Phospholipid hydrolysis caused by clostridium perfringens α-toxin facilitates the targeting of perfringolysin O to membrane bilayers

Biochemistry

Volumn 49, Issue 44, 2010, Pages 9498-9507

  Moe, Paul C ^a   Heuck, Alejandro P ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLOSTRIDIUM PERFRINGENS; EXTRACELLULAR PROTEINS; FREE CHOLESTEROLS; GAS GANGRENE; GASTROINTESTINAL DISEASE; MEMBRANE BILAYERS; PHOSPHATIDYLCHOLINE; PHOSPHOCHOLINE; PORE FORMATION; SPHINGOMYELIN; TARGET CELLS; TRANS-MEMBRANE PORES;

CHOLESTEROL; CLOSTRIDIUM; MEMBRANES; PATHOLOGY; PHOSPHOLIPIDS;

TOXIC MATERIALS;

CHOLESTEROL; CLOSTRIDIUM PERFRINGENS ALPHA TOXIN; CLOSTRIDIUM PERFRINGENS TOXIN; CLOSTRIDIUM TOXIN; PHOSPHATIDYLCHOLINE; PHOSPHOLIPID; UNCLASSIFIED DRUG;

ARTICLE; BILAYER MEMBRANE; CELL MEMBRANE; CLOSTRIDIUM PERFRINGENS; CYTOLYSIS; LIPID HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

BACTERIAL PROTEINS; BACTERIAL TOXINS; CALCIUM-BINDING PROTEINS; CHOLESTEROL; CLOSTRIDIUM PERFRINGENS; GAS GANGRENE; HEMOLYSIN PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; HYDROLYSIS; LIPOSOMES; MODELS, MOLECULAR; PHOSPHOLIPIDS; PROTEIN BINDING; TYPE C PHOSPHOLIPASES;

CLOSTRIDIUM PERFRINGENS;

EID: 78149343950     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1013886     Document Type: Article

References (90)

