Structural studies of streptococcus pyogenes streptolysin O provide insights into the early steps of membrane penetration

Journal of Molecular Biology

Volumn 426, Issue 4, 2014, Pages 785-792

  Feil, Susanne C ^a   Ascher, David B ^a   Kuiper, Michael J ^b   Tweten, Rodney K ^c   Parker, Michael W ^a,d  

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

^b UNIVERSITY OF MELBOURNE   (Australia)

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

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

conformational change; membrane insertion; molecular dynamics simulations; pore forming toxins; X ray crystallography

Indexed keywords

BACTERIAL TOXIN; CLOSTRIDIUM PERFRINGENS TOXIN; STREPTOLYSIN O; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CRYSTALLIZATION; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; SEQUENCE ANALYSIS; STREPTOCOCCUS PYOGENES;

BACTERIA (MICROORGANISMS); STREPTOCOCCUS PYOGENES;

ALO; ANTHROLYSIN; CDC; CHOLESTEROL-DEPENDENT CYTOLYSIN; CONFORMATIONAL CHANGE; ILY; INTERMEDILYSIN; MEMBRANE INSERTION; MOLECULAR DYNAMICS SIMULATIONS; NATIONAL HEALTH AND MEDICAL RESEARCH COUNCIL OF AUSTRALIA; NHMRC; PERFRINGOLYSIN O; PFO; PORE-FORMING TOXINS; SLO; SLY; STREPTOLYSIN O; SUILYSIN; X-RAY CRYSTALLOGRAPHY;

AMINO ACID MOTIFS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL MEMBRANE; CHOLESTEROL; CRYSTALLOGRAPHY, X-RAY; HEMOLYSIN PROTEINS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; STREPTOCOCCUS PYOGENES; STREPTOLYSINS;

EID: 84893639595     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.11.020     Document Type: Article

References (51)

