Association of Vibrio parahaemolyticus thermostable direct hemolysin with lipid rafts is essential for cytotoxicity but not hemolytic activity

Infection and Immunity

Volumn 78, Issue 2, 2010, Pages 603-610

  Matsuda, Shigeaki ^a   Kodama, Toshio ^b   Okada, Natsumi ^a   Okayama, Kanna ^b   Honda, Takeshi ^b   Iida, Tetsuya ^a  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CAVEOLIN 1; CHOLESTEROL; DETERGENT; FLOTILLIN 1; HEMOLYSIN; LIPID; LIPOSOME; METHYL BETA CYCLODEXTRIN; SPHINGOLIPID; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE; THERMOSTABLE DIRECT HEMOLYSIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; HELA CELL; HEMOLYSIS; HUMAN; HUMAN CELL; LIPID ABSORPTION; LIPID ANALYSIS; LIPID RAFT; LIPOGENESIS; MEMBRANE RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; THERMOSTABILITY; VIBRIO PARAHAEMOLYTICUS;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TOXINS; CELL LINE; ERYTHROCYTES; HELA CELLS; HEMOLYSIN PROTEINS; HEMOLYSIS; HUMANS; MEMBRANE MICRODOMAINS; SPHINGOMYELINS; VIBRIO PARAHAEMOLYTICUS;

EID: 76749161447     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00946-09     Document Type: Article

References (55)

