Structures of Perfringolysin O Suggest a Pathway for Activation of Cholesterol-dependent Cytolysins

Journal of Molecular Biology

Volumn 367, Issue 5, 2007, Pages 1227-1236

  Rossjohn, Jamie ^a   Polekhina, Galina ^a   Feil, Susanne C ^a   Morton, Craig J ^a   Tweten, Rodney K ^b   Parker, Michael W ^a  

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

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

Author keywords

cholesterol dependent cytolysins; membrane insertion; perfringolysin O; pore forming toxin; X ray crystallography

Indexed keywords

BACTERIAL TOXIN; CLOSTRIDIUM PERFRINGENS TOXIN; CYTOLYSIN; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; MEMBRANE BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; STRUCTURAL PROTEOMICS; STRUCTURE ACTIVITY RELATION; TOXIN ANALYSIS; TOXIN STRUCTURE;

BACTERIA (MICROORGANISMS);

EID: 33947163269     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.01.042     Document Type: Article

References (42)

1. Tweten R.K., Parker M.W., and Johnson A.E. The cholesterol-dependent cytolysins. Curr. Top. Microbiol. Immunol. 257 (2001) 15-33
2. Rossjohn J., Feil S.C., McKinstry W.J., Tweten R.K., and Parker M.W. Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form. Cell 89 (1997) 685-692
3. Polekhina G., Giddings K.S., Tweten R.K., and Parker M.W. Insights into the action of the superfamily of cholesterol-dependent cytolysins from studies of intermedilysin. Proc. Natl Acad. Sci. USA 102 (2005) 600-605
4. Nakamura M., Sekino N., Iwamoto M., and Ohno-Iwashita Y. Interaction of θ-toxin (perfringolysin O), a cholesterol-binding cytolysin, with liposomal membranes: change in the aromatic side chains upon binding and insertion. Biochemistry 34 (1995) 6513-6520
5. Sekino-Suzuki N., Nakamura M., Mitsui K.I., and Ohno-Iwashita Y. Contribution of individual tryptophan residues to the structure and activity of θ-toxin (perfringolysin-O), a cholesterol-binding cytolysin. Eur. J. Biochem. 241 (1996) 941-947
6. Palmer M., Saweljew P., Vulicevic I., Valeva A., Kehoe M., and Bhakdi S. Membrane-penetrating domain of streptolysin O identified by cysteine scanning mutagenesis. J. Biol. Chem. 271 (1996) 26662-26667
7. Shepard L.A., Heuck A.P., Hamman B.D., Rossjohn J., Parker M.W., Ryan K.R., et al. Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an alpha-helical to beta-sheet transition identified by fluorescence spectroscopy. Biochemistry 37 (1998) 14563-14574
8. Shatursky O., Heuck A.P., Shepard L.A., Rossjohn J., Parker M.W., Johnson A.E., and Tweten R.K. The mechanism of membrane insertion for a cholesterol-dependent cytolysin: a novel paradigm for pore-forming toxins. Cell 99 (1999) 293-299
9. Shepard L.A., Shatursky O., Johnson A.E., and Tweten R.K. The mechanism of pore assembly for a cholesterol-dependent cytolysin: formation of a large prepore complex precedes the insertion of the transmembrane beta-hairpins. Biochemistry 39 (2000) 10284-10293
10. Hotze E.M., Wilson-Kubalek E.M., Rossjohn J., Parker M.W., Johnson A.E., and Tweten R.K. Arresting pore formation of a cholesterol-dependent cytolysin by disulfide trapping synchronizes the insertion of the transmembrane beta-sheet from a prepore intermediate. J. Biol. Chem. 276 (2001) 8261-8268
11. Hotze E.M., Heuck A.P., Czajkowsky D.M., Shao Z., Johnson A.E., and Tweten R.K. Monomer-monomer interactions drive the prepore to pore conversion of a beta-barrel-forming cholesterol-dependent cytolysin. J. Biol. Chem. 277 (2002) 11597-11605
12. Heuck A.P., Tweten R.K., and Johnson A.E. Beta-barrel pore-forming toxins: intriguing dimorphic proteins. Biochemistry 40 (2001) 9065-9073
13. Czajkowsky D.M., Hotze E.M., Shao Z., and Tweten R.K. Vertical collapse of a cytolysin prepore moves its transmembrane β-hairpins to the membrane. EMBO J. 23 (2004) 3206-3215
14. Gilbert R.J.C., Jimenez J.L., Chen S., Tickle I.J., Rossjohn J., Parker M.W., et al. Two structural transitions in membrane pore formation by pneumolysin, the pore-forming toxin of Streptococcus pneumoniae. Cell 97 (1999) 647-655
15. Tilley S.J., Orlova E.V., Gilbert R.J.C., Andrew P.W., and Saibil H.R. Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 121 (2005) 247-256
16. Palmer M., Vulicevic I., Saweljew P., Valeva A., Kehoe M., and 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
