HDL particle size is a critical determinant of ABCA1-mediated macrophage cellular cholesterol export

Circulation Research

Volumn 116, Issue 7, 2015, Pages 1133-1142

  Du, Xian Ming ^a   Kim, Mi Jurng ^a   Hou, Liming ^a   Le Goff, Wilfried ^b,c   Chapman, M John ^b,c   Van Eck, Miranda ^d   Curtiss, Linda K ^e   Burnett, John R ^f,g   Cartland, Sian P ^a   Quinn, Carmel M ^a   Kockx, Maaike ^h   Kontush, Anatol ^b,c   Rye, Kerry Anne ^a   Kritharides, Leonard ^h,i   Jessup, Wendy ^h,i  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d LEIDEN UNIVERSITY   (Netherlands)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

^f ROYAL PERTH HOSPITAL   (Australia)

^g UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^h UNIVERSITY OF SYDNEY   (Australia)

ⁱ Department of Geriatric Medicine   (Australia)

Author keywords

ATP binding cassette transporter 1; ATP binding cassette transporters; Cholesterol, HDL; Cholesterol efflux regulatory protein; Foam cells; Macrophages

Indexed keywords

ABC TRANSPORTER A1; ABC TRANSPORTER G1; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN 3; HIGH DENSITY LIPOPROTEIN 3B; HIGH DENSITY LIPOPROTEIN 3C; UNCLASSIFIED DRUG; ABC TRANSPORTER; ABCA1 PROTEIN, HUMAN; ABCA1 PROTEIN, MOUSE; ABCG1 PROTEIN, HUMAN; ABCG1 PROTEIN, MOUSE; APOLIPOPROTEIN A1; HIGH DENSITY LIPOPROTEIN 2; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYBRID PROTEIN; LIPOPROTEIN;

ANIMAL CELL; ARTICLE; CHO CELL LINE; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; FEMALE; FOAM CELL; GENE DELETION; HUMAN; HUMAN CELL; LIPID COMPOSITION; MACROPHAGE; MEDIATOR RELEASE; MOUSE; NONHUMAN; PARTICLE SIZE; PLASMA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; STABLE EXPRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL LINE; COMPARATIVE STUDY; CRICETULUS; DEFICIENCY; ENZYMOLOGY; GENE SILENCING; GENETICS; HAMSTER; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; TANGIER DISEASE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; APOLIPOPROTEIN A-I; ATP BINDING CASSETTE TRANSPORTER 1; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CELL LINE; CHO CELLS; CHOLESTEROL; CHOLESTEROL, HDL; CRICETINAE; CRICETULUS; FOAM CELLS; GENE SILENCING; HUMANS; LIPOPROTEINS; LIPOPROTEINS, HDL; LIPOPROTEINS, HDL2; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PARTICLE SIZE; RECOMBINANT FUSION PROTEINS; TANGIER DISEASE;

EID: 84930741855     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.305485     Document Type: Article

References (40)

