Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin

Journal of Cell Biology

Volumn 147, Issue 1, 1999, Pages 175-184

  Abrami, Laurence ^a   Van Der Goot, F Gisou ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Sciences II   (Switzerland)

Author keywords

Aerolysin; Cholesterol; Glycosyl phosphatidylinositol anchored protein; Microdomains; Oligomerization

Indexed keywords

AEROLYSIN; PROTOXIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; HAMSTER; INTOXICATION; NONHUMAN; OLIGOMERIZATION; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING; TARGET CELL;

ANIMALS; BACTERIAL TOXINS; BETA-CYCLODEXTRINS; CELL LINE; CELL MEMBRANE; CHOLESTEROL; CRICETINAE; CYCLODEXTRINS; DOSE-RESPONSE RELATIONSHIP, DRUG; GLYCOSPHINGOLIPIDS; GLYCOSYLPHOSPHATIDYLINOSITOLS; KINETICS; OCTOXYNOL; POLYMERS; PORE FORMING CYTOTOXIC PROTEINS; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTORS, CELL SURFACE; SAPONINS; SOLUBILITY; TEMPERATURE;

ANIMALIA; BACTERIA (MICROORGANISMS); CRICETINAE;

EID: 0033523767     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.147.1.175     Document Type: Article

References (70)

