Rate-limiting factors of cholesterol efflux in reverse cholesterol transport: Acceptors and donors: Frontiers in research review: Physiological and pathological functions of high-density lipoprotein

Clinical and Experimental Pharmacology and Physiology

Volumn 37, Issue 7, 2010, Pages 703-709

  Fu, Ying ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

ATP binding cassette transporters; cholesteryl ester; high density lipoprotein; lecithin:cholesterol acyltransferase; liver X receptor; macrophage; reverse cholesterol transport; scavenger receptor BI

Indexed keywords

ABC TRANSPORTER A1; ABC TRANSPORTER G1; APOLIPOPROTEIN A1; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN; PHOSPHOLIPID; SCAVENGER RECEPTOR BI; ABC TRANSPORTER; ABCA1 PROTEIN, HUMAN; ABCA2 PROTEIN, HUMAN; SCAVENGER RECEPTOR;

ATHEROSCLEROSIS; CELL SECRETION; CHOLESTEROL TRANSPORT; HUMAN; MACROPHAGE; NONHUMAN; PROTEIN FUNCTION; REVERSE CHOLESTEROL TRANSPORT; REVIEW; BLOOD; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

ATHEROSCLEROSIS; ATP BINDING CASSETTE TRANSPORTER 1; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CHOLESTEROL; HUMANS; LIPOPROTEINS, HDL; PHOSPHOLIPIDS; RECEPTORS, SCAVENGER;

EID: 77953841479     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/j.1440-1681.2010.05386.x     Document Type: Review

References (81)

