Regulation of lipid droplet cholesterol efflux from macrophage foam cells

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 3, 2012, Pages 575-581

  Ouimet, Mireille ^a   Marcel, Yves L ^a  

^a UNIVERSITY OF OTTAWA HEART INSTITUTE   (Canada)

Author keywords

atherosclerosis; foam cells; lipoproteins; macrophages

Indexed keywords

ABC TRANSPORTER A1; ACID LIPASE; ADIPOPHILIN; APOLIPOPROTEIN A1; APOLIPOPROTEIN A4; AUTOPHAGY PROTEIN 5; CARBOXYLESTERASE; CARBOXYLESTERASE 1; CHAPERONE; CHOLESTEROL ACYLTRANSFERASE; CHOLESTEROL ESTER; CHOLESTEROL ESTERASE; COAT PROTEIN; FAT DROPLET; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HORMONE SENSITIVE LIPASE; NEUTRAL CHOLESTEROL ESTER HYDROLASE 1; OXIDIZED LOW DENSITY LIPOPROTEIN; PERILIPIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; TIP47 PROTEIN; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN;

ATHEROGENESIS; ATHEROSCLEROSIS; AUTOPHAGOSOME; CACHEXIA; CELL LEVEL; CELL MEMBRANE; CHOLESTEROL ESTER STORAGE DISEASE; CHOLESTEROL TRANSPORT; CORONARY ARTERY DISEASE; CYTOPLASM; CYTOSOL; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; ENDOSOME; ENDOTHELIUM CELL; ENZYME ACTIVITY; FEEDBACK SYSTEM; FOAM CELL; GAIN OF FUNCTION MUTATION; GOLGI COMPLEX; HUMAN; LIPID BILAYER; LIPID HYDROLYSIS; LIPID METABOLISM; LIPID STORAGE; LIPOLYSIS; LYSOSOME; MACROAUTOPHAGY; MACROPHAGE; MALABSORPTION; MICROAUTOPHAGY; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; WOLMAN DISEASE;

ANIMALS; ATHEROSCLEROSIS; AUTOPHAGY; BIOLOGICAL TRANSPORT; CHOLESTEROL; CHOLESTEROL ESTERS; FOAM CELLS; HUMANS; HYDROLYSIS; LIPOLYSIS; STEROL ESTERASE;

EID: 84857653989     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.240705     Document Type: Review

References (52)