1. Abrami, L., M. Fivaz, E. Decroly, N.G. Seidah, J. François, G. Thomas, S. Leppla, J.T. Buckley, and F.G. van der Goot. 1998a. The pore-forming toxin proaerolysin is processed by furin. J. Biol. Chem. 273:32656-32661.
2. Abrami, L., M. Fivaz, P.-E. Glauser, R.G. Parton, and F.G. van der Goot. 1998b. A pore-forming toxin interacts with a GPI-anchored protein and causes vacuolation of the endoplasmic reticulum. J. Cell Biol. 140:525-540.
3. Adam, G., and M. Delbrück. 1968. Structural Chemistry and Molecular Biology. A. Rich and N. Davidson, editors. W.H. Freeman & Co., NY.
4. Bhakdi, S., H. Bayley, A. Valeva, I. Walev, B. Walker, M. Kehoe, and M. Palmer. 1996. Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch. Microbiol. 165:73-79.
5. Bray, D., M.D. Levin, and C.J. Morton-Firth. 1998. Receptor clustering as a cellular mechanism to control sensitivity. Nature. 393:85-88.
6. Brown, D.A., and J.K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:533-544.
7. Brown, D.A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111-136.
8. Brown, R.E. 1998. Sphingolipid organization: what physical studies of model membranes reveal. J. Cell Sci. 111:1-9.
9. Buckley, J.T. 1990. Purification of cloned proaerolysin released by a low protease mutant of Aeromonas salmonicida. Biochem. Cell Biol. 68:221-224.
10. Cerneus, D.P., E. Ueffing, G. Posthuma, G.J. Strous, and A. van der Ende. 1993. Detergent insolubility of alkaline phosphatase during biosynthetic transport and endocytosis. Role of cholesterol. J. Biol. Chem. 268:3150-3155.
11. Chong, P.L. 1994. Evidence for regular distribution of sterols in liquid crystalline phosphatidylcholine bilayers. Proc. Natl. Acad. Sci. USA. 91:10069-10073.
12. Cowell, S., W. Aschauer, H.J. Gruber, K.L. Nelson, and J.T. Buckley. 1997. The erythrocyte receptor for the channel-forming toxin aerolysin is a novel glycosylphosphatidylinositol-anchored protein. Mol. Microbiol. 25:343-350.
13. Cruzeiro-Hansson, L., J.H. Ipsen, and O.G. Mouritsen. 1989. Intrinsic molecules in lipid membranes change the lipid-domain interfacial area: cholesterol at domain interfaces. Biochim. Biophys. Acta. 979:166-176.
14. Daily, O.P., S.W. Joseph, J.C. Coolbaugh, R.I. Walker, B.R. Merrell, D.M. Rollins, R.J. Seidler, R.R. Colwell, and C.R. Lissner. 1981. Association of Aeromonas sobria with human infection. J. Clin. Microbiol. 13:769-777.
15. Diep, D.B., K.L. Nelson, S.M. Raja, R.W. McMaster, and J.T. Buckley. 1998. Glycosylphosphatidylinositol anchors of membrane glycoproteins are binding determinants for the channel-forming toxin aerolysin. J. Biol. Chem. 273: 2355-2360.
16. Donta, S.T., and A.P. Haddow. 1978. Cytotoxic activity of Aeromonas hydrophila. Infec. Immun. 21:989-993.
17. Edidin, M. 1997. Lipid microdomains in cell surface membranes. Curr. Opin. Struct. Biol. 7:528-532.
18. Elias, P.M., J. Goerke, D.S. Friend, and B.E. Brown. 1978. Freeze-fracture identification of sterol-digitonin complexes in cell and liposome membranes. J. Cell Biol. 78:577-596.
19. Fivaz, M., L. Abrami, and F.G. van der Goot. 1999. Landing on lipid rafts. Trends Cell Biol. 9:212-213.
20. Fra, A.M., E. Williamson, K. Simons, and R.G. Parton. 1994. Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. J. Biol. Chem. 269:30745-30748.
21. Friedrichson, T., and T.V. Kurzchalia. 1998. Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature. 394:802-805.
22. Gil, T., J.H. Ipsen, O.G. Mouritsen, M.C. Sabra, M.M. Sperotto, and M.J. Zuckermann. 1998. Theoretical analysis of protein organization in lipid membranes. Biochim. Biophys. Acta. 1376:245-266.
23. Gruber, H.J., H.U. Wilmsen, S. Cowell, H. Schindler, and J.T. Buckley. 1994. Partial purification of the rat erythrocyte receptor for the channel-forming toxin aerolysin and reconstitution into planar lipid bilayers. Mol. Microbiol. 14:1093-1101.
24. Gruenberg, J., and K.E. Howell. 1989. Membrane traffic in endocytosis: insights from cell-free assays. Annu. Rev. Cell Biol. 5:453-481.
