A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis

Molecular Microbiology

Volumn 33, Issue 6, 1999, Pages 1210-1220

  O'Cellaghan, David ^a   Cazevieille, Chantal ^a   Allardet Servent, Annick ^a   Boschiroli, Maria Laura ^a   Bourg, Gisèle ^a   Foulongne, Vincent ^a   Frutos, Patrice ^a   Kulakov, Youri ^a   Ramuz, Michel ^a  

^a INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; LIPOPROTEIN; VIRULENCE FACTOR;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM CONJUGATION; BORDETELLA PERTUSSIS; BRUCELLA SUIS; CELL SURVIVAL; CONTROLLED STUDY; DNA SEQUENCE; DNA TRANSFER; MACROPHAGE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PLANT ROOT; PRIORITY JOURNAL; PROTEIN SECRETION; PSEUDOMONAS; RHIZOBIUM RADIOBACTER; SEQUENCE HOMOLOGY;

AGROBACTERIUM TUMEFACIENS; BORDETELLA PERTUSSIS; BRUCELLA SUIS;

EID: 0032868454     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01569.x     Document Type: Article

References (60)

1. Anderson, L.B., Hertzel, A.V., and Das, A. (1996) Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. Proc Natl Acad Sci USA 93: 8889-8894.
2. Andersson, S.G.E., Zomorodipour, A., Andersson, J.O., Sicheritz-Ponten, T., Alsmark, U.C.M., Podowski, R.M., et al. (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396: 133-140.
3. Bairoch, A, Bucher, P., and Hofmann, K. (1997) The PROSITE database, its status in 1997. Nucleic Acids Res 25: 217-221.
4. Baron, C., Thorstenson, Y.R., and Zambryski, P.C. (1997) The lipoprotein VirB7 interacts with VirB9 in the membrane of Agrobacterium tumefaciens. J Bacteriol 179: 1211-1218.
5. Bayer, M., Eferl, R., Zelling, G., Teferle, K., Dijkstra, A., Koraimann, G., et al. (1995) Gene 19 of plasmid R1 is required for both efficient conjugative DNA transfer and bacteriophage R19 infection. J Bacteriol 177: 4279-4288.
6. Berger, B.R., and Christie, P.J. (1993) The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain. J Bacteriol 175: 1723-1724.
7. Canning, P.C., Roth, J.A., and Deyoe, B.L. (1986) Release of 5′ guanosine monophosphate and adenine by Brucella abortus and their role in the intracellular survival of the bacteria. J Infect Dis 154: 464-470.
8. Caron, E., Gross, A., Liautard, J.-P., and Dornand, J. (1996) Brucella species release a specific, protease-sensitive, inhibitor of TNF-alpha expression, active on human macrophage-like cells. J Immunol 156: 2885-2893.
9. Censini, S., Lange, C., Xiang, Z., Crabtree, J.E., Ghiara, P., Brodovsky, M., et al. (1996) Cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA 93: 14648-14653.
10. Christie, P.J. (1997) Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multi-functional transporters in eubacteria. J Bacteriol 179: 3085-3094.
11. Cook, D.M., Farizo, K.M., and Burns, D.L. (1999) Identification and characterization of PtlC, an essential component of the pertussis toxin secretion system. Infect Immun 67: 754-759.
12. Cernelio, G.R., Boland, A., Bovd, A.P., Geuijen, C., Iriarte, M., Clevt C. et al. (1998) The virulence plasmid of Yersinia, an minost genome. Microbiol Mol Biol Rev 62: 1315-1352.
13. Covacci, A., and Rappuoli, R (1993) Pertussis toxin export requires accessory genes located downstream from the e tussis toxin operon. Mol Microbiol 8: 429-434.
14. Covacci, A., Falkow, S., Berg, D.E., and Rappuoli, R. (1997) Did the inheritance of a pathogenicity island modify the virulence of Helicobacter pylori? Trends Microbiol 5: 205-208.
15. Dang, T.A.T., and Christie, P.J. (1997) The VirB4 ATPase of -grobacterium tumefaciens is a cytoplasmic membrane protein exposed at the periplasmic surface. J Bacteriol 79: 453-462.
16. Das, A., Anderson, L.B., and Xie, Y.H. (1997) Delineation of the interaction domains of Agrobacterium tumefaciens VirB7 and VirB9 by use of the yeast two-hybrid assay. J Bacteriol 179: 3404-3409.
17. De Mot, R., Schoofs, G., Roelandt, A., Declerck, P., Proost, R., Van Damme, J., et al. (1994) Molecular characterization of the major outer-membrane protein OprF from oct-colonizing Pseudomonas fluorescens. Microbiology 40: 1377-1387.
