatory mechanism that fine-tunes the expression of the Rpl22 protein and by extension Rpl22p paralog composition according to the cellular demands for ribosome biogenesis. Public Library of Science 2016-04-20 /pmc/articles/PMC4838235/ /pubmed/27097027 http://dx.doi.org/10.1371/journal.pgen.1005999 Text en © 2016 Gabunilas, Chanfreau http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Gabunilas, Jason
Chanfreau, Guillaume
Splicing-Mediated Autoregulation Modulates Rpl22p Expression in Saccharomyces cerevisiae
title Splicing-Mediated Autoregulation Modulates Rpl22p Expression in Saccharomyces cerevisiae
title_full Splicing-Mediated Autoregulation Modulates Rpl22p Expression in Saccharomyces cerevisiae
title_fullStr Splicing-Mediated Autoregulation Modulates Rpl22p Expression in Saccharomyces cerevisiae
title_full_unstemmed Splicing-Mediated Autoregulation Modulates Rpl22p Expression in Saccharomyces cerevisiae
title_short Splicing-Mediated Autoregulation Modulates Rpl22p Expression in Saccharomyces cerevisiae
title_sort splicing-mediated autoregulation modulates rpl22p expression in saccharomyces cerevisiae
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4838235/
https://www.ncbi.nlm.nih.gov/pubmed/27097027
http://dx.doi.org/10.1371/journal.pgen.1005999
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