Antagonistic Regulation of Escherichia coli Ribosomal RNA rrnB P1 Promoter Activity by GreA and DksA

Potrykus, Katarzyna; Vinella, Daniel; Murphy, Helen; Szalewska-Pałasz, Agnieszka; D’Ari, Richard; Cashel, Michael

doi:10.1074/jbc.m601531200

Cited by 71 publications

(110 citation statements)

References 42 publications

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“…This organization could generate a gradient of superhelical density ( Fig. 3D) correlating with that of Eσ 70 targets and anti-correlating with Eσ S targets, as expected from the opposite supercoiling preferences of these holoenzymes (3,28) and in keeping with the requirement of high negative superhelicity for initiation of OriC replication (37).…”

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confidence: 59%

“…Thus, the originproximal region contains a five-to 10-fold higher average density of gyrase-binding sites than the Ter-proximal region (Fig. 3C) and also is the preferred target region for Eσ 70 holoenzyme and for FIS protein ( Fig. 3 A and E), implicated in evolutionary modulation of DNA superhelicity (25).…”

Section: Discussionmentioning

confidence: 99%

“…Not only are the genes coordinating the major regulatory pathways ordered; their targets are ordered as well. Analyses of the distribution density of binding sites for Eσ 70 and Eσ S holoenzymes compiled in RegulonDB (34) show opposite spatial biases. For the vegetative σ 70 factor the highest percentage of targets is found around the origin, whereas for the stationary phase σ S factor the highest target density is close to the terminus ( Fig.…”

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confidence: 96%

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Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle

Sobetzko

Travers²,

Muskhelishvili³

2011

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

200

261

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In Escherichia coli crosstalk between DNA supercoiling, nucleoid-associated proteins and major RNA polymerase σ initiation factors regulates growth phase-dependent gene transcription. We show that the highly conserved spatial ordering of relevant genes along the chromosomal replichores largely corresponds both to their temporal expression patterns during growth and to an inferred gradient of DNA superhelical density from the origin to the terminus. Genes implicated in similar functions are related mainly in trans across the chromosomal replichores, whereas DNA-binding transcriptional regulators interact predominantly with targets in cis along the replichores. We also demonstrate that macrodomains (the individual structural partitions of the chromosome) are regulated differently. We infer that spatial and temporal variation of DNA superhelicity during the growth cycle coordinates oxygen and nutrient availability with global chromosome structure, thus providing a mechanistic insight into how the organization of a complete bacterial chromosome encodes a spatiotemporal program integrating DNA replication and global gene expression. In Escherichia coli cells the physiological transitions induced by the changing growth environment are accompanied by changes in DNA superhelical density (1-3), nucleoid structure (4-6), and the promoter selectivity of the RNA polymerase (RNAP) holoenzyme (3, 7). During the growth cycle both the relative and absolute concentrations of the abundant nucleoid-associated proteins (NAPs ; Table S1) change substantially and correspondingly generate bacterial chromatin of variable composition (8, 9). The NAPs stabilize distinct supercoil structures (10-12) selectively favoring particular RNAP holoenzymes (13-15). These variable nucleoprotein complexes modulate DNA topology during the growth cycle (Fig. 1A), optimizing the channeling of supercoil energy into appropriate metabolic pathways (16,17).The expression of the genes determining superhelical density, polymerase selectivity, and nucleoid structure is coordinated by cross-regulation. Thus, factor for inversion stimulation (FIS), a NAP abundant during the early exponential phase (18), regulates expression not only of the superhelicity determinants DNA gyrase subunits A and B (gyrA and gyrB) and topoisomerase I (topA) (19-21) but also other NAP-encoding genes including hns, α subunit of histone-like protein from E. coli strain U93 (hupA), and DNA binding protein from starved cells (dps) (22-24) and components of the transcription machinery such as σ 38 subunit of RNA polymerase rpoS (25). Similarly mutations affecting the selectivity of RNAP influence NAP production (26-28). Again, mutations in the genes controlling DNA superhelicity affect the production of both NAPs and the basal transcription machinery (27,29). This pattern of integrated control constitutes a heterarchical network coordinating chromosome structure with cellular metabolism (27,28,30). A further pointer to this integrated network is the observed selection of mutations in fis...

