Defective cholesterol trafficking in Niemann-Pick C-deficient cells

FEBS Letters

Volumn 584, Issue 13, 2010, Pages 2731-2739

  Peake, Kyle B ^a   Vance, Jean E ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Cholesterol; Cyclodextrin; Ganglioside; Late endosome lysosome; Neurodegeneration; Niemann Pick C

Indexed keywords

5ALPHA PREGNANE 3,20 DIONE; CHOLESTEROL; CYCLODEXTRIN; GANGLIOSIDE GM2; IMATINIB; MEMBRANE PROTEIN; MIGLUSTAT; NEUROSTEROID; NIEMANN PICK C1 PROTEIN; NIEMANN PICK C2 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; APOPTOSIS; BRAIN DISEASE; CELL MEMBRANE TRANSPORT; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; CLINICAL TRIAL; DEGENERATIVE DISEASE; DRUG EFFECT; DRUG MECHANISM; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; GAUCHER DISEASE; GENE MUTATION; HOMEOSTASIS; HUMAN; INTRACELLULAR TRANSPORT; LIVER DISEASE; LYSOSOME; NERVE CELL NECROSIS; NEUROLOGIC DISEASE; NIEMANN PICK DISEASE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; REVIEW; SINGLE DRUG DOSE;

ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CHOLESTEROL; GLYCOPROTEINS; HUMANS; MEMBRANE GLYCOPROTEINS; MICE; MODELS, BIOLOGICAL;

MUS;

EID: 77953721860     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.04.047     Document Type: Review

References (120)

1. Vanier M.T., Millat G. Niemann-Pick disease type C. Clin. Genet. 2003, 64:269-281.
2. Wraith J.E., et al. Natural history of Niemann-Pick disease type C in a multicentre observational retrospective cohort study. Mol. Genet. Metab. 2009, 98:250-254.
3. Brown M.S., Goldstein J.L. A receptor-mediated pathway for cholesterol homeostasis. Science 1986, 232:34-47.
4. Brown M.S., Goldstein J.L. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 1997, 89:331-340.
5. Pentchev P.G., Comly M.E., Kruth H.S., Vanier M.T., Wenger D.A., Patel S., Brady R.O. A defect in cholesterol esterification in Niemann-Pick disease (type C) patients. Proc. Natl. Acad. Sci. USA 1985, 82:8247-8251.
6. Liscum L., Faust J.R. Low density lipoprotein (LDL)-mediated suppression of cholesterol synthesis and LDL uptake is defective in Niemann-Pick type C fibroblasts. J. Biol. Chem. 1987, 262:17002-17008.
7. Blanchette-Mackie E.J., et al. 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 1988, 85:8022-8026.
8. Carstea E.D., et al. Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997, 277:228-231.
9. Loftus S.K., et al. Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 1997, 277:232-235.
10. Huang X., Suyama K., Buchanan J., Zhu A.J., Scott M.P. A Drosophila model of the Niemann-Pick type C lysosome storage disease: dnpc1a is required for molting and sterol homeostasis. Development 2005, 132:5115-5124.
11. Higgins M.E., Davies J.P., Chen F.W., Ioannou Y.A. Niemann-Pick C1 is a late endosome-resident protein that transiently associates with lysosomes and the trans-Golgi network. Mol. Genet. Metab. 1999, 68:1-13.
12. Neufeld E.B., et al. The Niemann-Pick C1 protein resides in a vesicular compartment linked to retrograde transport of multiple lysosomal cargo. J. Biol. Chem. 1999, 274:9627-9635.
13. Davies J.P., Ioannou Y.A. 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. 2000, 275:24367-24374.
14. Naureckiene S., Sleat D.E., Lackland H., Fensom A., Vanier M.T., Wattiaux R., Jadot M., Lobel P. Identification of HE1 as the second gene of Niemann-Pick C disease. Science 2000, 290:2298-2301.
15. Okamura N., et al. A porcine homolog of the major secretory protein of human epididymis, HE1, specifically binds cholesterol. Biochim. Biophys. Acta 1999, 1438:377-387.
