VirB1, a component of the T-complex transfer machinery of Agrobacterium tumefaciens, is processed to a C-terminal secreted product, virB1

Journal of Bacteriology

Volumn 179, Issue 4, 1997, Pages 1203-1210

  Baron, Christian ^a,c   Llosa, Matxalen ^a   Zhou, Sharleen ^b   Zambryski, Patricia C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b USA   (United States)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL CELL WALL; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; DNA PROTEIN COMPLEX; ENZYME LOCALIZATION; GENETIC TRANSFORMATION; IMMUNOPRECIPITATION; NONHUMAN; OPERON; PLANT CELL; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; RHIZOBIUM RADIOBACTER;

AGROBACTERIUM; AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS); VIR;

EID: 0031038982     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.4.1203-1210.1997     Document Type: Article

References (73)

1. Allaoui, A., R. Ménard, P. J. Sansonetti, and C. Parsot. 1993. Characterization of the Shigella flexneri ipgD and ipgF genes, which are located in the proximal part of the mxi locus. Infect. Immun. 61:1707-1714.
2. Anderson, L. B., A. Vogel Hertzel, and A. Das. 1996. Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. Proc. Natl. Acad. Sci. USA 93:8889-8894.
3. Barinaga, M. 1996. A shared strategy for virulence. Science 272:1261-1263.
4. 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.
5. Baron, C., and P. C. Zambryski. 1996. Plant transformation: a pilus in Agrobacterium T-DNA transfer. Current Biol. 6:1567-1569.
6. 5a. Baron, C., and P. C. Zambryski. Unpublished data.
7. Bayer, M., R. Eferl, G. Zellnig, K. Terferle, A. Dijkstra, G. Koraimann, and G. Högenauer. 1995. Gene 19 of plasmid R1 is required for both efficient conjugative DNA transfer and bacteriophage R17 infection. J. Bacteriol. 177:4279-4288.
8. Beijersbergen, A., S. J. Smith, and P. J. J. Hooykaas. 1994. Localization and topology of VirB proteins of Agrobacterium tumefaciens. Plasmid 32:212-218.
9. 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.
10. 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.
11. Binns, A. N. C. E. Beaupré, 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.
12. Binns, A. N., and M. F. Tomashow. 1988. Cell biology of Agrobacterium infection and transformation of plants. Annu. Rev. Microbiol. 42:575-606.
13. 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.
14. 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.
15. Citovsky, V., M. L. Wong, and P. C. Zambryski, 1989. Cooperative interaction of Agrobacterium VirE2 protein with single-stranded DNA: implications for the T-DNA transfer process. Proc. Natl. Acad. Sci. USA 86:1193-1197.
16. Dijkstra, A. J., and W. Keck. 1996. Peptidoglycan as a barrier to transenvelope transport. J. Bacteriol. 178:555-5562.
17. Dijkstra, B. W., and A.-M. W. H. Thunnissen. 1994. Holy proteins II: the soluble lytic transglycosylase. Curr. Opin. Struct. Biol. 8:810-813.
18. Dürrenberger, M. B., W. Villiger, and T. Bachi. 1991. Conjugational junctions: morphology of specific contacts in conjugating Escherichia coli bacteria. J. Struct. Biol. 107:146-156.
19. Ehlert, K., J.-V. Höltje, and M. F. Templin. 1995. Cloning and expression of a murein hydrolase lipoprotein from Eschericliia coli. Mol. Microbiol. 16:761-768.
20. Fernandez, D., T. A. T. 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.
21. 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.
22. Finberg, K. E., T. R. Muth, S. P. Young, J. B. Maken, S. M. Heitritter, A. N. Binns, and L. M. Banta. 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.
23. Frost, L. S., K. Ippen-Ihler, and R. A. Skurray. 1994. Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol. Rev. 58:162-210.
24. Fullner, K., 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.
25. Fullner, K. J., J. L. Lara, and E. W. Nester. 1996. Pilus assembly by Agrobacterium T-DNA transfer genes. Science 273:1107-1109.