1. Hickey, M. J., Kwan, R. Y. Q., Awad, M. M., Kennedy, C. L., Young, L. F., Hall, P., Cordner, L. M., Lyras, D., Emmins, J. J., and Rood, J. I. (2008) Molecular and cellular basis of microvascular perfusion deficits induced by Clostridium perfringens and Clostridium septicum PLoS Pathogens 4, e1000045
2. Bryant, A. E. and Stevens, D. L. (2006) Clostridial toxins in the pathogenesis of gas gangrene, in The comprehensive sourcebook of bacterial protein toxins (Alouf, J. E. and Popoff, M. R., Eds.) pp 919-929, Academic Press, New York.
3. Awad, M. M., Bryant, A. E., Stevens, D. L., and Rood, J. I. (1995) Virulence studies on chromosomal alpha-toxin and theta-toxin mutants constructed by allelic exchange provide genetic evidence for the essential role of alpha-toxin in Clostridium perfringens -mediated gas gangrene Mol. Microbiol. 15, 191-202
4. Bunting, M., Lorant, D. E., Bryant, A. E., Zimmerman, G. A., McIntyre, T. M., Stevens, D. L., and Prescott, S. M. (1997) Alpha toxin from Clostridium perfringens induces proinflammatory changes in endothelial cells J. Clin. Invest. 100, 565-574
5. Ochi, S., Miyawaki, T., Matsuda, H., Oda, M., Nagahama, M., and Sakurai, J. (2002) Clostridium perfringens alpha-toxin induces rabbit neutrophil adhesion Microbiology 148, 237-245
6. Naylor, C. E., Eaton, J. T., Howells, A., Justin, N., Moss, D. S., Titball, R. W., and Basak, A. K. (1998) Structure of the key toxin in gas gangrene Nat. Struct. Biol. 5, 738-746
7. Tweten, R. K. (2005) Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins Infect. Immun. 73, 6199-6209
8. Gilbert, R. J. (2010) Cholesterol-dependent cytolysins Adv. Exp. Med. Biol. 677, 56-66
9. Heuck, A. P., Moe, P. C., and Johnson, B. B. (2010) The cholesterol-dependent cytolysins family of Gram-positive bacterial toxins, in Cholesterol binding proteins and cholesterol transport (Harris, J. R., Ed.) pp 551-577, Springer, New York.
10. Heuck, A. P., Tweten, R. K., and Johnson, A. E. (2001) Beta-barrel pore-forming toxins: Intriguing dimorphic proteins Biochemistry 40, 9065-9073
11. Flanagan, J. J., Tweten, R. K., Johnson, A. E., and Heuck, A. P. (2009) Cholesterol exposure at the membrane surface is necessary and sufficient to trigger perfringolysin O binding Biochemistry 48, 3977-3987
12. Soltani, C. E., Hotze, E. M., Johnson, A. E., and Tweten, R. K. (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
13. Soltani, C. E., Hotze, E. M., Johnson, A. E., and Tweten, R. K. (2007) Specific protein-membrane contacts are required for prepore and pore assembly by a cholesterol-dependent cytolysin J. Biol. Chem. 282, 15709-15716
14. Giddings, K. S., Johnson, A. E., and Tweten, R. K. (2003) Redefining cholesterol's role in the mechanism of the cholesterol-dependent cytolysins Proc. Natl. Acad. Sci. U.S.A. 100, 11315-11320
15. Ramachandran, R., Heuck, A. P., Tweten, R. K., and Johnson, A. E. (2002) Structural insights into the membrane-anchoring mechanism of a cholesterol-dependent cytolysin Nat. Struct. Mol. Biol. 9, 823-827
16. Heuck, A. P., Hotze, E. M., Tweten, R. K., and Johnson, A. E. (2000) Mechanism of membrane insertion of a multimeric β-barrel protein: Perfringolysin O creates a pore using ordered and coupled conformational changes Mol. Cell 6, 1233-1242
17. Hotze, E. M., Wilson-Kubalek, E. M., Rossjohn, J., Parker, M. W., Johnson, A. E., and Tweten, R. K. (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
18. Shepard, L. A., Shatursky, O., Johnson, A. E., and Tweten, R. K. (2000) 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, 10284-10293