1. R.K. Tweten, M.W. Parker, and A.E. Johnson The cholesterol-dependent cytolysins F.G. van der Goot, Pore-forming toxins 2001 Springer Heidelberg, Germany 1 14
2. M.W. Parker, and S.C. Feil Pore-forming proteins: from structure to function Prog Biophys Mol Biol 88 2005 91 124
3. R.K. Tweten Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins (minireview) Infect Immun 73 2005 6199 6209 (Pubitemid 41368781)
4. E.M. Hotze, and R.K. Tweten Membrane assembly of the cholesterol- dependent cytolysin pore complex Biochim Biophys Acta 1818 2012 1028 1038
5. M.W. Cunningham Pathogenesis of group A streptococcal infections Clin Microbiol Rev 13 2000 470 511 (Pubitemid 30452618)
6. A. Håkansson, C.C. Bentley, E.A. Shakhnovic, and M.R. Wessels Cytolysin-dependent evasion of lysosomal killing Proc Natl Acad Sci USA 102 2005 5192 5197
7. L.K. Logsdon, A.P. Häkansson, G. Cortés, and M.R. Wessels Streptolysin O inhibits clathrin-dependent internalization of group A Streptococcus mBio 2 2011 10.1128/mBio.00332-10
8. J.C. Madden, N. Ruiz, and M. Caparon Cytolysin-mediated translocation (CMT): a functional equivalent of type III secretion in Gram-positive bacteria Cell 104 2001 143 152 (Pubitemid 32144979)
9. N. Magassa, S. Chandrasekaran, and M.G. Caparon Streptococcus pyogenes cytolysin-mediated translocation does not require pore formation by streptolysin O EMBO Rep 5 2010 400 405
10. M.A. Kehoe, and K.N. Timmins Cloning and expression in Escherichia coli of the streptolysin O determinant and demonstration of the absence of substantial homology with determinants from other thiol-activated toxins Infect Immun 43 1984 804 810
11. M.A. Kehoe, L. Miller, J.A. Walker, and G.J. Boulnais Nucleotide sequence of the streptolysin O (SLO) gene: structural homologies between SLO and other membrane-damaging thiol-activated toxins Infect Immun 55 1987 3228 3232 (Pubitemid 18008307)
12. D. Gerlach, W. Kohler, E. Gunther, and K. Mann Purification and characterization of streptolysin O secreted by Streptococcus equisimilis (group C) Infect Immun 61 1993 27227 27231
13. S. Bhakdi, H. Bayley, A. Valeva, I. Walev, B. Walker, and M. Kehoe et al. Staphylococcal alpha-toxin, streptolysin-O, and Escherichia coli hemolysin: prototypes of pore-forming bacterial cytolysins Arch Microbiol 165 1996 73 79 (Pubitemid 26081834)
14. U. Weller, L. Miller, M. Messner, M. Palmer, A. Valeva, and J. Tranum-Jensen et al. 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 1996 34 39 (Pubitemid 26074858)
15. M.A. Meehl, and M.G. Caparon Specificity of streptolysin O in cytolysin-mediated translocation Mol Microbiol 52 2004 1665 1676 (Pubitemid 38822676)
16. +-glycohydrolase acts as an intracellular toxin to enhance the extracellular survival of group A streptococci Mol Microbiol 44 2002 257 269 (Pubitemid 34429780)
17. R.R. Dourmashkin, and W.F. Rosse Morphologic changes in the membranes of red blood cells undergoing hemolysis Am J Med 41 1966 699 700
18. J.L. Duncan, and R. Schlegel Effect of streptolysin O on erythrocyte membranes, liposomes, and lipid dispersions. A protein-cholesterol interaction J Cell Biol 67 1975 160 174
19. E. Rosenqvist, T.E. Michaelsen, and A.I. Vistnes Effect on streptolysin O on egg lecithin/cholesterol vesicles Biochim Biophys Acta 600 1980 91 102 (Pubitemid 11192800)
20. L. Buckingham, and J.L. Duncan Approximate dimensions of membrane lesions produced by streptolysin S and streptolysin O Biochim Biophys Acta 729 1983 115 122 (Pubitemid 13084602)
21. S. Bhakdi, J. Tranum-Jensen, and A. Sziegoleit Mechanism of membrane damage by streptolysin-O Infect Immun 47 1985 52 60 (Pubitemid 15194590)
22. K. Sekiya, R. Satoh, H. Danbara, and Y. Futaesaku A ring shaped structure with a crown formed by streptolysin O on the erythrocyte membrane J Bacteriol 175 1993 5953 5961 (Pubitemid 23277444)
23. W. Niedermeyer Interaction of streptolysin-O with biomembranes: kinetic and morphological Toxicon 23 1985 425 439 (Pubitemid 15061508)
24. F. Hugo, J. Reichwein, M. Arvand, S. Kraemer, and S. Bhakdi Use of a monoclonal antibody to determine the mode of transmembrane pore formation by streptolysin O Infect Immun 54 1986 641 645 (Pubitemid 17186431)
25. K.S. Giddings, A.E. Johnson, and R.K. Tweten Redefining cholesterol's role in the mechanism of the cholesterol-dependent cytolysins Proc Natl Acad Sci USA 100 2003 11315 11320 (Pubitemid 37205932)
26. L.A. Shepard, A.P. Heuck, B.D. Hamman, J. Rossjohn, M.W. Parker, and K.R. Ryan 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 (Pubitemid 28489065)
