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Staphylococcus aureus alpha-toxin-induced pores: Channel-like behavior in lipid bilayers and patch clamped cells

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Abstract

The conductance of pores induced by Staphylococcus aureus α-toxin in Lettre cells has been compared to that in bilayers composed of synthetic lipids or Lettre cell membrane constituents. Previously described characteristics of toxin-induced conductance changes in lipid bilayers, namely rectification, voltage-dependent closure, and closure at low pH or in the presence of divalent cations (Menestrina, 1986) are displayed also in bilayers prepared from Lettre cell membranes and in patch clamped Lettre cells. It is concluded that endogenous proteins do not affect the properties of α-toxininduced channels significantly and that the relative lack of ion channels in Lettre cells makes them ideal for studies of pore-forming toxins by the patch clamp technique.

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References

  • Bashford, C.L., Alder, G.M., Graham, J.M., Menestrina, G., Pasternak, C.A. 1988a. Ion modulation of membrane permeability: Effect of cations on intact cells and on cells and phospholipid bilayers treated with pore-forming agents. J. Membrane Biol., 103:79–94

    Google Scholar 

  • Bashford, C.L., Alder, G.M., Patel, K., Pasternak, C.A. 1984. Common action of certain viruses, toxins, and activated complement: pore formation and its prevention by extracellular Ca2+. Biosci. Rep. 4:797–805

    Google Scholar 

  • Bashford, C.L., Alder, G.M., Menestrina, G., Micklem, K.J., Murphy, J.J., Pasternak, C.A. 1986. Membrane damage by hemolytic viruses, toxins, complement, and other cytotoxic agents. A common mechanism blocked by divalent cations. J. Biol. Chem. 261:9300–9308

    Google Scholar 

  • Bashford, C.L., Menestrina, G., Henkart, P.A., Pasternak, C.A. 1988b. Cell damage by cytolysin. Spontaneous recovery and reversible inhibition by divalent cations. J. Immunol. 141:3965–3974

    Google Scholar 

  • Bashford, C.L., Micklem, K.J., Pasternak, C.A. 1985. Sequential onset of permeability changes in mouse ascites cells induced by Sendai virus. Biochim. Biophys. Acta 814:247–255

    Google Scholar 

  • Bashford, C.L., Pasternak, C.A. 1984. Plasma membrane potential of Lettre cells does not depend on cation gradients but on pumps. J. Membrane Biol. 79:275–284

    Google Scholar 

  • Bashford, C.L., Pasternak, C.A. 1990. Setting of membrane potential. In: Monovalent Cations in Biological Systems. C.A. Pasternak, ed. pp. 171–186. CRC, Boca Raton, Florida

    Google Scholar 

  • Benham, C.D., Bolton, T.B., Lang, R.J., Takewaki, T. 1986. Calciumactivated potassium channels in single smooth muscle cells of rabbit jejunum and guinea-pig mesenteric artery. J. Physiol. 371:45–67

    Google Scholar 

  • Bhakdi, S., Tranum-Jensen, J. 1987. Damage to mammalian cells by proteins that form transmembrane pores. Rev. Physiol. Biochem. Pharmacol. 107:147–223

    Google Scholar 

  • Bhakdi, S., Tranum-Jensen, J. 1991. Alpha-toxin of Staphylococcus aureus. Microbiol. Rev. 55:733–751

    Google Scholar 

  • Bussey, H. 1991. K1 killer toxin, a pore-forming protein from yeast. Mol. Microbiol. 5:2339–2343

    Google Scholar 

  • Easmon, C.S.F., Adlam, C. 1983. Staphylococci and Staphylococcal Infections, vols. 1 and 2. Academic, London

    Google Scholar 

  • Forti, S., Menestrina, G. 1989. Staphylococcal alpha-toxin increases the permeability of lipid vesicles by cholesterol- and pH-dependent assembly of oligomeric channels. Eur. J. Biochem. 181:767–773

