Intracellular cholesterol trafficking: Role of the NPC1 protein

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1486, Issue 1, 2000, Pages 171-183

  Blanchette Mackie, E Joan ^a  

^a Pain Neurosensory Mechanisms Br N   (United States)

Author keywords

Cholesterol trafficking; Golgi; Late endosome; Niemann Pick type C disease; NPC1 protein

Indexed keywords

ABC TRANSPORTER; CELL PROTEIN; CHOLESTEROL; CHOLESTEROL ACYLTRANSFERASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; NIEMANN PICK C 1 PROTEIN; RECEPTOR PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

CELLULAR DISTRIBUTION; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; ENDOPLASMIC RETICULUM; GENE FUNCTION; GOLGI COMPLEX; HUMAN; INTRACELLULAR TRANSPORT; LIPID STORAGE; NIEMANN PICK DISEASE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

ANDROSTENES; ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CELL MEMBRANE; CHO CELLS; CHOLESTEROL; CHOLESTEROL, LDL; CRICETINAE; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; FIBROBLASTS; GOLGI APPARATUS; HOMEOSTASIS; HUMANS; MEMBRANE GLYCOPROTEINS; MUTATION; PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 0034717894     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1388-1981(00)00055-X     Document Type: Review

References (78)

1. Brown M.S., Goldstein J.L. A receptor-mediated pathway for cholesterol homeostasis. Science. 232:1986;34-47.
2. Goldstein J.L., Dana S.E., Faust J.R., Beaudet A.L., Brown M.S. 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. 250:1975;8487-8495.
3. Pentchev P.G., Comly M.E., Kruth H.S., Tokoro T., Butler J.D., Sokol J., Filling-Katz M., Quirk J.M., Marshall D.C., Patel S., Vanier M.T., Brady R.O. Group C Niemann-Pick disease: faulty regulation of low-density lipoprotein uptake and cholesterol storage in cultured fibroblasts. FASEB J. 1:1987;40-45.
4. Blanchette-Mackie E.J., Dwyer N.K., Amende L.M., Kruth H.S., Butler J.D., Sokol J., Comly M.E., Vanier M.T., August J.T., Brady R.O., Pentchev P.G. 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. 85:1988;8022-8026.
5. Roitelman J., Olender E.H., Bar-Nun S., Dun W.A.J., Simoni R.D. Immunological evidence for eight spans in the membrane domain of 3-hydroxy-3-methylglutaryl coenzyme A reductase: implications for enzyme degradation in the endoplasmic reticulum. J. Cell Biol. 117:1992;959-973.
6. Kumagi H., Chun K.T., Simoni R.D. Molecular dissection of the role of the membrane domain in the regulated degradation of 3-hydroxy-3-methylglutaryl coenzyme A reductase. J. Biol. Chem. 270:1995;19107-19113.
7. Sakai J., Nohturfft A., Cheng D., Ho Y.K., Brown M.S., Goldstein J.L. Identification of complexes between the COOH-terminal domains of sterol regulatory element-binding proteins (SREBPS) and SREBP cleavage-activating protein. J. Biol. Chem. 272:1997;20213-20221.
8. E.J. Blanchette-Mackie, P.G. Pentchev, in: T.Y. Chang, D.H. Freeman (Eds.), Intracellular Cholesterol Trafficking, Kluwer Academic Publishers, Boston, MA, 1998, pp. 53-73.
9. Carstea E.D., Morris J.A., Coleman K.G., Loftus S.K., Zhang D., Cummings C., Gu J., Rosenfeld M.A., Pavan W.J., Krizman D.B., Nagle J., Polymeropoulos M.H., Sturley S.T., Ioannou Y.A., Higgens M.E., Comly M., Cooney A., Brown A., Kaneski C.R., Blanchette-Mackie E.J., Dwyer N.K., Neufeld E.B., Chang T.Y., Liscum L., Strauss J.F., Ohno K., Zeigler M., Garrni R., Sokol J., Markie D., O'Neill R.R., van Diggelen O.P., Elleder M., Patterson M.C., Brady R.O., Vanier M.T., Pentchev P.G., Tagle D.A. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science. 277:1997;228-231.