18. Dorrel, N., Guigue-Tallet, P., Spencer, S., Foulongne, V., O'Callaghan, D., and Wren, B.W. (1999) Investigation to the role of the response regulator NtrC in the meta-polism and virulence of Brucella suis. Microb Pathog 27: 6-11.
19. Dorrell, N., Spencer, S., Foulongne, V., Guigue-Talet, P., O'Callaghan, D., and Wren, B.W. (1998) Identification, cloning and initial characterisation of FeuPQ in Brucella abortus: a new sub-family of two-component regulatory systems. FEMS Microbiol Lett 162: 143-150.
20. Elzer P.H., Phillips, R.W., Kovach, M.E., Peterson, K.M., and Roop R.M. (1994) Characterization and genetic complementation of a Brucella abortus high-temperature-requirement A (htrA) deletion mutant. Infect Immun 62: 4135-4139.
21. Farizo, K.M., Cafarella, T.G., and Burns, D.L. (1996) Evidence for a ninth gene, ptll, in the locus encoding the pertussis toxin secretion system of Bordetella pertussis and formation of a Ptll-Ptlf complex. J Biol Chem 271: 31643-31649.
22. Fullner, K.J., Stephens, K.M., and Nester, E.W. (1994) An essential virulence protein of Agrobacterium tumefaciens, VirB4, requires an intact mononucleotide binding domain to function in transfer of T-DNA. Mol Gen Genet 245: 704-715.
23. Godfroid, F., Taminiau B., Danese, I., Denoel, P., Tibor, A., Wevants. V., et al. (1998) Identification of the perosamine synthetase gene of Brucella melitensis 16M and involvement of lipopolysaccharide O side chain in Brucella survival in mice and in macrophages. Infect Immun 66: 5485-5493.
24. Halling, S.M., and Bricker, B.J. (1994) Characterization and occurrence of two repeated palindromic DNA elements of Brucella spp. Bru-RS1 and Bru-RS2. Mol Microbiol 14: 681-689.
25. Jerse A.E., and Kaper, J.B. (1991) The eae gene of enteropathogenic Escherichia coli encodes a 94-kilodalton membrane protein, the expression of which is influenced by the EAF plasmid. Infect Immun 59: 4302-4309.
26. Jumas-Bilak, E., Michaux-Charachon, S., Bourg, G., O'Callaghan, D., and Ramuz, M. (1998) Differences in chromosome number and genome rearrangements in the genus Brucella. Mol Microbiol 27: 99-106.
27. Kohler, S., Teyssier, J., Cloeckaert, A., Rouot, B., and Liautard, J.P. (1996) Participation of the molecular chaperone DnaK in intracellular growth of Brucella suis within U937-derived phagocytes. Mol Microbiol 20: 701-712.
28. Kotob, S.I., and Burns, D.L. (1997) The essential role of a consensus nucleotide binding site of PtlH in secretion of pertussis toxin from Bordetella pertussis. Infect Immun 179: 7577-7580.
29. Kovach, M.E., Phillips, R.W., Elzer, P.H., Roop, R.M., and Peterson, K.M. (1994) pBBR1MCS: a broad-host-range cloning vector. Biotechniques 16: 800-802.
30. Kuldau, G.A., De Vos, G., Owen, J., McCaffery, G., and Zambryski, P. (1990) The virB operon of Agrobacterium tumefaciens pTiC58 encodes 11 open reading frames. Mol Gen Genet 221: 256-266.
31. Lee, C.A. (1997) Type III secretion systems: machines to deliver bacterial proteins into eukaryotic cells? Trends Microbiol 5: 148-156.S.
32. Li, P., Everhart, D.M., and Farrand, S.K. (1998) Genetic and sequence analysis of the pTiC58 trb locus, encoding a mating pair formation system related to members of the type IV secretion family. J Bacteriol 180: 6164-6172.
33. Lin, J., and Ficht, T.A. (1995) Protein synthesis in Brucella abortus induced during macrophage infection. Infect Immun 63: 1409-1414.
34. Mekalanos, J.J. (1992). Environmental signals controlling expression of virulence determinants in bacteria. J Bacteriol 174: 1-7.
35. Michaux-Charachon, S., Bourg, G., Jumas-Bilak, E., Guigue-Talet, P., Allardet-Servent, A., O'Callaghan, D., et al. (1997) Genome structure and phylogeny in the genus Brucella. J Bacteriol 179, 3244-2349.
36. Miller, V.L., and Mekalanos, J.J. (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.
