Transcriptional control of yeast ribosomal protein synthesis during carbon-source upshift

Herruer, Martien H.; Mager, Willem H.; Woudt, Lambertus P.; Nieuwint, René T. M.; Wassenaar, Gertrude M.; Ph, Groeneveld; Planta, Rudi J.

doi:10.1093/nar/15.24.10133

Cited by 84 publications

(70 citation statements)

References 30 publications

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“…This is true of responses to heat shock (11,24), to a defect in the secretory pathway (34 and this paper), to growth conditions such as C source (16,22), to levels of cAMP (25,39), and to the deprivation of amino acids (37,62). During the growth cycle, RP genes are repressed as the cells enter late log phase (6,21) and are induced dramatically within 10 min after stationary cells are diluted into a fresh medium (unpublished data).…”

Section: Fig 8 Neithermentioning

confidence: 71%

“…4A) resembles the promoters of most RP genes, with two Rap1p binding sites as the major UAS, and one or two T-rich regions which have some promoter activity (41,45,47), followed by a less well defined region that contains the putative TATA box. Previous work has implicated the Rap1p binding sites as the elements mediating the regulation of transcription, in the response to a carbon source shift (7,16), to amino acid starvation (37), and to cyclic AMP (cAMP) (25,39), but not in the response to a temperature shift (41,45).…”

Section: Resultsmentioning

confidence: 99%

“…The 78 RPs are synthesized in nearly equimolar amounts that are matched to the synthesis of rRNA. Furthermore, the synthesis of these components is coordinately responsive to many changes within or outside the cell, including heat shock, carbon source, and nutrient availability (reviewed in references 44 and 59).The primary level of regulation is at transcription (7,16,24). Most RP genes have similar promoter motifs, consisting of two Rap1p binding sites in tandem arrangement 250 to 400 bp upstream of the transcription initiation site recently compiled by Lascaris et al (26), followed by one or two T-rich regions, and then a region of about 180 bp that includes the putative TATA element.…”

mentioning

confidence: 99%

“…The primary level of regulation is at transcription (7,16,24). Most RP genes have similar promoter motifs, consisting of two Rap1p binding sites in tandem arrangement 250 to 400 bp upstream of the transcription initiation site recently compiled by Lascaris et al (26), followed by one or two T-rich regions, and then a region of about 180 bp that includes the putative TATA element.…”

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confidence: 99%

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Transcriptional Elements Involved in the Repression of Ribosomal Protein Synthesis

Nierras

Warner

1999

Molecular and Cellular Biology

103

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The ribosomal proteins (RPs) of Saccharomyces cerevisiae are encoded by 137 genes that are among the most transcriptionally active in the genome. These genes are coordinately regulated: a shift up in temperature leads to a rapid, but temporary, decline in RP mRNA levels. A defect in any part of the secretory pathway leads to greatly reduced ribosome synthesis, including the rapid loss of RP mRNA. Here we demonstrate that the loss of RP mRNA is due to the rapid transcriptional silencing of the RP genes, coupled to the naturally short lifetime of their transcripts. The data suggest further that a global inhibition of polymerase II transcription leads to overestimates of the stability of individual mRNAs. The transcription of most RP genes is activated by two Rap1p binding sites, 250 to 400 bp upstream from the initiation of transcription. Rap1p is both an activator and a silencer of transcription. The swapping of promoters between RPL30 and ACT1 or GAL1 demonstrated that the Rap1p binding sites of RPL30 are sufficient to silence the transcription of ACT1 in response to a defect in the secretory pathway. Sir3p and Sir4p, implicated in the Rap1p-mediated repression of silent mating type genes and of telomere-proximal genes, do not influence such silencing of RP genes. Sir2p, implicated in the silencing both of the silent mating type genes and of genes within the ribosomal DNA locus, does not influence the repression of either RP or rRNA genes. Surprisingly, the 180-bp sequence of RPL30 that lies between the Rap1p sites and the transcription initiation site is also sufficient to silence the Gal4p-driven transcription in response to a defect in the secretory pathway, by a mechanism that requires the silencing region of Rap1p. We conclude that for Rap1p to activate the transcription of an RP gene it must bind to upstream sequences; yet for Rap1p to repress the transcription of an RP gene it need not bind to the gene directly. Thus, the cell has evolved a two-pronged approach to effect the rapid extinction of RP synthesis in response to the stress imposed by a heat shock or by a failure of the secretory pathway. Calculations based on recent transcriptome data and on the half-life of the RP mRNAs suggest that in a rapidly growing cell the transcription of RP mRNAs accounts for nearly 50% of the total transcriptional events initiated by RNA polymerase II. Thus, the sudden silencing of the RP genes must have a dramatic effect on the overall transcriptional economy of the cell.The Saccharomyces cerevisiae cell invests enormous resources in the synthesis of ribosomes. In a rapidly growing cell, the 100 or more rRNA genes are responsible for at least 60% of total transcription (59). The 137 ribosomal protein (RP) genes are among the most active in the genome (57). As a result, the cell has evolved mechanisms that tightly control the synthesis of the components of the ribosome. The 78 RPs are synthesized in nearly equimolar amounts that are matched to the synthesis of rRNA. Furthermore, the synthesis of these components is coo...

