Aerolysin - The ins and outs of a model channel-forming toxin

Molecular Microbiology

Volumn 19, Issue 2, 1996, Pages 205-212

  Parker, Michael W ^a   Van Der Goot Gisou, F ^b   Buckley, J Thomas ^c  

^a ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF GENEVA   (Switzerland)

^c UNIVERSITY OF VICTORIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AEROLYSIN; BACTERIAL TOXIN; UNCLASSIFIED DRUG;

AEROMONAS; ANIMAL CELL; CELL MEMBRANE; CONTROLLED STUDY; ERYTHROCYTE; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE; RAT; REVIEW;

AEROMONAS; ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 0030043134     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1996.355887.x     Document Type: Review

References (46)

1. Ahnert-Hilger, G. (1994) Permeabilization by alpha-toxin and streptolysin O. In Cell Biology: A Laboratory Handbook. New York: Academic Press, pp. 77-82.
2. Ballard, J., Sokolov, Y., Yuan, W.-L., Kagan, B.L., and Tweten, R.K. (1993) Activation and mechanism of Clostridium septicum alpha toxin. Mol Microbiol 10: 627-634.
3. Ballard, J., Crabtree, J., Roe, B.A., and Tweten, R.K. (1995) The primary structure of Clostridium septicum alpha-toxin exhibits similarity with that of Aeromonas hydrophila aerolysin. Infect Immun 63: 340-344.
4. Bayley, H. (1994) Triggers and switches in a self-assembling pore-forming protein. J Cellular Biochem 56: 177-182.
5. Bennett, M.J., Choe, S., and Eisenberg, D. (1994) Domain swapping: entangling alliances between proteins. Proc Natl Acad Sci USA 91: 3127-3131.
6. Bernheimer, A.W., and Rudy, B. (1986) Interactions between membranes and cytolytic peptides. Biochim Biophys Acta 864: 123-141.
7. Bernheimer, A.W., Avigad, L.S., and Avigad, G. (1975) Interactions between aerolysin, erythrocytes, and erythrocyte membranes. Infect Immun 11: 1312-1319.
8. Boulnois, G.J., Paton, J.C., Mitchell, T.J., and Andrew, P.W. (1991) Structure and function of pneumolysin, the multi-functional, thiol-activated toxin of Streptococcus pneumoniae. Mol Microbiol 5: 2611-2616.
9. Braun, V., and Focareta, T. (1991) Pore-forming bacterial protein hemolysins (cytolysins). Crit Rev Microbiol 18: 115-158.
10. Eriksson, A.E., Baase, W.A., Zhang, X.-J., Heinz, D.W., Blaber, M., Baldwin, E.P., and Matthews, B.W. (1991) Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science 255: 178-193.
11. Garland, W.J., and Buckley, J.T. (1988) The cytolytic toxin aerolysin must aggregate to disrupt erythrocytes, and aggregation is stimulated by human glycophorin. Infect Immun 56: 1249-1253.
12. Green, M.J., and Buckley, J.T. (1990) Site-directed mutagenesis of the hole-forming toxin aerolysin: studies on the roles of histidines in receptor binding and oligomerization of the monomer. Biochemistry 29: 2177-2180.
13. Gordon, V.M., and Leppla, S.H. (1994) Proteolytic activation of bacterial toxins: role of bacterial and host cell proteases. Infect Immun 62: 333-340.
14. Gordon, V.M., Klimpel, K.R., Arora, N., Henderson, M.A., and Leppla, S.H. (1995) Proteolytic activation of bacterial toxins by eukaryotic cells is performed by furin and by additional cellular proteases. Infect Immun 63: 82-87.
15. Gouaux, J.E., Braha, O., Hobaugh, M.R., Song, L., Cheley, S., Shustak, C., and Bayley, H. (1994) Subunit stoichiometry of staphylococcal alpha-hemolysin in crystals and on membranes: a heptameric transmembrane pore. Proc Natl Acad Sci USA 91: 12828-12831.
16. van der Goot, F.G., Lakey, J., Pattus, F., Kay, C.M., Sorokine, O., Van Dorsselaer, A., and Buckley, J.T. (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
17. van der Goot, F.G., Ausio, J. , Wong, K.R., Pattus, F, and Buckley, J.T. (1993a) Dimerization stabilizes the pore-forming toxin aerolysin in solution. J Biol Chem 268: 18272-18279.
18. van der Goot, F.G., Pattus, F., Wong, K., and Buckley, J.T. (1993b) Oligomerization of the channel-forming toxin aerolysin precedes insertion into lipid bilayers. Biochemistry 32: 2636-2642.
19. van der Goot, F.G., Hardie, K.R., Parker, M.W., and Buckley, J.T. (1994a) 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.
20. van der Goot, F.G., Pattus, F., Parker, M.W., and Buckley, J.T. (1994b) Aerolysin: from the soluble form to the transmembrane channel. Toxicol 87: 19-28.