26. Gopalan, S., D. W. Bauer, J. R. Alfano, A. O. Loniello, S. Y. He, and A. Collmer. 1996. Expression of the Pseudomonas syringae avirulence protein AvrB in plant cells alleviates its dependence on the hypersensitive response and pathogenicity (Hrp) secretion system in dieting genotype-specific hypersensitive cell death. Plant Cell 8:1095-1105.
27. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
28. Hobbs, M., and J. S. Mattick. 1993. Common components in the assembly of type 4 fimbrae. DNA transfer systems, filamentous phage and protein-secretion apparatus: a general system for the formation of surface-associated protein complexes. Mol. Microbiol. 10:233-243.
29. Höltje, J.-V. 1995. From growth to autolysis: the murein hydrolases in Escherichia coli. Arch. Microbiol. 164:243-254.
30. Hooykaas, P. J. J., and A. G. M. Beiersbergen. 1994. The virulence system of Agrobacterium tumefaciens. Annu. Rev. Phytopathol. 32:157-179.
31. Jacob-Dubuisson, F., C. Buisine, N. Mielcarek, E. Clement, F. D. Menozzi, and C. Locht. 1996. Amino-terminal maturation of the Bordetella pertussis filamentous hemagglutinin. Mol. Microbiol. 19:65-78.
32. Jones, A. L., E.-M. Lai, K. Shirasu, and C. I. Kado. 1996. VirB2 is a processed pilin-like protein encoded by the Agrobacterium tumefaciens Ti plasmid. J. Bacteriol. 178:5706-5711.
33. Jones, A. L., K. Shirasu, and C. I. Kado. 1994. The product of the virB4 gene of Agrobacterium tumefaciens promotes accumulation of VirB3 protein. J. Bacteriol. 176:5255-5261.
34. Kado, C. I. 1994. Promiscuous DNA transfer system of Agrobacterium tumefaciens: role of the virB opcron in sex pilus assembly an synthesis. Mol. Microbiol. 12:17-22.
35. Keleti, G., and W. H. Lederer. 1974. Handbook of micromethods for the biological sciences, p. 74-75. Van Nostrand Reinhold Co., New York, N.Y.
36. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
37. Lessl, M., and E. Lanka. 1994. Common mechanisms in bacterial conjugation and Ti-mediated T-DNA transfer to plant cells. Cell 77:321-324.
38. McIver, K. S., E. Kessler, J. C. Olson, and D. E. Ohman. 1995. The elastase propeptide functions as an intramolecular chaperone required for elastase activity and secretion in Pseudomonas aeruginosa. Mol. Microbiol. 18:877-889.
39. Mushegian, A. R., K. J. Fullner, E. V. Koonin, and E. W. Nester. 1996. A family of lysozyme-like virulence factors in bacterial pathogens. Proc. Natl. Acad. Sci. USA 93:7321-7326.
40. Noelken, M. E., B. J. Wisdom, and B. G. Hudson. 1981. Estimation of the size of collagenous polypeptides by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Anal. Biochem. 110:131-136.
41. O'Farrell, P. C. Z., H. M. Goodman, and P. H. O'Farrell. 1977. High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell 12:1133-1142.
42. Okamoto, S., A. Toyoda-Yamamoto, K. Ho, I. Takebe, and Y. Machida. 1988. Localization and orientation of the VirD4 protein of Agrobacterium tumefaciens in the cell membrane. Mol. Gen. Genet. 228:24-32.
43. Osborn, M. J., J. E. Gander, E. Parisi, and J. Carson. 1972. Mechanism of assembly of the outer membrane of Salmonella typhimurium: isolation and characterization of cytoplasmic and outer membrane. J. Biol. Chem. 247:3962-3972.
44. 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.
45. 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.
46. Pohlner, J., R. Halter, K. Beyreuther, and T. F. Meyer. 1987. Gene structure and extracellular secretion of Neisseria gonorrhoeas IgA protease. Nature 325:458-462.
47. Pohlner, J., U. Langenberg, U. Wölk, S. C. Beck, and T. F. Meyer. 1995. Uptake and nuclear transport of Neisseria IgA1 protcase-associated α-proteins in human cells. Mol. Microbiol. 17:1073-1083.
48. Pugsley, A. P. 1993. The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57:50-108.
49. Pugsley, A. P. 1996. Multimers of the precursor of a type IV pilin-like component of the general secretory pathway are unrelated to pili. Mol. Microbiol. 20:1235-1245.
50. Pugsley, A. P., and O. Possot. 1993. The general secretory pathway of Klebsiella oxytoca: no evidence for relocalization or assembly of pilin-like PulG into a multiprotein complex. Mol. Microbiol. 10:665-674.
