<i>Escherichia coli</i> ribosomal RNA transcription: regulatory roles for ppGpp, NTPs, architectural proteins and a polymerase‐binding protein

Gralla, Jay D.

doi:10.1111/j.1365-2958.2004.04455.x

Cited by 72 publications

(69 citation statements)

References 34 publications

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“…rRNA transcription initiation is also regulated by the concentration of the first nucleotide in the transcript (8,14) and by at least one DNA binding factor, the 11.2-kDa Fis protein (15). Together, ppGpp, DksA, the concentration of the first NTP (iNTP), and Fis match ribosome synthesis rates to the availability of nutrients (8,11,(14)(15)(16)(17)(18)(19).…”

mentioning

confidence: 99%

Direct regulation of Escherichia coli ribosomal protein promoters by the transcription factors ppGpp and DksA

Lemke

Sanchez-Vazquez²,

Burgos³

et al. 2011

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

140

144

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We show here that the promoters for many of the Escherichia coli ribosomal protein operons are regulated directly by two transcription factors, the small RNA polymerase-binding protein DksA and the nutritional stress-induced nucleotide ppGpp. ppGpp and DksA work together to inhibit transcription initiation from ribosomal protein promoters in vitro and in vivo. The degree of promoter regulation by ppGpp/DksA varies among the r-protein promoters, but some are inhibited almost as much as rRNA promoters. Thus, many r-protein operons are regulated at the level of transcription in addition to their control by the classic translational feedback systems discovered ∼30 y ago. We conclude that direct control of r-protein promoters and rRNA promoters by the same signal, ppGpp/DksA, makes a major contribution to the balanced and coordinated synthesis rates of all of the ribosomal components.ribosome synthesis | transcriptional control | stringent response | translational control P rotein synthesis is the major consumer of cellular energy in bacteria. Because the number of ribosomes is the primary determinant of the level of translation, and ribosome synthesis itself is an energy-intensive process, there are mechanisms that prevent over-or underinvestment of cellular resources in ribosome synthesis (1). Both ribosomal RNA (rRNA) and ribosomal protein (r-protein) synthesis rates are thereby tightly regulated in Escherichia coli (for reviews, see refs. 2, 3).One of the earliest reported examples of regulation of bacterial ribosome synthesis is a stress response referred to as "the stringent response," in which rRNA transcription is inhibited in cells starved for amino acids or some other nutrients (4). In this response, uncharged tRNAs induce the ribosome-associated RelA and/or SpoT proteins to synthesize ppGpp (5-7). [The term "ppGpp" is used here to describe both the unusual nucleotide guanosine-3′,5′-(bis)pyrophosphate and its pentaphosphate precursor.] ppGpp concentrations change not only after complete starvations but also after less severe shifts in nutritional conditions, coordinating rRNA synthesis with the need for protein synthesis. Shifts to a more favorable nutritional condition result in a decrease in the concentration of ppGpp and a corresponding increase in rRNA promoter activity, whereas shifts to a less favorable condition result in an increase in ppGpp and a corresponding decrease in rRNA transcription (8).ppGpp binds directly to E. coli RNA polymerase (RNAP) and inhibits transcription from rRNA promoters (9), although the identity of the ppGpp binding site on RNAP remains unclear (10). However, for ppGpp to exert its full effect on transcription, RNAP has to be modified by the small protein, DksA (11,12). Unlike ppGpp, DksA is present at high concentrations in cells under all conditions that have been examined (11,13). rRNA transcription initiation is also regulated by the concentration of the first nucleotide in the transcript (8,14) and by at least one DNA binding factor, the 11.2-kDa Fis protein (15). Tog...

