Self-interaction of pneumolysin, the pore-forming protein toxin of Streptococcus pneumoniae

Journal of Molecular Biology

Volumn 284, Issue 4, 1998, Pages 1223-1237

  Gilbert, Robert J C ^a   Rossjohn, Jamie ^b   Parker, Michael W ^b   Tweten, Rodney K ^c   Morgan, Peter J ^a,e   Mitchell, Timothy J ^d   Errington, Neil ^a   Rowe, Arthur J ^a   Andrew, Peter W ^a   Byron, Olwyn ^d  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

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

^c UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e Murex Biotech Ltd   (United Kingdom)

Author keywords

Analytical ultracentrifugation; Electron microscopy; Neutron scattering; Oligomerization; Pneumolysin

Indexed keywords

BACTERIAL PROTEIN; CHOLESTEROL; OLIGOMER; PNEUMOLYSIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; COMPLEMENT ACTIVATION; CONTROLLED STUDY; DERIVATIZATION; ELECTRON MICROSCOPY; MEMBRANE BINDING; MOLECULAR MODEL; NEUTRON SCATTERING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STREPTOCOCCUS PNEUMONIA; STREPTOCOCCUS PNEUMONIAE;

BACTERIA (MICROORGANISMS); POSIBACTERIA; STREPTOCOCCUS; STREPTOCOCCUS PNEUMONIAE;

EID: 0032509103     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2258     Document Type: Article

References (59)

