Cyclodextrin overcomes deficient lysosome-to-endoplasmic reticulum transport of cholesterol in Niemann-Pick type C cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 46, 2009, Pages 19316-19321

  Abi Mosleh, Lina ^a   Infante, Rodney E ^a   Radhakrishnan, Arun ^a,b   Goldstein, Joseph L ^a   Brown, Michael S ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Cholesterol esterification; NPC1 and NPC2 proteins; Sphingomyelinase

Indexed keywords

25 HYDROXYCHOLESTEROL; CELL PROTEIN; CHOLESTEROL; CHOLESTEROL ACYLTRANSFERASE; CHOLESTEROL ESTER; CYCLODEXTRIN; SOLUBLE NIEMANN PICK C2 PROTEIN; SPHINGOMYELIN PHOSPHODIESTERASE; STEROL REGULATORY ELEMENT BINDING PROTEIN; UNCLASSIFIED DRUG; 2 HYDROXYPROPYL BETA CYCLODEXTRIN; 2-HYDROXYPROPYL-BETA-CYCLODEXTRIN; BETA CYCLODEXTRIN DERIVATIVE; CARRIER PROTEIN; GLYCOPROTEIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MEMBRANE PROTEIN; NPC1 PROTEIN, HUMAN; NPC2 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CELL MUTANT; CELL TRANSPORT; CELL TYPE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; CYTOSOL; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ESTERIFICATION; HUMAN; HUMAN CELL; LYSOSOME; NIEMANN PICK DISEASE; PRIORITY JOURNAL; PROTEIN DOMAIN; ANIMAL; CELL CULTURE; DRUG EFFECT; GENETICS; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BETA-CYCLODEXTRINS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELLS, CULTURED; CHOLESTEROL, LDL; ENDOPLASMIC RETICULUM; GLYCOPROTEINS; HUMANS; LYSOSOMES; MEMBRANE GLYCOPROTEINS; NIEMANN-PICK DISEASE, TYPE C;

EID: 73349138621     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0910916106     Document Type: Article

References (32)

