Assembly of streptolysin O pores assessed by quartz crystal microbalance and atomic force microscopy provides evidence for the formation of anchored but incomplete oligomers

Biochimica et Biophysica Acta - Biomembranes

Volumn , Issue Part A, 2015, Pages 115-126

  Stewart, Sarah E ^a   D'Angelo, Michael E ^a   Piantavigna, Stefania ^a   Tabor, Rico F ^a   Martin, Lisandra L ^a   Bird, Phillip I ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Atomic force microscopy; Bacterial toxin; Cholesterol dependent cytolysin; Pore; Quartz crystal microbalance; Streptolysin O

Indexed keywords

CELL PENETRATING PEPTIDE; CHOLESTEROL; MUTANT PROTEIN; OLIGOMER; STREPTOLYSIN O; BACTERIAL PROTEIN; DIMYRISTOYLPHOSPHATIDYLCHOLINE; LIPID BILAYER; MEMBRANE LIPID; PROTEIN BINDING; STREPTOLYSIN;

ADSORPTION KINETICS; ARTICLE; ATOMIC FORCE MICROSCOPY; CHANNEL GATING; ISOTHERM; LIPID BILAYER; MEMBRANE BINDING; NONHUMAN; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; QUARTZ CRYSTAL MICROBALANCE; VISCOELASTICITY; WILD TYPE; ANIMAL; BIOLOGICAL MODEL; CELL MEMBRANE; CHEMISTRY; GENETICS; KINETICS; METABOLISM; MUTATION; PROCEDURES; PROTEIN MULTIMERIZATION; SHEEP;

ANIMALS; BACTERIAL PROTEINS; CELL MEMBRANE; CHOLESTEROL; DIMYRISTOYLPHOSPHATIDYLCHOLINE; KINETICS; LIPID BILAYERS; MEMBRANE LIPIDS; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; QUARTZ CRYSTAL MICROBALANCE TECHNIQUES; SHEEP; STREPTOLYSINS;

EID: 84908200578     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2014.10.012     Document Type: Article

References (36)

