Supercoiling Effects on Short-Range DNA Looping in E. coli

Mogil, Lauren S.; Becker, Nicole A.; Maher, Jim

doi:10.1371/journal.pone.0165306

Cited by 11 publications

(7 citation statements)

References 61 publications

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“…2013 ), nonB-DNA structures are expected to modify the process by relieving the torsional tension of nearby DNA, increasing the energy required for it to bend ( Benham etal. 2010 ; Mogil etal. 2016 ; fig.…”

Section: Links To Enhancer Functionmentioning

confidence: 99%

Functional Mechanisms of Microsatellite DNA in Eukaryotic Genomes

Bagshaw

2017

Genome Biology and Evolution

109

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Microsatellite repeat DNA is best known for its length mutability, which is implicated in several neurological diseases and cancers, and often exploited as a genetic marker. Less well-known is the body of work exploring the widespread and surprisingly diverse functional roles of microsatellites. Recently, emerging evidence includes the finding that normal microsatellite polymorphism contributes substantially to the heritability of human gene expression on a genome-wide scale, calling attention to the task of elucidating the mechanisms involved. At present, these are underexplored, but several themes have emerged. I review evidence demonstrating roles for microsatellites in modulation of transcription factor binding, spacing between promoter elements, enhancers, cytosine methylation, alternative splicing, mRNA stability, selection of transcription start and termination sites, unusual structural conformations, nucleosome positioning and modification, higher order chromatin structure, noncoding RNA, and meiotic recombination hot spots.

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Section: Links To Enhancer Functionmentioning

confidence: 99%

Functional Mechanisms of Microsatellite DNA in Eukaryotic Genomes

Bagshaw

2017

Genome Biology and Evolution

109

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“…Several reports in the literature have shown that the probability of forming loops oscillates as a function of the rotational offset determined by the contour length between the binding sites ( 30–32 ). This may be important for loops between the O1 and O3 operators of the lac operon in E. coli , which are separated by a torsionally rigid 92 bp segment, and may be relevant to observations of the supercoiling-driven modulation of in vivo repression of a reporter gene by protein-mediated DNA loops 70–85 bp-long ( 33 ). As shown previously, supercoiling-induced and HU-stabilized kinks likely bent the segment and optimized the orientation of the binding sites enhanced the formation of the 113 bp loop mediated by the gal repressor ( 27 ).…”

Section: Introductionmentioning

confidence: 99%

Protein-mediated looping of DNA under tension requires supercoiling

Yan

Leng

Finzi

et al. 2018

Nucleic Acids Research

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Protein-mediated DNA looping is ubiquitous in chromatin organization and gene regulation, but to what extent supercoiling or nucleoid associated proteins promote looping is poorly understood. Using the lac repressor (LacI), a paradigmatic loop-mediating protein, we measured LacI-induced looping as a function of either supercoiling or the concentration of the HU protein, an abundant nucleoid protein in Escherichia coli. Negative supercoiling to physiological levels with magnetic tweezers easily drove the looping probability from 0 to 100% in single DNA molecules under slight tension that likely exists in vivo. In contrast, even saturating (micromolar) concentrations of HU could not raise the looping probability above 30% in similarly stretched DNA or 80% in DNA without tension. Negative supercoiling is required to induce significant looping of DNA under any appreciable tension.

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“…1G) in topoisomerase mutant strains exhibiting a global SC shift either in the direction of DNA relaxation (gyrB mutant) or SC increase (topA). This feature was reproduced using the experimentally measured SC levels of these strains [34], suggesting that the two A/Tricher mutant promoters have reached a plateau where the denaturation energy, and hence the expression level, is almost independent of SC.…”

Section: Resultsmentioning

confidence: 65%

“…In vivo SC levels used in the computations of Fig. 1 were taken from [20,16] (E. coli strains with norfloxacin), and [34] (topoisomerase mutants of E. coli). In the data of [19] (Fig.…”

Section: Superhelical Densitiesmentioning

confidence: 99%

The discriminator sequence is a primary determinant in the supercoiling response of bacterial promoters

Forquet

Pineau

Nasser

et al. 2020

Preprint

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DNA supercoiling acts as a basal transcriptional regulator, which contributes to the quick and global transcriptional response of bacteria to many environmental changes. In spite of this importance, mechanistic models explaining the differential response of promoters to global topological variations of the chromosome remain essentially lacking. Here, we present the first quantitative transcriptional regulatory model by DNA supercoiling, focusing on the specific step of promoter opening during transcription initiation. Based on the known physico-chemical properties of DNA denaturation, it involves only one global adjustable parameter and is yet able to predict the global supercoiling response of promoters in a wide range of bacteria, based on the sequence content of their "discriminator" element. We first show that it quantitatively predicts both \emph{in vitro} and \emph{in vivo} data from transcription assays focusing on individual model promoters. We then assess the universality of the mechanism by analyzing transcriptomes of phylogenetically distant bacteria under conditions of supercoiling variation: (1) by gyrase-inhibiting antibiotics, (2) by biologically relevant environmental stresses, (3) naturally acquired and inherited in the longest-running evolution experiment. The model robustly predicts a significant contribution of the entire transcriptomic response to transient or inherited supercoiling variations in various species. This study strongly suggests that the proposed physical mechanism is used as an ubiquitous regulatory mechanism in the whole prokaryotic kingdom, based on the fundamental mechanical properties of the double-helix. Importance: DNA supercoiling acts as a global yet underestimated transcriptional regulator in bacteria. We propose the first quantitative model of this regulation mode, based on the specific step of promoter opening during transcription initiation, explaining the differential response of promoters to global topological variations of the chromosome. In contrast to classical mechanisms requiring dedicated regulatory molecules to bind target promoters, we show that global deformations of the DNA template itself underpin a selective response of each particular promoter, according to its "discriminator" sequence, by modulating the ability of RNA Polymerase to initiate transcription. This study defines the first systematic rule underpinning the ubiquitous regulatory action of DNA supercoiling on the core transcriptional machinery, in particular in response to quick environmental changes.

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Supercoiling Effects on Short-Range DNA Looping in E. coli

Cited by 11 publications

References 61 publications

Functional Mechanisms of Microsatellite DNA in Eukaryotic Genomes

Functional Mechanisms of Microsatellite DNA in Eukaryotic Genomes

Protein-mediated looping of DNA under tension requires supercoiling

The discriminator sequence is a primary determinant in the supercoiling response of bacterial promoters

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