1. Glass CK, Witztum JL. Atherosclerosis: the road ahead. Cell. 2001;104: 503-516. (Pubitemid 32201946)
2. Webb NR, Moore KJ. Macrophage-derived foam cells in atherosclerosis: lessons from murine models and implications for therapy. Curr Drug Targets. 2007;8:1249-1263.
3. Cuchel M, Rader DJ. Macrophage reverse cholesterol transport: key to the regression of atherosclerosis? Circulation. 2006;113:2548-2555. (Pubitemid 43948034)
4. Maxfield FR, van Meer G. Cholesterol, the central lipid of mammalian cells. Curr Opin Cell Biol. 2010;22:422-429.
5. Maxfield FR, Tabas I. Role of cholesterol and lipid organization in disease. Nature. 2005;438:612-621. (Pubitemid 41740565)
6. Brasaemle DL. Thematic review series: adipocyte biology: the perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. J Lipid Res. 2007;48:2547-2559. (Pubitemid 350272839)
7. Coleman RA, Lee DP. Enzymes of triacylglycerol synthesis and their regulation. Prog Lipid Res. 2004;43:134-176. (Pubitemid 37492937)
8. Lin S, Cheng D, Liu MS, Chen J, Chang TY. Human acyl-CoA:cholesterol acyltransferase-1 in the endoplasmic reticulum contains seven transmembrane domains. J Biol Chem. 1999;274:23276-23285.
9. Persson J, Degerman E, Nilsson J, Lindholm MW. Perilipin and adipophilin expression in lipid loaded macrophages. Biochem Biophys Res Commun. 2007;363:1020-1026. (Pubitemid 47559155)
10. Lada AT, Willingham MC, St Clair RW. Triglyceride depletion in THP-1 cells alters cholesteryl ester physical state and cholesterol efflux. J Lipid Res. 2002;43:618-628. (Pubitemid 34252337)
11. Paul A, Chang BH, Li L, Yechoor VK, Chan L. Deficiency of adipose differentiation-related protein impairs foam cell formation and protects against atherosclerosis. Circ Res. 2008;102:1492-1501.
12. Brown MS, Goldstein JL, Krieger M, Ho YK, Anderson RG. Reversible accumulation of cholesteryl esters in macrophages incubated with acetylated lipoproteins. J Cell Biol. 1979;82:597-613. (Pubitemid 10222832)
13. McGookey DJ, Anderson RG. Morphological characterization of the cholesteryl ester cycle in cultured mouse macrophage foam cells. J Cell Biol. 1983;97:1156-1168. (Pubitemid 13019376)
14. Brown MS, Ho YK, Goldstein JL. The cholesteryl ester cycle in macrophage foam cells: continual hydrolysis and re-esterification of cytoplasmic cholesteryl esters. J Biol Chem. 1980;255:9344-9352. (Pubitemid 11202897)
15. Ghosh S, Zhao B, Bie J, Song J. Macrophage cholesteryl ester mobilization and atherosclerosis. Vasc Pharmacol. 2010;52;1-10.
16. Zhao B, Fisher BJ, St Clair RW, Rudel LL, Ghosh S. Redistribution of macrophage cholesteryl ester hydrolase from cytoplasm to lipid droplets upon lipid loading. J Lipid Res. 2005;46:2114-2121. (Pubitemid 41377463)
17. Zhao B, Song J, St Clair RW, Ghosh S. Stable overexpression of human macrophage cholesteryl ester hydrolase results in enhanced free cholesterol efflux from human THP1 macrophages. Am J Physiol Cell Physiol. 2007;292:C405-C412. (Pubitemid 46115148)
18. Zhao B, Song J, Chow WN, St Clair RW, Rudel LL, Ghosh S. Macrophage-specific transgenic expression of cholesteryl ester hydrolase significantly reduces atherosclerosis and lesion necrosis in Ldlr mice. J Clin Invest. 2007;117:2983-2992. (Pubitemid 47529628)
19. Yeaman SJ. Hormone-sensitive lipase-new roles for an old enzyme. Biochem J. 2004;379:11-22. (Pubitemid 38491354)
20. Sekiya M, Osuga J, Igarashi M, Okazaki H, Ishibashi S. The role of neutral cholesterol ester hydrolysis in macrophage foam cells. J Atheroscler Thromb. 2011;18:359-364.
21. Choy HA, Wang XP, Schotz MC. Reduced atherosclerosis in hormonesensitive lipase transgenic mice overexpressing cholesterol acceptors. Biochim Biophys Acta. 2003;1634:76-85. (Pubitemid 37487711)