19. Shatursky, O., Heuck, A. P., Shepard, L. A., Rossjohn, J., Parker, M. W., Johnson, A. E., and Tweten, R. K. (1999) The mechanism of membrane insertion for a cholesterol-dependent cytolysin: A novel paradigm for pore-forming toxins Cell 99, 293-299
20. Shepard, L. A., Heuck, A. P., Hamman, B. D., Rossjohn, J., Parker, M. W., Ryan, K. R., Johnson, A. E., and Tweten, R. K. (1998) 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, 14563-14574
21. Czajkowsky, D. M., Hotze, E. M., Shao, Z., and Tweten, R. K. (2004) Vertical collapse of a cytolysin prepore moves its transmembrane beta-hairpins to the membrane EMBO J. 23, 3206-3215
22. Dang, T. X., Hotze, E. M., Rouiller, I., Tweten, R. K., and Wilson-Kubalek, E. M. (2005) Prepore to pore transition of a cholesterol-dependent cytolysin visualized by electron microscopy J. Struct. Biol. 150, 100-108
23. Farrand, A. J., LaChapelle, S., Hotze, E. M., Johnson, A. E., and Tweten, R. K. (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
24. Ramachandran, R., Tweten, R. K., and Johnson, A. E. (2004) Membrane-dependent conformational changes initiate cholesterol-dependent cytolysin oligomerization and intersubunit beta-strand alignment Nat. Struct. Mol. Biol. 11, 697-705
25. Awad, M. M., Ellemor, D. M., Boyd, R. L., Emmins, J. J., and Rood, J. I. (2001) Synergistic effects of alpha-toxin and perfringolysin O in Clostridium perfringens -mediated gas gangrene Infect. Immun. 69, 7904-7910
26. Heuck, A. P. and Johnson, A. E. (2005) Membrane recognition and pore formation by bacterial pore-forming toxins, in Protein-lipid interactions. From membrane domains to cellular networks (Tamm, L. K., Ed.) pp 163-186, Wiley-VCH, Weinheim.
27. Radhakrishnan, A. and McConnell, H. M. (1999) Condensed complexes of cholesterol and phospholipids Biophys. J. 77, 1507-1517
28. Huang, J. and Feigenson, G. W. (1999) A microscopic interaction model of maximum solubility of cholesterol in lipid bilayers Biophys. J. 76, 2142-2157 (Pubitemid 29266367)
29. Heuck, A. P., Savva, C. G., Holzenburg, A., and Johnson, A. E. (2007) Conformational changes that effect oligomerization and initiate pore formation are triggered throughout perfringolysin O upon binding to cholesterol J. Biol. Chem. 282, 22629-22637
30. Nelson, L. D., Johnson, A. E., and London, E. (2008) How interaction of perfringolysin O with membranes is controlled by sterol structure, lipid structure, and physiological low pH: Insights into the origin of perfringolysin O-lipid raft interaction J. Biol. Chem. 283, 4632-4642
31. Moore, N. F., Patzer, E. J., Barenholz, Y., and Wagner, R. R. (1977) Effect of phospholipase C and cholesterol oxidase on membrane integrity, microviscosity, and infectivity of vesicular stomatitis virus Biochemistry 16, 4708-4715
32. Patzer, E. J. and Wagner, R. R. (1978) Cholesterol oxidase as a probe for studying membrane organisation Nature 274, 394-395
33. Ali, M. R., Cheng, K. H., and Huang, J. (2007) Assess the nature of cholesterol-lipid interactions through the chemical potential of cholesterol in phosphatidylcholine bilayers Proc. Natl. Acad. Sci. U.S.A. 104, 5372-5377
34. Ohvo, H. and Slotte, J. P. (1996) Cyclodextrin-mediated removal of sterols from monolayers: Effects of sterol structure and phospholipids on desorption rate Biochemistry 35, 8018-8024
35. Radhakrishnan, A. and McConnell, H. M. (2000) Chemical activity of cholesterol in membranes Biochemistry 39, 8119-8124
36. Leventis, R. and Silvius, J. R. (2001) Use of cyclodextrins to monitor transbilayer movement and differential lipid affinities of cholesterol Biophys. J. 81, 2257-2267
37. Lange, Y. and Steck, T. L. (2008) Cholesterol homeostasis and the escape tendency (activity) of plasma membrane cholesterol Prog. Lipid Res. 47, 319-332
