Cyclodextrin mediates rapid changes in lipid balance in Npc1-/- mice without carrying cholesterol through the bloodstream

Journal of Lipid Research

Volumn 53, Issue 11, 2012, Pages 2331-2342

  Taylor, Anna M ^a   Liu, Bing ^a   Mari, Yelenis ^a   Liu, Benny ^a   Repa, Joyce J ^a  

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

Author keywords

Cholesterol balance; Hippocampal neurons; Inflammation; Lipoprotein profiles; Liver; Lysosome; Macrophage; Niemann Pick type C; Spleen

Indexed keywords

2 HYDROXYPROPYL BETA CYCLODEXTRIN; BETA CYCLODEXTRIN SULFOBUTYL ETHER; CD68 ANTIGEN; CHOLESTEROL; CHOLESTEROL ESTER; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 6; LIPID; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOACCUMULATION; BLOOD FLOW; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFECT; DRUG MECHANISM; DRUG RESPONSE; FEMALE; HOMEOSTASIS; LIPID ANALYSIS; LIPID METABOLISM; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LIPID INTERACTION; SINGLE DRUG DOSE;

ANIMALS; BETA-CYCLODEXTRINS; CELLS, CULTURED; CHOLESTEROL; CYTOKINES; LIPID METABOLISM; LIPOPROTEINS; LYSOSOMES; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; NIEMANN-PICK DISEASE, TYPE C; PROTEINS;

EID: 84867365407     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M028241     Document Type: Article

References (51)