25. Hanada, K., K. Izawa, M. Nishijima, and Y. Akamatsu. 1993. Sphingolipid deficiency induces hypersensitivity of CD14, a glycosyl phosphatidylinositol-anchored protein, to phosphatidylinositol-specific phospholipase C. J. Biol. Chem. 268:13820-13823.
26. Hanada, K., M. Nishijima, Y. Akamatsu, and R.E. Pagano. 1995. Both sphingolipids and cholesterol participate in the detergent insolubility of alkaline phosphatase, a glycosylphosphatidylinositol-anchored protein, in mammalian membranes. J. Biol. Chem. 270:6254-6260.
27. Hannan, L.A., M.P. Lisanti, B.E. Rodriguez, and M. Edidin. 1993. Correctly sorted molecules of a GPI-anchored protein are clustered and immobile when they arrive at the apical surface of MDCK cells. J. Cell Biol. 120:353-358.
28. Harder, T., and K. Simons. 1997. Caveolae, DIGs, and the dynamics of shingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9:534-542.
29. Harder, T., P. Scheiffele, P. Verkade, and K. Simons. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:929-942.
30. Hooper, N.M. 1998. Membrane biology: do glycolipid microdomains really exist? Curr. Biol. 8:R114-R116.
31. Howard, S.P., and J.T. Buckley. 1985. Activation of the hole forming toxin aerolysin by extracellular processing. J. Bacteriol. 163:336-340.
32. Ilangumaran, S., and D.C. Hoessli. 1998. Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane. Biochem. J. 335:433-440.
33. Jacobs, T., A. Darji, N. Frahm, M. Ronde, J. Wehland, T. Chakraborty, and S. Weiss. 1998. Listeriolysin O: cholesterol inhibits cytolysis but not binding to cellular membranes. Mol. Microbiol. 28:1081-1089.
34. Jacobson, K., and C. Dietrich. 1999. Looking at lipid rafts? Trends Cell Biol. 9:87-91.
35. Janda, J.M., D.J. Bottone, C.V. Sinner, and D. Calcaterra. 1984. Phenotype markers associated with gastrointestinal Aeromonas hydrophila isolates from symptomatic children. J. Clin. Microbiol. 17:588-591.
36. Jones, D.R., and I. Varela-Nieto. 1998. The role of glycosyl-phosphatidylinositol in signal transduction. Int. J. Biochem. Cell Biol. 30:313-326.
37. Kaper, J.B., H. Lockman, and R.R. Colwell. 1981. Aeromonas hydrophila: ecology and toxigenicity of isolates from an estuary. J. Appl. Bacteriol. 50:359-377.
38. Kenworthy, A.K., and M. Edidin. 1998. Distribution of a glycosylphosphatidylinositol-anchored protein at the apical surface of MDCK cells examined at a resolution of 100 Å using imaging fluorescence resonance energy transfer. J. Cell Biol. 142:69-84.
39. Kilsdonk, E.P., P.G. Yancey, G.W. Stoudt, F.W. Bangerter, W.J. Johnson, M.C. Phillips, and G.H. Rothblat. 1995. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 270:17250-17256.
40. Kinoshita, T., K. Ohishi, and J. Takeda. 1997. GPI-anchor synthesis in mammalian cells: genes, their products, and a deficiency. J. Biochem. 122:251-257.
41. 2+ release from intracellular stores in human granulocytes. J. Biol. Chem. 273:18122-18129.
42. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
43. Lange, S., F. Nussler, E. Kauschke, G. Lutsch, E.L. Cooper, and A. Herrmann. 1997. Interaction of earthworm hemolysin with lipid membranes requires sphingolipids. J. Biol. Chem. 272:20884-20892.
44. Lesieur, C., B. Vecsey-Semjn, L. Abrami, M. Fivaz, and F.G. van der Goot. 1997. Membrane insertion: the strategy of toxins. Mol. Memb. Biol. 14:45-64.
45. McLaughlin, S., and A. Aderem. 1995. The myristoyl-electrostatic switch: a modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20:272-276.
46. Molloy, S.S., E.D. Anderson, F. Jean, and G. Thomas. 1999. Bi-cycling the furin pathway: from TGN localization to pathogen activation and embryogenesis. Trends Cell Biol. 9:28-35.
47. Moniatte, M., F.G. van der Goot, J.T. Buckley, F. Pattus, and A. Van Dorsselaer. 1996. Characterization of the heptameric pore-forming complex of the Aeromonas toxin aerolysin using MALDI-TOF mass spectrometry. FEBS Lett. 384:269-272.
