The concerted action of the Helicobacter pylori cytotoxin VacA and of the v-ATPase proton pump induces swelling of isolated endosomes

Cellular Microbiology

Volumn 9, Issue 6, 2007, Pages 1481-1490

  Genisset, Christophe ^a,c   Puhar, Andrea ^a   Calore, Federica ^a,b   de Bernard, Marina ^a,b   Dell'Antone, Paolo ^a   Montecucco, Cesare ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c INSTITUT PASTEUR DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; AMINO ACID; ANION; BROMINE; CHLORIDE ION; IODIDE ION; PROTON PUMP; PYRUVIC ACID; THIOCYANATE; VACUOLATING TOXIN;

ACIDIFICATION; AMINO ACID SUBSTITUTION; ANION TRANSPORT; ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; CELL CULTURE; CONFOCAL MICROSCOPY; ENDOSOME; ENZYME ACTIVATION; ENZYME ACTIVITY; HELICOBACTER PYLORI; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANIONS; BACTERIAL PROTEINS; CELL-FREE SYSTEM; CELLS, CULTURED; CRICETINAE; ENDOSOMES; HELA CELLS; HELICOBACTER PYLORI; HUMANS; VACUOLAR PROTON-TRANSLOCATING ATPASES; VACUOLES;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI;

EID: 34248640142     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2006.00886.x     Document Type: Article

References (58)

