Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway

Traffic

Volumn 4, Issue 4, 2003, Pages 222-231

  Mobius W ^a   van Donselaar, E ^a   Ohno Iwashita, Y ^b   Shimada, Y ^b   Heijnen, H F G ^a   Slot, J W ^a   Geuze, H J ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

Author keywords

B lymphocytes; Bis(monoacylglycero)phosphate; Cholesterol localization; Endocytosis; Exosomes; Immunoelectron microscopy; Lysobisphosphatidic acid; Multivesicular bodies

Indexed keywords

BOVINE SERUM ALBUMIN; CELL MARKER; CHOLESTEROL; COLLOIDAL GOLD; MONOACYLGLYCEROL; PHOSPHATIDIC ACID;

ARTICLE; B LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL ORGANELLE; CELLULAR DISTRIBUTION; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; INTRACELLULAR MEMBRANE; LYSOSOME; PRIORITY JOURNAL; TRANSPORT KINETICS; TRANSPORT VESICLE;

EID: 0038620205     PISSN: 13989219     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-0854.2003.00072.x     Document Type: Article

References (77)

1. Brown MS, Goldstein JL. A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc Natl Acad Sci USA 1999;96:11041-11048.
2. Brown MS, Goldstein JL. A receptor-mediated pathway for cholesterol homeostasis. Science 1986;232:34-47.
3. Pentchev PG, Comly ME, Kruth HS, Tokoro T, Butler J, Sokol J, Filling-Katz M, Quirk JM, Marshall DC, Patel S, Vanier MT, Brady RO. Group C Niemann-Pick disease: faulty regulation of low-density lipoprotein uptake and cholesterol storage in cultured fibroblasts. FASEB J 1987;1:40-45.
4. Goldstein JL, Dana SE, Faust JR, Beaudet AL, Brown MS. Role of lysosomal acid lipase in the metabolism of plasma low density lipoprotein. Observations in cultured fibroblasts from a patient with cholesteryl ester storage disease. J Biol Chem 1975;250:8487-8495.
5. Liscum L, Dahl NK. Intracellular cholesterol transport. J Lipid Res 1992;33:1239-1254.
6. 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 et al. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997;277:228-231.
7. Vanier MT, Duthel S, Rodriguez-Lafrasse C, Pentchev P, Carstea ED. Genetic heterogeneity in Niemann-Pick C disease: a study using somatic cell hybridization and linkage analysis. Am J Hum Genet 1996;58:118-125.
8. Naureckiene S, Sleat DE, Lackland H, Fensom A, Vanier MT, Wattiaux R, Jadot M, Lobel P. Identification of HE1 as the second gene of Niemann-Pick C disease. Science 2000;290:2298-2301.
9. Neufeld EB, Cooney AM, Pitha J, Dawidowicz EA, Dwyer NK, Pentchev PG, Blanchette-Mackie EJ. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J Biol Chem 1996;271:21604-21613.
10. Warnock DE, Roberts C, Lutz MS, Blackburn WA, Young WW Jr, Baenziger JU. Determination of plasma membrane lipid mass and composition in cultured Chinese hamster ovary cells using high gradient magnetic affinity chromatography. J Biol Chem 1993;268: 10145-10153.
11. Lange Y, Swaisgood MH, Ramos BV, Stack TL. Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts. J Biol Chem 1989;264: 3786-3793.
12. Liscum L, Munn NJ. Intracellular cholesterol transport. Biochim Biophys Acta 1999;1438:19-37.
13. Blanchette-Mackie EJ. Intracellular cholesterol trafficking: role of the NPC1 protein. Biochim Biophys Acta 2000;1486:171-183.
14. Hornick CA, Hui DY, DeLamatre JG. A role for retrosomes in intracellular cholesterol transport from endosomes to the plasma membrane. Am J Physiol 1997;273 (3 Part 1):C1075-C1081.
15. Hao M, Lin SX, Karylowski OJ, Wustner D, McGraw TE, Maxfield FR. Vesicular and non-vesicular sterol transport-in living cells. The endocytic recycling compartment is a major sterol storage organelle. J Biol Chem 2002;277:609-617.
16. Gagescu R, Demaurex N, Parton RG, Hunziker W, Huber LA, Gruenberg J. The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol Biol Cell 2000;11:2775-2791.
