The versatile bacterial type IV secretion systems (original) (raw)

• Cavelli-Sforza, L., Lederberg, J. & Lederberg. E. An infective factor controlling sex compatibility in B. coli. J. Gen. Microbiol. 8, 89–103 (1953).
  Google Scholar
• Lawley, T. D., Klimke, W. A., Gubbins, M. J. & Frost, L. S. F factor conjugation is a true type IV secretion system. FEMS Microbiol. Lett. 224, 1–15 (2003).
  Article CAS PubMed Google Scholar
• Winans, S. C., Burns, D. L. & Christie, P. J. Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol. 4, 64–68 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Censini, S. et al. 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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). Reports the discovery of a type IV secretion system that is evolutionarily related to the IncI plasmids and functions dually in conjugative transfer and effector translocation.
  Article CAS PubMed Google Scholar
• Bacon, D. J. et al. Involvement of a plasmid in virulence of Campylobacter jejuni 81–176. Infect. Immun. 68, 4384–4390 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Dillard, J. P. & Seifert, H. S. A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates. Mol. Microbiol. 41, 263–277 (2001). References 6–8 report the discoveries of new type IV translocation systems, herein termed the 'DNA uptake and release' subfamily.
  Article CAS PubMed Google Scholar
• Bundock, P., den Dulk Ras, A., Beijersbergen, A. & Hooykaas, P. J. Trans-kingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J. 14, 3206–3214 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Bates, S., Cashmore, A. M. & Wilkins, B. M. IncP plasmids are unusually effective in mediating conjugation of Escherichia coli and Saccharomyces cerevisiae. J. Bacteriol. 180, 6538–6543 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Zhu, J. et al. The bases of crown gall tumorigenesis. J. Bacteriol. 182, 3885–3895 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Waters, V. L. Conjugation between bacterial and mammalian cells. Nature Genet. 29, 375–376 (2001).
  Article CAS PubMed Google Scholar
• Grohmann, E., Muth, G. & Espinosa, M. Conjugative plasmid transfer in Gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67, 277–301 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• de la Cruz, I. & Davies, J. Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol. 8, 128–133 (2000).
  Article CAS PubMed Google Scholar
• Ghigo, J. M. Natural conjugative plasmids induce bacterial biofilm development. Nature 412, 442–445 (2001).
  Article CAS PubMed Google Scholar
• Schlievert, P. M. et al. Aggregation and binding substances enhance pathogenicity in rabbit models of Enterococcus faecalis endocarditis. Infect. Immun. 66, 218–223 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Bacon, D. J. et al. DNA sequence and mutational analyses of the pVir plasmid of Campylobacter jejuni 81–176. Infect. Immun. 70, 6242–6250 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Hofreuter, D., Odenbreit, S., Puls, J., Schwan, D. & Haas, R. Genetic competence in Helicobacter pylori: mechanisms and biological implications. Res. Microbiol. 151, 487–491 (2000).
  Article CAS PubMed Google Scholar
• Hamilton, H. L., Schwartz, K. J. & Dillard, J. P. Insertion-duplication mutagenesis of Neisseria: use in characterization of DNA transfer genes in the gonococcal genetic island. J. Bacteriol. 183, 4718–4726 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, I. & Dubnau, D. DNA transport during transformation. Front. Biosci. 8, S544–S556 (2003).
  Article CAS PubMed Google Scholar
• Blocker, A., Komoriya, K. & Aizawa, S. Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc. Natl Acad. Sci. USA 100, 3027–3030 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Christie, P. J. The Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria. J. Bacteriol. 179, 3085–3094 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Hilbi, H., Segal, G. & Shuman, H. A. Icm/Dot-dependent upregulation of phagocytosis by Legionella pneumophila. Mol. Microbiol. 42, 603–617 (2001).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Boschiroli, M. L. et al. The Brucella suis virB operon is induced intracellularly in macrophages. Proc. Natl Acad. Sci. USA 99, 1544–1549 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Seubert, A., Hiestand, R., de la Cruz, F. & Dehio, C. A bacterial conjugation machinery recruited for pathogenesis. Mol. Microbiol. 49, 1253–1266 (2003).
