A novel sheathed surface organelle of the Helicobacter pylori cag type IV secretion system

Molecular Microbiology

Volumn 49, Issue 1, 2003, Pages 219-234

  Rohde, Manfred ^b   Püls, Jürgen ^a   Buhrdorf, Renate ^a   Fischer, Wolfgang ^a   Haas, Rainer ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CAGA PROTEIN; INTERLEUKIN 8; PROTEIN CAG7; PROTEIN CAGY; PROTEIN HP0527; PROTEIN KINASE P60; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; CAG PATHOGENICITY ISLAND; CELL CONTACT; CELL ORGANELLE; CELL SECRETION; CONFOCAL LASER MICROSCOPY; CYTOKINE RELEASE; DNA STRUCTURE; FIELD EMISSION SCANNING ELECTRON MICROSCOPY; HELICOBACTER PYLORI; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT;

ANTIGENS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CELL MEMBRANE STRUCTURES; CELLS, CULTURED; EPITHELIAL CELLS; GENOMIC ISLANDS; HELICOBACTER PYLORI; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON; RECOMBINANT FUSION PROTEINS;

BACTERIA (MICROORGANISMS); EUKARYOTA; HELICOBACTER; HELICOBACTER PYLORI; NEGIBACTERIA;

EID: 0038046757     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.2003.03549.x     Document Type: Article

References (45)

