Regulation of the RNA Polymerase I and III Transcription Systems in Response to Growth Conditions

Clarke, Eileen M. W.; Peterson, Cheryl L.; Brainard, Aaron V.; Riggs, Daniel L.

doi:10.1074/jbc.271.36.22189

Cited by 47 publications

(35 citation statements)

References 43 publications

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“…Gcn4p thus appears to be a key regulatory protein in the global remodeling of RNA Pol II-dependent genome expression elicited by diverse signals of starvation and stress. Several environmentally stressful conditions, such as nutrient limitation, secretion defects, and treatment with DNA-damaging agents, are known to severely downregulate RNA Pol III-dependent transcription in yeast (9,12,21,34,49,52,58). The reduction in the level of initiator tRNA Met resulting from such perturbations might contribute to GCN4 translational activation and the consequent, genome-wide reprogramming of RNA Pol II-dependent transcription.…”

Section: Discussionmentioning

confidence: 99%

“…The triplication of the transcriptional machinery may provide a selective advantage to the eukaryotic cell, compared to the unique bacterial and archaeal RNA polymerases, by allowing independent or coordinated regulations of gene expression in response to environmental changes. Previous studies both in yeast and in higher eukaryotes have shown that Pol III transcription is coordinately regulated with Pol I transcription under many circumstances, e.g., upon nitrogen starvation or in response to a nutritional upshift (6,9,53,58). Under other conditions, the regulatory pathways of Pol I and Pol III transcription are uncoupled.…”

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confidence: 99%

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Modulation of Yeast Genome Expression in Response to Defective RNA Polymerase III-Dependent Transcription

Conesa

Ruotolo

Soularue³

et al. 2005

Molecular and Cellular Biology

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We used genome-wide expression analysis in Saccharomyces cerevisiae to explore whether and how the expression of protein-coding, RNA polymerase (Pol) II-transcribed genes is influenced by a decrease in RNA Pol III-dependent transcription. The Pol II transcriptome was characterized in four thermosensitive, slowgrowth mutants affected in different components of the RNA Pol III transcription machinery. Unexpectedly, we found only a modest correlation between altered expression of Pol II-transcribed genes and their proximity to class III genes, a result also confirmed by the analysis of single tRNA gene deletants. Instead, the transcriptome of all of the four mutants was characterized by increased expression of genes known to be under the control of the Gcn4p transcriptional activator. Indeed, GCN4 was found to be translationally induced in the mutants, and deleting the GCN4 gene eliminated the response. The Gcn4p-dependent expression changes did not require the Gcn2 protein kinase and could be specifically counteracted by an increased gene dosage of initiator tRNA Met . Initiator tRNA Met depletion thus triggers a GCN4-dependent reprogramming of genome expression in response to decreased Pol III transcription. Such an effect might represent a key element in the coordinated transcriptional response of yeast cells to environmental changes.

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Modulation of Yeast Genome Expression in Response to Defective RNA Polymerase III-Dependent Transcription

Conesa

Ruotolo

Soularue³

et al. 2005

Molecular and Cellular Biology

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“…In fact, the main evidence for coordinated control of the transcriptional synthesis of rRNA, ribosomal protein mRNAs, and tRNAs is that blocking protein secretion inhibits these three processes in a way that requires protein kinase C (19). On the other hand, rRNA and tRNA synthesis can be uncoupled under physiological conditions, such as amino acid starvation (6,23). Even under balanced growth conditions, the cellular levels of tRNAs and rRNAs are roughly but not strictly constant, since rRNAs are more strongly affected than tRNAs in slow-growing cells (15,32,37).…”

Section: Discussionmentioning

confidence: 99%

Cross Talk between tRNA and rRNA Synthesis in Saccharomyces cerevisiae

Briand

Navarro

Gadal

et al. 2001

Molecular and Cellular Biology

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Temperature-sensitive RNA polymerase III (rpc160-112 and rpc160-270) mutants were analyzed for the synthesis of tRNAs and rRNAs in vivo, using a double-isotopic-labeling technique in which cells are pulselabeled with [ 33 P]orthophosphate and coextracted with [ 3 H]uracil-labeled wild-type cells. Individual RNA species were monitored by Northern blot hybridization or amplified by reverse transcription. These mutants impaired the synthesis of RNA polymerase III transcripts with little or no influence on mRNA synthesis but also largely turned off the formation of the 25S, 18S, and 5.8S mature rRNA species derived from the common 35S transcript produced by RNA polymerase I. In the rpc160-270 mutant, this parallel inhibition of tRNA and rRNA synthesis also occurred at the permissive temperature (25°C) and correlated with an accumulation of 20S pre-rRNA. In the rpc160-112 mutant, inhibition of rRNA synthesis and the accumulation of 20S pre-rRNA were found only at 37°C. The steady-state rRNA/tRNA ratio of these mutants reflected their tRNA and rRNA synthesis pattern: the rpc160-112 mutant had the threefold shortage in tRNA expected from its preferential defect in tRNA synthesis at 25°C, whereas rpc160-270 cells completely adjusted their rRNA/tRNA ratio down to a wild-type level, consistent with the tight coupling of tRNA and rRNA synthesis in vivo. Finally, an RNA polymerase I (rpa190-2) mutant grown at the permissive temperature had an enhanced level of pre-tRNA, suggesting the existence of a physiological coupling between rRNA synthesis and pre-tRNA processing.The existence of three nuclear transcription systems is documented for all eukaryotes investigated so far. RNA polymerase I synthesizes the three largest rRNAs, RNA polymerase II produces mRNAs and many noncoding RNAs, and RNA polymerase III makes tRNAs and 5S rRNA, as well as a few small noncoding RNAs. Exceptions to this transcriptional specialization are rare and mostly concern noncoding RNA species that can be produced by either RNA polymerase II or III, depending on the phylum considered (reference 39 and references therein). Given its universality, the triplication of the transcriptional apparatus must provide a major selective advantage to the eukaryotic cell, probably by facilitating the separate control of mRNA, rRNA, and tRNA synthesis in response to changes in the environment or in the cell growth rate. On the other hand, RNA polymerases I and III deliver matching amounts of tRNAs and rRNAs to the protein synthesis machinery and may thus need to operate in a closely coordinated way (references 21, 38, and 39 and references therein). In fact, the extent to which the three nuclear RNA polymerases are coordinated relative to each other remains largely undetermined, although this is presumably a key aspect of the transcriptional regulation of growth.Yeast (Saccharomyces cerevisiae) is a particularly convenient model organism to study transcription and its regulation. Its three nuclear RNA polymerases are biochemically and genetically well characterized ...

