Localization of the murine niemann-pick C1 protein to two distinct intracellular compartments

Journal of Lipid Research

Volumn 41, Issue 5, 2000, Pages 673-687

  Garver, William S ^a   Heidenreich, Randall A ^a   Erickson, Robert P ^a,b   Thomas, Mitchell A ^a   Wilson, Jean M ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b The University of Arizona   (United States)

Author keywords

Cholesterol; Niemann Pick C1 protein; Niemann Pick type C

Indexed keywords

CAVEOLIN; CELL MEMBRANE PROTEIN; CELL PROTEIN; CHLOROQUINE; FILIPIN; LOW DENSITY LIPOPROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; NIEMANN PICK C1 PROTEIN; PROGESTERONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ORGANELLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; FIBROBLAST; LIVER HOMOGENATE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES; CELL COMPARTMENTATION; CELL FRACTIONATION; CENTRIFUGATION, DENSITY GRADIENT; CHOLESTEROL; FEMALE; FIBROBLASTS; LIVER; MALE; MICE; MICE, INBRED BALB C; MICE, MUTANT STRAINS; MICROSCOPY, FLUORESCENCE; MICROSCOPY, IMMUNOELECTRON; MOLECULAR SEQUENCE DATA; NIEMANN-PICK DISEASES; PROTEINS; RABBITS;

EID: 0034025322     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (60)