17. Sokol J, Blanchette-Mackie J, Knuth HS, Dwyer NK, Amende LM, Butler JD, Robinson E, Patel S, Brady RO, Comly ME. Type C Niemann-Pick disease. Lysosomal accumulation and defective intracellular mobilization of low density lipoprotein cholesterol. J Biol Chem 1988;263:3411-3417.
18. Lange Y, Ye J, Stack TL. Circulation of cholesterol between lysosomes and the plasma membrane. J Biol Chem 1998;273:18915-18922.
19. Schoer JK, Gallegos AM, McIntosh AL, Starodub O, Kier AB, Billheimer JT, Schroeder F. Lysosomal membrane cholesterol dynamics. Biochemistry 2000;39:7662-7677.
20. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997;387:569-572.
21. Brown DA, London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 2000;275:17221-17224.
22. Ridgway ND. Interactions between metabolism and intracellular distribution of cholesterol and sphingomyelin. Biochim Biophys Acta 2000;1484:129-141.
23. Iwamoto M, Morita I, Fukuda M, Murota S, Ando S, Ohno-Iwashita Y. A biotinylated perfringolysin O derivative: a new probe for detection of cell surface cholesterol. Biochim Biophys Acta 1997;1327:222-230.
24. Möbius W, Ohno-Iwashita Y, van Donselaar EG, Oorschot VM, Shimada Y, Fujimoto T, Heijnen HF, Geuze HJ, Slot JW. Immunoelectron microscopic localization of cholesterol using biotinylated and non-cytolytic perfringolysin O. J Histochem Cytochem 2002;50:43-55.
25. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 1987;26:9412-9420.
26. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996;183:1161-1172.
27. Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W, Geuze HJ. Exosome from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 2000;113(Part 19):3365-3374.
28. Stoorvogel W, Kleijmeer MJ, Geuze HJ, Raposo G. The biogenesis and functions of exosomes. Traffic 2002;3:321-330.
29. Kleijmeer M, Ramm G, Schuurhuis D, Griffith J, Rescigno M, Ricciardi-Castagnoli P, Rudensky AY, Ossendorp F, Melief CJ, Stoorvogel W, Geuze HJ. Reorganization of multivesicular bodies regulates MHC class II antigen presentation by dendritic cells. J Cell Biol 2001;155: 53-63.
30. Denzer K, van Eijk M, Kleijmeer MJ, Jakobson E, de Groot C, Geuze HJ. Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface. J Immunol 2000;165:1259-1265.
31. Brotherus J, Renkonen O, Fischer W, Herrmann J. Novel stereoconfiguration in lyso-bis-phosphatidic acid of cultured BHK-cells. Chem Phys Lipids 1974;13:178-182.
32. Joutti A, Brotherus J, Renkonen O, Laine R, Fischer W. The stereo-chemical configuration of lysobisphosphatidic acid from rat liver, rabbit lung and pig lung. Biochim Biophys Acta 1976;450:206-209.
33. Wherrett JR, Huterer S. Enrichment of bis-(monoacylglyceryl) phosphate in lysosomes from rat liver. J Biol Chem 1972;247:4114-4120.
34. Stremmel W, Debuch H. [Bis (monoacylglycero) phosphate - a marker lipid of secondary lysosomes? (author's translation)] Hoppe Seylers Z Physiol Chem 1976;357:803-810.
35. Poorthuis BJ, Hostetler KY. Studies on the subcellular localization and properties of bis (monoacylglyceryl) phosphate biosynthesis in rat liver. J Biol Chem 1976;251:4596-4602.
36. Bleistein J, Heidrich HG, Debuch H. The phospholipids of liver lysosomes from untreated rats. Hoppe Seylers Z Physiol Chem 1980;361: 595-597.
37. Wilkening G, Linke T, Uhlhorn-Dierks G, Sandhoff K. Degradation of membrane-bound ganglioside GM1. Stimulation by bis (manoacylglycero) phosphate and the activator proteins SAP-B and GM2-AP. J Biol Chem 2000;275:35814-35819.
38. Linke T, Wilkening G, Sadeghlar F, Mozcall H, Bernardo K, Schuchman E, Sandhoff K. Interfacial regulation of acid ceramidase activity. Stimulation of ceramide degradation by lysosomal lipids and sphingolipid activator proteins. J Biol Chem 2001;276:5760-5768.