37. Mushegian, A.R., Fullner, K.J., Koonili, E.V., and Nester, E.W. (1996) A family of lysozyme-like virulence factors in bacterial pathogens of plants and animals. Proc Natl Acad Sci USA 93: 7321-7326.
38. Pizarro-Cerda, J., Moreno, E., Sanguedolce, V., Mege, J.L., and Gorvel, J.P. (1998a) Virulent Brucella abortus avoids lysosome fusion and distributes within autophagosome-like compartments. Infect Immun 66: 2387-2392.
39. Pizarro-Cerda, J., Meresse, S., Parton, R.G., Van der Goot, G., Sola-Landa, A., Lopez-Goni, I.J., et al. (1998b) Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect Immun 66: 5711-5724.
40. Pohlman, R.F., Genetti, H.D., and Winans, S.C. (1994) Common ancestry between IncN conjugal transfer genes and macromolecular export systems of plant and animal pathogens Mol Microbiol 14: 655-668.
41. Samartino, L.E., and Enright, F.M. (1993) Pathogenesis of abortion of bovine brucellosis. Comp Immun Microbiol Infect Dis 16: 95-105.
42. 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.
43. Segal, G., Purcell, M., and Shuman, H.A. (1998) Host cell killing and bacterial conjugation require overlapping sets of genes within a 22 kb region of the Legionella pneumophila genome. Proc Natl Acad Sci USA 95: 1669-1674.
44. Shirasu, K., Morel, P., and Kado, I.C. (1990) Characterization of the virB operon of an Agrobacterium tumefaciens Ti plasmid. Mol Microbiol 4: 1153-1163.
45. Smith, L.D., and Ficht, T.A., (1990) Pathogenesis of Brucella. Crit Rev Microbiol 17: 209-230.
46. Sola-Landa, A., Pizarro-Cerda, J., Grillo, M.J., Moreno, E., Moriyon, I., Blasco, J.M., et al. (1998) A two-component regulatory system playing a critical role in plant pathogens and endosymbionts is present in Brucella abortus and controls cell invasion and virulence. Mol Microbiol 29: 125-138.
47. Spudich, G.M., Fernandez, D., Zho, X., and Christie, P.J. (1996) Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T-complex transport apparatus. Proc Natl Acad Sci USA 93: 7512-7517.
48. Stephens, K.M., Roush, C., and Nester, E. (1995) Agrobacterium tumefaciens VirB11 protein requires a consensus nucleotide-binding site for function in virulence. J Bacteriol 177: 27-36.
49. Tadayyon, M., and Broome-Smith, J.K. (1992) TnblaM: a transposon for directly tagging bacterial genes encoding cell envelope and secreted proteins. Gene 111: 21-26.
50. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
51. Thorsted, P.B., Macartney, D.P., Akhtar, P., Haines, A.S., Ali, N., Davidson, P., et al. (1998) Complete sequence of the IncPβ plasmid R751: implications for the evolution and organisation of the IncP backbone. J Mol Biol 282: 969-990.
52. Tomb, J.-F., White, O., Kerlavage, A.R., Clayton, R.A., Sutton, G.G., Fleischmann, R.D., et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.
53. Vogel, J.P., Andrew, H.L., Wong, S.K., and Isberg, R.R. (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
54. Ward, J.E., Akiyoshi, D.E., Regier, D., Datta, A., Gordon, M.P., and Nester, E.W. (1988) Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid. J Biol Chem 263: 5804-5814.
55. Weiss, A.A., Johnson, F.D., and Burns, D.L. (1993) Molecular characterization of an operon required for pertussis toxin secretion. Proc Natl Acad Sci USA 90: 2970-2974.
56. Whitchurch, C.B., Hobbs, M., Livingstone, S.P., Krishnapillai, V., and Mattick, J.S. (1991) Characterisation of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialised protein export system widespread in eubacteria. Gene 101: 33-44.
57. Winans, S.C., Burns, D.L., and Christie, P.J. (1996) Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol 4: 64-68.
58. Woese, C.R. (1987) Bacterial evolution. Microbiol Rev 51: 221-271.
59. Young, E.J. (1983) Human brucellosis. Rev Infect Dis 5: 821-842.
60. Zupan, J.R., Ward, D., and Zambryski, P. (1998) Assembly of the VirB transport complex for DNA transfer from Agrobacterium tumefaciens to plant cells. Curr Opin Microbiol 1: 649-655.