1. Alm, R.A., Ling, L.S., Moir, D.T., King, B.L., Brown, E.D., Doig, P.C., et al. (1999) Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397: 176-180.
2. Asahi, M., Azuma, T., Ito, S., Ito, Y., Suto, H., Nagai, Y., Tsubokawa, M., Tohyama, Y., et al. (2000) Helicobacter pylori CagA protein can be tyrosine phosphorylated in gastric epithelial cells. J Exp Med 191: 593-602.
3. Backert, S., Ziska, E., Brinkmann, V., Zinny-Arndt, U., Fauconnier, A., Jungblut, P.R., et al. (2000) Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell Microbiol 2: 155-164.
4. Backert, S., Moese, S., Selbach, M., Brinkmann, V., and Meyer, T.F. (2001) 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.
5. Blocker, A., Jouihri, N., Larquet, E., Gounon, P., Ebel, F., Parsot, C., et al. (2001) Structure and composition of the Shigella flexneri 'needle complex', a part of its type III secreton. Mol Microbiol 39: 652-663.
6. Christie, P.J., and Vogel, J.P. (2000) Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol 8: 354-360.
7. Churin, Y., Kardalinou, E., Meyer, T.F., and Naumann, M. (2001) Pathogenicity island-dependent activation of Rho GTPases Rac1 and Cdc42 in Helicobacter pylori infection. Mol Microbiol 40: 815-823.
8. Covacci, A., Telford, J.L., Del Giudice, G., Parsonnet, J., and Rappuoli, R. (1999) Helicobacter pylori virulence and genetic geography. Science 284: 1328-1333.
9. Crabtree, J.E., Xiang, Z., Lindley, I.J.D., Tompkins, D.S., Rappuoli, R., and Covacci, A. (1995) Induction of interleukin-8 secretion from gastric epithelial cells by a cagA negative isogenic mutant of Helicobacter pylori. J Clin Pathol 48: 967-969.
10. Ebel, F., Podzadel, T., Rohde, M., Kresse, A.U., Kramer, S., Deibel, C., et al. (1998) Initial binding of Shiga toxin-producing Eschedchia coli to host cells and subsequent induction of actin rearrangements depend on filamentous EspA-containing surface appendages. Mol Microbiol 30: 147-161.
11. Fischer, W., Püls, J., Buhrdorf, R., Gebert, B., Odenbreit, S., and Haas, R. (2001a) 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.
12. Fischer, W., Buhrdorf, R., Gerland, E., and Haas, R. (2001b) Outer membrane targeting of passenger proteins by the vacuolating cytotoxin autotransporter of Helicobacter pylori. Infect Immun 69: 6769-6775.
13. Fischer, W., Haas, R., and Odenbreit, S. (2002) Type IV secretion systems in pathogenic bacteria. Int J Med Microbiol 292: 159-168.
14. Foryst-Ludwig, A., and Naumann, M. (2000) PAK1 activates the NIK-IKK NF-kappaB pathway and proinflammatory cytokines in H. pylori-infection. J Biol Chem 275: 39779-39785.
15. Galan, J.E., and Collmer, A. (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284: 1322-1328.
16. Ginocchio, C.C., Olmsted, S.B., Wells, C.L., and Galan, J.E. (1994) Contact with epithelial cells induces the formation of surface appendages on Salmonella typhimurium. Cell 76: 717-724.
17. Higashi, H., Tsutsumi, R., Muto, S., Sugiyama, T., Azuma, T., Asaka, M., and Hatakeyama, M. (2001) SHP-2 tyrosine phosphatase as an intracellular target of Helicobacter pylori CagA protein. Science 295: 683-686.
18. Higashi, H., Tsutsumi, R., Fujita, A., Yamazaki, S., Asaka, M., Azuma, T., and Hatakeyama, M. (2002) Biological activity of the Helicobacter pylori virulence factor CagA is determined by variation in the tyrosine phosphorylation sites. Proc Natl Acad Sci USA 99: 14428-14433.
19. Hoiczyk, E., and Blobel, G. (2001) Polymerization of a single protein of the pathogen Yersinia enterocolitica into needles punctures eukaryotic cells. Proc Natl Acad Sci USA 98: 4669-4674.
20. Holmes, D.S., and Quigley, M. (1981) A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem 114: 193-197.
21. International Agency for Research on Cancer. (1994) IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Lyon: World Health Organization.
22. Jin, Q., Hu, W., Brown, I., McGhee, G., Hart, P., Jones, A.L., and He, S.Y. (2001) Visualization of secreted Hrp and Avr proteins along the Hrp pilus during type III secretion in Erwinia amylovora and Pseudomonas syringae. Mol Microbiol 40: 1129-1139.
23. Josenhans, C., Eaton, K.A., Thevenot, T., and Suerbaum, S. (2000) Switching of flagellar motility in Helicobacter pylori by reversible length variation of a short homopolymeric sequence repeat in fliP, a gene encoding a basal body protein. Infect Immun 68: 4598-4603.
24. Kelly, B.A., and Kado, C.I. (2003) Agrobacterium -mediated T-DNA transfer and integration into the chromosome of Streptomyces lividans. Mol Plant Pathol 3: 125-134.
25. Knutton, S., Rosenshine, I., Pallen, M.J., Nisan, I., Neves, B.C., Bain, C., et al. (1998) A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. EMBO J 17: 2166-2176.
26. Kubori, T., Matsushima, Y., Nakamura, D., Uralil, J., Lara-Tejero, M., Sukhan, A., et al. (1998) Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science 280: 602-605.
27. Kumar, R.B., and Das, A. (2002) Polar location and functional domains of the Agrobacterium tumefaciens DNA transfer protein VirD4. Mol Microbiol 43: 1523-1532.
28. Kumar, R.B., Xie, Y.H., and Das, A. (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.
29. Kwok, T., Backert, S., Schwarz, H., Berger, J., and Meyer, T.F. (2002) Specific entry of Helicobacter pylori into cultured gastric epithelial cells via a zipper-like mechanism. Infect Immun 70: 2108-2120.
30. Liu, G., McDaniel, T.K., Falkow, S., and Karlin, S. (1999) Sequence anomalies in the Cag7 gene of the Helicobacter pylori pathogenicity island. Proc Natl Acad Sci USA 96: 7011-7016.
31. Mimuro, H., Suzuki, T., Tanaka, J., Asahi, M., Haas, R., and Sasakawa, C. (2002) Grb2 is a key mediator of Helicobacter pylori CagA protein activities. Mol Cell 10: 745-755.
32. Neesen, J., Padmanabhan, S., and Bunemann, H. (1994) Tandemly arranged repeats of a novel highly charged 16-amino-acid motif representing the major component of the sperm-tail-specific axoneme-associated protein family Dhmst101 form extended alpha-helical rods within the extremely elongated spermatozoa of Drosophila hydei. Eur J Biochem 225: 1089-1095.
33. Neesen, J., Heinlein, U.A., Heinz, G.K., and Bunemann, H. (1999) Proteins with tandemly arranged repeats of a highly charged 16-amino-acid motif encoded by the Dhmst101 gene family are structural components of the outer sheath of the extremely elongated sperm tails of Drosophila hydei. Dev Growth Differ 41: 93-99.
34. Nouwen, N., Ranson, N., Saibil, H., Wolpensinger, B., Engel, A., Ghazi, A., and Pugsley, A.P. (1999) Secretin PuID: association with pilot PuIS, structure, and ion-conducting channel formation. Proc Natl Acad Sci USA 96: 8173-8177.
35. Odenbreit, S., Püls, J., Sedlmaier, B., Gerland, E., Fischer, W., and Haas, R. (2000) Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287: 1497-1500.
36. Odenbreit, S., Gebert, B., Püls, J., Fischer, W., and Haas, R. (2001) Interaction of Helicobacter pylori with professional phagocytes: role of the cag pathogenicity island and translocation, phosphorylation and specific processing of CagA. Cell Microbiol 3: 21-31.
37. Pohlner, J., Krämer, J., and Meyer, T.F. (1993) A plasmid system for high-level expression and in vitro processing of recombinant proteins. Gene 130: 121-126.
38. Püls, J., Fischer, W., and Haas, R. (2002) 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.
39. Rieder, G., Hatz, R.A., Moran, A.P., Walz, A., Stolte, M., and Enders, G. (1997) Role of adherence in interleukin-8 induction in Helicobacter pylori-associated gastritis. Infect Immun 65: 3622-3630.
40. Roine, E., Wei, W., Yuan, J., Nurmiaho-Lassila, E.L., Kalkkinen, N., Romantschuk, M., and He, S.Y. (1997) Hrp pilus: an hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci USA 94: 3459-3464.
41. Segal, E.D., Cha, J., Lo, J., Falkow, S., and Tompkins, L.S. (1999) 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.
42. Spurr, A.R. (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26: 31-43.
43. Stein, M., Rappuoli, R., and Covacci, A. (2000) Tyrosine phosphorylation of the Helicobacter pylori CagA antigen after cag-driven host cell translocation. Proc Natl Acad Sci USA 97: 1263-1268.
44. Stein, M., Bagnoli, F., Halenbeck, R., Rappuoli, R., Fantl, W.J., and Covacci, A. (2002) c-Src/Lyn kinases activate Helicobacter pylori CagA through tyrosine phosphorylation of the EPIYA motifs. Mol Microbiol 43: 971-980.
45. Tomb, J.-F., White, O., Kerlavage, A.R., Clayton, R.A., Sutton, G.G., Fleischmann, R.D., et al. (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547.