Characterization of the pilin ortholog of the Helicobacter pylori type IV cag pathogenicity apparatus, a surface-associated protein expressed during infection

Journal of Bacteriology

Volumn 188, Issue 16, 2006, Pages 5865-5877

  Andrzejewska, Joanna ^a,e   Lee, Sae Kyung ^a   Olbermann, Patrick ^b   Lotzing, Nina ^b   Katzowitsch, Elena ^a   Linz, Bodo ^c   Achtman, Mark ^c   Kado, Clarence I ^d   Suerbaum, Sebastian ^a,b   Josenhans, Christine ^a,b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e ICON Clinical Research   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISERUM; BACTERIAL PROTEIN; EPITOPE; HYBRID PROTEIN; INTERLEUKIN 8; MEMBRANE PROTEIN; PEPTIDE; PILIN; PROTEIN CAG PAI; PROTEIN HP0546; PROTEIN SUBUNIT; PROTEIN VIR; PROTEIN VIRB2; UNCLASSIFIED DRUG; BACTERIAL ANTIGEN; CAGA PROTEIN, HELICOBACTER PYLORI; FIMBRIA PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; BACTERIUM PILUS; CAG PATHOGENICITY ISLAND; CELL FRACTIONATION; CONTROLLED STUDY; EPITHELIUM CELL; FLAG TAG; GENE FUNCTION; HELICOBACTER PYLORI; HOST; HP0546 GENE; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; MOLECULAR WEIGHT; NONHUMAN; ORTHOLOGY; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RHIZOBIUM RADIOBACTER; SEQUENCE HOMOLOGY; STOMACH EPITHELIUM; STRAIN DIFFERENCE; TYPE IV SECRETION SYSTEM; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HELICOBACTER INFECTION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; TUMOR CELL LINE;

AGROBACTERIUM TUMEFACIENS; ESCHERICHIA COLI; HELICOBACTER PYLORI; VIR;

AMINO ACID SEQUENCE; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL LINE, TUMOR; EPITHELIAL CELLS; FIMBRIAE PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN SUBUNITS;

EID: 33748667977     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00060-06     Document Type: Article

References (48)

