The Helicobacter pylori VacA cytotoxin activates RBL-2H3 cells by inducing cytosolic calcium oscillations

Cellular Microbiology

Volumn 7, Issue 2, 2005, Pages 191-198

  de Bernard, Marina ^a,b   Cappon, Andrea ^a,b   Pancotto, Laura ^c   Ruggiero, Paolo ^c   Rivera, Juan ^d   Del Giudice, Giuseppe ^c   Montecucco, Cesare ^a,b  

^a UNIVERSITY OF PADOVA   (Italy)

^b Ist Veneto di Medicina Molecolare   (Italy)

^c CHIRON VACCINES   (Italy)

^d NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR NECROSIS FACTOR ALPHA; VACUOLATING TOXIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL ACTIVATION; CELL LINE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXOCYTOSIS; HELICOBACTER PYLORI; IMMUNE RESPONSE; MAST CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SECRETORY GRANULE;

ANIMALS; BACTERIAL PROTEINS; CALCIUM SIGNALING; CELL DEGRANULATION; CELL LINE; CELLS, CULTURED; CYTOPLASM; EGTAZIC ACID; EXOCYTOSIS; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; MAST CELLS; RATS; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI;

EID: 13844315698     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2004.00446.x     Document Type: Article

References (44)

1. Atherton, J.C., Cao, P., Peek, R.M., Jr, Tummuru, M.K., Blaser, M.J., and Cover, T.L. (1995) 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.
2. Bayguinov, O., Hagen, B, Bonev, A.D. Nelson, M.T., and Sanders, K.M. (2000) Intracellular calcium events activated by ATP in murine colonic myocytes. Am J Physiol 279: C126-C135.
3. Bechi, P., Dei, R., Di Bello, M.G., and Masini, E. (1993) Helicobacter pylori potentiates histamine release from serosal rat mast cells in vitro. Dig Dis Sci 38: 944-949.
4. de Bernard, M., Papini, E., de Filippis, V., Gottardi, E., Telford. J. L., 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.
5. 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.
6. Betten, A., Bylund, J., Cristophe, T., Boulay, F., Romero, A., Hellstrand, K., and Dahlgren, C. (2001) A prinflammatory peptide from Helicobacter pylori activates monocytes to induce lymphocyte disfunction and apoptosis. J Clin Invest 108: 1221-1228.
7. Blaser, M.J. (1993) Helicobacter pylori: microbiology of a 'slow' bacterial infection. Trends Microbiol 1: 255-259.
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. Cover, T.L., and Blaser, M.J. (1992) Purification and characterization of the vacuolating toxin from Helicobacter pylori. J Biol Chem 267: 10570-10575.
10. Cover, T.L., Hanson, P.I., and Heuser, J.E. (1997) Acid-induced dissociation of VacA, the Helicobacter pylori vacuolating toxin, reveals its pattern of assembly. J Cell Biol 138: 759-769.
11. 2+ oscillations in non-excitable cells. Annu Rev Physiol 55: 427-454.
12. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450.
13. 2+ on TNF-α and IL-6 secretion from RBL-2H3 mast cells. Cell Signal 14: 633-639.
14. 2+ responses and secretion in individual RBL-2H3 mucosal mast cells. J Biol Chem 272: 31225-31229.
15. Kurose, I., Granger, D.N., Evans, D.J., Jr, Evans, D.G., Graham, D.Y., Miyasaka, M., et al. (1994) Helicobacter pylori-induced microvascular protein leakage in rats: role of neutrophils, mast cells, and platelets. Gastroenterology 107: 70-79.
16. Malaviya, R., and Abraham, S.N. (2001) Mast cell modulation of immune response to bacteria. Immunol Rev 179: 16-24.
17. Manetti, R., Massari, P., Burroni, D., de Bernard, M., Marchini, A., Olivieri, L., et al. (1995) Helicobacter pylori cytotoxin: importance of native conformation for induction of neutralizing antibodies. Infect Immun 63: 4476-4480.
18. Marshall, B.J., Armstrong, J.A., McGeche, D.B., and Glancy, R.J. (1985) Attempt to fulfil Koch's postulates for pyloric Campylobacter. Med J Australia 142: 436-439.
19. Molinari, M., Galli, C., de Bernard, M., Norais, N., Ruysschaert, J. M., Rappuoli, R., and Montecucco, C. (1998) The acid activation of Helicobacter pylori toxin VacA: structural and membrane binding studies. Biochem Biophys Res Comun 248: 334-340.
20. Montecucco, C., and Rappuoli, R. (2001) Living dangerously: how Helicobacter pylori survives in the human stomach. Nat Rev Mol Cell Biol 2: 457-466.
