Reduced sensitivity of Niemann-Pick C1-deficient cells to θ-toxin (perfringolysin O): Sequestration of toxin to raft-enriched membrane vesicles

Histochemistry and Cell Biology

Volumn 121, Issue 4, 2004, Pages 263-272

  Ohsaki, Yuki ^a   Sugimoto, Yuko ^a   Suzuki, Michitaka ^a   Kaidoh, Toshiyuki ^a   Shimada, Yukiko ^b   Ohno Iwashita, Yoshiko ^b   Davies, Joanna P ^c   Ioannou, Yiannis A ^c   Ohno, Kousaku ^a   Ninomiya, Haruaki ^a  

^a TOTTORI UNIVERSITY   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

toxin; Cholesterol; Low density lipoprotein; Perfringolysin; Progesterone

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; CHOLESTEROL; CLOSTRIDIUM PERFRINGENS TOXIN; PROGESTERONE; TOXIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL SURFACE; CELL SURVIVAL; CHO CELL; CONFOCAL MICROSCOPY; CYTOTOXICITY; DENSITY GRADIENT; DRUG SENSITIVITY; ELECTRON MICROSCOPY; FRACTIONATION; MEMBRANE VESICLE; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BACTERIAL TOXINS; CARRIER PROTEINS; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL SURVIVAL; CHOLESTEROL; DRUG RESISTANCE; HEMOLYSIN PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPOPROTEINS, LDL; MEMBRANE GLYCOPROTEINS; MEMBRANE MICRODOMAINS; MICROSCOPY, ELECTRON; PROGESTERONE; PROTEIN-SERINE-THREONINE KINASES; TRANSFECTION;

CRICETINAE; CRICETULUS GRISEUS;

EID: 2442440946     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-004-0643-7     Document Type: Article

References (35)

