Type IV secretion systems in pathogenic bacteria

International Journal of Medical Microbiology

Volumn 292, Issue 3-4, 2002, Pages 159-168

  Fischer, Wolfgang ^a   Haas, Rainer ^a   Odenbreit, Stefan ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Natural transformation; Protein translocation; Type IV secretion; VirB

Indexed keywords

EID: 0036744276     PISSN: 14384221     EISSN: None     Source Type: Journal    
DOI: 10.1078/1438-4221-00199     Document Type: Short Survey

References (91)

1. Allen, L. A., Schlesinger, L. S., Kang, B.: Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J. Exp. Med. 191, 115-128 (2000).
2. Anderson, L. B., Hertzel, A. V., Das, A.: Agrobacterium tumefaciens VirB7 and VirB9 form a disulfide-linked protein complex. Proc. Natl. Acad. Sci. USA 93, 8889-8894 (1996).
3. Andersson, S. G., Zomorodipour, A., Andersson, J. O., Sicheritz-Ponten, T., Alsmark, U.C., Podowski, R. M., Naslund, A. K., Eriksson, A. S., Winkler, H. H., Kurland, C. G.: The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133-140 (1998).
4. Asahi, M., Azuma, T., Ito, S., Ito, Y., Suto, H., Nagai, Y., Tsubokawa, M., Tohyama, Y., Maeda, S., Omata, M., Suzuki, T., Sasakawa, C.: Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J. Exp. Med. 191, 593-602 (2000).
5. Backert, S., Moese, S., Selbach, M., Brinkmann, V., Meyer, T. F.: Phosphorylation of tyrosine 972 of the Helicobacter pylori CagA protein is essential for induction of a scattering phenotype in gastric epithelial cells. Mol. Microbiol. 42, 631-644 (2001).
6. Backert, S., Ziska, E., Brinkmann, V., Zimny-Arndt, U., Fauconnier, A., Jungblut, P. R., Naumann, M., Meyer, T. F.: Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell. Microbiol. 2, 155-164 (2000).
7. Bacon, D. J., Alm, R. A., Burr, D. H., Hu, L., Kopecko, D. J., Ewing, C. P., Trust, T. J., Guerry, P.: Involvement of a plasmid in virulence of Campylobacter jejuni 81-176. Infect. Immun. 68, 4384-4390 (2000).
8. Beaupré, C. E., Bohne, J., Dale, E. M., Binns, A. N.: Interactions between VirB9 and VirB10 membrane proteins involved in movement of DNA from Agrobacterium tumefaciens into plant cells. J. Bacteriol. 179, 78-89 (1997).
9. Berger, B. R., Christie, P. J.: Genetic complementation analysis of the Agrobacterium tumefaciens virB operon: virB2 through virB11 are essential virulence genes. J. Bacteriol. 176, 3646-3660 (1994).
10. Binet, R., Letoffe, S., Ghigo, J. M., Delepelaire, P., Wandersman, C.: Protein secretion by Gram-negative bacterial ABC exporters - a review. Gene 192, 7-11 (1997).
11. Bohne, J., Yim, A., Binns, A. N.: 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 (1998).
12. Burns, D. L.: Biochemistry of type IV secretion. Curr. Opin. Microbiol. 2, 25-29 (1999).
13. Cabezon, E., Sastre, J. I., De La Cruz, F.: Genetic evidence of a coupling role for the TraG protein family in bacterial conjugation. Mol. Gen. Genet. 254, 400-406 (1997).
14. Censini, S., Lange, C., Xiang, Z., Crabtree, J. E., Ghiara, P., Borodovsky, M., Rappuoli, R., Covacci, A.: cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA 93, 14648-14653 (1996).
15. Censini, S., Stein, M., Covacci, A.: Cellular responses induced after contact with Helicobacter pylori. Curr. Opin. Microbiol. 4, 41-46 (2001).
16. Chen, L., Li, C. M., Nester, E. W.: Transferred DNA (T-DNA)-associated proteins of Agrobacterium tumefaciens are exported independently of virB. Proc. Natl. Acad. Sci. USA 97, 7545-7550 (2000).
