Niemann-Pick C1 protects against atherosclerosis in mice via regulation of macrophage intracellular cholesterol trafficking

Journal of Clinical Investigation

Volumn 118, Issue 6, 2008, Pages 2281-2290

  Zhang, Jessie R ^a   Coleman, Trey ^a   Langmade, S Joshua ^a   Scherrer, David E ^a   Lane, Lindsay ^a   Lanier, M Hunter ^a   Feng, Chu ^a   Sands, Mark S ^a   Schaffer, Jean E ^a   Semenkovich, Clay F ^a   Ory, Daniel S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

26 HYDROXYCHOLESTEROL; CELL PROTEIN; CHOLESTEROL; LIPOPROTEIN; LIVER X RECEPTOR; NIEMANN PICK C1; STEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; ARTICLE; BONE MARROW CELL; CHIMERA; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL SYNTHESIS; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DISEASE COURSE; GENE DELETION; HOMEOSTASIS; KNOCKOUT MOUSE; LIPID DIET; LIPOPROTEIN BLOOD LEVEL; MACROPHAGE; MOUSE; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEROL METABOLISM; WILD TYPE;

ANIMAL FEED; ANIMALS; AORTA; ATHEROSCLEROSIS; BIOLOGICAL TRANSPORT; CHOLESTEROL; HYDROXYCHOLESTEROLS; MACROPHAGES; MICE; MICE, TRANSGENIC; MODELS, BIOLOGICAL; OXIDATIVE STRESS; PROTEINS; STEROLS; TIME FACTORS;

EID: 45749136703     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI32561     Document Type: Article

References (58)

