Characterization of membrane and protein interaction determinants of the Agrobacterium tumefaciens VirB11 ATPase

Journal of Bacteriology

Volumn 179, Issue 3, 1997, Pages 583-591

  Rashkova, Svetlana ^a   Spudich, Giulietta M ^a   Christie, Peter J ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; NUCLEOTIDE BINDING PROTEIN; UREA;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; GENE DELETION; GENE EXPRESSION; PLASMID; PRIORITY JOURNAL; PROTEIN INTERACTION; RHIZOBIUM RADIOBACTER;

EID: 0031037305     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.3.583-591.1997     Document Type: Article

References (54)

1. Anderson, L. B., A. V. Hertzel, and A. Das. 1996. Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. Proc. Natl. Acad. Sci. USA 93:8889-8894.
2. Baichwal, V., D. Liu, and G. F. Ames. 1993. The ATP-binding component of a procaryotic traffic ATPase is exposed to the periplasmic (external) surface Proc. Natl. Acad. Sci. USA 90:620-624.
3. Beijersbergen, A., A. D. Dulk-Ras, R. A. Schilperoort, and P. J. J. Hooykaas. 1992. Conjugative transfer by the virulence system of Agrobacterium tumefaciens. Science 256:1324-1327.
4. Berger, B. R., and P. J. Christie. 1993. The Agrobacterium tumefaciens virB4 gene product is an essential virulence protein requiring an intact nucleoside triphosphate-binding domain. J. Bacteriol. 175:1723-1734.
5. Berger, B. R., and P. J. Christie. 1994. Genetic complementation analysis of the Agrobacterium tumefaciens virB operon: virB2 through virB11 are essential virulence genes. J. Bacteriol. 176:3646-3660.
6. Binns, A. N., C. E. Beaupre, and E. M. Dale. 1995. Inhibition of VirB-mediated transfer of diverse substrates from Agrobacterium tumefaciens by the IncQ plasmid RSF1010. J. Bacteriol. 177:4890-4899.
7. Buchanan-Wollaston, V., J. E. Passiatore, and F. Cannon. 1987. The mob and oriT mobilization functions of a bacterial plasmid promote its transfer to plants. Nature 328:172-175.
8. Chen, C.-Y., and S. C. Winans. 1991. Controlled expression of the transcriptional activator gene virG in Agrobacterium tumefaciens by using the Escherichia coli lac promoter. J. Bacteriol. 173:1139-1144.
9. Christie, P. J., J. E. Ward, M. P. Gordon, and E. W. Nester. 1989. A gene required for transfer of T-DNA to plants encodes an ATPase with autophosphorylating activity. Proc. Natl. Acad. Sci. USA 86:9677-9681.
10. Christie, P. J., J. E. Ward, S. C. Winans, and E. W. Nester. 1988. The Agrobacterium tumefaciens virE2 gene product is a single-stranded DNA binding protein that associates with T-DNA. J. Bacteriol. 170:2659-2667.
11. Dang, T. A. T., and P. J. Christie. 1996. The VirB4 ATPase of Agrobacterium tumefaciens is a cytoplasmic membrane protein exposed at the periplasmic surface. J. Bacteriol. 179:453-462.
12. Ecunomou, A., and W. Wickner. 1994. SecA promotes pre-protein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell 78:835-843.
13. Fath, M. J., and R. Kolter. 1993. ABC transporters: bacterial exporters. Microbiol. Rev. 57:995-1017.
14. Fernandez, D., T. A. Dang, G. M. Spudich, X. R. Zhou, B. R. Berger, and P. J. Christie. 1996. Agrobacterium tumefaciens virB7 gene product, a proposed component of the T-complex transport apparatus, is a membrane-associated lipoprotein exposed at the periplasmic surface. J. Bacteriol. 178:3156-3167.
15. Fernandez, D., G. M. Spudich, X.-R. Zhou, and P. J. Christie. 1996. The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T-complex transport apparatus. J. Bacteriol. 178:3168-3176.
