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Transcription factor ?B plays an important role in the production of extracellular membrane-derived vesicles in Listeria monocytogenes.

ABSTRACT: Gram-negative bacteria produce extracellular outer membrane vesicles (OMVs) that interact with host cells. Unlike Gram-negative bacteria, less is known about the production and role of extracellular membrane vesicles (MVs) in Gram-positive bacteria. The food-borne pathogen Listeria monocytogenes can survive under extreme environmental and energy stress conditions and the transcription factor ?(B) is involved in this survival ability. Here, we first determined the production of MVs from L. monocytogenes and evaluated whether general stress transcription factor ?(B) affected production of MVs in L. monocytogenes. L. monocytogenes secreted MVs during in vitro broth culture. The wild-type strain actively produced MVs approximately nine times more and also produced more intact shapes of MVs than those of the isogenic ?sigB mutant. A proteomic analysis showed that 130 and 89 MV proteins were identified in the wild-type and ?sigB mutant strains, respectively. Wild-type strain-derived MVs contained proteins regulated by ?(B) such as transporters (OpuCA and OpuCC), stress response (Kat), metabolism (LacD), translation (InfC), and cell division protein (FtsZ). Gene Ontology (GO) enrichment analysis showed that wild-type-derived MV proteins corresponded to several GO terms, including response to stress (heat, acid, and bile resistance) and extracellular polysaccharide biosynthetic process, but not the ?sigB mutant. Internalin B (InlB) was almost three times more contained in MVs derived from the wild-type strain than in MVs derived from the ?sigB mutant. Taken together, these results suggest that ?(B) plays a pivotal role in the production of MVs and protein profiles contained in MVs. L. monocytogenes MVs may contribute to host infection and survival ability under various stressful conditions.

SUBMITTER: Lee JH

PROVIDER: S-EPMC3748028 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Transcription factor σB plays an important role in the production of extracellular membrane-derived vesicles in Listeria monocytogenes.

Lee Jung Hwa JH Choi Chi-Won CW Lee Taewon T Kim Seung Il SI Lee Je-Chul JC Shin Ji-Hyun JH

PloS one 20130820 8

Gram-negative bacteria produce extracellular outer membrane vesicles (OMVs) that interact with host cells. Unlike Gram-negative bacteria, less is known about the production and role of extracellular membrane vesicles (MVs) in Gram-positive bacteria. The food-borne pathogen Listeria monocytogenes can survive under extreme environmental and energy stress conditions and the transcription factor σ(B) is involved in this survival ability. Here, we first determined the production of MVs from L. monocy ...[more]

PMID: 23977379

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Project description:UnlabelledThe stress-responsive alternative sigma factor σ(B) is conserved across diverse Gram-positive bacterial genera. In Listeria monocytogenes, σ(B) regulates transcription of >150 genes, including genes contributing to virulence and to bacterial survival under host-associated stress conditions, such as those encountered in the human gastrointestinal lumen. An inhibitor of L. monocytogenes σ(B) activity was identified by screening ~57,000 natural and synthesized small molecules using a high-throughput cell-based assay. The compound fluoro-phenyl-styrene-sulfonamide (FPSS) (IC(50) = 3.5 µM) downregulated the majority of genes previously identified as members of the σ(B) regulon in L. monocytogenes 10403S, thus generating a transcriptional profile comparable to that of a 10403S ΔsigB strain. Specifically, of the 208 genes downregulated by FPSS, 75% had been identified previously as positively regulated by σ(B). Downregulated genes included key virulence and stress response genes, such as inlA, inlB, bsh, hfq, opuC, and bilE. From a functional perspective, FPSS also inhibited L. monocytogenes invasion of human intestinal epithelial cells and bile salt hydrolase activity. The ability of FPSS to inhibit σ(B) activity in both L. monocytogenes and Bacillus subtilis indicates its utility as a specific inhibitor of σ(B) across multiple Gram-positive genera.ImportanceThe σ(B) transcription factor regulates expression of genes responsible for bacterial survival under changing environmental conditions and for virulence; therefore, this alternative sigma factor is important for transmission of L. monocytogenes and other Gram-positive bacteria. Regulation of σ(B) activity is complex and tightly controlled, reflecting the key role of this factor in bacterial metabolism. We present multiple lines of evidence indicating that fluoro-phenyl-styrene-sulfonamide (FPSS) specifically inhibits activity of σ(B) across Gram-positive bacterial genera, i.e., in both Listeria monocytogenes and Bacillus subtilis. Therefore, FPSS is an important new tool that will enable novel approaches for exploring complex regulatory networks in L. monocytogenes and other Gram-positive pathogens and for investigating small-molecule applications for controlling pathogen transmission.

Dataset Information

Transcription factor ?B plays an important role in the production of extracellular membrane-derived vesicles in Listeria monocytogenes.

Publications

Transcription factor σB plays an important role in the production of extracellular membrane-derived vesicles in Listeria monocytogenes.

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