Targeting of Helicobacter pylori vacuolating toxin to lipid raft membrane domains analysed by atomic force microscopy

Biochemical Journal

Volumn 381, Issue 3, 2004, Pages 911-917

  Geisse, Nicholas A ^a   Cover, Timothy L ^b   Henderson, Robert M ^a   Edwardson, J Michael ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atomic force microscopy; Helicobacter pylori; Lipid bilayer; Lipid raft; VacA; Vacuolating toxin

Indexed keywords

ATOMIC FORCE MICROSCOPY; BIOLOGICAL MEMBRANES; BRAIN; CELL MEMBRANES; CHOLESTEROL; LIPIDS; TOXIC MATERIALS;

APOPTOSIS; BILAYERS; OLIGOMERIC COMPLEXES; PLASMA MEMBRANES;

BACTERIA;

BACTERIAL TOXIN; CHOLESTEROL; DIOLEOYLPHOSPHATIDYLCHOLINE; MEMBRANE LIPID; OLIGOMER; PHOSPHATIDYLSERINE; PHOSPHOLIPID; SPHINGOMYELIN; VACUOLATING TOXIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; BRAIN; CELL MEMBRANE; HELICOBACTER PYLORI; LIPID ANALYSIS; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ANALYSIS; TOXIN SYNTHESIS;

BACTERIAL PROTEINS; CHOLESTEROL; HYDROGEN-ION CONCENTRATION; LIPID BILAYERS; LIPOSOMES; MEMBRANE MICRODOMAINS; MICROSCOPY, ATOMIC FORCE; PHOSPHATIDYLCHOLINES; POLYMERS; SPHINGOMYELINS;

BACTERIA (MICROORGANISMS); HELICOBACTER; HELICOBACTER PYLORI; MAMMALIA;

EID: 4344690860     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031719     Document Type: Article

References (45)

