Quantitative role of LAL, NPC2, and NPC1 in lysosomal cholesterol processing defined by genetic and pharmacological manipulations

Journal of Lipid Research

Volumn 52, Issue 4, 2011, Pages 688-698

  Ramirez, Charina M ^a   Liu, Benny ^a   Aqul, Amal ^a   Taylor, Anna M ^a   Repa, Joyce J ^a   Turley, Stephen D ^a   Dietschy, John M ^a  

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

Author keywords

Cholesterol balance; Inflammation; Liver disease; Lysosomal acid lipase; Macrophage; Neurodegeneration; Niemann Pick type C disease; Wolman disease

Indexed keywords

ACID LIPASE; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CELL PROTEIN; CHOLESTEROL; CYCLODEXTRIN; LYSOSOMAL ACID LIPASE; MESSENGER RNA; NIEMANN PICK C1 PROTEIN; NIEMANN PICK C2 PROTEIN; UNCLASSIFIED DRUG;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BRAIN; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DIETARY INTAKE; ENZYME ACTIVITY; GENETIC MANIPULATION; KIDNEY; LIVER FUNCTION TEST; MOLECULAR INTERACTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; BIOLOGICAL TRANSPORT; CHOLESTEROL; CYCLODEXTRINS; LIPID METABOLISM; LIVER FUNCTION TESTS; LYSOSOMES; MICE; MICE, INBRED BALB C; MICE, MUTANT STRAINS; POLYMERASE CHAIN REACTION; PROTEINS; STEROL ESTERASE; VESICULAR TRANSPORT PROTEINS;

EID: 79953314773     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M013789     Document Type: Article

References (43)