    Google Scholar 

  • Gitler, C., Calef, E., Rosenberg, I. 1984. Cytopathogenicity of Entamoeba histolytica. Philos. Trans. R. Soc. Lond. B 307:73–85

    Google Scholar 

  • Graham, J.M., Coffey, K.H.M. 1979. Tissue-culture cell fractionation. Fractionation of cellular membranes from 125I/lactoperoxidaselabelled Lettre cells homogenized by bicarbonate-induced lysis: Resolution of membranes by zonal centrifugation and in sucrose and metrizamide gradients. Biochem. J. 182:173–180

    Google Scholar 

  • Impraim, C.C., Foster, K.A., Micklem, K.J., Pasternak, C.A. 1980. Nature of virally mediated changes in membrane permeability to small molecules. Biochem. J. 186:847–860

    Google Scholar 

  • Jeljaszewicz, C., Wadstrom, T. 1978. Bacterial Toxins and Cell Membranes. Academic, New York

    Google Scholar 

  • Kasianowicz, J.J., Moore, C.R., Zimmerberg, J., Pasternak, C., Bashford, C.L., Parsegian, V.A. 1991. Two-sided protonation of the alpha toxin channel inferred from the effects of transmembrane pH gradients. Biophys. J. 59:458a (Abstr.)

    Google Scholar 

  • Kerry, C.J., Kits, K.S., Ramsey, R.L., Sansom, M.S., Usherwood, P.N. 1987. Single channel kinetics of a glutamate receptor. Biophys. J. 51:137–144

    Google Scholar 

  • Krasilnikov, O.V., Sabirov, R.Z. 1989. Ion transport through channels formed in lipid bilayers by Staphylococcus aureus alpha-toxin. Gen. Physiol. Biophys. 8:213–222

    Google Scholar 

  • Krasilnikov, O.V., Sabirov, R.Z., Ternovsky, V.I., Merzliak, P.G., Tashmukhamedov, B.A. 1988. The structure of Staphylococcus aureus alpha-toxin-induced ionic channels. Gen. Physiol. Biophys. 7:467–473

    Google Scholar 

  • Krasilnikov, O.V., Sabirov, R.Z., Ternovsky, V.I., Merzliak, P.G., Muratkhodjaev, J.N. 1992. A simple method for the determination of the pore radius of ion channels in planar lipid bilayer membranes. FEMS Microbiol. Immunol. 5:93–100

    Google Scholar 

  • Lettre, R., Paweletz, N., Werner, D., Granzow, C. 1972. Sublines of the Ehrlich-Lettre mouse ascites tumour. A new tool for experimental cell research. Naturwissenschaften 59:59–63

    Google Scholar 

  • Menestrina, G. 1986. Ionic channels formed by Staphylococcus aureus alpha-toxin: Voltage-dependent inhibition by divalent and trivalent cations. J. Membrane Biol. 90:177–190

    Google Scholar 

  • Menestrina, G., Bashford, C.L., Pasternak, C.A. 1990. Pore-forming toxins: experiments with S. aureus alpha-toxin, C. perfringens theta-toxin and E. coli haemolysin in lipid bilayers, liposomes and intact cells. Toxicon 28:477–491

    Google Scholar 

  • Micklem, K.J., Alder, G.M., Buckley, C.D., Murphy, J., Pasternak, C.A. 1988. Protection against complement-mediated cell damage by Ca2+ and Zn2+. Complement 5:141–152

    Google Scholar 

  • Micklem, K.J., Nyaruwe, A., Pasternak, C.A. 1985. Permeability changes resulting from virus-cell fusion: temperature-dependence of the contributing processes. Mol. Cell. Biochem. 66:163–173

    Google Scholar 

  • Montal, M., Müller, P. 1972. Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. Proc. Natl. Acad. Sci. USA 69:3561–3566

    Google Scholar 

  • Morgan, B.P., Dankert, J.R., Esser, A.F. 1987. Recovery of human neutrophils from complement attack: Removal of the membrane attack complex by endocytosis and exocytosis. J. Immunol. 138:246–253