16. Cheruku S.R., Xu Z., Dutia R., Lobel P., Storch J. Mechanism of cholesterol transfer from the Niemann-Pick type C2 protein to model membranes supports a role in lysosomal cholesterol transport. J. Biol. Chem. 2006, 281:31594-31604.
17. Vanier M.T., Duthel S., Rodriguez-Lafrasse C., Pentchev P., Carstea E.D. Genetic heterogeneity in Niemann-Pick C disease: a study using somatic cell hybridization and linkage analysis. Am. J. Hum. Genet. 1996, 58:118-125.
18. Sleat D.E., et al. Genetic evidence for nonredundant functional cooperativity between NPC1 and NPC2 in lipid transport. Proc. Natl. Acad. Sci. USA 2004, 101:5886-5891.
19. Infante R.E., Radhakrishnan A., Abi-Mosleh L., Kinch L.N., Wang M.L., Grishin N.V., Goldstein J.L., Brown M.S. Purified NPC1 protein: II. Localization of sterol binding to a 240-amino acid soluble luminal loop. J. Biol. Chem. 2008, 283:1064-1075.
20. Xu S., Benoff B., Liou H.L., Lobel P., Stock A.M. Structural basis of sterol binding by NPC2, a lysosomal protein deficient in Niemann-Pick type C2 disease. J. Biol. Chem. 2007, 282:23525-23531.
21. Infante R.E., Abi-Mosleh L., Radhakrishnan A., Dale J.D., Brown M.S., Goldstein J.L. Purified NPC1 protein. I. Binding of cholesterol and oxysterols to a 1278-amino acid membrane protein. J. Biol. Chem. 2008, 283:1052-1063.
22. Liu R., Lu P., Chu J.W., Sharom F.J. Characterization of fluorescent sterol binding to purified human NPC1. J. Biol. Chem. 2009, 284:1840-1852.
23. Kwon H.J., Abi-Mosleh L., Wang M.L., Deisenhofer J., Goldstein J.L., Brown M.S., Infante R.E. Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol. Cell 2009, 137:1213-1224.
24. Infante R.E., Wang M.L., Radhakrishnan A., Kwon H.J., Brown M.S., Goldstein J.L. NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes. Proc. Natl. Acad. Sci. USA 2008, 105:15287-15292.
25. Ohgami N., Ko D.C., Thomas M., Scott M.P., Chang C.C., Chang T.Y. Binding between the Niemann-Pick C1 protein and a photoactivatable cholesterol analog requires a functional sterol-sensing domain. Proc. Natl. Acad. Sci. USA 2004, 101:12473-12478.
26. Davies J.P., Chen F.W., Ioannou Y.A. Transmembrane molecular pump activity of Niemann-Pick C1 protein. Science 2000, 290:2295-2298.
27. Passeggio J., Liscum L. Flux of fatty acids through NPC1 lysosomes. J. Biol. Chem. 2005, 280:10333-10339.
28. Urano Y., Watanabe H., Murphy S.R., Shibuya Y., Geng Y., Peden A.A., Chang C.C., Chang T.Y. Transport of LDL-derived cholesterol from the NPC1 compartment to the ER involves the trans-Golgi network and the SNARE protein complex. Proc. Natl. Acad. Sci. USA 2008, 105:16513-16518.
29. Cruz J.C., Chang T.Y. Fate of endogenously synthesized cholesterol in Niemann-Pick type C1 cells. J. Biol. Chem. 2000, 275:41309-41316.
30. Wojtanik K.M., Liscum L. The transport of low density lipoprotein-derived cholesterol to the plasma membrane is defective in NPC1 cells. J. Biol. Chem. 2003, 278:14850-14856.
31. Liu B., Xie C., Richardson J.A., Turley S.D., Dietschy J.M. Receptor-mediated and bulk-phase endocytosis cause macrophage and cholesterol accumulation in Niemann-Pick C disease. J. Lipid Res. 2007, 48:1710-1723.
32. Shamburek R.D., et al. 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. 1997, 38:2422-2435.
33. Karten B., Peake K.B., Vance J.E. Mechanisms and consequences of impaired lipid trafficking in Niemann-Pick type C1-deficient mammalian cells. Biochim. Biophys. Acta 2009, 1791:659-670.