16. Finberg, K. E., T. R. Muth, S. P. Young, J. B. Muken, S. M. Heitritter, A. N. Binns, and L. M. Bunta. 1995. Interactions of VirB9, -10, and -11 with the membrane fraction of Agrobacterium tumefaciens: solubility studies provide evidence for tight associations. J. Bacteriol. 177:4881-4889.
17. Foster, P. L. 1991. In vivo mutagenesis. Methods Enzymol. 204:114-125.
18. Fullner, K. J., K. M. Stephens, and E. W. Nester. 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.
19. Garfinkel, D. J., R. B. Simpson, L. W. Ream, F. F. White, M. P. Gordon, and E. W. Nester. 1981. Genetic analysis of crown gall: fine structure map of the T-DNA by site-directed mutagenesis. Cell 27:143-153.
20. Hooykaas, P. J. J., and A. G. M. Beijersbergen. 1994. The virulence system of Agrobacterium tumefaciens. Annu. Rev. Phytopathol. 32:157-179.
21. Kado, C. I. 1993. Agrobacterium-mediated transfer and stable incorporation of foreign genes in plants, p. 243-254. In D. B. Clewell (ed.), Bacterial conjugation. Plenum Press, New York, N.Y.
22. Kado, C. I. 1994. Promiscuous DNA transfer system of Agrobacterium tumefaciens: role of the virB operon in sex pilus assembly and synthesis. Mol. Microbiol. 12:17-22.
23. Kerppola, R. E., V. K. Shyamala, P. Klebba, and G. F.-L. Ames. 1991. The membrane-bound proteins of periplasmic permeases form a complex. J. Biol. Chem. 266:9857-9865.
24. Kunkel, T. A., K. Bebenek, and J. McClary. Efficient site-directed mutagenesis using uracil-containing DNA. Methods Enzymol. 204:125-139.
25. Lessl, M., D. Balzer, W. Pansegrau, and E. Lanka. 1992. Sequence similarities between the RP4 Tra2 and the Ti VirB region strongly support the conjugation model for T-DNA transfer. J. Biol. Chem. 267:20471-20480.
26. Lessl, M., and E. Lanka. 1994. Common mechanisms in bacterial conjugation and Ti-mediated T-DNA transfer to plant cells. Cell 77:321-324.
27. Maagd, R. A., and B. Lugtenberg. 1986. Fractionation of Rhizobium leguminosarum cells into outer membrane, cytoplasmic membrane, periplasmic, and cyloplasmic components. J. Bacteriol. 167:1083-1085.
28. Osborn, M. J., J. E. Gander, and E. Parisi. 1972. Mechanism of assembly of the outer membrane of Salmonella typhimurium. J. Biol. Chem. 247:3973-3986.
29. Ostrovsky, P. C., and S. Maloy. 1995. Protein phosphorylation on serine, threonine, and tyrosine residues modulates membrane-protein interactions and transcriptional regulation in Salmonella typhimurium. Genes Dev. 9:2034-2041.
30. Otten, L., H. De Greve, J. Leemans, R. Hain, P. Hooykaas, and J. Schell. 198-4. Restoration of virulence of vir region mutants of Agrobacterium tumefaciens strain B6S3 by coinfection with normal and mutant Agrobacterium strains Mol. Gen. Genet. 195:159-163.
31. Pansegrau, W., E. Lanka, P. T. Barth, D. H. Figurski, D. G. Guiney, D. Haas, D. K. Helinski, H. Schwab, V. A. Stanishich, and C. M. Thomas. 1994. Complete nucleotide sequence of Birmingham IncPα plasmids. J. Mol. Biol. 239:623-663.
32. Pohlman, R. F., H. D. Genetti, and S. C. Winans. 1994. Common ancestry between IncN conjugal transfer genes and macromolecular export systems of plant and animal pathogens. Mol. Microbiol. 14:655-668.
33. Possot, O., and A. P. Pugsley. 1994. Molecular characterization of PulE, a protein required for pullulanase secretion. Mol. Microbiol. 12:287-299.
34. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
35. Rajapandi, R., and D. Oliver. 1996. Integration of SecA protein into the Escherichia coli inner membrane is regulated by its amino terminal ATP-binding domain. Mol. Microbiol. 20:43-51.
36. Regensburg-Tuink, A. J. G., and P. J. J. Hooykaas. 1993. Transgenic N. glauca plants expressing bacterial virulence gene virF are converted into hosts for nopaline strains of A. tumefaciens. Nature 363:69-71.
37. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold spring Harbor Laboratory, Cold Spring Harbor, N.Y.
38. Sandkvist, M., M. Bagdasarian, S. P. Howard, and V. J. DiRita. 1995. Interaction between the autokinase EpsE and EpsL in the cytoplasmic membrane is required for extracellular secretion in Vibrio cholerae. EMBO J. 14:1664-1673.
39. Schneider, E., S. Hunke, and S. Tebbe. 1995, The MalK protein of the ATP-binding cassette transporter for maltose of Escherichia coli is accessible to protease digestion from the periplasmic side of the membrane. J. Bacteriol. 177:5364-5367.
40. Shirasu, K., Z. Koukolikova-Nicola, B. Hohn, and C. I. Kado. 1994. An inner-membrane-associaied virulence protein essential for T-DNA transfer from Agrobacterium tumefaciens to plants exhibits ATPase activity and similarities to conjugative transfer genes. Mol. Microbiol. 11:581-588.
41. Spudich, G. M., D. Fernandez, X.-R. Zhou, and P. J. Christie. 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.
42. Stephens, K. M., C. Roush, and E. W. Nester. 1995. Agrobacterium tumefaciens VirB11 protein requires a consensus nucleotide-binding site for function in virulence. J. Bacteriol. 177:27-36.
43. Sundberg, C., L. Meek, K. Carroll, A. Das, and W. Ream. 1996. VirE1 protein mediates export of the single-stranded DNA-binding protein VirE2 from Agrobacterium tumefaciens into plant cells. J. Bacteriol. 178:1207-1212.
44. Thorstenson, Y. R., G. A. Kuldau, and P. C. Zambryski 1993. Subcellular localization of seven VirB proteins of Agrobacterium tumefaciens: implications for the formation of a T-DNA transport structure. J. Bacteriol. 175:5233-5241.
45. Turner, L. R., J. C. Lara, D. N. Nunn, and S. Lory. 1993. Mutations in the consensus ATP-binding sites of XcpR and PilB eliminate extracellular protein secretion and pilus biogenesis in Pseudomonas aeruginosa. J. Bacteriol. 175:4962-4969.
46. Ward, J. E., D. E. Akiyoshi, D. Regier, A. Datta, M. P. Gordon, and E. W. Nester. 1988. Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid. J. Biol. Chem. 263:5804-5814.
47. Ward, J. E., D. E. Akiyoshi, D. Regier, A. Datta, M. P. Gordon, and E. W. Nester. 1990. Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid. J. Biol. Chem. 265:4768.
48. Ward, J. E., Jr., E. M. Dale, P. J. Christie, E. W. Nester, and A. N. Binns. 1990. Complementation analysis of Agrobacterium tumefaciens Ti plasmid virB genes by use of a vir promoter expression vector: virB9, virB10, and virB11 are essential virulence genes. J. Bacteriol. 172:5187-5199.
49. Watson, B., T. C. Curia, M. P. Gordon, M.-D. Chilton, and E. W. Nester. 1975. Plasmid required for virulence of Agrobacterium tumefaciens. J. Bacteriol. 123:255-264.
50. Weiss, A. A., F. D. Johnson, and D. L. Burns. 1993. Molecular characterization of an operon required for pertussis toxin secretion. Proc. Natl. Acad. Sci. USA 90:2970-2974.
51. Winans, S. C., R. A. Kersteller, J. E. Ward, and E. W. Nester. 1989. A protein required for transcriptional regulation of Agrobacterium virulence genes spans the cytoplasmic membrane. J. Bacteriol. 171:1616-1622.
52. Winans, S. C., D. L. Burns, and P. J. Christie. 1996. Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol. 4:1616-1622.
53. Yanofsky, M. F., S. G. Porter, C. Young, L. M. Albright, M. P. Gordon, and E. W. Nester. 1986. The virD operon of Agrobacterium tumefaciens encodes a site-specific endonuclease. Cell 47:471-477.
54. Zupan, J. R., and P. Zambryski. 1995. Transfer of T-DNA from Agrobacterium to the plant cell. Plant Physiol. 107:1041-1047.