VirB1 Orthologs from Brucella suis and pKM101 Complement Defects of the Lytic Transglycosylase Required for Efficient Type IV Secretion from Agrobacterium tumefaciens

Journal of Bacteriology

Volumn 186, Issue 5, 2004, Pages 1415-1422

  Höppner, Christoph ^a   Liu, Zhenying ^b   Domke, Natalie ^a   Binns, Andrew N ^b   Baron, Christian ^a,c  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; BACTERIAL PROTEIN; GLUTAMIC ACID; PROTEIN VIRB1; PROTEIN VIRB1S; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BACTERIUM PILUS; BRUCELLA SUIS; ENZYME ACTIVE SITE; EUKARYOTIC CELL; GENE TRANSFER; GENETIC COMPLEMENTATION; GRAM NEGATIVE BACTERIUM; HELICOBACTER PYLORI; NONHUMAN; OPEN READING FRAME; PATHOGENICITY ISLAND; PLANT DAMAGE; PLANT TUMOR; PLASMID; PRIORITY JOURNAL; RHIZOBIUM RADIOBACTER; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BRUCELLA SUIS; CONJUGATION, GENETIC; GENE DELETION; GENE TRANSFER, HORIZONTAL; GENETIC COMPLEMENTATION TEST; GLYCOSYLTRANSFERASES; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PLANT TUMORS; PLASMIDS; RHIZOBIUM RADIOBACTER; TOBACCO; VIRULENCE; VIRULENCE FACTORS;

AGROBACTERIUM TUMEFACIENS; ANIMALIA; BACTERIA (MICROORGANISMS); BRUCELLA; BRUCELLA MELITENSIS BIOVAR SUIS; EUKARYOTA; HELICOBACTER PYLORI; NEGIBACTERIA; PROKARYOTA;

EID: 10744225464     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.5.1415-1422.2004     Document Type: Article

References (56)