34. Lloyd-Evans E., et al. Niemann-Pick disease type C1 is a sphingosine storage disease that causes deregulation of lysosomal calcium. Nat. Med. 2008, 14:1247-1255.
35. Harmala A.S., Porn M.I., Mattjus P., Slotte J.P. Cholesterol transport from plasma membranes to intracellular membranes is inhibited by 3 beta-[2-(diethylamino)ethoxy]androst-5-en-17-one. Biochim. Biophys. Acta 1994, 1211:317-325.
36. Sexton R.C., Panini S.R., Azran F., Rudney H. Effects of 3 beta-[2-(diethylamino)ethoxy]androst-5-en-17-one on the synthesis of cholesterol and ubiquinone in rat intestinal epithelial cell cultures. Biochemistry 1983, 22:5687-5692.
37. Liu B., Li H., Repa J.J., Turley S.D., Dietschy J.M. Genetic variations and treatments that affect the lifespan of the NPC1 mouse. J. Lipid Res. 2008, 49:663-669.
38. Li H., Turley S.D., Liu B., Repa J.J., Dietschy J.M. GM2/GD2 and GM3 gangliosides have no effect on cellular cholesterol pools or turnover in normal or NPC1 mice. J. Lipid Res. 2008, 49:1816-1828.
39. Liu Y., et al. Alleviation of neuronal ganglioside storage does not improve the clinical course of the Niemann-Pick C disease mouse. Hum. Mol. Genet. 2000, 9:1087-1092.
40. Gondre-Lewis M.C., McGlynn R., Walkley S.U. Cholesterol accumulation in NPC1-deficient neurons is ganglioside dependent. Curr Biol 2003, 13:1324-1329.
41. Puri V., Watanabe R., Dominguez M., Sun X., Wheatley C.L., Marks D.L., Pagano R.E. Cholesterol modulates membrane traffic along the endocytic pathway in sphingolipid-storage diseases. Nat Cell Biol 1999, 1:386-388.
42. Puri V., Jefferson J.R., Singh R.D., Wheatley C.L., Marks D.L., Pagano R.E. Sphingolipid storage induces accumulation of intracellular cholesterol by stimulating SREBP-1 cleavage. J. Biol. Chem. 2003, 278:20961-20970.
43. Zervas M., Somers K.L., Thrall M.A., Walkley S.U. Critical role for glycosphingolipids in Niemann-Pick disease type C. Curr. Biol. 2001, 11:1283-1287.
44. Devlin, C., Pipalia, N.H., Liao, X., Schuchman, E.H., Maxfield, F.R. and Tabas, I. (in press). Improvement in lipid and protein trafficking in NPC1 cells by correction of a secondary enzyme defect. Traffic.
45. Patterson M.C., Vecchio D., Jacklin E., Abel L., Chadha-Boreham H., Luzy C., Giorgino R., Wraith J.E. Long-term miglustat therapy in children with Niemann-Pick disease type C. J. Child. Neurol. 2010, 25:300-305.
46. Pineda M., et al. Miglustat in patients with Niemann-Pick disease Type C (NP-C): a multicenter observational retrospective cohort study. Mol. Genet. Metab. 2009, 98:243-249.
47. Somsel Rodman J., Wandinger-Ness A. Rab GTPases coordinate endocytosis. J. Cell Sci. 2000, 113(Pt 2):183-192.
48. Choudhury A., Dominguez M., Puri V., Sharma D.K., Narita K., Wheatley C.L., Marks D.L., Pagano R.E. Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J. Clin. Invest. 2002, 109:1541-1550.
49. Choudhury A., Sharma D.K., Marks D.L., Pagano R.E. Elevated endosomal cholesterol levels in Niemann-Pick cells inhibit rab4 and perturb membrane recycling. Mol. Biol. Cell 2004, 15:4500-4511.
50. Kaptzan T., et al. Development of a Rab9 transgenic mouse and its ability to increase the lifespan of a murine model of Niemann-Pick type C disease. Am. J. Pathol. 2009, 174:14-20.