1. Brown, M. S., and J. L. Goldstein. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science. 232: 34-47.
2. Liu, B., C. Xie, J. A. Richardson, S. D. Turley, and J. M. Dietschy. 2007. Receptor-mediated and bulk-phase endocytosis cause macrophage and cholesterol accumulation in Niemann-Pick C disease. J. Lipid Res. 48: 1710-1723.
3. Du, H., M. Duanmu, D. Witte, and G. A. Grabowski. 1998. Targeted disruption of the mouse lysosomal acid lipase gene: long-term survival with massive cholesteryl ester and triglyceride storage. Hum. Mol. Genet. 7: 1347-1354.
4. Naureckiene, S., D. E. Sleat, H. Lackland, A. Fensom, M. T. Vanier, R. Wattiaux, M. Jadot, and P. Lobel. 2000. Identification of HE1 as the second gene of Niemann-Pick C disease. Science. 290: 2298-2301. (Pubitemid 32041569)
5. Carstea, E. D., J. A. Morris, K. G. Coleman, S. K. Loftus, D. Zhang, C. Cummings, J. Gu, M. A. Rosenfeld, W. J. Pavan, D. B. Krizman, et al. 1997. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science. 277: 228-231. (Pubitemid 27446076)
6. Goldstein, J. L., R. A. DeBose-Boyd, and M. S. Brown. 2006. Protein sensors for membrane sterols. Cell. 124: 35-46.
7. Chawla, A., J. J. Repa, R. M. Evans, and D. J. Mangelsdorf. 2001. Nuclear receptors and lipid physiology: opening the X-files. Science. 294: 1866-1870.
8. -/- mouse. Proc. Natl. Acad. Sci. USA. 106: 2377-2382.
9. Ramirez, C. M., B. L. Li, A. M. Taylor, J. J. Repa, D. K. Burns, A. G. Weinberg, S. D. Turley, and J. M. Dietschy. 2010. Weekly cyclodextrin administration normalizes cholesterol metabolism in nearly every organ of the Niemann-Pick type C1 mouse and markedly prolongs life. Pediatr. Res. 68: 309-315.
10. Davidson, C. D., N. F. Ali, M. C. Micsenyi, G. Stephney, S. Renault, K. Dobrenis, D. S. Ory, M. T. Vanier, and S. U. Walkley. 2009. Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS ONE. 4: e6951.
11. Thompson, D. O. 1997. Cyclodextrins-enabling excipients: their present and future use in pharmaceuticals. Crit. Rev. Ther. Drug Carrier Syst. 14: 1-104. (Pubitemid 27079973)
12. Christian, A. E., M. P. Haynes, M. C. Phillips, and G. H. Rothblat. 1997. Use of cyclodextrins for manipulating cellular cholesterol content. J. Lipid Res. 38: 2264-2272.
13. Small, D. M. 2003. Role of ABC transporters in secretion of cholesterol from liver into bile. Proc. Natl. Acad. Sci. USA. 100: 4-6. (Pubitemid 36078019)
14. Liu, B., C. M. Ramirez, A. M. Miller, J. J. Repa, S. D. Turley, and J. M. Dietschy. 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.
15. Okahata, Y., and Y. Xuanjing. 1989. Molecular selective assocations of cyclodextrins with lipid or cholesterol multibilayers cast on a piezoelectric crystal. J. Chem. Soc. Chem. Commun. 1147-1149.
16. Miyajima, K., H. Saito, and M. Nakagai. 1987. Interaction of cyclodextrins with lipid membrane. J. Chem. Soc. Jpn. 306: 306-312.
17. Sleat, D. E., J. A. Wiseman, M. El-Banna, S. M. Price, L. Verot, M. M. Shen, G. S. Tint, M. T. Vanier, S. U. Walkley, and P. Lobel. 2004. Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc. Natl. Acad. Sci. USA. 101: 5886-5891. (Pubitemid 38520498)
18. 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, et al. 1997. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science. 277: 232-235. (Pubitemid 27446077)
19. Xie, C., S. D. Turley, P. G. Pentchev, and J. M. Dietschy. 1999. Cholesterol balance and metabolism in mice with loss of function of Niemann-Pick C protein. Am. J. Physiol. 276: E336-E344.
20. Du, H., T. L. Cameron, S. J. Garger, G. P. Pogue, L. A. Hamm, E. White, K. M. Hanley, and G. A. Grabowski. 2008. Wolman disease/cholesteryl ester storage disease: efficacy of plant-produced human lysosomal acid lipase in mice. J. Lipid Res. 49: 1646-1657.
21. Liu, B., H. Li, J. J. Repa, S. D. Turley, and J. M. Dietschy. 2008. Genetic variations and treatments that affect the lifespan of the NPC1 mouse. J. Lipid Res. 49: 663-669.
22. Repa, J. J., S. D. Turley, G. Quan, and J. M. Dietschy. 2005. Delineation of molecular changes in intrahepatic cholesterol metabolism resulting from diminished cholesterol absorption. J. Lipid Res. 46: 779-789.
