Assembly mechanism of the oligomeric streptolysin O pore: The early membrane lesion is lined by a free edge of the lipid membrane and is extended gradually during oligomerization

EMBO Journal

Volumn 17, Issue 6, 1998, Pages 1598-1605

  Palmer, Michael ^a   Harris, Robin ^a   Freytag, Claudia ^b,d   Kehoe, Michael ^b,d   Tranum Jensen, Joørgen ^c   Bhakdi, Sucharit ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Pore forming toxins; Protein oligomerization; Streptolysin O; Thiol activated toxins

Indexed keywords

CALCEIN; CYSTEINE; DEXTRAN; SODIUM CHLORIDE; STREPTOLYSIN O; SULFONIC ACID DERIVATIVE;

ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; LIPID MEMBRANE; MEMBRANE BINDING; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY;

ANIMALS; BACTERIAL PROTEINS; CELL MEMBRANE PERMEABILITY; COMPLEMENT HEMOLYTIC ACTIVITY ASSAY; CYSTEINE; ERYTHROCYTE MEMBRANE; MEMBRANE LIPIDS; MUTATION; NAPHTHALENESULFONATES; PROTEIN CONFORMATION; RABBITS; STREPTOLYSINS;

BACTERIA (MICROORGANISMS);

EID: 0032536856     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.6.1598     Document Type: Article

References (27)