22. Igarashi M, Osuga J, Uozaki H, Sekiya M, Nagashima S, Takahashi M, Takase S, Takanashi M, Li Y, Ohta K, Kumagai M, Nishi M, Hosokawa M, Fledelius C, Jacobsen P, Yagyu H, Fukayama M, Nagai R, Kadowaki T, Ohashi K, Ishibashi S. The critical role of neutral cholesterol ester hydrolase 1 in cholesterol removal from human macrophages. Circ Res. 2010;107:1387-1395.
23. Sekiya M, Osuga J, Nagashima S, Ohshiro T, Igarashi M, Okazaki H, Takahashi M, Tazoe F, Wada T, Ohta K, Takanashi M, Kumagai M, Nishi M, Takase S, Yahagi N, Yagyu H, Ohashi K, Nagai R, Kadowaki T, Furukawa Y, Ishibashi S. Ablation of neutral cholesterol ester hydrolase 1 accelerates atherosclerosis. Cell Metab. 2009;10:219-228.
24. Quiroga AD, Lehner R. Role of endoplasmic reticulum neutral lipid hydrolases. Trends Endocrinol Metab. 2011;22:218-225.
25. Buchebner M, Pfeifer T, Rathke N, Chandak PG, Lass A, Schreiber R, Kratzer A, Zimmermann R, Sattler W, Koefeler H, Fröhlich E, Kostner GM, Birner-Gruenberger R, Chiang KP, Haemmerle G, Zechner R, Levak-Frank S, Cravatt B, Kratky D. Cholesteryl ester hydrolase activity is abolished in HSLα/βmacrophages but unchanged in macrophages lacking KIAA1363. J Lipid Res. 2010;51:2896-2908.
26. Kratky D. Neutral cholesterol ester hydrolases in macrophages: still a matter of debate. Circ Res. 2011;108:e13.
27. Du H, Heur M, Witte DP, Ameis D, Grabowski GA. Lysosomal acid lipase deficiency: correction of lipid storage by adenovirus-mediated gene transfer in mice. Hum Gene Ther. 2002;13:1361-1372. (Pubitemid 35034515)
28. Burton BK, Remy WT, Rayman L. Cholesterol ester and triglyceride metabolism in intact fibroblasts from patients with Wolman's disease and cholesterol ester storage disease. Pediatr Res. 1984;18:1242-1245. (Pubitemid 15221469)
29. Ouimet M, Franklin V, Mak E, Liao X, Tabas I, Marcel YL. Autophagy regulates cholesterol efflux from macrophage foam cells via lysosomal acid lipase. Cell Metab. 2011;13:655-667.
30. Swanson MS, Byrne BG, Dubuisson JF. Kinetic analysis of autophagosome formation and turnover in primary mouse macrophages. Methods Enzymol. 2009;452:383-402.
31. Singh R, Cuervo AM. Autophagy in the cellular energetic balance. Cell Metab. 2011;13:495-504.
32. Hamasaki M, Yoshimori T. Where do they come from? Insights into autophagosome formation. FEBS Lett. 2010;584:1296-1301.
33. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ. Autophagy regulates lipid metabolism. Nature. 2009;458:1131-1135.
34. Cheng J, Ohsaki Y, Tauchi-Sato K, Fujita A, Fujimoto T. Cholesterol depletion induces autophagy. Biochem Biophys Res Commun. 2006;351: 246-252. (Pubitemid 44635433)
35. Seo YK, Jeon TI, Chong HK, Biesinger J, Xie X, Osborne TF. Genome-wide localization of SREBP-2 in hepatic chromatin predicts a role in autophagy. Cell Metab. 2011;13:367-375.
36. Avart SJ, Bernard DW, Jerome WG, Glick JM. Cholesteryl ester hydrolysis in J774 macrophages occurs in the cytoplasm and lysosomes. J Lipid Res. 1999;40:405-414. (Pubitemid 29116143)
37. Zhang YL, Cao YJ, Zhang X, Liu HH, Tong T, Xiao GD, Yang YP, Liu CF. The autophagy-lysosome pathway: a novel mechanism involved in the processing of oxidized LDL in human vascular endothelial cells. Biochem Biophys Res Commun. 2010;394:377-382.
38. Tang C, Oram JF. The cell cholesterol exporter ABCA1 as a protector from cardiovascular disease and diabetes. Biochim Biophys Acta. 2009; 1791:563-572.
39. Denis M, Landry YD, Zha X. ATP-binding cassette A1-mediated lipidation of apolipoprotein A-I occurs at the plasma membrane and not in the endocytic compartments. J Biol Chem. 2008;283:16178-16186.
40. Maric J, Kiss RS, Franklin V, Marcel YL. Intracellular lipidation of newly synthesized apolipoprotein A-I in primary murine hepatocytes. J Biol Chem. 2005;280:39942-39949. (Pubitemid 41779129)
