Oligomerization of Clostridium perfringens Epsilon Toxin Is Dependent upon Caveolins 1 and 2

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Fennessey, Christine M ^a   Sheng, Jinsong ^a   Rubin, Donald H ^a,b   McClain, Mark S ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CAVEOLIN 2; CLOSTRIDIUM PERFRINGENS EPSILON TOXIN; CLOSTRIDIUM TOXIN; SHORT HAIRPIN RNA; TRANSFERRIN RECEPTOR; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL CELL; ARTICLE; CELL DEATH; CLOSTRIDIUM PERFRINGENS; COMPLEX FORMATION; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIPID RAFT; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ANIMALS; BACTERIAL TOXINS; CAVEOLIN 1; CAVEOLIN 2; CELL SURVIVAL; DOGS; GENE KNOCKDOWN TECHNIQUES; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RNA, SMALL INTERFERING;

CLOSTRIDIUM PERFRINGENS; MAMMALIA;

EID: 84867033127     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046866     Document Type: Article

References (78)

1. Petit L, Gibert M, Popoff MR, (1999) Clostridium perfringens: toxinotype and genotype. Trends in Microbiology 7: 104-110.
2. Rood JI, (1998) Virulence genes of Clostridium perfringens. Annual Review of Microbiology 52: 333-360.
3. Rood JI, Cole ST, (1991) Molecular genetics and pathogenesis of Clostridium perfringens. Microbiol Rev 55: 621-648.
4. Gleeson-White MH, Bullen JJ, (1955) Clostridium welchii epsilon toxin in the intestinal contents of man. Lancet 268: 384-385.
5. Kohn J, Warrack GH, (1955) Recovery of Clostridium welchii type D from man. Lancet 268: 385.
6. Miller C, Florman S, Kim-Schluger L, Lento P, De La Garza J, et al. (2004) Fulminant and fatal gas gangrene of the stomach in a healthy live liver donor. Liver Transpl 10: 1315-1319.
7. Morinaga G, Nakamura T, Yoshizawa J, Nishida S, (1965) Isolation of Clostridium perfringens Type D from a Case of Gas Gangrene. J Bacteriol 90: 826.
8. Ivie SE, Fennessey CM, Sheng J, Rubin DH, McClain MS, (2011) Gene-trap mutagenesis identifies mammalian genes contributing to intoxication by Clostridium perfringens epsilon-toxin. PLoS One 6: e17787.
9. Lindsay CD, Hambrook JL, Upshall DG, (1995) Examination of toxicity of Clostridium-perfringens epsilon-toxin in the MDCK cell line. Toxicology In Vitro 9: 213-218.
10. Miyakawa MEF, Zabal O, Silberstein C, (2011) Clostridium perfringens epsilon toxin is cytotoxic for human renal tubular epithelial cells. Human & Experimental Toxicology 30: 275-282.
11. Gill DM, (1982) Bacterial toxins: a table of lethal amounts. Microbiol Rev 46: 86-94.
12. Minami J, Katayama S, Matsushita O, Matsushita C, Okabe A, (1997) Lambda-toxin of Clostridium perfringens activates the precursor of epsilon-toxin by releasing its N- and C-terminal peptides. Microbiol Immunol 41: 527-535.
13. Bokori-Brown M, Savva CG, Fernandes da Costa SP, Naylor CE, Basak AK, et al. (2011) Molecular basis of toxicity of Clostridium perfringens epsilon toxin. FEBS J. 278: 4589-601.
14. Popoff MR, (2011) Epsilon toxin: a fascinating pore-forming toxin. FEBS J. 278: 4602-15.
15. Robertson SL, Li J, Uzal FA, McClane BA, (2011) Evidence for a prepore stage in the action of Clostridium perfringens epsilon toxin. PLoS One 6: e22053.
16. Nestorovich EM, Karginov VA, Bezrukov SM, (2010) Polymer partitioning and ion selectivity suggest asymmetrical shape for the membrane pore formed by epsilon toxin. Biophys J 99: 782-789.
17. Petit L, Gibert M, Gillet D, LaurentWinter C, Boquet P, et al. (1997) Clostridium perfringens epsilon-toxin acts on MDCK cells by forming a large membrane complex. Journal of Bacteriology 179: 6480-6487.