10. Neufeld E.B., Watsney M., Patel S., Suresh S., Cooney A.M., Dwyer N.K., Roff C.F., Ohno K., Morris J.A., Carstea E.D., Incardona J.P., Strauss J.F., Vanier M.T., Patterson M.C., Brady R.O., Pentchev P.G., Blanchette-Mackie E.J. The Niemann-Pick C I protein resides in a vesicular compartment linked to retrograde transport of multiple lysosomal cargo. J. Biol. Chem. 274:1999;9627-9635.
11. T.Y. Chang, D.H. Freeman (Eds.), Intracellular Cholesterol Trafficking, Kluwer Academic Publishers, Boston, MA, 1998.
12. Underwood K.W., Jacobs N.L., Howley A., Liscum L. Evidence for a cholesterol transport pathway from lysosomes to endoplasmic reticulum that is independent of the plasma membrane. J. Biol. Chem. 273:1998;4266-4274.
13. Vanier M.T., Duthel S., Rodriguiez-Lafrasse C., Pentchev P.G., Carstea E.D. Genetic heterogeneity in Niemann-Pick C disease: a study using somatic cell hybridization and linkage analysis. Am. J. Hum. Genet. 58:1996;118-125.
14. M.C. Patterson, M.T. Vanier, K. Suzuki, J.A. Morris, E.D. Carstea, E.B. Neufeld, E.J. Blanchette-Mackie, P.G. Pentchev, in: C.R. Schriver, A.L. Beaudet, W.S. Sly, D. Valle (Eds.), Metabolic and Molecular Bases of Inherited Disease, McGraw-Hill, New York, 1999.
15. Wattenberg B.W., Silbert D.F. Sterol partitioning among intracellular membranes. J. Biol. Chem. 258:1983;2284-2289.
16. Warnock D.E., Roberts C., Lutz M.S., Blackburn W.A., Young W.W. Jr., Baenziger J.U. Determination of plasma membrane lipid mass and composition in cultured Chinese hamster ovary cells using high gradient magnetic affinity chromatography. J. Biol. Chem. 268:1993;10145-10153.
17. Lange Y., Swaisgood M.H., Rarnos B.V., Steck T.L. Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts. J. Biol. Chem. 264:1989;3786-3793.
18. Brown D.A., Rose J.K. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell. 68:1992;533-544.
19. Brown D.A., London E. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:1998;111-136.
20. Mayor S., Maxfield F.R. Insolubility and redistribution of GPI-anchored proteins at the cell surface after detergent treatment. Mol. Biol. Cell. 6:1995;929-944.
21. Simons K., van Meer G. Lipid sorting in epithelial cells. Biochemistry. 27:1988;6197-6202.
22. Anderson R.G. The caveolae membrane system. Annu. Rev. Biochem. 67:1998;199-225.
23. Fielding C.F., Fielding P.E. Intracellular cholesterol transport. J. Lipid Res. 38:1997;1503-1521.
24. Schroeder F., Frolov A.A., Murphy E.J., Atshaves B.P., Jefferson J.R., Pu L., Wood W.G., Foxworth W.B., Kier A.B. Recent advances in membrane cholesterol domain dynamics and intracellular cholesterol trafficking. Proc. Soc. Exp. Biol. Med. 213:1996;150-177.
25. Boesze-Battaglia K., Clayton S.T., Schimmel R.J. Cholesterol redistribution within human platelet plasma membrane: evidence for a stimulus-dependent event. Biochemistry. 35:1996;6664-6673.
26. DeGrella R.F., Simoni R.D. Intracellular transport of cholesterol to the plasma membrane. J. Biol. Chem. 257:1982;14256-14262.
27. Kaplan M.R., Simoni R.D. Transport of cholesterol from the endoplasmic reticulum to the plasma membrane. J. Cell Biol. 101:1985;446-453.
28. Urbani L., Simoni R.D. Cholesterol and vesicular stomatitis virus G protein take separate routes from the endoplasmic reticulum to the plasma membrane. J. Biol. Chem. 265:1990;1919-1923.