1. Ory, D. 2004. Nuclear receptor signaling in control of cholesterol homeostasis: Have the orphans found a home? Circ. Res. 95:660-670.
2. Ory, D.S. 2004. The Niemann-Pick disease genes: regulators of cellular cholesterol homeostasis. Trends Cardiovasc. Med. 14:66-72.
3. Chawla, A., Repa, J.J., Evans, R.M., and Mangelsdorf, D.J. 2001. Nuclear receptors and lipid physiology: opening the X-files. Science. 294:1866-1870.
4. Willy, P.J., et al. 1995. LXR, a nuclear receptor that defines a distinct retinoid response pathway. Genes Dev. 9:1033-1045.
5. Fu, X., et al. 2001. 27-hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells. J. Biol. Chem. 276:38378-38387.
6. Chen, W., Chen, G., Head, D.L., Mangelsdorf, D.J., and Russell, D.W. 2007. Enzymatic reduction of oxysterols impairs LXR signaling in cultured cells and the livers of mice. Cell Metab. 5:73-79.
7. Björkhem, I., and Muri-Boberg, K. 1995. Inborn errors in bile acid biosynthesis and storage of sterols other than cholesterol. In The metabolic and molecular bases of inherited disease. 7th edition. C.R. Scriver, et al., editors. McGraw-Hill. New York, New York, USA. 2073-2099.
8. Steinberg, S.J., Mondal, D., and Fensom, A.H. 1996. Co-cultivation of Niemann-Pick type C fibroblasts belonging to complementation groups a and b stimulates LDL-derived cholesrterol esterification. J. Inher. Metab. Dis. 19:769-774.
9. Vanier, M.T., Duthel, S., Rodriguez-Lafrasse, C., Pentchev, P., and Carstea, E.D. 1996. Genetic heterogeneity in Niemann-Pick C disease: a study using somatic cell hybridization and linkage analysis. Am. J. Hum. Genet. 58:118-125.
10. Millard, E.E., Srivastava, K., Traub, L., Schaffer, J.E., and Ory, D.S. 2000. NPC1 overexpression alters cellular cholesterol homeostasis. J. Biol. Chem. 275:38445-38451.
11. Neufeld, E.B., et al. 1996. Intracellular trafficking of cholesterol monitored with a cyclodextrin. J. Biol. Chem. 271:21604-21613.
12. Wojtanik, K.M., and Liscum, L. 2003. The transport of LDL-derived cholesterol to the plasma membrane is defective in NPC1 cells. J. Biol. Chem. 278:14850-14856.
13. Liscum, L., and Faust, J.R. 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.
14. Pentchev, P.G., et al. 1985. A defect in cholesterol esterification in Niemann-Pick disease (type C) patients. Proc. Natl. Acad. Sci. U. S. A. 82:8247-8251.
15. Chen, W., et al. 2001. Preferential ATP-binding cassette transporter A1-mediated cholesterol efflux from late endosomes/lysosomes. J. Biol. Chem. 276:43564-43569.
16. Choi, H.Y., et al. 2003. Impaired ABCA1-dependent lipid efflux and hypoalphalipoproteinemia in human Niemann-Pick type C disease. J. Biol. Chem. 278:32569-32577.
17. Frolov, A., et al. 2003. NPC1 and NPC2 regulate cellular cholesterol homeostasis through generation of LDL-derived oxysterols. J. Biol. Chem. 278:25517-25525.
18. Zhang, J., et al. 2004. The steroidal analog GW707 activates the SREBP pathway through disruption of intracellular cholesterol trafficking. J. Lipid Res. 45:223-231.
19. Morris, M.D., Bhuvaneswaran, C., Shio, H., and Fowler, S. 1982. Lysosome lipid storage disorder in NCTR/BALB/c mice. I. Description of the disease and genetics. Am. J. Pathol. 108:140-149.
20. Ishibashi, S., et al. 1993. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J. Clin. Invest. 92:883-893.
21. Liu, F., Poursine-Laurent, J., and Link, D.C. 2000. Expression of the G-CSF receptor on hematopoietic progenitor cells is not required for their mobilization by G-CSF. Blood. 95:3025-3031.
22. Towler, D.A., Bidder, M., Latifi, T., Coleman, T., and Semenkovich, C.F. 1998. Diet-induced diabetes activates an osteogenic gene regulatory program in the aortas of low density lipoprotein receptor-deficient mice. J. Biol. Chem. 273:30427-30434.
23. -/- mice. Circulation. 116:2444-2452.
24. Langmade, S.J., et al. 2006. Pregnane X receptor (PXR) activation: A mechanism for neuroprotection in a mouse model of Niemann-Pick C disease Proc. Natl. Acad. Sci. 103:13807-13812.
25. Burkard, I., von Eckardstein, A., Waeber, G., Vollenweider, P., and Rentsch, K.M. 2007. Lipoprotein distribution and biological variation of 24S- and 27-hydroxycholesterol in healthy volunteers. Atherosclerosis. 194:71-78.
26. Duane, W.C., and Javitt, N.B. 1999. 27-hydroxycholesterol: production rates in normal human subjects. J. Lipid Res. 40:1194-1199.
27. Babiker, A., et al. 1999. Elimination of cholesterol as cholestenoic acid in human lung by sterol 27-hydroxylase: evidence that most of this steroid in the circulation is of pulmonary origin. J. Lipid Res. 40:1417-1425.
28. Tint, G., et al. 1998. Cholesterol and oxygenated cholesterol concentrations are markedly elevated in peripheral tissue but not in brain from mice with Niemann-Pick type C phenotype. J. Inher. Metab. Dis. 21:853-863.
29. Lund, E., and Bjorkhem, I. 1995. Role of oxysterols in the regulation of cholesterol homeostasis: a critical evaluation. Acc. Chem. Res. 28:241-249.
30. Bjorkhem, I., and Diczfalusy, U. 2002. Oxysterols: friends, foes, or just fellow passengers. Arterioscler. Thromb. Vasc. Biol. 22:734-742.