17. Christie, P. J.: Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria. J. Bacteriol. 179, 3085-3094 (1997).
18. Christie, P. J.: Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40, 294-305 (2001).
19. Christie, P. J., Vogel, J. P.: Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol. 8, 354-360 (2000).
20. Christie, P. J., Ward, J. E., Winans, S. C., Nester, E. W.: The Agrobacterium tumefaciens virE2 gene product is a single-stranded-DNA-binding protein that associates with T-DNA. J. Bacteriol. 170, 2659-2667 (1988).
21. Churin, Y., Kardalinou, E., Meyer, T. F., Naumann, M.: Pathogenicity island-dependent activation of Rho GTPases Rac1 and Cdc42 in Helicobacter pylori infection. Mol. Microbiol. 40, 815-823 (2001).
22. Citovsky, V., Zupan, J., Warnick, D., Zambryski, P.: Nuclear localization of Agrobacterium VirE2 protein in plant cells. Science 256, 1802-1805 (1992).
23. Coers, J., Monahan, C., Roy, C. R.: Modulation of phagosome biogenesis by Legionella pneumophila creates an organelle permissive for intracellular growth. Nat. Cell Biol. 1, 451-453 (1999).
24. Comerci, D. J., Martinez-Lorenzo, M. J., Sieira, R., Gorvel, J. P., Ugalde, R. A.: Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole. Cell. Microbiol. 3, 159-168 (2001).
25. Covacci, A., Censini, S., Bugnoli, M., Petracca, R., Burroni, D., Macchia, G., Massone, A., Papini, E., Xiang, Z., Figura, N., Rappuoli, R.: Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc. Natl. Acad. Sci. USA 90, 5791-5795 (1993).
26. Crabtree, J. E., Farmery, S. M., Lindley, I. J., Figura, N., Peichl, P., Tompkins, D. S.: CagA/cytotoxic strains of Helicobacter pylori and interleukin-8 in gastric epithelial cell lines. J. Clin. Pathol. 47, 945-950 (1994).
27. Craig-Mylius, K. A., Weiss, A. A.: Mutants in the ptlA-H genes of Bordetella pertussis are deficient for pertussis toxin secretion. FEMS Microbiol. Lett. 179, 479-484 (1999).
28. Dang, T. A., Zhou, X. R., Graf, B., Christie, P. J.: Dimerization of the Agrobacterium tumefaciens VirB4 ATPase and the effect of ATP-binding cassette mutations on the assembly and function of the T-DNA transporter. Mol. Microbiol. 32, 1239-1253 (1999).
29. Das, A., Xie, Y. H.: Construction of transposon Tn3phoA: its application in defining the membrane topology of the Agrobacterium tumefaciens DNA transfer proteins. Mol. Microbiol. 27, 405-414 (1998).
30. Das, A., Xie, Y. H.: The Agrobacterium T-DNA transport pore proteins VirB8, VirB9, and VirB10 interact with one another. J. Bacteriol. 182, 758-763 (2000).
31. Dehio, C.: Bartonella interactions with endothelial cells and erythrocytes. Trends Microbiol. 9, 279-285 (2001).
32. Delrue, R. M., Martinez-Lorenzo, M., Lestrate, P., Danese, I., Bielarz, V., Mertens, P., De Bolle, X., Tibor, A., Gorvel, J. P., Letesson, J. J.: Identification of Brucella spp. genes involved in intracellular trafficking. Cell. Microbiol. 3, 487-497 (2001).
33. Dubnau, D.: DNA uptake in bacteria. Annu. Rev. Microbiol. 53, 217-244 (1999).
34. Dumas, F., Duckely, M., Pelczar, P., Van Gelder, P., Hohn, B.: An Agrobacterium VirE2 channel for transferred-DNA transport into plant cells. Proc. Natl. Acad. Sci. USA 98, 485-490 (2001).
35. Duménil, G., Isberg, R. R.: The Legionella pneumophila IcmR protein exhibits chaperone activity for IcmQ by preventing its participation in high-molecular-weight complexes. Mol. Microbiol. 40, 1113-1127 (2001).
36. Eisenbrandt, R., Kalkum, M., Lai, E. M., Lurz, R., Kado, C. I., Lanka, E.: Conjugative pili of IncP plasmids, and the Ti plasmid T pilus are composed of cyclic subunits. J. Biol. Chem. 274, 22548-22555 (1999).
