The type III secreted protein BopD in Bordetella bronchiseptica is complexed with BopB for pore formation on the host plasma membrane

Journal of Bacteriology

Volumn 186, Issue 12, 2004, Pages 3806-3813

  Nogawa, Hisashi ^a   Kuwae, Asaomi ^a,b   Matsuzawa, Takeshi ^a,b   Abe, Akio ^a,b  

^a KITASATO UNIVERSITY   (Japan)

^b KITASATO INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LACTATE DEHYDROGENASE; MUTANT PROTEIN; PROTEIN BOPB; PROTEIN BOPD; PROTEIN BOPN; PROTEIN BSP22; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM CULTURE; BORDETELLA BRONCHISEPTICA; CELL MEMBRANE; CHANNEL GATING; COMPLEX FORMATION; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; WILD TYPE;

ANIMALS; BACTERIAL PROTEINS; BORDETELLA BRONCHISEPTICA; CELL DEATH; CELL LINE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; ERYTHROCYTES; GENE DELETION; HELA CELLS; HEMOLYSIS; HUMANS; L-LACTATE DEHYDROGENASE; VIRULENCE FACTORS, BORDETELLA;

BACTERIA (MICROORGANISMS); BORDETELLA BRONCHISEPTICA; NEGIBACTERIA;

EID: 2942552247     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.12.3806-3813.2004     Document Type: Article

References (53)