1. Akopyants, N. S., S. W. Clifton, D. Kersulyte, J. E. Crabtree, B. E. Youree, C. A. Reece, N. O. Bukanov, E. S. Drazek, B. A. Roe, and D. E. Berg. 1998. Analyses of the cag pathogenicity island of Helicobacter pylori. Mol. Microbiol. 28:37-53.
2. Alm, R. A., L.-S. L. Ling, D. T. Moir, B. L. King, E. D. Brown, P. C. Doig, D. R. Smith, B. Noonan, B. C. Guild, B. L. deJonge, G. Carmel, P. J. Tummino, A. Caruso, M. Uria-Nickelsen, D. M. Mills, C. Ives, R. Gibson, D. Merberg, S. D. Mills, Q. Jiang, D. E. Taylor, G. F. Vovis, and T. J. Trust. 1999. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176-180.
3. Backert, S., E. Ziska, V. Brinkmann, U. Zimny-Arndt, A. Fauconnier, P. R. Jungblut, M. Naumann, and T. F. Meyer. 2000. Translocation of the Helicobacter pylori CagA protein in gastric epithelial cells by a type IV secretion apparatus. Cell. Microbiol. 2:155-164.
4. Brandt, S., T. Kwok, R. Hartig, W. Konig, and S. Backert. 2005. NF-kappaB activation and potentiation of proinflammatory responses by the Helicobacter pylori CagA protein. Proc. Natl. Acad. Sci. USA 102:9300-9305.
5. Buhrdorf, R., C. Forster, R. Haas, and W. Fischer. 2003. 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.
6. Censini, S., C. Lange, Z. Xiang, J. E. Crabtree, P. Ghiara, M. Borodovsky, R. Rappuoli, and A. Covacci. 1996. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA 93:14648-14653.
7. Chesnokova, O., J. B. Coutinho, I. H. Khan, M. S. Mikhail, and C. I. Kado. 1997. Characterization of flagella genes of Agrobacterium tumefaciens, and the effect of a bald strain on virulence. Mol. Microbiol. 23:579-590.
8. Christie, P. J. 2001. Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40:294-305.
9. Christie, P. J., K. Atmakuri, V. Krishnamoorthy, S. Jakubowski, and E. Cascales. 2005. Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu. Rev. Microbiol. 59:451-485.
10. Churin, Y., L. Al Ghoul, O. Kepp, T. F. Meyer, W. Birchmeier, and M. Naumann. 2003. Helicobacter pylori CagA protein targets the c-Met receptor and enhances the motogenic response. J. Cell Biol. 161:249-255.
11. Eisenbrandt, R., M. Kalkum, E. M. Lai, R. Lurz, C. I. Kado, and E. Lanka. 1999. Conjugative pili of IncP plasmids, and the Ti plasmid T pilus are composed of cyclic subunits. J. Biol. Chem. 274:22548-22555.
12. Engelman, D. M., T. A. Steitz, and A. Goldman. 1986. Identifying nonpolar transbilayer helices in amino acid sequences of membrane proteins. Annu. Rev. Biophys. Biophys. Chem. 15:321-353.
13. Falush, D., T. Wirth, B. Linz, J. K. Pritchard, M. Stephens, M. Kidd, M. J. Blaser, D. Y. Graham, S. Vacher, G. I. Perez-Perez, Y. Yamaoka, F. Megraud, K. Otto, U. Reichard, E. Katzowitsch, X. Wang, M. Achtman, and S. Suerbaum. 2003. Traces of human migrations in Helicobacter pylori populations. Science 299:1582-1585.
14. Ferrero, R. L., V. Cussac, P. Courcoux, and A. Labigne. 1992. Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange. J. Bacteriol. 174:4212-4217.
15. Fischer, W., J. Puls, 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.
16. Hajdukiewicz, P., Z. Svab, and P. Maliga. 1994. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25:989-994.
17. Hatakeyama, M. 2004. Oncogenic mechanisms of the Helicobacter pylori CagA protein. Nat. Rev. Cancer 4:688-694.
18. Heuermann, D., and R. Haas. 1998. A stable shuttle vector system for efficient genetic complementation of Helicobacter pylori strains by transformation and conjugation. Mol. Gen. Genet. 257:519-528.
19. Jin, Q., and S. Y. He. 2001. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294:2556-2558.
20. Josenhans, C., K. A. Eaton, T. Thevenot, and S. Suerbaum. 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.
21. Kalkum, M., R. Eisenbrandt, R. Lurz, and E. Lanka. 2002. Tying rings for sex. Trends Microbiol. 10:382-387.
22. 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.
23. Labigne-Roussel, A., P. Courcoux, and L. Tompkins. 1988. Gene disruption and replacement as a feasible approach for mutagenesis of Campylobacter jejuni. J. Bacteriol. 170:1704-1708.
24. Lai, E. M., O. Chesnokova, L. M. Banta, and C. I. Kado. 2000. Genetic and environmental factors affecting T-pilin export and T-pilus biogenesis in relation to flagellation of Agrobacterium tumefaciens. J. Bacteriol. 182:3705-3716.
