Helicobacter pylori VacA, a paradigm for toxin multifunctionality (original) (raw)
Collier, R. J. Understanding the mode of action of diphtheria toxin: a perspective on progress during the 20th century. Toxicon39, 1793–803 (2001). ArticleCASPubMed Google Scholar
Alouf, J. E. & Freer, J. H. The Comprehensive Sourcebook of Bacterial Protein Toxins (Academic Press, London, San Diego, California, 1999). Google Scholar
Schiavo, G. & van der Goot, F. G. The bacterial toxin toolkit. Nature Rev. Mol. Cell Biol.2, 530–537 (2001). ArticleCAS Google Scholar
Parker, M. W. Cryptic clues as to how water-soluble protein toxins form pores in membranes. Toxicon42, 1–6 (2003). ArticleCASPubMed Google Scholar
Fivaz, M., Abrami, L., Tsitrin, Y. & van der Goot, F. G. Not as simple as just punching a hole. Toxicon39, 1637–1645 (2001). ArticleCASPubMed Google Scholar
Montecucco, C., Papini, E. & Schiavo, G. Bacterial protein toxins penetrate cells via a four-step mechanism. FEBS Lett.346, 92–98 (1994). ArticleCASPubMed Google Scholar
Marshall, B. J. & Warren, J. R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet1, 1311–1315 (1984). ArticleCASPubMed Google Scholar
Monack, D. M., Mueller, A. & Falkow, S. Persistent bacterial infections: the interface of the pathogen and the host immune system. Nature Rev. Microbiol.2, 747–765 (2004). ArticleCAS Google Scholar
Petersen, A. M., Sorensen, 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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Leunk, R. D., P. T., J., 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). The first description ofH. pylorivacuolating cytotoxic activity. ArticleCASPubMed Google Scholar
Cover, T. L. & Blaser, M. J. Purification and characterization of the vacuolating toxin from Helicobacter pylori. J. Biol. Chem.267, 10570–10575 (1992). Describes the initial purification and characterization ofH. pyloriVacA. CASPubMed Google Scholar
Cover, T. L., Tummuru, M. K. R., Cao, P., Thompson, S. A. & Blaser, M. J. Divergence of genetic sequences for the vacuolating cytotoxin among Helicobacter pylori strains. J. Biol. Chem.269, 10566–10573 (1994). CASPubMed Google Scholar
Telford, J. L. et al. Gene structure of the Helicobacter pylori cytotoxin and evidence of its key role in gastric disease. J. Exp. Med.179, 1653–1658 (1994). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Ilver, D., Barone, S., Mercati, D., Lupetti, P. & Telford, J. L. Helicobacter pylori toxin VacA is transferred to host cells via a novel contact-dependent mechanism. Cell. Microbiol.6, 167–174 (2004). ArticleCASPubMed Google Scholar
Lupetti, P. et al. Oligomeric and subunit structure of the Helicobacter pylori vacuolating cytotoxin. J. Cell. Biol.133, 801–807 (1996). ArticleCASPubMed Google Scholar
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). An analysis of the quaternary structure of VacA oligomers. ArticleCASPubMedPubMed Central Google Scholar
Lanzavecchia, S. et al. Three-dimensional reconstruction of metal replicas of the Helicobacter pylori vacuolating cytotoxin. J. Struct. Biol.121, 9–18 (1998). ArticleCASPubMed Google Scholar
Adrian, M., Cover, T. L., Dubochet, J. & Heuser, J. E. Multiple oligomeric states of the Helicobacter pylori vacuolating toxin demonstrated by cryo-electron microscopy. J. Mol. Biol.318, 121–133 (2002). ArticleCASPubMed Google Scholar
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. USA96, 2001–2006 (1999). ArticleCASPubMedPubMed Central Google Scholar
Tombola, F. et al. 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). ArticleCASPubMedPubMed Central Google Scholar
Iwamoto, H., Czajkowsky, D. M., Cover, T. L., Szabo, G. & Shao, Z. VacA from Helicobacter pylori: a hexameric chloride channel. FEBS Lett.450, 101–104 (1999). ArticleCASPubMed Google Scholar