1. Abrami, L., M. Fivaz, and F. G. van der Goot. 2000. Adventures of a pore-forming toxin at the target cell surface. Trends Microbiol. 8:168-172.
2. Abrami, L., S. Liu, P. Cosson, S. H. Leppla, and F. G. van der Goot. 2003. Anthrax toxin triggers endocytosis of its receptor via a lipid raft-mediated clathrin-dependent process. J. Cell Biol. 160:321-328.
3. Blake, P. A., R. E. Weaver, and D. G. Hollis. 1980. Diseases of humans (other than cholera) caused by vibrios. Annu. Rev. Microbiol. 34:341-367.
4. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37:911-917.
5. Fabbri, A., L. Falzano, C. Frank, G. Donelli, P. Matarrese, F. Raimondi, A. Fasano, and C. Fiorentini. 1999. Vibrio parahaemolyticus thermostable direct hemolysin modulates cytoskeletal organization and calcium homeostasis in intestinal cultured cells. Infect. Immun. 67:1139-1148.
6. Fukasawa, M., M. Nishijima, and K. Hanada. 1999. Genetic evidence for ATP-dependent endoplasmic reticulum-to-Golgi apparatus trafficking of ceramide for sphingomyelin synthesis in Chinese hamster ovary cells. J. Cell Biol. 144:673-685.
7. Fukasawa, M., M. Nishijima, H. Itabe, T. Takano, and K. Hanada. 2000. Reduction of sphingomyelin level without accumulation of ceramide in Chinese hamster ovary cells affects detergent-resistant membrane domains and enhances cellular cholesterol efflux to methyl-β-cyclodextrin. J. Biol. Chem. 275:34028-34034.
8. Gabel, B. R., C. Elwell, S. C. D. van Ijzendoorn, and J. N. Engel. 2004. Lipid raft-mediated entry is not required for Chlamydia trachomatis infection of cultured epithelial cells. Infect. Immun. 72:7367-7373.
9. Gurcel, L., L. Abrami, S. Girardin, J. Tschopp, and F. G. van der Goot. 2006. Caspase-1 activation of lipid metabolic pathways in response to bacterial pore-forming toxins promotes cell survival. Cell 126:1135-1145.
10. Hamada, D., T. Higurashi, K. Mayanagi, T. Miyata, T. Fukui, T. Iida, T. Honda, and I. Yanagihara. 2007. Tetrameric structure of thermostable direct hemolysin from Vibrio parahaemolyticus revealed by ultracentrifugation, small-angle X-ray scattering and electron microscopy. J. Mol. Biol. 365:187-195.
11. Hanada, K., T. Hara, M. Fukasawa, A. Yamaji, M. Umeda, and M. Nishijima. 1998. Mammalian cell mutants resistant to a sphingomyelin- directed cytolysin. Genetic and biochemical evidence for complex formation of the LCB1 protein with the LCB2 protein for serine palmitoyltransferase. J. Biol. Chem. 273:33787-33794.
12. Hanada, K., K. Kumagai, S. Yasuda, Y. Miura, M. Kawano, M. Fukasawa, and M. Nishijima. 2003. Molecular machinery for non-vesicular trafficking of ceramide. Nature 426:803-809.
13. Hancock, J. F. 2006. Lipid rafts: contentious only from simplistic standpoints. Nat. Rev. Mol. Cell Biol. 7:456-462.
14. Honda, T., Y. Ni, T. Miwatani, T. Adachi, and J. Kim. 1992. The thermostable direct hemolysin of Vibrio parahaemolyticus is a pore-forming toxin. Can. J. Microbiol. 38:1175-1180.
15. Honda, T., and T. Iida. 1993. The pathogenicity of Vibrio parahaemolyticus and the role of the thermostable direct hemolysin and related hemolysins. Rev. Med. Microbiol. 4:106-113.
16. Hooper, N. M. 1999. Detergent-insoluble glycosphingolipid/ cholesterol-rich microdomains, lipid rafts and caveolae. Mol. Membr. Biol. 16:145-156.
17. 2+-dependent endocytosis. J. Cell Biol. 180:905-914.
18. Igarashi, K., K. Asai, M. Kaneda, M. Umeda, and K. Inoue. 1995. Specific binding of a synthetic peptide derived from an antibody complementarity determining region to phosphatidylserine. J. Biochem. (Tokyo) 117:452-457.
19. Ikonen, E. 2001. Roles of lipid rafts in membrane transport. Curr. Opin. Cell Biol. 13:470-477.
20. Ishitsuka, R., A. Yamaji-Hasegasa, A. Makino, Y. Hirabayashi, and T. Kobayashi. 2004. A lipid-specific toxin reveals heterogeneity of sphingomyelincontaining membranes. Biophys. J. 86:296-307.
21. Ishitsuka, R., S. B. Saitoh, and T. Kobayashi. 2005. Imaging lipid rafts. J. Biochem. (Tokyo) 137:249-257.
22. Janda, J. M., C. Powers, R. G. Bryant, and S. L. Abbott. 1988. Current perspectives on the epidemiology and pathogenesis of clinically significant Vibrio spp. Clin. Microbiol. Rev. 1:245-267.
23. Kiyokawa, E., T. Baba, N. Otsuka, A. Makino, S. Ohno, and T. Kobayashi. 2005. Spatial and functional heterogeneity of sphingolipid-rich membrane domains. J. Biol. Chem. 280:24072-24084.
24. Kodama, T., M. Rokuda, K. S. Park, V. V. Cantarelli, S. Matsuda, T. Iida, and T. Honda. 2007. Identification and characterization of VopT, a novel ADP-ribosyltransferase effector protein secreted via the Vibrio parahaemolyticus type III secretion system 2. Cell. Microbiol. 9:2598-2609.
25. Lafont, F., L. Abrami, and F. G. van der Goot. 2004. Bacterial subversion of lipid rafts. Curr. Opin. Microbiol. 7:4-10.
26. Lai, E. C. 2003. Lipid rafts make for slippery platforms. J. Cell Biol. 162: 365-370.
27. Lang, P. A., S. Kaiser, S. Myssina, C. Birka, C. Weinstock, H. Northoff, T. Wieder, F. Lang, and S. M. Huber. 2004. Effect of Vibrio parahaemolyticus haemolysin on human erythrocytes. Cell. Microbiol. 6:391-400.
28. Lichtenberg, D., F. M. Goñi, and H. Heerklotz. 2005. Detergent-resistant membranes should not be identified with membrane rafts. Trends Biochem. Sci. 30:430-436.