1. Pentchev, P. G., M. T. Vanier, K. Suzuki, and M. C. Patterson. 1995. Niemann-Pick disease Type C: a cellular cholesterol lipidosis. In The Metabolic and Molecular Basis of Inherited Disease, C. Scriver, A. L. Beaudet, W. S. Sly, and D. Valle, editors. McGraw-Hill, Inc., New York, NY. 2625-2639.
2. Pentchev, P. G., M. E. Comly, H. S. Kruth, T. Tokoro, J. Butler, J. Sokol, M. Filling-Katz, J. M. Quirk, D. C. Marshall, S. Patel, M. T. Vanier, and R. O. Brady. 1987. Group C Niemann-Pick disease: faulty regulation of low-density lipoprotein uptake and cholesterol storage in cultured fibroblasts. FASEB J. 1: 40-5.
3. Liscum, L., and J. R. Faust. 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.
4. Pentchev, P. G., A. D. Boothe, H. S. Kruth, H. Weintroub, J. Stivers, and R. O. Brady. 1984. A genetic storage disorder in BALB/C mice with a metabolic block in esterification of exogenous cholesterol. J. Biol. Chem. 259: 5784-5791.
5. Pentchev, P. G., M. E. Comly, H. S. Kruth, M. T. Vanier, D. A. Wenger, S. Patel, and R. O. Brady. 1985. A defect in cholesterol esterification in Niemann-Pick disease (type C) patients. Proc. Natl. Acad. Sci. USA. 82: 8247-8251.
6. Pentchev, P. G., H. S. Kruth, M. E. Comly, J. D. Butler, M. T. Vanier, D. A. Wenger, and S. Patel. 1986. Type C Niemann-Pick disease. A parallel loss of regulatory responses in both the uptake and esterification of low density lipoprotein-derived cholesterol in cultured fibroblasts. J. Biol. Chem. 261: 16775-16780.
7. Brown, M., S. Dana, and J. Goldstein. 1973. Regulation of 3-hydroxy-3-methylglutaryl coenzyme A reductase activity in human fibroblasts by lipoproteins. Proc. Natl. Acad. Sci. USA. 70: 2162-2166.
8. Brown, M., and J. Goldstein. 1975. Regulation of the activity of the low density lipoprotein receptor in human fibroblasts. Cell. 6: 307-316.
9. Suckling, K., and E. Strange. 1985. Role of acyl-CoA:cholesterol acyltransferase in cellular cholesterol metabolism. J. Lipid Res. 26: 647-671.
10. Blown, M. S., and J. L. Goldstein. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science. 232: 34-47.
11. Sato, M., S. Akaboshi, T. Katsumoto, M. Taniguchi, K. Higaki, T. Tai, H. Sakuraba, and K. Ohno. 1998. Accumulation of cholesterol and GM2 ganglioside in cells cultured in the presence of progesterone: an implication for the basic defect in Niemann-Pick disease type C. Brain Dev. 20: 50-52.
12. Watanabe, Y., S. Akaboshi, G. Ishida, T. Takeshima, T. Yano, M. Taniguchi, K. Ohno, and K. Nakashima. 1998. Increased levels of GM2 ganglioside in fibroblasts from a patient with juvenile Niemann-Pick disease type C. Brain Dev. 20: 95-97.
13. Liscum, L., and K. W. Underwood. 1995. Intracellular cholesterol transport and compartmentation. J. Biol. Chem. 270: 15443-15446.
14. Fielding, C. J., and P. E. Fielding. 1997. Intracellular cholesterol transport. J. Lipid Res. 38: 1503-1521.
15. Lange, Y., J. Ye, and J. Chin. 1997. The fate of cholesterol exiting lysosomes. J. Biol. Chem. 272: 17018-17022.
16. Liscum, L., and J. R. Faust. 1989. The intracellular transport of low density lipoprotein-derived cholesterol is inhibited in Chinese hamster ovary cells cultured with 3-beta-[2-(diethylamino)ethoxy] androst-5-cn-17-one. J. Biol. Chem. 264: 11796-11806.
17. Brasaemle, D. L., and A. D. Attie. 1990. Rapid intracellular transport of LDL-derived cholesterol to the plasma membrane in cultured fibroblasts. J. Lipid Res. 31: 103-112.
18. Johnson, W. J., G. K. Chacko, M. C. Phillips, and G. H. Rothblat. 1990. The efflux of lysosomal cholesterol from cells. J. Biol. Chem. 265: 5546-5553.
19. Neufeld, E. B., A. M. Cooney, J. Pitha, E. A. Dawidowicz, N. K. Dwyer, P. G. Pentchev, and E. J. Blanchette-Mackie. 1996. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem. 271: 21604-21613.
20. Underwood, K. W., N. L. Jacobs, A. Howley, and L. Liscum. 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.
21. Blanchette-Mackie, E. J., N. K. Dwyer, L. M. Amende, H. S. Kruth, J. D. Butler, J. Sokol, M. E. Comly, M. T. Vanier, J. T. August, R. O. Brady, and P. G. Pentchev. 1988. 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: 8022-8026.