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mentioning

confidence: 99%

Direct regulation of Escherichia coli ribosomal protein promoters by the transcription factors ppGpp and DksA

Lemke

Sanchez-Vazquez²,

Burgos³

et al. 2011

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

140

144

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“…The oligomerization of H-NS is, therefore, essential for preferential binding and stabilization of the multimeric nucleoprotein complex (Spurio et al 1997). A recent study of an E. coli ribosomal gene promoter rrnB P1 has suggested that repression involves DNA looping and that the loop is closed by the association of two patches of H-NS-bound DNA in which the RNP is trapped, instead of being excluded (Schroder and Wagner 2000;Dame et al 2002;Dame 2005;Gralla 2005). According to this model, expression from an H-NS repressed promoter should require disruption of the nucleoprotein complex and the DNA loop by transcription factors.…”

mentioning

confidence: 99%

DNA looping-mediated repression by histone-like protein H-NS: specific requirement of Eσ⁷⁰ as a cofactor for looping

Shin¹,

Song²,

Rhee³

et al. 2005

Genes Dev.

149

102

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“…FIS is a nucleoid-binding protein involved in global regulatory circuits related to repression of genes that are not required Role of FIS in aromatic catabolic pathways of E. coli under conditions of optimal growth (González-Gil, et al, 1996). It is also well known that FIS acts as a positive regulator of the transcription of the genes that encode stable RNA species, such as rRNA and tRNA (Ross et al, 1990;Bosch et al, 1990;Nilsson & Emilson, 1994;Gralla, 2005). To investigate the putative role of FIS in the hpa regulatory system, we generated a FIS mutant of the E. coli strain W, named W16 (Table 1).…”

Section: Pg Repression Is Relieved In a Fis Mutant When Cultured In Lmentioning

confidence: 99%

The role of FIS protein in the physiological control of the expression of the Escherichia coli meta-hpa operon

et al. 2008

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Expression from the Escherichia coli W meta-hpa operon promoter (Pg) is under a strict catabolic repression control mediated by the cAMP-catabolite repression protein (CRP) complex in a glucose-containing medium. The Pg promoter is also activated by the integration host factor (IHF) and repressed by the specific transcriptional regulator HpaR when 4-hydroxyphenylacetate (4HPA) is not present in the medium. Expression from the hpa promoter is also repressed in undefined rich medium such as LB, but the molecular basis of this mechanism is not understood. We present in vitro and in vivo studies to demonstrate the involvement of FIS protein in this catabolic repression. DNase I footprinting experiments show that FIS binds to multiple sites within the Pg promoter. FIS-site I overlaps the CRP-binding site. By using an electromobility shift assay, we demonstrated that FIS efficiently competes with CRP for binding to the Pg promoter, suggesting an antagonist/competitive mechanism. RT-PCR showed that the Pg repression effect is relieved in a FIS deleted strain. The repression role of FIS at Pg was further demonstrated by in vitro transcription assays. These results suggest that FIS contributes to silencing the Pg promoter in the exponential phase of growth in an undefined rich medium when FIS is predominantly expressed.

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Escherichia coli ribosomal RNA transcription: regulatory roles for ppGpp, NTPs, architectural proteins and a polymerase‐binding protein

Cited by 72 publications

References 34 publications

Direct regulation of Escherichia coli ribosomal protein promoters by the transcription factors ppGpp and DksA

Direct regulation of Escherichia coli ribosomal protein promoters by the transcription factors ppGpp and DksA

DNA looping-mediated repression by histone-like protein H-NS: specific requirement of Eσ⁷⁰ as a cofactor for looping

The role of FIS protein in the physiological control of the expression of the Escherichia coli meta-hpa operon

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Escherichia coli ribosomal RNA transcription: regulatory roles for ppGpp, NTPs, architectural proteins and a polymerase‐binding protein

Cited by 72 publications

References 34 publications

Direct regulation of Escherichia coli ribosomal protein promoters by the transcription factors ppGpp and DksA

Direct regulation of Escherichia coli ribosomal protein promoters by the transcription factors ppGpp and DksA

DNA looping-mediated repression by histone-like protein H-NS: specific requirement of Eσ70 as a cofactor for looping

The role of FIS protein in the physiological control of the expression of the Escherichia coli meta-hpa operon

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DNA looping-mediated repression by histone-like protein H-NS: specific requirement of Eσ⁷⁰ as a cofactor for looping