1. Adrian, M., Cover, T.L., Dubochet, J., and Heuser, J.E. (2002) Multiple oligomeric states of the Helicobacter pylori vacuolating toxin demonstrated by cryo-electron microscopy. J Mol Biol 318: 121-133.
2. Barasch, J., Kiss, B., Prince, A., Saiman, L., Gruenert, D., and al-Awqati, Q. (1991) Defective acidification of intracellular organelles in cystic fibrosis. Nature 352: 70-73.
3. de Bernard, M., Papini, E., de Filippis, V., Gottardi, E., Telford, J., Manetti, R., et al. (1995) Low pH activates the vacuolating toxin of Helicobacter pylori, which becomes acid and pepsin resistant. J Biol Chem 270: 23937-23940.
4. de Bernard, M., Arico, B., Papini, E., Rizzuto, R., Grandi, G., Rappuoli, R., and Montecucco, C. (1997) Helicobacter pylori toxin VacA induces vacuole formation by acting in the cell cytosol. Mol Microbiol 26: 665-674.
5. de Bernard, M., Burroni, D., Papini, E., Rappuoli, R., Telford, J., and Montecucco, C. (1998) Identification of the Helicobacter pylori VacA toxin domain active in the cell cytosol. Infect Immun 66: 6014-6016.
6. de Bernard, M., Moschioni, M., Habermann, A., Griffiths, G., and Montecucco, C. (2002) Cell vacuolization induced by Helicobacter pylori VacA cytotoxin does not depend on late endosomal SNAREs. Cell Microbiol 4: 11-18.
7. Blanke, S.R. (2005) Micro-managing the executioner: Pathogen targeting of mitochondria. Trends Microbiol 13: 64-71.
8. Boncristiano, M., Paccani, S.R., Barone, S., Ulivieri, C., Patrussi, L., Ilver, D., et al. (2003) The Helicobacter pylori vacuolating toxin inhibits T cell activation by two independent mechanisms. J Exp Med 198: 1887-1897.
9. Cover, T.L., and Blanke, S.R. (2005) Helicobacter pylori VacA, a paradigm for toxin multifunctionality. Nat Rev Microbiol 3: 320-332.
10. Cover, T.L., and Blaser, M.J. (1992) Purification and characterization of the vacuolating toxin from Helicobacter pylori. J Biol Chem 267: 10570-10575.
11. Cover, T.L., Vaughn, S.G., Cao, P., and Blaser, M.J. (1992) Potentiation of Helicobacter pylori vacuolating toxin activity by nicotine and other weak bases. J Infect Dis 166: 1073-1078.
12. Cover, T.L., Reddy, L.Y., and Blaser, M.J. (1993) Effects of ATPase inhibitors on the response of HeLa cells to Helicobacter pylori vacuolating toxin. Infect Immun 61: 1427-1431.
13. Cover, T.L., Krishna, U.S., Israel, D.A., and Peek, R.M., Jr (2003) Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res 63: 951-957.
14. Czajkowsky, D.M., Iwamoto, H., Cover, T.L., and Shao, Z. (1999) The vacuolating toxin from Helicobacter pylori forms hexameric pores in lipid bilayers at low pH. Proc Natl Acad Sci USA 96: 2001-2006.
15. Debellis, L., Papini, E., Caroppo, R., Montecucco, C., and Curci, S. (2001) Helicobacter pylori cytotoxin VacA increases alkaline secretion in gastric epithelial cells. Am J Physiol Gastrointest Liver Physiol 281: G1440-G1448.
16. Dell'Antone, P. (1979) Evidence for an ATP-driven 'proton pump'in rat liver lysosomes by basic dyes uptake. Biochem Biophys Res Commun 86: 180-189.
17. Dell'Antone, P., and Piergallini, L. (1997) The antineoplastic drug lonidamine interferes with the acidification mechanism of cell organelles. Biochim Biophys Acta 1358: 46-52.
18. Fuchs, R., Schmid, S., and Mellman, I. (1989) A possible role for Na+, K+ -ATPase in regulating ATP-dependent endosome acidification. Proc Natl Acad Sci USA 86: 539-543.
19. Fuchs, R., Ellinger, A., Pavelka, M., Mellman, I., and Klapper, H. (1994) Rat liver endocytic coated vesicles do not exhibit ATP-dependent acidification in vitro. Proc Natl Acad Sci USA 91: 4811-4815.
20. Galmiche, A., Rassow, J., Doye, A., Cagnol, S., Chambard, J.C., Contamin, S., et al. (2000) The N-terminal 34kDa fragment of Helicobacter pylori vacuolating cytotoxin targets mitochondria and induces cytochrome c release. EMBO J 19: 6361-6370.
21. Gebert, B., Fischer, W., Weiss, E., Hoffmann, R., and Haas, R. (2003) Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301: 1099-1102.
22. Genisset, C., Galeotti, C.L., Lupetti, P., Mercati, D., Skibinski, D.A., Barone, S., etal. (2006) A Helicobacter pylori vacuolating toxin mutant that fails to oligomerize has a dominant negative phenotype. Infect Immun 74: 1786-1794.
23. Gorvel, J.P., Chavrier, P., Zerial, M., and Gruenberg, J. (1991) rab5 controls early endosome fusion in vitro. Cell 64: 915-925.
24. Gruenberg, J. (2001) The endocytic pathway: A mosaic of domains. Nat Rev Mol Cell Biol 2: 721-730.
25. Gunther, W., Luchow, A., Cluzeaud, F., Vandewalle, A., and Jentsch, T.J. (1998) ClC-5, the chloride channel mutated in Dent's disease, colocalizes with the proton pump in endocytotically active kidney cells. Proc Natl Acad Sci USA 95: 8075-8080.
26. Hotchin, N.A., Cover, T.L., and Akhtar, N. (2000) Cell vacuolation induced by the VacA cytotoxin of Helicobacter pylori is regulated by the Rac1 GTPase. J Biol Chem 275: 14009-14012.
27. Ilver, D., Barone, S., Mercati, D., Lupetti, P., and Telford, J.L. (2004) Helicobacter pylori toxin VacA is transferred to host cells via a novel contact-dependent mechanism. Cell Microbiol 6: 167-174.
28. Kobayashi, T., Stang, E., Fang, K.S., de Moerloose, P., Parton, R.G., and Gruenberg, J. (1998) A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392: 193-197.
29. Lupetti, P., Heuser, J.E., Manetti, R., Massari, P., Lanzavecchia, S., Bellon, P.L., et al. (1996) Oligomeric and subunit structure of the Helicobacter pylori vacuolating cytotoxin. J Cell Biol 133: 801-807.
30. McClain, M.S., Iwamoto, H., Cao, P., Vinion-Dubiel, A.D., Li, Y., Szabo, G., et al. (2003) Essential role of a GXXXG motif for membrane channel formation by Helicobacter pylori vacuolating toxin. J Biol Chem 278: 12101-12108.
31. Manetti, R., Massari, P., Burroni, D., de Bernard, M., Marchini, A., Olivieri, R., et al. (1995) Helicobacter pylori cytotoxin: Importance of native conformation for induction of neutralizing antibodies. Infect Immun 63: 4476-4480.
