The cholesterol-dependent cytolysin signature motif: A critical element in the allosteric pathway that couples membrane binding to pore assembly

PLoS Pathogens

Volumn 8, Issue 7, 2012, Pages 44-

  Dowd, Kelley J ^a   Tweten, Rodney K ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CD59 ANTIGEN; CLOSTRIDIUM PERFRINGENS TOXIN; CYTOLYSIN; INTERMEDILYSIN; LYSINE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BACTERIAL TOXIN; BACTERIOCIN; CHOLESTEROL; CLOSTRIDIUM PERFRINGENS THETA TOXIN; CLOSTRIDIUM PERFRINGENS THETA-TOXIN; CYTOTOXIN; HEMOLYSIN; INTERMEDILYSIN PROTEIN, STREPTOCOCCUS INTERMEDIUS;

ARTICLE; CHEMICAL STRUCTURE; FLUORESCENCE SPECTROSCOPY; GENE MUTATION; HUMAN; MEMBRANE BINDING; ALLOSTERISM; BINDING SITE; CELL MEMBRANE; CHEMISTRY; CLOSTRIDIUM PERFRINGENS; ERYTHROCYTE; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE;

BACTERIA (MICROORGANISMS); POSIBACTERIA;

ALLOSTERIC REGULATION; AMINO ACID MOTIFS; BACTERIAL PROTEINS; BACTERIAL TOXINS; BACTERIOCINS; BINDING SITES; CELL MEMBRANE; CHOLESTEROL; CLOSTRIDIUM PERFRINGENS; CYTOTOXINS; ERYTHROCYTES; HEMOLYSIN PROTEINS; HUMANS; PROTEIN STRUCTURE, TERTIARY;

EID: 84864593970     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002787     Document Type: Article

References (58)