39. Werth N, Schuette CG, Wilkening G, Lemm T, Sandhoff K. Degradation of membrane-bound ganglioside GM2 by beta -hexosaminidase A. Stimulation by GM2 activator protein and lysosomal lipids. J Biol Chem 2001;276:12685-12690.
40. Kobayashi T, Beuchat MH, Chevallier J, Makino A, Mayran N, Escola JM, Lebrand C, Cosson P, Gruenberg J. Separation and characterization of late endosomal membrane domains. J Biol Chem 2002;277: 32157-32164.
41. Kobayashi T, Beuchat MH, Lindsay M, Frias S, Palmiter RD, Sakuraba H, Parton RG, Gruenberg J. Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat Cell Biol 1999;1: 113-118.
42. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ. Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 1998;273:20121-20127.
43. Liou W, Geuze HJ, Slot JW. Improving structural integrity of cryosections for immunogold labeling. Histochem Cell Biol 1996;106:41-58.
44. Kleijmeer MJ, Morkowski S, Griffith JM, Rudensky AY, Geuze HJ. Major histocompatibility complex class II compartments in human and mouse B lymphoblasts represent conventional endocytic compartments. J Cell Biol 1997;139:639-649.
45. Geuze HJ, Slot JW, Strous GJ, Lodish HF, Schwartz AL. Intracellular site of asialoglycoprotein receptor-ligand uncoupling: double-label immunoelectron microscopy during receptor-mediated endocytosis. Cell 1983;32:277-287.
46. Stoorvogel W, Oorschot V, Geuze HJ. A novel class of clathrin-coated vesicles budding from endosomes. J Cell Biol 1996;132 :21-33.
47. Hopkins CR. Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells. Cell 1983;35:321-330.
48. Klumperman J, Hille A, Veenendaal T, Oorschot V, Stoorvogel W, von Figura K, Geuze HJ, Differences in the endosomal distributions of the two mannose 6-phosphate receptors. J Cell Biol 1993;121: 997-1010.
49. Carlsson SR, Roth J, Pillar F, Fukuda M. Isolation and characterization of human lysosomal membrane glycoproteins, h-lamp-1 and h-lamp-2. Major sialoglycoproteins carrying polylactosaminoglycan. J Biol Chem 1988;263:18911-18919.
50. Fielding PE, Fielding CJ. Intracellular transport of low density lipoprotein derived free cholesterol begins at clathrin-coated pits and terminates at cell surface caveolae. Biochemistry 1996;35:14932-14938.
51. Grechishnikova IV, Bergstrom F, Johansson LB, Brown RE, Molotkovsky JG. New fluorescent cholesterol analogs as membrane probes. Biochim Biophys Acta 1999;1420:189-202.
52. Mukherjee S, Zha X, Tabas I, Maxfield FR. Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys J 1998;75:1915-1925.
53. Schroeder F, Jefferson JR, Kier AB, Knittel J, Scallen TJ, Wood WG, Hapala I. Membrane cholesterol dynamics: cholesterol domains and kinetic pools. Proc Soc Exp Biol Med 1991;196:235-252.
54. Kruth HS, Vaughan M. Quantification of low density lipoprotein binding and cholesterol accumulation by single human fibroblasts using fluorescence microscopy. J Lipid Res 1980;21:123-130.
55. Blanchette-Mackie EJ, Dwyer NK, Amence LM, Kruth HS, Butler JD, Sokol J, Comly ME, Vanier MT, August JT, Brady RO, Pentchev PG. Type-C Niemann-Pick disease: low density lipoprotein uptake is associated with premature cholesterol accumulation in the Golgi complex and excessive cholesterol storage in lysosomes. Proc Natl Acad Sci USA 1988;85:8022-8026.
56. Coxey RA, Pentchev PG, Campbell G, Blanchette-Mackie EJ. Differential accumulation of cholesterol in Golgi compartments of normal and Niemann-Pick type C fibroblasts incubated with LDL. a cytochemical freeze-fracture study. J Lipid Res 1993;34:1165-1176.
57. Ohno-Iwashita Y, Iwamoto M, Mitsui K, Ando S, Nagai Y. Protease-nicked theta-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 1988;176: 95-101.
