<i>Trans</i>-acting antisense RNAs mediate transcriptional gene cosuppression in <i>S. cerevisiae</i>

Camblong, Jurgi; Beyrouthy, Nissrine; Guffanti, Elisa; Schlaepfer, Guillaume; Steinmetz, Lars M.; Stutz, Françoise

doi:10.1101/gad.522509

Cited by 143 publications

(152 citation statements)

References 46 publications

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“…Accumulation of these ncRNAs, called XUTs, in the absence of 5′-3′ exoribonuclease activity could explain the down-regulation of the expression of specific genes. This model also relies on previously published work in which it was demonstrated that the expression of the PHO84 and TY1 genes can be down-regulated by the accumulation of antisense transcripts that are substrates of the exoribonucleases Rrp6 and Xrn1, respectively (28)(29)(30). We therefore checked to see whether any of the genes corresponding to the down-regulated proteins in our 2D gel analysis also contained potential XUTs (16), but did not find any.…”

Section: Table 1 Dcs Family Proteins and Activation Of Exoribonucleamentioning

confidence: 83%

Activation of 5′-3′ exoribonuclease Xrn1 by cofactor Dcs1 is essential for mitochondrial function in yeast

Sinturel

Bréchemier-Baey

Kiledjian

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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The scavenger decapping enzyme Dcs1 has been shown to facilitate the activity of the cytoplasmic 5′-3′ exoribonuclease Xrn1 in eukaryotes. Dcs1 has also been shown to be required for growth in glycerol medium. We therefore wondered whether the capacity to activate RNA degradation could account for its requirement for growth on this carbon source. Indeed, a catalytic mutant of Xrn1 is also unable to grow in glycerol medium, and removal of the nuclear localization signal of Rat1, the nuclear homolog of Xrn1, restores glycerol growth. A cytoplasmic 5′-3′ exoribonuclease activity is therefore essential for yeast growth on glycerol, suggesting that Xrn1 activation by Dcs1 is physiologically important. In fact, Xrn1 is essentially inactive in the absence of Dcs1 in vivo. We analyzed the role of Dcs1 in the control of exoribonuclease activity in vitro and propose that Dcs1 is a specific cofactor of Xrn1. Dcs1 does not stimulate the activity of other 5′-3′ exoribonucleases, such as Rat1, in vitro. We demonstrate that Dcs1 improves the apparent affinity of Xrn1 for RNA and that Xrn1 and Dcs1 can form a complex in vitro. We examined the biological significance of this regulation by performing 2D protein gel analysis. We observed that a set of proteins showing decreased levels in a DCS deletion strain, some essential for respiration, are also systematically decreased in an XRN1 deletion mutant. Therefore, we propose that the activation of Xrn1 by Dcs1 is important for respiration.RNA turnover | ribonuclease | post-transcriptional control | porin T urnover of messenger RNA (mRNA) is a regulated process and a key step in the control of gene expression (1). In eukaryotic cells, most cytoplasmic mRNAs are degraded through two alternative pathways, each of which is initiated by the removal of the poly(A) tail by deadenylases. Subsequently, the cap (5′-m 7 GpppN) structure is removed by the decapping complex Dcp1/Dcp2, and the mRNA is degraded in the 5′ to 3′ direction by the major cytoplasmic enzyme Xrn1. Alternatively, deadenylated mRNAs can be degraded from their 3′-ends by the exosome, a multimeric complex possessing 3′ to 5′ exoribonuclease activity (2). The cap structure resulting from 3′-end decay is hydrolyzed by conserved scavenger decapping enzyme Dcs1 (3). Dcs1 is also necessary for the 5′ to 3′ exonucleolytic activity of Xrn1, a requirement that functionally links these two alternative degradation pathways (4). The 5′-3′ exoribonuclease Xrn1 is highly conserved in eukaryotes and has been extensively described for its role in the degradation of cytoplasmic mRNAs (5, 6). Xrn1 also participates in the degradation of nonfunctional mRNAs (7) and noncoding RNAs (8,9).In addition to causing direct defects in RNA turnover, it has been known for a long time that a deletion of XRN1 is detrimental to other cellular functions. XRN1 mutants exhibit pleiotropic phenotypes, including slow growth, loss of viability upon nitrogen starvation, meiotic arrest, defective sporulation, defects in microtubule-related processes, telomere sho...