1. Alexander J. E., Berry A. M., Paton J. C., Rubins J. B., Andrew P. W., Mitchell T. J. Amino acid changes affecting the activity of pneumolysin alter the behaviour of pneumococci in pneumonia. Micro. Pathogen. 24:1998;167-174.
2. Alouf J. E., Geoffroy C. The family of the antigenically-related, cholesterol-binding ('sulphydryl-activated') cytolytic toxins. Alouf J. E., Freer J. H. Sourcebook of Bacterial Protein Toxins. 1991;147-186 Academic Press, London.
3. Austrian R. Pneumococcus: the first 100 years. Rev. Infect. Dis. 3:1981;183-189.
4. Bayley H. Structure of a pore-forming toxin: part of a hole? Curr. Biol. 7:1997;R763-R767.
5. Bhakdi S., Tranum-Jensen J. Damage to cell-membranes by pore-forming bacterial cytolysins. Prog. Allergy. 40:1988;1-43.
6. Bhakdi S., Tranum-Jensen J., Sziegoleit A. Mechanism of membrane damage by Streptolysin-O. Infect. Immun. 47:1985;52-60.
7. Bhakdi S., Bayley H., Valeva A., Walev I., Walker B., Weller U., Kehoe M., Palmer M. Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins. Arch. Microbiol. 165:1996;73-79.
8. Blake C., Serpell L. Synchotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous β-sheet helix. Structure. 4:1996;989-998.
9. Bridgman W. B. Some physical chemical properties of glycogen. J. Am. Chem. Soc. 64:1942;2349-2350.
10. Byron O. Construction of hydrodynamic bead models from high-resolution X-ray crystallographic or nuclear magnetic resonance data. Biophys. J. 72:1997;408-415.
11. Clewlow A. C., Errington N., Rowe A. J. Analysis of data captured by an on-line image capture system from an analytical ultracentrifuge using Schlieren optics. Eur. Biophys. J. 25:1997;311-317.
12. Cowell J. L., Kim K.-S., Bernheimer A. W. Alteration by cereolysin of the structure of cholesterol-containing membranes. Biochim. Biophys. Acta. 507:1978;230-241.
13. Deisenhofer J., Colman P. M., Epp O., Huber R. Crystallographic structural studies of a human Fc fragment. II. A complete model based on a Fourier map at 3.5 Å resolution. Hoppe-Seyler's Z. Physiol. 357:1976;1421-1434.
14. Garcia de la Torre J., Navarro S., Lopez Martinez M. C., Diaz F. G., Lopez Cascales J. J. HYDRO: a computer program for the prediction of hydrodynamic properties of macromolecules. Biophys. J. 67:1994;530-531.
15. Guinier A., Fournet G. Small-Angle Scattering of X-rays. 1955;Wiley, New York.
16. Hamilton J. A., Steinrauf L. K., Braden B. C., Liepnieks J., Benson M. D., Holmgren G., Sandgren O., Steen L. The X-ray crystal structure refinements of normal human transthyretin and the amyloidogenic Val-30-Met variant to 1.7 Å resolution. J. Biol. Chem. 268:1993;2416-2424.
17. Harris R. W., Sims P. J., Tweten R. K. Kinetic aspects of the aggregation of Clostridium perfringensθ-toxin on erythrocyte membranes. J. Biol. Chem. 266:1991;6936-6941.
18. Heenan R. K. Rutherford-Appleton Laboratory Report. 1989;. p. 89-129.
19. Iwamoto M., Ohno-Iwashita Y., Ando S. Role of the essential thiol group in the thiol-activated cytolysin from Clostridium perfringens. Eur. J. Biochem. 167:1987;425-430.
20. Kelly J. W. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr. Opin. Struct. Biol. 8:1998;101-106.
21. Laemmli U. K. Cleavage of structural proteins during the assembly of the bead of bacteriophage T4. Nature. 227:1970;680-685.
22. Mitchell T. J., Walker J. A., Saunders F. K., Andrew P. W., Boulnois G. J. Expression of the pneumolysin gene in Escherichia coli-rapid purification and biological properties. Biochim. Biophys. Acta. 1007:1989;67-72.
23. Mitchell T. J., Andrew P. W., Saunders F. K., Smith A. N., Boulnois G. J. Complement activation and antibody-binding by pneumolysin via a region of the toxin homolgous to a human acute-phase protein. Mol. Microbiol. 5:1991;1883-1888.
24. Mitsui K.I., Sekiya T., Okamura S., Nozawa Y., Hase J.I. Ring formation of perfringolysin-O as revealed by negative stain electron microscopy. Biochim. Biophys. Acta. 558:1979;307-313.
25. Morgan P. J., Varley P. G., Rowe A. J., Andrew P. W., Mitchell T. J. Characterization of the solution properties and conformation of pneumolysin, the membrane-damaging toxin ofStreptococcus pneumoniae. Biochem. J. 296:1993;671-674.
26. Morgan P. J., Hyman S. C., Byron O., Andrew P. W., Mitchell T. J., Rowe A. J. Modeling the bacterial protein toxin, pneumolysin, in its monomeric and oligomeric form. J. Biol. Chem. 269:1994;25315-25320.
27. Morgan P. J., Hyman S. C., Rowe A. J., Mitchell T. J., Andrew P. W., Saibil H. R. Subunit organisation and symmetry of pore-forming oligomeric pneumolysin. FEBS Letters. 371:1995;77-80.
28. Morgan P. J., Andrew P. W., Mitchell T. J. Thiol-activated cytolysins. Rev. Med. Microbiol. 7:1996;221-229.
29. Morgan P. J., Harrison G., Freestone P., Crane D., Rowe A. J., Mitchell T. J., Andrew P. W., Gilbert R. J. C. Structural and functional characterisation of two proteolytic fragments of the bacterial protein toxin, pneumolysin. FEBS Letters. 412:1997;563-567.
30. Niedermeyer W. Interaction of streptolysin-O with biomembranes: kinetic and morphological studies on erythrocyte membranes. Toxicon. 23:1985;425-439.
