DNA supercoiling and transcription in Escherichia coli: The FIS connection

Travers, Andrew; Schneider, Robert; Muskhelishvili, Georgi

doi:10.1016/s0300-9084(00)01217-7

Cited by 79 publications

(57 citation statements)

References 53 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Fis was originally discovered as an E. coli protein essential for the action of a bacteriophage-encoded sitespecific recombinase (34). However, Fis is now known to play important phage-independent functions and affect multiple processes, including replication, recombination, and transcription (35,36). Although HP119-related proteins have a molecular mass of 40 to 50 kDa, they contain repeated sequences that could form separate functional domains, each equivalent to an HLP.…”

Section: Discussionmentioning

confidence: 99%

A Novel DNA-Binding Protein Plays an Important Role in Helicobacter pylori Stress Tolerance and Survival in the Host

Wang

Maier

2015

J Bacteriol

View full text Add to dashboard Cite

The gastric pathogen Helicobacter pylori must combat chronic acid and oxidative stress. It does so via many mechanisms, including macromolecule repair and gene regulation. Mitomycin C-sensitive clones from a transposon mutagenesis library were screened. One sensitive strain contained the insertion element at the locus of hp119, a hypothetical gene. No homologous gene exists in any (non-H. pylori) organism. Nevertheless, the predicted protein has some features characteristic of histone-like proteins, and we showed that purified HP119 protein is a DNA-binding protein. A ⌬hp119 strain was markedly more sensitive (viability loss) to acid or to air exposure, and these phenotypes were restored to wild-type (WT) attributes upon complementation of the mutant with the wild-type version of hp119 at a separate chromosomal locus. The mutant strain was approximately10-fold more sensitive to macrophage-mediated killing than the parent or the complemented strain. Of 12 mice inoculated with the wild type, all contained H. pylori, whereas 5 of 12 mice contained the mutant strain; the mean colonization numbers were 158-fold less for the mutant strain. A proteomic (two-dimensional PAGE with mass spectrometric analysis) comparison between the ⌬hp119 mutant and the WT strain under oxidative stress conditions revealed a number of important antioxidant protein differences; SodB, Tpx, TrxR, and NapA, as well as the peptidoglycan deacetylase PgdA, were significantly less expressed in the ⌬hp119 mutant than in the WT strain. This study identified HP119 as a putative histone-like DNA-binding protein and showed that it plays an important role in Helicobacter pylori stress tolerance and survival in the host. Helicobacter pylori infects the stomachs of approximately 50% of humans and results in a series of human gastric diseases, including gastritis, peptic ulcers, and gastric cancer (1-4). The pathogenesis of H. pylori relies on its persistence in surviving a harsh environment, including acidity, peristalsis, and attack by phagocyte cells and their released reactive oxygen species (5). H. pylori survives on the surface of the stomach lining, often for the lifetime of its host, and causes a chronic inflammatory response. Under physiological conditions, H. pylori is thought to frequently suffer oxidative and acid stress (6, 7). H. pylori is equipped with diverse oxidant detoxification enzymes (e.g., superoxide dismutase, catalase, and peroxiredoxins) (8) and potent acid avoidance mechanisms (mainly urease) (9). To survive the harsh conditions, H. pylori regulates its gene expression in response to the stress signals; however, the bacterium lacks many response regulators known to occur in model microorganisms, such as the SOS response, OxyR/SoxR, and RpoS. Our current knowledge of the stress tolerance mechanisms cannot account for the well-described dynamic survival abilities of H. pylori.Studies in recent years have indicated that DNA recombination and repair play a significant role in H. pylori's persistent colonization of the host (10-14). ...

show abstract

Section: Discussionmentioning

confidence: 99%

A Novel DNA-Binding Protein Plays an Important Role in Helicobacter pylori Stress Tolerance and Survival in the Host

Wang

Maier

2015

J Bacteriol

View full text Add to dashboard Cite

show abstract

“…An increase in the ATP/ADP ratio (energy charge) due to nutritional upshift enhances gyrase activity (because of the enhanced phosphorylation potential of the cell) resulting in higher negative superhelicity (Balke and Gralla 1987;Travers et al 2001;Hatfield and Benham 2002). The stress-induced duplex destabilization (SIDD) model of Benham et al indicates that high superhelical density results in the formation of localized non-B DNA motifs to counter superhelical stress, which exert regulatory control in E. coli (Singh et al 1995;Hatfield and Benham 2002).…”

Section: Discussionmentioning

confidence: 99%

Genome-wide prediction of G4 DNA as regulatory motifs: Role inEscherichia coliglobal regulation

Rawal¹,

Kummarasetti²,

Ravindran³

et al. 2006

Genome Res.