Szabo, I. et al. 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). The first demonstration that VacA forms anion-selective membrane channels in cells. ArticleCASPubMedPubMed Central Google Scholar
de Bernard, M. et al. Low pH activates the vacuolating toxin of Helicobacter pylori, which becomes acid and pepsin resistant. J. Biol. Chem.270, 23937–23940 (1995). ArticleCASPubMed Google Scholar
Molinari, M. et al. The acid activation of Helicobacter pylori toxin VacA: structural and membrane binding studies. Biochem. Biophys. Res. Commun.248, 334–340 (1998). ArticleCASPubMed Google Scholar
Yahiro, K. et al. 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). ArticleCASPubMed Google Scholar
Nguyen, V. Q., Caprioli, R. M. & Cover, T. L. Carboxy-terminal proteolytic processing of Helicobacter pylori vacuolating toxin. Infect. Immun.69, 543–546 (2001). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Torres, V. J., McClain, M. S. & Cover, T. L. Interactions between p-33 and p-55 domains of the Helicobacter pylori vacuolating cytotoxin (VacA). J. Biol. Chem.279, 2324–2331 (2004). ArticleCASPubMed Google Scholar
Garner, J. A. & Cover, T. L. Binding and internalization of the Helicobacter pylori vacuolating cytotoxin by epithelial cells. Infect. Immun.64, 4197–4203 (1996). CASPubMedPubMed Central Google Scholar
Pagliaccia, C. et al. The m2 form of the Helicobacter pylori cytotoxin has cell type-specific vacuolating activity. Proc. Natl Acad. Sci. USA95, 10212–10217 (1998). ArticleCASPubMedPubMed Central Google Scholar
Wang, W. -C., Wang, H. -J. & Kuo, C. -H. Two distinctive cell binding patterns by vacuolating toxin fused with glutathione _S_-transferase: one high-affinity m1-specific binding and the other lower-affinity binding for variant m forms. Biochemistry40, 11887–11896 (2001). ArticleCASPubMed Google Scholar
Wang, H. J. & Wang, W. C. Expression and binding analysis of GST–VacA fusions reveals that the Cterminal approximately 100-residue segment of exotoxin is crucial for binding in HeLa cells. Biochem. Biophys. Res. Commu.n278, 449–454 (2000). ArticleCAS Google Scholar
Reyrat, J. M. et al. 3D imaging of the 58-kDa cell binding subunit of the Helicobacter pylori cytotoxin. J. Mol. Biol.290, 459–470 (1999). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
de Bernard, M. et al. Identification of the Helicobacter pylori VacA toxin domain active in the cell cytosol. Infect. Immun.66, 6014–6016 (1998). CASPubMedPubMed Central Google Scholar
de Bernard, M. et al. Helicobacter pylori toxin VacA induces vacuole formation by acting in the cell cytosol. Mol. Microbiol.26, 665–674 (1997). ArticleCASPubMed Google Scholar
Vinion-Dubiel, A. D. et al. A dominant negative mutant of Helicobacter pylori vacuolating toxin (VacA) inhibits VacA-induced cell vacuolation. J. Biol. Chem.274, 37736–37742 (1999). ArticleCASPubMed Google Scholar
McClain, M. S. et al. Essential role of a GXXXG motif for membrane channel formation by Helicobacter pylori vacuolating toxin. J. Biol. Chem.278, 12101–12108 (2003). Demonstration that membrane channel formation has an important role in VacA cytotoxicity. ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Kim, S., Chamberlain, A. K. & Bowie, J. U. Membrane channel structure of Helicobacter pylori vacuolating toxin: role of multiple GXXXG motifs in cylindrical channels. Proc. Natl Acad. Sci. USA101, 5988–5991 (2004). ArticleCASPubMedPubMed Central Google Scholar
Ye, D. & Blanke, S. R. Mutational analysis of the Helicobacter pylori vacuolating toxin amino terminus: identification of amino acids essential for cellular vacuolation. Infect. Immun.68, 4354–4357 (2000). ArticleCASPubMedPubMed Central Google Scholar