22. Coxey, R. A., P. G. Pentchev, G. Campbell, and E. J. Blanchette-Mackie. 1993. 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: 1165-1176.
23. Mendez, A. J. 1995. Monensin and brefeldin A inhibit high density lipoprotein-mediated cholesterol efflux from cholesterol-enriched cells. Implications for intracellular cholesterol transport. J. Biol. Chem. 270: 5891-5900.
24. Mendez, A. J., and L. Uint. 1996. Apolipoprotein-mediated cellular cholesterol and phospholipid efflux depend on a functional Golgi apparatus. J. Lipid Res. 37: 2510-2524.
25. Murata, M., J. Peranen, R. Schreiner, F. Wieland, T. V. Kurzchalia, and K. Simons. 1995. VIP21/caveolin is a cholesterol-binding protein. Proc. Natl. Acad. Sci., USA. 92: 10339-10343.
26. Fielding, P. E., and C. J. Fielding. 1995. Plasma membrane caveolae mediate the efflux of cellular free cholesterol. Biochemistry. 34: 14288-14292.
27. Carstea, E. D., J. A. Morris, K. G. Coleman, S. K. Loftus, D. Zhang, C. Cummings, J. Gu, M. A. Rosenfeld, W. J. Paven, D. B. Krizman, J. Nagle, M. H. Polymeropoulos, S. L. Sturley, Y. A. Ioannou, M. E. Higgins, M. Comly, A. Cooney, A. Brown, C. R. Kaneski, E. J. Blanchette-Mackie, N. K. Dwyer, E. B. Neufeld, T. Chang, L. Liscum, J. F. Strauss, K. Ohno, M. Zeigler, R. Carmi, J. Sokol, D. Markie, R. R. O'Neill, O. P. Van Diggelen, M. Elleder, M. C. Patterson, R. O. Brady, M. T. Vanier, P. G. Pentchev, and D. A. Tagle. 1997. Niemann-Pick Cl disease gene: Homology to mediators of cholesterol homeostasis. Science. 277: 228-231.
28. Loftus, S. K., J. A. Morris, E. D. Carstea, J. Z. Gu, C. Cummings, A. Brown, J. Ellison, K. Ohno, M. A. Rosenfeld, D. A. Tagle, P. G. Pentchev, and W. J. Pavan. 1997. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science. 277: 232-235.
29. Cooper, M. K., J. A. Porter, K. E. Young, and P. A. Beachy. 1998. Teratogen-mediated inhibition of target tissue response to Shh signaling. Science. 280: 1603-1607.
30. Beachy, P. A., M. K. Cooper, K. E. Young, D. P. von Kessler, W. J. Park, T. M. Hall, D. J. Leahy, and J. A. Porter. 1997. Multiple roles of cholesterol in hedgehog protein biogenesis and signaling. Cold Spring Harb. Symp. Quant. Biol. 62: 191-204.
31. Goldstein, J. L., and M. Brown. 1990. Regulation of the mevalonate pathway. Nature. 343: 425-430.
32. Brown, M. S., and J. L. Goldstein. 1997. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell. 89: 331-340.
33. Gabilondo, A. M., J. Hegler, C. Krasel, V. Boivin-Jahns, L. Hein, and M. J. Lohse. 1997. A dileucine motif in the C terminus of the beta2-adrenergic receptor is involved in receptor internalization. Proc. Natl. Acad. Sci. USA. 94: 12285-12290.
34. Zhong, G., P. Romagnoli, and R. N. Germain. 1997. Related leucine-based cytoplasmic targeting signals in invariant chain and major histocompatibility complex class II molecules control endocytic presentation of distinct determinants in a single protein. J. Exp. Med. 185: 429-438.
35. Watari, H., E. J. Blanchette-Mackie, N. K. Dwyer, J. M. Glick, S. Patel, E. B. Nuefeld, R. O. Brady, P. G. Pentchev, and J. F. Strauss. 1999. Niemann-pick Cl protein: obligatory roles for N-terminal domains and lysosomal targeting in cholesterol mobilization. Proc. Natl. Acad. Sci. USA. 96: 805-810.
36. Patel, S. C., S. Suresh, U. Kumar, C. Y. Hu, A. Cooney, E. J. Blanchette-Mackie, E. B. Neufeld, R. C. Patel, R. O. Brady, Y. C. Patel, P. G. Pentchev, and W. Ong. 1999. Localization of Niemann-Pick Cl protein in astrocytes: implications for neuronal degeneration in Niemann-Pick type C disease. Proc. Natl. Acad. Sci. USA. 96: 1657-1662.
37. Neufeld, E. B., M. Wastney, S. Patel, S. Suresh, A. M. Cooney, N. K. Dwyer, C. F. Roff, K. Ohno, J. A. Morris, E. D. Carstea, J. P. Incardona, J. F. Strauss, M. T. Vanier, M. C. Patterson, R. O. Brady, P. G. Pentchev, and E. J. Blanchette-Machie. 1999. The Niemann-Pick Cl protein resides in a vesicular compartment linked to retrograd transport of multiple lysosomal cargo. J. Biol. Chem. 274: 9627-9635.
