The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica

Molecular Microbiology

Volumn 28, Issue 5, 1998, Pages 945-959

  Yuk, Ming Huam ^a   Harvill, Eric T ^a   Miller, Jeff F ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BORDETELLA BRONCHISEPTICA; GENE EXPRESSION REGULATION; GENE LOCUS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN SECRETION; TRANSCRIPTION REGULATION;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; BORDETELLA BRONCHISEPTICA; CARRIER PROTEINS; CELL LINE; CLONING, MOLECULAR; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; MICE; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PEPTIDES; PHOSPHORYLATION; RATS; TRANSCRIPTION FACTORS; TYROSINE; VIRULENCE;

BACTERIA (MICROORGANISMS); BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; NEGIBACTERIA; OVIS; POSIBACTERIA; YERSINIA;

EID: 0042368152     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.00850.x     Document Type: Article

References (64)

1. Abu Kwaik, Y., and Pederson, L.L. (1996) The use of differential display-PCR to isolate and characterize a Legionella pneumophila locus induced during the intracellular infection of macrophages. Mol Microbiol 21: 543-556.
2. Akerley, B.J., and Miller, J.F. (1993) Flagellin gene transcription in Bordetella bronchiseptica is regulated by the BvgAS virulence control system. J Bacteriol 175: 3468-3479.
3. Akerley, B.J., Monack, D.M., Falkow, S., and Miller, J.F. (1992) The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica. J Bacteriol 174: 980-990.
4. Akerley, B.J., Cotter, P.A., and Miller, J.F. (1995) Ectopic expression of the flagellar regulon alters development of the Bordetella-host interaction. Cell 80: 611-620.
5. Allaoui, A., Schulte, R., and Cornelis, G.R. (1995) Mutational analysis of the Yersinia enterocolitica virC operon: characterization of yscE, F, G, I, J, K required for Yop secretion and yscH encoding YopR. Mol Microbiol 18: 343-355.
6. Andersson, K., Carballeira, N., Magnusson, K.E., Persson, C., Stendahl, O., Wolf-Watz, H., et al. (1996) YopH of Yersinia pseudotuberculosis interrupts early phosphotyrosine signalling associated with phagocytosis. Mol Microbiol 20: 1057-1069.
7. Bajaj, V., Lucas, R.L., Hwang, C., and Lee, C.A. (1996) Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22: 703-714.
8. Bergman, T., Erickson, K., Galyov, E., Persson, C., and Wolf-Watz, H. (1994) The IcrB (yscN/U) gene cluster of Yersinia pseudotuberculosis is involved in Yop secretion and shows high homology to the spa gene clusters of Shigella flexneri and Salmonella typhimurium. J Bacteriol 176: 2619-2626.
9. Black, D.S., and Bliska, J.B. (1997) Identification of p130Cas as a substrate of Yersinia YopH (Yop51), a bacterial protein tyrosine phosphatase that translocates into mammalian cells and targets focal adhesions. EMBO J 16: 2730-2744.
10. Bogdanove, A.J., Wei, Z.M., Zhao, L., and Beer, S.V. (1996) Erwinia amylovora secretes harpin via a type III pathway and contains a homolog of yopN of Yersinia spp. J Bacteriol 178: 1720-1730.
11. Collazo, C.M., and Galan, J.E. (1997) The invasion-associated type-III protein secretion system in Salmonella - a review. Gene 192: 51-59.
12. Cornelis, G.R., and Wolf-Watz, H. (1997) The Yersinia Yop virulon: a bacterial system for subverting eukaryotic cells. Mol Microbiol 23: 861-867.
13. Cornelis, G.R., Biot, T., Lambert de Rouvroit, C., Michiels, T., Mulder, B., Sluiters, C., et al. (1989) The Yersinia yop regulon. Mol Microbiol 3: 1455-1459.
14. Cotter, P.A., and Miller, J.F. (1994) BvgAS-mediated signal transduction: analysis of phase-locked regulatory mutants of Bordetella bronchiseptica in a rabbit model. Infect Immun 62: 3381-3390.
15. Cotter, P.A., and Miller, J.F. (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.
16. Cullinane, L.C., Alley, M.R., Marshall, R.B., and Manktelow, B.W. (1987) Bordetella parapertussis from lambs. NZ Vet J 55: 175.
17. Galan, J.E., and Bliska, J.B. (1996) Cross-talk between bacterial pathogens and their host cells. Annu Rev Cell Dev Biol 12: 221-255.