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. Akerley, B. J., D. M. Monack, S. Falkow, and J. F. Miller. 1992. The bvgAS locus negatively controls motility and synthesis of flagella in Bordetella bronchiseptica. J. Bacteriol. 174:980-990.
4. Andor, A., K. Trulzsch, M. Essler, A. Roggenkamp, A. Wiedemann, J. Heesemann, and M. Aepfelbacher. 2001. YopE of Yersinia, a GAP for Rho GTPases, selectively modulates Rac-dependent actin structures in endothelial cells. Cell. Microbiol. 3:301-310.
5. Arico, B., J. F. Miller, C. Roy, S. Stibitz, D. Monack, S. Falkow, R. Gross, and R. Rappuoli. 1989. Sequences required for expression of Bordetella pertussis virulence factors share homology with prokaryotic signal transduction proteins. Proc. Natl. Acad. Sci. USA 86:6671-6675.
6. Barz, C., T. N. Abahji, K. Trulzsch, and J. Heesemann. 2000. The Yersinia Ser/Thr protein kinase YpkA/YopO directly interacts with the small GTPases RhoA and Rac-1. FEBS Lett. 482:139-143.
7. Blocker, A., P. Gounon, E. Larquet, K. Niebuhr, V. Cabiaux, C. Parsot, and P. Sansonetti. 1999. The tripartite type III secreton of Shigella flexneri inserts IpaB and IpaC into host membranes. J. Cell Biol. 147:683-693.
8. 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.
9. Buttner, D., and U. Bonas. 2002. Port of entry-the type III secretion translocon. Trends Microbiol. 10:186-192.
10. 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.
11. 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.
12. Cotter, P. A., M. H. Yuk, S. Mattoo, B. J. Akerley, J. Boschwitz, D. A. Relman, and J. F. Miller. 1998. Filamentous hemagglutinin of Bordetella bronchiseptica is required for efficient establishment of tracheal colonization. Infect. Immun. 66:5921-5929.
13. Donnenberg, M. S., and J. B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
14. Fauconnier, A., A. Veithen, P. Gueirard, R. Antoine, L. Wacheul, C. Locht, A. Bollen, and E. Godfroid. 2001. Characterization of the type III secretion locus of Bordetella pertussis. Int. J. Med. Microbiol. 290:693-705.
15. Francis, M. S., and H. Wolf-Watz. 1998. YopD of Yersinia pseudotuberculosis is translocated into the cytosol of HeLa epithelial cells: evidence of a structural domain necessary for translocation. Mol. Microbiol. 29:799-813.
16. Frithz-Lindsten, E., A. Holmstrom, L. Jacobsson, M. Soltani, J. Olsson, R. Rosqvist, and A. Forsberg. 1998. Functional conservation of the effector protein translocators PopB/YopB and PopD/YopD of Pseudomonas aeruginosa and Yersinia pseudotuberculosis. Mol. Microbiol. 29:1155-1165.
17. Goodnow, R. A. 1980. Biology of Bordetella bronchiseptica. Microbiol. Rev. 44:722-738.
18. Hakansson, S., K. Schesser, C. Persson, E. E. Galyov, R. Rosqvist, F. Homble, and H. Wolf-Watz. 1996. The YopB protein of Yersinia pseudotuberculosis is essential for the translocation of Yop effector proteins across the target cell plasma membrane and displays a contact-dependent membrane disrupting activity. EMBO J. 15:5812-5823.
19. Hernandez, L. D., M. Pypaert, R. A. Flavell, and J. E. Galan. 2003. A Salmonella protein causes macrophage cell death by inducing autophagy. J. Cell Biol. 163:1123-1131.
20. Holmstrom, A., J. Olsson, P. Cherepanov, E. Maier, R. Nordfelth, J. Pettersson, R. Benz, H. Wolf-Watz, and A. Forsberg. 2001. LcrV is a channel size-determining component of the Yop effector translocon of Yersinia. Mol. Microbiol. 39:620-632.
21. Ide, T., S. Laarmann, L. Greune, H. Schillers, H. Oberleithner, and M. A. Schmidt. 2001. Characterization of translocation pores inserted into plasma membranes by type III-secreted Esp proteins of enteropathogenic Escherichia coli. Cell. Microbiol. 3:669-679.
22. Keen, N. T., S. Tamaki, D. Kobayashi, and D. Trollinger. 1988. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70:191-197.
23. Kuwae, A., M. Ohishi, M. Watanabe, M. Nagai, and A. Abe. 2003. BopB is a type III secreted protein in Bordetella bronchiseptica and is required for cytotoxicity against cultured mammalian cells. Cell. Microbiol. 5:973-983.
24. Ladant, D., C. Brezin, J. M. Alonso, I. Crenon, and N. Guiso. 1986. Bordetella pertussis adenylate cyclase: purification, characterization, and radioimmunoassay. J. Biol. Chem. 261:16264-16269.
25. Locht, C., P. A. Barstad, J. E. Coligan, L. Mayer, J. J. Munoz, S. G. Smith, and J. M. Keith. 1986. Molecular cloning of pertussis; toxin genes. Nucleic Acids Res. 14:3251-3261.
26. Magyar, T., N. Chanter, A. J. Lax, J. M. Rutter, and G. A. Hall. 1988. The pathogenesis of turbinate atrophy in pigs caused by Bordetella bronchiseptica. Vet. Microbiol. 18:135-146.
27. Marenne, M. N., L. Journet, L. J. Mota, and G. R. Cornelis. 2003. Genetic analysis of the formation of the Ysc-Yop translocation pore in macrophages by Yersinia enterocolitica: role of LcrV, YscF and YopN. Microb. Pathog. 35:243-258.
28. 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.
29. Menard, R., P. Sansonetti, C. Parsot, and T. Vasselon. 1994. Extracellular association and cytoplasmic partitioning of the IpaB and IpaC invasins of S. fiexneri. Cell 79:515-525.
