Autoregulation is essential for precise temporal and steady-state regulation by the Bordetella BvgAS phosphorelay

Journal of Bacteriology

Volumn 189, Issue 5, 2007, Pages 1974-1982

  Williams, Corinne L ^a   Cotter, Peggy A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; COMPLEMENTARY DNA; RNA; RNA POLYMERASE; SIGMA FACTOR; VIRULENCE FACTOR;

ARTICLE; AUTOREGULATION; BACTERIAL GENE; BACTERIAL VIRULENCE; BORDETELLA; BORDETELLA BRONCHISEPTICA; BVGAS GENE; DNA SYNTHESIS; ENZYME ASSAY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; REAL TIME POLYMERASE CHAIN REACTION; STEADY STATE; STRAIN DIFFERENCE;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BORDETELLA BRONCHISEPTICA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HOMEOSTASIS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

BORDETELLA; BORDETELLA BRONCHISEPTICA;

EID: 33947394044     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01684-06     Document Type: Article

References (52)

1. Akerley, B. J., P. A. Cotter, and J. F. Miller. 1995. Ectopic expression of the flagellar regulon alters development of the Bordetella-host interaction. Cell 80:611-620.
2. Akerley, B. J., and J. F. Miller. 1993. Flagellin gene transcription in Bordetella bronchiseptica is regulated by the BvgAS virulence control system. J. Bacteriol. 175:3468-3479.
3. Arico, B., and R. Rappuoli. 1987. Bordetella parapertussis and Bordetella bronchiseptica contain transcriptionally silent pertussis toxin genes. J. Bacteriol. 169:2847-2853.
4. Beier, D., and R. Gross. 2006. Regulation of bacterial virulence by two-component systems. Curr. Opin. Microbiol. 9:143-152.
5. Boucher, P. E., A. E. Maris, M. S. Yang, and S. Stibitz. 2003. 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 11:163-173.
6. Boucher, P. E., F. D. Menozzi, and C. Locht. 1994. The modular architecture of bacterial response regulators. Insights into the activation mechanism of the BvgA transactivator of Bordetella pertussis. J. Mol. Biol. 241:363-377.
7. Boucher, P. E., K. Murakami, A. Ishihama, and S. Stibitz. 1997. Nature of DNA binding and RNA polymerase interaction of the Bordetella pertussis BvgA transcriptional activator at the fha promoter. J. Bacteriol. 179:1755-1763.
8. Boucher, P. E., M. S. Yang, D. M. Schmidt, and S. Stibitz. 2001. Genetic and biochemical analyses of BvgA interaction with the secondary binding region of the fha promoter of Bordetella pertussis. J. Bacteriol. 183:536-544.
9. Cherry, J. D. 1999. Epidemiological, clinical, and laboratory aspects of pertussis in adults. Clin. Infect. Dis. 28(Suppl. 2):S112-S117.
10. Cotter, P. A., and A. M. Jones. 2003. Phosphorelay control of virulence gene expression in Bordetella. Trends Microbiol. 11:367-373.
11. Cotter, P. A., and J. F. Miller. 2001. Bordetella, p. 619-674. In E. A. Groisman (ed.), Principles of bacterial pathogenesis. Academic Press, San Diego, CA.
12. Cotter, P. A., and J. F. Miller. 1994. BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect. Immun. 62:3381-3390.
13. Cotter, P. A., and J. F. Miller. 1997. A mutation in the Bordetella bronchiseptica bvgS gene results in reduced virulence and increased resistance to starvation, and identifies a new class of Bvg-regulated antigens. Mol. Microbiol. 24:671-685.
14. Cummings, C. A., H. J. Bootsma, D. A. Relman, and J. F. Miller. 2006. Species- and strain-specific control of a complex, flexible regulon by Bordetella BvgAS. J. Bacteriol. 188:1775-1785.
15. Deora, R., H. J. Bootsma, J. F. Miller, and P. A. Cotter. 2001. Diversity in the Bordetella virulence regulon: transcriptional control of a Bvg-intermediate phase gene. Mol. Microbiol. 40:669-683.
16. De Wulf, P., O. Kwon, and E. C. Lin. 1999. The CpxRA signal transduction system of Escherichia coli: growth-related autoactivation and control of un-anticipated target operons. J. Bacteriol. 181:6772- 6778.
17. Domenighini, M., D. Relman, C. Capiau, S. Falkow, A. Prugnola, V. Scarlato, and R. Rappuoli. 1990. Genetic characterization of Bordetella pertussis filamentous haemagglutinin: a protein processed from an unusually large precursor. Mol. Microbiol. 4:787-800.
18. Fuchslocher, B., L. L. Millar, and P. A. Cotter. 2003. Comparison of bipA alleles within and across Bordetella species. Infect. Immun. 71:3043-3052.
19. Fujita, M., and R. Losick. 2005. Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev. 19:2236-2244.
20. Groisman, E. A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183:1835-1842.
21. Gross, R., and R. Rappuoli. 1988. Positive regulation of pertussis toxin expression. Proc. Natl. Acad. Sci. USA 85:3913-3917.
22. Hoch, J. A. 1991. Spo0 genes, the phosphorelay, and the initiation of sporulation, p. 747-755. In A. L. Sonenshein et al. (ed.), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, DC.
23. Idigbe, E. O., R. Parton, and A. C. Wardlaw. 1981. Rapidity of antigenic modulation of Bordetella pertussis in modified Hornibrook medium. J. Med. Microbiol. 14:409-418.