Atherton, J. C. et al. 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). Description of multiple families ofvacAalleles. ArticleCASPubMed Google Scholar
Van Doorn, L. J. et al. Geographic distribution of vacA allelic types of Helicobacter pylori. Gastroenterology116, 823–830 (1999). ArticleCASPubMed Google Scholar
McClain, M. S. et al. A 12-amino-acid segment, present in type s2 but not type s1 Helicobacter pylori VacA proteins, abolishes cytotoxin activity and alters membrane channel formation. J. Bacteriol.183, 6499–6508 (2001). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
Letley, D. P. & Atherton, J. C. Natural diversity in the N terminus of the mature vacuolating cytotoxin of Helicobacter pylori determines cytotoxin activity. J. Bacteriol.182, 3278–3280 (2000). ArticleCASPubMedPubMed Central Google Scholar
Ji, X. et al. Cell specificity of Helicobacter pylori cytotoxin is determined by a short region in the polymorphic midregion. Infect. Immun.68, 3754–3757 (2000). ArticleCASPubMedPubMed Central Google Scholar
Tombola, F. et al. How the loop and middle regions influence the properties of Helicobacter pylori VacA channels. Biophys. J.81, 3204–3215 (2001). ArticleCASPubMedPubMed Central Google Scholar
Eaton, K. A., Cover, T. L., Tummuru, M. K., Blaser, M. J. & Krakowka, S. Role of vacuolating cytotoxin in gastritis due to Helicobacter pylori in gnotobiotic piglets. Infect. Immun.65, 3462–3464 (1997). CASPubMedPubMed Central Google Scholar
Wirth, H. P., Beins, M. H., Yang, M., Tham, K. T. & Blaser, M. J. Experimental infection of Mongolian gerbils with wild-type and mutant Helicobacter pylori strains. Infect. Immun.66, 4856–4866 (1998). CASPubMedPubMed Central Google Scholar
Ogura, K. et al. Virulence factors of Helicobacter pylori responsible for gastric diseases in mongolian gerbil. J. Exp. Med.192, 1601–1610 (2000). ArticleCASPubMedPubMed Central Google Scholar
Salama, N. R., Otto, G., Tompkins, L. & Falkow, S. Vacuolating cytotoxin of Helicobacter pylori plays a role during colonization in a mouse model of infection. Infect. Immun.69, 730–736 (2001). Demonstration of a role for VacA in colonization of the stomach byH. pylori. ArticleCASPubMedPubMed Central Google Scholar
Guo, B. P. & Mekalanos, J. J. Rapid genetic analysis of Helicobacter pylori gastric mucosal colonization in suckling mice. Proc. Natl Acad. Sci. USA99, 8354–8359 (2002). ArticleCASPubMedPubMed Central Google Scholar
Marchetti, M. et al. Development of a mouse model of Helicobacter pylori infection that mimics human disease. Science267, 1655–1658 (1995). ArticleCASPubMed Google Scholar
Marchetti, M. et al. Protection against Helicobacter pylori infection in mice by intragastric vaccination with H. pylori antigens is achieved using a non-toxic mutant of E. coli heat-labile enterotoxin (LT) as adjuvant. Vaccine16, 33–37 (1998). ArticleCASPubMed Google Scholar
Ghiara, P. et al. Therapeutic intragastric vaccination against Helicobacter pylori in mice eradicates an otherwise chronic infection and confers protection against re-infection. Infect. Immun.65, 4996–5002 (1997). CASPubMedPubMed Central Google Scholar
van Doorn, L. J. et al. Clinical relevance of the cagA, vacA and iceA status of Helicobacter pylori. Gastroenterology115, 58–66 (1998). ArticleCASPubMed Google Scholar
Figueiredo, C. et al. Helicobacter pylori and interleukin 1 genotyping: an opportunity to identify high-risk individuals for gastric carcinoma. J. Natl Cancer Inst.94, 1680–1687 (2002). ArticleCASPubMed Google Scholar
Atherton, J. C., Peek, R. M. Jr, Tham, K. T., Cover, T. L. & Blaser, M. J. Clinical and pathological importance of heterogeneity in vacA, the vacuolating cytotoxin gene of Helicobacter pylori. Gastroenterology112, 92–99 (1997). ArticleCASPubMed Google Scholar