29. London, E., and D. A. Brown. 2000. Insolubility of lipids in Triton X-100: physical origin and relationship to sphingolipid/cholesterol membrane domains (rafts). Biochim. Biophys. Acta 1508:182-195.
30. Mañes, S., G. del Real, and C. Martinez-A. 2003. Pathogens: raft hijackers. Nat. Rev. Immunol. 3:557-568.
31. Miyamoto, Y., T. Kato, Y. Obara, S. Akiyama, K. Takizawa, and S. Yamai. 1969. In vitro hemolytic characteristic of Vibrio parahaemolyticus: its close correlation with human pathogenicity. J. Bacteriol. 100:1147-1149.
32. Miyamoto, Y., Y. Obara, T. Nikkawa, S. Yamai, T. Kato, Y. Yamada, and M. Ohashi. 1980. Simplified purification and biophysicochemical characteristics of Kanagawa phenomenon-associated hemolysin of Vibrio parahaemolyticus. Infect. Immun. 28:567-576.
33. Naim, R., I. Yanagihara, T. Iida, and T. Honda. 2001. Vibrio parahaemolyticus thermostable direct hemolysin can induce an apoptotic cell death in Rat-1 cells from inside and outside of the cells. FEMS Micriobiol. Lett. 195:237-244.
34. Naim, R., T. Iida, A. Takahashi, and T. Honda. 2001. Monodansylcadaverine inhibits cytotoxicity of Vibrio parahaemolyticus thermostable direct hemolysin on cultured rat embryonic fibroblast cells. FEMS Micriobiol. Lett. 196: 99-105.
35. Nakamura, K., and S. Handa. 1984. Coomassie brilliant blue staining of lipids on thin-layer plates. Anal. Biochem. 142:406-410.
36. Nishibuchi, M., A. Fasano, R. G. Russell, and J. B. Kaper. 1992. Enterotoxigenicity of Vibrio parahaemolyticus with and without genes encoding thermostable direct hemolysin. Infect. Immun. 60:3539-3545.
37. Nishibuchi, M., and J. B. Kaper. 1995. Thermostable direct hemolysin gene of Vibrio parahaemolyticus: a virulence gene acquired by a marine bacterium. Infect. Immun. 63:2093-2099.
38. Park, K. S., T. Ono, M. Rokuda, M. H. Jang, T. Iida, and T. Honda. 2004. Cytotoxicity and enterotoxicity of the thermostable direct hemolysin-deletion mutants of Vibrio parahaemolyticus. Microbiol. Immunol. 48:313-318.
39. Raimondi, F., J. P. Kao, C. Fiorentini, A. Fabbri, G. Donelli, N. Gasparini, A. Rubino, and A. Fasano. 2000. Enterotoxicity and cytotoxicity of Vibrio parahaemolyticus thermostable direct hemolysin in in vitro systems. Infect. Immun. 68:3180-3185.
40. Rosenberger, C. M., J. H. Brumell, and B. B. Finlay. 2000. Microbial pathogenesis: lipid rafts as pathogen portals. Curr. Biol. 10:R823-R825.
41. Sakazaki, T., K. Tamura, T. Kato, Y. Obata, and S. Yamai. 1968. Studies on the enteropathogenic, facultatively halophilic bacterium, Vibrio parahaemolyticus. III. Enteropathogenicity. Jpn. J. Med. Sci. Biol. 21:325-331.
42. Schraw, W., Y. Li, M. S. McClain, F. G. van der Goot, and T. L. Cover. 2002. Association of Helicobacter pylori vacuolating toxin (VacA) with lipid rafts. J. Biol. Chem. 277:34642-34650.
43. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387:569-572.
44. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1:31-39.
45. Takeda, Y., T. Takeda, T. Honda, J. Sakurai, N. Ohtomo, and T. Miwatani. 1975. Inhibition of hemolytic activity of the thermostable direct hemolysin of Vibrio parahaemolyticus by ganglioside. Infect. Immun. 12:931-933.
46. Takeda, Y., T. Takeda, T. Honda, and T. Miwatani. 1976. Inactivation of the biological activities of the thermostable direct hemolysin of Vibrio parahaemolyticus by ganglioside GT1. Infect. Immun. 14:1-5.
47. Tang, G. Q., T. Iida, K. Yamamoto, and T. Honda. 1994. A mutant toxin of Vibrio parahaemolyticus thermostable direct hemolysin which has lost hemolytic activity but retains ability to bind to erythrocytes. Infect. Immun. 62: 3299-3304.
48. Tang, G. Q., T. Iida, K. Yamamoto, and T. Honda. 1995. Ca(2+)-independent cytotoxicity of Vibrio parahaemolyticus thermostable direct hemolysin (TDH) on Intestine 407, a cell line derived from human embryonic intestine. FEMS Microbiol. Lett. 134:233-238.
49. Tang, G. Q., T. Iida, H. Inoue, M. Yutsudo, K. Yamamoto, and T. Honda. 1997. A mutant cell line resistant to Vibrio parahaemolyticus thermostable direct hemolysin (TDH): its potential in identification of putative receptor for TDH. Biochim. Biophys. Acta 1360:277-282.
50. Tang, G., T. Iida, K. Yamamoto, and T. Honda. 1997. Analysis of functional domains of Vibrio parahaemolyticus thermostable direct hemolysin using monoclonal antibodies. FEMS Microbiol. Lett. 150:289-296.
51. Tweten, R. K. 2005. Cholesterol-dependent cytolysins, a family of versatile pore-forming toxins. Infect. Imuun. 73:6199-6209.
52. Walev, I., S. C. Bhakdi, F. Hofmann, N. Djonder, A. Valeva, K. Aktories, and S. Bhakdi. 2000. Delivery of proteins into living cells by reversible membrane permeabilization with streptolysin-O. Proc. Natl. Acad. Sci. U. S. A. 98:3185-3190.
53. Yamaji, A., Y. Sekizawa, K. Emoto, H. Sakuraba, K. Inoue, H. Kobayashi, and M. Umeda. 1998. Lysenin, a novel sphingomyelin-specific binding protein. J. Biol. Chem. 273:5300-5306.
54. Yoh, M., T. Honda, and T. Miwatani. 1988. Comparison of hemolysins of Vibrio cholerae non-O1 and Vibrio hollisae with thermostable direct hemolysin of Vibrio parahaemolyticus. Can. J. Microbiol. 34:1321-1324.
55. Yoh, M., N. Morinaga, M. Noda, and T. Honda. 1995. The binding of Vibrio parahaemolyticus 125I-labeled thermostable direct hemolysin to erythrocytes. Toxicon 33:651-657.