38. Sokolov, A. and Radhakrishnan, A. (2010) Accessibility of cholesterol in endoplasmic reticulum (ER) membranes and activation of SREBP-2 switch abruptly at a common cholesterol threshold. J. Biol. Chem. 285, 29480-29490.
39. O'Brien, D. K. and Melville, S. B. (2000) The anaerobic pathogen Clostridium perfringens can escape the phagosome of macrophages under aerobic conditions Cell. Microbiol. 2, 505-519
40. O'Brien, D. K. and Melville, S. B. (2004) Effects of Clostridium perfringens alpha-toxin (PLC) and perfringolysin O (PFO) on cytotoxicity to macrophages, on escape from the phagosomes of macrophages, and on persistence of C. perfringens in host tissues Infect. Immun. 72, 5204-5215
41. Vazquez-Boland, J. A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., Gonzalez-Zorn, B., Wehland, J., and Kreft, J. (2001) Listeria pathogenesis and molecular virulence determinants Clin. Microbiol. Rev. 14, 584-640
42. Schnupf, P. and Portnoy, D. A. (2007) Listeriolysin O: A phagosome-specific lysin Microb. Infect. 9, 1176-1187
43. Heuck, A. P., Tweten, R. K., and Johnson, A. E. (2003) Assembly and topography of the prepore complex in cholesterol-dependent cytolysins J. Biol. Chem. 278, 31218-31225
44. Mayer, L. D., Hope, M. J., and Cullis, P. R. (1986) Vesicles of variable sizes produced by a rapid extrusion procedure Biochim. Biophys. Acta 858, 161-168
45. Ye, J., Esmon, N. L., Esmon, C. T., and Johnson, A. E. (1991) The active site of thrombin is altered upon binding to thrombomodulin: Two distinct structural changes are detected by fluorescence, but only one correlates with protein C activation J. Biol. Chem. 266, 23016-23021
46. Jameson, D. M., Croney, J. C., Moens, P. D. J., Gerard, Marriott, and Ian, P. (2003) Fluorescence: Basic concepts, practical aspects, and some anecdotes Methods Enzymol. 360, 1-43
47. Pace, C. N. and Scholtz, J. M. (1989) Measuring conformational stability of a protein, in Protein structure: A practical approach (Creighton, T. E., Ed.) pp 299-321, Oxford University Press, Oxford, U.K.
48. Bortoleto, R. K., de Oliveira, A. H., Ruller, R., Arni, R. K., and Ward, R. J. (1998) Tertiary structural changes of the alpha-hemolysin from Staphylococcus aureus on association with liposome membranes Arch. Biochem. Biophys. 351, 47-52
49. Santoro, M. M. and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants Biochemistry 27, 8063-8068
50. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves Methods Enzymol. 131, 266-280
51. Tweten, R. K. (1988) Nucleotide sequence of the gene for perfringolysin O (theta-toxin) from Clostridium perfringens: Significant homology with the genes for streptolysin O and pneumolysin Infect. Immun. 56, 3235-3240
52. Tweten, R. K. (1988) Cloning and expression in Escherichia coli of the perfringolysin O (theta-toxin) gene from Clostridium perfringens and characterization of the gene product Infect. Immun. 56, 3228-3234
53. Rossjohn, J., Feil, S. C., McKinstry, W. J., Tweten, R. K., and Parker, M. W. (1997) Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form Cell 89, 685-692
54. Lange, Y., Ye, J., Duban, M.-E., and Steck, T. L. (2009) Activation of membrane cholesterol by 63 amphipaths Biochemistry 48, 8505-8515
55. Ohno-Iwashita, Y., Iwamoto, M., Mitsui, K.-i., Ando, S., and Iwashita, S. (1991) A cytolysin, λ-toxin, preferentially binds to membrane cholesterol surrounded by phospholipids with 18-carbon hydrocarbon chains in cholesterol-rich region J. Biochem. (Tokyo) 110, 369-375