Fujikawa, A. et al. Mice deficient in protein tyrosine phosphatase receptor type Z are resistant to gastric ulcer induction by VacA of Helicobacter pylori. Nature Genet.33, 375–381 (2003).In vivoanalysis of the role of RPTPβ as a VacA receptor. ArticleCASPubMed Google Scholar
Supajatura, V. et al. 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 (2002). ArticleCASPubMed Google Scholar
Smoot, D. T., Resau, J. H., Earlington, M. H., Simpson, M. & Cover, T. L. Effects of Helicobacter pylori vacuolating cytotoxin on primary cultures of human gastric epithelial cells. Gut39, 795–799 (1996). ArticleCASPubMedPubMed Central Google Scholar
Cover, T. L., Puryear, W., Pérez-Pérez, G. I. & Blaser, M. J. Effect of urease on HeLa cell vacuolation induced by Helicobacter pylori cytotoxin. Infect. Immun.59, 1264–1270 (1991). CASPubMedPubMed Central Google Scholar
Papini, E. et al. Cellular vacuoles induced by Helicobacter pylori originate from late endosomal compartments. Proc. Natl Acad. Sci. USA91, 9720–9724 (1994). Demonstration that VacA-induced vacuoles arise from late endosomes. ArticleCASPubMedPubMed Central Google Scholar
Cover, T. L., Halter, S. A. & Blaser, M. J. Characterization of HeLa cell vacuoles induced by Helicobacter pylori broth culture supernatant. Hum. Pathol.23, 1004–1010 (1992). ArticleCASPubMed Google Scholar
Catrenich, C. E. & Chestnut, M. H. Character and origin of vacuoles induced in mammalian cells by the cytotoxin of Helicobacter pylori. J. Med. Microbiol.37, 389–395 (1992). ArticleCASPubMed Google Scholar
Molinari, M. et al. Vacuoles induced by Helicobacter pylori toxin contain both late endosomal and lysosomal markers. J. Biol. Chem.272, 25339–25344 (1997). ArticleCASPubMed Google Scholar
Li, Y., Wandinger-Ness, A., Goldenring, J. R. & Cover, T. L. Clustering and redistribution of late endocytic compartments in response to Helicobacter pylori vacuolating toxin. Mol. Biol. Cell15, 1946–1959 (2004). ArticleCASPubMedPubMed Central Google Scholar
Morbiato, L. et al. Vacuolation induced by VacA toxin of Helicobacter pylori requires the intracellular accumulation of membrane permeant bases, Cl− and water. FEBS Lett.508, 479–483 (2001). ArticleCASPubMed Google Scholar
Cover, T. L., Vaughn, S. G., Cao, P. & Blaser, M. J. Potentiation of Helicobacter pylori vacuolating toxin activity by nicotine and other weak bases. J. Infect. Dis.166, 1073–1078 (1992). ArticleCASPubMed Google Scholar
Satin, B. et al. 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). ArticleCASPubMed Google Scholar
Molinari, M. et al. Selective inhibition of Ii-dependent antigen presentation by Helicobacter pylori toxin VacA. J. Exp. Med.187, 135–140 (1998). Describes the inhibitory effects of VacA on antigen presentation. ArticleCASPubMedPubMed Central Google Scholar
Kimura, M. et al. Vacuolating cytotoxin purified from Helicobacter pylori causes mitochondrial damage in human gastric cells. Microb. Pathog.26, 45–52 (1999). ArticleCASPubMed Google Scholar
Galmiche, A. et al. The N-terminal 34-kDa fragment of Helicobacter pylori vacuolating cytotoxin targets mitochondria and induces cytochrome c release. EMBO. J19, 6361–6370 (2000). Identifies mitochondria as a target for VacA. ArticleCASPubMedPubMed Central Google Scholar
Willhite, D. C. & Blanke, S. R. Helicobacter pylori vacuolating cytotoxin enters cells, localizes to the mitochondria, and induces mitochondrial membrane permeability changes correlated to toxin channel activity. Cell. Microbiol.6, 143–154 (2004). ArticleCASPubMed Google Scholar
Willhite, D. C., Cover, T. L. & Blanke, S. R. 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 (2003). ArticleCASPubMed Google Scholar
Kuck, D. et al. Vacuolating cytotoxin of Helicobacter pylori induces apoptosis in the human gastric epithelial cell line AGS. Infect. Immun.69, 5080–5087 (2001). ArticleCASPubMedPubMed Central Google Scholar
