A fork junction DNA-protein switch that controls promoter melting by the bacterial enhancer-dependent sigma factor

Guo, Yanjie; Wang, Lei; Gralla, Jay D.

doi:10.1093/emboj/18.13.3736

Cited by 53 publications

(90 citation statements)

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“…During enhancer-promoter interaction, intervening DNA is looped out (20,21). Interaction of NtrCϳP with the 54 subunit of the holoenzyme probably drives the transition from the closed into the open complex (22)(23)(24).In this work, a multiple-round in vitro transcription assay was used to investigate the role of DNA structure during enhancer action. It was found that when the enhancer is separated from the promoter by a large distance (2.5 kb), enhancer-promoter communication constitutes the rate-limiting step for initiation of transcription on relaxed plasmid DNA.…”

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confidence: 99%

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DNA supercoiling allows enhancer action over a large distance

Liu

Бондаренко

Ninfa

et al. 2001

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

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Enhancers are regulatory DNA elements that can activate their genomic targets over a large distance. The mechanism of enhancer action over large distance is unknown. Activation of the glnAp2 promoter by NtrC-dependent enhancer in Escherichia coli was analyzed by using a purified system supporting multiple-round transcription in vitro. The data suggest that DNA supercoiling is an essential requirement for enhancer action over a large distance (2,500 bp) but not over a short distance (110 bp). DNA supercoiling facilitates functional enhancer-promoter communication over a large distance, probably by bringing the enhancer and promoter into close proximity.T ranscriptional enhancers are relatively short (30 -200 bp) DNA sequences usually composed of several binding sites for activator protein(s). The landmark of enhancers is their ability to communicate with promoters and activate genes over a large distance (up to 60 kb; see ref. 1 for a review). Prokaryotic and eukaryotic enhancers share several key properties such as ability to activate transcription over a large distance, tight coupling of DNA melting with ATP hydrolysis and high stability of the initiation complexes (see refs. 2 and 3 for recent reviews). In contrast to eukaryotic enhancers, prokaryotic enhancers can activate transcription over a large distance in vitro. This ability allows detailed analysis of the mechanism of enhancer action impossible in the case of eukaryotic enhancers.The mechanism of enhancer action over a large distance is unknown. It is most likely that proteins bound at the enhancer and promoter directly interact such that intervening DNA forms a loop (see refs. 4 and 5 for reviews). The main problem for communication over a large distance is low concentration of the DNA regions in the vicinity of each other (see ref. 4 for a review). Measurements of local concentration of linear DNA ends in the vicinity of each other suggest that it is relatively high (10 Ϫ7 M) only when the distance between DNA ends is 100-900 bp (6). When distance between the DNA ends is increased to 3 kb, their local concentration is decreased by an order of magnitude (6). Thus, it is remarkable that DNA regions positioned far away from each other (such as an enhancer and a promoter) can communicate efficiently.Several models have been proposed to explain the mechanism of enhancer action over a large distance. One class of models suggests that initial communication of an enhancer with a promoter leads to formation of a stable DNA-protein complex in the vicinity of the promoter. This stable complex may facilitate subsequent rounds of transcription serving as a ''memory'' of initial enhancer-promoter interaction (see ref. 1 for a review). Alternatively, the average distance between promoter and enhancer could be considerably decreased if the intervening DNA is supercoiled (sc) or bent (see ref. 4 for a review). It has also been shown that sequence-dependent superhelical DNA inserts can facilitate enhancer action (7).The mechanism of action of the NtrC-dependent, 54...

