Novel activities of the Helicobacter pylori vacuolating cytotoxin: From epithelial cells towards the immune system

International Journal of Medical Microbiology

Volumn 293, Issue 7-8, 2004, Pages 539-547

  Fischer, Wolfgang ^a   Gebert, Bettina ^a   Haas, Rainer ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Calcineurin; Cell vacuolation; Helicobacter; IL 2 secretion; Immunophilins; NFAT

Indexed keywords

CAGA PROTEIN; VACUOLATING TOXIN; VIRULENCE FACTOR;

BACTERIAL SURVIVAL; CELL VACUOLE; CONFERENCE PAPER; EPITHELIUM CELL; HELICOBACTER PYLORI; HOST RESISTANCE; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; NONHUMAN; REVIEW; STOMACH EPITHELIUM;

EID: 2442637780     PISSN: 14384221     EISSN: None     Source Type: Journal    
DOI: 10.1078/1438-4221-00300     Document Type: Conference Paper

References (79)

1. Amieva, M. R., Salama, N. R., Tompkins, L. S., Falkow, S.: Helicobacter pylori enter and survive within multivesicular vacuoles of epithelial cells. Cell. Microbiol. 4, 677-690 (2002).
2. Amieva, M. R., Vogelmann, R., Covacci, A., Tompkins, L. S., Nelson, W. J., Falkow, S.: Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science 300, 1430-1434 (2003).
3. Atherton, J. C., Cao, P., Peek Jr., R. M., Tummuru, M. K. R., Blaser, M. J., Cover, T. L.: Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration. J. Biol. Chem. 270, 17771-17777 (1995).
4. Boncristiano, M., Paccani, S. R., Barone, S., Ulivieri, C., Patrussi, L., Ilver D., Amedei, A., D'Elios, M. M., Telford, J. L., Baldari, C. T.: The Helicobacter pylori vacuolating toxin inhibits T cell activation by two independent mechanisms. J. Exp. Med. 198, 1887-1897 (2003).
5. Carpenter, G., Ji, Q.: Phospholipase C-gamma as a signal-transducing element. Exp. Cell Res. 253, 15-24 (1999).
6. Clipstone, N. A., Crabtree, G. R.: Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature 357, 695-697 (1992).
7. Cover, T. L., Blaser, M. J.: Purification and characterization of the vacuolating toxin from Helicobacter pylori. J. Biol. Chem. 267(5), 10570-10575 (1992).
8. Cover, T. L., Hanson, P. I., Heuser, J. E.: Acid-induced dissociation of VacA, the Helicobacter pylori vacuolating cytotoxin, reveals its pattern of assembly. J. Cell Biol. 138, 759-769 (1997).
9. Cover, T. L., Krishna, U. S., Israel, D. A., Peek, R. M. J.: Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res. 63, 951-957 (2003).
10. 2+ ATPases in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 2226-2237 (1996).
11. Czajkowsky, D. M., Iwamoto, H., Cover, T. L., Shao, Z.: The vacuolating toxin from Helicobacter pylori forms hexameric pores in lipid bilayers at low pH. Proc. Natl. Acad. Sci. USA 96, 2001-2006 (1999).
12. De Bernard, M., Burroni, D., Papini, E., Rappuoli, R., Telford, J., Montecucco, C.: Identification of the Helicobacter pylori VacA toxin domain active in the cell cytosol. Infect. Immun. 66, 6014-6016 (1998).
13. De Bernard, M., Moschioni, M., Habermann, A., Griffiths, G., Montecucco, C.: Cell vacuolization induced by Helicobacter pylori VacA cytotoxin does not depend on late endosomal SNAREs. Cell. Microbiol. 4, 11-18 (2002).
14. + T-cell clones from peripheral blood and gastric biopsies. Infect. Immun. 63, 1102-1106 (1995).