30. Merzlyak, P. G., L. N. Yuldasheva, C. G. Rodrigues, C. M. Carneiro, O. V. Krasilnikov, and S. M. Bezrukov. 1999. Polymeric nonelectrolytes to probe pore geometry: application to the α-toxin transmembrane channel. Biophys. J. 77:3023-3033.
31. Mooi, F. R., W. H. Jansen, H. Brunings, H. Gielen, H. G. van der Heide, H. C. Walvoort, and P. A. Guinee. 1992. Construction and analysis of Bordetella pertussis mutants defective in the production of fimbriae. Microb. Pathog. 12:127-135.
32. Neyt, C., and G. R. Cornelis. 1999. Insertion of a Yop translocation pore into the macrophage plasma membrane by Yersinia enterocolitica: requirement for translocators YopB and YopD, but not LcrG. Mol. Microbiol. 33:971-981.
33. Neyt, C., and G. R. Cornelis. 1999. Role of SycD, the chaperone of the Yersinia Yop translocators YopB and YopD. Mol. Microbiol. 31:143-156.
34. Parkhill, J., M. Sebaihia, A. Preston, L. D. Murphy, N. Thomson, D. E. Harris, M. T. Holden, C. M. Churcher, S. D. Bentley, K. L. Mungall, A. M. Cerdeno-Tarraga, L. Temple, K. James, B. Harris, M. A. Quail, M. Achtman, R. Atkin, S. Baker, D. Basham, N. Bason, I. Cherevach, T. Chillingworth, M. Collins, A. Cronin, P. Davis, J. Doggett, T. Feltwell, A. Goble, N. Hamlin, H. Hauser, S. Holroyd, K. Jagels, S. Leather, S. Moule, H. Norberczak, S. O'Neil, D. Ormond, C. Price, E. Rabbinowitsch, S. Rutter, M. Sanders, D. Saunders, K. Seeger, S. Sharp, M. Simmonds, J. Skelton, R. Squares, S. Squares, K. Stevens, L. Unwin, S. Whitehead, B. G. Barrell, and D. J. Maskell. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat. Genet. 35:32-40.
35. Pittman, M. 1979. Pertussis toxin: the cause of the harmful effects and prolonged immunity of whooping cough: a hypothesis. Rev. Infect. Dis. 1:401-412.
36. Reiman, 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.
37. Roberts, M., N. F. Fairweather, E. Leininger, D. Pickard, E. L. Hewlett, A. Robinson, C. Hayward, G. Dougan, and I. G. Charles. 1991. Construction and characterization of Bordetella pertussis mutants lacking the vir-regulated P.69 outer membrane protein. Mol. Microbiol. 5:1393-1404.
38. Sansonetti, P. J., A. Ryter, P. Clerc, A. T. Maurelli, and J. Mounier. 1986. Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect. Immun. 51:461-469.
39. Sarker, M. R., C. Neyt, I. Stainier, and G. R. Cornelis. 1998. The Yersinia Yop virulon: LcrV is required for extrusion of the translocators; YopB and YopD. J. Bacteriol. 180:1207-1214.
40. Scherrer, R., and P. Gerhardt. 1971. Molecular sieving by the Bacillus megaterium cell wall and protoplast. J. Bacteriol. 107:718-735.
41. Sekiya, K., M. Ohishi, T. Ogino, K. Tamano, C. Sasakawa, and A. Abe. 2001. Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc. Natl. Acad. Sci. USA 98:11638-11643.
42. Shaw, R. K., S. Daniell, F. Ebel, G. Frankel, and S. Knutton. 2001. EspA filament-mediated protein translocation into red blood cells. Cell. Microbiol. 3:213-222.
43. Stibitz, S., W. Aaronson, D. Monack, and S. Falkow. 1989. Phase variation in Bordetella pertussis by frameshift mutation in a gene for a novel two-component system. Nature 338:266-269.
44. Stockbauer, K. E., A. K. Foreman-Wykert, and J. F. Miller. 2003. Bordetella type III secretion induces caspase 1-independent necrosis. Cell. Microbiol. 5:123-132.
45. Tardy, F., F. Homble, C. Neyt, R. Wattiez, G. R. Cornelis, J. M. Ruysschaert, and V. Cabiaux. 1999. Yersinia enterocolitica type III secretion-translocation system: channel formation by secreted Yops. EMBO J. 18:6793-6799.
46. Walker, K. E., and A. A. Weiss. 1994. Characterization of the dermonecrotic toxin in members of the genus Bordetella. Infect. Immun. 62:3817-3828.
47. Wattiau, P., B. Bernier, P. Deslee, T. Michiels, and G. R. Cornelis. 1994. Individual chaperones required for Yop secretion by Yersinia. Proc. Natl. Acad. Sci. USA 91:10493-10497.
48. Weiss, A. A., E. L. Hewlett, G. A. Myers, and S. Falkow. 1984. Pertussis toxin and extracytoplasmic adenylate cyclase as virulence factors of Bordetella pertussis. J. Infect. Dis. 150:219-222.
49. Weiss, A. A., E. L. Hewlett, G. A. Myers, and S. Falkow. 1983. Tn5-induced mutations affecting virulence factors of Bordetella pertussis. Infect. Immun. 42:33-41.
50. Yuk, M. H., E. T. Harvill, P. A. Cotter, and J. F. Miller. 2000. Modulation of host immune responses, induction of apoptosis and inhibition of NF-κB activation by the Bordetella type III secretion system. Mol. Microbiol. 35: 991-1004.
51. Yuk, M. H., E. T. Harvill, and J. F. Miller. 1998. The BvgAS virulence control system regulates type III secretion in Bordetella bronchiseptica. Mol. Microbiol. 28:945-959.
52. Zhang, Z. Y., J. C. Clemens, H. L. Schubert, J. A. Stuckey, M. W. Fischer, D. M. Hume, M. A. Saper, and J. E. Dixon. 1992. Expression, purification, and physicochemical characterization of a recombinant Yersinia protein tyrosine phosphatase. J. Biol. Chem. 267:23759-23766.
53. Zumbihl, R., M. Aepfelbacher, A. Andor, C. A. Jacobi, K. Ruckdeschel, B. Rouot, and J. Heesemann. 1999. The cytotoxin YopT of Yersinia enterocolitica induces modification and cellular redistribution of the small GTP-binding protein RhoA. J. Biol. Chem. 274:29289-29293.