Activation mobilizes the cholesterol in the late endosomes-lysosomes of Niemann Pick type C cells

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Lange, Yvonne ^a   Ye, Jin ^a   Steck, Theodore L ^b  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXYPROPYL BETA CYCLODEXTRIN; CHOLESTEROL; CHOLESTEROL OXIDASE; STEROL; 3 BETA (2 (DIETHYLAMINO)ETHOXY)ANDROST 5 EN 17 ONE; 3-BETA-(2-(DIETHYLAMINO)ETHOXY)ANDROST-5-EN-17-ONE; ANDROSTANE DERIVATIVE; CHLORPROMAZINE;

ARTICLE; CELL MEMBRANE; CELL SURFACE; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; CYTOPLASM; ENDOSOME; EXTRACELLULAR SPACE; FIBROBLAST; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; LYSOSOME; NIEMANN PICK DISEASE; WILD TYPE; CELL CULTURE; DRUG EFFECT; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ANDROSTENES; BIOLOGICAL TRANSPORT; CELLS, CULTURED; CHLORPROMAZINE; CHOLESTEROL; CHOLESTEROL OXIDASE; ENDOSOMES; FIBROBLASTS; HUMANS; LYSOSOMES; NIEMANN-PICK DISEASES;

EID: 84856034999     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030051     Document Type: Article

References (69)

1. Coxey RA, Pentchev PG, Campbell G, Blanchette-Mackie EJ, (1993) Differential Accumulation of Cholesterol in Golgi Compartments of Normal and Niemann-Pick Type-C Fibroblasts Incubated with LDL- a Cytochemical Freeze-Fracture Study. Journal of Lipid Research 34: 1165-1176.
2. Bi X, Liao G, (2010) Cholesterol in Niemann-Pick Type C disease. Subcell Biochem 51: 319-335.
3. Infante RE, Wang ML, Radhakrishnan A, Kwon HJ, Brown MS, et al. (2008) NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes. Proceedings of the National Academy of Sciences 105: 15287-15292.
4. Kwon HJ, Abi-Mosleh L, Wang ML, Deisenhofer J, Goldstein JL, et al. (2009) Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 137: 1213-1224.
5. Storch J, Xu Z, (2009) Niemann-Pick C2 (NPC2) and intracellular cholesterol trafficking. Biochimica et Biophysica Acta (BBA)- Molecular and Cell Biology of Lipids 1791: 671-678.
6. Abdul-Hammed M, Breiden B, Adebayo MA, Babalola JO, Schwarzmann G, et al. (2010) Role of endosomal membrane lipids and NPC2 in cholesterol transfer and membrane fusion. J Lipid Res 51: 1747-1760.
7. Prinz WA, (2010) Lipid Trafficking sans Vesicles: Where, Why, How? Cell 143: 870-874.
8. Vance JE, Peake KB, (2011) Function of the Niemann-Pick type C proteins and their bypass by cyclodextrin. Curr Opin Lipidol 22: 204-209.
9. Liu B, Ramirez CM, Miller AM, Repa JJ, Turley SD, et al. (2010) Cyclodextrin overcomes the transport defect in nearly every organ of NPC1 mice leading to excretion of sequestered cholesterol as bile acid. J Lipid Res 51: 933-944.
10. Cruz JC, Sugii S, Yu C, Chang TY, (2000) Role of Niemann-Pick type C1 protein in intracellular trafficking of low density lipoprotein-derived cholesterol. J Biol Chem 275: 4013-4021.
11. Lange Y, Ye J, Rigney M, Steck T, (2000) Cholesterol movement in Niemann-Pick type C cells and in cells treated with amphiphiles. J Biol Chem 275: 17468-17475.
12. Lange 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.
13. Liu B, Turley SD, Burns DK, Miller AM, Repa JJ, et al. (2009) Reversal of defective lysosomal transport in NPC disease ameliorates liver dysfunction and neurodegeneration in the npc1-/- mouse. Proc Natl Acad Sci USA 106: 2377-2382.