51. Schweitzer J.K., Pietrini S.D., D'Souza-Schorey C. ARF6-mediated endosome recycling reverses lipid accumulation defects in Niemann-Pick type C disease. PLoS One 2009, 4:e5193.
52. Goldman S.D., Krise J.P. Niemann-Pick C1 functions independently of Niemann-Pick C2 in the initial stage of retrograde transport of membrane-impermeable lysosomal cargo. J. Biol. Chem. 2010, 285:4983-4994.
53. Gong Y., Duvvuri M., Duncan M.B., Liu J., Krise J.P. Niemann-Pick C1 protein facilitates the efflux of the anticancer drug daunorubicin from cells according to a novel vesicle-mediated pathway. J. Pharmacol. Exp. Ther. 2006, 316:242-247.
54. Charman M., Kennedy B.E., Osborne N., Karten B. MLN64 mediates egress of cholesterol from endosomes to mitochondria in the absence of functional Niemann-Pick type C1 protein. J. Lipid Res. 2009, 51:1023-1034.
55. Fernandez A., Llacuna L., Fernandez-Checa J.C., Colell A. Mitochondrial cholesterol loading exacerbates amyloid beta peptide-induced inflammation and neurotoxicity. J. Neurosci. 2009, 29:6394-6405.
56. Mari M., et al. Mitochondrial free cholesterol loading sensitizes to TNF- and Fas-mediated steatohepatitis. Cell Metab. 2006, 4:185-198.
57. Yu W., Gong J.S., Ko M., Garver W.S., Yanagisawa K., Michikawa M. Altered cholesterol metabolism in Niemann-Pick type C1 mouse brains affects mitochondrial function. J. Biol. Chem. 2005, 280:11731-11739.
58. Xie C., Turley S.D., Dietschy J.M. Cholesterol accumulation in tissues of the Niemann-pick type C mouse is determined by the rate of lipoprotein-cholesterol uptake through the coated-pit pathway in each organ. Proc. Natl. Acad. Sci. USA 1999, 96:11992-11997.
59. Beltroy E.P., Richardson J.A., Horton J.D., Turley S.D., Dietschy J.M. Cholesterol accumulation and liver cell death in mice with Niemann-Pick type C disease. Hepatology 2005, 42:886-893.
60. Kelly D.A., Portmann B., Mowat A.P., Sherlock S., Lake B.D. Niemann-Pick disease type C: diagnosis and outcome in children, with particular reference to liver disease. J. Pediatr. 1993, 123:242-247.
61. Kulinski A., Vance J.E. Lipid homeostasis and lipoprotein secretion in Niemann-Pick C1-deficient hepatocytes. J. Biol. Chem. 2007, 282:1627-1637.
62. Wang M.D., Franklin V., Sundaram M., Kiss R.S., Ho K., Gallant M., Marcel Y.L. Differential regulation of ATP binding cassette protein A1 expression and ApoA-I lipidation by Niemann-Pick type C1 in murine hepatocytes and macrophages. J. Biol. Chem. 2007, 282:22525-22533.
63. Turley S.D., Burns D.K., Rosenfeld C.R., Dietschy J.M. Brain does not utilize low density lipoprotein-cholesterol during fetal and neonatal development in the sheep. J. Lipid Res. 1996, 37:1953-1961.
64. Quan G., Xie C., Dietschy J.M., Turley S.D. Ontogenesis and regulation of cholesterol metabolism in the central nervous system of the mouse. Brain Res. Dev. Brain Res. 2003, 146:87-98.
65. Nieweg K., Schaller H., Pfrieger F.W. Marked differences in cholesterol synthesis between neurons and glial cells from postnatal rats. J. Neurochem. 2009, 109:125-134.
66. Vance, J.E. and Hayashi, H. (in press) Formation and function of apolipoprotein E-containing lipoproteins in the nervous system. Biochim. Biophys. Acta.
67. Lund E.G., Xie C., Kotti T., Turley S.D., Dietschy J.M., Russell D.W. Knockout of the cholesterol 24-hydroxylase gene in mice reveals a brain-specific mechanism of cholesterol turnover. J. Biol. Chem. 2003, 278:22980-22988.