    Google Scholar 

  • Pasternak, C.A. 1986. Effect of pore formers on intracellular calcium. Cell Calcium 7:387–397

    Google Scholar 

  • Pasternak, C.A., Alder, G.M., Bashford, C.L., Korchev, Y.E., Pederzolli, C., Rostovtseva, T.K. 1992. Membrane damage: common mechanisms of induction and prevention. FEMS Microbiol. Immunol. 105:83–92

    Google Scholar 

  • Pasternak, C.A., Bashford, C.L., Menestrina, G. 1989. Mechanisms of attack and defence at the cell surface: the use of phospholipid bilayers as models for cell membrane. Biosci. Rep. 9:503–507

    Google Scholar 

  • Pershadsingh, H.A., Johnstone, R.M., Laris, P.C. 1978. Influence of (DL)-propranolol and Ca2+ on membrane potential and amino acid transport in Ehrlich ascites tumor cells. Biochim. Biophys. Acta 509:360–373

    Google Scholar 

  • Ramm, L.E., Whitlow, M.B., Koski, C.L., Shin, M.L., Mayer, M.M. 1983. Elimination of complement channels from the plasma membranes of U937, a nucleated mammalian cell line: temperature dependence of the elimination rate. J. Immunol. 131:1411–1415

    Google Scholar 

  • Reichwein, J., Hugo, F., Roth, M., Sinner, A., Bhakdi, S. 1987. Quantitative analysis of the binding and oligomerization of staphylococcal alpha-toxin in target erythrocyte membranes. Infect. Immun. 55:2940–2944

    Google Scholar 

  • Schein, S.J., Kagan, B.L., Finkelstein, A. 1978. Colicin K acts by forming voltage-dependent channels in phospholipid bilayer membranes. Nature 276:159–163

    Google Scholar 

  • Schindler, H. 1980. Formation of planar bilayer from artificial or native membrane vesicles. FEBS Lett. 122:77–79

    Google Scholar 

  • Stein, W.D., Lieb, W.R. 1986. Transport and Diffusion Across Cell Membranes. Academic, London

    Google Scholar 

  • Suttorp, N., Seeger, W., Dewein, E., Bhakdi, S., Roka, L. 1985. Staphylococcal alpha-toxin-induced PGI2 production in endothelial cells: role of calcium. Am. J. Physiol. 248:C127-C134

    Google Scholar 

  • Thelestam, M., Mollby, R. 1980. Interaction of streptolysin O from Streptococcus pyogenes and theta-toxin from Clostridium perfringens with human fibroblasts. Infect. Immun. 29:863–872

    Google Scholar 

  • Thelestam, M. 1983. Membrane damage by staphylococcal alpha-toxin to different types of cultured mammalian cell. Biochim. Biohys. Acta 762:481–488

    Google Scholar 

  • Thelestam, M., Blomqvist, L. 1988. Staphylococcal alpha toxin—recent advances. Toxicon 26:55–65

    Google Scholar 

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Dr. Sviderskaya is on leave of absence from the Physiology Institute, University of St. Petersburg, Russia

We are grateful to Dr. J.P. Arbuthnott and Dr. K. Hungerer for gifts of S. aureus α-toxin, to Dr. T.B. Bolton for collaboration with patch clamped cells and to Dr. J.M. Graham for help with the preparation of Lettre cell plasma membranes. This study was supported by the Cell Surface Research Fund, Medical Research Council, Science and Engineering Research Council, UNESCO (Molecular and Cell Biology Network) and The Wellcome Trust.

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Korchev, Y.E., Alder, G.M., Bakhramov, A. et al. Staphylococcus aureus alpha-toxin-induced pores: Channel-like behavior in lipid bilayers and patch clamped cells. J. Membarin Biol. 143, 143–151 (1995). https://doi.org/10.1007/BF00234660

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  • DOI: https://doi.org/10.1007/BF00234660

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