14. Davidson CD, Ali NF, Micsenyi MC, Stephney G, Renault S, et al. (2009) Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS One 4: e6951.
15. Abi-Mosleh L, Infante RE, Radhakrishnan A, Goldstein JL, Brown MS, (2009) Cyclodextrin overcomes deficient lysosome-to-endoplasmic reticulum transport of cholesterol in Niemann-Pick type C cells. Proc Natl Acad Sci USA 106: 19316-19321.
16. Rosenbaum AI, Zhang G, Warren JD, Maxfield FR, (2010) Endocytosis of beta-cyclodextrins is responsible for cholesterol reduction in Niemann-Pick type C mutant cells. Proceedings of the National Academy of Sciences 107: 5477-5482.
17. Ramirez CM, Liu B, Aqul A, Taylor AM, Repa JJ, et al. (2011) Quantitative role of LAL, NPC2, and NPC1 in lysosomal cholesterol processing defined by genetic and pharmacological manipulations. J Lipid Res 52: 688-698.
18. Devlin C, Pipalia NH, Liao X, Schuchman EH, Maxfield FR, et al. (2010) Improvement in lipid and protein trafficking in Niemann-Pick C1 cells by correction of a secondary enzyme defect. Traffic 11: 601-615.
19. Lange Y, Steck TL, (2008) Cholesterol homeostasis and the escape tendency (activity) of plasma membrane cholesterol. Prog Lipid Res 47: 319-332.
20. Steck TL, Lange Y, (2010) Cell cholesterol homeostasis: Mediation by active cholesterol. Trends in Cell Biology 20: 680-687.
21. Lange Y, Steck TL, Ye J, Lanier MH, Molugu V, et al. (2009) Regulation of fibroblast mitochondrial 27-hydroxycholesterol production by active plasma membrane cholesterol. J Lipid Res 50: 1881-1888.
22. Lange Y, Cutler HB, Steck TL, (1980) The effect of cholesterol and other intercalated amphipaths on the contour and stability of the isolated red cell membrane. J Biol Chem 255: 9331-9337.
23. Lange Y, Ye J, Steck TL, (2004) How cholesterol homeostasis is regulated by plasma membrane cholesterol in excess of phospholipids. Proc Natl Acad Sci USA 101: 11664-11667.
24. Lange Y, Ye J, Steck TL, (2005) Activation of membrane cholesterol by displacement from phospholipids. J Biol Chem 280: 36126-36131.
25. Lange Y, Ye J, Duban ME, Steck TL, (2009) Activation of membrane cholesterol by 63 amphipaths. Biochemistry 48: 8505-8515.
26. Lange Y, Matthies H, Steck TL, (1984) Cholesterol oxidase susceptibility of the red cell membrane. Biochim Biophys Acta 769: 551-562.
27. Slotte JP, Hedstrom G, Rannstrom S, Ekman S, (1989) Effects of sphingomyelin degradation on cell cholesterol oxidizability and steady-state distribution between the cell surface and the cell interior. Biochim Biophys Acta 985: 90-96.
28. Lange Y, Ye J, Steck TL, (2007) Scrambling of phospholipids activates red cell membrane cholesterol. Biochemistry 46: 2233-2238.
29. Blanchette-Mackie EJ, (2000) Intracellular cholesterol trafficking: role of the NPC1 protein. Biochim Biophys Acta 1486: 171-183.
30. Pham NA, Gal M, Bagshaw R, Mohr A, Chue B, et al. (2005) A comparative study of cytoplasmic granules imaged by the real-time microscope, Nile Red and Filipin in fibroblasts from patients with lipid storage diseases. Journal of Inherited Metabolic Disease 28: 991-1004.
31. Mukherjee S, Zha X, Tabas I, Maxfield FR, (1998) Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys J 75: 1915-1925.