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confidence: 59%

Section: Discussionmentioning

confidence: 99%

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confidence: 96%

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Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle

Sobetzko

Travers²,

Muskhelishvili³

2011

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

200

261

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“…Second, although there is good evidence that DksA binds around and projects into the secondary channel like Gre proteins, there is no atomic structure of a bound complex, and hence no indication of exactly how the active center might be affected. In fact, there must be some common effect of DksA and Gre binding in the secondary channel, because the variant GreB can replace DksA for stringent regulation in vitro, and both GreB and GreA replace DksA in vivo if they are overexpressed at high concentration (Potrykus et al 2006;Rutherford et al 2007). …”

Section: +mentioning

confidence: 99%

Promoter-specific control of E. coli RNA polymerase by ppGpp and a general transcription factor

Roberts¹

2009

Genes Dev.

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The stringent response of Escherichia coli reflects a global influence of the nucleotide ppGpp on gene expression in response to nutrient starvation. For critical elements of the response, the target of ppGpp is RNA polymerase, which can be either repressed or activated in a promoter-dependent way. A small protein, DksA, which binds in the secondary channel of RNA polymerase, possibly along with other general regulatory factors, contributes to ppGpp-dependent transcription regulation. Rutherford and colleagues (pp. 236–248) identify mutations in genes for the core subunits of RNA polymerase that circumvent the need for DksA in the regulation; the sites of these mutations suggest that DksA acts allosterically through the RNA polymerase active site to destabilize transcription initiation complexes.

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“…The Gre factors are involved in restarting these paused complexes to relieve the genome of these obstacles (Borukhov et al, 1993;Erie et al, 1993;Orlova et al, 1995). Although the Gre factors have only been thought to regulate mRNA ECs, there is some evidence that they may also be involved in regulating initiation from both mRNA and rRNA promoters (Hsu et al, 1995;Potrykus et al, 2006;Stepanova et al, 2007). …”

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Transcription factor dynamics

2008

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Gene expression is a fundamental process that is highly conserved from humans to bacteria. The first step in gene expression, transcription, is performed by structurally conserved DNAdependent RNA polymerases (RNAPs), which results in the synthesis of an RNA molecule from a DNA template. In bacteria, a single species of RNAP is responsible for transcribing both stable RNA (i.e. t-and rRNA) and protein-encoding genes (i.e. mRNA), unlike eukaryotic systems, which use three distinct RNAP species to transcribe the different gene classes (RNAP I transcribes most rRNA, RNAP II transcribes mRNA, and RNAP III transcribes tRNA and 5S rRNA). The versatility of bacterial RNAP is dependent on both dynamic interactions with co-factors and the coding sequence of the template DNA, which allows RNAP to respond appropriately to the transcriptional needs of the cell. Although the majority of the research on gene expression has focused on the initiation stage, regulation of the elongation phase is essential for cell viability and represents an important topic for study. The elongation factors that associate with RNAP are unique and highly conserved among prokaryotes, making disruption of their interactions a potentially important target for antibiotic development. One of the most significant advances in molecular biology over the last decade has been the use of green fluorescent protein (GFP) and its spectral variants to observe the subcellular localization of proteins in live intact cells. This review discusses transcription dynamics with respect to RNAP and its associated transcription elongation factors in the two best-studied prokaryotes, Escherichia coli and Bacillus subtilis. RNAP and the transcription machineryProkaryotic RNA polymerase (RNAP) is a large (~400 kDa) multi-subunit enzyme comprising a 2 bb9v subunits which form a crab-claw-like structure. Although little sequence homology exists between eubacterial RNAP, archaeal RNAP and eukaryotic RNAPII, the crab-claw structure is remarkably conserved (Zhang et al., 1999;Cramer et al., 2001;Hirata et al., 2008). The two a subunits act as a scaffold to hold the catalytic b and b9 subunits together, forming the crab-claw-like structure (Zhang et al., 1999). The exact role of the v subunit is unclear but it is related in both structure and sequence to the eukaryotic polymerase subunit Rpb6 (Minakhin et al., 2001). It appears to be responsible for controlling transcription in response to nutrient shifts, correct folding of the b9 subunit and its assembly into the core multi-subunit enzyme (Mukherjee et al., 1999;Vrentas et al., 2005;Chatterji et al., 2007). The channel formed by b and b9 is referred to as the primary channel, which contains a deep positively charged cleft housing the enzyme's active site. During transcription, downstream double-stranded DNA separates into a singlestranded DNA template, which enters the primary channel and contacts the active site to allow polymerization of RNA (Borukhov & Nudler, 2008). Due to the crowding of the primary channel by the DNA : R...

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Antagonistic Regulation of Escherichia coli Ribosomal RNA rrnB P1 Promoter Activity by GreA and DksA

Cited by 71 publications

References 42 publications

Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle

Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle

Promoter-specific control of E. coli RNA polymerase by ppGpp and a general transcription factor

Transcription factor dynamics

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