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Section: Table 1 Dcs Family Proteins and Activation Of Exoribonucleamentioning

confidence: 83%

Activation of 5′-3′ exoribonuclease Xrn1 by cofactor Dcs1 is essential for mitochondrial function in yeast

Sinturel

Bréchemier-Baey

Kiledjian

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…In this case, antisense transcription was found to result in the recruitment of the histone deacetylase Hda1 and thereby downregulate the authentic PHO84 promoter (Camblong et al 2007). Importantly, antisense at PHO84 was found to act both in cis and in trans, as shown by ectopic expression of the antisense and use of a ribozyme inserted in the antisense sequence to cleave the antisense after its synthesis (Camblong et al 2009). In a third study carried out on the KCS1 locus, both antisense and intragenic transcripts were detected (Nishizawa et al 2008).…”

Section: Regulation By Noncoding Rnasmentioning

confidence: 99%

Regulation of Amino Acid, Nucleotide, and Phosphate Metabolism in Saccharomyces cerevisiae

2012

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Ever since the beginning of biochemical analysis, yeast has been a pioneering model for studying the regulation of eukaryotic metabolism. During the last three decades, the combination of powerful yeast genetics and genome-wide approaches has led to a more integrated view of metabolic regulation. Multiple layers of regulation, from suprapathway control to individual gene responses, have been discovered. Constitutive and dedicated systems that are critical in sensing of the intra- and extracellular environment have been identified, and there is a growing awareness of their involvement in the highly regulated intracellular compartmentalization of proteins and metabolites. This review focuses on recent developments in the field of amino acid, nucleotide, and phosphate metabolism and provides illustrative examples of how yeast cells combine a variety of mechanisms to achieve coordinated regulation of multiple metabolic pathways. Importantly, common schemes have emerged, which reveal mechanisms conserved among various pathways, such as those involved in metabolite sensing and transcriptional regulation by noncoding RNAs or by metabolic intermediates. Thanks to the remarkable sophistication offered by the yeast experimental system, a picture of the intimate connections between the metabolomic and the transcriptome is becoming clear.

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“…Finally, as more efforts are put forth to decipher the role of the non-coding genome, it must be emphasized that some of these long non-coding RNAs have been detected with translating ribosomes. 88 Although no examples of lncRNAs that produce functional peptides have been documented to date, we should continue to view the term 29 Promotes induction MMF1 Mitochondrial protein YES ASP3 lncRNA 98 Upregulation ASP3 Asparagine catabolism YES PHO84 AS RNA [99][100][101] Repression PHO84 Phosphate metabolism YES SRG1 28,50,51 Repression SER3 Serine / glycine biogenesis YES PHO5 AS RNA 102 Promotes induction PHO5 Phosphate metabolism YES usURA2. 103 Repression URA2 Pyrimidine biogenesis YES usDCI1.…”

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confidence: 99%

LncRNAs: Bridging environmental sensing and gene expression

2016

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The survival of all organisms is dependent on complex, coordinated responses to environmental cues. Non-coding RNAs have been identified as major players in regulation of gene expression, with recent evidence supporting roles for long non-coding (lnc)RNAs in both transcriptional and post-transcriptional control. Evidence from our laboratory shows that lncRNAs have the ability to form hybridized structures called R-loops with specific DNA target sequences in S. cerevisiae, thereby modulating gene expression. In this Point of View, we provide an overview of the nature of lncRNA-mediated control of gene expression in the context of our studies using the GAL gene cluster as a model for controlling the timing of transcription.

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Trans-acting antisense RNAs mediate transcriptional gene cosuppression in S. cerevisiae

Cited by 143 publications

References 46 publications

Activation of 5′-3′ exoribonuclease Xrn1 by cofactor Dcs1 is essential for mitochondrial function in yeast

Activation of 5′-3′ exoribonuclease Xrn1 by cofactor Dcs1 is essential for mitochondrial function in yeast

Regulation of Amino Acid, Nucleotide, and Phosphate Metabolism in Saccharomyces cerevisiae

LncRNAs: Bridging environmental sensing and gene expression

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