The ATP‐dependent ClpXP and Lon proteases regulate expression of the <i>Yersinia pestis</i> type III secretion system via regulated proteolysis of YmoA, a small histone‐like protein

Jackson, Michael; Silva-Herzog, Eugenia; Plano, Gregory V.

doi:10.1111/j.1365-2958.2004.04353.x

Cited by 124 publications

(131 citation statements)

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“…Furthermore, in Salmonella spp., the Lon protease degrades the transcriptional activators HilC and HilD, which are involved in the regulation of the SPI-1-encoded T3S system (539). In Yersinia spp., the Lon protease and the ATP-dependent ClpXP protease degrade a small histone-like protein designated YmoA, which represses the expression of T3S genes (246). In conclusion, these findings suggest that the Lon protease is involved in the regulation of T3S gene expression in both plant-and animal-pathogenic bacteria.…”

Section: Regulation Of T3s Gene Expression In P Syringae By the Regumentioning

confidence: 71%

Protein Export According to Schedule: Architecture, Assembly, and Regulation of Type III Secretion Systems from Plant- and Animal-Pathogenic Bacteria

Büttner

2012

Microbiol Mol Biol Rev

366

482

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SUMMARY Flagellar and translocation-associated type III secretion (T3S) systems are present in most Gram-negative plant- and animal-pathogenic bacteria and are often essential for bacterial motility or pathogenicity. The architectures of the complex membrane-spanning secretion apparatuses of both systems are similar, but they are associated with different extracellular appendages, including the flagellar hook and filament or the needle/pilus structures of translocation-associated T3S systems. The needle/pilus is connected to a bacterial translocon that is inserted into the host plasma membrane and mediates the transkingdom transport of bacterial effector proteins into eukaryotic cells. During the last 3 to 5 years, significant progress has been made in the characterization of membrane-associated core components and extracellular structures of T3S systems. Furthermore, transcriptional and posttranscriptional regulators that control T3S gene expression and substrate specificity have been described. Given the architecture of the T3S system, it is assumed that extracellular components of the secretion apparatus are secreted prior to effector proteins, suggesting that there is a hierarchy in T3S. The aim of this review is to summarize our current knowledge of T3S system components and associated control proteins from both plant- and animal-pathogenic bacteria.

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Section: Regulation Of T3s Gene Expression In P Syringae By the Regumentioning

confidence: 71%

Protein Export According to Schedule: Architecture, Assembly, and Regulation of Type III Secretion Systems from Plant- and Animal-Pathogenic Bacteria

Büttner

2012

Microbiol Mol Biol Rev

366

482

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“…Recently, Jackson et al (21) demonstrated that ClpXP and another ATP-dependent protease, Lon, together control TTSS expression by regulating the stability of a small histone-like protein, YmoA, in Yersinia pestis. YmoA is a homologue of E. coli Hha protein, which has been reported to regulate LEE expression through Ler in EHEC (46).…”

Section: Discussionmentioning

confidence: 99%

ClpXP Protease Controls Expression of the Type III Protein Secretion System through Regulation of RpoS and GrlR Levels in EnterohemorrhagicEscherichia coli