308

343

View full text Add to dashboard Cite

The role of nonlinear DNA in replication, recombination, and transcription has become evident in recent years. Although several studies have predicted and characterized regulatory elements at the sequence level, very few have investigated DNA structure as regulatory motifs. Here, using G-quadruplex or G4 DNA motifs as a model, we have researched the role of DNA structure in transcription on a genome-wide scale. Analyses of >61,000 open reading frames (ORFs) across 18 prokaryotes show enrichment of G4 motifs in regulatory regions and indicate its predominance within promoters of genes pertaining to transcription, secondary metabolite biosynthesis, and signal transduction. Based on this, we predict that G4 DNA may present regulatory signals. This is supported by conserved G4 motifs in promoters of orthologous genes across phylogenetically distant organisms. We hypothesized a regulatory role of G4 DNA during supercoiling stress, when duplex destabilization may result in G4 formation. This is in line with our observations from target site analysis for 55 DNA-binding proteins in Escherichia coli, which reveals significant (P < 0.001) association of G4 motifs with target sites of global regulators FIS and Lrp and the sigma factor RpoD ( 70 ). These factors together control >1000 genes in the early growth phase and are believed to be induced by supercoiled DNA. We also predict G4 motif-induced supercoiling sensitivity for >30 operons in E. coli, and our findings implicate G4 DNA in DNA-topology-mediated global gene regulation in E. coli.

show abstract

“…The torsion angle deviates out of plane at the edges of the 15-bp core, beginning at the bends at G À7 -T À6 and G +6 -C +7 , and the negative dihedral angle is further enhanced in the flanking DNA segments. Fis weakly constrains negative supercoils in vitro, which is incongruent with the sign of the dihedral angle present in the crystals (Travers et al 2001;Johnson et al 2005). A more planar curvature axis would also create a better correspondence between DNA-binding properties of mutations at residues making flanking DNA backbone contacts and H-bonding distances (see below).…”

Section: Dna Conformational Changesmentioning

confidence: 98%

The shape of the DNA minor groove directs binding by the DNA-bending protein Fis

Stella¹,

Cascio²,

Johnson³

2010

Genes Dev.

179

261

View full text Add to dashboard Cite

The bacterial nucleoid-associated protein Fis regulates diverse reactions by bending DNA and through DNAdependent interactions with other control proteins and enzymes. In addition to dynamic nonspecific binding to DNA, Fis forms stable complexes with DNA segments that share little sequence conservation. Here we report the first crystal structures of Fis bound to high-and low-affinity 27-base-pair DNA sites. These 11 structures reveal that Fis selects targets primarily through indirect recognition mechanisms involving the shape of the minor groove and sequence-dependent induced fits over adjacent major groove interfaces. The DNA shows an overall curvature of 65°, and the unprecedented close spacing between helix-turn-helix motifs present in the apodimer is accommodated by severe compression of the central minor groove. In silico DNA structure models show that only the roll, twist, and slide parameters are sufficient to reproduce the changes in minor groove widths and recreate the curved Fis-bound DNA structure. Models based on naked DNA structures suggest that Fis initially selects DNA targets with intrinsically narrow minor grooves using the separation between helix-turn-helix motifs in the Fis dimer as a ruler. Then Fis further compresses the minor groove and bends the DNA to generate the bound structure.[Keywords: DNA structure; protein-DNA recognition; DNA bending; nucleoid protein; X-ray crystallography] Supplemental material is available at http://www.genesdev.org.

show abstract

DNA supercoiling and transcription in Escherichia coli: The FIS connection

Cited by 79 publications

References 53 publications

A Novel DNA-Binding Protein Plays an Important Role in Helicobacter pylori Stress Tolerance and Survival in the Host

A Novel DNA-Binding Protein Plays an Important Role in Helicobacter pylori Stress Tolerance and Survival in the Host

Genome-wide prediction of G4 DNA as regulatory motifs: Role inEscherichia coliglobal regulation

The shape of the DNA minor groove directs binding by the DNA-bending protein Fis

Contact Info

Product

Resources

About