32. Marchetti, M., Arico, B., Burroni, D., Figura, N., Rappuoli, R., and Ghiara, P. (1995) Development of a mouse model of Helicobacter pylori infection that mimics human disease. Science 267: 1655-1658.
33. Marshall, B.J., and Warren, J.R. (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 1: 1311-1315.
34. Mendz, G.L., Hazell, S.L., and van Gorkom, L. (1994) Pyruvate metabolism in Helicobacter pylori. Arch Microbiol 162: 187-192.
35. Molinari, M., Galli, C., Norais, N., Telford, J.L., Rappuoli, R., Luzio, J.P., and Montecucco, C. (1997) Vacuoles induced by Helicobacter pylori toxin contain both late endosomal and lysosomal markers. J Biol Chem 272: 25339-25344.
36. Molinari, M., Salio, M., Galli, C., Norais, N., Rappuoli, R., Lanzavecchia, A., and Montecucco, C. (1998) Selective inhibition of Ii-dependent antigen presentation by Helicobacter pylori toxin VacA. J Exp Med 187: 135-140.
37. Montecucco, C., and Rappuoli, R. (2001) Living dangerously: How Helicobacter pylori survives in the human stomach. Nat Rev Mol Cell Biol 2: 457-466.
38. Moschioni, M., Tombola, F., de Bernard, M., Coelho, A., Zitzer, A., Zoratti, M., and Montecucco, C. (2002) The Vibrio cholerae haemolysin anion channel is required for cell vacuolation and death. Cell Microbiol 4: 397-409.
39. Papini, E., Bugnoli, M., De Bernard, M., Figura, N., Rappuoli, R., and Montecucco, C. (1993a) Bafilomycin A1 inhibits Helicobacter pylori -induced vacuolization of HeLa cells. Mol Microbiol 7: 323-327.
40. Papini, E., de Bernard, M., Bugnoli, M., Milia, E., Rappuoli, R., and Montecucco, C. (1993b) Cell vacuolization induced by Helicobacter pylori: Inhibition by bafilomycins A1, B1, C1 and D. FEMS Microbiol Lett 113: 155-159.
41. Papini, E., de Bernard, M., Milia, E., Bugnoli, M., Zerial, M., Rappuoli, R., and Montecucco, C. (1994) Cellular vacuoles induced by Helicobacter pylori originate from late endosomal compartments. Proc Natl Acad Sci USA 91: 9720-9724.
42. Papini, E., Gottardi, E., Satin, B., de Bernard, M., Massari, P., Telford, J., et al. (1996) The vacuolar ATPase proton pump is present on intracellular vacuoles induced by Helicobacter pylori. J Med Microbiol 45: 84-89.
43. Papini, E., Satin, B., Bucci, C., de Bernard, M., Telford, J.L., Manetti, R., et al. (1997) The small GTP binding protein rab7 is essential for cellular vacuolation induced by Helicobacter pylori cytotoxin. EMBO J 16: 15-24.
44. Papini, E., Satin, B., Norais, N., de Bernard, M., Telford, J.L., Rappuoli, R., and Montecucco, C. (1998) Selective increase of the permeability of polarized epithelial cell monolayers by Helicobacter pylori vacuolating toxin. J Clin Invest 102: 813-820.
45. Parsonnet, J., Hansen, S., Rodriguez, L., Gelb, A.B., Warnke, R.A., Jellum, E., et al. (1994) Helicobacter pylori infection and gastric lymphoma. N Engl J Med 330: 1267-1271.
46. Ricci, V., Sommi, P., Fiocca, R., Romano, M., Solcia, E., and Ventura, U. (1997) Helicobacter pylori vacuolating toxin accumulates within the endosomal-vacuolar compartment of cultured gastric cells and potentiates the vacuolating activity of ammonia. J Pathol 183: 453-459.
47. Salama, N.R., Otto, G., Tompkins, L., and Falkow, S. (2001) Vacuolating cytotoxin of Helicobacter pylori plays a role during colonization in a mouse model of infection. Infect Immun 69: 730-736.
48. Sato, S.B., and Toyama, S. (1994) Interference with the endosomal acidification by a monoclonal antibody directed toward the 116 (100)-kD subunit of the vacuolar type proton pump. J Cell Biol 127: 39-53.
49. Skibinski, D.A., Genisset, C., Barone, S., and Telford, J.L. (2006) The cell-specific phenotype of the polymorphic vacA midregion is independent of the appearance of the cell surface receptor protein tyrosine phosphatase beta. Infect Immun 74: 49-55.
50. Sonawane, N.D., Thiagarajah, J.R., and Verkman, A.S. (2002) Chloride concentration in endosomes measured using a ratioable fluorescent Cl- indicator: Evidence for chloride accumulation during acidification. J Biol Chem 277: 5506-5513.
51. Sundrud, M.S., Torres, V.J., Unutmaz, D., and Cover, T.L. (2004) Inhibition of primary human T cell proliferation by Helicobacter pylori vacuolating toxin (VacA) is independent of VacA effects on IL-2 secretion. Proc Natl Acad Sci USA 101: 7727-7732.
52. Szabo, I., Brutsche, S., Tombola, F., Moschioni, M., Satin, B., Telford, J.L., et al. (1999) 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.
53. Telford, J.L., Ghiara, P., Dell'Orco, M., Comanducci, M., Burroni, D., Bugnoli, M., et al. (1994) Gene structure of the Helicobacter pylori cytotoxin and evidence of its key role in gastric disease. J Exp Med 179: 1653-1658.
54. Tombola, F., Carlesso, C., Szabo, I., de Bernard, M., Reyrat, J.M., Telford, J.L., et al. (1999) 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.
55. Willhite, D.C., Cover, T.L., and Blanke, S.R. (2003) Cellular vacuolation and mitochondrial cytochrome c release are independent outcomes of Helicobacter pylori vacuolating cytotoxin activity that are each dependent on membrane channel formation. J Biol Chem 278: 48204-48209.
56. Yamasaki, E., Wada, A., Kumatori, A., Nakagawa, I., Funao, J., Nakayama, M., et al. (2006) Helicobacter pylori vacuolating cytotoxin induces activation of the proapoptotic protein Bax and Bak, leading to cytochrome c release and cell death, independent of vacuolation. J Biol Chem 281: 11250-11259.
57. Ye, D., and Blanke, S.R. (2000) Mutational analysis of the Helicobacter pylori vacuolating toxin amino terminus: Identification of amino acids essential for cellular vacuolation. Infect Immun 68: 4354-4357.
58. Ye, D., Willhite, D.C., and Blanke, S.R. (1999) Identification of the minimal intracellular vacuolating domain of the Helicobacter pylori vacuolating toxin. J Biol Chem 274: 9277-9282.