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A role for the leucine-responsive regulatory protein and integration host factor in the regulation of the Salmonella plasmid virulence (spv) locus in Salmonella typhimurium.
Mol Microbiol. 1999 Oct; 34(1):134-45.MM

Abstract

The Salmonella plasmid virulence (spv) genes of Salmonella typhimurium are activated at the level of transcription as the bacteria enter stationary phase in vitro or in response to signals received during intracellular growth. Activation requires the LysR-like transcription factor SpvR and the alternative sigma factor RpoS. In this report, we show by biochemical and genetic analyses that two chromosomally encoded DNA-binding proteins contribute to the control of spv expression. These are the integration host factor (IHF), which binds to DNA sequences upstream of the spvR regulatory gene, and the leucine-responsive regulatory protein (Lrp), which binds to sequences upstream of the spvABCD operon. Under all conditions tested, inactivation of IHF expression reduces the level of spvR transcription by twofold. It also alters the response of the spv regulon to loss of DNA gyrase activity, consistent with a role for IHF in organizing DNA structure in the vicinity of the spvR promoter. Lrp represses spvA gene expression by up to fivefold and Lrp-mediated repression is antagonized by leucine. The Lrp binding site upstream of the spvA gene overlaps one of the binding sites for the positive regulator SpvR, suggesting a mechanism by which Lrp repression is exerted. This is a first demonstration of a role for Lrp in controlling genes that are also subject to intracellular regulation. These data show that the spv virulence genes belong simultaneously to several regulons in the cell, raising the possibility that spv expression can be fine-tuned in response to multiple environmental inputs.

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Authors+Show Affiliations

Marshall DG
Department of Microbiology, Moyne Institute of Preventive Medicine, University of Dublin, Trinity College, Dublin 2, Ireland.
Sheehan BJ
No affiliation info available
Dorman CJ
No affiliation info available

MeSH

Bacterial ProteinsDNA Topoisomerases, Type IIDNA, BacterialDNA-Binding ProteinsGene Expression Regulation, BacterialIntegration Host FactorsLeucineLeucine-Responsive Regulatory ProteinPlasmidsRegulatory Sequences, Nucleic AcidRepressor ProteinsSalmonella typhimuriumTranscription FactorsTranscription, GeneticVirulence

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

10540292

Citation

Marshall, D G., et al. "A Role for the Leucine-responsive Regulatory Protein and Integration Host Factor in the Regulation of the Salmonella Plasmid Virulence (spv) Locus in Salmonella Typhimurium." Molecular Microbiology, vol. 34, no. 1, 1999, pp. 134-45.
Marshall DG, Sheehan BJ, Dorman CJ. A role for the leucine-responsive regulatory protein and integration host factor in the regulation of the Salmonella plasmid virulence (spv) locus in Salmonella typhimurium. Mol Microbiol. 1999;34(1):134-45.
Marshall, D. G., Sheehan, B. J., & Dorman, C. J. (1999). A role for the leucine-responsive regulatory protein and integration host factor in the regulation of the Salmonella plasmid virulence (spv) locus in Salmonella typhimurium. Molecular Microbiology, 34(1), 134-45.
Marshall DG, Sheehan BJ, Dorman CJ. A Role for the Leucine-responsive Regulatory Protein and Integration Host Factor in the Regulation of the Salmonella Plasmid Virulence (spv) Locus in Salmonella Typhimurium. Mol Microbiol. 1999;34(1):134-45. PubMed PMID: 10540292.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - A role for the leucine-responsive regulatory protein and integration host factor in the regulation of the Salmonella plasmid virulence (spv) locus in Salmonella typhimurium. AU - Marshall,D G, AU - Sheehan,B J, AU - Dorman,C J, PY - 1999/12/14/pubmed PY - 1999/12/14/medline PY - 1999/12/14/entrez SP - 134 EP - 45 JF - Molecular microbiology JO - Mol Microbiol VL - 34 IS - 1 N2 - The Salmonella plasmid virulence (spv) genes of Salmonella typhimurium are activated at the level of transcription as the bacteria enter stationary phase in vitro or in response to signals received during intracellular growth. Activation requires the LysR-like transcription factor SpvR and the alternative sigma factor RpoS. In this report, we show by biochemical and genetic analyses that two chromosomally encoded DNA-binding proteins contribute to the control of spv expression. These are the integration host factor (IHF), which binds to DNA sequences upstream of the spvR regulatory gene, and the leucine-responsive regulatory protein (Lrp), which binds to sequences upstream of the spvABCD operon. Under all conditions tested, inactivation of IHF expression reduces the level of spvR transcription by twofold. It also alters the response of the spv regulon to loss of DNA gyrase activity, consistent with a role for IHF in organizing DNA structure in the vicinity of the spvR promoter. Lrp represses spvA gene expression by up to fivefold and Lrp-mediated repression is antagonized by leucine. The Lrp binding site upstream of the spvA gene overlaps one of the binding sites for the positive regulator SpvR, suggesting a mechanism by which Lrp repression is exerted. This is a first demonstration of a role for Lrp in controlling genes that are also subject to intracellular regulation. These data show that the spv virulence genes belong simultaneously to several regulons in the cell, raising the possibility that spv expression can be fine-tuned in response to multiple environmental inputs. SN - 0950-382X UR - https://www.unboundmedicine.com/medline/citation/10540292/A_role_for_the_leucine_responsive_regulatory_protein_and_integration_host_factor_in_the_regulation_of_the_Salmonella_plasmid_virulence__spv__locus_in_Salmonella_typhimurium_ L2 - https://onlinelibrary.wiley.com/resolve/openurl?genre=article&sid=nlm:pubmed&issn=0950-382X&date=1999&volume=34&issue=1&spage=134 DB - PRIME DP - Unbound Medicine ER -