27. J.P. Zeelen, J.K. Hiltunen, T.A. Ceska, and R.K. Wierenga Crystallisation experiments with 2-enoyl-CoA hydratase, using an automated "fast screening" crystallization protocol Acta Crystallogr Sect D Biol Crystallogr 50 1994 443 447
28. J.W. Plugrath The finer things in X-ray diffraction data collection Acta Crystallogr Sect D Biol Crystallogr 55 1999 1718 1725
29. B.W. Matthews Solvent content of protein crystals J Mol Biol 33 1968 491 497
30. A. Vagin, and A. Teplyakov MOLREP, an automated program for molecular replacement J Appl Crystallogr 30 1997 1022 1025 (Pubitemid 127485985)
31. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, and P.R. Evans et al. Overview of the CCP4 suite and current developments Acta Crystallogr Sect D Biol Crystallogr 67 2011 235 242
32. J. Rossjohn, S.C. Feil, W.J. McKinstry, R.K. Tweten, and M. Parker Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form Cell 89 1997 685 692 (Pubitemid 27516171)
33. J. Rossjohn, G. Polekhina, S.C. Feil, C.J. Morton, R.K. Tweten, and M.W. Parker Structures of perfringolysin O suggest a pathway for activation of cholesterol-dependent cytolysins J Mol Biol 367 2007 1227 1238
34. G. Polekhina, K.S. Giddings, R.K. Tweten, and M.W. Parker Insight into the action of the superfamily of cholesterol-dependent cytolysins from studies of intermedilysin Proc Natl Acad Sci USA 102 2005 600 605 (Pubitemid 40282711)
35. R.W. Bourdeau, E. Malito, A. Chenal, B.L. Bishop, M.W. Musch, and E.B.C. Villereal et al. Cellular functions and X-ray structure of anthrolysin O, a cholesterol-dependent cytolysin secreted by Bacillus anthracis J Biol Chem 284 2009 14645 14656
36. L. Xu, B. Huang, H. Du, X.C. Zhang, J. Xu, and Z. Rao Crystal structure of cytotoxin protein suilysin from Streptococcus suis Protein Cell 1 2010 96 105
37. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr Sect D Biol Crystallogr 60 2004 2126 2132 (Pubitemid 41742764)
38. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr Sect D Biol Crystallogr 53 1997 240 255 (Pubitemid 27235885)
39. P.D. Adams, R.W. Grosse-Kunstleve, L.W. Hung, T.R. Ioerger, A.J. McCoy, and N.W. Moriarty et al. PHENIX: building new software for automated crystallographic structure determination Acta Crystallogr Sect D Biol Crystallogr 58 2002 1948 1954 (Pubitemid 35337293)
40. R. Ramachandran, A.P. Heuck, R.K. Tweten, and A.E. Johnson Structural insights into the membrane-anchoring mechanism of a cholesterol-dependent cytolysin Nat Struct Mol Biol 9 2002 823 827 (Pubitemid 35257781)
41. C.E. Soltani, E.M. Hotze, A.E. Johnson, and R.K. Tweten Structural elements of the cholesterol-dependent cytolysins that are responsible for their cholesterol-sensitive membrane interactions Proc Natl Acad Sci USA 104 2007 20226 20231
42. A.J. Farrand, S. LaChapelle, E.M. Hotze, A.E. Johnson, and R.K. Tweten Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface Proc Natl Acad Sci USA 107 2010 4341 4346
43. E. Chiarot, C. Faralla, N. Chiappini, G. Tuscano, F. Falugi, and G. Gambellini et al. Targeted amino acid substitutions impair streptolysin O toxicity and group A Streptococcus virulence mBio 4 2013 e00387 e003912
44. W.S. Yang, S.-O. Park, A.-R. Yoon, J.Y. Yoo, M.K. Kim, and C.-O. Yun et al. Suicide cancer gene therapy using pore-forming toxin, streptolysin O Mol Cancer Ther 5 2006 1610 1619 (Pubitemid 44070499)
45. P.A. Keyel, R. Roth, W.M. Yokoyama, J.E. Heuser, and R.D. Salter Reduction of streptolysin O (SLO) pore-forming activity enhances inflammasome activation Toxins 5 2013 1105 1118
46. R.J. Gilbert Inactivation and activity of cholesterol-dependent cytolysins: what structural studies tell us Structure 13 2005 1097 1106 (Pubitemid 41111478)
47. A.S. Solovyoya, M. Noellmann, T.J. Mitchell, and O. Byron The solution structure and oligomerization behaviour of two bacterial toxins: pneumolysin and perfringolysin O Biophys J 87 2004 540 552 (Pubitemid 38880107)
48. B.B. Johnson, P.C. Moe, Y. Chang, D. Wang, K. Rossi, and B.L. Trigatti et al. Modifications in perfringolysin O domain 4 alter the threshold of cholesterol concentration required for binding Biochemistry 51 2012 3373 3382
49. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, and E. Villa et al. Scalable molecular dynamics with NAMD J Comput Chem 26 2005 1781 1802 (Pubitemid 43078511)
50. K.J. Dowd, A.J. Farrand, and R.K. Tweten The cholesterol-dependent cytolysin signature motif: a critical element in the allosteric pathway that couples membrane binding to pore assembly PLoS Pathog 8 2012 e1002787
51. C.N. Pace, B.A. Shirley, M. McNutt, and K. Gajiwala Forces contributing to the conformational stability of proteins FASEB J 10 1996 75 83 (Pubitemid 26035509)