1. Irie, T., K. Fukunaga, M. K. Garwood, T. O. Carpenter, J. Pitha, and J. Pitha. 1992. Hydroxypropylcyclodextrins in parenteral use. II: Effects on transport and disposition of lipids in rabbit and humans. J. Pharm. Sci. 81: 524-528.
2. 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)
3. Stella, V. J., and Q. He. 2008. Cyclodextrins. Toxicol. Pathol. 36: 30-42.
4. Gould, S., and R. C. Scott. 2005. 2-Hydroxypropyl-β-cyclodextrin (HP-β-CD): a toxicology review. Food Chem. Toxicol. 43: 1451-1459.
5. -/- mouse. Proc. Natl. Acad. Sci. USA. 106: 2377-2382.
6. Patterson, M. C. 2003. A riddle wrapped in a mystery: understanding Niemann-Pick disease, type C. Neurologist. 9: 301-310. (Pubitemid 37484849)
7. Patterson, M. C., M. T. Vanier, K. Suzuki, J. A. Morris, E. D. Carstea, E. B. Neufeld, J. E. Blanchette-Mackie, and P. G. Pentchev. 2001. Niemann-Pick Disease Type C: a lipid trafficking disorder. In The Metabolic and Molecular Bases of Inherited Disease. C. R. Scriver, editor. McGraw-Hill, New York. 3611-3633.
8. Vanier, M. T. 2010. Niemann-Pick disease type C. Orphanet J. Rare Dis. 5: 16.
9. 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.
10. Ward, S., P. O'Donnell, S. Fernandez, and C. H. Vite. 2010. 2-Hydroxypropyl-β-cyclodextrin raises hearing threshold in normal cats and in cats with Niemann-Pick type C disease. Pediatr. Res. 68: 52-56.
11. 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 neuornal cholesterol and glycosphingolipid storage and disease progression. PLoS ONE. 4: e6951.
12. Ramirez, C. M., B. Liu, 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.
13. Aqul, A., B. Liu, C. M. Ramirez, A. A. Pieper, S. J. Estill, D. K. Burns, B. Liu, J. J. Repa, S. D. Turley, and J. M. Dietschy. 2011. Unesterified cholesterol accumulation in late endosomes/lysosomes causes neurodegeneration and is prevented by driving cholesterol export from this compartment. J. Neurosci. 31: 9404-9413.
14. 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.
15. Rosenbaum, A. I., G. Zhang, J. D. Warren, and F. R. Maxfield. 2010. Endocytosis of beta-cyclodextrins is responsible for cholesterol reduction in Niemann-Pick type C mutant cells. Proc. Natl. Acad. Sci. USA. 107: 5477-5482.
16. McCauliff, L. A., Z. Xu, and J. Storch. 2011. Sterol transfer between cyclodextrin and membranes: similar but not identical mechanism to NPC2-mediated cholesterol transfer. Biochemistry. 50: 7341-7349.
17. Ramirez, C. M., B. Liu, A. Aqul, A. M. Taylor, J. J. Repa, S. D. Turley, and J. M. Dietschy. 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. 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.
19. 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)
20. Dietschy, J. M., and D. K. Spady. 1984. Measurement of rates of cholesterol synthesis using tritiated water. J. Lipid Res. 25: 1469-1476. (Pubitemid 15169463)
21. Turley, S. D., M. W. Herndon, and J. M. Dietschy. 1994. Reevaluation and application of the dual-isotope plasma ratio method for the measurement of intestinal cholesterol absorption in the hamster. J. Lipid Res. 35: 328-339. (Pubitemid 24050446)
22. Beltroy, E. P., B. Liu, J. M. Dietschy, and S. D. Turley. 2007. Lysosomal unesterifed cholesterol content correlates with liver cell death in murine Niemann-Pick type C disease. J. Lipid Res. 48: 869-881. (Pubitemid 46557892)
23. Valasek, M. A., J. Weng, P. W. Shaul, R. G. W. Anderson, and J. J. Repa. 2005. Caveolin-1 is not required for murine intestinal cholesterol transport. J. Biol. Chem. 280: 28103-28109. (Pubitemid 41076928)
24. 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. (Pubitemid 39119058)
25. Schmittgen, T. D., and K. J. Livak. 2008. Analyzing real-time PCR data by the comparative C T method. Nat. Protoc. 3: 1101-1108. (Pubitemid 351818697)
26. Dheda, K., J. F. Huggett, S. A. Bustin, M. A. Johnson, G. Rook, and A. Zumla. 2004. Validation of housekeeping genes for normalizing RNA expression in real-time PCR. Biotechniques. 37: 112-114, 116, 118-119.
27. Kosir, R., J. Acimovic, M. Golicnik, M. Perse, G. Majdic, M. Fink, and D. Rozman. 2010. Determination of reference genes for circadian studies in different tissues and mouse strains. BMC Mol. Biol. 11: 60.
28. Li, H., J. J. Repa, M. A. Valasek, E. P. Beltroy, S. D. Turley, D. C. German, and J. M. Dietschy. 2005. Molecular, anatomical, and biochemical events associated with neurodegeneration in mice with Niemann-Pick Type C disease. J. Neuropathol. Exp. Neurol. 64: 323-333. (Pubitemid 40489559)
29. Jo, Y., and R. A. DeBose-Boyd. 2010. Control of cholesterol synthesis through regulated ER-associated degradation of HMG CoA reductase. Crit. Rev. Biochem. Mol. Biol. 45: 185-198.