32. Chen FW, Li C, Ioannou YA, (2010) Cyclodextrin induces calcium-dependent lysosomal exocytosis. PLoS One 5: e15054.
33. Kodavanti UP, Lockard VG, Mehendale HM, (1990) In vivo toxicity and pulmonary effects of promazine and chlorpromazine in rats. J Biochem Toxicol 5: 245-251.
34. Kuroda Y, Saito M, (2010) Prediction of phospholipidosis-inducing potential of drugs by in vitro biochemical and physicochemical assays followed by multivariate analysis. Toxicol In Vitro 24: 661-668.
35. Matsuzawa Y, Hostetler KY, (1980) Studies on drug-induced lipidosis: subcellular localization of phospholipid and cholesterol in the liver of rats treated with chloroquine or 4,4′-bis (diethylaminoethoxy)alpha, beta-diethyldiphenylethane. J Lipid Res 21: 202-214.
36. Lange Y, Ye J, Steck TL, (1998) Circulation of cholesterol between lysosomes and the plasma membrane. J Biol Chem 273: 18915-18922.
37. Koh CHV, Cheung NS, (2006) Cellular mechanism of U18666A-mediated apoptosis in cultured murine cortical neurons: Bridging Niemann-Pick disease type C and Alzheimer's disease. Cellular Signalling 18: 1844-1853.
38. Cenedella RJ, (2009) Cholesterol synthesis inhibitor U18666A and the role of sterol metabolism and trafficking in numerous pathophysiological processes. Lipids 44: 477-487.
39. Ahn KW, Sampson NS, (2004) Cholesterol oxidase senses subtle changes in lipid bilayer structure. Biochemistry 43: 827-836.
40. Lange Y, Ramos BV, (1983) Analysis of the distribution of cholesterol in the intact cell. J Biol Chem 258: 15130-15134.
41. Prinz WA, (2007) Non-vesicular sterol transport in cells. Prog Lipid Res 46: 297-314.
42. Mesmin B, Maxfield FR, (2009) Intracellular sterol dynamics. Biochimica et Biophysica Acta (BBA)- Molecular and Cell Biology of Lipids 1791: 636-645.
43. Jansen M, Ohsaki Y, Rega LR, Bittman R, Olkkonen VM, et al. (2011) Role of ORPs in Sterol Transport from Plasma Membrane to ER and Lipid Droplets in Mammalian Cells. Traffic 12: 218-231.
44. Sokol J, Blanchettemackie EJ, Kruth HS, Dwyer NK, Amende LM, et al. (1988) Type-C Niemann-Pick Disease- Lysosomal Accumulation and Defective Intracellular Mobilization of Low-Density Lipoprotein Cholesterol. Journal of Biological Chemistry 263: 3411-3417.
45. Garver WS, Jelinek D, Meaney FJ, Flynn J, Pettit KM, et al. (2010) The National Niemann-Pick Type C1 Disease Database: correlation of lipid profiles, mutations, and biochemical phenotypes. J Lipid Res 51: 406-415.
46. Millat G, Chikh K, Naureckiene S, Sleat DE, Fensom AH, et al. (2001) Niemann-Pick disease type C: spectrum of HE1 mutations and genotype/phenotype correlations in the NPC2 group. Am J Hum Genet 69: 1013-1021.
47. Gallala HD, Breiden B, Sandhoff K, (2011) Regulation of the NPC2 protein-mediated cholesterol trafficking by membrane lipids. J Neurochem 116: 702-707.
48. Frolov A, Zielinski SE, Crowley JR, Dudley-Rucker N, Schaffer JE, et al. (2003) NPC1 and NPC2 regulate cellular cholesterol homeostasis through generation of low density lipoprotein cholesterol-derived oxysterols. J Biol Chem 278: 25517-25525.
49. Olsen BN, Schlesinger PH, Baker NA, (2009) Perturbations of Membrane Structure by Cholesterol and Cholesterol Derivatives Are Determined by Sterol Orientation. Journal of the American Chemical Society 131: 4854-4865.