29. Smart E.J., Ying Y.S., Donzell W.C., Anderson R.G.W. A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J. Biol. Chem. 271:1996;29427-29435.
30. Lange Y., Strebel F., Steek T.L. Role of the plasma membrane in cholesterol esterification in rat hepatoma cells. J. Biol. Chem. 268:1993;13838-13843.
31. Liscum L., Dahl N.K. Intracellular cholesterol transport. J. Lipid Res. 33:1992;1239-1254.
32. Sokol J., Blanchette-Mackie E.J., Kruth H.S., Dwyer N.K., Amende L.M., Butler J.D., Robinson E., Patel S., Brady R.O., Comly M.E., Vanier M.T., Pentchev P.G. Type-C Niemann-Pick disease: lysosomal accumulation and defective intracellular mobilization of LDL-cholesterol. J. Biol. Chem. 263:1988;3411-3417.
33. Coxey R.A., Pentchev P.G., Campbell G., Blanchette-Mackie E.J. 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. 34:1993;1165-1176.
34. Neufeld E.B., Cooney A.M., Pitha J., Dawidowitcz E.A., Dwyer N.K., Pentchev P.G., Blanchette-Mackie E.J. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem. 271:1996;21604-21613.
35. Liscum L., Ruggiero R.M., Faust J.R. The intracellular transport of low density lipoprotein-derived cholesterol is defective in Niemann-Pick type C fibroblasts. J. Cell Biol. 108:1989;1625-1636.
36. Butler J., Blanchette-Mackie E.J., Goldin E., O'Neill R.R., Carstea E.D., Roff C.F., Patterson M.C., Patel S., Comly M.E., Cooney A.M., Vanier M.T., Brady R.O., Pentchev P.G. Progesterone blocks cholesterol translocation from lysosomes. J. Biol. Chem. 267:1992;23797-23805.
37. Chang C.C.Y., Chen J., Thomas M.A., Cheng D., Del Priore V.A., Newton R.S., Pape M.E., Chang T.Y. Regulation and immunolocalization of acyl-coenzyme A:cholesterol acyltransferase in mammalian cells as studied with specific antibodies. J. Biol. Chem. 270:1995;29532-29540.
38. Lange Y. Disposition of intracellular cholesterol in human fibroblasts. J. Lipid Res. 32:1991;329-339.
39. Urbani L., Simoni R.D. Cholesterol and vesicular stomatitis virus G protein take separate routes from the endoplasmic reticulum to the plasma membrane. J. Biol. Chem. 265:1990;1919-1923.
40. Jamal Z., Siffolk A., Boyd G.S., Suckling K.E. Metabolism of cholesterol ester in monolayers of bovine adrenal cortical cells. Effect of an inhibitor of acyl-CoA:cholesterol acyltransferase. Biochim. Biophys. Acta. 834:1985;230-237.
41. Bolender R.P. Correlation of morphometry and stereology with biochemical analysis of cell fractions. Int. Rev. Cytol. 55:1978;247-289.
42. Voelker D.R. Organelle biogenesis and intracellular lipid transport in eukaryotes. Microbiol. Rev. 55:1991;543-560.
43. Tabas I., Rosoff W.J., Boykow G.C. Acyl-coenzyme A:cholesterol acyltransferase in macrophages utilizes a cellular pool of oxidase accessible cholesterol as substrate. J. Biol. Chem. 263:1988;1266-1272.
44. Loftus S.K., Morris J.A., Carstea E.D., Gu J.Z., Cummings C., Brown A., Elison J., Ohno K., Rosenfeld M.A., Tagle D.A., Pentchev P.G., Pavan W.J. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science. 277:1997;232-235.
45. Letourneur F., Klausner R.D. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell. 69:1992;1143-1157.
46. Watari H., Blanchette-Mackie E.J., Dwyer N.K., Glick J.M., Patel S., Neufeld E.B., Brady R.O., Pentchev P.O., Strauss J.F. III. Niemann-Pick C1 protein: obligatory roles for N-terminal domains and lysosomal targeting in cholesterol mobilization. Proc. Natl. Acad. Sci. USA. 96:1999;805-810.