18. Petit L, Maier E, Gibert M, Popoff MR, Benz R, (2001) Clostridium perfringens epsilon toxin induces a rapid change of cell membrane permeability to ions and forms channels in artificial lipid bilayers. J Biol Chem 276: 15736-15740.
19. Dorca-Arevalo J, Martin-Satue M, Blasi J, (2012) Characterization of the high affinity binding of epsilon toxin from Clostridium perfringens to the renal system. Veterinary Microbiology 157: 179-189.
20. Nagahama M, Sakurai J, (1992) High-affinity binding of Clostridium perfringens epsilon-toxin to rat brain. Infect Immun 60: 1237-1240.
21. Li JH, Sayeed S, Robertson S, Chen JM, McClane BA, (2011) Sialidases affect the host cell adherence and epsilon toxin-induced cytotoxicity of Clostridium perfringens type D strain CN3718. PLoS Pathogens 7: e1002429.
22. Bellier A, Chen CS, Kao CY, Cinar HN, Aroian RV, (2009) Hypoxia and the hypoxic response pathway protect against pore-forming toxins in C. elegans. PLoS Pathog 5: e1000689.
23. Bischof LJ, Kao CY, Los FC, Gonzalez MR, Shen Z, et al. (2008) Activation of the unfolded protein response is required for defenses against bacterial pore-forming toxin in vivo. PLoS Pathog 4: e1000176.
24. Gonzalez MR, Bischofberger M, Pernot L, van der Goot FG, Freche B, (2008) Bacterial pore-forming toxins: the (w)hole story? Cell Mol Life Sci 65: 493-507.
25. Gurcel L, Abrami L, Girardin S, Tschopp J, van der Goot FG, (2006) Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126: 1135-1145.
26. Huffman DL, Abrami L, Sasik R, Corbeil J, van der Goot FG, et al. (2004) Mitogen-activated protein kinase pathways defend against bacterial pore-forming toxins. Proc Natl Acad Sci U S A 101: 10995-11000.
27. Zhang X, Candas M, Griko NB, Taussig R, Bulla LA Jr, (2006) A mechanism of cell death involving an adenylyl cyclase/PKA signaling pathway is induced by the Cry1Ab toxin of Bacillus thuringiensis. Proc Natl Acad Sci U S A 103: 9897-9902.
28. Soletti RC, Alves T, Vernal J, Terenzi H, Anderluh G, et al. (2010) Inhibition of MAPK/ERK, PKC and CaMKII signaling blocks cytolysin-induced human glioma cell death. Anticancer Res 30: 1209-1215.
29. Borrmann E, Gunther H, Kohler H, (2001) Effect of Clostridium perfringens epsilon toxin on MDCK cells. FEMS Immunol Med Microbiol 31: 85-92.
30. Lindsay CD, (1996) Assessment of aspects of the toxicity of Clostridium perfringens epsilon-toxin using the MDCK cell line. Hum Exp Toxicol 15: 904-908.
31. Nagahama M, Itohayashi Y, Hara H, Higashihara M, Fukatani Y, et al. (2011) Cellular vacuolation induced by Clostridium perfringens epsilon-toxin. FEBS J 278: 3395-3407.
32. Couet J, Li S, Okamoto T, Ikezu T, Lisanti MP, (1997) Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. Journal of Biological Chemistry 272: 6525-6533.
33. Pany S, Krishnasastry MV, (2007) Aromatic residues of Caveolin-1 binding motif of alpha-hemolysin are essential for membrane penetration. Biochem Biophys Res Commun 363: 197-202.
34. Pany S, Vijayvargia R, Krishnasastry MV, (2004) Caveolin-1 binding motif of alpha-hemolysin: its role in stability and pore formation. Biochem Biophys Res Commun 322: 29-36.
35. Srivastava SS, Pany S, Sneh A, Ahmed N, Rajman A, Musti K, (2009) Membrane bound monomer of Staphylococcal α-toxin induces caspase activation and apoptotic cell death despite initiation of membrane repair pathway. Plos One 4: e6293.
36. Vijayvargia R, Kaur S, Sangha N, Sahasrabuddhe AA, Surolia I, et al. (2004) Assembly of alpha-hemolysin on A431 cells leads to clustering of Caveolin-1. Biochem Biophys Res Commun 324: 1124-1129.