Cover, T. L., Krishna, U. S., Israel, D. A. & Peek, R. M. Jr. Induction of gastric epithelial cell apoptosis by Helicobacter pylori vacuolating cytotoxin. Cancer Res.63, 951–957 (2003). CASPubMed Google Scholar
Nakayama, M. et al. Helicobacter pylori VacA activates the p38/ATF-2-mediated signal pathway in AZ-521 cells. J. Biol. Chem.279, 7024–7028 (2004). ArticleCASPubMed Google Scholar
Boncristiano, M. et al. The Helicobacter pylori vacuolating toxin inhibits T cell activation by two independent mechanisms. J. Exp. Med.198, 1887–1897 (2003). ArticleCASPubMedPubMed Central Google Scholar
de Bernard, M. et al. The Helicobacter pylori VacA cytotoxin activates RBL-2H3 cells by inducing cytosolic calcium oscillations. Cell. Microbiol.7, 191–198 (2005). ArticleCASPubMed Google Scholar
Papini, E. et al. Selective increase of the permeability of polarized epithelial cell monolayers by Helicobacter pylori vacuolating toxin. J. Clin. Invest.102, 813–820 (1998). ArticleCASPubMedPubMed Central Google Scholar
Tombola, F. et al. The Helicobacter pylori VacA toxin is a urea permease that promotes urea diffusion across epithelia. J. Clin. Invest.108, 929–937 (2001). ArticleCASPubMedPubMed Central Google Scholar
Debellis, L., Papini, E., Caroppo, R., Montecucco, C. & Curci, S. Helicobacter pylori cytotoxin VacA increases alkaline secretion in gastric epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol.281, G1440–G1448 (2001). ArticleCASPubMed Google Scholar
Guarino, A. et al. Enterotoxic effect of the vacuolating toxin produced by Helicobacter pylori in Caco-2 cells. J. Infect. Dis.178, 1373–1378 (1998). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Allen, L. A., Schlesinger, L. S. & Kang, B. Virulent strains of Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J. Exp. Med.191, 115–128 (2000). ArticleCASPubMedPubMed Central Google Scholar
Rittig, M. G. et al. _Helicobacter pylori_-induced homotypic phagosome fusion in human monocytes is independent of the bacterial vacA and cag status. Cell. Microbiol.5, 887–899 (2003). ArticleCASPubMed Google Scholar
Gebert, B., Fischer, W., Weiss, E., Hoffman, R. & Haas, R. Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science301, 1099–1102 (2003). The first description of the effects of VacA on T lymphocytes. ArticleCASPubMed Google Scholar
Sundrud, M. S., Torres, V. J., Unutmaz, D. & Cover, T. L. 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. USA101, 7727–7732 (2004). ArticleCASPubMedPubMed Central Google Scholar
Yahiro, K. et al. Protein-tyrosine phosphatase α, RPTPα, is a Helicobacter pylori VacA receptor. J. Biol. Chem.278, 19183–19189 (2003). ArticleCASPubMed Google Scholar
Moll, G. et al. Lipid interaction of the 37-kDa and 58-kDa fragments of the Helicobacter pylori cytotoxin. Eur. J. Biochem.234, 947–952 (1995). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Utt, M., Danielsson, B. & Wadstrom, T. Helicobacter pylori vacuolating cytotoxin binding to a putative cell surface receptor, heparan sulfate, studied by surface plasmon resonance. FEMS Immunol. Med. Microbiol.30, 109–113 (2001). ArticleCASPubMed Google Scholar
Massari, P. et al. Binding of the Helicobacter pylori vacuolating cytotoxin to target cells. Infect. Immun.66, 3981–3984 (1998). CASPubMedPubMed Central Google Scholar
McClain, M. S., Schraw, W., Ricci, V., Boquet, P. & Cover, T. L. Acid-activation of Helicobacter pylori vacuolating cytotoxin (VacA) results in toxin internalization by eukaryotic cells. Mol. Microbiol.37, 433–442 (2000). ArticleCASPubMed Google Scholar
Ricci, V. et al. 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. Cell11, 3897–3909 (2000). ArticleCASPubMedPubMed Central Google Scholar