17. Abdel Ghani E.M., Weis S., Walev I., Kehoe M., Bhakdi S., and Palmer M. Streptolysin O: inhibition of the conformational change during membrane binding of the monomer prevents oligomerization and pore formation. Biochemistry 38 (1999) 15204-15211
18. Heuck A.P., Hotze E.M., Tweten R.K., and Johnson A.E. Mechanism of membrane insertion of a multimeric beta-barrel protein: perfringolysin O creates a pore using ordered and coupled conformational changes. Mol. Cell 6 (2000) 1233-1242
19. Ramachandran R., Heuck A.P., Tweten R.K., and Johnson A.E. Structural insights into the membrane-anchoring mechanism of a cholesterol-dependent cytolysin. Nature Struct. Biol. 11 (2002) 823-827
20. Feil S.C., Rossjohn J., Rhode K., Tweten R.K., and Parker M.W. Crystallization and preliminary X-ray analysis of a thiol-activated cytolysin. FEBS Letters 397 (1996) 290-292
21. Polekhina G., Feil S.C., Tang J., Rossjohn J., Giddings K.S., Tweten R.K., and Parker M.W. Comparative three-dimensional structure of cholesterol-dependent cytolysins. In: Alouf J.E., and Popoff M.R. (Eds). The Comprehensive Sourcebook of Bacterial Protein Toxins. 3rd edit. (2006), Elsevier, London 659-670
22. Morgan P.J., Hyman S.C., Byron O., Andrew P.W., Mitchell T.J., and Rowe A.J. Modeling the bacterial protein toxin, pneumolysin, in its monomeric and oligomeric form. J. Biol. Chem. 269 (1994) 25315-25320
23. Gilbert R.J.C., Rossjohn J., Parker M.W., Tweten R.K., Morgan P.J., Mitchell T.J., et al. Self-interaction of pneumolysin, the pore-forming protein toxin of Streptococcus pneumoniae. J. Mol. Biol. 284 (1998) 1223-1237
24. Solovyova A.S., Nöllmann M., Mitchell T.J., and Byron O. The solution structure and oligomerization behavior of two bacterial toxins: pneumolysin and perfringolysin O. Biophys. J. 87 (2004) 540-552
25. Gilbert R.J.C. Inactivation and activity of cholesterol-dependent cytolysins: what structural studies tell us. Structure 13 (2005) 1097-1106
26. Painter J., and Merritt E.A. TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallog. 39 (2006) 109-111
27. Painter J., and Merritt E.A. Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallog. sect D 62 (2006) 439-450
28. Ramachandran R., Tweten R.K., and Johnson A.E. The domains of a cholesterol-dependent cytolysin undergo a major FRET-detected rearrangement during pore formation. Proc. Natl Acad. USA 102 (2005) 7139-7144
29. Giddings K.S., Johnson A.E., and Tweten R.K. Redefining cholesterol's role in the mechanism of the cholesterol-dependent cytolysins. Proc. Natl Acad. Sci. USA 100 (2003) 11315-11320
30. Parker M.W., and Pattus F. Rendering a membrane protein soluble in water: a common packing motif in bacterial protein toxins. Trends Biochem. Sci. 18 (1993) 391-395
31. Choe S., Bennett M.J., Fujii G., Curmi P.M., Kantardjieff K.A., Collier R.J., and Eisenberg D. The crystal structure of diphtheria toxin. Nature 357 (1992) 216-222
32. Glomski I.J., Gedde M.M., Tsang A.W., Swanson J.A., and Portnoy D.A. The Listeria monocytogenes hemolysin has an acidic pH optimum to compartmentalize activity and prevent damage to infected cells. J. Cell Biol. 156 (2002) 1029-1038
33. Portnoy D.A., Tweten R.K., Kehoe M., and Bielecki J. Capacity of listeriolysin O, streptolysin O, and perfringolysin O to mediate growth of Bacillus subtilis within mammalian cells. Infect. Immun. 60 (1992) 2710-2717
34. Yang A.S., Gunner M.R., Sampogna R., Sharp K., and Honig B. On the calculation of pKas in proteins. Proteins: Struct. Funct. Genet. 15 (1993) 252-265
35. van der Goot F.G., González-Mañas J.M., Lakey J.H., and Pattus F. A 'molten-globule' membrane-insertion intermediate of the pore-forming domain of colicin A. Nature 354 (1991) 408-410
36. Kraulis P. MOLSCRIPT: a program to produce both detailed and schematic plots of proteins. J. Appl. Crystallog. 24 (1991) 946-950
37. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in the oscillation mode. Methods Enzymol. 276 (1997) 307-326
38. Brünger A.T. XPLOR: A System for X-ray Crystallography and NMR (1993), Yale University, New Haven, CT
39. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect D 54 (1998) 905-921
40. Laskowski R.A., McArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 282-291
41. Yeates T.O. Detecting and overcoming crystal twinning. Methods Enzymol. 276 (1997) 344-358
42. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect D 50 (1994) 750-763