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DNA supercoiling allows enhancer action over a large distance

Liu

Бондаренко

Ninfa

et al. 2001

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

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“…This is otherwise known as a fork-junction structure. (24) Therefore it would appear that the conformation of s 54 when bound to this promoter probe is favourable for PspF interactions. It was also observed that the ternary complex between the smallest fragment of PspF and s 54 bound to the early-melted probe gave a different DNase I footprint, when compared to the s 54 early-melted probe complex alone.…”

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Investigating protein–protein interfaces in bacterial transcription complexes: a fragmentation approach

Burrows

2003

BioEssays

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SummaryTranscription initiation by s 54 -RNA polymerase (RNAP) relies explicitly on a transient interaction with a complex molecular machine belonging to the AAAþ (ATPases associated with various cellular activities) superfamily. Members of the AAAþ superfamily convert chemical energy derived from NTP hydrolysis to a mechanical force used to remodel their target substrate. Recently Bordes and colleagues, (1) using a protein fragmentation approach, identified a unique sequence within s 54 -dependent transcriptional activators that constitutes a s 54 -binding interface. This interface is not static, but subject to nucleotide-dependent movement which may represent a common mechanism for controlling output that has been adopted by other AAAþ proteins. IntroductionDefining the types of strategy and the mechanisms used to control gene expression is important for a full understanding of how the genetic information stored within DNA can be unlocked. Elaborate signal pathways exist to ensure that genes are only expressed when required, thus enabling flexible adaptation in response to changing environmental conditions. At the heart of these pathways lie transcription factors, which regulate the activity of DNA-dependent RNA polymerase (RNAP), the central enzyme in gene expression. Bacterial RNAP is a multisubunit enzyme with subunit composition a 2 bb 0 o; In this 'core' form, the RNAP is catalytically competent but incapable of locating specific DNA target sequences,

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“…Initiation of s 54 -RNAP-dependent transcription resembles eukaryotic transcription initiation by RNAP II. (Guo et al, 1999(Guo et al, , 2000Fu et al, 2000). A closed complex of s class I -RNAP-promoter isomerizes spontaneously to the active, open complex.…”

Section: Introductionmentioning

confidence: 99%

“…Contact between the activator and the s 54 -RNAP-promoter complex is achieved by DNA looping, facilitated either by the integration host factor (IHF) protein or by intrinsic DNA topology (Pérez-Martin et al, 1994;Carmona et al, 1997). Control, imposed on the DNA melting step, requires ATP hydrolysis and involves the promoter 212/211 element (Guo et al, 1999(Guo et al, , 2000 bound inside the RNAP channel (Polyakov et al, 1995;Zhang et al, 1999;Severinov, 2000;Foster et al, 2001). …”

Section: Introductionmentioning

confidence: 99%

A σ 54-dependent promoter in the regulatory region of the Escherichia coli rpoH gene

et al. 2007

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The Escherichia coli rpoH gene is transcribed from four known and differently regulated promoters: P1, P3, P4 and P5. This study demonstrates that the conserved consensus sequence of the s 54 promoter in the regulatory region of the rpoH gene, described previously, is a functional promoter, P6. The evidence for this conclusion is: (i) the specific binding of the s 54 -RNAP holoenzyme to P6, (ii) the location of the transcription start site at the predicted position (C, 30 nt upstream of ATG) and (iii) the dependence of transcription on s 54 and on an ATP-dependent activator. Nitrogen starvation, heat shock, ethanol and CCCP treatment did not activate transcription from P6 under the conditions examined. Two activators of s 54 promoters, PspF and NtrC, were tested but neither of them acted specifically. Therefore, PspFDHTH, a derivative of PspF, devoid of DNA binding capability but retaining its ATPase activity, was used for transcription in vitro, taking advantage of the relaxed specificity of ATP-dependent activators acting in solution. In experiments in vivo overexpression of PspFDHTH from a plasmid was employed. Thus, the s 54 -dependent transcription capability of the P6 promoter was demonstrated both in vivo and in vitro, although the specific conditions inducing initiation of the transcription remain to be elucidated. The results clearly indicate that the closed s 54 -RNAP-promoter initiation complex was formed in vitro and in vivo and needed only an ATP-dependent activator to start transcription.

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A fork junction DNA-protein switch that controls promoter melting by the bacterial enhancer-dependent sigma factor

Cited by 53 publications

References 49 publications

DNA supercoiling allows enhancer action over a large distance

DNA supercoiling allows enhancer action over a large distance

Investigating protein–protein interfaces in bacterial transcription complexes: a fragmentation approach

A σ 54-dependent promoter in the regulatory region of the Escherichia coli rpoH gene

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