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“…We then investigated the relationships between gene activity and occupancy by the Pol III machinery. Pol III transcription is high in rich medium, and repressed during nutrient deprivation (17). Accordingly, we subjected yeast cultures bearing tagged Pol III machinery to the following regimen: logarithmic growth (nutrient replete), nutrient deprivation, and nutrient reintroduction.…”

Section: B-e)mentioning

confidence: 99%

“…Several conditions related to nutrient deprivation and cell stress can lead to a rapid and͞or dramatic reduction in Pol III transcription (17)(18)(19)(20). Stress conditions are relayed to the Pol III machinery by various signaling pathways, including those mediated by CK2 and Pkc1 (19)(20)(21).…”

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confidence: 99%

The RNA polymerase III transcriptome revealed by genome-wide localization and activity–occupancy relationships

Roberts

Stewart

Huff

et al. 2003

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

165

203

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RNA polymerase III (Pol III) transcribes small untranslated RNAs, such as tRNAs. To define the Pol III transcriptome in Saccharomyces cerevisiae, we performed genome-wide chromatin immunoprecipitation using subunits of Pol III, TFIIIB and TFIIIC. Virtually all of the predicted targets of Pol III, as well as several novel candidates, were occupied by Pol III machinery. Interestingly, TATA boxbinding protein occupancy was greater at Pol III targets than virtually all Pol II targets, and the highly occupied Pol II targets are generally strongly transcribed. The temporal relationships between factor occupancy and gene activity were then investigated at selected targets. Nutrient deprivation rapidly reduced both Pol III transcription and Pol III occupancy of both a tRNA gene and RPR1. In contrast, TFIIIB remained bound, suggesting that TFIIIB release is not a critical aspect of the onset of repression. Remarkably, TFIIIC occupancy increased dramatically during repression. Nutrient addition generally reestablished transcription and initial occupancy levels. Our results are consistent with active Pol III displacing TFIIIC, and with inactivation͞release of Pol III enabling TFIIIC to bind, marking targets for later activation. These studies reveal new aspects of the kinetics, dynamics, and targets of the Pol III system. R NA polymerase III (Pol III) in Saccharomyces cerevisiae transcribes genes for small structural RNAs important for many cellular processes. Among the known Pol III targets are structural RNAs for translation (all tRNAs, 5S ribosomal RNA, 7SL RNA), tRNA processing (RPR1; the RNA of the ribonuclease P complex), and splicing (i.e., U6). The S. cerevisiae genome is predicted to contain 280 targets, including 275 tRNA genes. The Pol III transcription machinery is highly conserved in eukaryotes, and consists of the multisubunit Pol III polymerase, two complexes (TFIIIB and TFIIIC) required for promoter recognition and͞or initiation, and an additional factor (TFIIIA) required only for 5S rDNA transcription (1-3).Several reviews have addressed the function and regulation of the Pol III machinery in detail (2-4), and here we provide a brief summary. Pol III promoters contain two conserved DNA sequence elements, termed A and B boxes, which are located within the transcribed region and direct the Pol III machinery to target genes (5, 6). The A and B boxes are recognized by the TFIIIC complex, which can bind in the absence of TFIIIB and Pol III, establishing TFIIIC as the promoter specificity factor (7-11). Because most Pol III targets are relatively short (Ͻ100 bases), TFIIIC can encompass nearly the entire gene (12).TFIIIC interacts with TFIIIB, enabling recruitment of TFIIIB to Pol III promoters (13,14). TFIIIB contains the subunits Brf1 (TFIIB-related factor), Bdp1͞Tfc5͞BЉ, and the TATA-binding protein (TBP). TBP is the only subunit of the basal factors not dedicated solely to Pol III transcription; TBP is used by all three RNA polymerases and is required for transcription at both TATAcontaining and TATA-less pr...

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Regulation of the RNA Polymerase I and III Transcription Systems in Response to Growth Conditions

Cited by 47 publications

References 43 publications

Modulation of Yeast Genome Expression in Response to Defective RNA Polymerase III-Dependent Transcription

Modulation of Yeast Genome Expression in Response to Defective RNA Polymerase III-Dependent Transcription

Cross Talk between tRNA and rRNA Synthesis in Saccharomyces cerevisiae

The RNA polymerase III transcriptome revealed by genome-wide localization and activity–occupancy relationships

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