68. Xie C., Burns D.K., Turley S.D., Dietschy J.M. Cholesterol is sequestered in the brains of mice with Niemann-Pick type C disease but turnover is increased. J. Neuropathol. Exp. Neurol. 2000, 59:1106-1117.
69. Karten B., Vance D.E., Campenot R.B., Vance J.E. Cholesterol accumulates in cell bodies, but is decreased in distal axons, of Niemann-Pick C1-deficient neurons. J. Neurochem. 2002, 83:1154-1163.
70. Reid P.C., Sakashita N., Sugii S., Ohno-Iwashita Y., Shimada Y., Hickey W.F., Chang T.Y. A novel cholesterol stain reveals early neuronal cholesterol accumulation in the Niemann-Pick type C1 mouse brain. J. Lipid Res. 2004, 45:582-591.
71. German D.C., Quintero E.M., Liang C., Xie C., Dietschy J.M. Degeneration of neurons and glia in the Niemann-Pick C mouse is unrelated to the low-density lipoprotein receptor. Neuroscience 2001, 105:999-1005.
72. Erickson R.P., Garver W.S., Camargo F., Hossain G.S., Heidenreich R.A. Pharmacological and genetic modifications of somatic cholesterol do not substantially alter the course of CNS disease in Niemann-Pick C mice. J. Inherit Metab. Dis. 2000, 23:54-62.
73. Reid P.C., Lin S., Vanier M.T., Ohno-Iwashita Y., Harwood H.J., Hickey W.F., Chang C.C., Chang T.Y. Partial blockage of sterol biosynthesis with a squalene synthase inhibitor in early postnatal Niemann-Pick type C npcnih null mice brains reduces neuronal cholesterol accumulation, abrogates astrogliosis, but may inhibit myelin maturation. J. Neurosci. Methods 2008, 168:15-25.
74. Repa J.J., Li H., Frank-Cannon T.C., Valasek M.A., Turley S.D., Tansey M.G., Dietschy J.M. Liver X receptor activation enhances cholesterol loss from the brain, decreases neuroinflammation, and increases survival of the NPC1 mouse. J. Neurosci. 2007, 27:14470-14480.
75. Li H., Repa J.J., Valasek M.A., Beltroy E.P., Turley S.D., German D.C., Dietschy J.M. Molecular, anatomical, and biochemical events associated with neurodegeneration in mice with Niemann-Pick type C disease. J. Neuropathol. Exp. Neurol. 2005, 64:323-333.
76. Sarna J.R., Larouche M., Marzban H., Sillitoe R.V., Rancourt D.E., Hawkes R. Patterned Purkinje cell degeneration in mouse models of Niemann-Pick type C disease. J. Comp. Neurol. 2003, 456:279-291.
77. German D.C., Quintero E.M., Liang C.L., Ng B., Punia S., Xie C., Dietschy J.M. Selective neurodegeneration, without neurofibrillary tangles, in a mouse model of Niemann-Pick C disease. J. Comp. Neurol. 2001, 433:415-425.
78. Luan Z., Saito Y., Miyata H., Ohama E., Ninomiya H., Ohno K. Brainstem neuropathology in a mouse model of Niemann-Pick disease type C. J. Neurol. Sci. 2008, 268:108-116.
79. Ong W.Y., Kumar U., Switzer R.C., Sidhu A., Suresh G., Hu C.Y., Patel S.C. Neurodegeneration in Niemann-Pick type C disease mice. Exp. Brain Res. 2001, 141:218-231.
80. Amritraj A., Peake K., Kodam A., Salio C., Merighi A., Vance J.E., Kar S. Increased activity and altered subcellular distribution of lysosomal enzymes determine neuronal vulnerability in Niemann-Pick type C1-deficient mice. Am. J. Pathol. 2009, 175:2540-2556.
81. Ko D.C., Milenkovic L., Beier S.M., Manuel H., Buchanan J., Scott M.P. Cell-autonomous death of cerebellar purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet. 2005, 1:81-95.
82. Elrick M.J., Pacheco C.D., Yu T., Dadgar N., Shakkottai V.G., Ware C., Paulson H.L., Lieberman A.P. Conditional Niemann-Pick C mice demonstrate cell autonomous Purkinje cell neurodegeneration. Hum. Mol. Genet. 2010, 19:837-847.