1. Assmann G, Gotto Jr. AM. HDL cholesterol and protective factors in atherosclerosis. Circulation 2004 109 (Suppl. I III8 14.
2. Toth PP. High-density lipoprotein and cardiovascular risk. Circulation 2004 109: 1809 1812.
3. Johnson WJ, Mahlberg FH, Rothblat GH, Phillips MC. Cholesterol transport between cells and high-density lipoproteins. Biochim. Biophys. Acta 1991 1085: 273 298.
4. Cuchel M, Rader DJ. Macrophage reverse cholesterol transport. Key to the regression of atherosclerosis? Circulation 2006 113: 2548 2555.
5. Kennedy MA, Barrera GC, Nakamura K et al. ABCG1 has a critical role in mediating cholesterol efflux to HDL and preventing cellular lipid accumulation. Cell Metab. 2005 1: 121 131.
6. Wang N, Lan D, Chen W, Matsuura F, Tall AR. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc. Natl Acad. Sci. USA 2004 101: 9774 9779.
7. Yancey PG, de la Llera-Moya M, Swarnakar S et al. High density lipoprotein phospholipid composition is a major determinant of the bi-directional flux and net movement of cellular free cholesterol mediated by scavenger receptor BI. J. Biol. Chem. 2000 275: 36596 36604.
8. Rust S, Rosier M, Funke H et al. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat. Genet. 1999 22: 352 355.
9. Zannis VI, Chroni A, Krieger M. Role of apoA-I, ABCA1, LCAT, and SR-BI in the biogenesis of HDL. J. Mol. Med. 2006 84: 276 294.
10. Brunham LR, Kruit JK, Iqbal J et al. Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. J. Clin. Invest. 2006 116: 1052 1062.
11. Curtiss LK, Valenta DT, Hime NJ, Rye KA. What is so special about apolipoprotein AI in reverse cholesterol transport? Arterioscler. Thromb. Vasc. Biol. 2006 26: 12 19.
12. Lee JY, Parks JS. ATP-binding cassette transporter AI and its role in HDL formation. Curr. Opin. Lipidol. 2005 16: 19 25.
13. Singaraja RR, Fievet C, Castro G et al. Increased ABCA1 activity protects against atherosclerosis. J. Clin. Invest. 2002 110: 35 42.
14. Yokoyama S. ABCA1 and biogenesis of HDL. J. Atheroscler. Thromb. 2006 13: 1 15.
15. Timmins JM, Lee JY, Boudyguina E et al. Targeted inactivation of hepatic Abca1 causes profound hypoalphalipoproteinemia and kidney hypercatabolism of apoA-I. J. Clin. Invest. 2005 115: 1333 1342.
16. Sviridov D, Nestel P. Dynamics of reverse cholesterol transport: Protection against atherosclerosis. Atherosclerosis 2002 161: 245 254.
17. Sorci-Thomas MG, Thomas MJ. The effects of altered apolipoprotein A-I structure on plasma HDL concentration. Trends Cardiovasc. Med. 2002 12: 121 128.
18. Hoang A, Huang W, Sasaki J, Sviridov D. Natural mutations of apolipoprotein A-I impairing activation of lecithin: Cholesterol acyltransferase. Biochim. Biophys. Acta 2003 1631: 72 6.
19. Franceschini G, Calabresi L, Chiesa G et al. Increased cholesterol efflux potential of sera from ApoA-IMilano carriers and transgenic mice. Arterioscler. Thromb. Vasc. Biol. 1999 19: 1257 1262.
20. Weibel GL, Alexander ET, Joshi MR et al. Wild-type ApoA-I and the Milano variant have similar abilities to stimulate cellular lipid mobilization and efflux. Arterioscler. Thromb. Vasc. Biol. 2007 27: 2022 2029.
21. Moore RE, Navab M, Millar JS et al. Increased atherosclerosis in mice lacking apolipoprotein A-I attributable to both impaired reverse cholesterol transport and increased inflammation. Circ. Res. 2005 97: 763 771.
22. Shah PK. Apolipoprotein A-I/HDL infusion therapy for plaque stabilization-regression: A novel therapeutic approach. Curr. Pharm. Des. 2007 13: 1031 1038.
23. Tall AR, Yvan-Charvet L, Terasaka N, Pagler T, Wang N. HDL, ABC transporters, and cholesterol efflux-Implications for the treatment of atherosclerosis. Cell Metab. 2008 7: 365 375.
24. Young SG, Fielding CJ. The ABCs of cholesterol efflux. Nat. Genet. 1999 22: 316 318.
25. Bodzioch M, Orso E, Klucken J et al. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat. Genet. 1999 22: 347 351.
26. Brooks-Wilson A, Marcil M, Clee SM et al. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet. 1999 22: 336 345. (Pubitemid 29369523)
27. Kielar D, Dietmaier W, Langmann T et al. Rapid quantification of human ABCA1 mRNA in various cell types and tissues by real-time reverse transcription-PCR. Clin. Chem. 2001 47: 2089 2097.
28. Croop JM. Evolutionary relationships among ABC transporters. Methods Enzymol. 1998 292: 101 116.
29. Remaley AT, Stonik JA, Demosky SJ et al. Apolipoprotein specificity for lipid efflux by the human ABCAI transporter. Biochem. Biophys. Res. Commun. 2001 280: 818 823.
30. Oram JF, Lawn RM. ABCA1. The gatekeeper for eliminating excess tissue cholesterol. J. Lipid Res. 2001 42: 1173 1179.
31. Oram JF, Vaughan AM. ABCA1-mediated transport of cellular cholesterol and phospholipids to HDL apolipoproteins. Curr. Opin. Lipidol. 2000 11: 253 260.