30. Panda, S., M. P. Antoch, B. H. Miller, A. I. Su, A. B. Schook, M. Straume, P. G. Schultz, S. A. Kay, J. S. Takahashi, and J. B. Hogenesch. 2002. Coordinated transcription of key pathways in the mouse by the circadian clock. Cell. 109: 307-320. (Pubitemid 34606874)
31. Singaraja, R. R., E. R. James, J. Crim, H. Visscher, A. Chatterjee, and M. R. Hayden. 2005. Alternate transcripts expressed in response to diet reflect tissue-specific regulation of ABCA1. J. Lipid Res. 46: 2061-2071. (Pubitemid 41377458)
32. Xie, C., D. K. Burns, S. D. Turley, and J. M. Dietschy. 2000. Cholesterol is sequestered in the brains of mice with Niemann-Pick Type C disease but turnover is increased. J. Neuropathol. Exp. Neurol. 59: 1106-1117. (Pubitemid 32006313)
33. Wu, Y-P., H. Mizukami, J. Matsuda, Y. Saito, R. L. Proia, and K. Suzuki. 2005. Apoptosis accompanied by up-regulation of TNF-α death pathway genes in the brain of Niemann-Pick type C disease. Mol. Genet. Metab. 84: 9-17. (Pubitemid 40082600)
34. Langmade, S. J., S. E. Gale, A. Frolov, I. Mohri, K. Suzuki, S. H. Mellon, S. U. Walkley, D. F. Covey, J. E. Schaffer, and D. S. Ory. 2006. Pregnane X receptor (PXR) activation: a mechanism for neuroprotection in a mouse model of Niemann-Pick C disease. Proc. Natl. Acad. Sci. USA. 103: 13807-13812. (Pubitemid 44413989)
35. 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.
36. Yancey, P. G., W. V. Rodriguez, E. P. C. Kilsdonk, G. W. Stoudt, W. J. Johnson, M. C. Phillips, and G. H. Rothblat. 1996. Cellular cholesterol efflux mediated by cyclodextrins. Demonstration of kinetic pools and mechanism of efflux. J. Biol. Chem. 271: 16026-16034. (Pubitemid 26236215)
37. 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. (Pubitemid 27097681)
38. Zidovetzki, R., and I. Levitan. 2007. Use of cyclodextrins to manipulate plasma membrane cholesterol content: evidence, misconceptions and control strategies. Biochim. Biophys. Acta. 1768: 1311-1324. (Pubitemid 46782714)
39. Puglisi, G., M. Fresta, and C. A. Ventura. 1996. Interaction of natural and modified β-cyclodextrins with a biological membrane model of dipalmitoylphosphatidylcholine. J. Colloid Interface Sci. 180: 542-547. (Pubitemid 26233934)
40. López, C. A., A. H. de Vries, and S. J. Marrink. 2011. Molecular mechanism of cyclodextrin mediated cholesterol extraction. PLOS Comput. Biol. 7: e1002020.
41. Rajewski, R. A., G. Traiger, J. Bresnahan, P. Jaberaboansari, V. J. Stella, and D. O. Thompson. 1995. Preliminary safety evaluation of parenterally administered sulfoalkyl ether β-cyclodextrin derivatives. J. Pharm. Sci. 84: 927-932.
42. 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.
43. Deffieu, M. S., and S. R. Pfeffer. 2011. Niemann-Pick type C 1 function requires lumenal domain residues that mediate cholesterol-dependent NPC2 binding. Proc. Natl. Acad. Sci. USA. 108: 18932-18936.
44. Lachmann, R. 2010. Treatments for lysosomal storage disorders. Biochem. Soc. Trans. 38: 1465-1468.
45. Urbanelli, L., A. Magini, A. Polchi, M. Polidoro, and C. Emiliani. 2011. Recent developments in therapeutic approaches for lysosomal storage diseases. Recent Pat. CNS Drug Discov. 6: 1-19.
46. Alvarez, A. R., A. Klein, J. Castro, G. I. Cancino, J. Amigo, M. Mosqueira, L. M. Vargas, L. F. Yevenes, F. C. Bronfman, and S. Zanlungo. 2008. Imatinib therapy blocks cerebellar apoptosis and improves neurological symptoms in a mouse model of Niemann-Pick type C disease. FASEB J. 22: 3617-3627.
47. Smith, D., K-L. Wallom, I. M. Williams, M. Jeyakumar, and F. M. Platt. 2009. Beneficial effects of anti-inflammatory therapy in a mouse model of Niemann-Pick disease type C1. Neurobiol. Dis. 36: 242-251.
48. Zervas, M., K. L. Somers, M. A. Thrall, and S. U. Walkley. 2001. Critical role for glycosphingolipids in Niemann-Pick disease type C. Curr. Biol. 11: 1283-1287. (Pubitemid 32774086)
49. Plazzo, A. P., C. T. Höfer, L. Jicinszky, E. Fenyvesi, L. Szente, J. Schiller, A. Herrmann, and P. Muller. 2012. Uptake of a fluorescent methyl-β-cyclodextrin via clathrin-dependent endocytosis. Chem. Phys. Lipids. 165: 505-511.
50. Peake, K. B., and J. E. Vance. 2012. Normalization of cholesterol homeostasis by 2-hydroxypropyl-β-cyclodextrin in neurons and glia from Niemann-Pick C1 (NPC1)-deficient mice. J. Biol. Chem. 287: 9290-9298.
51. Pitha, J., A. Gerloczy, and A. Olivi. 1994. Parenteral hydroxypropyl cyclodextrins: intravenous and intracerebral administration of lipophiles. J. Pharm. Sci. 83: 833-837. (Pubitemid 24233760)