25. Lai, E. M., R. Eisenbrandt, M. Kalkum, E. Lanka, and C. I. Kado. 2002. Biogenesis of T pili in Agrobacterium tumefaciens requires precise VirB2 propilin cleavage and cyclization. J. Bacteriol. 184:327-330.
26. 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.
27. Lai, E. M., and C. I. Kado. 2000. The T-pilus of Agrobacterium tumefaciens. Trends Microbiol. 8:361-369.
28. Lai, E. M., and C. I. Kado. 2002. The Agrobacterium tumefaciens T pilus composed of cyclic T pilin is highly resilient to extreme environments. FEMS Microbiol. Lett. 210:111-114.
29. Manchak, J., K. G. Anthony, and L. S. Frost. 2002. Mutational analysis of F-pilin reveals domains for pilus assembly, phage infection and DNA transfer. Mol. Microbiol. 43:195-205.
30. Moese, S., M. Selbach, T. Kwok, V. Brinkmann, W. Konig, T. F. Meyer, and S. Backert. 2004. Helicobacter pylori induces AGS cell motility and elongation via independent signaling pathways. Infect. Immun. 72:3646-3649.
31. Odenbreit, S., J. Püls, B. Sedlmaier, E. Gerland, W. Fischer, and R. Haas. 2000. Translocation of Helicobacter pylori CagA into gastric epithelial cells by type IV secretion. Science 287:1497-1500.
32. Peabody, C. R., Y. J. Chung, M. R. Yen, D. Vidal-Ingigliardi, A. P. Pugsley, and M. H. Saier, Jr. 2003. Type II protein secretion and its relationship to bacterial type IV pili and archaeal flagella. Microbiology 149:3051-3072.
33. Rohde, M., J. Puls, R. Buhrdorf, W. Fischer, and R. Haas. 2003. A novel sheathed surface organelle of the Helicobacter pylori cag type IV secretion system. Mol. Microbiol. 49:219-234.
34. 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.
35. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
36. Sauvonnet, N., G. Vignon, A. P. Pugsley, and P. Gounon. 2000. Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J. 19:2221-2228.
37. Segal, E. D., J. Cha, J. Lo, S. Falkow, and L. S. Tompkins. 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.
38. Selbach, M., S. Moese, T. F. Meyer, and S. Backert. 2002. Functional analysis of the Helicobacter pylori cag pathogenicity island reveals both VirD4-CagA-dependent and VirD4-CagA-independent mechanisms. Infect. Immun. 70:665-671.
39. Shimoyama, T., and J. E. Crabtree. 1997. Mucosal chemokines in Helicobacter pylori infection. J. Physiol. Pharmacol. 48:315-323.
40. Shimoyama, T., and J. E. Crabtree. 1998. Bacterial factors and immune pathogenesis in Helicobacter pylori infection. Gut 43(Suppl. 1):S2-S5.
41. Suerbaum, S., J. Maynard Smith, K. Bapumia, G. Morelli, N. H. Smith, E. Kunstmann, I. Dyrek, and M. Achtman. 1998. Free recombination within Helicobacter pylori. Proc. Natl. Acad. Sci. USA. 95:12619-12624.
42. Suerbaum, S., and P. Michetti. 2002. Helicobacter pylori infection. N. Engl. J. Med. 347:1175-1186.
43. Tanaka, J., T. Suzuki, H. Mimuro, and C. Sasakawa. 2003. Structural definition on the surface of Helicobacter pylori type IV secretion apparatus. Cell. Microbiol. 5:395-404.
44. 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, E. K. Hickey, D. E. Berg, J. D. Gocayne, T. R. Utterback, J. D. Peterson, J. M. Kelley, M. D. Cotton, J. M. Weidman, C. Fujii, C. Bowman, L. Watthey, E. Wallin, W. S. Hayes, M. Borodovsky, P. D. Karp, H. O. Smith, C. M. Fraser, and J. C. Venter. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539-547.
45. Viala, J., C. Chaput, I. G. Boneca, A. Cardona, S. E. Girardin, A. P. Moran, R. Athman, S. Memet, M. R. Huerre, A. J. Coyle, P. S. DiStefano, P. J. Sansonetti, A. Labigne, J. Bertin, D. J. Philpott, and R. L. Ferrero. 2004. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5:1166-1174.
46. Webb, P. M., J. E. Crabtree, D. Forman, et al. 1999. Gastric cancer, cytotoxin-associated gene A-positive Helicobacter pylori, and serum pepsinogens: an international study. Gastroenterology 116:269-276.
47. Yamada, H., T. Aihara, and S. Okabe. 2001. Mechanism for Helicobacter pylori stimulation of interleukin-8 production in a gastric epithelial cell line (MKN 28): roles of mitogen-activated protein kinase and interleukin-1beta. Biochem. Pharmacol. 61:1595-1604.
48. Yuan, Q., A. Carle, C. Gao, D. Sivanesan, K. A. Aly, C. Hoppner, L. Krall, N. Domke, and C. Baron. 2005. Identification of the VirB4-VirB8-VirB5- VirB2 pilus assembly sequence of type IV secretion systems. J. Biol. Chem. 280:26349-26359.