38. Higgins, M. E., J. P. Davies, F. W. Chen, and Y. A. Ioannou. 1999. Niemann-Pick Cl is a late endosome-resident protein that transiently associates with lysosomes and the trans-Golgi network. Mol. Genet. Metab. 68: 1-13.
39. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature. 387: 569-572.
40. Graham, J. M., T. Ford, and D. Rickwood. 1990. Isolation of the major subcellular organelles from mouse liver using Nycodenz gradients without the use of an ultracentrifuge. Anal. Biochem. 187: 318-323.
41. Lisanti, M. P., P. E. Scherer, J. Vidugiriene, Z. L. Tang, A. Hermanowski-Vosatka, Y. H. Tu, R. F. Cook, and M. Sargiacomo. 1994. Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: Implications for human disease. J. Cell Biol. 126: 111-126.
42. Laemmli, U. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227: 680-685.
43. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitroncellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76: 4350-4354.
44. Oram, J. R. 1986. Receptor-mediated transport of cholesterol between cultured cells and high density lipoprotein. Methods Enzymol. 129: 645-659.
45. Lange, Y., and T. L. Steck. 1994. Cholesterol homeostasis. Modulation by amphiphiles. J. Biol. Chem. 269: 29371-29374.
46. Porpaczy, Z., J. J. Tomasek, and D. A. Freeman. 1997. Internalized plasma membrane cholesterol passes through an endosomal compartment that is distinct from the acid vesicle-lysosome compartment. Exper. Cell Res. 234: 217-224.
47. Butler, J. D., J. Blanchette-Mackie, E. Goldin, R. R. O'Neill, G. Carstea, C. F. Roff, M. C. Patterson, S. Patel, M. E. Comly, A. Cooney, and P. G. Pentcher. 1992. Progesterone blocks cholesterol translocation from lysosomes. J. Biol. Chem. 267: 23797-23805.
48. Lange, Y., J. Ye, and T. L. Steck. 1998. Circulation of cholesterol between lysosomes and the plasma membrane. J. Biol. Chem. 273: 18915-18922.
49. Dupree, P., R. G. Parton, G. Raposo, T. V. Kurzchalia, and K. Simons. 1993. Caveolae and sorting in the trans-Golgi network of epithelial cells. EMBO J. 12: 1597-1605.
50. Zurzolo, C., W. van't Hof, G. van Meer, and E. Rodriguez-Boulan. 1994. VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. EMBO J. 13:42-53.
51. Kurzchalia, T. V., P. Dupree, and S. Monier. 1994. VIP21-Caveolin, a protein of the trans-golgi network and caveolae. FEBS Lett. 346: 88-91.
52. Smart, E. J., Y. S. Ying, P. A. Conrad, and R. G. Anderson. 1994. Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J. Cell Biol. 127: 1185-1197.
53. Smart, E. J., Y. Ying, W. C. Donzell, and R. G. Anderson. 1996. A role for caveolin in transport of cholesterol from endoplasmic reticulum to plasma membrane. J. Biol. Chem. 271: 29427-29435.
54. Garver, W. S., R. P. Erickson, J. M. Wilson, T. L. Colton, G. S. Hossain, M. A. Kozloski, and R. A. Heidenreich. 1997. 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.
55. Garver, W. S., G. S. Hossain, M. M. Winscott, and R. A. Heidenreich. 1999. The NPCl mutation causes an altered expression and phosphorylation of caveolin-1 in livers of mice with Niemann-Pick type C disease. Biochim. Biophys. Acta. 1453: 193-206.
56. Hailstones, D., L. S. Sleer, R. G. Parton, and K. K. Stanley. 1998. Regulation of caveolin and caveolae by cholesterol in MDCK cells. J. Lipid Res. 39: 369-379.
57. Fielding, C. J., A. Bist, and P. E. Fielding. 1997. Caveolin mRNA levels are up-regulated by free cholesterol and down-regulated by oxysterols in fibroblast monolayers. Proc. Natl. Acad. Sci. USA. 94: 3753-3758.
58. Uttenbogaard, A., Y. Ying, and E. J. Smart. 1998. Characterization of a cytosolic heat-shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking. J. Biol. Chem. 273: 6525-6532.
59. Roy, S., R. Leuttetforst, A. Harding, A. Apolloni, M. Etheridge, E. Stang, B. Rolls, J. F. Hancock, and R. G. Parton. 1999. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 1: 98-105.
60. Furuchi, T., and R. G. Anderson. 1998. Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase (ERK). J. Biol. Chem. 273: 21099-21104.