24. Jacob-Dubuisson, F., B. Kehoe, E. Willery, N. Reveneau, C. Locht, and D. A. Relman. 2000. Molecular characterization of Bordetella bronchiseptica filamentous haemagglutinin and its secretion machinery. Microbiology 146:1211-1221.
25. Jones, A. M., P. E. Boucher, C. L. Williams, S. Stibitz, and P. A. Cotter. 2005. Role of BvgA phosphorylation and DNA binding affinity in control of Bvg-mediated phenotypic phase transition in Bordetella pertussis. Mol. Microbiol. 58:700-713.
26. Julio, S. M., and P. A. Cotter. 2005. Characterization of the filamentous hemagglutinin-like protein FhaS in Bordetella bronchiseptica. Infect. Immun. 73:4960-4971.
27. Karimova, G., J. Bellalou, and A. Ullmann. 1996. Phosphorylation-dependent binding of BvgA to the upstream region of the cyaA gene of Bordetella pertussis. Mol. Microbiol. 20:489-496.
28. Kasuga, T., Y. Nakase, K. Ukishima, and K. Takatsu. 1954. Studies on Haemophilus pertussis. V. Relation between the phase of bacilli and the progress of the whooping-cough. Kitasato Arch. Exp. Med. 27:57-62.
29. - phase nor the vrg6 locus of Bordetella pertussis is required for respiratory infection in mice. Infect. Immun. 66:2762-2768.
30. Martinez de Tejada, G., J. F. Miller, and P. A. Cotter. 1996. Comparative analysis of the virulence control systems of Bordetella pertussis and Bordetella bronchiseptica. Mol. Microbiol. 22:895-908.
31. McPheat, W. L., A. C. Wardlaw, and P. Novotny. 1983. Modulation of Bordetella pertussis by nicotinic acid. Infect. Immun. 41:516-522.
32. Miller, J. F., C. R. Roy, and S. Falkow. 1989. Analysis of Bordetella pertussis virulence gene regulation by use of transcriptional fusions in Escherichia coli. J. Bacteriol. 171:6345-6348.
33. Miller, V. L., and J. J. Mekalanos. 1988. 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. 170:2575-2583.
34. Relman, D. A., M. Domenighini, E. Tuomanen, R. Rappuoli, and S. Falkow. 1989. Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc. Natl. Acad. Sci. USA 86:2637-2641.
35. Sambrook, J., E. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Scarlato, V., B. Arico, A. Prugnola, and R. Rappuoli. 1991. Sequential activation and environmental regulation of virulence genes in Bordetella pertussis. EMBO J. 10:3971-3975.
37. Scarlato, V., A. Prugnola, B. Arico, and R. Rappuoli. 1990. Positive transcriptional feedback at the bvg locus controls expression of virulence factors in Bordetella pertussis. Proc. Natl. Acad. Sci. USA 87:6753-6757.
38. 4 modulation. J. Bacteriol. 173:7401-7404.
39. Soncini, F. C., E. G. Vescovi, and E. A. Groisman. 1995. Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J. Bacteriol. 177:4364-4371.
40. Stainer, D. W., and M. J. Scholte. 1970. A simple chemically defined medium for the production of phase I Bordetella pertussis. J. Gen. Microbiol. 63:211-220.
41. Steffen, P., S. Goyard, and A. Ullmann. 1996. Phosphorylated BvgA is sufficient for transcriptional activation of virulence-regulated genes in Bordetella pertussis. EMBO J. 15:102-109.
42. Stock, A. M., V. L. Robinson, and P. N. Goudreau. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183-215.
43. Stockbauer, K. E., B. Fuchslocher, J. F. Miller, and P. A. Cotter. 2001. Identification and characterization of BipA, a Bordetella Bvg-intermediate phase protein. Mol. Microbiol. 39:65-78.
44. Tzeng, Y. L., X. Zhou, S. Bao, S. Zhao, C. Noble, and D. S. Stephens. 2006. Autoregulation of the MisR/MisS two-component signal transduction system in Neisseria meningitidis. J. Bacteriol. 188:5055-5065.
45. Uhl, M. A., and J. F. Miller. 1994. Autophosphorylation and phosphotransfer in the Bordetella pertussis BvgAS signal transduction cascade. Proc. Natl. Acad. Sci. USA 91:1163-1167.
46. Uhl, M. A., and J. F. Miller. 1995. BvgAS is sufficient for activation of the Bordetella pertussis ptx locus in Escherichia coli. J. Bacteriol. 177:6477-6485.
47. Uhl, M. A., and J. F. Miller. 1996. Central role of the BvgS receiver as a phosphorylated intermediate in a complex two-component phosphorelay. J. Biol. Chem. 271:33176-33180.
48. Uhl, M. A., and J. F. Miller. 1996. Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BvgAS phosphorelay. EMBO J. 15:1028-1036.
49. Veal-Carr, W. L., and S. Stihitz. 2005. Demonstration of differential virulence gene promoter activation in vivo in Bordetella pertussis using RIVET. Mol. Microbiol. 55:788-798.
50. Williams, C. L., P. E. Boucher, S. Stibitz, and P. A. Cotter. 2005. BvgA functions as both an activator and a repressor to control Bvg phase expression of bipA in Bordetella pertussis. Mol. Microbiol. 56:175-188.
51. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pUC19 vectors. Gene 33:103-119.
52. Zu, T., R. Manetti, R. Rappuoli, and V. Scarlato. 1996. Differential binding of BvgA to two classes of virulence genes of Bordetella pertussis directs promoter selectivity by RNA polymerase. Mol. Microbiol. 21:557-565.