23. Beltroy, E. P., B. Liu, J. M. Dietschy, and S. D. Turley. 2007. Lysosomal unesterified cholesterol content correlates with liver cell death in murine Niemann-Pick type C disease. J. Lipid Res. 48: 869-881.
24. Valasek, M. A., and J. J. Repa. 2005. The power of real-time PCR. Adv. Physiol. Educ. 29: 151-159.
25. Kurrasch, D. M., J. Huang, T. M. Wilkie, and J. J. Repa. 2004. Quantitative real-time polymerase chain reaction measurement of regulators of G-protein signaling mRNA levels in mouse tissues. Methods Enzymol. 389: 3-15.
26. Xie, C., E. G. Lund, S. D. Turley, D. W. Russell, and J. M. Dietschy. 2003. Quantitation of two pathways for cholesterol excretion from the brain in normal mice and mice with neurodegeneration. J. Lipid Res. 44: 1780-1789.
27. DeBose-Boyd, R. A. 2008. Feedback regulation of cholesterol synthesis: sterol-accelerated ubiquitination and degradation of HMG CoA reductase. Cell Res. 18: 609-621.
28. Frijlink, H. W., J. Visser, N. R. Hefting, R. Oosting, D. K. Meijer, and C. F. Lerk. 1990. The pharmacokinetics of β-cyclodextrin and hydroxypropyl-β-cyclodextrin in the rat. Pharm. Res. 7: 1248-1252.
29. Saito, A., H. Sato, N. Iino, and T. Takeda. 2010. Molecular mechanisms of receptor-mediated endocytosis in the renal proximal tubular epithelium. J. Biomed. Biotechnol. 2010: 1-7.
30. Small, D. M. 1977. Liquid crystals in living and dying systems. J. Colloid Interface Sci. 58: 581-602.
31. Rajewski, R. A., G. Traiger, J. Breshahan, P. Jaberaboansari, V. J. Stella, and D. O. Thompson. 1995. Preliminary safety evaluation of parenterally administered sulfoalkyl ether beta-cyclodextrin derivatives. J. Pharm. Sci. 84: 927-932.
32. Dietschy, J. M. 2009. Central nervous system: cholesterol turnover, brain development and neurodegeneration. Biol. Chem. 390: 287-293.
33. Posse de Chaves, E. I., D. E. Vance, R. B. Campenot, R. S. Kiss, and J. E. Vance. 2000. Uptake of lipoproteins for axonal growth of sympathetic neurons. J. Biol. Chem. 275: 19883-19890.
34. Repa, J. J., H. Li, T. C. Frank-Cannon, M. A. Valasek, S. D. Turley, M. G. Tansey, and J. M. Dietschy. 2007. Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse. J. Neurosci. 27: 14470-14480.
35. Hamilton, J. A., and D. M. Small. 1982. Solubilization and localization of cholesteryl oleate in egg phosphatidylcholine vesicles. J. Biol. Chem. 257: 7318-7321.
36. Chevallier, J., Z. Chamoun, G. Jiang, G. Prestwich, N. Sakai, S. Matile, R. G. Parton, and J. Gruenberg. 2008. Lysobisphosphatidic acid controls endosomal cholesterol levels. J. Biol. Chem. 283: 27871-27880.
37. Golan, D. E., M. R. Alecio, W. R. Veatch, and R. R. Rando. 1984. Lateral mobility of phospholipid and cholesterol in the human erythrocyte membrane: effects of protein-lipid interactions. Biochemistry. 23: 332-339.
38. Goodman, D. S., R. P. Noble, and R. B. Dell. 1973. Three-pool model of the long-term turnover of plasma cholesterol in man. J. Lipid Res. 14: 178-188.
39. Atger, V. M., M. de la Llera Moya, G. W. Stoudt, W. V. Rodrigueza, M. C. Phillips, and G. H. Rothblat. 1997. Cyclodextrins as catalysts for the removal of cholesterol from macrophage foam cells. J. Clin. Invest. 99: 773-780.
40. Kwon, H. J., L. Abi-Mosleh, M. L. Wang, J. Deisenhofer, J. L. Goldstein, M. S. Brown, and R. E. Infante. 2009. Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell. 137: 1213-1224.
41. Abi-Mosleh, L., R. E. Infante, A. Radhakrishnan, J. L. Goldstein, and M. S. Brown. 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.
42. Möbius, W., E. van Donselaar, Y. Ohno-Iwashita, Y. Shimada, H. F. G. Heijnen, J. W. Slot, and H. J. Geuze. 2003. Recycling compartments and the internal vesicles of multivesicular bodiesharbor most of the cholesterol found in the endocytic pathway. Traffic. 4: 222-231.
43. Pentchev, P. G., E. J. Blanchette-Mackie, and E. A. Dawidowicz. 1994. The NP-C gene: a key to pathways of intracellular cholesterol transport. Trends Cell Biol. 4: 365-369.