Agrobacterium tumefaciens VirB6 protein participates in formation of VirB7 and VirB9 complexes required for type IV secretion

Journal of Bacteriology

Volumn 185, Issue 9, 2003, Pages 2867-2878

  Jakubowski, Simon J ^a   Krishnamoorthy, Vidhya ^a   Christie, Peter J ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DIMER; GLUTATHIONE TRANSFERASE; MEMBRANE PROTEIN; MUTANT PROTEIN; PROTEIN VIRB6; PROTEIN VIRB7; PROTEIN VIRB9; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM PILUS; BIOGENESIS; CROSS LINKING; DISULFIDE BOND; GENE DELETION; GENETIC COMPLEMENTATION; IMMUNOPRECIPITATION; NONHUMAN; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN ISOLATION; PROTEIN POLYMERIZATION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN SYNTHESIS; RHIZOBIUM RADIOBACTER; STOICHIOMETRY; WILD TYPE;

BACTERIAL PROTEINS; FIMBRIAE, BACTERIAL; GENE DELETION; MEMBRANE PROTEINS; MUTATION; RECOMBINANT FUSION PROTEINS; RHIZOBIUM RADIOBACTER; TEMPERATURE; VIRULENCE FACTORS;

AGROBACTERIUM; AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 0037407708     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.9.2867-2878.2003     Document Type: Article

References (51)