56. Zitzer, A., Bittman, R., Verbicky, C. A., Erukulla, R. K., Bhakdi, S., Weis, S., Valeva, A., and Palmer, M. (2001) Coupling of cholesterol and cone-shaped lipids in bilayers augments membrane permeabilization by the cholesterol-specific toxins streptolysin O and Vibrio cholerae cytolysin J. Biol. Chem. 276, 14628-14633
57. Clarke, J. and Fersht, A. R. (1993) Engineered disulfide bonds as probes of the folding pathway of barnase: Increasing the stability of proteins against the rate of denaturation Biochemistry 32, 4322-4329
58. Goni, F. M. and Alonso, A. (2000) Membrane fusion induced by phospholipase C and sphingomyelinases Biosci. Rep. 20, 443-463
59. Nieva, J. L., Goni, F. M., and Alonso, A. (1989) Liposome fusion catalytically induced by phospholipase C Biochemistry 28, 7364-7367
60. Takahashi, T., Sugahara, T., and Ohsaka, A. (1981) Phospholipase C from Clostridium perfringens Methods Enzymol. 7, 710-725
61. Palmer, M. (2004) Cholesterol and the activity of bacterial toxins FEMS Microbiol. Lett. 238, 281-289
62. Alouf, J. E., Billington, S. J., and Jost, B. H. (2006) Repertoire and general features of the family of cholesterol-dependent cytolysins, in The comprehensive sourcebook of bacterial protein toxins (Alouf, J. E. and Popoff, M. R., Eds.) pp 643-658, Academic Press, Oxford, England.
63. Ohno-Iwashita, Y., Iwamoto, M., Ando, S., and Iwashita, S. (1992) Effect of lipidic factors on membrane cholesterol topology-Mode of binding of λ-toxin to cholesterol in liposomes Biochim. Biophys. Acta 1109, 81-90
64. Lange, Y., Ye, J., and Steck, T. L. (2005) Activation of membrane cholesterol by displacement from phospholipids J. Biol. Chem. 280, 36126-36131
65. Alving, C. R., Habig, W. H., Urban, K. A., and Hardegree, M. C. (1979) Cholesterol-dependent tetanolysin damage to liposomes Biochim. Biophys. Acta 551, 224-228
66. Rosenqvist, E., Michaelsen, T. E., and Vistnes, A. I. (1980) Effect of streptolysin O and digitonin on egg lecithin/cholesterol vesicles Biochim. Biophys. Acta 600, 91-102
67. Bavdek, A., Gekara, N. O., Priselac, D., Gutierrez Aguirre, I., Darji, A., Chakraborty, T., MacÌek, P., Lakey, J. H., Weiss, S., and Anderluh, G. (2007) Sterol and pH interdependence in the binding, oligomerization, and pore formation of listeriolysin O Biochemistry 46, 4425-4437
68. Hotze, E. M., Heuck, A. P., Czajkowsky, D. M., Shao, Z., Johnson, A. E., and Tweten, R. K. (2002) Monomer-monomer interactions drive the prepore to pore conversion of a beta-barrel-forming cholesterol-dependent cytolysin J. Biol. Chem. 277, 11597-11605
69. Yeagle, P. L. and Young, J. E. (1986) Factors contributing to the distribution of cholesterol among phospholipid vesicles J. Biol. Chem. 261, 8175-8181
70. Veatch, S. L. and Keller, S. L. (2005) Miscibility phase diagrams of giant vesicles containing sphingomyelin Phys. Rev. Lett. 94, 148101-148104
71. Ziblat, R., Leiserowitz, L., and Addadi, L. (2010) Crystalline domain structure and cholesterol crystal nucleation in single hydrated DPPC:cholesterol:POPC bilayers J. Am. Chem. Soc. 132, 9920-9927
72. Jacobs, T., Cima-Cabal, M. D., Darji, A., Méndez, F. J., Vázquez, F., Jacobs, A. A. C., Shimada, Y., Ohno-Iwashita, Y., Weiss, S., and de los Toyos, J. R. (1999) The conserved undecapeptide shared by thiol-activated cytolysins is involved in membrane binding FEBS Lett. 459, 463-466
73. Polekhina, G., Feil, S. C., Tang, J., Rossjohn, J., Giddings, K. S., Tweten, R. K., and Parker, M. W. (2006) Comparative three-dimensional structure of cholesterol-dependent cytolysins, in The comprehensive sourcebook of bacterial protein toxins (Alouf, J. E. and Popoff, M. R., Eds.) pp 659-670, Academic Press, Oxford, England.