48. Nelson, K.L., S.M. Raja, and J.T. Buckley. 1997. The GPI-anchored surface glycoprotein Thy-1 is a receptor for the channel-forming toxin aerolysin. J. Biol. Chem. 272:12170-12174.
49. Neufeld, E.B., A.M. Cooney, J. Pitha, E.A. Dawidowicz, N.K. Dwyer, P.G. Pentchev, and E.J. Blanchette-Mackie. 1996. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem. 271:21604-21613.
50. Parker, M.W., F.G. van der Goot, and J.T. Buckley. 1996. Aerolysin: the ins and outs of a channel forming toxin. Mol. Microbiol. 19:205-212.
51. Parton, R.G., and K. Simons. 1995. Digging into caveolae. Science. 269:1398-1399.
52. Peitsch, M., and J. Tschopp. 1991. Assembly of the macromolecular pores by immune defense systems. Curr. Opin. Cell Biol. 3:710-716.
53. Rietveld, A., and K. Simons. 1998. The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim. Biophys. Acta. 1376:467-479.
54. Rossjohn, J., S.C. Feil, W.J. Mckinstry, F.G. van der Goot, J.T. Buckley, and M.W. Parker. 1998. Aerolysin: a paradigm for membrane insertion of beta-sheet protein toxins. J. Struct. Biol. 121:92-100.
55. Scheiffele, P., M.G. Roth, and K. Simons. 1997. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO (Eur. Mol. Biol. Organ.) J. 16:5501-5508.
56. Schroeder, R.J., S.N. Ahmed, Y. Zhu, E. London, and D.A. Brown. 1998. Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. J. Biol. Chem. 273:1150-1157.
57. Seidah, N.G., and M. Chretien. 1997. Eukaryotic protein processing: endoproteolysis of precursor proteins. Curr. Opin. Biotechnol. 8:602-607.
58. Sheets, E.D., G.M. Lee, R. Simson, and K. Jacobson. 1997. Transient confinement of a glycosylphosphatidylinositol-anchored protein in the plasma membrane. Biochemistry. 36:12449-12458.
59. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
60. Tweten, R.K. 1995. Pore-forming toxins of Gram-positive bacteria. In Virulence Mechanisms of Bacterial Pathogens. J.A. Roth, C.A. Bolin, K.A. Brogden, C. Minion, and M.J. Wannemuehler, editors. American Society of Microbiology, Washington, D.C. 207-229.
61. van der Goot, F.G., J.H. Lakey, F. Pattus, C.M. Kay. O. Sorokine, A. Van Dorsselaer, and T. Buckley. 1992. Spectroscopic study of the activation and oligomerization of the channel-forming toxin aerolysin: identification of the site of proteolytic activation. Biochemistry. 31:8566-8570.
62. van der Goot, F.G., J. Ausio, K.R. Wong, F. Pattus, and J.T. Buckley. 1993a. Dimerization stabilizes the pore-forming toxin aerolysin in solution. J. Biol. Chem. 268:18272-18279.
63. van der Goot, F.G., K.R. Wong, F. Pattus, and J.T. Buckley. 1993b. Oligomerization of the channel-forming toxin aerolysin precedes its insertion into lipid bilayer. Biochemistry. 32:2636-2642.
64. van der Goot, F.G., F. Pattus, and J.T. Buckley. 1994a. The pore-forming toxin aerolysin: from the soluble form to the transmembrane channel. In Structure, Biogenesis and Dynamics of Biological Membranes. Vol. 82. J. Op den Kamp, editor. Springer-Verlag, Berlin, Heidelberg. 181-190.
65. van der Goot, F.G., K.R. Hardie, M.W. Parker, and J.T. Buckley. 1994b. The C-terminal peptide produced upon proteolytic activation of the cytolytic toxin aerolysin is not involved in channel formation. J. Biol. Chem. 269: 30496-30501.
66. Varma, R., and S. Mayor. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature. 394:798-801.
67. Wilmsen, H.U., K.R. Leonard, W. Tichelaar, J.T. Buckley, and F. Pattus. 1992. The aerolysin membrane channel is formed by heptamerization of the monomer. EMBO (Eur. Mol. Biol. Organ.) J. 11:2457-2463.
68. Yamaji, A., Y. Sekizawa, K. Emoto, H. Sakuraba, K. Inoue, H. Kobayashi, and M. Umeda. 1998. Lysenin, a novel sphingomyelin-specific binding protein. J. Biol. Chem. 273:5300-5306.
69. Zhang, F., B. Crise, B. Su, Y. Hou, J.K. Rose, A. Bothwell, and K. Jacobson. 1992. The lateral mobility of some membrane proteins is determined by their ectodomains. Biophys. J. 62:92-94.
70. Zitzer, A., O. Zitzer, S. Bhakdi, and M. Palmer. 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.