15. Dorner, B. G., Scheffold, A., Rolph, M. S., Hüser, M. B., Kaufmann, S. H., Radbruch, A., Flesch, I. E., Kroczek, R. A.: MIP-1α, MIP-1β, RANTES, and ATAC/lymphotactin function together with IFN-γ as type 1 cytokines. Proc. Natl. Acad. Sci. USA 99, 6181-6186 (2002).
16. Ermak, T. H., Giannasca, P. J., Nichols, R., Myers, G. A., Nedrud, J., Weltzin, R., Lee, C. K., Kleanthous, H., Monath, T. P.: Immunization of mice with urease vaccine affords protection against Helicobacter pylori infection in the absence of antibodies and is mediated by MHC class II-restricted responses. J. Exp. Med. 188, 2277-2288 (1998).
17. Ernst, P. B., Gold, B. D.: The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu. Rev. Microbiol. 54, 615-640 (2000).
18. Fan, X., Crowe, S. E., Behar, S., Gunasena, H., Ye, G., Haeberle, H., Van Houten, N., Gourley, W. K., Ernst, P. B., Reyes, V. E.: The effect of class II major histocompatibility complex expression on adherence of Helicobacter pylori and induction of apoptosis in gastric epithelial cells: a mechanism for T helper cell type 1-mediated damage. J. Exp. Med. 187, 1659-1669 (1998).
19. Fan, X., Gunasena, H., Cheng, Z., Espejo, R., Crowe, S. E., Ernst, P. B., Reyes, V. E.: Helicobacter pylori urease binds to class II MHC on gastric epithelial cells and induces their apoptosis. J. Immunol. 165, 1918-1924 (2000).
20. Ferrari, G., Langen, H., Naito, M., Pieters, J.: A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97, 435-447 (1999).
21. Fischer, W., Buhrdorf, R., Gerland, E., Haas, R.: Outer membrane targeting of passenger proteins by the vacuolating cytotoxin autotransporter of Helicobacter pylori. Infect. Immun. 69, 6769-6775 (2001).
22. Flanagan, W. M., Corthesy, B., Bram, R. J., Crabtree, G. R.: Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature 352, 803-807 (1991).
23. Fujikawa, A., Shirasaka, D., Yamamoto, S., Ota, H., Yahiro, K., Fukada, M., Shintani, T., Wada, A., Aoyama, N., Hirayama, T., Fukamachi, H., Noda, M.: Mice deficient in protein tyrosine phosphatase receptor type Z are resistant to gastric ulcer induction by VacA of Helicobacter pylori. Nat. Genet. 33, 375-381 (2003).
24. Galmiche, A., Rassow, J., Doye, A., Cagnol, S., Chambard, J. C., Contamin, S., de Thillot, V., Just, I., Ricci, V., Solcia, E., Van Obberghen, E., Boquet, P.: The N-terminal 34 kDa fragment of Helicobacter pylori vacuolating cytotoxin targets mitochondria and induces cytochrome c release. EMBO J. 19, 6361-6370 (2000).
25. Garner, J. A., Cover, T. L.: Binding and internalization of the Helicobacter pylori vacuolating cytotoxin by epithelial cells. Infect. Immun. 64, 4197-4203 (1996).
26. Gebert, B., Fischer, W., Weiss, E., Hoffmann, R., Haas, R.: Helicobacter pylori vacuolating cytotoxin inhibts T-lymphocyte activation. Science 301, 1099-1102 (2003).
27. +-ATPase assembly. Genetics 141, 833-844 (1995).
28. Hotchin, N. A., Cover, T. L., Akhtar, N.: Cell vacuolation induced by the VacA cytotoxin of Helicobacter pylori is regulated by the Rac1 GTPase. J. Biol. Chem. 275, 14009-14012 (2000).