  Article CAS PubMed Google Scholar
• Rouot, B. et al. Production of the type IV secretion system differs among Brucella species as revealed with VirB5- and VirB8-specific antisera. Infect. Immun. 71, 1075–1082 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Baron, C., O'Callaghan, D. & Lanka, E. Bacterial secrets of secretion: EuroConference on the biology of type IV secretion processes. Mol. Microbiol. 43, 1359–1365 (2002).
  Article CAS PubMed Google Scholar
• Llosa, M., Gomis-Ruth, F. X., Coll, M. & de la Cruz, F. Bacterial conjugation: a two-step mechanism for DNA transport. Mol. Microbiol. 45, 1–8 (2002).
  Article CAS PubMed Google Scholar
• Gomis-Ruth, F. X. & Coll, M. Structure of TrwB, a gatekeeper in bacterial conjugation. Int. J. Biochem. Cell Biol. 33, 839–843 (2001).
  Article CAS PubMed Google Scholar
• Gomis-Ruth, F. X. et al. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409, 637–641 (2001). Reports the first structure of a coupling protein, a hexameric F1-ATPase-like multimer that is highly indicative of a translocase function.
  Article CAS PubMed Google Scholar
• Hormaeche, I. et al. Purification and properties of TrwB, a hexameric, ATP-binding integral membrane protein essential for R388 plasmid conjugation. J. Biol. Chem. 277, 46456–46462 (2002).
  Article CAS PubMed Google Scholar
• Errington, J., Bath, J. & Wu, L. J. DNA transport in bacteria. Nature Rev. Mol. Cell Biol. 2, 538–545 (2001).
  Article CAS Google Scholar
• Schroder, G. et al. TraG-like proteins of DNA transfer systems and of the Helicobacter pylori type IV secretion system: inner membrane gate for exported substrates? J. Bacteriol. 184, 2767–2779 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Gilmour, M. W., Gunton, J. E., Lawley, T. D. & Taylor, D. E. Interaction between the IncHI1 plasmid R27 coupling protein and type IV secretion system: TraG associates with the coiled-coil mating pair formation protein TrhB. Mol. Microbiol. 49, 105–116 (2003).
  Article CAS PubMed Google Scholar
• Llosa, M., Zunzunegui, S. & de la Cruz, F. Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes. Proc. Natl Acad. Sci. USA 100, 10465–10470 ( 2003).
  Article CAS PubMed PubMed Central Google Scholar
• Kumar, R. B. & Das, A. Polar location and functional domains of the Agrobacterium tumefaciens DNA transfer protein VirD4. Mol. Microbiol. 43, 1523–1532 (2002).
  Article CAS PubMed Google Scholar
• Ding, Z. et al. 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 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Atmakuri, K., Ding, Z. & Christie, P. J. VirE2, a type IV secretion substrate, interacts with the VirD4 transfer protein at the cell poles of Agrobacterium tumefaciens. Mol. Microbiol. 49, 1699–1713 (2003). Reports the first direct evidence for recruitment of a protein effector to a coupling protein, supporting a proposal that the coupling proteins function as general recruitment factors for type IV secretion substrates.
  Article CAS PubMed PubMed Central Google Scholar
• Vergunst, A. C. et al. VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290, 979–982 (2000). This elegant study supplied the first incontrovertible evidence for protein trafficking by the A. tumefaciens VirB/D4 type IV secretion system.
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Schrammeijer, B., den Dulk-Ras A, Vergunst, A. C., Jurado Jacome, E. & Hooykaas, P. J. Analysis of Vir protein translocation from Agrobacterium tumefaciens using Saccharomyces cerevisiae as a model: evidence for transport of a novel effector protein VirE3. Nucl. Acids Res. 31, 860–868 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Selbach, M., Moese, S., Meyer, T. F. & Backert, S. Functional analysis of the Helicobacter pylori cag pathogenicity island reveals both VirD4-CagA-dependent and VirD4-CagA-independent mechanisms. Infect. Immun. 70, 665–667 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Conover, G. M., Derre, I., Vogel, J. P. & Isberg, R. R. The Legionella pneumophila LidA protein: a translocated substrate of the Dot/Icm system associated with maintenance of bacterial integrity. Mol. Microbiol. 48, 305–321 (2003). Describes the discovery of a novel effector, LidA, that is required for elaboration of the L. pneumophila Dot/Icm complex in the bacterium and, on translocation, functions in vesicle recruitment during biogenesis of the replication vacuole.