18. Goodnow, R.A. (1980) Biology of Bordetella bronchiseptica. Microbiol Rev 44: 722-738.
19. Groisman, E.A., and Ochman, H. (1996) Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87: 791-794.
20. Guzman, C.A., Rohde, M., Bock, M., and Timmis, K.N. (1994) Invasion and intracellular survival of Bordetella bronchiseptica in mouse dendritic cells. Infect Immun 62: 5528-5537.
21. Hewlett, E.L. (1995) Bordetella species. In Principles and Practice of Infectious Diseases, 3rd edn. Mandell, G.L., Douglas, Jr, R.G., and Bennett, J.E. (eds). New York: Churchill Livingstone, pp. 2078-2084.
22. Hewlett, E.L., and Gordon, V.M. (1988) Adenylate cyclase toxin of Bordetella pertussis. In Pathogenesis and Immunity in Pertussis. Wardlaw, A., and Parton, R. (eds). New York: Wiley & Sons, pp. 193-209.
23. Hsia, R.C., Pannekoek, Y., Ingerowski, E., and Bavoil, P.M. (1997) Type III secretion genes identify a putative virulence locus of Chlamydia. Mol Microbiol 25: 351-359.
24. Hueck, C.J., Hantman, M.J., Bajaj, V., Johnston, C., Lee, C.A., and Miller, S.I. (1995) Salmonella typhimurium secreted invasion determinants are homologous to Shigella lpa proteins. Mol Microbiol 18: 479-490.
25. Jarvis, K.G., Girün, J.A., Jerse, A.E., McDaniel, T.K., Donnenberg, M.S., and Kaper, J.B. (1995) Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc Natl Acad Sci USA 92: 7996-8000.
26. Johnston, C., Pegues, D.A., Hueck, C.J., Lee, A., and Miller, S.I. (1996) Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response-regulator superfamily. Mol Microbiol 22: 715-727.
27. Kaniga, K., Tucker, S., Trollinger, D., and Galan, J.E. (1995) Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J Bacteriol 177: 3965-3971.
28. Lee, C.A. (1997) Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol 5: 148-156.
29. Liang, P., and Pardee, A.B. (1992) Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257: 967-971.
30. Locht, C., Barstad, P.A., Coligan, J.E., Mayer, L., Munoz, J.J., Smith, S.G., et al. (1986) Molecular cloning of pertussis toxin genes. Nucleic Acids Res 14: 3251-3261.
31. Martinez de Tejada, G., Miller, J.F., and Cotter, P.A. (1996) Comparative analysis of the virulence control systems of Bordetella pertussis and Bordetella bronchiseptica. Mol Microbiol 22: 895-908.
32. Menard, R., Sansonetti, P., and Parsot, C. (1994) The secretion of the Shigella flexneri lpa invasins is activated by epithelial cells and controlled by lpaB and lpaD. EMBO J 13: 5293-5302.
33. Menard, R., Prevost, M.C., Gounon, P., Sansonetti, P., and Dehio, C. (1996) The secreted lpa complex of Shigella flexneri promotes entry into mammalian cells. Proc Natl Acad Sci USA 93: 1254-1258.
34. Michiels, T., Vanooteghem, J.C., Lambert de Rouvroit, C., China, B., Gustin, A., Boudry, P., et al. (1991) Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica. J Bacteriol 173: 4994-5009.
35. Mooi, F.R., Jansen, W.H., Brunings, H., Gielen, H., van der Heide, H.G., Walvoort, H.C., et al. (1992) Construction and analysis of Bordetella pertussis mutants defective in the production of fimbriae. Microb Pathog 12: 127-135.
36. Muller, M., and Hildebrandt, A. (1993) Nucleotide sequences of the 23S RNA genes from Bordetella pertussis, B. parapertussis, B. bronchiseptica and B. avium, and their implications for phylogenetic analysis. Nucleic Acids Res 21: 3320.
37. Musser, J.M., Hewlett, E.L., Peppler, M.S., and Selander, R.K. (1986) Genetic diversity and relationships in populations of Bordetella spp. J Bacteriol 166: 230-237.
38. Pegues, D.A., Hantman, M.J., Behlau, I., and Miller, S.I. (1995) PhoP/PhoQ transcriptional repression of Salmonella typhimurium invasion genes: evidence for a role in protein secretion. Mol Microbiol 17: 169-181.
39. Persson, C., Nordfelth, R., Holmstrom, A., Hakansson, S., Rosqvist, R., and Wolf-Watz, H. (1995) Cell-surface-bound Yersinia translocate the protein tyrosine phosphatase YopH by a polarized mechanism into the target cell. Mol Microbiol 18: 135-150.
40. Persson, C., Carballeira, N., Wolf-Watz, H., and Fallman, M. (1997) The PTPase YopH inhibits uptake of Yersinia, tyrosine phosphorylation of p. 130Cas and FAK, and the associated accumulation of these proteins in peripheral focal adhesions. EMBO J 16: 2307-2318.