31. Tam, S.P., Mok, L., Chimini, G., Vasa, M., and Deeley, R.G. 2006. ABCA1 mediates high-affinity uptake of 25-hydroxycholesterol by membrane vesicles and rapid efflux of oxysterol by intact cells. Am. J. Physiol. Cell Physiol. 291:C490-C502.
32. Terasaka, N., Wang, N., Yvan-Charvet, L., and Tall, A.R. 2007. High-density lipoprotein protects macrophages from oxidized low-density lipoproteininduced apoptosis by promoting efflux of 7-ketocholesterol via ABCG1. Proc. Natl. Acad. Sci. U. S. A. 104:15093-15098.
33. Wang, N., et al. 2007. ATP-binding cassette transporters G1 and G4 mediate cholesterol and desmosterol efflux to HDL and regulate sterol accumulation in the brain. FASEB J. 22:1073-1082.
34. Smith, L.L. 1981. Cholesterol autoxidation. Plenum Press. New York, New York, USA. 704 pp.
35. Borradaile, N.M., et al. 2006. A critical role for eukaryotic elongation factor 1A-1 in lipotoxic cell death. Mol. Biol. Cell. 17:770-778.
36. Boadu, E., et al. 2006. Correction of apolipoprotein AI-mediated lipid efflux and high density lipoprotein particle formation in human Niemann-Pick type C disease fibroblasts. J. Biol. Chem. 281:37081-37090.
37. Feng, B., et al. 2003. Niemann-Pick C heterozygosity confers resistance to lesional necrosis and macrophage apoptosis in murine atherosclerosis. Proc. Natl. Acad. Sci. U. S. A. 100:10423-10428.
38. Mari, M., et al. 2006. Mitochondrial free cholesterol loading sensitizes to TNF- and Fas-mediated steatohepatitis. Cell Metab. 4:185-198.
39. Yu, W., et al. 2005. Altered cholesterol metabolism in Niemann-Pick type C1 mouse brains affects mitochondrial function. J. Biol. Chem. 280:11731-11739.
40. Axelson, M., and Larsson, O. 1996. 27-hydroxylated low density lipoprotein (LDL) cholesterol can be converted to 7α,27-dihydroxy-4- cholesten-3-one (cytosterone) before suppressing cholesterol production in normal human fibroblasts. J. Biol. Chem. 271:12724-12736.
41. Wang, X., et al. 2007. Macrophage ABCA1 and ABCG1, but not SR-BI, promote macrophage reverse cholesterol transport in vivo. J. Clin. Invest. 117:2216-2224.
42. Aiello, R.J., et al. 2002. Increased atherosclerosis in hyperlipidemic mice with inactivation of ABCA1 in macrophages. Arterioscler. Thromb. Vasc. Biol. 22:630-637.
43. van Eck, M., et al. 2002. Leukocyte ABCA1 controls susceptibility to atherosclerosis and macrophage recruitment into tissues. Proc. Natl. Acad. Sci. U. S. A. 99:6298-6303.
44. Out, R., et al. 2007. Total body ABCG1 expression protects against early atherosclerotic lesion development in mice. Arterioscler. Thromb. Vasc. Biol. 27:594-599.
45. Yvan-Charvet, L., et al. 2007. Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J. Clin. Invest. 117:3900-3908.
46. Out, R., et al. 2008. Combined deletion of macrophage ABCA1 and ABCG1 leads to massive lipid accumulation in tissue macrophages and distinct atherosclerosis at relatively low plasma cholesterol levels. Arterioscler. Thromb. Vasc. Biol. 28:258-264.
47. Janssen-Heininger, Y.M., Poynter, M.E., and Baeuerle, P.A. 2000. Recent advances towards understanding redox mechanisms in the activation of nuclear factor kappaB. Free Radic. Biol. Med. 28:1317-1327.
48. de Winther, M.P., Kanters, E., Kraal, G., and Hofker, M.H. 2005. Nuclear factor kappaB signaling in atherogenesis. Arterioscler. Thromb. Vasc. Biol. 25:904-914.
49. Tordjman, K., et al. 2001. PPARα deficiency reduces insulin resistance and atherosclerosis in apoE-null mice. J. Clin. Invest. 107:1025-1034.
50. Usui, S., Hara, Y., Hosaki, S., and Okazaki, M. 2002. A new on-line dual enzymatic method for simultaneous quantification of cholesterol and triglycerides in lipoproteins by HPLC. J. Lipid Res. 43:805-814.
51. Semenkovich, C.F., Coleman, T., and Daugherty, A. 1998. Effects of heterozygous lipoprotein lipase deficiency on diet-induced atherosclerosis in mice. J. Lipid Res. 39:1141-1151.
52. Reid, P.C., et al. 2004. A novel cholesterol stain reveals early neuronal cholesterol accumulation in the Niemann-Pick type C1 mouse brain. J. Lipid Res. 45:582-591.
53. Jones, C., et al. 2007. Disruption of LDL but not VLDL clearance in autosomal recessive hypercholesterolemia. J. Clin. Invest. 117:165-174.
54. Abdel-Fattah, G., Fernandez, M.L., and McNamara, D.J. 1995. Regulation of guinea pig very low density lipoprotein secretion rates by dietary fat saturation. J. Lipid Res. 36:1188-1198.
55. Westover, E.J., et al. 2006. Rapid transient absorption and biliary secretion of enantiomeric cholesterol in hamsters. J. Lipid Res. 47:2374-2381.
56. Abe, T., et al. 2004. Kupffer cell-derived interleukin 10 is responsible for impaired bacterial clearance in bile duct-ligated mice. Hepatology. 40:414-423.
57. Mak, P.A., et al. 2002. Regulated expression of the apolipoprotein E/C-I/C-IV/C-II gene cluster in murine and human macrophages. A critical role for nuclear liver X receptors alpha and beta. J. Biol. Chem. 277:31900-31908.
58. Dzeletovic, S., Breuer, O., Lund, E., and Diczfalusy, U. 1995. Determination of cholesterol oxidation products in human plasma by isotope dilutionmass spectrometry. Anal. Biochem. 225:73-80.