83. -/- mouse brain. Am. J. Pathol. 2007, 171:962-975.
84. Pacheco C.D., Kunkel R., Lieberman A.P. Autophagy in Niemann-Pick C disease is dependent upon Beclin-1 and responsive to lipid trafficking defects. Hum. Mol. Genet. 2007, 16:1495-1503.
85. Wu Y.P., Mizukami H., Matsuda J., Saito Y., Proia R.L., Suzuki K. Apoptosis accompanied by up-regulation of TNF-alpha death pathway genes in the brain of Niemann-Pick type C disease. Mol. Genet. Metab. 2005, 84:9-17.
86. Alvarez A.R., et al. Imatinib therapy blocks cerebellar apoptosis and improves neurological symptoms in a mouse model of Niemann-Pick type C disease. FASEB J. 2008, 22:3617-3627.
87. Karten B., Vance D.E., Campenot R.B., Vance J.E. Trafficking of cholesterol from cell bodies to distal axons in Niemann-Pick C1-deficient neurons. J. Biol. Chem. 2003, 278:4168-4175.
88. Karten B., Campenot R.B., Vance D.E., Vance J.E. The Niemann-Pick C1 protein in recycling endosomes of presynaptic nerve terminals. J. Lipid Res. 2006, 47:504-514.
89. Wasser C.R., Ertunc M., Liu X., Kavalali E.T. Cholesterol-dependent balance between evoked and spontaneous synaptic vesicle recycling. J. Physiol. 2007, 579:413-429.
90. Xu S., Zhou S., Xia D., Xia J., Chen G., Duan S., Luo J. Defects of synaptic vesicle turnover at excitatory and inhibitory synapses in Niemann-Pick C1-deficient neurons. Neuroscience 2010, 167:608-620.
91. Zervas M., Dobrenis K., Walkley S.U. Neurons in Niemann-Pick disease type C accumulate gangliosides as well as unesterified cholesterol and undergo dendritic and axonal alterations. J. Neuropathol. Exp. Neurol. 2001, 60:49-64.
92. Bu B., Klunemann H., Suzuki K., Li J., Bird T., Jin L.W., Vincent I. Niemann-Pick disease type C yields possible clue for why cerebellar neurons do not form neurofibrillary tangles. Neurobiol. Dis. 2002, 11:285-297.
93. Suzuki K., Parker C.C., Pentchev P.G., Katz D., Ghetti B., D'Agostino A.N., Carstea E.D. Neurofibrillary tangles in Niemann-Pick disease type C. Acta Neuropathol. 1995, 89:227-238.
94. Bu B., Li J., Davies P., Vincent I. Deregulation of cdk5, hyperphosphorylation, and cytoskeletal pathology in the Niemann-Pick type C murine model. J. Neurosci. 2002, 22:6515-6525.
95. Karten B., Hayashi H., Francis G.A., Campenot R.B., Vance D.E., Vance J.E. Generation and function of astroglial lipoproteins from Niemann-Pick type C1-deficient mice. Biochem. J. 2005, 387:779-788.
96. Baudry M., Yao Y., Simmons D., Liu J., Bi X. Postnatal development of inflammation in a murine model of Niemann-Pick type C disease: immunohistochemical observations of microglia and astroglia. Exp. Neurol. 2003, 184:887-903.
97. Patel S.C., et al. Localization of Niemann-Pick C1 protein in astrocytes: implications for neuronal degeneration in Niemann-Pick type C disease. Proc. Natl. Acad. Sci. USA 1999, 96:1657-1662.
98. Chen G., Li H.M., Chen Y.R., Gu X.S., Duan S. Decreased estradiol release from astrocytes contributes to the neurodegeneration in a mouse model of Niemann-Pick disease type C. Glia 2007, 55:1509-1518.
99. -/- mice. J. Neurosci. Res. 2008, 86:2848-2856.
100. Nimmerjahn A., Kirchhoff F., Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318.
101. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996, 19:312-318.
102. German D.C., Liang C.L., Song T., Yazdani U., Xie C., Dietschy J.M. Neurodegeneration in the Niemann-Pick C mouse: glial involvement. Neuroscience 2002, 109:437-450.