47. Watari H., Blanchene-Mackie E.J., Dwyer N.K., Watari M., Neufeld E.B., Patel S., Pentchev P.G., Strauss J.F. III. Mutations in the leucine zipper motif and sterol-sensing domain inactivate the Niemann-Pick C1 glycoprotein. J. Biol. Chem. 274:1999;21861-21866.
48. Cadigan K.M., Spillane D.M., Chang T.Y. Isolation and characterization of Chinese hamster ovary cell mutants defective in intracellular low density lipoprotein-cholesterol trafficking. J. Cell Biol. 110:1990;295-308.
49. Shamburek R.D., Pentchev P.G., Zech L.A., Blanchette-Mackie E.J., Castea E.D., VandenBrock J.M., Cooper P.S., Neufeld E.B., Phair R.D., Brewer H.B. Jr., Brady R.O., Schwartz C.C. Intracellular trafficking of the free cholesterol derived from LDL cholesteryl ester is defective in vivo in Niemann-Pick C disease: insights on normal metabolism of HDL and LDL gained from the NP-C mutation. J. Lipid Res. 38:1997;2422-2435.
50. Chen J.W., Murphy T.L., Willingham M.C., Pastan I., August J. Identification of two lysosomal membrane glycoproteins. J. Cell Biol. 101:1985;85-95.
51. Griffiths G., Matteoni R., Bach R., Hoflack B. Characterization of the cation-independent mannose 6-phosphate receptor-enriched prelysosomal compartment in NRK cells. J. Cell Sci. 95:1990;441-461.
52. Hirst J., Futter C.E., Hopkins C.R. The kinetics of mannose 6-phosphate receptor trafficking in the endocytic pathway in BEp-2 cells: the receptor enters and rapidly leaves multivesicular endosomes without accumulating in a prelysosomal compartment. Mol. Biol. Cell. 9:1998;809-816.
53. Novick P., Zerial M. The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol. 4:1997;496-504.
54. Feng Y., Press B., Wandinger-Ness A. Rab 7: an important regulator of late endocytic membrane traffic. J. Cell Biol. 131:1995;1435-1452.
55. Meresse S., Gorvel J.P., Chavrier P. The rab7 GTPase resides on a vesicular compartment connected to lysosomes. J. Cell Sci. 108:1995;3349-3358.
56. Higgins M.E., Davies J.P., Chen F.W., loannou Y.A. Niemann-Pick C1 is a late endosome-resident protein that transiently associates with lysosomes and the trans-Golgi network. Mol. Genet. Metab. 1:1999;1-13.
57. Lombardi D., Soldati T., Riederer M.A., Goda Y., Zerial M., Pfeffer S.R. Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J. 12:1993;677-682.
58. Press B., Feng Y., Hoflack B., Wandinger-Ness A. Mutant Rab7 causes the accumulation of cathepsin D and cation-independent mannose 6-phosphate receptor in an early endocytic compartment. J. Cell Biol. 140:1998;1075-1089.
59. Osborne T.F., Rosenfeld J.M. Related membrane domains in proteins of sterol sensing and cell signaling provide a glimpse of treasures still buried within the dynamic realm of intracellular metabolic regulation. Curr. Opin. Lipidol. 9:1998;137-140.
60. Chin D.J., Gil G., Russell D.W., Liscum L., Luskey K.L., Basu S.K., Okayama H., Berg P., Goldstein J.L., Brown M.S. Nucleotide sequence of 3-hydroxy-3-methyl-glutaryl coenzyme A reductase, a glycoprotein of endoplasmic reticulum. Nature. 308:1984;613-617.
61. Roitelman J., Ofender E.H., Bar-Nun S., Dun W.A. Jr., Simoni R.D. Immunological evidence for eight spans in the membrane domain of 3-hydroxy-3-methylglutaryl coenzyme A reductase: implications for enzyme degradation in the endoplasmic reticulum. J. Cell Biol. 5:1992;959-973.
