Cellular vacuolation induced by Clostridium perfringens epsilon-toxin

FEBS Journal

Volumn 278, Issue 18, 2011, Pages 3395-3407

  Nagahama, Masahiro ^a   Itohayashi, Yukari ^a   Hara, Hideki ^b   Higashihara, Masahiro ^a   Fukatani, Yusuke ^a   Takagishi, Teruhisa ^a   Oda, Masataka ^a   Kobayashi, Keiko ^a   Nakagawa, Ichiro ^c   Sakurai, Jun ^a  

^a TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

C. perfringens epsilon toxin; endocytosis; endosomes; lysosomes; vacuolation

Indexed keywords

ADENOSINE TRIPHOSPHATASE INHIBITOR; BAFILOMYCIN A1; CLOSTRIDIUM TOXIN; COLCHICINE; EARLY ENDOSOME ANTIGEN 1; EPSILON TOXIN; GREEN FLUORESCENT PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MACROGOL 4000; METHYL BETA CYCLODEXTRIN; MICROTUBULE DEPOLYMERIZING AGENT; MONOMER; MUTANT PROTEIN; NOCODAZOLE; OLIGOMER; RAB PROTEIN; RAB5 PROTEIN; RAB7 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL VACUOLE; CLOSTRIDIUM PERFRINGENS; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOSOME; INTERNALIZATION; KIDNEY CELL; LIPID RAFT; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALS; BACTERIAL TOXINS; BETA-CYCLODEXTRINS; BIOLOGICAL MARKERS; CELL LINE; DOGS; ENDOCYTOSIS; ENDOSOMES; KIDNEY; KINETICS; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 2; LYSOSOMES; MEMBRANE MICRODOMAINS; MICROTUBULES; MUTANT PROTEINS; POLYETHYLENE GLYCOLS; RAB GTP-BINDING PROTEINS; TUBULIN MODULATORS; VACUOLES; VESICULAR TRANSPORT PROTEINS;

CLOSTRIDIUM PERFRINGENS;

EID: 80052429006     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08263.x     Document Type: Article

References (32)

