Oligomer formation of Clostridium perfringens epsilon-toxin is induced by activation of neutral sphingomyelinase

Biochimica et Biophysica Acta - Biomembranes

Volumn 1858, Issue 11, 2016, Pages 2681-2688

  Takagishi, Teruhisa ^a   Oda, Masataka ^b   Takehara, Masaya ^a   Kobayashi, Keiko ^a   Nagahama, Masahiro ^a  

^a TOKUSHIMA BUNRI UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

C. perfringens epsilon toxin; Ceramide; Neutral sphingomyelinase; Oligomer

Indexed keywords

3,3' (1,4 PHENYLENE)BIS[N [4 (4,5 DIHYDRO 1H IMIDAZOL 2 YL)PHENYL]ACRYLAMIDE]; CERAMIDE; SPHINGOMYELIN PHOSPHODIESTERASE; ANILINE DERIVATIVE; BACTERIAL TOXIN; BENZYLIDENE DERIVATIVE; CLOSTRIDIUM PERFRINGENS EPSILON-TOXIN; ENZYME INHIBITOR; SMALL INTERFERING RNA;

ACHN CELL LINE; ARTICLE; CELL DEATH; CELL LINE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CLOSTRIDIUM PERFRINGENS; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE SILENCING; IMMUNOFLUORESCENCE; LIPID ANALYSIS; LIPOGENESIS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; TOXIN ANALYSIS; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CHEMISTRY; CYTOLOGY; DOG; DRUG EFFECTS; ENZYME ASSAY; ENZYMOLOGY; FIBROBLAST; GENE EXPRESSION; GENETICS; HUMAN; MDCK CELL LINE; MEMBRANE MICRODOMAIN; METABOLISM; PROTEIN MULTIMERIZATION;

ANILINE COMPOUNDS; ANIMALS; BACTERIAL TOXINS; BENZYLIDENE COMPOUNDS; CELL LINE; CERAMIDES; CLOSTRIDIUM PERFRINGENS; DOGS; ENZYME ACTIVATION; ENZYME ASSAYS; ENZYME INHIBITORS; FIBROBLASTS; GENE EXPRESSION; HUMANS; MADIN DARBY CANINE KIDNEY CELLS; MEMBRANE MICRODOMAINS; PROTEIN MULTIMERIZATION; RNA, SMALL INTERFERING; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 84982862052     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2016.07.009     Document Type: Article

References (30)