50. Olsen BN, Schlesinger PH, Ory DS, Baker NA, (2011) 25-hydroxycholesterol increases the availability of cholesterol in phospholipid membranes. Biophys J 100: 948-956.
51. Lange Y, Ye J, Rigney M, Steck TL, (1999) Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol. J Lipid Res 40: 2264-2270.
52. Lange Y, Ye J, Strebel F, (1995) Movement of 25-hydroxycholesterol from the plasma membrane to the rough endoplasmic reticulum in cultured hepatoma cells. J Lipid Res 36: 1092-1097.
53. Lange Y, Steck TL, (1994) Cholesterol homeostasis. Modulation by amphiphiles. J Biol Chem 269: 29371-29374.
54. Jimenez-Lopez J, Rios-Marco P, Marco C, Segovia J, Carrasco M, (2010) Alterations in the homeostasis of phospholipids and cholesterol by antitumor alkylphospholipids. Lipids in Health and Disease 9: 33.
55. Radhakrishnan A, Sun LP, Kwon HJ, Brown MS, Goldstein JL, (2004) Direct binding of cholesterol to the purified membrane region of SCAP: mechanism for a sterol-sensing domain. Mol Cell 15: 259-268.
56. Adams CM, Goldstein JL, Brown MS, (2003) Cholesterol-induced conformational change in SCAP enhanced by Insig proteins and mimicked by cationic amphiphiles. Proc Natl Acad Sci USA 100: 10647-10652.
57. Underwood KW, Andemariam B, McWilliams GL, Liscum L, (1996) Quantitative analysis of hydrophobic amine inhibition of intracellular cholesterol transport. J Lipid Res 37: 1556-1568.
58. Hayat MA, (2000) Principles and techniques of electron microscopy: Biological applications Cambridge, UK; New York Cambridge University Press.
59. Steck TL, Ye J, Lange Y, (2002) Probing red cell membrane cholesterol movement with cyclodextrin. Biophys J 83: 2118-2125.
60. Toulmay A, Prinz WA, (2011) Lipid transfer and signaling at organelle contact sites: the tip of the iceberg. Curr Opin Cell Biol 23: 458-463.
61. Du X, Kumar J, Ferguson C, Schulz TA, Ong YS, et al. (2011) A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking. The Journal of Cell Biology 192: 121-135.
62. Russell AD, Hopwood D, (1976) The biological uses and importance of glutaraldehyde. Prog Med Chem 13: 271-301.
63. Rothblat GH, de la Llera-Moya M, Atger V, Kellner-Weibel G, Williams DL, et al. (1999) Cell cholesterol efflux: integration of old and new observations provides new insights. J Lipid Res 40: 781-796.
64. Johnson WJ, Mahlberg FH, Rothblat GH, Phillips MC, (1991) Cholesterol transport between cells and high-density lipoproteins. Biochim Biophys Acta 1085: 273-298.
65. Schoer JK, Gallegos AM, McIntosh AL, Starodub O, Kier AB, et al. (2000) Lysosomal membrane cholesterol dynamics. Biochemistry 39: 7662-7677.
66. Lange Y, Steck TL, (1997) Quantitation of the pool of cholesterol associated with acyl-CoA:cholesterol acyltransferase in human fibroblasts. J Biol Chem 272: 13103-13108.
67. Ohvo-Rekila H, Ramstedt B, Leppimaki P, Slotte JP, (2002) Cholesterol interactions with phospholipids in membranes. Prog Lipid Res 41: 66-97.
68. Lange Y, Echevarria F, Steck TL, (1991) Movement of zymosterol, a precursor of cholesterol, among three membranes in human fibroblasts. J Biol Chem 266: 21439-21443.
69. Jacquez JA, (1985) Compartmental analysis in biology and medicine Ann Arbor University of Michigan Press.