32. Haghpassand M, Bourassa PA, Francone OL, Aiello RJ. Monocyte/macrophage expression of ABCA1 has minimal contribution to plasma HDL levels. J. Clin. Invest. 2001 108: 1315 1320.
33. van Eck M, Bos IS, Kaminski WE et al. Leukocyte ABCA1 controls susceptibility to atherosclerosis and macrophage recruitment into tissues. Proc. Natl Acad. Sci. USA 2002 99: 6298 6303.
34. Costet P, Luo Y, Wang N, Tall AR. Sterol-dependent transactivation of the ABC1 promoter by the liver X receptor/retinoid X receptor. J. Biol. Chem. 2000 275: 28240 28245.
35. Tontonoz P, Mangelsdorf DJ. Liver X receptor signaling pathways in cardiovascular disease. Mol. Endocrinol. 2003 17: 985 993.
36. Jiang YJ, Lu B, Kim P, Elias PM, Feingold KR. Regulation of ABCA1 expression in human keratinocytes and murine epidermis. J. Lipid Res. 2006 47: 2248 2258.
37. Lund EG, Menke JG, Sparrow CP. Liver X receptor agonists as potential therapeutic agents for dyslipidemia and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2003 23: 1169 1177.
38. Venkateswaran A, Laffitte BA, Joseph SB et al. Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXR alpha. Proc. Natl Acad. Sci. USA 2000 97: 12097 12102.
39. Miao B, Zondlo S, Gibbs S et al. Raising HDL cholesterol without inducing hepatic steatosis and hypertriglyceridemia by a selective LXR modulator. J. Lipid Res. 2004 45: 1410 1417.
40. Hoekstra M, Kruijt JK, Van Eck M, Van Berkel TJ. Specific gene expression of ATP-binding cassette transporters and nuclear hormone receptors in rat liver parenchymal, endothelial, and Kupffer cells. J. Biol. Chem. 2003 278: 25448 25453.
41. Delvecchio CJ, Bilan P, Nair P, Capone JP. LXR-induced reverse cholesterol transport in human airway smooth muscle is mediated exclusively by ABCA1. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008 295: L949 57.
42. Aiello RJ, Brees D, Bourassa PA et al. Increased atherosclerosis in hyperlipidemic mice with inactivation of ABCA1 in macrophages. Arterioscler. Thromb. Vasc. Biol. 2002 22: 630 637.
43. Arakawa R, Yokoyama S. Helical apolipoproteins stabilize ATP-binding cassette transporter A1 by protecting it from thiol protease-mediated degradation. J. Biol. Chem. 2002 277: 22426 22429.
44. Wang N, Silver DL, Costet P, Tall AR. Specific binding of ApoA-I, enhanced cholesterol efflux, and altered plasma membrane morphology in cells expressing ABC1. J. Biol. Chem. 2000 275: 33053 33058.
45. Yvan-Charvet L, Wang N, Tall AR. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler. Thromb. Vasc. Biol. 2009 30: 139 143.
46. Nandi S, Ma L, Denis M et al. ABCA1-mediated cholesterol efflux generates microparticles in addition to HDL through processes governed by membrane rigidity. J. Lipid Res. 2009 50: 456 466.
47. Vedhachalam C, Duong PT, Nickel M et al. Mechanism of ATP-binding cassette transporter A1-mediated cellular lipid efflux to apolipoprotein A-I and formation of high density lipoprotein particles. J. Biol. Chem. 2007 282: 25123 25130.
48. Neufeld EB, Remaley AT, Demosky SJ et al. Cellular localization and trafficking of the human ABCA1 transporter. J. Biol. Chem. 2001 276: 27584 27590.
49. Cavelier C, Rohrer L, von Eckardstein A. ATP-binding cassette transporter A1 modulates apolipoprotein A-I transcytosis through aortic endothelial cells. Circ. Res. 2006 99: 1060 1066.
50. Rohrer L, Cavelier C, Fuchs S, Schluter MA, Volker W, von Eckardstein A. Binding, internalization and transport of apolipoprotein A-I by vascular endothelial cells. Biochim. Biophys. Acta 2006 1761: 186 194.
51. Akiyama M, Sugiyama-Nakagiri Y, Sakai K et al. Mutations in lipid transporter ABCA12 in harlequin ichthyosis and functional recovery by corrective gene transfer. J. Clin. Invest. 2005 115: 1777 1784.
52. Jiang YJ, Lu B, Kim P et al. PPAR and LXR activators regulate ABCA12 expression in human keratinocytes. J. Invest. Dermatol. 2008 128: 104 109.
53. Lefevre C, Audebert S, Jobard F et al. Mutations in the transporter ABCA12 are associated with lamellar ichthyosis type 2. Hum. Mol. Genet. 2003 12: 2369 2378.
54. Thomas AC, Cullup T, Norgett EE et al. ABCA12 is the major harlequin ichthyosis gene. J. Invest. Dermatol. 2006 126: 2408 2413.
55. Yanagi T, Akiyama M, Nishihara H et al. Harlequin ichthyosis model mouse reveals alveolar collapse and severe fetal skin barrier defects. Hum. Mol. Genet. 2008 17: 3075 3083.
56. Smyth I, Hacking DF, Hilton AA et al. A mouse model of harlequin ichthyosis delineates a key role for Abca12 in lipid homeostasis. PLoS Genet. 2008 4: E1000192.
57. Sakai K, Akiyama M, Sugiyama-Nakagiri Y, McMillan JR, Sawamura D, Shimizu H. Localization of ABCA12 from Golgi apparatus to lamellar granules in human upper epidermal keratinocytes. Exp. Dermatol. 2007 16: 920 926.