58. Waheed AA, Shimada Y, Heijnen HF, Nakamura M, Inomata M, Hayashi M, Iwashita S, Slot JW, Ohno-Iwashita Y. Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). Proc Natl Acad Sci USA 2001;98:4926-4931.
59. Rodal SK, Skretting G, Garred O, Vilhardt F, van Deurs B, Sandvig K. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol Biol Cell 1999;10: 961-974.
60. Tooze J, Hollinshead M. Tubular early endosomal networks in AtT20 and other cells. J Cell Biol 1991;115:635-653.
61. Miwako I, Yamamoto A, Kitamura T, Nagayama K, Ohashi M. Cholesterol requirement for cation-independent mannose 6-phosphate receptor exit from multivesicular late endosomes to the Golgi. J Cell Sci 2001;114:1765-1776.
62. Hölttä-Vuori M, Tanhuanpää K, Möbius W, Somerharju P, Ikonen E. Modulation of cellular cholesterol transport and homeostasis by Rab11. Mol Biol Cell 2002;13:3107-3122.
63. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 1996;135:913-924.
64. Gruenberg J, Griffiths G, Howell KE. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J Cell Biol 1989;108:1301-1316.
65. Neufeld EB, Wastney M, Patel S, Suresh S, Cooney AM, Dwyer NK, Roff CF, Ohno K, Morris JA, Carstea ED, Incardona JP, Strauss JF, 3rd, Vanier MT, Patterson MC, Brady RO et al. The Niemann-Pick C1 protein resides in a vesicular compartment linked to retrograde transport of multiple lysosomal cargo. J Biol Chem 1999;274: 9627-9635.
66. Alpy F, Stoeckel ME, Dierich A, Escola JM, Wendling C, Chenard MP, Vanier MT, Gruenberg J, Tomasetto C, Rio MC. The steroidogenic acute regulatory protein homolog MLN64, a late endosomal cholesterol-binding protein. J Biol Chem 2001;276:4261-4269.
67. Hölttä-Vuori M. Määttä J, Ullrich O, Kuismanen E, Ikonen E. Mobilization of late-endosomal cholesterol is inhibited by Rab guanine nucleotide dissociation inhibitor. Curr Biol 2000;10:95-98.
68. Kobayashi T, Stang E, Fang KS, de Moerloose P, Parton RG, Gruenberg J. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 1998;392:193-197.
69. Chang WJ, Rothberg KG, Kamen BA, Anderson RG. Lowering the cholesterol content of MA104 cells inhibits receptor-mediated transport of folate. J Cell Biol 1992;118:63-69.
70. Thiele C, Hannah MJ, Fahrenholz F, Huttner WB. Cholesterol binds to synaptophysin and is required for biogenesis of synaptic vesicles. Nat Cell Biol 2000;2:42-49.
71. Ohno-Iwashita Y, Iwamoto M, Mitsui K, Kawasaki H, Ando S. Cold-labile hemolysin produced by limited proteolysis of theta-toxin from Clostridium perfringens. Biochemistry 1986;25:6048-6053.
72. Sekino-Suzuki N, Nakamura M, Mitsui KI, Ohno-Iwashita Y. Contribution of individual tryptophan residues to the structure and activity of theta-toxin (perfringolysin O), a cholesterol-binding cytolysin. Eur J Biochem 1996;241:941-947.
73. Slot JW, Geuze HJ. A new method of preparing gold probes for multiple-labeling cytochemistry. Eur J Cell Biol 1985;38:87-93.
74. Roth J, Bendayan M, Orci L. Ultrastructural localization of intracellular antigens by the use of protein A-gold complex. J Histochem Cytochem 1978;26:1074-1081.
75. Morton PA, Zacheis ML, Giacoletto KS, Manning JA, Schwartz BD. Delivery of nascent MHC class II-invariant chain complexes to lysosomal compartments and proteolysis of invariant chain by cysteine proteases precedes peptide binding in B-lymphoblastoid cells. J Immunol 1995;154:137-150.
76. White S, Miller K, Hopkins C, Trowbridge IS. Monoclonal antibodies against defined epitopes of the human transferrin receptor cytoplasmic tail. Biochim Biophys Acta 1992;1136:28-34.
77. Tikkanen R, Obermuller S, Denzer K, Pungitore R, Geuze HJ, von Figura K, Honing S. The dileucine motif within the tail of MPR46 is required for sorting of the receptor in endosomes. Traffic 2000;1: 631-640.