Salmonella enterica Response Regulator SsrB Relieves H-NS Silencing by Displacing H-NS Bound in Polymerization Mode and Directly Activates Transcription

Walthers, Don; Li, You; Liu, Yingjie; Anand, Ganesh S.; Yan, Jie; Kenney, Linda J.

doi:10.1074/jbc.m110.164962

Cited by 85 publications

(104 citation statements)

References 47 publications

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“…The RovA and Ler proteins have been shown to counteract H-NS-mediated silencing in Yersinia enterocolitica and E. coli, respectively (Bustamante et al, 2001;Ellison & Miller, 2006). In Salmonella, H-NS silencing of SPI-2 is antagonized by HilD or by SsrB proteins in response to different environmental conditions (Walthers et al, 2007(Walthers et al, , 2011Bustamante et al, 2008). It has been reported before that IHF antagonizes H-NS-dependent repression.…”

Section: Discussionmentioning

confidence: 99%

Integration host factor alleviates H-NS silencing of the Salmonella enterica serovar Typhimurium master regulator of SPI1, hilA

et al. 2011

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Coordination of the expression of Salmonella enterica invasion genes on Salmonella pathogenicity island 1 (SPI1) depends on a complex circuit involving several regulators that converge on expression of the hilA gene, which encodes a transcriptional activator (HilA) that modulates expression of the SPI1 virulence genes. Two of the global regulators that influence hilA expression are the nucleoid-associated proteins Hha and H-NS. They interact and form a complex that modulates gene expression. A chromosomal transcriptional fusion was constructed to assess the effects of these modulators on hilA transcription under several environmental conditions as well as at different stages of growth. The results obtained showed that these proteins play a role in silencing hilA expression at both low temperature and low osmolarity, irrespective of the growth phase. H-NS accounts for the main repressor activity. At high temperature and osmolarity, H-NS-mediated silencing completely ceases when cells enter the stationary phase, and hilA expression is induced. Mutants lacking IHF did not induce hilA in cells entering the stationary phase, and this lack of induction was dependent on the presence of H-NS. Band-shift assays and in vitro transcription data showed that for hilA induction under certain growth conditions, IHF is required to alleviate H-NS-mediated silencing.

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Section: Discussionmentioning

confidence: 99%

Integration host factor alleviates H-NS silencing of the Salmonella enterica serovar Typhimurium master regulator of SPI1, hilA

et al. 2011

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“…The ability of H-NS to influence nucleoid structure and gene expression at the level of transcription initiation has been variously attributed to its different yet inter-related mechanistic properties, including those of high-affinity and low-affinity DNA binding, assembly into a polymeric scaffold, and induction of alterations in DNA architecture such as bending, bridging, stiffening, coating, looping, and supercoiling (16,20,23,32,39,61). H-NS has also been implicated in direct RNA binding and translational regulation (41).…”

Section: Discussionmentioning

confidence: 99%

“…YdgT overexpression was associated also with derepressed proU expression, suggesting that proper architecture of the polymer scaffold constituted by the H-NS family of proteins is necessary, but by itself not sufficient, for the gene silencing function (that is, gene regulation could still be defective despite the existence of a proper architecture as, for example, in the case of H-NS variants with substitutions in the DNA-binding domain). A recent report has also implicated H-NS binding in the polymerization or stiffening mode (as opposed to the bridging mode) in silencing of gene expression (61).…”

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confidence: 99%

“…The presence of the two dimerization interfaces allows H-NS to assemble (either alone or with its paralogous partner StpA [53,55,60,65,67]) into a helical polymeric scaffold around which DNA is bound (3,22). Binding of H-NS to DNA results in several structural (including supercoiling) alterations that have been variously referred to as bending, bridging, coating, looping, and stiffening of the DNA (16,20,23,32,39,61). YdgT and Hha bear structural resemblance to, and also interact with, the N-terminal oligomerization domains of H-NS and StpA; in this manner, YdgT and Hha are believed to modulate the DNA-binding and nucleoid-organizing properties of H-NS and StpA even though they do not bind DNA by themselves (23,30,33,38,42,55).…”

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confidence: 99%

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Modulation of Rho-Dependent Transcription Termination in Escherichia coli by the H-NS Family of Proteins