1. E.M. Hotze, and R.K. Tweten Membrane assembly of the cholesterol-dependent cytolysin pore complex Biochim. Biophys. Acta 1818 2012 1028 1038
2. 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. 107 2010 4341 4346
3. Y. Ohno-Iwashita, M. Iwamoto, K. Mitsui, S. Ando, and S. Iwashita A cytolysin, theta-toxin, preferentially binds to membrane cholesterol surrounded by phospholipids with 18-carbon hydrocarbon chains in cholesterol-rich region J. Biochem. 110 1991 369 375
4. E.M. Hotze, E. Wilson-Kubalek, A.J. Farrand, L. Bentsen, M.W. Parker, A.E. Johnson, and R.K. Tweten Monomer-monomer interactions propagate structural transitions necessary for pore formation by the cholesterol-dependent cytolysins J. Biol. Chem. 287 2012 24534 24543
5. M. Palmer, I. Vulicevic, P. Saweljew, A. Valeva, M. Kehoe, and S. Bhakdi Streptolysin O: a proposed model of allosteric interaction between a pore-forming protein and its target lipid bilayer † Biochemistry 37 1998 2378 2383
6. E.M. Abdel Ghani, S. Weis, I. Walev, M. Kehoe, S. Bhakdi, and M. Palmer Streptolysin O: inhibition of the conformational change during membrane binding of the monomer prevents oligomerization and pore formation † Biochemistry 38 1999 15204 15211
7. D.M. Czajkowsky, E.M. Hotze, Z. Shao, and R.K. Tweten Vertical collapse of a cytolysin prepore moves its transmembrane beta-hairpins to the membrane EMBO J. 23 2004 3206 3215
8. L.A. Shepard, O. Shatursky, A.E. Johnson, and R.K. Tweten 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
9. E.M. Hotze, E.M. Wilson-Kubalek, J. Rossjohn, M.W. Parker, A.E. Johnson, and R.K. Tweten 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
10. N. Magassa, S. Chandrasekaran, and M.G. Caparon Streptococcus pyogenes cytolysin-mediated translocation does not require pore formation by streptolysin O EMBO Rep. 11 2010 400 405
11. S. Bhakdi, J. Tranum-Jensen, and A. Sziegoleit Mechanism of membrane damage by streptolysin-O Infect. Immun. 47 1985 52 60
12. K. Sekiya, H. Danbara, and Y. Futaesaku [Mechanism of pore formation on erythrocyte membrane by streptolysin-O] Kansenshogaku Zasshi 67 1993 736 740
13. M. Walch, U. Ziegler, and P. Groscurth Effect of streptolysin O on the microelasticity of human platelets analyzed by atomic force microscopy Ultramicroscopy 82 2000 259 267
14. W. Niedermeyer Interaction of streptolysin-O with biomembranes: kinetic and morphological studies on erythrocyte membranes Toxicon 23 1985 425 439
15. I. Walev, S.C. Bhakdi, F. Hofmann, N. Djonder, A. Valeva, K. Aktories, and S. Bhakdi Delivery of proteins into living cells by reversible membrane permeabilization with streptolysin-O Proc. Natl. Acad. Sci. U. S. A. 98 2001 3185 3190
16. S. Bhakdi, U. Weller, I. Walev, E. Martin, D. Jonas, and M. Palmer A guide to the use of pore-forming toxins for controlled permeabilization of cell membranes Med. Microbiol. Immunol. 182 1993 167 175
17. T. Wilkop, D. Xu, and Q. Cheng Characterization of pore formation by streptolysin O on supported lipid membranes by impedance spectroscopy and surface plasmon resonance spectroscopy Langmuir 23 2007 1403 1409
18. H. Helmholz Selective toxin-lipid membrane interactions of natural, haemolytic Scyphozoan toxins analyzed by surface plasmon resonance Biochim. Biophys. Acta 1798 2010 1944 1952
19. J.R. Harris, M. Adrian, S. Bhakdi, and M. Palmer Cholesterol-streptolysin O interaction: an em study of wild-type and mutant streptolysin O J. Struct. Biol. 121 1998 343 355
20. M. Palmer, R. Harris, C. Freytag, M. Kehoe, J. Tranum-Jensen, and S. Bhakdi 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 J. 17 1998 1598 1605
21. U. Weller, L. Muller, M. Messner, M. Palmer, A. Valeva, J. Tranum-Jensen, P. Agrawal, C. Biermann, A. Dobereiner, M.A. Kehoe, and S. Bhakdi 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
22. M. Palmer, A. Valeva, M. Kehoe, and S. Bhakdi Kinetics of streptolysin O self-assembly Eur. J. Biochem. 231 1995 388 395
23. S.E. Stewart, S.C. Kondos, A.Y. Matthews, M.E. D'Angelo, M.A. Dunstone, J.C. Whisstock, J.A. Trapani, and P.I. Bird The perforin pore facilitates the delivery of cationic cargos J. Biol. Chem. 289 2014 9172 9181
24. S. Piantavigna, G.A. McCubbin, S. Boehnke, B. Graham, L. Spiccia, and L.L. Martin A mechanistic investigation of cell-penetrating Tat peptides with supported lipid membranes Biochim. Biophys. Acta 1808 2011 1811 1817
25. A. Mechler, S. Praporski, S. Piantavigna, S.M. Heaton, K.N. Hall, M.I. Aguilar, and L.L. Martin Structure and homogeneity of pseudo-physiological phospholipid bilayers and their deposition characteristics on carboxylic acid terminated self-assembled monolayers Biomaterials 30 2009 682 689
26. G. Sauerbrey Verwendung von Schwingquarzen zur Wägung dünner Schichten und zur Mikrowägung Z. Phys. 155 1959 206 222
27. R.F. Tabor, J. Eastoe, and P.J. Dowding A two-step model for surfactant adsorption at solid surfaces J. Colloid Interface Sci. 346 2010 424 428
28. L.H. Torn, L.K. Koopal, A. de Keizer, and J. Lyklema Adsorption of nonionic surfactants on cellulose surfaces: adsorbed amounts and kinetics Langmuir 21 2005 7768 7775
29. G.A. McCubbin, S. Praporski, S. Piantavigna, D. Knappe, R. Hoffmann, J.H. Bowie, F. Separovic, and L.L. Martin QCM-D fingerprinting of membrane-active peptides Eur. Biophys. J. 40 2011 437 446
30. R. Ramachandran, R.K. Tweten, and A.E. Johnson Membrane-dependent conformational changes initiate cholesterol-dependent cytolysin oligomerization and intersubunit beta-strand alignment Nat. Struct. Mol. Biol. 11 2004 697 705
31. A. Mechler, S. Praporski, K. Atmuri, M. Boland, F. Separovic, and L.L. Martin Specific and selective peptide-membrane interactions revealed using quartz crystal microbalance Biophys. J. 93 2007 3907 3916
32. A.P. Heuck, E.M. Hotze, R.K. Tweten, and A.E. Johnson 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
33. J.J. Flanagan, R.K. Tweten, A.E. Johnson, and A.P. Heuck Cholesterol exposure at the membrane surface is necessary and sufficient to trigger perfringolysin O binding Biochemistry 48 2009 3977 3987
34. T. Wilkop, D. Xu, and Q. Cheng Electrochemical characterization of pore formation by bacterial protein toxins on hybrid supported membranes Langmuir 24 2008 5615 5621
35. F. Hugo, J. Reichwein, M. Arvand, S. Kramer, 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
36. R.J. Gilbert Inactivation and activity of cholesterol-dependent cytolysins: what structural studies tell us Structure 13 2005 1097 1106