  Article CAS PubMed Google Scholar
• Burns, D. L. Type IV transporters of pathogenic bacteria. Curr. Opin. Microbiol. 6, 29–34 (2003).
  Article CAS PubMed Google Scholar
• O'Callaghan, D. et al. 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).
  Article CAS PubMed Google Scholar
• Lai, E. M. & Kado, C. I. The T-pilus of Agrobacterium tumefaciens. Trends Microbiol. 8, 361–369 (2000).
  Article CAS PubMed Google Scholar
• Eisenbrandt, R. et al. Conjugative pili of IncP plasmids, and the Ti plasmid T pilus are composed of cyclic subunits. J. Biol. Chem. 274, 22548–22555 (1999). Provides evidence that the pilin subunits of the A. tumefaciens VirB/D4 and the plasmid RP4 Tra systems undergo head-to-tail cyclization during maturation, a completely new reaction in bacteria.
  Article CAS PubMed Google Scholar
• Schmidt-Eisenlohr, H. et al. Vir proteins stabilize VirB5 and mediate its association with the T pilus of Agrobacterium tumefaciens. J. Bacteriol. 181, 7485–7492 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• 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 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Baron, C., Llosa, M., Zhou, S. & Zambryski, P. C. VirB1, a component of the T-complex transfer machinery of Agrobacterium tumefaciens, is processed to a C-terminal secreted product, VirB1*. J. Bacteriol. 179, 1203–1210 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Das, A., Anderson, L. B. & Xie, Y. H. Delineation of the interaction domains of Agrobacterium tumefaciens VirB7 and VirB9 by use of the yeast two-hybrid assay. J. Bacteriol. 179, 3404–3409 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Beauprè, 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).
  Article PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Ward, D. V., Draper, O., Zupan, J. R. & Zambryski, P. C. Peptide linkage mapping of the _Agrobacterium tumefaciens vir_-encoded type IV secretion system reveals protein subassemblies. Proc. Natl Acad. Sci. USA 99, 11493–11500 (2002). Reports a comprehensive linkage map of the VirB proteins by yeast dihybrid screens.
  Article CAS PubMed PubMed Central Google Scholar
• Krall, L. et al. 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 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Jakubowski, S. J., Krishnamoorthy, V. & Christie, P. J. Agrobacterium tumefaciens VirB6 protein participates in formation of VirB7 and VirB9 complexes required for type IV secretion. J. Bacteriol. 185, 2867–2878 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Rambow-Larsen, A. A. & Weiss, A. A. The PtlE protein of Bordetella pertussis has peptidoglycanase activity required for Ptl-mediated pertussis toxin secretion. J. Bacteriol. 184, 2863–2869 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Farizo, K. M., Cafarella, T. G. & Burns, D. L. Evidence for a ninth gene, ptlI, in the locus encoding the pertussis toxin secretion system of Bordetella pertussis and formation of a PtlI–PtlF complex. J. Biol. Chem. 271, 31643–31649 (1996).
  Article CAS PubMed Google Scholar
• Harris, R. L., Hombs, V. & Silverman, P. M. Evidence that F-plasmid proteins TraV, TraK and TraB assemble into an envelope-spanning structure in Escherichia coli. Mol. Microbiol. 42, 757–766 (2001).
  Article CAS PubMed Google Scholar
• Liu, Z. & Binns, A. N. 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 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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 system. Mol. Cell 6, 1461–1472 (2000). Reports the first structure of a member of the VirB11 superfamily of traffic ATPases.
  Article CAS PubMed Google Scholar
• Savvides, S. N. et al. VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J. 22, 1969–1980 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Rabel, C., Grahn, A. M., Lurz, R. & Lanka, E. The VirB4 family of proposed traffic nucleoside triphosphatases: Common motifs in plasmid RP4 TrbE are essential for conjugation and phage adsorption. J. Bacteriol. 185, 1045–1058 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• 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 assembly and function of the T-DNA transporter. Mol. Microbiol. 32, 1239–1251 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Sagulenko, Y., Sagulenko, V., Chen, J. & Christie, P. J. Role of Agrobacterium VirB11 ATPase in T-pilus assembly and substrate selection. J. Bacteriol. 183, 5813–5825 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Rohde, M., Puls, J., Buhrdorf, R., Fischer, W. & Haas, R. A novel sheathed surface organelle of the Helicobacter pylori cag type IV secretion system. Mol. Microbiol. 49, 219–234 (2003).