1. Aktories, K. and Wegner, A. (1992) Mechanisms of the cytopathic action of actin-ADP-ribosylating toxins. Mol. Microbiol. 6, 2905-2908.
2. Alouf, J.E. and Geoffroy, C. (1991) The family of antigenically related, cholesterol-binding ('sulphhydryl-activated') cytolytic toxins. In Alouf, J.E. and Freer, J.H. (eds), Sourcebook of Bacterial Protein Toxins. Academic Press, London, pp. 147-186.
3. Bhakdi, S. and Tranum Jensen, J. (1984) Mechanism of complement cvtolysis and the concept of channel-forming proteins. Philos. Trans. R. Soc. Lond. Biol., 306, 311-324.
4. Bhakdi, S., Tranum Jensen, J. and Sziegoleit, A. (1985) Mechanism of membrane damage by streptolysin-O. Infect. Immun., 47, 52-60.
5. Bhakdi, S., Weller, U., Walev, I., Martin, E., Jonas, D. and Palmer, M. (1993) A guide to the use of pore-forming toxins for controlled permeabilization of cell membranes. Med. Microbiol. Immunol., 182, 167-175.
6. Cormack, B. (1987) Mutagenesis by the polymerase chain reaction. In Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.M., Seidman, J.G., Smith, J.A. and Struhl, K. (eds), Current Protocols in Molecular Biology. Wiley & Sons, New York.
7. Eriksen, S., Olsnes, S., Sandvig, K. and Sand, O. (1994) Diphtheria toxin at low pH depolarizes the membrane, increases the membrane conductance and induces a new type of ion channel in Vero cells. EMBO J., 13, 4433-4439.
8. Fuessle, R., Bhakdi, S., Sziegoleit, A., Tranum Jensen, J., Kranz, T. and Wellensiek, H.J. (1981) On the mechanism of membrane damage by Staphylococcus aureus alpha-toxin. J. Cell Biol., 91, 83-94.
9. Hugo, F., Reichwein, J., Arvand, M., Kramer, S. and Bhakdi, S. (1986) Use of a monoclonal antibody to determine the mode of transmembrane pore formation by streptolysin O. Infect. Immun., 54, 641-645.
10. Martoglio, B., Hofmann, M.W., Brunner, J. and Dobberstein, B. (1995) The protein-conducting channel in the membrane of the endoplasmic reticulum is open laterally toward the lipid bilayer. Cell, 81, 207-214.
11. Mayer, L.D., Hope, M.J. and Cullis, P.R. (1986) Vesicles of variable sizes produced by a rapid extrusion procedure. Biochim. Biophys. Acta, 858, 161-168.
12. Montecucco, C., Papini, E., Schiavo, G., Padovan, E. and Rossetto, O. (1992) Ion channel and membrane translocation of diphtheria toxin. FEMS Microbiol. Immunol., 5, 101-111.
13. Ohno Iwashita, Y., Iwamoto, M., Mitsui, K., Ando, S. and Iwashita, S. (1991) A cytolsin, theta-toxin, preferentially binds to membrane cholesterol surrounded by phospholipids with 18-carbon hydrocarbon chains in cholesterol-rich region. J. Biochem., Tokyo, 110, 369-375.
14. Palmer, M., Jursch, R., Weller, U., Valeva, A., Hilgert, K., Kehoe, M. and Bhakdi, S. (1993) Staphylococcus aureus alpha-toxin. Production of functionally intact, site-specifically modifiable protein by introduction of cysteine at positions 69, 130, and 186. J. Biol. Chem., 268, 11959-11962.
15. Palmer, M., Valeva, A., Kehoe, M. and Bhakdi, S. (1995) Kinetics of streptolysin O self-assembly. Eur. J. Biochem., 231, 388-395.
16. Palmer, M., Saweljew, P., Vulicevic, I., Valeva, A., Kehoe, M. and Bhakdi, S. (1996) Membrane-inserting domain of streptolysin O identified by cysteine scanning mutagenesis. J. Biol. Chem., 271, 26664-26667.
17. Palmer, M., Buchkremer, M., Valeva, A. and Bhakdi, S. (1997) Cysteine-specific radioiodination of proteins with fluorescein maleimide. Anal. Biochem., 253, 175-179.
18. Parker, M.W., Buckley, J.T., Postma, J.P., Tucker, A.D., Leonard, K., Pattus, F. and Tsernoglou, D. (1994) Structure of the Aeromonas toxin proaerolysin in its water-soluble and membrane-channel states. Nature, 367, 292-295.
19. Pinkney, M., Beachey, E. and Kehoe, M. (1989) The thiol-activated toxin streptolysin O does not require a thiol group for cytolytic activity. Infect. Immun., 57, 2553-2558.
20. Rossjohn, J., Feil, S.C., McKinstrey, W.J., Tweten, R.K. and Parker, M.W. (1997) Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form. Cell, 89, 685-692.
21. Scherrer, R. and Gerhardt, P. (1971) Molecular sieving by the Bacillus megaterium cell wall and protoplast. J. Bacteriol., 107, 718-735.
22. Sekiya, K., Satoh, R., Danbara, H. and Futaesaku, Y. (1993) A ring-shaped structure with a crown formed by streptolysin O on the erythrocyte membrane. J. Bacteriol. 175, 5953-5961.
23. Song, L., Hobaugh, M.R., Shustak, C., Cheley, S., Bayley, H. and Gouaux, J.E. (1996) Structure of staphylococca alpha-hemolysin, a heptameric transmembrane pore. Science, 274, 1859-1866.
24. Valeva, A., Weisser, A., Walker, B., Kehoe, M., Bayley, H., Bhakdi, S. and Palmer, M. (1996) Molecular architecture of a toxin pore: a 15-residue sequence lines the transmembrane channel of staphylococcal alpha-toxin. EMBO J., 15, 1857-1864.
25. Valeva, A., Palmer, M. and Bhakdi, S. (1997) Staphylococcal α-toxin: formation of the heptameric pore is partially cooperative and proceeds through multiple intermediate stages. Biochemistry, 36, 13298-13304.
26. Walker, B., Krishnasastry, M., Zorn, L. and Bayley, H. (1992) Assembly of the oligomeric membrane pore formed by staphylococcal alpha-hemolysin examined by truncation mutagenesis. J. Biol. Chem., 267, 21782-21786.
27. Weller, U. et al. (1996) Expression of active streptolysin O in Escherichia coli as a maltose binding protein-streptolysin O fusion protein: the N-terminal 70 amino acids are not required for hemolytic activity. Eur. J. Biochem., 236, 34-39.