37. Vijayvargia R, Suresh CG, Krishnasastry MV, (2004) Functional form of Caveolin-1 is necessary for the assembly of α-hemolysin. Biochemical and Biophysical Research Communications 324: 1130-1136.
38. Wilke GA, Wardenburg JB, (2010) Role of a disintegrin and metalloprotease 10 in Staphylococcus aureus alpha-hemolysin-mediated cellular injury. Proc Nat Acad of Sci USA 107: 13473-13478.
39. Dorca-Arevalo J, Soler-Jover A, Gibert M, Popoff MR, Martin-Satue M, et al. (2008) Binding of varepsilon-toxin from Clostridium perfringens in the nervous system. Vet Microbiol 131: 14-25.
40. Pelish TM, McClain MS, (2009) Dominant-negative inhibitors of the Clostridium perfringens epsilon-toxin. J Biol Chem 284: 29446-29453.
41. Soler-Jover A, Blasi J, de Aranda IG, Navarro P, Gibert M, et al. (2004) Effect of Epsilon Toxin-GFP on MDCK Cells and Renal Tubules In Vivo. J Histochem Cytochem 52: 931-942.
42. Soler-Jover A, Dorca J, Popoff MR, Gibert M, Saura J, et al. (2007) Distribution of Clostridium perfringens epsilon toxin in the brains of acutely intoxicated mice and its effect upon glial cells. Toxicon 50: 530-540.
43. Shimada H, Kitada S, (2011) Mega assemblages of oligomeric aerolysin-like toxins stabilized by toxin-associating membrane proteins. Journal of Biochemistry 149: 103-115.
44. Miyata S, Matsushita O, Minami J, Katayama S, Shimamoto S, et al. (2001) Cleavage of a C-terminal peptide is essential for heptamerization of Clostridium perfringens epsilon-toxin in the synaptosomal membrane. J Biol Chem 276: 13778-13783.
45. Nagahama M, Ochi S, Sakurai J, (1998) Assembly of Clostridium perfringens epsilon-toxin on MDCK cell membrane. J Nat Toxins 7: 291-302.
46. Petit L, Gibert M, Gillet D, Laurent-Winter C, Boquet P, et al. (1997) Clostridium perfringens epsilon-toxin acts on MDCK cells by forming a large membrane complex. J Bacteriol 179: 6480-6487.
47. Parolini I, Sargiacomo M, Galbiati F, Rizzo G, Grignani F, et al. (1999) Expression of caveolin-1 is required for the transport of caveolin-2 to the plasma membrane- Retention of caveolin-2 at the level of the Golgi complex. Journal of Biological Chemistry 274: 25718-25725.
48. Miyata S, Minami J, Tamai E, Matsushita O, Shimamoto S, et al. (2002) Clostridium perfringens epsilon-toxin forms a heptameric pore within the detergent-insoluble microdomains of Madin-Darby canine kidney cells and rat synaptosomes. J Biol Chem 277: 39463-39468.
49. Turkcan S, Masson JB, Casanova D, Mialon G, Gacoin T, et al. (2012) Observing the confinement potential of bacterial pore-forming toxin receptors inside rafts with nonblinking Eu3+-doped oxide nanoparticles. Biophysical Journal 102: 2299-2308.
50. Abrami L, Fivaz M, van der Goot FG, (2000) Surface dynamics of aerolysin on the plasma membrane of living cells. International Journal of Medical Microbiology 290: 363-367.
51. Abrami L, van Der Goot FG, (1999) Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin. J Cell Biol 147: 175-184.
52. Alegre-Cebollada J, Rodriguez-Crespo I, Gavilanes JG, del Pozo AM, (2006) Detergent-resistant membranes are platforms for actinoporin pore-forming activity on intact cells. FEBS J 273: 863-871.
53. Garcia-Saez AJ, Buschhorn SB, Keller H, Anderluh G, Simons K, et al. (2011) Oligomerization and pore formation by equinatoxin II inhibit endocytosis and lead to plasma membrane reorganization. Journal of Biological Chemistry 286: 37768-37777.
54. Nagahama M, Hayashi S, Morimitsu S, Sakurai J, (2003) Biological activities and pore formation of Clostridium perfringens beta toxin in HL 60 cells. J Biol Chem 278: 36934-36941.
55. Schraw W, Li Y, McClain MS, van der Goot FG, Cover TL, (2002) Association of Helicobacter pylori vacuolating toxin (VacA) with lipid rafts. J Biol Chem 277: 34642-34650.