37. Farizo, K. M., Huang, T., Burns, D. L.: Importance of holotoxin assembly in Ptl-mediated secretion of pertussis toxin from Bordetella pertussis. Infect. Immun. 68, 4049-4054 (2000).
38. Fischer, W., Püls, J., Buhrdorf, R., Gebert, B., Odenbreit, S., Haas, R.: 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 (2001).
39. Foulongne, V., Bourg, G., Cazevieille, C., Michaux-Charachon, S., O'Callaghan, D.: Identification of Brucella suis genes affecting intracellular survival in an in vitro human macrophage infection model by signature-tagged transposon mutagenesis. Infect. Immun. 68, 1297-1303 (2000).
40. Galli, D. M., Chen, J., Novak, K. F., Leblanc, D. J.: Nucleotide sequence and analysis of conjugative plasmid pVT745. J. Bacteriol. 183, 1585-1594 (2001).
41. 1-ATPase. Nature 409, 637-641 (2001).
42. Hamilton, C. M., Lee, H., Li, P. L., Cook, D. M., Piper, K. R., von Bodman, S. B., Lanka, E., Ream, W., Farrand, S. K.: TraG from RP4 and TraG and VirD4 from Ti plasmids confer relaxosome specificity to the conjugal transfer system of pTiC58. J. Bacteriol. 182, 1541-1548 (2000).
43. Hapfelmeier, S., Domke, N., Zambryski, P. C., Baron, C.: VirB6 is required for stabilization of VirB5 and VirB3 and formation of VirB7 homodimers in Agrobacterium tumefaciens. J. Bacteriol. 182, 4505-4511 (2000).
44. Henderson, I. R., Cappello, R., Nataro, J. P.: Autotransporter proteins, evolution and redefining protein secretion. Trends Microbiol. 8, 529-532 (2000).
45. Hilbi, H., Segal, G., Shuman, H. A.: Icm/Dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol. Microbiol. 42, 603-617 (2001).
46. Hobbs, M., Mattick, J. S.: Common components in the assembly of type 4 fimbriae, 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 (1993).
47. Hofreuter, D., Odenbreit, S., Püls, J., Schwan, D., Haas, R.: Genetic competence in Helicobacter pylori: mechanisms and biological implications. Res. Microbiol. 151, 487-491 (2000).
48. Hofreuter, D., Odenbreit, S., Haas, R.: Natural transformation competence in Helicobacter pylori is mediated by the basic components of a type IV secretion system. Mol. Microbiol. 41, 379-391 (2001).
49. Hong, P. C., Tsolis, R. M., Ficht, T. A.: Identification of genes required for chronic persistence of Brucella abortus in mice. Infect. Immun. 68, 4102-4107 (2000).
50. Keates, S., Sougioultzis, S., Keates, A. C., Zhao, D., Peek, R. M. J., Shaw, L. M., Kelly, C. P.: cag+Helicobacter pylori induce transactivation of the epidermal growth factor receptor in AGS gastric epithelial cells. J. Biol. Chem. 276, 48127-48134 (2001).
51. Kirby, J. E., Vogel, J. P., Andrews, H. L., Isberg, R. R.: Evidence for pore-forming ability by Legionella pneumophila. Mol. Microbiol. 27, 323-336 (1998).
52. Krause, S., Barcena, M., Pansegrau, W., Lurz, R., Carazo, J. M., Lanka, E.: Sequence-related protein export NTPases encoded by the conjugative transfer region of RP4 and by the cag pathogenicity island of Helicobacter pylori share similar hexameric ring structures. Proc. Natl. Acad. Sci. USA 97, 3067-3072 (2000a).
53. Krause, S., Pansegrau, W., Lurz, R., De La Cruz, F., Lanka, E.: Enzymology of type IV macromolecule secretion systems: the conjugative transfer regions of plasmids RP4 and R388 and the cag pathogenicity island of Helicobacter pylori encode structurally and functionally related nucleoside triphosphate hydrolases. J. Bacteriol. 182, 2761-2770 (2000b).
54. Kumar, R. B., Xie, Y. H., Das, A.: 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 (2000).
55. Méresse, S., Steele-Mortimer, O., Moreno, E., Desjardins, M., Finlay, B., Gorvel, J. P.: Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nat. Cell Biol. 1, E183-E188 (1999).