1. Cover, T. L., Berg, D. E., Blaser, M. J. and Mobley, H. L. T. (2001) Helicobacter pylori pathogenesis. In Principles of Bacterial Pathogenesis (Groisman, E. A., ed.), pp. 510-558, Academic Press, San Diego, CA
2. Dunn, B. E., Cohen, H. and Blaser, M. J. (1997) Helicobacter pylori. Clin. Microbiol. Rev. 10, 720-741
3. Atherton, J. C., Cover, T. L., Papini, E. and Telford, J. L. (2001) Vacillating cytotoxin. In Helicobacter pylori: Physiology and Genetics (Mobley, H. L. T., Mendz, G. L. and Hazell, S. L., eds.), pp. 97-110, ASM Press, Washington, DC
4. Montecucco, C., Papini, E., de Bernard, M., Telford, J. L. and Rappuoli, R. (1999) Helicobacter pylori vacuolating cytotoxin and associated pathogenic factors. In The Comprehensive Sourcebook of Bacterial Protein Toxins (Alouf, J. E. and Freer, J. H., eds.), pp. 264-286, Academic Press, San Diego, CA
5. Papini, E., Zoratti, M. and Cover, T. L. (2001) In search of the Helicobacter pylori VacA mechanism of action. Toxicon 39, 1757-1767
6. Molinari, M., Salio, M., Galli, C., Norais, N., Rappuoli, R., Lanzavecchia, A. and Montecucco, C. (1998) Selective inhibition of li-dependent antigen presentation by Helicobacter pylori toxin VacA. J. Exp. Med. 187, 135-140
7. Gebert, B., Fischer, W., Weiss, E., Hoffman, R. and Haas, R. (2003) Helicobacter pylori vacuolating cytotoxin inhibits T lymphocyte activation. Science 301, 1099-1102
8. Nguyen, V. Q., Caprioli, R. M. and Cover, T. L. (2001) Carboxy-terminal proteolytic processing of Helicobacter pylori vacuolating toxin. Infect. Immun. 69, 543-546
9. 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
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. Lupetti, P., Heuser, J. E., Manetti, R., Massari, P., Lanzavecchia, S., Bellon, P. L., Dallai, R., Rappuoli, R. and Telford, J. L. (1996) Oligomeric and subunit structure of the Helicobacter pylori vacuolating cytotoxin. J. Cell Biol. 133, 801-807
12. McClain, M. S., Schraw, W., Ricci, V., Boquet, P. and Cover, T. L. (2000) Acid activation of Helicobacter pylori vacuolating cytotoxin (VacA) results in toxin internalization by eukaryotic cells. Mol. Microbiol. 37, 433-442
13. de Bernard, M., Papini, E., de Filippis, V., Gottardi, E., Telford, J., Manetti, R., Fontana, A., Rappuoli, R. and Montecucco, C. (1995) Low pH activates the vacuolating toxin of Helicobacter pylori, which becomes acid and pepsin resistant. J. Biol. Chem. 270, 23937-23940
14. Yahiro, K., Niidome, T., Kimura, M., Hatakeyama, T., Aoyagi, H., Kurazano, H., Imagawa, K., Wada, A., Moss, J. and Hirayama, T. (1999) 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
15. 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. Commun. 248, 334-340
16. 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. U.S.A. 96, 2001-2006
17. Brown, D. A. and Rose, J. K. (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical surface. Cell (Cambridge, Mass.) 68, 533-544
18. Brown, D. A. and London, E. (2000) Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 275, 17221-17224
19. Simons, K. and Toomre, D. (2000) Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31-39
20. Sprong, H., van der Sluijs, P. and van Meer, G. (2001) How proteins move lipids and lipids move proteins. Nat. Rev. Mol. Cell Biol. 2, 504-513
21. Chamberlain, L. H., Burgoyne, R. D. and Gould, G. W. (2002) SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc. Natl. Acad. Sci. U.S.A. 98, 5619-5624
22. Lang, T., Bruns, D., Wenzel, D., Riedel, D., Holroyd, P., Thiele, C. and Jahn, R. (2002) SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20, 2202-2213
23. Nichols, B. J. and Lippincott-Schwartz, J. (2001) Endocytosis without clathrin coats. Trends Cell. Biol. 11, 406-412
24. van der Goot, F. G. and Harder, T. (2001) Raft membrane domains: from a liquid-ordered membrane phase to a site of pathogen attack. Semin. Immunol. 13, 89-97
25. Waheed, A. A., Shimada, Y., Heijnen, H. F. G., Nakamura, M., Inomata, M., Hayashi, M., Iwashita, S., Slot, J. W. and Ohno-Iwashita, Y. (2001) Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). Proc. Natl. Acad. Sci. U.S.A. 98, 4926-4931
26. Yamaji-Hasegawa, A., Makino, A., Baba, T., Senoh, Y., Kimura-Suda, H., Sato, S. B., Terada, N., Ohno, S., Kiyokawa, E., Umeda, M. et al. (2003) Oligomerization and pore formation of a sphingomyelin-specific toxin, lysenin. J. Biol. Chem. 278, 22762-22770
27. Zitzer, A., Zitzer, O., Bhakdi, S. and Palmer, M. (1999) Oligomerization of Vibrio cholerae cytolysin yields a pentameric pore and has a dual specificity for cholesterol and sphingolipids in the target membrane. J. Biol. Chem. 274, 1375-1380
28. Abrami, L. and van der Goot, F. G. (1999) Plasma membrane microdomains act as concentration platforms to facilitate intoxication byaerolysin. J. Cell Biol. 147, 175-184
29. Orlandi, P. A. and Fishman, P. H. (1998) Filipin-dependent inhibition of cholera toxin: evidence for toxin internalization and activation through caveolae-like domains. J. Cell Biol. 141, 905-915
30. Wolf, A. A., Jobling, M. G., Wimer-Mackin, S., Fergsuon-Maltzman, M., Madara, J. L., Holmes, R. K. and Lencer, W. I. (1998) Ganglioside structure dictates signal transduction by cholera toxin and association with caveolae-like membrane domains in polarized epithelia. J. Cell Biol. 141, 917-927
31. Schraw, W., Li, Y., McClain, M. S., van der Groot, F. G. and Cover, T. L. (2002) Association of Helicobacter pylori vacuolating toxin (VacA) with lipid rafts. J. Biol. Chem. 277, 34642-34650
32. Kuo, C.-H. and Wang, W.-C. (2003) Binding and internalization of Helicobacter pylori VacA via cellular lipid rafts in epithelial cells. Biochem. Biophys. Res. Commun. 303, 640-644
33. Patel, H. K., Willhite, D. C., Patel, R. M., Ye, D., Williams, C. L., Torres, E. M., Marty, K. B., MacDonald, R. A. and Blanke, S. R. (2002) Plasma membrane cholesterol modulates cellular vacuolation induced by the Helicobacter pylori vacuolating cytotoxin. Infect. Immun. 70, 4112-4123
34. Ricci, V., Galmiche, A., Doye, A., Necchi, V., Solcia, E. and Boquet, P. (2000) 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
35. Saslowsky, D. E., Lawrence, J., Ren, X., Brown, D. A., Henderson, R. M. and Edwardson, J. M. (2002) Placental alkaline phosphatase is efficiently targeted to rafts in supported lipid bilayers. J. Biol. Chem. 277, 26966-26970
36. Lawrence, J. C., Saslowsky, D. E., Edwardson, J. M. and Henderson, R. M. (2003) Real-time analysis of the effects of cholesterol on lipid raft behavior using atomic force microscopy. Biophys. J. 84, 1827-1832
37. Saslowsky, D. E., Lawrence, J. C., Henderson, R. M. and Edwardson, J. M. (2003) Syntaxin is efficiently excluded from sphingomyelin-enriched domains in supported lipid bilayers containing cholesterol. J. Membr. Biol. 194, 153-164
38. Milhiet, P. E., Domec, C., Giocondi, M. C., Van Mau, N., Hertz, F. and Le Grimellec, C. (2001) Domain formation in models of the renal brush border membrane outer leaflet. Biophys. J. 81, 547-555
39. Milhiet, P. E., Giocondi, M. C., Baghdadi, O., Ronzon, F., Roux, B. and Le Grimellec, C. (2002) Spontaneous insertion and partitioning of alkaline phosphatase into model lipid rafts. EMBO Rep. 3, 485-490
40. Milhiet, P. E., Giocondi, M.-C. and Le Grimellec, C. (2002) Cholesterol is not crucial for the existence of microdomains in kidney brush border membrane models. J. Biol. Chem. 277, 875-878
41. Rinia, H. A., Snel, M. M. E., van der Eerden, J. P. J. M. and de Kruijff, B. (2001) Visualising detergent resistant domains in model membranes with atomic force microscopy. FEBS Lett. 501, 92-96
42. Hodel, A., An, S. J., Hansen, N. J., Lawrence, J., Wäsle, B., Schrader, M. and Edwardson, J. M. (2001) Cholesterol-dependent interaction of syncollin with the membrane of the pancreatic zymogen granule. Biochem. J. 356, 843-550
43. Schneider, S. W., Lärmer, J., Henderson, R. M. and Oberleithner, H. (1998) Molecular weights of individual proteins correlate with molecular volumes measured by atomic force microscopy. Pflugers Arch. 435, 362-367
44. Devaux, P. F. (1991) Static and dynamic lipid asymmetry in cell membranes. Biochemistry 30, 1163-1173
45. Willhite, D. C. and Blanke, S. R. (2004) 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