1. 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.
2. Baron, C., M. Llosa, S. Zhou, and P. C. Zambryski. 1997. C-terminal processing and cellular localization of VirB1, a component of the T-complex transfer machinery of Agrobacterium tumefaciens. J. Bacteriol. 179:1203-1210.
3. Baron, C., D. O'Callaghan, and E. Lanka. 2002. Bacterial secrets of secretion: EuroConference on the biology of type IV secretion processes. Mol. Microbiol. 43:1359-1366.
4. Baron, C., Y. R. Thorstenson, and P. C. Zambryski. 1997. Biochemical analysis of the complex between the lipoprotein VirB7 and VirB9 in the membranes of Agrobacterium tumefaciens. J. Bacteriol. 179:1211-1218.
5. Bayer, M., R. Eferl, G. Zellnig, K. Terferie, 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.
6. Bayer, M., R. Iberer, K. Bischof, E. Rassi, E. Stabentheiner, G. Zellnig, and G. Koraimann. 2001, Functional and mutational analysis of P19, a DNA transfer protein with muramidase activity. J. Bacteriol. 183:3176-3183.
7. 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.
8. 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.
9. 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.
10. Cellini, C., V. S. Kalogeraki, and S. C. Winans. 1997. The hydrophobic TraM protein of pKM101 is required for conjugal transfer and sensitivity to donor-specific bacteriophage. Plasmid 37:181-188.
11. Christie, P. J. 2001. Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40:294-305.
12. Covacci, A., J. L. Telford, G. Del Giudice, J. Parsonnet, and R. Rappuoli. 1999. Helicobacterpylori virulence and genetic geography. Science 284:1328-1333.
13. Das, A., L. B. Anderson, and Y.-H. Xie. 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.
14. 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.
15. Dijkstra, A. J., and W. Keck. 1996. Peptidoglycan as a barrier to transenvelope transport. J. Bacteriol. 178:5555-5562.
16. Dijkstra, B. W., and A.-M. W. H. Thunnissen. 1994. Holy proteins II: the soluble lytic transglycosylase. Curr. Opin. Struct. Biol. 8:810-813.
17. Eisenbrandt, R., M. Kalkum, R. Lurz, and E. Lanka. 2000. Maturation of IncP pilin precursors resembles the catalytic dyad-like mechanism of leader peptidases. J. Bacteriol. 182:6751-6761.
18. 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.
19. 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.
20. Fischer, W., R. Haas, and S. Odenbreit. 2002, Type IV secretion systems in pathogenic bacteria. Int. J. Med. Microbiol. 292:159-168.
21. Fischer, W., J. Püls, R. Buhrdorf, B. Gebert, S. Odenbreit, and R. Haas. 2001. Systematic mutagenesis of the Helicobacter pylori cag pathogenicity island: essential genes for CagA translocation in host cells and induction of interleukin-8. Mol. Microbiol. 42:1337-1348.
22. 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.
23. 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.
24. Guzman, L. M., D. Belin, M. J. Carson, and J. Beckwith. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose pBAD promoter. J. Bacteriol. 177:4121-4130.
25. 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.
26. Höltje, J. V. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181-203.
27. Jakubowski, S. J., V. Krishnamoorthy, and P. J. Christie. 2003. Agrobacterium tumefaciens VirB6 protein participates in formation of VirB7 and VirB9 complexes required for type IV secretion. J. Bacteriol. 185:2867-2878.
28. Koraimann, G. 2003. Cell wall degrading enzymes in macromolecular transport systems of Gram-negative bacteria. Cell. Mol. Life Sci. 60:2371-2378.
29. 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.
30. 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.
31. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
32. 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.
33. Lai, E.-M., and C. I. Kado. 2000. The T-pilus of Agrobacterium tumefaciens. Trends Microbiol. 8:361-369.
34. Lessl, M., and E. Lanka. 1994. Common mechanisms in bacterial conjugation and Ti-mediated T-DNA transfer to plant cells. Cell 77:321-324.
35. Liu, Z., and A. N. Binns. 2003. Functional subsets of the VirB type IV transport complex proteins involved in the capacity of Agrobacterium tumefaciens to serve as a recipient in virB-mediated conjugal transfer of plasmid RSF1010. J. Bacteriol. 185:3259-3269.
36. 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.
37. Llosa, M., J. Zupan, C. Baron, and P. C. Zambryski. 2000. The N- and C-terminal portions of the Agrobacterium VirB1 protein independently enhance tumorigenesis. J. Bacteriol. 182:3437-3445.
38. Maniatis, T. A., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
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. O'Callaghan, D., C. Cazevieille, A. Allardet-Servent, M. L. Boschiroli, G. Bourg, V. Foulongne, P. Frutus, Y. Kulakov, and M. Ramuz. 1999. A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis. Mol. Microbiol. 33:1210-1220.
41. 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.
42. Rohde, M., J. Püls, R. Buhrdorf, W. Fischer, and R. Haas. 2003. A novel sheathed surface organelle of the Helicobacter pylori type IV secretion system. Mol. Microbiol. 49:219-234.
43. 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.
44. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range of 1 to 100 kDa. Anal. Biochem. 166:368-379.
45. Schmidt-Eisenlohr, H., N. Domke, C. Angerer, G. Wanner, P. C. Zambryski, and C. Baron. 1999. Vir proteins stabilize VirB5 and mediate its association with the T pilus of Agrobacterium tumefaciens. J. Bacteriol. 181:7485-7492.
46. Schmidt-Eisenlohr, H., N. Domke, and C. Baron. 1999. TraC of IncN plasmid pKM101 associates with membranes and extracellular high molecular weight structures in Escherichia coli. J. Bacteriol. 181:5563-5571.
47. Stahl, L. E., A. Jacobs, and A. N. Binns. 1998. The conjugal intermediate of plasmid RSF1010 inhibits Agrobactetium tumefaciens virulence and VirB-dependent export of VirE2. J. Bacteriol. 180:3933-3939.
48. Tabor, S., and C. Richardson. 1985. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. USA 82:1074-1078.
49. Tomb, J. F., O. White, A. R. Kerlavage, R. A. Clayton, G. G. Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quackenbush, L. Zhou, E. F. Kirkness, S. Peterson, B. Loftus, D. Richardson, R. Dodson, H. G. Khalak, A. Glodek, K. McKenney, L. M. Fitzegerald, N. Lee, M. D. Adams, and J. C. Venter. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
50. van Asselt, E. J., K. H. Kalk, and B. W. Dijkstra. 2000. Crystallographic studies of the interactions of Escherichia coli lytic transglycosylase Slt35 with peptidoglycan. Biochemistry 39:1924-1934.
51. van Asselt, E. J., A. M. Thunissen, and B. W. Dijstra. 1999. High resolution crystal structures of the Escherichia coli lytic transglycosylase Slt70 and its complex with a peptidoglycan fragment. J. Mol. Biol. 291:877-898.
52. 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.
53. Ward, D., O. Draper, J. R. Zupan, and P. C. Zambryski. 2002. Peptide linkage mapping of the A. tumefaciens vir-encoded type IV secretion system reveals novel protein subassemblies. Proc. Natl. Acad. Sci. USA 99:11493-11500.
54. Winans, S. C., and G. C. Walker. 1985. Conjugal transfer system of the N incompatibility plasmid pKM101. J. Bacteriol. 161:402-410.
55. Yanisch-Perron, C., J. Viera, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequence of the M13mp18 and pUC18 vectors. Gene 33:103-119.
56. Zechner, E. L., F. de la Cruz, R. Eisenbrandt, A. M. Grahn, G. Koraimann, E. Lanka, G. Muth, W. Pansegrau, C. M. Thomas, B. M. Wilkins, and M. Zatyka. 2000. Conjugative DNA transfer processes. Harwood Academic Publishers, Amsterdam, The Netherlands.