Padilla, P. I. et al. 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). ArticleCASPubMed Google Scholar
Yahiro, K. et al. Essential domain of receptor tyrosine phosphatase β (RPTPβ) for interaction with Helicobacter pylori vacuolating cytotoxin. J. Biol. Chem.279, 51013–51021 (2004). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
Patel, H. K. et al. Plasma membrane cholesterol modulates cellular vacuolation induced by the Helicobacter pylori vacuolating cytotoxin. Infect. Immun.70, 4112–4123 (2002). ArticleCASPubMedPubMed Central Google Scholar
Kuo, C. H. & Wang, W. C. Binding and internalization of Helicobacter pylori VacA via cellular lipid rafts in epithelial cells. Biochem. Biophys. Res. Commun.303, 640–644 (2003). ArticleCASPubMed Google Scholar
Geisse, N. A., Cover, T. L., Henderson, R. M. & Edwardson, J. M. Targeting of Helicobacter pylori vacuolating toxin to lipid raft membrane domains analysed by atomic force microscopy. Biochem. J.381, 911–917 (2004). ArticleCASPubMedPubMed Central Google Scholar
Gauthier, N. C. et al. Glycosylphosphatidylinositol-anchored proteins and actin cytoskeleton modulate chloride transport by channels formed by the Helicobacter pylori vacuolating cytotoxin VacA in HeLa cells. J. Biol. Chem.279, 9481–9489 (2004). ArticleCASPubMed Google Scholar
Fiocca, R. et al. Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles. Uptake of released toxin and vesicles by gastric epithelium. J. Pathol.188, 220–226 (1999). ArticleCASPubMed Google Scholar
Ricci, V. et al. 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 (1997). ArticleCASPubMed Google Scholar
Tombola, F. et al. Inhibition of the vacuolating and anion channel activities of the VacA toxin of Helicobacter pylori. FEBS Lett.460, 221–225 (1999). ArticleCASPubMed Google Scholar
de Bernard, M., Moschioni, M., Napolitani, G., Rappuoli, R. & Montecucco, C. The VacA toxin of Helicobacter pylori identifies a new intermediate filament-interacting protein. EMBO J.19, 48–56 (2000). ArticleCASPubMedPubMed Central Google Scholar
Hennig, E. E., Butruk, E. & Ostrowski, J. RACK1 protein interacts with Helicobacter pylori VacA cytotoxin: the yeast two-hybrid approach. Biochem. Biophys. Res. Commun.289, 103–110 (2001). ArticleCASPubMed Google Scholar
Ricci, V. et al. Effect of Helicobacter pylori on gastric epithelial cell migration and proliferation in vitro: role of VacA and CagA. Infect. Immun.64, 2829–2833 (1996). CASPubMedPubMed Central Google Scholar
Kobayashi, H. et al. The effect of Helicobacter pylori on gastric acid secretion by isolated parietal cells from a guinea pig. Association with production of vacuolating toxin by H. pylori. Scand. J. Gastroenterol.31, 428–433 (1996). ArticleCASPubMed Google Scholar
Bantel, H. et al. α-Toxin is a mediator of _Staphylococcus aureus_-induced cell death and activates caspases via the intrinsic death pathway independently of death receptor signaling. J. Cell Biol.155, 637–648 (2001). ArticleCASPubMedPubMed Central Google Scholar
De Haan, L. & Hirst, T. R. Cholera toxin: a paradigm for multi-functional engagement of cellular mechanisms. Mol. Membr. Biol.21, 77–92 (2004). ArticleCASPubMed Google Scholar
Tamura, M., Nogimori, K., Yajima, M., Ase, K. & Ui, M. A role of the B-oligomer moiety of islet-activating protein, pertussis toxin, in development of the biological effects on intact cells. J. Biol. Chem.258, 6756–6761 (1983). CASPubMed Google Scholar
Pizza, M., Masignani, V. & Rappuoli, R. in The Comprehensive Sourcebook of Bacterial Protein Toxins Second Edition 45–72 (Academic Press, 1999). Google Scholar
Abrami, L., Fivaz, M., Glauser, P. E., Parton, R. G. & van der Goot, F. G. A pore-forming toxin interacts with a GPI-anchored protein and causes vacuolation of the endoplasmic reticulum. J. Cell Biol.140, 525–540 (1998). ArticleCASPubMedPubMed Central Google Scholar