29. Ikonomov, O. C., Sbrissa, D., Yoshimori, T., Cover, T. L., Shisheva, A.: PIKfyve Kinase and SKD1 AAA ATPase define distinct endocytic compartments. Only PIKfyve expression inhibits the cell-vacuolating activity of Helicobacter pylori VacA toxin. J. Biol. Chem. 277, 46785-46790 (2002).
30. Jones, N. L., Day, A. S., Jennings, H. A., Sherman, P. M.: Helicobacter pylori induces gastric epithelial cell apoptosis in association with increased Fas receptor expression. Infect. Immun. 67, 4237-4242 (1999).
31. Knipp, U., Birkholz, S., Kaup, W., Mahnke, K., Opferkuch, W.: Suppression of human mononuclear cell response by Helicobacter pylori: effects on isolated monocytes and lymphocytes. FEMS Immunol. Med. Microbiol. 8, 157-166 (1994).
32. Knipp, U., Birkholz, S., Kaup, W., Opferkuch, W.: Partial characterization of a cell proliferation-inhibiting protein produced by Helicobacter pylori. Infect. Immun. 64, 3491-3496 (1996).
33. Kuck, D., Kolmerer, B., Iking-Konert, C., Krammer, P. H., Stremmel, W., Rudi, J.: Vacuolating cytotoxin of Helicobacter pylori induces apoptosis in the human gastric epithelial cell line AGS. Infect. Immun. 69, 5080-5087 (2001).
34. Letley, D. P., Rhead, J. L., Twells, R. J., Dove, B., Atherton, J. C.: Determinants of non-toxicity in the gastric pathogen Helicobacter pylori. J. Biol. Chem. 278, 26734-26741 (2003).
35. Leunk, R. D., Johnson, P. T., David, B. C., Kraft, W. G., Morgan, D. R.: Cytotoxic activity in broth-culture filtrates of Campylobacter pylori. J. Med. Microbiol. 26, 93-99 (1988).
36. + T cells specific for subunit A of Helicobacter pylori urease reduces H. pylori stomach colonization in mice in the absence of interleukin-4 (IL-4)/IL-13 receptor signaling. Infect. Immun. 69, 1714-1721 (2001).
37. high regulatory T cells suppress memory T-cell responses to H. pylori in infected individuals. Infect. Immun. 71, 1755-1762 (2003).
38. Lupetti, P., Heuser, J. E., Manetti, R., Massari, P., Lanzavecchia, S., Bellon, P. L., Dallai, R., Rappuoli, R., Telford, J. L.: Oligomeric and subunit structure of the Helicobacter pylori vacuolating cytotoxin. J. Cell Biol. 133, 801-807 (1996).
39. Marchetti, M., Arico, B., Burroni, D., Figura, N., Rappuoli, R., Ghiara, P.: Development of a mouse model of Helicobacter pylori infection that mimics human disease. Science 267, 1655-1658 (1995).
40. McClain, M. S., Cao, P., Cover, T. L.: Amino-terminal hydrophobic region of Helicobacter pylori vacuolating cytotoxin (VacA) mediates transmembrane protein dimerization. Infect. Immun. 69, 1181-1184 (2001).
41. McClain, M. S., Iwamoto, H., Cao, P., Vinion-Dubiel, A.D., Li, Y., Szabo, G., Shao, Z., Cover, T. L.: Essential role of a GXXXG motif for membrane channel formation by Helicobacter pylori vacuolating toxin. J. Biol. Chem. 278, 12101-12108 (2003).
42. Molinari, M., Galli, C., De Bernard, M., Norais, N., Ruysschaert, J. M., Rappuoli, R., Montecucco, C.: The acid activation of Helicobacter pylori toxin VacA: structural and membrane binding studies. Biochem. Biophys. Res. Commun. 248, 334-340 (1998a).
43. Molinari, M., Galli, C., Norais, N., Telford, J. L., Rappuoli, R., Luzio, J. P., Montecucco, C.: Vacuoles induced by Helicobacter pylori toxin contain both late endosomal and lysosomal markers. J. Biol. Chem. 272, 25339-25344 (1997).