  Article CAS PubMed Google Scholar
• Tanaka, J., Suzuki, T., Mimuro, H. & Sasakawa, C. Structural definition on the surface of Helicobacter pylori type IV secretion apparatus. Cell. Microbiol. 5, 395–404 (2003). References 70 and 71 report that the Cag type IV secretion system elaborates new sheathed surface structures that contribute to H. pylori pathogenesis.
  Article CAS PubMed Google Scholar
• Schulein, R. & Dehio, C. The VirB/VirD4 type IV secretion system of Bartonella is essential for establishing intraerythrocytic infection. Mol. Microbiol. 46, 1053–1067 (2002).
  Article CAS PubMed Google Scholar
• Watarai, M., Andrews, H. L. & Isberg, 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 (2001).
  Article CAS PubMed Google Scholar
• Farizo, K. M., Fiddner, S., Cheung, A. M. & Burns, D. L. Membrane localization of the S1 subunit of pertussis toxin in Bordetella pertussis and implications for pertussis toxin secretion. Infect. Immun. 70, 1193–1201 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Grahn, A. M., Haase, J., Bamford, D. H. & Lanka, E. Components of the RP4 conjugative transfer apparatus form an envelope structure bridging inner and outer membranes of donor cells: implications for related macromolecule transport systems. J. Bacteriol. 182, 1564–1574 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Pantoja, M., Chen, L., Chen, Y. & Nester, E. W. 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 (2002).
  Article CAS PubMed Google Scholar
• Galan, J. E. & Collmer, A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284, 1322–1328 (1999).
  Article CAS PubMed Google Scholar
• Ward, D. V. & Zambryski, P. C. The six functions of Agrobacterium VirE2. Proc. Natl Acad. Sci. USA 98, 385–386 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Deng, W. et al. Agrobacterium VirD2 protein interacts with plant host cyclophilins. Proc. Natl Acad. Sci. USA 95, 7040–7045 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Gelvin, S. B. _Agrobacterium_-mediated plant transformation: the biology behind the 'gene-jockeying' tool. Microbiol. Mol. Biol. Rev. 67, 16–37 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Tzfira, T. & Citovsky, V. Partners-in-infection: host proteins involved in the transformation of plant cells by Agrobacterium. Trends Cell Biol. 12, 121–129 (2002).
  Article CAS PubMed Google Scholar
• Zhu, Y. et al. Identification of Arabidopsis rat mutants. Plant Physiol. 132, 494–505 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Roberts, R. L. et al. Purine synthesis and increased Agrobacterium tumefaciens transformation of yeast and plants. Proc. Natl Acad. Sci. USA 100, 6634–6639 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Segal, E., Cha, J., Lo, J., Falkow, S. & Tompkins, L. 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 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Hatakeyama, M. Helicobacter pylori CagA — a potential bacterial oncoprotein that functionally mimics the mammalian Gab family of adaptor proteins. Microbes Infect. 5, 143–150 (2003).
  Article CAS PubMed Google Scholar
• Asahi, M. et al. Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J. Exp. Med. 191, 593–602 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Odenbreit, S. et al. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287, 1497–1500 (2000).
  Article CAS PubMed Google Scholar
• Stein, M. et al. c-Src/Lyn kinases activate Helicobacter pylori CagA through tyrosine phosphorylation of the EPIYA motifs. Mol. Microbiol. 43, 971–980 (2002).
  Article CAS PubMed Google Scholar
• Backert, S. et al. Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell. Microbiol. 2, 155–164 (2000). References 84, 86, 87, 88 and 90 report the first evidence for CagA translocation and subsequent phosphorylation in human cells.
  Article CAS PubMed Google Scholar
• Selbach, M., Moese, S., Hauck, C. R., Meyer, T. F. & Backert, S. Src is the kinase of the Helicobacter pylori CagA protein in vitro and in vivo. J. Biol. Chem. 277, 6775–6778 (2002).