21. Montecucco, C., and de Bernard, M. (2003) Molecular and cellular mechanisms of action of the vacuolating cytotoxin (VacA) and neutrophil-activating protein (HP-NAP) virulence factors of Helicobacter pylori. Microbes Infect 5: 715-721.
22. Montecucco, C., de Bernard, M., Papini, E., and Zoratti, M. (2001) Helicobacter pylori vacuolating cytotoxin. Cell intoxication and anion-specific channel activity. In Current Topics in Microbiology and Immunology, Vol. 257 Pore-Forming Toxins. Van der Goot, F.G. (ed.). Berlin: Springer-Verlag, pp. 113-129.
23. Nakajima, S., Krishnan, B., Ota, H., Segura, A.M., Hattori, T., Graham, D.Y., and Genta, R.M. (1997) Mast cell involvement in gastritis with or without Helicobacter pylori infection. Gastroenterology 113: 746-754.
24. NIH Consensus Development Panel on Helicobacter pylori in Peptic Ulcer Disease (1994) Helicobacter pylori in peptic ulcer disease. JAMA 272: 65-69.
25. Pagliaccia, C., Wang, X.M., Tardy, F., Telford, J.L., Ruysschaert, J.M., and Cabiaux, V. (2000) Structure and interaction of VacA of Helicobacter pylori with a lipid membrane. Eur J Biochem 267: 104-109.
26. Papini, E, de Bernard, M., Milia, E., 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.
27. 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.
28. Papini, E., Zoratti, M., and Cover, T.L. (2001) In search of the Helicobacter pylori VacA mechanism of action. Toxicon 39: 1757-1767.
29. Phadnis, S.H., Ilver, D., Janzon, L., Normark, S., and Westblom, T.U. (1994) Pathological significance and molecular characterization of the vacuolating toxin gene of Helicobacter pylori. Infect Immun 62: 1557-1565.
30. Saitoh, S., Arudchandran, R., Manetz, T.S., Zhang, W., Sommers, C.L., Love, P.E., et al. (2000) LAT is essential for Fc(epsilon)RI-mediated mast cell activation. Immunity 12: 525-535.
31. 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.
32. Schwartz, L.B., Austen, K.F., and Wasserman, S.I. (1979) Immunologic release of β-hexosaminidase and β-glucoronidase from purified rat serosal mast cells. J Immunol 123: 1445-1450.
33. Supajatu, V., Ushio, H., Wada, A., Yahiro, K., Okumura, K., Ogawa, H., et al. (2002) Cutting edge: VacA, a vacuolating cytotoxin of Helicobacter pylori, directly activates mast cells for migration and production of proinflammatory cytokines. J Immunol 168: 2603-2607.
34. Szabò, 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.
35. Taylor, D.E., and Blaser, M.J. (1991) The epidemiology of Helicobacter pylori infection. Epidemiol Rev 13: 42-59.
36. Tombola, F., Morbiato, L., Del Giudice, G., Rappuoli, R., Zoratti, M., and Papini, E. (2001) The Helicobacter pylori VacA toxin is a urea permease that promotes urea diffusion across epithelia. J Clin Invest 108: 929-937.
37. Tsien, R.Y. (1980) New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry 19: 2396-23404.
38. 2+ oscillations in renal epithelial cells. Nature 405: 694-697.
39. + Helicobacter pylori strain. Clin Exp Immunol 115: 421-427.
40. Warren, J.R., and Marshall, B.J. (1983) Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1: 1273-1275.
41. Wershil, B.K., Wang, Z.S., Gordon, J.R., and Galli, S.J. (1991) Recruitment of neuthrophils during Ig-E-dependent cutaneous late phase reactions in the mouse is mast cell-dependent: partial inhibition of the reaction with antiserum against tumor necrosis factor-alpha. J Clin Invest 87: 446-453.
42. Wershil, B.K., Furuta, G.T., Wang, Z.S., and Galli, S.J. (1996) Mast cell-dependent neutrophil and mononuclear cell recruitment in immunoglobulin E-induced gastric reactions in mice. Gastroenterology 110: 1482-1490.
43. White, J., Pluznik, D.H., Ishizaka, K., and Ishizaka, T. (1985) Antigen-induced increase in protein kinase C activity in plasma membrane of mast cells. Proc Natl Acad Sci USA 82: 8193-8197.
44. Yahiro, K., Niidome, T., Kimura, M., Hatakeyama, T., Aoyagi, H., Kurazono, H., et al. (1999) Activation of Helicobacter pylori VacA toxin by alkaline or acid conditions increases its binding to a 250-kDa receptor protein-tyrosine phosphatase beta. J Biol Chem 274: 36693-36699.