44. Molinari, M., Salio, M., Galli, C., Norais, N., Rappuoli, R., Lanzavecchia, A., Montecucco, C.: Selective inhibition of Ii-dependent antigen presentation by Helicobacter pylori toxin VacA. J. Exp. Med. 187, 135-140 (1998b).
45. Ogura, K., Maeda, S., Nakao, M., Watanabe, T., Tada, M., Kyutoku, T., Yoshida, H., Shiratori, Y., Omata, M.: Virulence factors of Helicobacter pylori responsible for gastric diseases in Mongolian gerbil. J. Exp. Med. 192, 1601-1610 (2000).
46. Padilla, P. I., Wada, A., Yahiro, K., Kimura, M., Niidome, T., Aoyagi, H., Kumatori, A., Anami, M., Hayashi, T., Fujisawa, J., Saito, H., Moss, J., Hirayama, T.: Morphologic differentiation of HL-60 cells is associated with appearance of RPTPβ and induction of Helicobacter pylori VacA sensitivity. J. Biol. Chem. 275, 15200-15206 (2000).
47. Pagliaccia, C., De Bernard, M., Lupetti, P., Ji, X., Burroni, D., Cover, T. L., Papini, E., Rappuoli, R., Telford, J. L., Reyrat, J. M.: The m2 form of the Helicobacter pylori cytotoxin has cell type-specific vacuolating activity. Proc. Natl. Acad. Sci. USA 95, 10212-10217 (1998).
48. Papini, E., Bugnoli, M., De Bernard, M., Figura, N., Rappuoli, R., Montecucco, C.: Bafilomycin A1 inhibits Helicobacter pylori-induced vacuolization of HeLa cells. Mol. Microbiol. 7, 323-327 (1993).
49. Papini, E., Satin, B., Bucci, C., De Bernard, M., Telford, J. L., Manetti, R., Rappuoli, R., Zerial, M., Montecucco, C.: The small GTP binding protein rab7 is essential for cellular vacuolation induced by Helicobacter pylori cytotoxin. EMBO J. 16, 15-24 (1997).
50. Papini, E., Satin, B., Norais, N., De Bernard, M., Telford, J. L., Rappuoli, R., Montecucco, C.: Selective increase of the permeability of polarized epithelial cell monolayers by Helicobacter pylori vacuolating toxin. J. Clin. Invest. 102, 813-820 (1998).
51. Peek, R. M. J., Blaser, M. J.: Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat. Rev. Cancer 2, 28-37 (2002).
52. Peek, R. M. J., Wirth, H. P., Moss, S. F., Yang, M., Abdalla, A. M., Tham, K. T., Zhang, T., Tang, L. H., Modlin, I. M., Blaser, M. J.: Helicobacter pylori alters gastric epithelial cell cycle events and gastrin secretion in Mongolian gerbils. Gastroenterology 118, 48-59 (2000).
53. Pelicic, V., Reyrat, J. M., Sartori, L., Pagliaccia, C., Rappuoli, R., Telford, J. L., Montecucco, C., Papini, E.: Helicobacter pylori VacA cytotoxin associated with the bacteria increases epithelial permeability independently of its vacuolating activity. Microbiology 145, 2043-2050 (1999).
54. Petersen, A. M., Sørensen, K., Blom, J., Krogfelt, K. A.: Reduced intracellular survival of Helicobacter pylori vacA mutants in comparison with their wild-types indicates the role of VacA in pathogenesis. FEMS Immunol. Med. Microbiol. 30, 103-108 (2001).
55. + regulatory T cells is associated with a loss of regulation leading to increased pathology in Helicobacter pylori-infected mice. Clin. Exp. Immunol. 132, 393-400 (2003).