1. [1] Songer, J.G., Clostridial enteric diseases of domestic animals. Clin. Microbiol. Rev. 9 (1996), 216–234.
2. [2] Sakurai, J., Nagahama, M., Ochi, S., Major toxins of Clostridium perfringens. J. Toxicol. Toxin Rev. 16 (1997), 195–214.
3. [3] Popoff, M.R., Bouvet, P., Clostridial toxins. Future Microbiol 4 (2009), 1021–1064.
4. [4] Bokori-Brown, M., Savva, C.G., Fernandes da Costa, S.P., Naylor, C.E., Basak, A.K., Titball, R.W., Molecular basis of toxicity of Clostridium perfringens epsilon toxin. FEBS J 278:23 (2011), 4589–4601.
5. [5] Gill, D.M., Bacterial toxins: a table of lethal amounts. Microbiol. Rev. 46:1 (1982), 86–94.
6. [6] Popoff, M.R., Epsilon toxin: a fascinating pore-forming toxin. FEBS J 278 (2011), 4602–4615.
7. [7] Rumah, K.R., Linden, J., Fischetti, V.A., Vartanian, T., Isolation of Clostridium perfringens type B in an individual at first clinical presentation of multiple sclerosis provides clues for environmental triggers of the disease. PLoS One, 8, 2013, e76395.
8. [8] Parker, M.W., van der Goot, F.G., Buckley, J.T., Aerolysin: the ins and outs of a model channel-forming toxin. Mol. Microbiol 19 (1996), 205–212.
9. [9] Popoff, M.R., Clostridial pore-forming toxins: powerful virulence factors. Anaerobe 30 (2014), 220–238.
10. [10] Cole, A.R., Gibert, M., Popoff, M., Moss, D.S., Titball, R.W., Basak, A.K., Clostridium perfringens epsilon-toxin shows structural similarity to the pore-forming toxin aerolysin. Nat. Struct. Mol. Biol 11:8 (2004), 797–798.
11. [11] Ivie, S.E., Fennessey, C.M., Sheng, J., Rubin, D.H., McClain, M.S., Gene-trap mutagenesis identifies mammalian genes contributing to intoxication by Clostridium perfringens epsilon-toxin. PLoS One, 6, 2011, e17787.
12. [12] Nagahama, M., Ochi, S., Sakurai, J., Assembly of Clostridium perfringens epsilon-toxin on MDCK cell membrane. J. Nat. Toxins 7 (1998), 291–302.
13. [13] Chassin, C., Bens, M., de Barry, J., Courjaret, R., Bossu, J.L., Cluzeaud, F., Mkaddem, S.B., Gibert, M., Poulain, B., Popoff, M.R., Vandewalle, A., Pore-forming epsilon toxin causes membrane permeabilization and rapid ATP depletion-mediated cell death in renal collecting duct cells. Am. J. Physiol. Ren. Physiol 293 (2007), F927–F937.
14. [14] Nagahama, M., Itohayashi, Y., Hara, H., Higashihara, M., Fukatani, Y., Takagishi, T., Oda, M., Kobayashi, K., Nakagawa, I., Sakurai, J., Cellular vacuolation induced by Clostridium perfringens epsilon-toxin. FEBS J 278 (2011), 3395–3407.
15. [15] Ivie, S.E., McClain, M.S., Identification of amino acids important for binding of Clostridium perfringens epsilon-toxin to host cells and to HAVCR1. Biochemistry 51 (2012), 7588–7595.
16. [16] Nagahama, M., Hara, H., Fernandez-Miyakawa, M., Itohayashi, Y., Sakurai, J., Oligomerization of Clostridium perfringens epsilon-toxin is dependent upon membrane fluidity in liposomes. Biochemistry 45 (2006), 296–302.
17. [17] Gil, C., Dorca, A.J., Blasi, J., Clostridium perfringens epsilon toxin binds to membrane lipids and its cytotoxic action depends on sulfatide. PLoS One, 10(10), 2015, e0140321.
18. [18] Abrami, L., van Der Goot, F.G., Plasma membrane microdomains act as concentration platforms to facilitate intoxication by aerolysin. J. Cell Biol 147 (1999), 175–184.
19. [19] Miyata, S., Minami, J., Tamai, E., Matsushita, O., Shimamoto, S., Okabe, A., Clostridium perfringens epsilon-toxin forms a heptameric pore within the detergent-insoluble microdomains of MDCK cells and rat synaptosomes. J. Biol. Chem 277 (2002), 39463–39468.
20. [20] Nagahama, M., Hayashi, S., Morimitsu, S., Sakurai, J., Biological activities and pore formation of Clostridium perfringens beta toxin in HL 60 cells. J. Biol. Chem 278 (2003), 36934–36941.
21. [21] Abe, Y., Shimada, H., Kitada, S., Raft-targeting and oligomerization of Parasporin-2, a Bacillus thuringiensis crystal protein with anti-tumor activity. J. Biochem 143 (2008), 269–275.
22. [22] Fennessey, C.M., Sheng, J., Rubin, D.H., McClain, M.S., Oligomerization of Clostridium perfringens epsilon toxin is dependent upon caveolins 1 and 2. PLoS One, 7, 2012, e46866.
23. [23] Rumah, K.R., Ma, Y., Linden, J.R., Oo, M.L., Anrather, J., Schaeren-Wiemers, N., Alonso, M.A., Fischetti, V.A., McClain, M.S., Vartanian, T., The myelin and lymphocyte protein MAL is required for binding and activity of Clostridium perfringens epsilon-toxin. PLoS Pathog, 11, 2015, e1004896.
24. [24] Linden, J.R., Ma, Y., Zhao, B., Harris, J.M., Rumah, K.R., Schaeren-Wiemers, N., Vartanian, T., Clostridium perfringens epsilon toxin causes selective death of mature oligodendrocytes and central nervous system demyelination. mBio, 6, 2015, e02513.
25. [25] Pettus, B.J., Chalfant, C.E., Hannun, Y.A., Ceramide in apoptosis: an overview and current perspectives. Biochim. Biophys. Acta 1585 (2002), 114–125.
26. [26] Gómez-Muñoz, A., Ceramide 1-phosphate/ceramide, a switch between life and death. Biochim. Biophys. Acta 1758:12 (2006), 2049–2056.
27. [27] Stancevic, B., Kolesnick, R., Ceramide-rich platforms in transmembrane signaling. FEBS Lett 584 (2010), 1728–1740.
28. [28] Li, J., Sayeed, S., Robertson, S., Chen, J., McClane, B.A., Sialidases affect the host cell adherence and epsilon toxin-induced cytotoxicity of Clostridium perfringens type D strain CN3718. PLoS Pathog, 7(12), 2011, e1002429.
29. [29] Grassmé, H., Jendrossek, V., Riehle, A., von Kürthy, G., Berger, J., Schwarz, H., Weller, M., Kolesnick, R., Gulbins, E., Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Med 9 (2003), 322–330.
30. [30] Hauck, C.R., Grassmé, H., Bock, J., Jendrossek, V., Ferlinz, K., Meyer, T.F., Gulbins, E., Acid sphingomyelinase is involved in CEACAM receptor-mediated phagocytosis of Neisseria gonorrhoeae. FEBS Lett 478 (2000), 260–266.