1. Songer JG, (1996) Clostridial enteric diseases of domestic animals. Clin Microbiol Rev 9, 216-234.
2. Sakurai J, Nagahama M, &, Ochi S, (1997) Major toxins of Clostridium perfringens. J Toxicol Toxin Rev 16, 195-214.
3. Popoff MR, &, Bouvet P, (2009) Clostridial toxins. Future Microbiol 4, 1021-1064.
4. Minami J, Katayama S, Matsushita O, Matsushita C, &, Okabe A, (1997) Epsilon-toxin of Clostridium perfringens activates the precursor of lambda-toxin by releasing its N- and C-terminal peptides. Microbiol Immunol 41, 527-535.
5. Nagahama M, &, Sakurai J, (1991) Distribution of labeled Clostridium perfringens epsilon toxin in mice. Toxicon 29, 211-217.
6. Nagahama M, &, Sakurai J, (1992) High-affinity binding of Clostridium perfringens epsilon-toxin to rat brain. Infect Immun 6, 1237-1240.
7. Finnie JW, (2003) Pathogenesis of brain damage produced in sheep by Clostridium perfringens type D epsilon toxin. Aust Vet J 81, 219-221.
8. Petit L, Gibert M, Gillet D, Laurent-Winter C, Boquet P, &, Popoff MR, (1997) Clostridium perfringens epsilon-toxin acts on MDCK cells by forming a large membrane complex. J Bacteriol 179, 6480-6487.
9. Nagahama M, Ochi S, &, Sakurai J, (1998) Assembly of Clostridium perfringens epsilon-toxin on MDCK cell membrane. J Nat Toxins 7, 291-302.
10. 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.
11. 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.
12. Miyata S, Minami J, Tamai E, Matsushita O, Shimamoto S, &, Okabe A, (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.
13. Chassin C, Bens M, de Barry J, Courjaret R, Bossu JL, Cluzeaud F, Mkaddem SB, Gibert M, Poulain B, Popoff MR, et al. (2007) Pore-forming epsilon toxin causes membrane permeabilization and rapid ATP depletion-mediated cell death in renal collecting duct cells. Am J Physiol Renal Physiol 293, F927-F937.
14. Parker MW, van der Goot FG, &, Buckley JT, (1996) Aerolysin: the ins and outs of a model channel-forming toxin. Mol Microbiol 19, 205-212.
15. Cole AR, Gibert M, Popoff MR, Moss DS, Titball RW, &, Basak AK, (2004) Clostridium perfringens epsilon-toxin shows structural similarity to the pore-forming toxin aerolysin. Nat Struct Mol Biol 11, 797-798.
16. Abrami L, Fivaz M, Glauser PE, Parton RG, &, van der Goot FG, (1998) A pore-forming toxin interacts with a GPI-anchored protein and causes vacuolation of the endoplasmic reticulum. J Cell Biol 140, 525-540.
17. Kilsdonk EP, Yancey PG, Stoudt GW, Bangerter FW, Johnson WJ, Phillips MC, &, Rothblat GH, (1995) Cellular cholesterol efflux mediated by cyclodextrins. J Biol Chem 270, 17250-17256.
18. 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.
19. Cover TL, Reddy LY, &, Blaser MJ, (1993) Effects of ATPase inhibitors on the response of HeLa cells to Helicobacter pylori vacuolating toxin. Infect Immun 61, 1427-1431.
20. Papini E, de Bernard M, Milia E, Bugnoli M, Zerial M, Rappuoli R, &, Montecucco C, (1994) Cellular vacuoles induced by Helicobacter pylori originate from late endosomal compartments. Proc Natl Acad Sci USA 91, 9720-9724.
21. Tombola F, Oregna F, Brutsche S, Szabo I, Del Giudice G, Rappuoli R, Montecucco C, Papini E, &, Zoratti M, (1999) Inhibition of the vacuolating and anion channel activities of the VacA toxin of Helicobacter pylori. FEBS Lett 460, 221-225.
22. Li Y, Wandinger-Ness A, Goldenring JR, &, Cover TL, (2004) Clustering and redistribution of late endocytic compartments in response to Helicobacter pylori vacuolating toxin. Mol Biol Cell 15, 1946-1959.
23. Papini E, Satin B, Bucci C, de Brnard M, Telford JL, Manetti R, Rappuoli R, Zerial M, &, Montecucco C, (1997) The small GTP binding protein rab7 is essential for cellular vacuolation induced by Helicobacter pylori cytotoxin. EMBO J 16, 15-24.
24. Nakayama M, Hisatsune J, Yamasaki E, Nishi Y, Wada A, Kurazono H, Sap J, Yahiro K, Moss J, &, Hirayama T, (2006) Clustering of Helicobacter pylori VacA in lipid rafts, mediated by its receptor, receptor-like protein tyrosine phosphatase beta, is required for intoxication in AZ-521 cells. Infect Immun 74, 6571-6580.
25. 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.
26. Brumell JH, &, Scidmore MA, (2007) Manipulation of rab GTPase function by intracellular bacterial pathogens. Microbiol Mol Biol Rev 71, 636-652.
27. Figueroa-Arredondo P, Heuser JE, Akoyants NS, Morisaki JH, Giono-Cerezo S, Enríquez-Rincón F, &, Berg DE, (2001) Cell vacuolation caused by Vibrio cholerae hemolysin. Infect Immun 69, 1613-1624.
28. Cover TL, &, Blanke SR, (2005) Helicobacter pylori VacA: a paradigm for toxin multifunctionality. Nat Rev Microbiol 3, 320-332.
29. Sakurai J, Nagahama M, &, Fujii Y, (1983) Effect of Clostridium perfringens epsilon toxin on the cardiovascular system of rats. Infect Immun 42, 1183-1186.
30. Nagahama M, Kobayashi K, Ochi S, &, Sakurai J, (1991) Enzyme-linked immunosorbent assay for rapid detection of toxins from Clostridium perfringens. FEMS Microbiol Lett 84, 41-44.
31. Morinaga N, Yahiro K, Matsuura G, Watanabe M, Nomura F, Moss J, &, Noda M, (2007) Two distinct cytotoxic activities of subtilase cytotoxin produced by shiga-toxigenic Escherichia coli. Infect Immun 75, 488-496.
32. Nagahama M, Hagiyama T, Kojima T, Aoyanagi K, Takahashi C, Oda M, Sakaguchi Y, Oguma K, &, Sakurai J, (2009) Binding and internalization of Clostridium botulinum C2 toxin. Infect Immun 77, 5139-5148.