56. Moncalian, G., Cabezon, E., Alkorta, I., Valle, M., Moro, F., Valpuesta, J. M., Goni, F. M., De La Cruz, F.: Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation. J. Biol. Chem. 274, 36117-36124 (1999).
57. Nagai, H., Roy, C. R.: The DotA protein from Legionella pneumophila is secreted by a novel process that requires the Dot/Icm transporter. EMBO J. 20, 5962-5970 (2001).
58. Naumann, M.: Host cell signaling in Helicobacter pylori infection. Int. J. Med. Microbiol. 291, 299-305 (2001).
59. O'Callaghan, D., Cazevieille, C., Allardet-Servent, A., Boschiroli, M. L., Bourg, G., Foulongne, V., Frutos, P., Kulakov, Y., Ramuz, M.: 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 (1999).
60. Odenbreit, S., Gebert, B., Püls, J., Fischer, W., Haas, R.: Interaction of Helicobacter pylori with professional phagocytes: role of the cag pathogenicity island and translocation, phosphorylation and processing of CagA. Cell. Microbiol. 3, 21-31 (2001).
61. Odenbreit, S., Püls, J., Sedlmaier, B., Gerland, E., Fischer, W., Haas, R.: Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287, 1497-1500 (2000).
62. Ogata, H., Audic, S., Renesto-Audiffren, P., Fournier, P. E., Barbe, V., Samson, D., Roux, V., Cossart, P., Weissenbach, J., Claverie, J. M., Raoult, D.: Mechanisms of evolution in Rickettsia conorii and R. prowazekii. Science 293, 2093-2098 (2001).
63. Padmalayam, I., Karem, K., Baumstark, B., Massung, R.: The gene encoding the 17-kDa antigen of Bartonella henselae is located within a cluster of genes homologous to the virB virulence operon. DNA Cell Biol. 19, 377-382 (2000).
64. Planet, P. J., Kachlany, S. C., DeSalle, R., Figurski, D. H.: Phylogeny of genes for secretion NTPases: identification of the widespread tadA subfamily and development of a diagnostic key for gene classification. Proc. Natl. Acad. Sci. USA 98, 2503-2508 (2001).
65. Plano, G. V., Day, J. B., Ferracci, F.: Type III export: new uses for an old pathway. Mol. Microbiol. 40, 284-293 (2001).
66. Püls, J., Fischer, W., Haas, R.: Activation of Helicobacter pylori CagA by tyrosine phosphorylation is essential for dephosphorylation of host cell proteins in gastric epithelial cells. Mol. Microbiol. 43, 961-969 (2002).
67. Ramarao, N., Gray-Owen, S. D., Backert, S., Meyer, T. F.: Helicobacter pylori inhibits phagocytosis by professional phagocytes involving type IV secretion components. Mol. Microbiol. 37, 1389-1404 (2000).
68. Roy, C. R., Berger, K. H., Isberg, R. R.: Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol. Microbiol. 28, 663-674 (1998).
69. Sagulenko, E., Sagulenko, V., Chen, J., Christie, P. J.: Role of Agrobacterium VirB11 ATPase in T-pilus assembly and substrate selection. J. Bacteriol. 183, 5813-5825 (2001b).
70. Sagulenko, V., Sagulenko, E., Jakubowski, S., Spudich, E., Christie, P. J.: VirB7 lipoprotein is exocellular and associates with the Agrobacterium tumefaciens T pilus. J. Bacteriol. 183, 3642-3651 (2001a).
71. Sandkvist, M.: Biology of type II secretion. Mol. Microbiol. 40, 271-283 (2001).
72. Schmidt-Eisenlohr, H., Domke, N., Angerer, C., Wanner, G., Zambryski, P. C., Baron, C.: Vir proteins stabilize VirB5 and mediate its association with the T pilus of Agrobacterium tumefaciens. J. Bacteriol. 181, 7485-7492 (1999).
73. Schmiederer, M., Anderson, B.: Cloning, sequencing, and expression of three Bartonella henselae genes homologous to the Agrobacterium tumefaciens VirB region. DNA Cell Biol. 19, 141-147 (2000).
74. Schmiederer, M., Arcenas, R., Widen, R., Valkov, N., Anderson, B.: Intracellular induction of the Bartonella henselae virB operon by human endothelial cells. Infect. Immun. 69, 6495-6502 (2001).