56. Reyrat, J. M., Lanzavecchia, S., Lupetti, P., De Bernard, M., Pagliaccia, C., Pelicic, V., Charrel, M., Ulivieri, C., Norais, N., Ji, X., Cabiaux, V., Papini, E., Rappuoli, R., Telford, J. L.: 3D imaging of the 58 kDa cell binding subunit of the Helicobacter pylori cytotoxin. J. Mol. Biol. 290, 459-470 (1999).
57. Ricci, V., Ciacci, C., Zarrilli, R., Sommi, P., Tummuru, M. K. R., Blanco, C. D., Bruni, C. B., Cover, T. L., Blaser, M. J., Romano, M.: Effect of Helicobacter pylori on gastric epithelial cell migration and proliferation in vitro - role of VacA and CagA. Infect. Immun. 64, 2829-2833 (1996).
58. Ricci, V., Galmiche, A., Doye, A., Necchi, V., Solcia, E., Boquet, P.: High cell sensitivity to Helicobacter pylori VacA toxin depends on a GPI-anchored protein and is not blocked by inhibition of the clathrin-mediated pathway of endocytosis. Mol. Biol. Cell 11, 3897-3909 (2000).
59. Rudi, J., Kuck, D., Strand, S., von Herbay, A., Mariani, S. M., Krammer, P. H., Galle, P. R., Stremmel, W.: Involvement of the CD95 (APO-1/Fas) receptor and ligand system in Helicobacter pylori-induced gastric epithelial apoptosis. J. Clin. Invest. 102, 1506-1514 (1998).
60. Salomon, B., Bluestone, J. A.: Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Annu. Rev. Immunol. 19, 225-252 (2001).
61. Satin, B., Norais, N., Telford, J., Rappuoli, R., Murgia, M., Montecucco, C., Papini, E.: Effect of Helicobacter pylori vacuolating toxin on maturation and extracellular release of procathepsin D and on epidermal growth factor degradation. J. Biol. Chem. 272, 25022-25028 (1997).
62. Schmitt, W., Haas, R.: Genetic analysis of the Helicobacter pylori vacuolating cytotoxin: structural similarities with the IgA protease type of exported protein. Mol. Microbiol. 12, 307-319 (1994).
63. Schraw, W., Li, Y., McClain, M. S., van der Goot, F. G., Cover, T. L.: Association of Helicobacter pylori vacuolating toxin (VacA) with lipid rafts. J. Biol. Chem. 277, 34642-34650 (2002).
64. Seto, K., Hayashi-Kuwabara, Y., Yoneta, T., Suda, H., Tamaki, H.: Vacuolation induced by cytotoxin from Helicobacter pylori is mediated by the EGF receptor in HeLa cells. FEBS Lett. 431, 347-350 (1998).
65. Smythies, L. E., Waites, K. B., Lindsey, J. R., Harris, P. R., Ghiara, P., Smith, P. D.: Helicobacter pylori-induced mucosal inflammation is Th1 mediated and exacerbated in IL-4, but not IFN-γ, gene-deficient mice. J. Immunol. 165, 1022-1029 (2000).
66. Suzuki, J., Ohnishi, H., Wada, A., Hirayama, T., Ohno, H., Ueda, N., Yasuda, H., Iiri, T., Wada, Y., Futai, M., Mashima, H.: Involvement of syntaxin 7 in human gastric epithelial cell vacuolation induced by the Helicobacter pylori-produced cytotoxin VacA. J. Biol. Chem. 278, 25585-25590 (2003).
67. Suzuki, J., Ohnsihi, H., Shibata, H., Wada, A., Hirayama, T., Iiri, T., Ueda, N., Kanamaru, C., Tsuchida, T., Mashima, H., Yasuda, H., Fujita, T.: Dynamin is involved in human epithelial cell vacuolation caused by the Helicobacter pylori-produced cytotoxin VacA. J. Clin. Invest. 107, 363-370 (2001).
