Bacterial nucleoid-associated proteins, nucleoid structure and gene expression

Dillon, Shane C.; Dorman, Charles J.

doi:10.1038/nrmicro2261

Cited by 768 publications

(922 citation statements)

References 124 publications

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“…This difference has been attributed, in part, to a lack of functional redundancy in Gram-positive bacteria. Unlike E. coli, which has a variety of NAPs, including H-NS, Fis, Dps and IHF, Gram-positive bacteria have a more limited repertoire (Dillon & Dorman, 2010;Grove, 2011). The P. gingivalis genome is predicted to encode 13 genes that are annotated as histone-like DNAbinding proteins, related to but longer than HU.…”

Section: Discussionmentioning

confidence: 99%

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The nucleoid-associated protein HUβ affects global gene expression in Porphyromonas gingivalis

et al. 2013

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HU is a non-sequence-specific DNA-binding protein and one of the most abundant nucleoidassociated proteins in the bacterial cell. Like Escherichia coli, the genome of Porphyromonas gingivalis is predicted to encode both the HUa (PG1258) and the HUb (PG0121) subunit. We have previously reported that PG0121 encodes a non-specific DNA-binding protein and that PG0121 is co-transcribed with the K-antigen capsule synthesis operon. We also reported that deletion of PG0121 resulted in downregulation of capsule operon expression and produced a P. gingivalis strain that is phenotypically deficient in surface polysaccharide production. Here, we show through complementation experiments in an E. coli MG1655 hupAB double mutant strain that PG0121 encodes a functional HU homologue. Microarray and quantitative RT-PCR analysis were used to further investigate global transcriptional regulation by HUb using comparative expression profiling of the PG0121 (HUb) mutant strain to the parent strain, W83. Our analysis determined that expression of genes encoding proteins involved in a variety of biological functions, including iron acquisition, cell division and translation, as well as a number of predicted nucleoid associated proteins were altered in the PG0121 mutant. Phenotypic and quantitative real-time-PCR (qRT-PCR) analyses determined that under iron-limiting growth conditions, cell division and viability were defective in the PG0121 mutant. Collectively, our studies show that PG0121 does indeed encode a functional HU homologue, and HUb has global regulatory functions in P. gingivalis; it affects not only production of capsular polysaccharides but also expression of genes involved in basic functions, such as cell wall synthesis, cell division and iron uptake. INTRODUCTIONPorphyromonas gingivalis is a Gram-negative obligate anaerobe belonging to the family Bacteroidaceae that persists as a natural member of the human oral microbiota. A shift in the microbial community leading to outgrowth of this anaerobe is directly linked to periodontitis, a chronic inflammatory disease that leads to destruction of the tissues supporting the gums and ultimately, exfoliation of the teeth (Choil et al., 1990;Dzink et al., 1988;Grossi et al., 1994;Lamont & Jenkinson, 2000;Moore et al., 1991). This commensal can colonize, invade and multiply within gingival epithelial cells, as well as penetrate into deeper epithelial cell layers, potentially releasing the whole organism and/or virulence factors into the bloodstream (reviewed by Yilmaz, 2008). In addition to its ability to cause disease in the oral cavity, there are data indicating a role in systemic disease, including its ability to invade vascular endothelial cells (Dorn et al., 2000(Dorn et al., , 2002Jandik et al., 2008) and to cause aggregation of platelets (Pham et al., 2002). For many pathogenic bacteria, surface polysaccharides play a key role in immune modulation et al., 1996). HU typically acts as an accessory protein in virtually all types of nucleoprotein-mediated processes (reviewed by...

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Section: Discussionmentioning

confidence: 99%

“…The prokaryotic nucleoid is a defined, yet dynamic, structure, organized by complex interactions with nucleoid-associated proteins (NAPs) (Dillon & Dorman, 2010). HU protein is one of the most abundant NAPs in the bacterial cell.…”

Section: Introductionmentioning

confidence: 99%

The nucleoid-associated protein HUβ affects global gene expression in Porphyromonas gingivalis

et al. 2013

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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%

“…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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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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Structural similarities and differences in H‐NS family proteins revealed by the N‐terminal structure of TurB in Pseudomonas putida KT2440

et al. 2016

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H-NS family proteins play key roles in bacterial nucleoid compaction and global transcription. MvaT homologues in Pseudomonas have almost negligible amino acid sequence identity with H-NS, but can complement an hns-related phenotype of Escherichia coli. Here, we report the crystal structure of the N-terminal dimerization/oligomerization domain of TurB, an MvaT homologue in Pseudomonas putida KT2440. Our data identify two dimerization sites; the structure of the central dimerization site is almost the same as the corresponding region of H-NS, whereas the terminal dimerization sites are different. Our results reveal similarities and differences in dimerization and oligomerization mechanisms between H-NS and TurB.

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Bacterial nucleoid-associated proteins, nucleoid structure and gene expression

Cited by 768 publications

References 124 publications

The nucleoid-associated protein HUβ affects global gene expression in Porphyromonas gingivalis

The nucleoid-associated protein HUβ affects global gene expression in Porphyromonas gingivalis

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

Structural similarities and differences in H‐NS family proteins revealed by the N‐terminal structure of TurB in Pseudomonas putida KT2440

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