56. Valeva A, Hellmann N, Walev I, Strand D, Plate M, et al. (2006) Evidence that clustered phosphocholine head groups serve as sites for binding and assembly of an oligomeric protein pore. Journal of Biological Chemistry 281: 26014-26021.
57. Nelson KL, Buckley JT, (2000) Channel formation by the glycosylphosphatidylinositol-anchored protein binding toxin aerolysin is not promoted by lipid rafts. Journal of Biological Chemistry 275: 19839-19843.
58. Allen JA, Halverson-Tamboli RA, Rasenick MM, (2007) Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci 8: 128-140.
59. Simons K, Toomre D, (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Bio 1: 31-39.
60. Parton RG, Simons K, (2007) The multiple faces of caveolae. Nat Rev Mol Cell Bio 8: 185-194.
61. Galdiero S, Gouaux E, (2009) High resolution crystallographic studies of alpha-hemolysin-phospholipid complexes define heptamer-lipid head group interactions: implication for understanding protein-lipid interactions. Protein Science 13: 1503-1511.
62. Buxton D, (1976) Use of horseradish peroxidase to study the antagonism of Clostridium welchii (Cl. perfringens) type D epsilon toxin in mice by the formalinized epsilon prototoxin. J Comp Pathol 86: 67-72.
63. Nagahama M, Sakurai J, (1991) Distribution of labeled Clostridium perfringens epsilon toxin in mice. Toxicon 29: 211-217.
64. Shortt SJ, Titball RW, Lindsay CD, (2000) An assessment of the in vitro toxicology of Clostridium perfringens type D epsilon-toxin in human and animal cells. Hum Exp Toxicol 19: 108-116.
65. Cai CX, Zhu H, Chen JW, (2004) Overexpression of caveolin-1 increases plasma membrane fluidity and reduces P-glycoprotein function in Hs578T/Dox. Biochemical and Biophysical Research Communications 320: 868-874.
66. Hoffmann C, Berking A, Agerer F, Buntru A, Neske F, et al. (2010) Caveolin limits membrane microdomain mobility and integrin-mediated uptake of fibronectin-binding pathogens. Journal of Cell Science 123: 4280-4291.
67. Pol A, Luetterforst R, Lindsay M, Heino S, Ikonen E, et al. (2001) A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. Journal of Cell Biology 152: 1057-1070.
68. Brulet P, Mcconnell HM, (1976) Lateral hapten mobility and immunochemistry of model membranes. Proc Natl Acad Sci USA 73: 2977-2981.
69. Byfield FJ, Aranda-Espinoza H, Romanenko VG, Rothblat GH, Levitan I, (2004) Cholesterol depletion increases membrane stiffness of aortic endothelial cells. Biophysical Journal 87: 3336-3343.
70. Cooper RA, (1978) Influence of increased membrane cholesterol on membrane fluidity and cell-function in human red blood-cells. J Supramol Struct 8: 413-430.
71. Xu XL, London E, (2000) The effect of sterol structure on membrane lipid domains reveals how cholesterol can induce lipid domain formation. Biochemistry 39: 843-849.
72. Nagahama M, Hara H, Fernandez-Miyakawa M, Itohayashi Y, Sakurai J, (2006) Oligomerization of Clostridium perfringens epsilon-Toxin Is Dependent upon Membrane Fluidity in Liposomes. Biochemistry 45: 296-302.
73. Lewis M, Weaver CD, McClain MS, (2010) Identification of Small Molecule Inhibitors of Clostridium perfringens epsilon-Toxin Cytotoxicity Using a Cell-Based High-Throughput Screen. Toxins (Basel) 2: 1825-1847.
74. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
75. Schagger H, Cramer WA, von Jagow G, (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal Biochem 217: 220-230.
76. Schagger H, von Jagow G, (1991) Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form. Anal Biochem 199: 223-231.
77. Swamy M, Siegers GM, Minguet S, Wollscheid B, Schamel WW, (2006) Blue native polyacrylamide gel electrophoresis (BN-PAGE) for the identification and analysis of multiprotein complexes. Sci STKE 2006: pl4.
78. Wittig I, Braun HP, Schagger H, (2006) Blue native PAGE. Nat Protoc 1: 418-428.