31. Ohno-Iwashita Y., Iwamoto M., Mitsui K.-i., Ando S., Iwashita S. A cytolysin, θ-toxin, preferentially binds to membrane cholesterol surrounded by phospholipids with 18-carbon hydrocarbon chains in cholesterol-rich regions. J. Biochem. 110:1991;369-375.
32. Owen R. H. G., Boulnois G. J., Andrew P. W., Mitchell T. J. A role in cell-binding for the C-terminus of pneumolysin, the thiol-activated toxin of Streptococcus pneumoniae. FEMS Microbiol. Letters. 121:1994;217-222.
33. Palmer M., Valeva A., Kehoe M., Bhakdi S. Kinetics of streptolysin O self-assembly. Eur. J. Biochem. 231:1995;388-395.
34. Palmer M., Saweljew P., Vulicevic I., Valeva A., Kehoe M., Bhakdi S. Membrane-penetrating domain of streptolysin O identified by cysteine scanning mutagenesis. J. Biol. Chem. 271:1996;26664-26667.
35. Palmer M., Vulicevic I., Saweljew P., Valeva A., Kehoe M., Bhakdi S. Streptolysin O: a proposed model of allosteric interaction between a pore-forming protein and its target lipid bilayer. Biochemistry. 37:1998;2378-2383.
36. Parker M. W., Buckley J. T., Postma J. P. M., Tucker A. D., Leonard K., Pattus F., Tsernoglou D. Structure of the Aeromonas toxin proaerolysin in its water-soluble and membrane-channel states. Nature. 367:1994;292-295.
37. Parker M. W., van der Goot F. G., Buckley J. T. Aerolysin - the ins and outs of a model channel-forming toxin. Mol. Microbiol. 19:1996;205-212.
38. Perkins S. J. Protein volumes and hydration effects. Eur. J. Biochem. 157:1986;169-180.
39. Perkins S. J. X-ray and neutron solution scattering. Neuberger A., van Deenen L. L. M. Modern Physical Methods in Biochemistry. 1988;143-265 Elsevier, Amsterdam.
40. Perkins S. J. Jones C., Mulloy B., Thomas A. H. Methods in Molecular Biology. 1994;Humana Press, Totowa.
41. Perkins S. J., Weiss H. Low resolution structural studies of mitochondrial ubiquinol-cytochrome c reductase in detergent solutions by neutron scattering. J. Mol. Biol. 168:1983;847-866.
42. Petosa C., Collier R. J., Klimpel K. R., Leppla S. H., Liddington R. C. Crystal structure of the anthrax toxin protective antigen. Nature. 385:1997;833-838.
43. Pilz I., Glatter O., Kratky O. Small-angle X-ray scattering. Methods Enzymol. 61:1979;148-249.
44. Rossjohn J., Feil S. C., McKinstry W. J., Tweten R. K., Parker M. W. Structure of a cholesterol-binding, thiol-activated cytolysin in water-soluble and membrane forms. Cell. 89:1997;685-692.
45. Rossjohn J., Gilbert R. J. C., Crane D., Morgan P. J., Mitchell T. J., Rowe A. J., Andrew P. W., Tweten R. K., Parker M. W. The molecular mechanism of pneumolysin, a virulence factor from Streptococcus pneumoniae. J. Mol. Biol. 284:1998;449-461.
46. Rottem S., Hardegree M. C., Grabowski M. W., Fornwald R., Barile M. F. Interaction between tetanolysin and mycoplasma cell membrane. Biochim. Biophys. Acta. 455:1976;876-888.
47. Semenyuk A. V., Svergun D. I. GNOM-a program package for small-angle scattering data processing. J. Appl. Crystallog. 24:1991;537-540.
48. Smyth C. J., Duncan J. L. Thiol-activated (oxygen-labile) cytolysins. Jeljaszewicz J., Wadstrom T. Bacterial Toxins and Cell Membranes. 1978;129-183 Academic Press, London.
49. Song L., Hobaugh M. R., Shustak C., Cheley S., Bayley H., Gouaux J. E. Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science. 274:1996;1859-1866.
50. Sowdhamini R., Mitchell T. J., Andrew P. W., Morgan P. J. Structural and functional analogy between pneumolysin and aerolysin. Protein Eng. 10:1997;207-215.
51. Stafford W. F. III. Methods for obtaining sedimentation coefficient distributions. Harding S. E., Rowe A. J., Horton J. C. Analytical Ultracentrifugation in Biochemistry and Polymer Science. 1992;359-393 Royal Society of Chemistry, Cambridge.
52. Stafford W. F. III. Rapid molecular-weight determination by sedimentation-velocity analysis. Biophys. J. 70:1996;A231.
53. Svergun D. I., Richard S., Koch M. H. J., Sayers Z., Kuprin S., Zaccai G. Protein hydration in solution: experimental obsevration by x-ray and neutron scattering. Proc. Natl Acad. Sci. USA. 95:1998;2267-2272.
54. Tweten R. K. Pore-forming toxins in Gram-positive bacteria. Roth J. A., Bolin C. A., Brogden K. A., Minion C., Wannemuehler M. J. Virulence Mechanisms of Bacterial Pathogens. 1995;207-229 American Society for Microbiology, Washington.
55. Wang P.-F., Veine D. M., Ahn S. H., Williams C. H. A stable mixed disulfide between thioredoxin reductase and its substrate, thioredoxin: preparation and characterization. Biochemistry. 35:1996;4812-4819.
56. Watson K. C., Kerr E. J. C. Sterol structural requirements for inhibition of streptolysin O activity. Biochem. J. 140:1974;95-98.
57. Wright J. K., Tschopp J., Jaton J.-T., Engel J. Dimeric, trimeric and tetrameric complexes of immunoglobulin G fix complement. Biochem. J. 187:1980;775-780.
58. Yamakawa Y., Ohsaka A. Hydrophobic interaction between θ-toxin of Clostridium perfringens and erythrocyte membrane. Jap. J. Med. Sci. Biol. 39:1986;254-255.
59. Yphantis D. A. Equilibrium ultracentrifugation in dilute solutions. Biochemistry. 3:1964;297-317.