Autoregulation is Essential for Precise Temporal and Steady-state Regulation by the Bordetella BvgAS Phosphorelay

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 2006 Dec 13

PMID 17158656

Citations 23

Authors

Corinne L Williams

Peggy A Cotter

Affiliations

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Abstract

The Bordetella BvgAS virulence control system is prototypical of phosphorelays that use a polydomain sensor and a response regulator to control gene expression in response to environmental cues. BvgAS controls the expression of at least three distinct phenotypic phases (Bvg(-), Bvg(i), and Bvg(+)) by differentially regulating the expression of at least four classes of genes. Among the loci regulated by BvgAS is bvgAS itself. We investigated the role of autoregulation in the ability of BvgAS to control multiple gene expression patterns in a temporal and steady-state manner by constructing Bordetella bronchiseptica strains in which the bvgAS promoter was replaced with constitutively active promoters. Our results show that positive autoregulation of bvgAS transcription is required for the temporal expression of multiple phenotypic phases that occurs in response to a shift from Bvg(-)-phase conditions to Bvg(+)-phase conditions. Autoregulation was also shown to contribute to steady-state regulation; it influences the sensitivity of the system in response to subtle differences in signal intensity. In addition, considered in relation to BvgA and BvgS activities demonstrated in vitro, our results provide insight into how BvgA and BvgS function mechanistically.

Citing Articles

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A balancing act in transcription regulation by response regulators: titration of transcription factor activity by decoy DNA binding sites.

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Two Component Regulatory Systems and Antibiotic Resistance in Gram-Negative Pathogens.

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Quantifying dynamic mechanisms of auto-regulation in Escherichia coli with synthetic promoter in response to varying external phosphate levels.

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References

De Wulf P, Kwon O, Lin E . The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of unanticipated target operons. J Bacteriol. 1999; 181(21):6772-8. PMC: 94143. DOI: 10.1128/JB.181.21.6772-6778.1999. View

Zu T, Manetti R, Rappuoli R, Scarlato V . Differential binding of BvgA to two classes of virulence genes of Bordetella pertussis directs promoter selectivity by RNA polymerase. Mol Microbiol. 1996; 21(3):557-65. DOI: 10.1111/j.1365-2958.1996.tb02564.x. View

Stock A, Robinson V, Goudreau P . Two-component signal transduction. Annu Rev Biochem. 2000; 69:183-215. DOI: 10.1146/annurev.biochem.69.1.183. View

Stockbauer K, Fuchslocher B, Miller J, Cotter P . Identification and characterization of BipA, a Bordetella Bvg-intermediate phase protein. Mol Microbiol. 2000; 39(1):65-78. DOI: 10.1046/j.1365-2958.2001.02191.x. View

Boucher P, Yang M, Schmidt D, Stibitz S . Genetic and biochemical analyses of BvgA interaction with the secondary binding region of the fha promoter of Bordetella pertussis. J Bacteriol. 2001; 183(2):536-44. PMC: 94909. DOI: 10.1128/JB.183.2.536-544.2001. View

Groisman E . The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol. 2001; 183(6):1835-42. PMC: 95077. DOI: 10.1128/JB.183.6.1835-1842.2001. View

Deora R, Bootsma H, Miller J, Cotter P . Diversity in the Bordetella virulence regulon: transcriptional control of a Bvg-intermediate phase gene. Mol Microbiol. 2001; 40(3):669-83. DOI: 10.1046/j.1365-2958.2001.02415.x. View

Boucher P, Maris A, Yang M, Stibitz S . The response regulator BvgA and RNA polymerase alpha subunit C-terminal domain bind simultaneously to different faces of the same segment of promoter DNA. Mol Cell. 2003; 11(1):163-73. DOI: 10.1016/s1097-2765(03)00007-8. View

Fuchslocher B, Millar L, Cotter P . Comparison of bipA alleles within and across Bordetella species. Infect Immun. 2003; 71(6):3043-52. PMC: 155730. DOI: 10.1128/IAI.71.6.3043-3052.2003. View

10.

Cotter P, Jones A . Phosphorelay control of virulence gene expression in Bordetella. Trends Microbiol. 2003; 11(8):367-73. DOI: 10.1016/s0966-842x(03)00156-2. View

11.

STAINER D, Scholte M . A simple chemically defined medium for the production of phase I Bordetella pertussis. J Gen Microbiol. 1970; 63(2):211-20. DOI: 10.1099/00221287-63-2-211. View

12.

Idigbe E, Parton R, Wardlaw A . Rapidity of antigenic modulation of Bordetella pertussis in modified Hornibrook medium. J Med Microbiol. 1981; 14(4):409-18. DOI: 10.1099/00222615-14-4-409. View

13.

McPheat W, Wardlaw A, Novotny P . Modulation of Bordetella pertussis by nicotinic acid. Infect Immun. 1983; 41(2):516-22. PMC: 264671. DOI: 10.1128/iai.41.2.516-522.1983. View

14.

Vieira J, Messing J . Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985; 33(1):103-19. DOI: 10.1016/0378-1119(85)90120-9. View

15.

Arico B, Rappuoli R . Bordetella parapertussis and Bordetella bronchiseptica contain transcriptionally silent pertussis toxin genes. J Bacteriol. 1987; 169(6):2847-53. PMC: 212198. DOI: 10.1128/jb.169.6.2847-2853.1987. View

16.

Miller V, Mekalanos J . A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol. 1988; 170(6):2575-83. PMC: 211174. DOI: 10.1128/jb.170.6.2575-2583.1988. View

17.

Gross R, Rappuoli R . Positive regulation of pertussis toxin expression. Proc Natl Acad Sci U S A. 1988; 85(11):3913-7. PMC: 280330. DOI: 10.1073/pnas.85.11.3913. View

18.

Relman D, Domenighini M, Tuomanen E, Rappuoli R, Falkow S . Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc Natl Acad Sci U S A. 1989; 86(8):2637-41. PMC: 286972. DOI: 10.1073/pnas.86.8.2637. View

19.

Miller J, Roy C, Falkow S . Analysis of Bordetella pertussis virulence gene regulation by use of transcriptional fusions in Escherichia coli. J Bacteriol. 1989; 171(11):6345-8. PMC: 210509. DOI: 10.1128/jb.171.11.6345-6348.1989. View

20.

Domenighini M, Relman D, Capiau C, Falkow S, Prugnola A, Scarlato V . Genetic characterization of Bordetella pertussis filamentous haemagglutinin: a protein processed from an unusually large precursor. Mol Microbiol. 1990; 4(5):787-800. DOI: 10.1111/j.1365-2958.1990.tb00649.x. View