58. Klucken J, Buchler C, Orso E et al. ABCG1 (ABC8), the human homolog of the Drosophila white gene, is a regulator of macrophage cholesterol and phospholipid transport. Proc. Natl Acad. Sci. USA 2000 97: 817 822.
59. Wang N, Ranalletta M, Matsuura F, Peng F, Tall AR. LXR-induced redistribution of ABCG1 to plasma membrane in macrophages enhances cholesterol mass efflux to HDL. Arterioscler. Thromb. Vasc. Biol. 2006 26: 1310 1316.
60. Kobayashi A, Takanezawa Y, Hirata T et al. Efflux of sphingomyelin, cholesterol, and phosphatidylcholine by ABCG1. J. Lipid Res. 2006 47: 1791 1802.
61. Larrede S, Quinn CM, Jessup W et al. Stimulation of cholesterol efflux by LXR agonists in cholesterol-loaded human macrophages is ABCA1-dependent but ABCG1-independent. Arterioscler. Thromb. Vasc. Biol. 2009 29: 1930 1936.
62. Gelissen IC, Harris M, Rye KA et al. ABCA1 and ABCG1 synergize to mediate cholesterol export to apoA-I. Arterioscler. Thromb. Vasc. Biol. 2006 26: 534 540.
63. Out R, Jessup W, Le Goff W et al. Coexistence of foam cells and hypocholesterolemia in mice lacking the ABC transporters A1 and G1. Circ. Res. 2008 102: 113 120.
64. Wang MD, Franklin V, Marcel YL. In vivo reverse cholesterol transport from macrophages lacking ABCA1 expression is impaired. Arterioscler. Thromb. Vasc. Biol. 2007 27: 1837 1842.
65. Trigatti BL, Krieger M, Rigotti A. Influence of the HDL receptor SR-BI on lipoprotein metabolism and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2003 23: 1732 1738.
66. Schwartz CC, Halloran LG, Vlahcevic ZR, Gregory DH, Swell L. Preferential utilization of free cholesterol from high-density lipoproteins for biliary cholesterol secretion in man. Science 1978 200: 62 4.
67. Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 1996 271: 518 520.
68. Rigotti A, Trigatti B, Babitt J, Penman M, Xu S, Krieger M. Scavenger receptor BI: A cell surface receptor for high density lipoprotein. Curr. Opin. Lipidol. 1997 8: 181 188.
69. Ueda Y, Royer L, Gong E et al. Lower plasma levels and accelerated clearance of high density lipoprotein (HDL) and non-HDL cholesterol in scavenger receptor class B type I transgenic mice. J. Biol. Chem. 1999 274: 7165 7171.
70. Lambert G, Chase MB, Dugi K, Bensadoun A, Brewer Jr. HB, Santamarina-Fojo S. Hepatic lipase promotes the selective uptake of high density lipoprotein-cholesteryl esters via the scavenger receptor B1. J. Lipid Res. 1999 40: 1294 1303.
71. Ji Y, Jian B, Wang N et al. Scavenger receptor BI promotes high density lipoprotein-mediated cellular cholesterol efflux. J. Biol. Chem. 1997 272: 20982 20985.
72. Lorenzi I, von Eckardstein A, Cavelier C, Radosavljevic S, Rohrer L. Apolipoprotein A-I but not high-density lipoproteins are internalised by RAW macrophages. Roles of ATP-binding cassette transporter A1 and scavenger receptor BI. J. Mol. Med. 2008 86: 171 183.
73. Braun A, Trigatti BL, Post MJ et al. Loss of SR-BI expression leads to the early onset of occlusive atherosclerotic coronary artery disease, spontaneous myocardial infarctions, severe cardiac dysfunction, and premature death in apolipoprotein E-deficient mice. Circ. Res. 2002 90: 270 276.
74. Zhang W, Yancey PG, Su YR et al. Inactivation of macrophage scavenger receptor class B type I promotes atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 2003 108: 2258 2263.
75. Lorenzi I, von Eckardstein A, Radosavljevic S, Rohrer L. Lipidation of apolipoprotein A-I by ATP-binding cassette transporter (ABC) A1 generates an interaction partner for ABCG1 but not for scavenger receptor BI. Biochim. Biophys. Acta 2008 1781: 306 313.
76. Nicholson AC, Febbraio M, Han J, Silverstein RL, Hajjar DP. CD36 in atherosclerosis. The role of a class B macrophage scavenger receptor. Ann. NY Acad. Sci. 2000 902: 128 131.
77. Ansell BJ. The two faces of the 'good' cholesterol. Cleve. Clin. J. Med. 2007 74: 3 5.
78. Nicholls SJ, Tuzcu EM, Brennan DM, Tardif JC, Nissen SE. Cholesteryl ester transfer protein inhibition, high-density lipoprotein raising, and progression of coronary atherosclerosis: insights from ILLUSTRATE (Investigation of Lipid Level Management Using Coronary Ultrasound to Assess Reduction of Atherosclerosis by CETP Inhibition and HDL Elevation). Circulation 2008 118: 2506 2514.
79. Cho KH. Synthesis of reconstituted high density lipoprotein (rHDL) containing apoA-I and apoC-III. The functional role of apoC-III in rHDL. Mol. Cells 2009 27: 291 297.
80. Tanigawa H, Billheimer JT, Tohyama J et al. Lecithin:cholesterol acyltransferase expression has minimal effects on macrophage reverse cholesterol transport in vivo. Circulation 2009 120: 160 169.
81. Zheng L, Nukuna B, Brennan ML et al. Apolipoprotein A-I is a selective target for myeloperoxidase-catalyzed oxidation and functional impairment in subjects with cardiovascular disease. J. Clin. Invest. 2004 114: 529 541.