sRNA-mediated activation of gene expression by inhibition of 5'-3’ exonucleolytic mRNA degradation
Abstract
Post-transcriptional control by small regulatory RNA (sRNA) is critical for rapid adaptive processes. sRNAs can directly modulate mRNA degradation in Proteobacteria without interfering with translation. However, Firmicutes have a fundamentally different set of ribonucleases for mRNA degradation and whether sRNAs can regulate the activity of these enzymes is an open question. We show that Bacillus subtilis RoxS, a major trans-acting sRNA shared with Staphylococus aureus, prevents degradation of the yflS mRNA, encoding a malate transporter. In the presence of malate, RoxS transiently escapes from repression by the NADH-sensitive transcription factor Rex and binds to the extreme 5’-end of yflS mRNA. This impairs the 5’-3’ exoribonuclease activity of RNase J1, increasing the half-life of the primary transcript and concomitantly enhances ribosome binding to increase expression of the transporter. Globally, the different targets regulated by RoxS suggest that it helps readjust the cellular NAD+/NADH balance when perturbed by different stimuli.
Article and author information
Author details
Funding
Université Paris Diderot (UMR8261)
- Ciarán Condon
Agence Nationale de la Recherche (ANR-10-LABX-0036 NETRNA)
- Pascale Romby
Agence Nationale de la Recherche (ANR-16-CE12-0002-01 BaRR)
- Sylvain Durand
Agence Nationale de la Recherche (ANR-12-BSV6-0007 asSUPYCO)
- Ciarán Condon
Centre National de la Recherche Scientifique (UMR8261,UPR9002)
- Sylvain Durand
- Frédérique Braun
- Anne-Catherine Helfer
- Pascale Romby
- Ciarán Condon
Université de Strasbourg (UPR9002)
- Pascale Romby
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Jörg Vogel, University of Würzburg, Germany
Version history
- Received: November 23, 2016
- Accepted: April 23, 2017
- Accepted Manuscript published: April 24, 2017 (version 1)
- Version of Record published: May 5, 2017 (version 2)
Copyright
© 2017, Durand et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 2,397
- Page views
-
- 474
- Downloads
-
- 34
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Chromosomes and Gene Expression
- Structural Biology and Molecular Biophysics
Eukaryotic gene expression is linked to chromatin structure and nucleosome positioning by ATP-dependent chromatin remodelers that establish and maintain nucleosome-depleted regions (NDRs) near transcription start sites. Conserved yeast RSC and ISW2 remodelers exert antagonistic effects on nucleosomes flanking NDRs, but the temporal dynamics of remodeler search, engagement, and directional nucleosome mobilization for promoter accessibility are unknown. Using optical tweezers and two-color single-particle imaging, we investigated the Brownian diffusion of RSC and ISW2 on free DNA and sparse nucleosome arrays. RSC and ISW2 rapidly scan DNA by one-dimensional hopping and sliding, respectively, with dynamic collisions between remodelers followed by recoil or apparent co-diffusion. Static nucleosomes block remodeler diffusion resulting in remodeler recoil or sequestration. Remarkably, both RSC and ISW2 use ATP hydrolysis to translocate mono-nucleosomes processively at ~30 bp/s on extended linear DNA under tension. Processivity and opposing push–pull directionalities of nucleosome translocation shown by RSC and ISW2 shape the distinctive landscape of promoter chromatin.
-
- Chromosomes and Gene Expression
- Structural Biology and Molecular Biophysics
To find nucleosomes, chromatin remodelers slide and hop along DNA, and their direction of approach affects the direction that nucleosomes slide in.