21. Gruber, H.J., Wilmsen, H.U., Cowell, S., Schindler, H., and Buckley, J.T. (1994) Partial purification of the rat erythrocyte receptor for the channel-forming toxin aerolysin and reconstitution into planar lipid bilayers. Mol Microbiol 14: 1093-1011.
22. Hardie, K.R., Schulze, A., Parker, M.W., and Buckley, J.T. (1995) Vibrio sp. secrete proaerolysin as a folded dimer without the need for disulphide bond formation. Mol Microbiol 17: 1035-1044.
23. Harshman, S., and Sugg, N. (1985) Effect of calcium ions on staphyloccocal alpha-toxin-induced hemolysis of rabbit erythrocytes. Infect Immun 47: 37-40.
24. Hayashi, T., Kamio, Y., Hishinuma, F., Usami, Y., Titani, K., and Terawaki, Y. (1989) Pseudomonas aeruginosa cytotoxin: the nucleotide sequence of the gene and the mechanism of activation of the protoxin. Mol Microbiol 3: 861-868.
25. Howard, S.P., and Buckley, J.T. (1982) Membrane glycoprotein receptor and hole-forming properties of a cytolytic protein toxin. Biochemistry 21: 1662-1667.
26. Howard, S.P., Garland, W. J, Green, M.J., and Buckley, J.T. (1987) Nucleotide sequence of the gene for the hole-forming toxin of Aeromonas hydrophila. J Bacteriol 169: 2869-2871.
27. Hucho, F. (1995) Toxins as tools in neurochemistry. Angew Chem Int Ed Engl 34: 39-50.
28. Jahagirdar, R., and Howard, S.P. (1994) Isolation and characterization of a second exe operon required for extracellular protein secretion in Aeromonas hydrophila. J Bacteriol 176: 6819-6826.
29. Jap, B.K., and Walian, P.J. (1990) Biophysics of the structure and function of porins. Quart Rev Biophys 23: 367-403.
30. Korchev, Y.E., Bashford, C.L., and Pasternak, C.A. (1992) Differential sensitivity of pneumolysin-induced channels to gating by divalent cations. J Memb Biol 127: 195-203.
31. Milne, J.C., Furlong, D., Hannah, P.C., Wall, J.S., and Collier, R.J. (1994) Anthrax protective antigen forms oligomers during intoxication of mammalian cells. J Biol Chem 269: 20607-20612.
32. Montecucco, C., Papini, E., and Schiavo, G. (1994) Bacterial protein toxins penetrate cells via a four-step mechanism. FEBS Lett 346: 92-98.
33. Morgan, P.J., Hyman, S.C., Rowe, A.J., Mitchell, T.J., Andrew, P.W., and Saibil, H.R. (1995) Subunit organization and symmetry of pore-forming oligomeric pneumolysin. FEBS Lett 371: 77-80.
34. Okazaki, I.J., Zolkiewska, A., Nightingale, M.S., and Moss, J. (1994) Immunological and structural conservation of mammalian skeletal muscle glycosylphosphatidylinositol-linked ADP-ribosyltransferases. Biochemistry 33: 12828-12836.
35. Parker, M.W., and Pattus, F. (1993) Rendering a membrane protein soluble in water - a common packing motif in bacterial protein toxins. Trends Biochem Sci 18: 391-395
36. Parker, M.W., Buckley, J.T., Postma, J.P.M., 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.
37. Paul, C., and Rosenbusch, J.P. (1985) Folding patterns of porin and bacteriorhodopsin. EMBO J 4: 1593-1597.
38. Pinkey, 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.
39. Prigent, D., and Alouf, J.E. (1976). Interaction of streptolysin O with sterols. Biochim Biophys Acta 443: 288-300.
40. Pugsley, A.P. (1993) The complete General Secretory Pathway in Gram-negative bacteria. Microbiol Rev 57: 50-108.
41. Russel, M. (1994) Phage assembly: a paradigm for bacterial virulence factor export? Science 265: 612-614.
42. Sen, K., and Nikaido, H. (1990) In vitro trimerization of OmpF porin secreted by spheroplasts of Escherichia coli. Proc Natl Acad Sci USA 87: 743-747.
43. Sibbald, P.R., and Argos, P. (1990) Scrutineer: a computer program that flexibly seeks and describes motifs and profiles in protein sequence databases. CABIOS 6: 279-288.
44. Takada, T., Iida, K., and Moss, J. (1994) Expression of NAD glycohydrolase activity by rat mammary adenocarcinoma cells transformed with rat T cell alloantigen RT6.2. J Biol Chem. 269: 9420-9423.
45. Wilmsen, H.U., Leonard, K.R., Tichelaar, W., Buckley, J.T., and Pattus, F. (1992) The aerolysin membrane channel is formed by heptamerization of the monomer. EMBO J 11: 2457-2463.
46. Wong, K.R., and Buckley, J.T. (1991) Site-directed mutagenesis of a single tryptophan near the middle of the channel-forming toxin aerolysin inhibits its transfer across the outer membrane of Aeromonas salmonicida. J Biol Chem 266: 14451-14456.