1. Pentchev PG, Vanier MT, Suzuki K, Patterson MC (1995) in The Metabolic and Molecular Bases of Inherited Disease, eds Scriver CR, Beaudet AL, Sly WS, Valle D (McGraw-Hill, New York), 7th Ed, Vol II, pp 2625-2639.
2. Liscum L, Sturley SL (2004) Intracellular trafficking of Niemann-Pick C proteins 1 and 2: Obligate components of subcellular lipid transport. Biochim Biophys Acta 1685:22-27.
3. Brown MS, Goldstein JL (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232:34-47.
4. -/- mouse. Proc Natl Acad Sci USA 106:2377-2382.
5. Liou H-L, et al. (2006) NPC2, the protein deficient in Niemann-Pick C2 disease, consists of multiple glycoforms that bind a variety of sterols. J Biol Chem 281:36710-36723.
6. Infante RE, et al. (2008) Purified NPC1 protein: II. Localization of sterol binding to a 240-amino acid soluble luminal loop. J Biol Chem 283:1064-1075.
7. Friedland N, Liou H-L, Lobel P, Stock AM (2003) Structure of a cholesterol-binding protein deficient in Niemann-Pick type C2 disease. Proc Natl Acad Sci USA 100:2512-2517.
8. Carstea ED, et al. (1997) Niemann-Pick C1 disease gene: Homology to mediators of cholesterol homeostasis. Science 277:228-231.
9. Davies JP, Ioannou YA (2000) Topological analysis of Niemann-Pick C1 protein reveals that the membrane orientation of the putative sterol-sensing domain is identical to those of 3-hydroxy-3-methylglutaryl-CoA reductase and sterol regulatory element binding protein cleavage-activating protein. J Biol Chem 275:24367-24374.
10. Kwon HJ, et al. (2009) Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 137:1213-1224.
11. 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.
12. Cruz JC, Sugii S, Yu C, Chang T-Y (2000) Role of Niemann-Pick type C1 protein in intracellular trafficking of low density lipoprotein-derived cholesterol. J Biol Chem 275:4013-4021.
13. Brown MS, Goldstein JL (1997) The SREBP pathway: Regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89:331-340.
14. Goldstein JL, Basu SK, Brown MS (1983) Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol 98:241-260.
15. Pentchev PG, et al. (1986) The cholesterol storage disorder of the mutant BALB/c mouse. A primary genetic lesion closely linked to defective esterification of exogenously derived cholesterol and its relationship to human type C Neimann-Pick disease. J Biol Chem 261:2772-2777.
16. Liscum L, Faust JR (1987) Low density lipoprotein (LDL)-mediated suppression of cholesterol synthesis and LDL uptake is defective in Niemann-Pick type C fibroblasts. J Biol Chem 262:17002-17008.
17. Brown MS, Dana SE, Goldstein JL (1975) Cholesteryl ester formation in cultured human fibroblasts: Stimulation by oxygenated sterols. J Biol Chem 250:4025-4027.
18. 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.
19. Zambrano F, Fleischer S, Fleischer B (1975) Lipid composition of the Golgi apparatus of rat kidney and liver in comparison with other subcellular organelles. Biochim Biophys Acta 380:357-369.
20. Radhakrishnan A, Goldstein JL, McDonald JG, Brown MS (2008) Switch-like control of SREBP-2 transport triggered by small changes in ER cholesterol: A delicate balance. Cell Metab 8:512-521.
21. Wojtanik KM, Liscum L (2003) The transport of low density lipoprotein-derived cholesterol to the plasma membrane is defective in NPC1 cells. J Biol Chem 278:14850-14856.
22. Kaplan MR, Simoni RD (1985) Transport of cholesterol from the endoplasmic reticulum to the plasma membrane. J Cell Biol 101:446-453.
23. Infante RE, et al. (2008) Purified NPC1 protein: I. Binding of cholesterol and oxysterols to a 1278-amino acid membrane protein. J Biol Chem 283:1052-1063.
24. Krieger M, Goldstein JL, Brown MS (1978) Receptor-mediated uptake of low density lipoprotein reconstituted with 25-hydroxycholesteryl oleate suppresses 3-hydroxy-3-methylglutaryl-coenzyme A reductase and inhibits growth of human fibroblasts. Proc Natl Acad Sci USA 75:5052-5056.
25. Dahl NK, Reed KL, Daunais MA, Faust JR, Liscum L (1992) Isolation and characterization of Chinese hamster ovary cells defective in the intracellular metabolism of low density lipoprotein-derived cholesterol. J Biol Chem 267:4889-4896.
26. Scheek S, Brown MS, Goldstein JL (1997) Sphingomyelin depletion in cultured cells blocks proteolysis of sterol regulatory element binding proteins at site 1. Proc Natl Acad Sci USA 94:11179-11183.
27. Jacobs NL, et al. (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.
28. Cheng D, Chang CCY, Qu X-M, Chang T-Y (1995) Activation of acyl-coenzyme A: Cholesterol acyltransferase by cholesterol or by oxysterol in a cell-free system. J Biol Chem 270:685-695.
29. Underwood KW, Jacobs NL, Howley A, Liscum L (1998) Evidence for a cholesterol transport pathway from lysosomes to endoplasmic reticulum that is independent of the plasma membrane. J Biol Chem 273:4266-4274.
30. Camargo F, et al. (2001) Cyclodextrins in the treatment of a mouse model of Niemann-Pick C disease. Life Sci 70:131-142.
31. Loftus SK, et al. (1997) Murine model of Niemann-Pick C disease: Mutation in a cholesterol homeostasis gene. Science 277:232-235.
32. Basu SK, et al. (1982) Biochemical and genetic studies of the apoprotein E secreted by mouse macrophages and human monocytes. J Biol Chem 257:9788-9795.