41. Pettersson, J., Nordfelth, R., Dubinina, E., Bergman, T., Gustafsson, M., Magnusson, K.E., et al. (1996) Modulation of virulence factor expression by pathogen target cell contact. Science 273: 1231-1233.
42. Pittman, M. (1984) Genus Bordetella. In Bergey's Manual of Systematic Bacteriology. Kreig, N.B., and Holt, J.G. (eds). Baltimore: The Williams and Wilkins Company, pp. 338-393.
43. Porter, J.F., Connor, K., and Donachie, W. (1994) Isolation and characterization of Bordetella parapertussis-like bacteria from ovine lungs. Microbiology 140: 255-261.
44. Relman, D.A., Domenighini, M., Tuomanen, E., Rappuoli, R., and Falkow, S. (1989) Filamentous hemagglutinin of Bordetella pertussis: nucleotide sequence and crucial role in adherence. Proc Natl Acad Sci USA 86: 2637-2641.
45. Roberts, M., Fairweather, N.F., Leininger, E., Pickard, D., Hewlett, E.L., Robinson, A., et al. (1991) Construction and characterization of Bordetella pertussis mutants lacking the vir-regulated P.69 outer membrane protein. Mol Microbiol 5: 1393-1404.
46. Rosqvist, R., Forsberg, A., and Wolf-Watz, H. (1991) Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption. Infect Immun 59: 4562-4569.
47. Rosqvist, R., Magnusson, K.E., and Wolf-Watz, H. (1994) Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J 13: 964-972.
48. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
49. Sasakawa, C., Buysse, J.M., and Watanabe, H. (1992) The large virulence plasmid of Shigella. Curr Topics Microbiol Immunol 180: 21-44.
50. Savelkoul, P.H., Kremer, B., Kusters, J.G., van der Zeijst, B.A., and Gaastra, W. (1993) Invasion of HeLa cells by Bordetella bronchiseptica. Microb Pathog 14: 161-168.
51. Schipper, H., Krohne, G.F., and Gross, R. (1994) Epithelial cell invasion and survival of Bordetella bronchiseptica. Infect Immun 62: 3008-3011.
52. Stibitz, S., and Yang, M.S. (1991) Subcellular localization and immunological detection of proteins encoded by the vir locus of Bordetella pertussis. J Bacteriol 173: 4288-4296.
53. Stibitz, S., Weiss, A.A., and Falkow, S. (1988) Genetic analysis of a region of the Bordetella pertussis chromosome encoding filamentous hemagglutinin and the pleiotropic regulatory locus vir. J Bacteriol 170: 2904-2913.
54. Uhl, M.A., and Miller, J.F. (1994) Autophosphorylation and phosphotransfer in the Bordetella pertussis BvgAS signal transduction cascade. Proc Natl Acad Sci USA 91: 1163-1167.
55. Uhl, M.A., and Miller, J.F. (1996a) Central role of the BvgS receiver as a phosphorylated intermediate in a complex two-component phosphorelay. J Biol Chem 271: 33176-33180.
56. Uhl, M.A., and Miller, J.F. (1996b) Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BvgAS phosphorelay. EMBO J 15: 1028-1036.
57. Walker, J.E., Saraste, M., Runswick, M.J., and Gay, N.J. (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1: 945-951.
58. Walker, K.E., and Weiss, A.A. (1994) Characterization of the dermonecrotic toxin in members of the genus Bordetella. Infect Immun 62: 3817-3828.
59. Watarai, M., Tobe, T., Yoshikawa, M., and Sasakawa, C. (1995) Contact of Shigella with host cells triggers release of lpa invasins and is an essential function of invasiveness. EMBO J 14: 2461-2470.
60. Weiss, A.A., and Hewlett, E.L. (1986) Virulence factors of Bordetella pertussis. Annu Rev Microbiol 40: 661-686.
61. Woestyn, S., Allaoui, A., Wattiau, P., and Cornelis, G.R. (1994) YscN, the putative energizer of the Yersinia Yop secretion machinery. J Bacteriol 176: 1561-1569.
62. Wong, K.K., and McClelland, M. (1994) Stress-inducible gene of Salmonella typhimurium identified by arbitrarily primed PCR of RNA. Proc Natl Acad Sci USA 91: 639-643.
63. Yahr, T.L., Goranson, J., and Frank, D.W. (1996) Exoenzyme S of Pseudomonas aeruginosa is secreted by a type III pathway. Mol Microbiol 22: 991-1003.
64. Zierler, M.K., and Galan, J.E. (1995) Contact with cultured epithelial cells stimulates secretion of Salmonella typhimurium invasion protein InvJ. Infect Immun 63: 4024-4028.