1. Alouf JE, Billington SJ, Jost BH, (2005) Repertoire and general features of the cholesterol-dependent cytolysins. In: Alouf JE, Popoff MR, editors. Bacterial Toxins: A Comprehensive Sourcebook. 3rd edition London Academic Press pp. 643-658.
2. Calbo E, Garau J, (2011) Factors affecting the development of systemic inflammatory response syndrome in pneumococcal infections. Curr Opin Infect Dis 24: 241-247.
3. Keyel PA, Heid ME, Salter RD, (2011) Macrophage responses to bacterial toxins: a balance between activation and suppression. Immunol Res 50: 118-123.
4. Mostowy S, Cossart P, (2012) Virulence factors that modulate the cell biology of Listeria infection and the host response. Adv Immunol 113: 19-32.
5. Tweten RK, Caparon M, (2005) Injectosomes of the Gram Positive Bacteria. In: Hultgren SJ, Caparon M, Waksman G, editors. Structural Basis of Bacterial Pathogenesis Washington, D.C. American Society of Microbiology pp. 223-240.
6. Polekhina G, Giddings KS, Tweten RK, Parker MW, (2005) Insights into the action of the superfamily of cholesterol-dependent cytolysins from studies of intermedilysin. Proc Natl Acad Sci U S A 102: 600-605.
7. Rossjohn J, Feil SC, McKinstry WJ, Tweten RK, Parker MW, (1997) Structure of a cholesterol-binding thiol-activated cytolysin and a model of its membrane form. Cell 89: 685-692.
8. Xu L, Huang B, Du H, Zhang XC, Xu J, et al. (2010) Crystal structure of cytotoxin protein suilysin from Streptococcus suis. Protein Cell 1: 96-105.
9. Bourdeau RW, Malito E, Chenal A, Bishop BL, Musch MW, et al. (2009) Cellular functions and X-ray structure of anthrolysin O, a cholesterol-dependent cytolysin secreted by Bacillus anthracis. J Biol Chem 284: 14645-14656.
10. Saunders FK, Mitchell TJ, Walker JA, Andrew PW, Boulnois GJ, (1989) Pneumolysin, the thiol-activated toxin of Streptococcus pneumoniae, does not require a thiol group for in vitro activity. Infect Immun 57: 2547-2552.
11. Pinkney M, Beachey E, Kehoe M, (1989) The thiol-activated toxin streptolysin O does not require a thiol group for activity. Infect Immun 57: 2553-2558.
12. Michel E, Reich KA, Favier R, Berche P, Cossart P, (1990) Attenuated mutants of the intracellular bacterium Listeria monocytogenes obtained by single amino acid substitutions in listeriolysin O. Mol Microbiol 4: 2167-2178.
13. Sekino-Suzuki N, Nakamura M, Mitsui KI, Ohno-Iwashita Y, (1996) Contribution of individual tryptophan residues to the structure and activity of theta-toxin (perfringolysin o), a cholesterol-binding cytolysin. Eur J Biochem 241: 941-947.
14. Korchev YE, Bashford CL, Pederzolli C, Pasternak CA, Morgan PJ, et al. (1998) A Conserved Tryptophan In Pneumolysin Is a Determinant Of the Characteristics Of Channels Formed By Pneumolysin In Cells and Planar Lipid Bilayers. Biochem J 329: 571-577.
15. Billington SJ, Songer JG, Jost BH, (2002) The variant undecapeptide sequence of the Arcanobacterium pyogenes haemolysin, pyolysin, is required for full cytolytic activity. Microbiology 148: 3947-3954.
16. Iwamoto M, Ohno-Iwashita Y, Ando S, (1987) Role of the essential thiol group in the thiol-activated cytolysin from Clostridium perfringens. Eur J Biochem 167: 425-430.
17. Tweten RK, (2005) The cholesterol-dependent cytolysins; a family of versatile pore-forming toxins. Infect Immun 73: 6199-6209.
18. Nakamura M, Sekino N, Iwamoto M, Ohno-Iwashita Y, (1995) Interaction of theta-toxin (perfringolysin O), a cholesterol-binding cytolysin, with liposomal membranes: change in the aromatic side chains upon binding and insertion. Biochemistry 34: 6513-6520.
19. Ramachandran R, Heuck AP, Tweten RK, Johnson AE, (2002) Structural insights into the membrane-anchoring mechanism of a cholesterol-dependent cytolysin. Nat Struct Biol 9: 823-827.
20. Heuck AP, Hotze E, Tweten RK, Johnson AE, (2000) Mechanism of membrane insertion of a multimeric b-barrel protein: Perfringolysin O creates a pore using ordered and coupled conformational changes. Molec Cell 6: 1233-1242.
21. Heuck AP, Tweten RK, Johnson AE, (2003) Assembly and topography of the prepore complex in cholesterol-dependent cytolysins. J Biol Chem 278: 31218-31225.
22. Farrand AJ, LaChapelle S, Hotze EM, Johnson AE, Tweten RK, (2010) Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface. Proc Natl Acad Sci U S A 107: 4341-4346.
23. Czajkowsky DM, Hotze EM, Shao Z, Tweten RK, (2004) Vertical collapse of a cytolysin prepore moves its transmembrane β-hairpins to the membrane. EMBO J 23: 3206-3215.
24. Ramachandran R, Tweten RK, Johnson AE, (2005) The domains of a cholesterol-dependent cytolysin undergo a major FRET-detected rearrangement during pore formation. Proc Natl Acad Sci U S A 102: 7139-7144.
25. Ramachandran R, Tweten RK, Johnson AE, (2004) Membrane-dependent conformational changes initiate cholesterol-dependent cytolysin oligomerization and intersubunit β-strand alignment. Nat Struct Mol Biol 11: 697-705.
26. Shatursky O, Heuck AP, Shepard LA, Rossjohn J, Parker MW, et al. (1999) The mechanism of membrane insertion for a cholesterol dependent cytolysin: A novel paradigm for pore-forming toxins. Cell 99: 293-299.
27. Shepard LA, Heuck AP, Hamman BD, Rossjohn J, Parker MW, et al. (1998) Identification of a membrane-spanning domain of the thiol-activated pore-forming toxin Clostridium perfringens perfringolysin O: an α-helical to β-sheet transition identified by fluorescence spectroscopy. Biochemistry 37: 14563-14574.
28. Feil SC, Rossjohn J, Rohde K, Tweten RK, Parker MW, (1996) Crystallization and preliminary X-ray analysis of a thiol-activated cytolysin. FEBS Lett 397: 290-292.