103. Takikita S., Fukuda T., Mohri I., Yagi T., Suzuki K. Perturbed myelination process of premyelinating oligodendrocyte in Niemann-Pick type C mouse. J. Neuropathol. Exp. Neurol. 2004, 63:660-673.
104. Suzuki H., Sakiyama T., Harada N., Abe M., Tadokoro M. Pathologic changes of glial cells in murine model of Niemann-Pick disease type C: immunohistochemical, lectin-histochemical and ultrastructural observations. Pediatr. Int. 2003, 45:1-4.
105. Watabe K., et al. Establishment and characterization of immortalized Schwann cells from murine model of Niemann-Pick disease type C (spm/spm). J. Peripher. Nerv. Syst. 2001, 6:85-94.
106. Higashi Y., Murayama S., Pentchev P.G., Suzuki K. Peripheral nerve pathology in Niemann-Pick type C mouse. Acta Neuropathol. 1995, 90:158-163.
107. Goodrum J.F., Pentchev P.G. Cholesterol reutilization during myelination of regenerating PNS axons is impaired in Niemann-Pick disease type C mice. J. Neurosci. Res. 1997, 49:389-392.
108. Goodrum J.F., Brown J.C., Fowler K.A., Bouldin T.W. Axonal regeneration, but not myelination, is partially dependent on local cholesterol reutilization in regenerating nerve. J. Neuropathol. Exp. Neurol. 2000, 59:1002-1010.
109. Cox T., et al. Novel oral treatment of Gaucher's disease with N-butyldeoxynojirimycin (OGT 918) to decrease substrate biosynthesis. Lancet 2000, 355:1481-1485.
110. Griffin L.D., Gong W., Verot L., Mellon S.H. Niemann-Pick type C disease involves disrupted neurosteroidogenesis and responds to allopregnanolone. Nat. Med. 2004, 10:704-711.
111. Ahmad I., et al. Allopregnanolone treatment, both as a single injection or repetitively, delays demyelination and enhances survival of Niemann-Pick C mice. J. Neurosci. Res. 2005, 82:811-821.
112. -/- mouse brain. Brain Res. 2009, 1270:140-151.
113. Langmade S.J., et al. Pregnane X receptor (PXR) activation: a mechanism for neuroprotection in a mouse model of Niemann-Pick C disease. Proc. Natl. Acad. Sci. USA 2006, 103:13807-13812.
114. Kilsdonk E.P., Yancey P.G., Stoudt G.W., Bangerter F.W., Johnson W.J., Phillips M.C., Rothblat G.H. Cellular cholesterol efflux mediated by cyclodextrins. J. Biol. Chem. 1995, 270:17250-17256.
115. -/- mouse. Proc. Natl. Acad. Sci. USA 2009, 106:2377-2382.
116. Davidson C.D., et al. Chronic cyclodextrin treatment of murine Niemann-Pick C disease ameliorates neuronal cholesterol and glycosphingolipid storage and disease progression. PLoS One 2009, 4:e6951.
117. Abi-Mosleh L., Infante R.E., Radhakrishnan A., Goldstein J.L., Brown M.S. Cyclodextrin overcomes deficient lysosome-to-endoplasmic reticulum transport of cholesterol in Niemann-Pick type C cells. Proc. Natl. Acad. Sci. USA 2009, 106:19316-19321.
118. Rosenbaum A.I., Zhang G., Warren J.D., Maxfield F.R. Endocytosis of beta-cyclodextrins is responsible for cholesterol reduction in Niemann-Pick type C mutant cells. Proc. Natl. Acad. Sci. USA 2010, 107:5477-5482.
119. Yanjanin N.M., et al. Linear clinical progression, independent of age of onset, in Niemann-Pick disease, type C. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2010, 153B:132-140.
120. Liu B., Ramirez C.M., Miller A.M., Repa J.J., Turley S.D., Dietschy J.M. Cyclodextrin overcomes the transport defect in nearly every organ of the newborn or mature NPC1 mouse leading to excretion of the sequestered cholesterol as bile acid. J. Lipid Res. 2010, 51:933-944.