1. Billington SJ, Jost BH, Songer JG (2000) Thiol-activated cytolysins: structure, function and role in pathogenesis. FEMS Microbiol Lett 182:197-205
2. Butler JD, Blanchette-Mackie EJ, Goldin E, O'Neill RR, Carstea G, Roff CF, Patterson MC, Patel S, Comly ME, Cooney A (1992) Progesterone blocks cholesterol translocation from lysosomes. J Biol Chem 267:23797-23805
3. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, Gu J, Rosenfeld MA, Pavan WJ, Krizman DB, Nagle J, Polymeropoulos MH, Sturley SL, Ioannou YA, Higgins ME, Comly M, Cooney A, Brown A, Kaneski CR, Blanchette-Mackie EJ, Dwyer NK, Neufeld EB, Chang TY, Liscum L, Strauss JF III, Ohno K, Zeigler M, Karmi R, Sokol J, Markie D, O'Neill RR, van Diggelen OP, Elleder M, Patterson MC, Brady RO, Vanier MT, Pentchev PG, Tagle DA (1997) Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 277:228-231
4. Coleman ML, Sahai EA, Yeo M, Bosch M, Dewar A, Olson MF (2001) Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat Cell Biol 3:339-345
5. Davies JP, Chen FW, Ioannou YA (2000) Transmembrane molecular pump activity of Niemann-Pick C1 protein. Science 290:2295-2298
6. De Kruijff B (1990) Cholesterol as a target for toxins. Biosci Rep 10:127-130
7. Dolo V, Li R, Dillinger M, Flati S, Manela J, Taylor BJ, Pavan A, Ladisch S (2000) Enrichment and localization of ganglioside G(D3) and caveolin-1 in shed tumor cell membrane vesicles. Biochim Biophys Acta 1486:265-274
8. Fujimoto T, Hayashi M, Iwamoto M, Ohno-Iwashita Y (1997) Crosslinked plasmalemmal cholesterol is sequestered to caveolae: analysis with a new cytochemical probe. J Histochem Cytochem 45:1197-1205
9. Garver WS, Erickson RP, Wilson JM, Colton TL, Hossain GS, Kozloski MA, Heidenreich RA (1997a) Altered expression of caveolin-1 and increased cholesterol in detergent insoluble membrane fractions from liver in mice with Niemann-Pick disease type C. Biochim Biophys Acta 1361:272-280
10. Garver WS, Hsu SC, Erickson RP, Greer WL, Byers DM, Heidenreich RA (1997b) Increased expression of caveolin-1 in heterozygous Niemann-Pick type II human fibroblasts. Biochem Biophys Res Commun 236:189-193
11. Hagiwara H, Kogure S, Nakamura M, Shimada Y, Ohno-Iwashita Y, Fujimoto T (1999) Cross-linking of plasmalemmal cholesterol in lymphocytes induces capping, membrane shedding, and endocytosis through coated pits. Biochem Biophys Res Commun 260:516-521
12. Higaki K, Ninomiya H, Sugimoto Y, Suzuki T, Taniguchi M, Niwa, H, Pentchev PG, Vanier MT, Ohno K (2001) Isolation of NPC1-deficient Chinese hamster ovary cell mutants by gene trap mutagenesis. J Biochem 129:875-880
13. Higgins ME, Davies JP, Chen FW, Ioannou YA (1999) Niemann-Pick C1 is a late endosome-resident protein that transiently associates with lysosomes and the trans-Golgi network. Mol Genet Metab 68:1-13
14. Iwamoto M, Morita I, Fukuda M, Murota S, Ando S, Ohono-Iwashita Y (1997) A biotinylated perfringolysin O derivative: a new probe for detection of cell surface cholesterol. Biochim Biophys Acta 1327:222-230
15. Jacobs NL, Andemariam B, Underwood KW, Panchalingam K, Sternberg D, Kielian M, Liscum L (1997) Analysis of a Chinese hamster ovary cell mutant with defective mobilization of cholesterol from the plasma membrane to the endoplasmic reticulum. J Lipid Res 38:1973-1987
16. Koike T, Ishida G, Taniguchi M, Higaki K, Ayaki Y, Saito M, Sakakihara Y, Iwamori M, Ohno K (1998) Decreased membrane fluidity and unsaturated fatty acids in Niemann-Pick disease type C fibroblasts. Biochim Biophys Acta 1406:327-335
17. Lang Y, Ye J, Rigney M, Steck TL (2002) Dynamics of lysosomal cholesterol in Niemann-Pick type C and normal human fibroblasts. J Lipid Res 43:198-204
18. Liscum L, Munn NJ (1999) Intracellular cholesterol transport. Biochim Biophys Acta 1438:19-37
19. Lusa S, Blom TS, Eskelinen EL, Kuismanen E, Mansson JE, Ikonen E (2001) Depletion of rafts in late endocytic membranes is controlled by NPC1-dependent recycling of cholesterol to the plasma membrane. J Cell Sci 114:1893-1200
20. Möbius W, Ohno-Iwashita Y, van Donselaar EG, Oorschot VM, Shimada Y, Fujimoto T, Heijnen HF, Geuze HJ, Slot JW (2002) Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfringolysin O. J Histochem Cytochem 50:43-55
21. Ohno K, Nanba E, Nakano T, Inui K, Okada S, Takeshita K (1993) Altered sensitivities to potential inhibitors of cholesterol biosynthesis in Niemann-Pick type C fibroblasts. Cell Struct Funct 18:231-240
22. Ohno-Iwashita Y, Iwamoto M, Mitsui K, Ando S, Nagai Y (1988) Protease-nicked θ-toxin of Clostridium perfringens, a new membrane probe with no cytolytic effect, reveals two classes of cholesterol as toxin-binding sites on sheep erythrocytes. Eur J Biochem 176:95-101
23. Ohno-Iwashita Y, Iwamoto M, Mitsui K, Ando S, Iwashita S (1991) A cytolysin, θ-toxin, preferentially binds to membrane cholesterol surrounded by phospholipids with 18-carbon hydrocarbon chains in cholesterol-rich region. J Biochem 110:369-375
24. Ohno-Iwashita Y, Iwamoto M, Ando S, Iwashita S (1992) Effect of lipidic factors on membrane cholesterol topology: mode of binding of θ-toxin to cholesterol in liposomes. Biochim Biophys Acta 1109:81-90
25. Okazawa M, Shiraki T, Ninomiya H, Kobayashi S, Masaki T (1998) Endothelin-induced apoptosis of A375 human melanoma cells. J Biol Chem 273:12584-12592
26. Ory DS (2000) Niemann-Pick type C: a disorder of cellular cholesterol trafficking. Biochim Biophys Acta 1529:331-339
27. Reid PC, Sakashita N, Sugii S, Ohno-Iwashita Y, Shimada Y, Hickey WF, Chang TY (2004) A novel cholesterol stain reveals early neuronal cholesterol accumulation in the Niemann-Pick type C1 mouse brain. J Lipid Res (Epub ahead of print)
28. Shimada Y, Nakamura M, Naito Y, Nomura K, Ohno-Iwashita Y (1999) C-terminal amino acid residues are required for the folding and cholesterol binding property of perfringolysin O, a pore-forming cytolysin. J Biol Chem 274:18536-18542
29. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569-572
30. Sugii S, Reid PC, Ohgami N, Shimada Y, Maue RA, Ninomiya H, Ohno-Iwashita Y, Chang TY (2003) Biotinylated θ-toxin derivative as a probe to examine intracellular cholesterol-rich domains in normal and Niemann-Pick type C1 cells. J Lipid Res 44:1033-1041
31. Sugimoto Y, Ninomiya H, Ohsaki Y, Higaki K, Davies JP, Ioannou YA, Ohno K (2001) Accumulation of cholera toxin and GM1 ganglioside in the early endosome of Niemann-Pick C1-deficient cells. Proc Natl Acad Sci U S A 98:12391-12396
32. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M, Narumiya S (1997) Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389:990-994
33. Vanier MT, Suzuki K (1998) Recent advances in elucidating Niemann-Pick C disease. Brain Pathol 8:163-174
34. Waheed AA, Shimada Y, Heijnen HF, Nakamura M, Inomata M, Hayashi M, Iwashita S, Slot JW, Ohno-Iwashita Y (2001) Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). Proc Natl Acad Sci U S A 98:4926-4931
35. Yamamoto T, Ninomiya H, Matusmoto M, Ohta Y, Nanba E, Tsutsumi Y, Yamakawa K, Millat G, Vanier MT, Pentchev PG, Ohno K (2000) Genotype-phenotype relationship of Niemann-Pick disease type C: a possible correlation between clinical onset and levels of NPC1 protein in isolated skin fibroblasts. J Med Genet 37:707-712