74. Pinkney, M., Beachey, E., and Kehoe, M. (1989) The thiol-activated toxin streptolysin O does not require a thiol group for cytolytic activity Infect. Immun. 57, 2553-2558
75. Saunders, F. K., Mitchell, T. J., Walker, J. A., Andrew, P. W., and Boulnois, G. J. (1989) Pneumolysin, the thiol-activated toxin of Streptococcus pneumoniae, does not require a thiol group for in vitro activity Infect. Immun. 57, 2547-2552
76. Korchev, Y. E., Bashford, C. L., Pederzolli, C., Pasternak, C. A., Morgan, P. J., Andrew, P. W., and Mitchell, T. J. (1998) A conserved tryptophan in pneumolysin is a determinant of the characteristics of channels formed pneumolysin in cells and planar lipid bilayers Biochem. J. 329, 571-577
77. Michel, E., Reich, K. A., Favier, R., Berche, P., and 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
78. Stachowiak, R., Wisniewski, J., Osinska, O., and Bielecki, J. (2009) Contribution of cysteine residue to the properties of Listeria monocytogenes listeriolysin O Can. J. Microbiol. 55, 1153-1159
79. Cooper, R. A., Leslie, M. H., Fischkoff, S., Shinitzky, M., and Shattil, S. J. (1978) Factors influencing the lipid composition and fluidity of red cell membranes in vitro: Production of red cells possessing more than two cholesterols per phospholipid Biochemistry 17, 327-331
80. Jacobs, T., Darji, A., Frahm, N., Rohde, M., Wehland, J., Chakraborty, T., and Weiss, S. (1998) Listeriolysin O: Cholesterol inhibits cytolysis but not binding to cellular membranes Mol. Microbiol. 28, 1081-1089
81. Gaus, K., Rodriguez, M., Ruberu, K. R., Gelissen, I., Sloane, T. M., Kritharides, L., and Jessup, W. (2005) Domain-specific lipid distribution in macrophage plasma membranes J. Lipid Res. 46, 1526-1538
82. Harwood, C. R. and Cranenburgh, R. (2008) Bacillus protein secretion: An unfolding story Trends Microbiol. 16, 73-79
83. Rafii, F., Park, M., Bryant, A. E., Johnson, S. J., and Wagner, R. D. (2007) Enhanced production of phospholipase C and perfringolysin O (alpha and theta toxins) in a gatifloxacin-resistant strain of Clostridium perfringens Antimicrob. Agents Chemother. 52, 895-900
84. Hamman, B. D., Hendershot, L. M., and Johnson, A. E. (1998) BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation Cell 92, 747-758
85. Urbina, P., Flores-Díaz, M., Alape-Girón, A., Alonso, A., and Goni, F. M. (2009) Phospholipase C and sphingomyelinase activities of the Clostridium perfringens α-toxin Chem. Phys. Lipids 159, 51-57
86. Goldfine, H., Knob, C., Alford, D., and Bentz, J. (1995) Membrane permeabilization by Listeria monocytogenes phosphatidylinositol-specific phospholipase C is independent of phospholipid hydrolysis and cooperative with listeriolysin O Proc. Natl. Acad. Sci. U.S.A. 92, 2979-2983
87. Smith, G. A., Marquis, H., Jones, S., Johnston, N. C., Portnoy, D. A., and Goldfine, H. (1995) The two distinct phospholipases C of Listeria monocytogenes have overlapping roles in escape from a vacuole and cell-to-cell spread Infect. Immun. 63, 4231-4237
88. Birmingham, C. L., Canadien, V., Kaniuk, N. A., Steinberg, B. E., Higgins, D. E., and Brumell, J. H. (2008) Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles Nature 451, 350-354
89. Alberti-Segui, C., Goeden, K. R., and Higgins, D. E. (2007) Differential function of Listeria monocytogenes listeriolysin O and phospholipases C in vacuolar dissolution following cell-to-cell spread Cell. Microbiol. 9, 179-195
90. Barlic, A., Gutierrez-Aguirre, I., Caaveiro, J. M., Cruz, A., Ruiz-Arguello, M. B., Perez-Gil, J., and Gonzalez-Manas, J. M. (2004) Lipid phase coexistence favors membrane insertion of equinatoxin-II, a pore-forming toxin from Actinia equina J. Biol. Chem. 279, 34209-34216