41. Neufeld EB, Remaley AT, Demosky SJ, Stonik JA, Cooney AM, Comly M, Dwyer NK, Zhang M, Blanchette-Mackie J, Santamarina-Fojo S, Brewer HB Jr. Cellular localization and trafficking of the human ABCA1 transporter. J Biol Chem. 2001;276:27584-27590.
42. Chen W, Sun Y, Welch C, Gorelik A, Leventhal AR, Tabas I, Tall AR. Preferential ATP-binding cassette transporter A1-mediated cholesterol efflux from late endosomes/lysosomes. J Biol Chem. 2001;276: 43564-43569.
43. Chen W, Wang N, Tall AR. A PEST deletion mutant of ABCA1 shows impaired internalization and defective cholesterol efflux from late endosomes. J Biol Chem. 2005;280:29277-29281. (Pubitemid 41161382)
44. Boadu E, Choi HY, Lee DW, Waddington EI, Chan T, Asztalos B, Vance JE, Chan A, Castro G, Francis GA. Correction of apolipoprotein A-Imediated lipid efflux and high density lipoprotein particle formation in human Niemann-Pick type C disease fibroblasts. J Biol Chem. 2006;281: 37081-37090. (Pubitemid 46042178)
45. Azuma Y, Takada M, Shin HW, Kioka N, Nakayama K, Ueda K. Retroendocytosis pathway of ABCA1/apoA-I contributes to HDL formation. Genes Cells. 2009;14:191-204.
46. Du H, Grabowski GA. Lysosomal acid lipase and atherosclerosis. Curr Opin Lipidol. 2004;15:539-544. (Pubitemid 39336581)
47. Du H, Schiavi S, Wan N, Levine M, Witte DP, Grabowski GA. Reduction of atherosclerotic plaques by lysosomal acid lipase supplementation. Arterioscler Thromb Vasc Biol. 2004;24:147-154. (Pubitemid 38082426)
48. Bowden KL, Bilbey NJ, Bilawchuk LM, Boadu E, Sidhu R, Ory DS, Du H, Chan T, Francis GA. Lysosomal acid lipase deficiency impairs regulation of ABCA1 gene and formation of high density lipoproteins in cholesteryl ester storage disease. J Biol Chem. 2011;286:30624-30635.
49. Elleder M, Chlumska A, Hyanek J, Poupetova H, Ledvinova J, Maas S, Lohse P. Subclinical course of cholesteryl ester storage disease in an adult with hypercholesterolemia, accelerated atherosclerosis, and liver cancer. J Hepatol. 2000;32:528-534. (Pubitemid 30136871)
50. Seedorf U, Wiebusch H, Muntoni S, Christensen NC, Skovby F, Nickel V, Roskos M, Funke H, Ose L, Assmann G. A novel variant of lysosomal acid lipase (Leu336-Pro) associated with acid lipase deficiency and cholesterol ester storage disease. Arterioscler Thromb Vasc Biol. 1995;15:773-778.
51. Coronary Artery Disease (C4D) Genetics Consortium. A genome-wide association study in Europeans and South Asians identifies five new loci for coronary artery disease. Nat Genet. 2011;43:339-344.
52. Wild PS, Zeller T, Schillert A, Szymczak S, Sinning CR, Deiseroth A, Schnabel RB, Lubos E, Keller T, Eleftheriadis MS, Bickel C, Rupprecht HJ, Wilde S, Rossmann H, Diemert P, Cupples LA, Perret C, Erdmann J, Stark K, Kleber ME, Epstein SE, Voight BF, Kuulasmaa K, Li M, Schäfer AS, Klopp N, Braund PS, Sager HB, Demissie S, Proust C, König IR, Wichmann HE, Reinhard W, Hoffmann MM, Virtamo J, Burnett MS, Siscovick D, Wiklund PG, Qu L, El Mokthari NE, Thompson JR, Peters A, Smith AV, Yon E, Baumert J, Hengstenberg C, März W, Amouyel P, Devaney J, Schwartz SM, Saarela O, Mehta NN, Rubin D, Silander K, Hall AS, Ferrieres J, Harris TB, Melander O, Kee F, Hakonarson H, Schrezenmeir J, Gudnason V, Elosua R, Arveiler D, Evans A, Rader DJ, Illig T, Schreiber S, Bis JC, Altshuler D, Kavousi M, Witteman JC, Uitterlinden AG, Hofman A, Folsom AR, Barbalic M, Boerwinkle E, Kathiresan S, Reilly MP, O'Donnell CJ, Samani NJ, Schunkert H, Cambien F, Lackner KJ, Tiret L, Salomaa V, Munzel T, Ziegler A, Blankenberg S. A genome-wide association study identifies LIPA as a susceptibility gene for coronary artery disease. Circ Cardiovasc Genet. 2011;4:403-412.