2005

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Expression of the type III protein secretion system (TTSS), encoded in the locus of enterocyte effacement (LEE) of enterohemorrhagic Escherichia coli (EHEC), has been shown to be controlled by various regulators. In a search for additional regulatory genes, we identified a DNA fragment containing clpX and clpP that has a positive regulatory effect on LEE expression in EHEC O157. The expression of LEE-encoded Esp proteins was significantly reduced in a clpXP deletion mutant. Deletion of grlR, a negative regulatory gene within LEE, markedly increased LEE expression even in the clpXP mutant. To verify the regulatory mechanism of GrlR expression, a chromosomal epitope-tagged allele of grlR (grlR-FLAG) was constructed. GrlR-FLAG expression was increased significantly in the clpXP deletion mutant, suggesting that the GrlR level is under the control of ClpXP, and this regulation is critical for the ClpXP-dependent expression of LEE in EHEC. Deletion of rpoS, the gene encoding a stationary-phase-inducing sigma factor that is a substrate for ClpXP protease, partially restored LEE expression in the clpXP mutant. A multicopy plasmid carrying rpoS strongly repressed expression of Esp proteins, suggesting that positive regulation by ClpXP is partially mediated through a negative effect of RpoS on LEE expression. We also found that rpoS deletion induces transcription of pchA, which encodes one of the positive regulators for LEE expression in EHEC. These results suggest that ClpXP controls expression of LEE through the regulation of RpoS and GrlR levels in EHEC.Enterohemorrhagic Escherichia coli (EHEC) strains are lifethreatening human pathogens and cause hemorrhagic colitis, bloody diarrhea, and hemolytic uremic syndrome (40). EHEC is a member of the attaching and effacing pathogens (40, 56), a group that includes enteropathogenic E. coli (EPEC) (39) and the mouse pathogen Citrobacter rodentium (45). The attaching/effacing lesion on intestinal epithelial cells is characterized by destruction of microvilli and formation of a pedestal-like structure, triggered by rearrangement of cytoskeletal proteins (30, 42). The genes essential for causing the attaching/ effacing lesion are encoded in a pathogenicity island designated the locus of enterocyte effacement (LEE). LEE consists of more than 40 genes organized into five major operons, designated LEE1 to LEE5 (6,8,43). LEE1, -2 and -3 operons contain mostly genes encoding the structural and auxiliary proteins necessary for formation of a dedicated type III protein secretion system (TTSS) (22). The LEE4 operon encodes several secreted proteins (e.g., EspA, EspB, EspD, and EspF), all of which are secreted through TTSS (28, 29, 34, 37). The LEE5 operon encodes an adhesion factor, designated intimin (23, 24), and Tir, a protein that is also translocated through TTSS and acts as a receptor for intimin at the host cell membrane (27).A transcriptional activator, Ler, is encoded by the first gene of the LEE1 operon and is essential for the expression of almost all LEE genes (9, 38). Deng et...

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“…In addition, growth at 37°C permits the transcription and translation of LcrF, the master transcriptional activator of T3SS genes. Transcription of lcrF is prohibited at lower temperatures by DNA bends in its promoter and through association with the nucleoidassociated protein YmoA; upon temperature upshift, YmoA is degraded by Clp/Lon proteases to alleviate the transcriptional repression of the yscW-lcrF operon (13,14). Furthermore, synthesis of the LcrF protein is repressed by a two-stem-loop structure in the transcript that sequesters the ribosome binding site (RBS) at 26°C, which then melts at 37°C as part of a thermosensing mechanism (15).…”

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confidence: 99%

Genome-Wide Analysis of Small RNAs Expressed by Yersinia pestis Identifies a Regulator of the Yop-Ysc Type III Secretion System

et al. 2014

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bSmall noncoding RNA (sRNA) molecules are integral components of the regulatory machinery for many bacterial species and are known to posttranscriptionally regulate metabolic and stress-response pathways, quorum sensing, virulence factors, and more. The Yop-Ysc type III secretion system (T3SS) is a critical virulence component for the pathogenic Yersinia species, and the regulation of this system is tightly controlled at each step from transcription to translocation of effectors into host cells. The contribution of sRNAs to the regulation of the T3SS in Yersinia has been largely unstudied, however. Previously, our lab identified a role for the sRNA chaperone protein Hfq in the regulation of components of the T3SS in the gastrointestinal pathogen Yersinia pseudotuberculosis. Here we present data demonstrating a similar requirement for Hfq in the closely related species Yersinia pestis. Through deep sequencing analysis of the Y. pestis sRNA-ome, we found 63 previously unidentified putative sRNAs in this species. We identified a Yersinia-specific sRNA, Ysr141, carried by the T3SS plasmid pCD1 that is required for the production of multiple T3SS proteins. In addition, we show that Ysr141 targets an untranslated region upstream of yopJ to posttranscriptionally activate the synthesis of the YopJ protein. Furthermore, Ysr141 may be an unstable and/or processed sRNA, which could contribute to its function in the regulation of the T3SS. The discovery of an sRNA that influences the synthesis of the T3SS adds an additional layer of regulation to this tightly controlled virulence determinant of Y. pestis.

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The ATP‐dependent ClpXP and Lon proteases regulate expression of the Yersinia pestis type III secretion system via regulated proteolysis of YmoA, a small histone‐like protein

Cited by 124 publications

References 75 publications

Protein Export According to Schedule: Architecture, Assembly, and Regulation of Type III Secretion Systems from Plant- and Animal-Pathogenic Bacteria

Protein Export According to Schedule: Architecture, Assembly, and Regulation of Type III Secretion Systems from Plant- and Animal-Pathogenic Bacteria

ClpXP Protease Controls Expression of the Type III Protein Secretion System through Regulation of RpoS and GrlR Levels in EnterohemorrhagicEscherichia coli

Genome-Wide Analysis of Small RNAs Expressed by Yersinia pestis Identifies a Regulator of the Yop-Ysc Type III Secretion System

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