29. Giddings KS, Zhao J, Sims PJ, Tweten RK, (2004) Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nat Struct Mol Biol 11: 1173-1178.
30. Wickham SE, Hotze EM, Farrand AJ, Polekhina G, Nero TL, et al. (2011) Mapping the intermedilysin-human CD59 receptor interface reveals a deep correspondence with the binding site on CD59 for complement binding proteins C8alpha and C9. J Biol Chem 286: 20952-20962.
31. Gelber SE, Aguilar JL, Lewis KL, Ratner AJ, (2008) Functional and phylogenetic characterization of Vaginolysin, the human-specific cytolysin from Gardnerella vaginalis. J Bacteriol 190: 3896-3903.
32. Soltani CE, Hotze EM, Johnson AE, Tweten RK, (2007) Specific protein-membrane contacts are required for prepore and pore assembly by a cholesterol-dependent cytolysin. J Biol Chem 282: 15709-15716.
33. LaChapelle S, Tweten RK, Hotze EM, (2009) Intermedilysin-receptor interactions during assembly of the pore complex: assembly intermediates increase host cell susceptibility to complement-mediated lysis. J Biol Chem 284: 12719-12726.
34. Nakamura M, Sekino-Suzuki N, Mitsui K, Ohno-Iwashita Y, (1998) Contribution of tryptophan residues to the structural changes in perfringolysin O during interaction with liposomal membranes. J Biochem (Tokyo) 123: 1145-1155.
35. Hotze EM, Heuck AP, Czajkowsky DM, Shao Z, Johnson AE, et al. (2002) Monomer-monomer interactions drive the prepore to pore conversion of a beta-barrel-forming cholesterol-dependent cytolysin. J Biol Chem 277: 11597-11605.
36. Shepard LA, Shatursky O, Johnson AE, Tweten RK, (2000) The mechanism of assembly and insertion of the membrane complex of the cholesterol-dependent cytolysin perfringolysin O: Formation of a large prepore complex. Biochemistry 39: 10284-10293.
37. Harris RW, Sims PJ, Tweten RK, (1991) Kinetic aspects of the aggregation of Clostridium perfringens theta toxin on erythrocyte membranes: A fluorescence energy transfer study. J Biol Chem 266: 6936-6941.
38. Haugland RP, (2010) The Molecular Probes Handbook: A Guide to Fluorescent Probes and Labeling Technologies. 11th edition Life Technologies.
39. Chen RF, Knutson JR, (1988) Mechanism of fluorescence concentration quenching of carboxyfluorescein in liposomes: energy transfer to nonfluorescent dimers. Anal Biochem 172: 61-77.
40. Rex S, Schwarz G, (1998) Quantitative studies on the melittin-induced leakage mechanism of lipid vesicles. Biochemistry 37: 2336-2345.
41. Schlesinger PH, Saito M, (2006) The Bax pore in liposomes, Biophysics. Cell Death Differ 13: 1403-1408.
42. Giddings KS, Johnson AE, Tweten RK, (2003) Redefining cholesterol's role in the mechanism of the cholesterol-dependent cytolysins. Proc Natl Acad Sci U S A 100: 11315-11320.
43. Xu L, Huang B, Du H, Zhang XC, Xu J, et al. (2010) Crystal structure of cytotoxin protein suilysin from Streptococcus suis. Protein Cell 1: 96-105.
44. Hotze EM, Wilson-Kubalek EM, Rossjohn J, Parker MW, Johnson AE, et al. (2001) 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: 8261-8268.
45. Farrand S, Hotze E, Friese P, Hollingshead SK, Smith DF, et al. (2008) Characterization of a streptococcal cholesterol-dependent cytolysin with a lewis y and b specific lectin domain. Biochemistry 47: 7097-7107.
46. Wickham SE, Hotze EM, Farrand AJ, Polekhina G, Nero TL, et al. (2011) Mapping the Intermedilysin-Human CD59 Receptor Interface Reveals a Deep Correspondence with the Binding Site on CD59 for Complement Binding Proteins C8alpha and C9. J Biol Chem 286: 20952-20962.
47. Hadders MA, Beringer DX, Gros P, (2007) Structure of C8alpha-MACPF reveals mechanism of membrane attack in complement immune defense. Science 317: 1552-1554.
48. Rosado CJ, Buckle AM, Law RH, Butcher RE, Kan WT, et al. (2007) A common fold mediates vertebrate defense and bacterial attack. Science 317: 1548-1551.
49. Slade DJ, Lovelace LL, Chruszcz M, Minor W, Lebioda L, et al. (2008) Crystal structure of the MACPF domain of human complement protein C8 alpha in complex with the C8 gamma subunit. J Mol Biol 379: 331-342.
50. Law RH, Lukoyanova N, Voskoboinik I, Caradoc-Davies TT, Baran K, et al. (2010) The structural basis for membrane binding and pore formation by lymphocyte perforin. Nature 468: 447-451.
51. Lovelace LL, Cooper CL, Sodetz JM, Lebioda L, (2011) Structure of human C8 protein provides mechanistic insight into membrane pore formation by complement. J Biol Chem 286: 17585-17592.
52. Kafsack BF, Pena JD, Coppens I, Ravindran S, Boothroyd JC, et al. (2009) Rapid membrane disruption by a perforin-like protein facilitates parasite exit from host cells. Science 323: 530-533.
53. Kadota K, Ishino T, Matsuyama T, Chinzei Y, Yuda M, (2004) Essential role of membrane-attack protein in malarial transmission to mosquito host. Proc Natl Acad Sci U S A 101: 16310-16315.
54. Kaiser K, Camargo N, Coppens I, Morrisey JM, Vaidya AB, et al. (2004) A member of a conserved Plasmodium protein family with membrane-attack complex/perforin (MACPF)-like domains localizes to the micronemes of sporozoites. Mol Biochem Parasitol 133: 15-26.
55. Ishino T, Chinzei Y, Yuda M, (2005) A Plasmodium sporozoite protein with a membrane attack complex domain is required for breaching the liver sinusoidal cell layer prior to hepatocyte infection. Cell Microbiol 7: 199-208.
56. Soltani CE, Hotze EM, Johnson AE, Tweten RK, (2007) Structural elements of the cholesterol-dependent cytolysins that are responsible for their cholesterol-sensitive membrane interactions. Proc Natl Acad Sci U S A 104: 20226-20231.
57. Tilley SJ, Orlova EV, Gilbert RJ, Andrew PW, Saibil HR, (2005) Structural basis of pore formation by the bacterial toxin pneumolysin. Cell 121: 247-256.
58. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38.