  Article CAS PubMed Google Scholar
• Higashi, H. et al. SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295, 683–686 (2002).
  Article CAS PubMed Google Scholar
• Churin, Y. et al. Helicobacter pylori CagA protein targets the c-Met receptor and enhances the motogenic response. J. Cell Biol. 161, 249–255 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Mimuro, H. et al. Grb2 is a key mediator of Helicobacter pylori CagA protein activities. Mol. Cell 10, 745–755 (2002).
  Article CAS PubMed Google Scholar
• Amieva, M. R. et al. Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 300, 1430–1434 (2003). Shows that non-phosphorylated CagA induces formation of an aberrant apical-junction protein complex, resulting in loss of cell polarity, proliferation and differentiation.
  Article CAS PubMed PubMed Central Google Scholar
• Fischer, W. et al. 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).
  Article CAS PubMed Google Scholar
• Stein, P. E. et al. The crystal structure of pertussis toxin. Structure 2, 45–57 (1994).
  Article CAS PubMed Google Scholar
• Albert, P. R. & Robillard, L. G-protein specificity: traffic direction required. Cell Signal. 14, 407–418 (2002).
  Article CAS PubMed Google Scholar
• Vogel, J. P. & Isberg, R. R. Cell biology of Legionella pneumophila. Curr. Opin. Microbiol. 2, 30–34 (1999).
  Article CAS PubMed Google Scholar
• Swanson, M. S. & Sturgill-Koszycki, S. Exploitation of macrophages as a replication niche by Legionella pneumophila. Trends Microbiol. 8, 47–49 (2000).
  Article CAS PubMed Google Scholar
• Segal, G., Purcell, M. & Schuman, H. A. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl Acad. Sci. USA 95, 1669–1674 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Segal, G. & Shuman, H. A. Intracellular multiplication and human macrophage killing by Legionella pneumophila are inhibited by conjugal components of IncQ plasmid RSF1010. Mol. Microbiol. 30, 197–208 (1998).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Nagai, H., Kagan, J. C., Zhu, X., Kahn, R. A. & Roy, C. R. A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 295, 679–682 (2002).
  Article CAS PubMed Google Scholar
• Boschiroli, M. L. et al. Type IV secretion and Brucella virulence. Vet. Microbiol. 90, 341–348 (2002).
  Article CAS PubMed Google Scholar
• Novak, K. F., Dougherty, B. & Pelaez, M. Actinobacillus actinomycetemcomitans harbours type IV secretion system genes on a plasmid and in the chromosome. Microbiology 147, 3027–3035 (2001).
  Article CAS PubMed Google Scholar
• Ohashi, N., Zhi, N., Lin, Q. & Rikihisa, Y. Characterization and transcriptional analysis of gene clusters for a type IV secretion machinery in human granulocytic and monocytic ehrlichiosis agents. Infect. Immun. 70, 2128–2138 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Masui, S., Sasaki, T. & Ishikawa, H. Genes for the type IV secretion system in an intracellular symbiont, Wolbachia, a causative agent of various sexual alterations in arthropods. J. Bacteriol. 182, 6529–6531 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Andersson, S. G. et al. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133–140 (1998).
  Article CAS PubMed Google Scholar
• Bhattacharyya, A. et al. Whole-genome comparative analysis of three phytopathogenic Xylella fastidiosa strains. Proc. Natl Acad. Sci. USA 99, 12403–12408 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Zusman, T., Yerushalmi, G. & Segal, G. Functional similarities between the icm/dot pathogenesis systems of Coxiella burnetii and Legionella pneumophila. Infect. Immun. 71, 3714–3723 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Burghdorf, R., Forster, C., Haas, R. & Fischer, W. Topological analysis of a putative VirB8 homologue essential for the cag type IV secretion system in Helicobacter pylori. Int. J. Med. Microbiol. 293, 213–217 (2003).
  Article Google Scholar
• Cao, T. B. & Saier, M. H. Jr. Conjugal type IV macromolecular transfer systems of Gram-negative bacteria: organismal distribution, structural constraints, and evolutionary conclusions. Microbiology 147, 3201–3214 (2001).
  Article CAS PubMed Google Scholar