68. Szabo, I., Brutsche, S., Tombola, F., Moschioni, M., Satin, B., Telford, J. L., Rappuoli, R., Montecucco, C., Papini, E., Zoratti, M.: Formation of anion-selective channels in the cell plasma membrane by the toxin VacA of Helicobacter pylori is required for its biological activity. EMBO J. 18, 5517-5527 (1999).
69. Telford, J. L., Ghiara, P., Dell'Orco, M., Comanducci, M., Burroni, D., Bugnoli, M., Tecce, M. F., Censini, S., Covacci, A., Xiang, Z., Papini, E., Montecucco, C., Parente, L., Rappuoli, R.: Gene structure of the Helicobacter pylori cytotoxin and evidence of its key role in gastric disease. J. Exp. Med. 179, 1653-1658 (1994).
70. Tombola, F., Carlesso, C., Szabo, I., De Bernard, M., Reyrat, J. M., Telford, J. L., Rappuoli, R., Montecucco, C., Papini, E., Zoratti, M.: Helicobacter pylori vacuolating toxin forms anion-selective channels in planar lipid bilayers: possible implications for the mechanism of cellular vacuolation, Biophys. J. 76, 1401-1409 (1999).
71. Vinion-Dubiel, A. D., McClain, M. S., Czajkowsky, D. M., Iwamoto, H., Ye, D., Cao, P., Schraw, W., Szabo, G., Blanke, S. R., Shao, Z., Cover, T. L.: A dominant negative mutant of Helicobacter pylori vacuolating toxin (VacA) inhibits VacA-induced cell vacuolation. J. Biol. Chem. 274, 37736-37742 (1999).
72. Wagner, S., Beil, W., Westermann, J., Logan, R. P., Bock, C. T., Trautwein, C., Bleck, J. S., Manns, M. P.: Regulation of gastric epithelial cell growth by Helicobacter pylori: offdence for a major role of apoptosis. Gastroenterology 113, 1836-1847 (1997).
73. Wang, J., Brooks, E. G., Bamford, K. B., Denning, T. L., Pappo, J., Ernst, P. B.: Negative selection of T cells by Helicobacter pylori as a model for bacterial strain selection by immune evasion. J. Immunol. 167, 926-934 (2001).
74. Willhite, D. C., Ye, D., Blanke, S. R.: Fluorescence resonance energy transfer microscopy of the Helicobacter pylori vacuolating cytotoxin within mammalian cells. Infect. Immun. 70, 3824-3832 (2002).
75. Yahiro, K., Niidome, T., Kimura, M., Hatakeyama, T., Aoyagi, H., Kurazono, H., Imagawa, K., Wada, A., Moss, J., Hirayama, T.: Activation of Helicobacter pylori VacA toxin by alkaline or acid conditions increases its binding to a 250-kDa receptor protein-tyrosine phosphatase β. J. Biol. Chem. 274, 36693-36699 (1999).
76. Yahiro, K., Wada, A., Nakayama, M., Kimura, T., Ogushi, K., Niidome, T., Aoyagi, H., Yoshino, K., Yonezawa, K., Moss, J., Hirayama, T.: Protein-tyrosine phosphatase α, RPTP α, is a Helicobacter pylori VacA receptor. J. Biol. Chem. 278, 19183-19189 (2003).
77. Ye, D., Blanke, S. R.: Functional complementation reveals the importance of intermolecular monomer interactions for Helicobacter pylori VacA vacuolating activity. Mol. Microbiol. 43, 1243-1253 (2002).
78. Ye, D., Willhite, D. C., Blanke, S. R.: Identification of the minimal intracellular vacuolating domain of the Helicobacter pylori vacuolating toxin. J. Biol. Chem. 274, 9277-9282 (1999).
79. Zheng, P. Y., Jones, N. L.: Helicobacter pylori strains expressing the vacuolating cytotoxin interrupt phagosome maturation in macrophages by recruiting and retaining TACO (coronin 1) protein. Cell. Microbiol. 5, 25-40 (2003).