Agrawal, A. et al. Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature424, 329–334 (2003). ArticleCASPubMed Google Scholar
Friedlander, A. M. Macrophages are sensitive to anthrax lethal toxin through an acid-dependent process. J. Biol. Chem.261, 7123–7126 (1986). CASPubMed Google Scholar
Obrig, T. G. et al. Direct cytotoxic action of Shiga toxin on human vascular endothelial cells. Infect. Immun.56, 2373–2378 (1988). CASPubMedPubMed Central Google Scholar
Tesh, V. L., Ramegowda, B. & Samuel, J. E. Purified Shiga-like toxins induce expression of proinflammatory cytokines from murine peritoneal macrophages. Infect. Immun.62, 5085–5094 (1994). CASPubMedPubMed Central Google Scholar
Ling, H. et al. Structure of the shiga-like toxin I B-pentamer complexed with an analogue of its receptor Gb3. Biochemistry37, 1777–1788 (1998). ArticleCASPubMed Google Scholar
Stein, P. E. et al. Structure of a pertussis toxin-sugar complex as a model for receptor binding. Nature Struct. Biol.1, 591–596 (1994). ArticleCASPubMed Google Scholar
Barbieri, J. T. & Sun, J. Pseudomonas aeruginosa ExoS and ExoT. Rev. Physiol. Biochem. Pharmacol.152, 79–92 (2004). ArticleCASPubMed Google Scholar
Goehring, U. M., Schmidt, G., Pederson, K. J., Aktories, K. & Barbieri, J. T. The N-terminal domain of Pseudomonas aeruginosa exoenzyme S is a GTPase-activating protein for Rho GTPases. J. Biol. Chem.274, 36369–36372 (1999). ArticleCASPubMed Google Scholar
Vincent, T. S., Fraylick, J. E., McGuffie, E. M. & Olson, J. C. ADP-ribosylation of oncogenic Ras proteins by Pseudomonas aeruginosa exoenzyme S in vivo. Mol. Microbiol.32, 1054–1064 (1999). ArticleCASPubMed Google Scholar
Hewlett, E. L., Kim, K. J., Lee, S. J. & Gray, M. C. Adenylate cyclase toxin from Bordetella pertussis: current concepts and problems in the study of toxin functions. Int. J. Med. Microbiol.290, 333–335 (2000). ArticleCASPubMed Google Scholar
Ladant, D. & Ullmann, A. Bordetella pertussis adenylate cyclase: a toxin with multiple talents. Trends Microbiol.7, 172–176 (1999). ArticleCASPubMed Google Scholar
Cover, T. L., Reddy, L. Y. & Blaser, M. J. Effects of ATPase inhibitors on the response of HeLa cells to Helicobacter pylori vacuolating toxin. Infect. Immun.61, 1427–1431 (1993). CASPubMedPubMed Central Google Scholar
Papini, E. et al. Bafilomycin A1 inhibits _Helicobacter pylori_-induced vacuolization of HeLa cells. Mol. Microbiol.7, 323–327 (1993). ArticleCASPubMed Google Scholar
Papini, E. et al. The vacuolar ATPase proton pump is present on intracellular vacuoles induced by Helicobacter pylori. J. Med. Microbiol.45, 84–89 (1996). ArticleCASPubMed Google Scholar
Papini, E. et al. The small GTP binding protein rab7 is essential for cellular vacuolation induced by Helicobacter pylori cytotoxin. EMBO J.16, 15–24 (1997). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
Suzuki, J. et al. 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). ArticleCASPubMed Google Scholar
Suzuki, J. et al. Dynamin is involved in human epithelial cell vacuolation caused by the _Helicobacter pylori_-produced cytotoxin VacA. J. Clin. Invest.107, 363–370 (2001). ArticleCASPubMedPubMed Central Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMed Google Scholar
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). ArticleCASPubMedPubMed Central Google Scholar
Amieva, M. R. et al. Disruption of the epithelial apical-junctional complex by Helicobacter pylori CagA. Science300, 1430–1434 (2003). ArticleCASPubMedPubMed Central Google Scholar
Terres, A. M. et al. Helicobacter pylori disrupts epithelial barrier function in a process inhibited by protein kinase C activators. Infect. Immun.66, 2943–2950 (1998). CASPubMedPubMed Central Google Scholar