62. Gil G., Faust J.R., Chin D.J., Goldstein J.L. Membrane-bound domain of HMG CoA reductase is required for sterol-enhanced degradation of the enzyme. Cell. 41:1985;249-258.
63. Hua X., Nohturffi A., Goldstein J.L., Brown M.S. Sterol resistance in CHO cells traced to point mutation in SREBP cleavage-activating protein. Cell. 87:1996;415-426.
64. Brown M.S., Goldstein J.L. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell. 89:1997;331-340.
65. Nohturfft A., Russell A., DeBose-Boyd, Scheek S., Goldstein J.L., Brown M.S. Sterols regulate cycling of SREBP cleavage-activating protein (SCAP) between endoplasmic reticulum and Golgi. Proc. Natl. Acad. Sci. USA. 96:1999;11235-11240.
66. Russell A., DeBose-Boyd, Brown M.S., Li W.-P., Nohturfft A., Goldstein J.L., Espenshade P.J. Transport-dependent proteolysis of SREBP: relocation of site-1 protease from Golgi to ER obviates the need for SREBP transport to Golgi. Cell. 99:1999;703-712.
67. Chang C.C.Y., Huh H.Y., Cadigan K.M., Chang T.Y. Molecular cloning and functional expression of human acyl-coenzyme A:cholesterol acyltransferase CDNA in mutant Chinese hamster ovary cells. J. Biol. Chem. 268:1993;20747-20755.
68. Chang T.Y., Chang C.C.Y., Cheng D. Acyl-coenzyme A:cholesterol acyltransferase. Annu. Rev. Biochem. 66:1997;613-638.
69. Farse R.V. Jr. Acyl-coenzyme A:cholesterol acyltransferase genes and knockout mice. Curr. Opin. Lipidol. 9:1998;119-124.
70. Blanchette-Mackie E.J., Dwyer N.K., Barber T., Coxey R.A., Takeda T., Rondinone C.M., Theodorakis J.L., Greenberg A.S., Londos C. Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes. J. Lipid Res. 36:1995;1211-1226.
71. Luciani M.F., Denizot F., Savary S., Mattei M.G., Chimini G. Cloning of two novel ABC transporters mapping on human chromosome 9. Genomics. 21:1994;150-159.
72. Brooks-Wilson A., Marcill M., Clee S.M., Zhang L.H., Roomp K., van Dam M., Yu L., Brewer C., Collins J.A., Molhuizen H.O.F., Loubser O., Ouelette B.F.F., Fichter K., Ashboume-Excoffon K.J.D., Sensen C.W., Scherer S., Mott S., Denis M., Martindale D., Frohlich J., Morgan K., Koop B., Pimstone S., Kastelein J.J.P., Genest J. Jr., Hayden M.R. Mutations in ABCI in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet. 22:1999;347-351.
73. Bodzioch M., Orso E., Klucken J., Langinann T., Bottcher A., Diederich W., Drobnik W., Barlage S., Buchler C., Porsch-Ozcurumez M., Kaminski W.E., Hahmann H.W., Oette K., Rothe G., Aslanidis C., Lackner K.J., Schmitz G. The gene encoding ATP-binding cassette transporter is mutated in Tangier disease. Nat. Genet. 22:1999;347-351.
74. Rust S., Rosier M., Funke H.J., Real J., Amouras Z., Piette J.C., Deleuze J.F., Brewer H.B., Duverger N., Denefle P., Assmann G. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat. Genet. 22:1999;352-355.
75. Debry P., Nash E.A., Neklason D.W., Metherall J.E. Role of multidrug resistance P-glycoproteins in cholesterol esterification. J. Biol. Chem. 272:1997;1026-1031.
76. Dean M., Allikmets R. Evolution of ATP-binding cassette transporter genes. Curr. Opin. Genet. Dev. 5:1995;779-785.
77. Porter J.A., Young K.E., Beachy P.A. Cholesterol modification of hedgehog signaling proteins in animal development. Science. 274:1996;255-259.
78. Porter J.A., Ekker S.C., Park W.J., von Kessler D.P., Young K.E., Chen C.H., Yong M., Woods A.S., Cotter R.J., Koonin V., Beachy P.A. Hedgehog patterning activity: role of a lipophilic modification mediated by the carboxy-terminal autoprocessing domain. Cell. 86:1996;21-34.