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. Anthony, K. G., W. A. Klimke, J. Manchak, and L. A. Frost. 1999. Comparison of proteins involved in pilus synthesis and mating pair stabilization from the related plasmids F and R100-1: insights into the mechanism of conjugation. J. Bacteriol. 181:5149-5159.
3. Bacon, D. J., R. A. Alm, D. H. Burr, L. Hu, D. J. Kopecko, C. P. Ewing, T. J. Trust, and P. Guerry. 2000. Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect. Immun. 68:4384-4390.
4. Baron, C., N. Domke, M. Beinhofer, and S. Hapfelmeier. 2001. Elevated temperature differentially affects virulence, VirB protein accumulation, and T-pilus formation in different Agrobacterium tumefaciens and Agrobacterium vitis strains. J. Bacteriol. 183:6852-6861.
5. Baron, C., Y. R. Thorstenson, and P. C. Zambryski. 1997. The lipoprotein VirB7 interacts with VirB9 in the membranes of Agrobacterium tumefaciens. J. Bacteriol. 179:1211-1218.
6. Beaupré, C. E., J. Bohne, E. M. Dale, and A. N. Binns. 1997. Interactions between VirB9 and VirB10 membrane proteins involved in movement of DNA from Agrobacterium tumefaciens into plant cells. J. Bacteriol. 179:78-89.
7. 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.
8. Bohne, J., A. Yim, and A. N. Binns. 1998. The Ti plasmid increases the efficiency of Agrobacterium tumefaciens as a recipient in virB-mediated conjugal transfer of an IncQ plasmid. Proc. Natl. Acad. Sci. USA 95:7057-7062.
9. Burns, D. L. 1999. Biochemistry of type IV secretion. Curr. Opin. Microbiol. 2:25-29.
10. Calamia, J., and C. Manoil. 1990. lac permease of Escherichia coli: topology and sequence elements promoting membrane insertion. Proc. Natl. Acad. Sci. USA 87:4937-4941.
11. 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.
12. Chen, L., C. M. Li, and E. W. Nester. 2000. Transferred DNA (T-DNA)-associated proteins of Agrobacterium tumefaciens are exported independently of virB. Proc. Natl. Acad. Sci. USA 97:7545-7550.
13. Christie, P. J. 2001. Type IV secretion: intercellular transfer of macromolecules by systems ancestrally-related to conjugation machines. Mol. Microbiol. 40:294-305.
14. Covacci, A., J. L. Telford, G. Del Giudice, J. Parsonnet, and R. Rappuoli. 1999. Helicobacter pylori virulence and genetic geography. Science 284:1328-1333.
15. Dang, T. A., X.-R. Zhou, B. Graf, and P. J. Christie. 1999. Dimerization of the Agrobacterium tumefaciens VirB4 ATPase and the effect of ATP-binding cassette mutations on assembly and function of the T-DNA transporter. Mol. Microbiol. 32:1239-1253.
16. Das, A., and Y.-H. Xie. 2000. The Agrobacterium T-DNA transport pore proteins VirB8, VirB9, and VirB10 interact with one another. J. Bacteriol. 182:758-763.
17. Dassa, E., and S. Muir. 1993. Membrane topology of MalG, an inner membrane protein from the maltose transport system of Escherichia coli. Mol. Microbiol. 7:29-38.
18. Ding, Z., Z. Zhao, S. Jakubowski, A. Krishnamohan, W. Margolin, and P. J. Christie. 2002. A novel cytology-based, two-hybrid screen for bacteria applied to protein-protein interaction studies of a type IV secretion system. J. Bacteriol. 184:5572-5582.
19. Fernandez, D., T. A. Dang, G. M. Spudich, X.-R. Zhou, B. R. Berger, and P. J. Christie. 1996, The 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.
20. 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.
21. Fullner, K. J. 1998. Role of Agrobacterium virB genes in transfer of T complexes and RSF1010. J. Bacteriol. 180:430-434.
22. 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.
23. Gouffi, K., C. L. Santini, and L. F. Wu. 2002. Topology determination and functional analysis of the Escherichia coli TatC protein. FEBS Lett. 525:65-70.
24. Hapfelmeier, S., N. Domke, P. C. Zambryski, and C. Baron. 2000. VirB6 is required for stabilization of VirB5 and VirB3 and formation of VirB7 homodimers in Agrobacterium tumefaciens. J. Bacteriol. 182:4505-4511.
25. Hofreuter, D., S. Odenbreit, and R. Haas. 2001. Natural transformation competence in Helicobacter pylori is mediated by the basic components of a type IV secretion system. Mol. Microbiol. 41:379-391.
26. Jin, S. G., T. Komari, M. P. Gordon, and E. W. Nester. 1987. Genes responsible for the supervirulence phenotype of Agrobacterium tumefaciens A281. J. Bacteriol. 169:4417-4425.
27. Krall, L., U. Wiedemann, G. Unsin, S. Weiss, N. Domke, and C. Baron. 2002. Detergent extraction identifies different VirB protein subassemblies of the type IV secretion machinery in the membranes of Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA 99:11405-11410.
28. Kumar, R. B., and A. Das. 2002. Polar location and functional domains of the Agrobacterium tumefaciens DNA transfer protein VirD4. Mol. Microbiol. 43:1523-1532.
29. Kumar, R. B., Y. H. Xie, and A. Das. 2000. Subcellular localization of the Agrobacterium tumefaciens T-DNA transport pore proteins: VirB8 is essential for the assembly of the transport pore. Mol. Microbiol. 36:608-617.
30. Lai, E. M., O. Chesnokova, L. M. Banta, and C. I. Kado. 2000. Genetic and environmental factors affecting T-pilin export and T-pilus biogenesis in relation to flagellation of Agrobacterium tumefaciens. J. Bacteriol. 182:3705-3716.
31. Lai, E. M., and C. I. Kado. 1998. Processed VirB2 is the major subunit of the promiscuous pilus of Agrobacterium tumefaciens. J. Bacteriol. 180:2711-2717.
32. Llosa, M., F. X. Gomis-Ruth, M. Coll, and F. de la Cruz. 2002. Bacterial conjugation: a two-step mechanism for DNA transport. Mol. Microbiol. 45:1-8.
33. Luirink, J., T. Samuelsson, and J. W. de Gier. 2001. YidC/Oxa1p/Alb3: evolutionarily conserved mediators of membrane protein assembly. FEBS Lett. 501:1-5.
34. Moore, D., K. Maneewannakul, S. Maneewannakul, J. H. Wu, K. Ippen-Ihler, and D. E. Bradley. 1990. Characterization of the F-plasmid conjugative transfer gene traU. J. Bacteriol. 172:4263-4270.
35. Otten, L., H. De Greve, J. Leemans, R. Hain, P. Hooykaas, and J. Schell. 1984. 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.
36. Pantoja, M., L. Chen, Y. Chen, and E. W. Nester. 2002. Agrobacterium type IV secretion is a two-step process in which export substrates associate with the virulence protein VirJ in the periplasm. Mol. Microbiol. 45:1325-1335.
37. Rashkova, S. 1998. Ph.D. thesis. The University of Texas-Houston Medical School, Houston.
38. Rashkova, S., G. M. Spudich, and P. J. Christie. 1997. Mutational analysis of the Agrobacterium tumefaciens VirB11 ATPase: identification of functional domains and evidence for multimerization. J. Bacteriol. 179:583-589.
39. Sagulenko, E., V. Sagulenko, J. Chen, and P. J. Christie. 2001. Role of Agrobacterium VirB11 ATPase in T-pilus assembly and substrate selection. J. Bacteriol. 183:5813-5825.
40. Sagulenko, V., E. Sagulenko, S. Jakubowski, E. Spudich, and P. J. Christie. 2001. VirB7 lipoprotein is exocellular and associates with the Agrobacterium tumefaciens T pilus. J. Bacteriol. 183:3642-3651.
41. Simon, R., U. Priefer, and A. Puhler. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1:37-45.
42. 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.
43. Stachel, S. E., and E. W. Nester. 1986. The genetic and transcriptional organization of the vir region of the A6 Ti. EMBO J. 5:1445-1454.
44. Vergunst, A. C., B. Schrammeijer, A. den Dulk-Ras, C. M. de Vlaam, T. J. Regensburg-Tuink, and P. J. Hooykaas. 2000. VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290:979-982.
45. Ward, D. V., O. Draper, J. R. Zupan, and P. C. Zambryski. 2002. Inaugural article: peptide linkage mapping of the Agrobacterium tumefaciens vir-encoded type IV secretion system reveals protein subassemblies. Proc. Natl. Acad. Sci. USA 99:11493-11500.
46. Ward, J. E., D. E. Akiyoshi, D. Reiger, 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., 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.
48. Watson, B., T. C. Currier, M. P. Gordon, M. D. Chilton, and E. W. Nester. 1975. Plasmid required for virulence of Agrobacterium tumefaciens. J. Bacteriol. 123:255-264.
49. Yakushi, T., K. Masuda, S. Narita, S. Matsuyama, and H. Tokuda. 2000. A new ABC transporter mediating the detachment of lipid-modified proteins from membranes. Nat. Cell Biol. 2:212-218.
50. Zhao, Z., E. Sagulenko, Z. Ding, and P. J. Christie. 2001. Activities of virE1 and the VirE1 secretion chaperone in export of the multifunctional VirE2 effector via an Agrobacterium type IV secretion pathway. J. Bacteriol. 183: 3855-3865.
51. Zhou, X.-R., and P. J. Christie. 1999. Mutagenesis of Agrobacterium VirE2 single-stranded DNA-binding protein identifies regions required for self-association and interaction with VirE1 and a permissive site for hybrid protein construction. J. Bacteriol. 181:4342-4352.