51. Renauld-Mongénie, G., J. Cornette, N. Mielcarek, F. D. Menozzi, and C. Locht. 1996. Distinct roles of the N-terminal and C-terminal precursor domains in the biogenesis of the Bordetella pertussis filamentous hemagglutinin. J. Bacteriol. 178:1053-1060.
52. Rosquist, R., K. E. Magnusson, and H. Wolf-Watz. 1994. Target cell contact triggers expression and polarized transfer of Yersinia YopE cytotoxin into mammalian cells. EMBO J. 13:964-972.
53. Salmond, G. P. C. 1994. Secretion of extracellular virulence factors by plant pathogenic bacteria. Annu. Rev. Phytopathol. 32:181-200.
54. Salmond, G. P. C., and P. J. Reeves. 1993. Membrane traffic wardens and protein secretion in gram-negative bacteria. Trends Biochem. Sci. 18:7-12.
55. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfatepolyacrylamide gel electrophoresis for the separation of proteins in the range of 1 to 100 kDa. Anal. Biochem. 166:368-379.
56. Shirasu, K., and C. I. Kado. 1993. Membrane localization of the Ti plasmid VirB proteins involved in the biosynthesis of a pilin-like structure in Agrobacterium tumefaciens, FEMS Microbiol. Lett. 111:287-294.
57. Shirasu, K., Z. Koukolikova-Nicola, B. Hohn, and C. I. Kado. 1994. An inner membrane-associated 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.
58. Sory, M.-P., A. Boland, I. Lambermont, and G. R. Cornells. 1995. Identification of the YopE and YopH domains required for secretion and internalization into the cytosol of macrophages, using the cyaA gene fusion approach. Proc. Natl. Acad. Sci. USA 92:11998-12002.
59. 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 93:7512-7515.
60. Stone, K. D., H.-Z. Zhang, L. D. Carlson, and M. S. Donnenberg. 1996. A cluster of fourteen genes from enteropathogenic Escherichia colt is sufficient for the biogenesis of a type IV pilus. Mol. Microbiol. 20:325-337.
61. Sundberg, C., L. Meek, K. Carrol, A. Das, and W. Ream. 1996. VirE1 protein mediates export of the single-stranded DNA-binding protein VirE2 from Agrobacteritum tumefaciens into plant cells. J. Bacteriol. 178:1207-1212.
62. Templin, M. F., D. H. Edwards, and J.-V. Höltje. 1992. A murein hydrolase is the specific target of bulgecin in Escherichia coli. J. Biol. Chem. 267:20039-20043.
63. Thorstenson, Y. R., G. A. Kuldau, and P. C. Zarnbryski. 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.
64. Thorstenson, Y. R., and P. C. Zambryski. 1994. The essential virulence protein VirB8 localizes to the inner membrane of Agrobacterium tumefaciens. J. Bacteriol. 176:1711-1717.
65. Tummuru, M. K. R., S. A. Sharma, and M. J. Blaser. 1995. Helibacter pylori picB, a homologue of the Bordetelia pertussis toxin secretion protein, is required for induction of IL-8 in gastric epithelial cells. Mol. Microbiol. 18:867-876.
66. Wandersman, C. 1989. Secretion, processing and activation of bacterial extracellular proteases. Mol. Microbiol. 3:1825-1831.
67. 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.
68. Winans, S. C., D. L. Burns, and P. J. Christie. 1996. Adaption of a conjugal system for the export of pathogenic macromolecules. Trends Microbiol. 4:64-68.
69. Zambryski, P. C. 1992. Chronicles from the Agrobacterium-plant cell DNA transfer story. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:465-490.
70. Zambryski, P. C., H. Joos, C. Genetello, J. Leemans, M. van Montagu, and J. Schell. 1983. Ti plasmid vector for the introduction of DNA into plant cells without alteration of their normal regeneration capacity. EMBO J. 2:2143-2150.
71. Zupan, J. R., V. C. Citovsky, and P. C. Zambryski. 1996. Agrobacterium VirE2 protein mediates nuclear uptake of single-stranded DNA in plant cells. Proc. Natl. Acad. Sci. USA 93:2392-2397.
72. Zupan, J. R., and P. C. Zambryski. The Agrobacterium DNA transfer complex. Crit. Rev. Plant Sci., in press.
73. Zupan, J. R., and P. C. Zambryski. 1995. Transfer of T-DNA from Agrobac terium to the plant cell. Plant Physiol. 107:1041-1047.