Saxena

Gowrishankar

2011

J Bacteriol

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Nascent transcripts in Escherichia coli that fail to be simultaneously translated are subject to a factordependent mechanism of termination (also termed a polarity) that involves the proteins Rho and NusG. In this study, we found that overexpression of YdgT suppressed the polarity relief phenotypes and restored the efficiency of termination in rho or nusG mutants. YdgT and Hha belong to the H-NS and StpA family of proteins that repress a large number of genes in Gram-negative bacteria. Variants of H-NS defective in one or the other of its two dimerization domains, but not those defective in DNA binding alone, also conferred a similar suppression phenotype in rho and nusG mutants. YdgT overexpression was associated with derepression of proU, a prototypical H-NS-silenced locus. Polarity relief conferred by rho or nusG was unaffected in a derivative completely deficient for both H-NS and StpA, although the suppression effects of YdgT or the oligomerizationdefective H-NS variants were abolished in this background. Transcription elongation rates in vivo were unaffected in any of the suppressor-bearing strains. Finally, the polarity defects of rho and nusG mutants were exacerbated by Hha and YdgT deficiency. A model is proposed that invokes a novel role for the polymeric architectural scaffold formed on DNA by H-NS and StpA independent of the gene-silencing functions of these nucleoid proteins, in modulating Rho-dependent transcription termination such that interruption of the scaffold (as obtained by expression either of the H-NS oligomerization variants or of YdgT) is associated with improved termination efficiency in the rho and nusG mutants.Translation is a cotranscriptional process in both eubacteria and archaebacteria (1,9,25,45,50), and it has been proposed that such coupling is a defining characteristic of prokaryotic life (34, 64). The maintenance of transcription-translation coupling in a prokaryotic cell would require dynamic inter-regulation between the binding and progression of a pioneer ribosome on the nascent transcript on the one hand and the rate of transcription elongation on the other (9, 45); however, the detailed mechanisms by which such regulation is achieved are not known. Furthermore, in bacteria such as Escherichia coli, nascent transcripts that are not simultaneously translated are subject to a mechanism of factor-dependent transcription termination (also referred to as transcriptional polarity) (reviewed in references 1, 6, 15, 40, 44, 47, and 52), so that the occurrence of translation-uncoupled transcription is minimized within the cells (11, 43).Factor-dependent (also called Rho-dependent) transcription termination is mediated by, among others, the Rho and NusG proteins (1,6,15,39,40,44,47,52). Although the structures of the two proteins have been determined and several of their biochemical properties have been characterized, the precise mechanisms of their action in transcription termination remain unclear, even controversial. Rho is an RNAbinding protein and possesses RNA-dependent ATPa...

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“…The protein can bind to a nucleation site and then spread along the DNA through a mechanism that can also involve the formation of DNA-protein-DNA bridges, where each of the DNA binding domains of the dimer can associate with a separate DNA molecule or spatially separate portions of the same DNA molecule (2,16,17,25,45,79). The binding and spreading and/or bridging activities lend themselves to transcriptional silencing by either excluding RNA polymerase from a promoter or trapping RNA polymerase at a promoter, preventing transcription initiation (15,65,77). The resulting repressive nucleoprotein complex can then be disrupted by a wide variety of mechanisms, many of which rely on DNA binding proteins that target either the same sites in DNA as those of H-NS or adjacent ones such that H-NS fails to maintain its repressive relationship with the target promoter.…”

mentioning

confidence: 99%

Rational Design of an Artificial Genetic Switch: Co-Option of the H-NS-Repressed proU Operon by the VirB Virulence Master Regulator

Kane

Dorman

2011

J Bacteriol

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The H-NS protein represses the transcription of hundreds of genes in Gram-negative bacteria. Derepression is achieved by a multitude of mechanisms, many of which involve the binding of a protein to DNA at the repressed promoter in a manner that compromises the maintenance of the H-NS-DNA nucleoprotein repression complex. The principal virulence gene promoters in Shigella flexneri, the cause of bacillary dysentery, are repressed by H-NS. VirB, a protein that closely resembles members of the ParB family of plasmid-partitioning proteins, derepresses the operons that encode the main structural components and the effector proteins of the S. flexneri type III secretion system. Bioinformatic analysis suggests that VirB has been co-opted into its current role as an H-NS antagonist in S. flexneri. To test this hypothesis, the potential for VirB to act as a positive regulator of proU, an operon that is repressed by H-NS, was assessed. Although VirB has no known relationship with the osmoregulated proU operon, it could relieve H-NS-mediated repression when the parS-like VirB binding site was placed appropriately upstream of the RpoD-dependent proU promoter. These results reveal the remarkable facility with which novel regulatory circuits can evolve, at least among those promoters that are repressed by H-NS.

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Salmonella enterica Response Regulator SsrB Relieves H-NS Silencing by Displacing H-NS Bound in Polymerization Mode and Directly Activates Transcription

Cited by 85 publications

References 47 publications

Integration host factor alleviates H-NS silencing of the Salmonella enterica serovar Typhimurium master regulator of SPI1, hilA

Integration host factor alleviates H-NS silencing of the Salmonella enterica serovar Typhimurium master regulator of SPI1, hilA

Modulation of Rho-Dependent Transcription Termination in Escherichia coli by the H-NS Family of Proteins

Rational Design of an Artificial Genetic Switch: Co-Option of the H-NS-Repressed proU Operon by the VirB Virulence Master Regulator

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