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Section: Fig 8 Neithermentioning

confidence: 71%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Transcriptional Elements Involved in the Repression of Ribosomal Protein Synthesis

Nierras

Warner

1999

Molecular and Cellular Biology

103

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“…In E. coli, some of this regulation is achieved by transcriptional attenuation and translational regulation via binding of ribosomal proteins to the RNAs of target operons (Freedman et al, 1985;Cole and Nomura, 1986). In yeast, regulation is partly transcriptional, via RAP1 and its binding site, the upstream activating sequence (UAS) rpg (Herruer et al, 1987;Moehle and Hinnebusch, 1991;Kraakman et al, 1993), although much of the regulation of ribosomal protein abundance is achieved by a competition between the assembly into ribosomes and the rapid degradation of unassembled ribosomal proteins (Warner et al, 1985;Maicas et al, 1988).Growth rate control clearly modulates the level of the translational machinery, which in turn influences the overall rate of protein synthesis. Changes in the rates of protein synthesis must, in turn, have profound implications for the protein chaperone system.…”

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confidence: 99%

Complex Regulation of the Yeast Heat Shock Transcription Factor

Bonner

Carlson

Fackenthal

et al. 2000

MBoC

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The yeast heat shock transcription factor (HSF) is regulated by posttranslational modification. Heat and superoxide can induce the conformational change associated with the heat shock response. Interaction between HSF and the chaperone hsp70 is also thought to play a role in HSF regulation. Here, we show that the Ssb1/2p member of the hsp70 family can form a stable, ATP-sensitive complex with HSF-a surprising finding because Ssb1/2p is not induced by heat shock. Phosphorylation and the assembly of HSF into larger, ATP-sensitive complexes both occur when HSF activity decreases, whether during adaptation to a raised temperature or during growth at low glucose concentrations. These larger HSF complexes also form during recovery from heat shock. However, if HSF is assembled into ATP-sensitive complexes (during growth at a low glucose concentration), heat shock does not stimulate the dissociation of the complexes. Nor does induction of the conformational change induce their dissociation. Modulation of the in vivo concentrations of the SSA and SSB proteins by deletion or overexpression affects HSF activity in a manner that is consistent with these findings and suggests the model that the SSA and SSB proteins perform distinct roles in the regulation of HSF activity. INTRODUCTIONIt has long been known that in cells of many species, including Escherichia coli and Saccharomyces cerevisiae, cell division rates are tightly coupled with the steady-state levels and rates of synthesis of ribosomal proteins and rRNA. For example, cells in rich media, with a short generation time, display higher abundance of rRNA and higher rates of synthesis of ribosomal proteins than do cells in poor media, with a long generation time. In E. coli, some of this regulation is achieved by transcriptional attenuation and translational regulation via binding of ribosomal proteins to the RNAs of target operons (Freedman et al., 1985;Cole and Nomura, 1986). In yeast, regulation is partly transcriptional, via RAP1 and its binding site, the upstream activating sequence (UAS) rpg (Herruer et al., 1987;Moehle and Hinnebusch, 1991;Kraakman et al., 1993), although much of the regulation of ribosomal protein abundance is achieved by a competition between the assembly into ribosomes and the rapid degradation of unassembled ribosomal proteins (Warner et al., 1985;Maicas et al., 1988).Growth rate control clearly modulates the level of the translational machinery, which in turn influences the overall rate of protein synthesis. Changes in the rates of protein synthesis must, in turn, have profound implications for the protein chaperone system. Newly synthesized polypeptides typically do not adopt their mature conformation immediately but instead follow a complex folding pathway. For many proteins, the cytoplasmic chaperone system plays an integral role in helping these polypeptides adopt their mature conformations (for review, see Hendrick and Hartl, 1995). The hsp70 proteins are generally believed to bind efficiently to nascent or newly synthesized polypeptides...

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