75. Segal, E. D., Cha, J., Lo, J., Falkow, S., Tompkins, L. S.: Altered states: involvement of phosphorylated CagA in the induction of host cellular growth changes by Helicobacter pylori. Proc. Natl. Acad. Sci. USA 96, 14559-14564 (1999a).
76. Segal, G., Russo, J. J., Shuman, H. A.: Relationships between a new type IV secretion system and the icm/ dot virulence system of Legionella pneumophila. Mol. Microbiol. 34, 799-809 (1999b).
77. Segal, G., Shuman, H. A.: Possible origin of the Legionella pneumophila virulence genes and their relation to Coxiella burnetii. Mol. Microbiol. 33, 669-670 (1999).
78. Sieira, R., Comerci, D. J., Sanchez, D. O., Ugalde, R. A.: A homologue of an operon required for DNA transfer in Agrobacterium is required in Brucella abortus for virulence and intracellular multiplication. J. Bacteriol. 182, 4849-4855 (2000).
79. Simone, M., McCullen, C. A., Stahl, L. E., Binns, A. N.: The carboxy-terminus of VirE2 from Agrobacterium tumefaciens is required for its transport to host cells by the virB-encoded type IV transport system. Mol. Microbiol. 41, 1283-1293 (2001).
80. Stein, M., Bagnoli, F., Halenbeck, R., Rappuoli, R., Fantl, W. J., Covacci, A.: c-Src/Lyn kinases activate Helicobacter pylori CagA through tyrosine-phosphorylation of the EPIYA motifs. Mol. Microbiol. 43, 971-980 (2002).
81. Stein, M., Rappuoli, R., Covacci, A.: Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc. Natl. Acad. Sci. USA 97, 1263-1268 (2000).
82. Swanson, M. S., Hammer, B. K.: Legionella pneumophila pathogenesis: a fateful journey from amoebae to macrophages. Annu. Rev. Microbiol. 54, 567-613 (2000).
83. Szpirer, C. Y., Faelen, M., Couturier, M.: Interaction between the RP4 coupling protein TraG and the pBHR1 mobilization protein Mob. Mol. Microbiol. 37, 1283-1292 (2000).
84. Vergunst, A. C., Schrammeijer, B., den Dulk-Ras, A., de Vlaam, C. M., Regensburg-Tuink, T. J., Hooykaas, P. J.: VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290, 979-982 (2000).
85. Vogel, J. P., Andrews, H. L., Wong, S. K., Isberg, R. R.: Conjugative transfer by the virulence system of Legionella pneumophila. Science 279, 873-876 (1998).
86. Watarai, M., Andrews, H. L., Isberg, R. R.: Formation of a fibrous structure on the surface of Legionella pneumophila associated with exposure of DotH and DotO proteins after intracellular growth. Mol. Microbiol. 39, 313-329 (2001b).
87. Watarai, M., Derre, I., Kirby, J., Growney, J. D., Dietrich, W. F., Isberg, R. R.: Legionella pneumophila is internalized by a macropinocytotic uptake pathway controlled by the Dot/Icm system and the mouse Lgn1 locus. J. Exp. Med. 194, 1081-1096 (2001a).
88. Weiss, A. A., Johnson, F. D., Burns, D. L.: Molecular characterization of an operon required for pertussis toxin secretion. Proc. Natl. Acad. Sci. USA 90, 2970-2974 (1993).
89. Yeo, H. J., Savvides, S. N., Herr, A. B., Lanka, E., Waksman, G.: Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion system. Mol. Cell 6, 1461-1472 (2000).
90. Zechner, E. L., De La Cruz, F., Eisenbrandt, R., Grahn, A. M., Koraimann, G., Lanka, E., Muth, G., Pansegrau, W., Thomas, C. M., Wilkins, B. M., Zatyka, M.: Conjugative DNA transfer processes. In: The horizontal gene pool: bacterial plasmids and gene spread (C. M. Thomas, ed.), pp. 87-174. Harwood Academic Publishers, Amsterdam, The Netherlands 1999.
91. Zhu, J., Oger, P. M., Schrammeijer, B., Hooykaas, P. J., Farrand, S. K., Winans, S. C.: The bases of crown gall tumorigenesis. J. Bacteriol. 182, 3885-3895 (2000).