1. Kontush A, Chapman MJ, High-density lipoproteins 2012 Hoboken, NJ: John Wiley & Sons
2. Nicholls SJ, Tuzcu EM, Sipahi I, Schoenhagen P, Crowe T, Kapadia S, Nissen SE, Relationship between atheroma regression and change in lumen size after infusion of apolipoprotein A-I Milano. J Am Coll Cardiol 2006; 47: 992-997. doi: 10.1016/j.jacc.2005.11.040.
3. Zhang Y, Zanotti I, Reilly MP, Glick JM, Rothblat GH, Rader DJ, Overexpression of apolipoprotein A-I promotes reverse transport of cholesterol from macrophages to feces in vivo. Circulation 2003; 108: 661-663. doi: 10.1161/01.CIR.0000086981.09834.E0.
4. Briel M, Ferreira-Gonzalez I, You JJ, Karanicolas PJ, Akl EA, Wu P, Blechacz B, Bassler D, Wei X, Sharman A, Whitt I, Silva SAd, Khalid Z, Nordmann AJ, Zhou Q, Walter SD, Vale N, Bhatnagar N, O'Regan C, Mills EJ, Bucher HC, Montori VM, Guyatt GH, Association between change in high density lipoprotein cholesterol and cardiovascular disease morbidity and mortality: Systematic review and meta-regression analysis. British Medical Journal 2009 338 b92
5. Khera AV, Rader DJ, Future therapeutic directions in reverse cholesterol transport. Curr Atheroscler Rep 2010; 12: 73-81. doi: 10.1007/s11883-009-0080-0.
6. Khera AV, Cuchel M, de la Llera-Moya M, Rodrigues A, Burke MF, Jafri K, French BC, Phillips JA, Mucksavage ML, Wilensky RL, Mohler ER, Rothblat GH, Rader DJ, Cholesterol efflux capacity, high-density lipoprotein function, and atherosclerosis. N Engl J Med 2011; 364: 127-135. doi: 10.1056/NEJMoa1001689.
7. Rye KA, Barter PJ, Cardioprotective functions of HDLs. J Lipid Res 2014; 55: 168-179. doi: 10.1194/jlr.R039297.
8. Oram JF, Lawn RM, Garvin MR, Wade DP, ABCA1 is the cAMP-inducible apolipoprotein receptor that mediates cholesterol secretion from macrophages. J Biol Chem 2000; 275: 34508-34511. doi: 10.1074/jbc.M006738200.
9. Kennedy MA, Barrera GC, Nakamura K, Baldán A, Tarr P, Fishbein MC, Frank J, Francone OL, Edwards PA, ABCG1 has a critical role in mediating cholesterol efflux to HDL and preventing cellular lipid accumulation. Cell Metab 2005; 1: 121-131. doi: 10.1016/j.cmet.2005.01.002.
10. Gelissen IC, Harris M, Rye KA, Quinn C, Brown AJ, Kockx M, Cartland S, Packianathan M, Kritharides L, Jessup W, ABCA1 and ABCG1 synergize to mediate cholesterol export to apoA-I. Arterioscler Thromb Vasc Biol 2006; 26: 534-540. doi: 10.1161/01.ATV.0000200082.58536.e1.
11. Wang X, Collins HL, Ranalletta M, Fuki IV, Billheimer JT, Rothblat GH, Tall AR, Rader DJ, Macrophage ABCA1 and ABCG1, but not SR-BI, promote macrophage reverse cholesterol transport in vivo. J Clin Invest 2007; 117: 2216-2224. doi: 10.1172/JCI32057.
12. Out R, Jessup W, Le Goff W, Hoekstra M, Gelissen IC, Zhao Y, Kritharides L, Chimini G, Kuiper J, Chapman MJ, Huby T, Van Berkel TJ, Van Eck M, Coexistence of foam cells and hypocholesterolemia in mice lacking the ABC transporters A1 and G1. Circ Res 2008; 102: 113-120. doi: 10.1161/CIRCRESAHA.107.161711.
13. Favari E, Calabresi L, Adorni MP, Jessup W, Simonelli S, Franceschini G, Bernini F, Small discoidal pre-beta1 HDL particles are efficient acceptors of cell cholesterol via ABCA1 and ABCG1. Biochemistry 2009; 48: 11067-11074. doi: 10.1021/bi901564g.
14. Diditchenko S, Gille A, Pragst I, Stadler D, Waelchli M, Hamilton R, Leis A, Wright SD, Novel formulation of a reconstituted high-density lipoprotein (CSL112) dramatically enhances ABCA1-dependent cholesterol efflux. Arterioscler Thromb Vasc Biol 2013; 33: 2202-2211. doi: 10.1161/ATVBAHA.113.301981.
15. Bortnick AE, Rothblat GH, Stoudt G, Hoppe KL, Royer LJ, McNeish J, Francone OL, The correlation of ATP-binding cassette 1 mRNA levels with cholesterol efflux from various cell lines. J Biol Chem 2000; 275: 28634-28640. doi: 10.1074/jbc.M003407200.
16. Francis GA, Knopp RH, Oram JF, Defective removal of cellular cholesterol and phospholipids by apolipoprotein A-I in Tangier Disease. J Clin Invest 1995; 96: 78-87. doi: 10.1172/JCI118082.
17. Remaley AT, Schumacher UK, Stonik JA, Farsi BD, Nazih H, Brewer HB Jr, Decreased reverse cholesterol transport from Tangier disease fibroblasts. Acceptor specificity and effect of brefeldin on lipid efflux. Arterioscler Thromb Vasc Biol 1997 17 1813 1821
18. Larrede S, Quinn CM, Jessup W, Frisdal E, Olivier M, Hsieh V, Kim MJ, Van Eck M, Couvert P, Carrie A, Giral P, Chapman MJ, Guerin M, Le Goff W, 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. doi: 10.1161/ATVBAHA.109.194548.
19. Kontush A, Chapman MJ, Antiatherogenic small, dense HDL-guardian angel of the arterial wall? Nat Clin Pract Cardiovasc Med 2006; 3: 144-153. doi: 10.1038/ncpcardio0500.
20. Gillotte-Taylor K, Nickel M, Johnson WJ, Francone OL, Holvoet P, Lund-Katz S, Rothblat GH, Phillips MC, Effects of enrichment of fibroblasts with unesterified cholesterol on the efflux of cellular lipids to apolipoprotein A-I. J Biol Chem 2002; 277: 11811-11820. doi: 10.1074/jbc.M108268200.
21. Vedhachalam C, Liu L, Nickel M, Dhanasekaran P, Anantharamaiah GM, Lund-Katz S, Rothblat GH, Phillips MC, Influence of ApoA-I structure on the ABCA1-mediated efflux of cellular lipids. J Biol Chem 2004; 279: 49931-49939. doi: 10.1074/jbc.M406924200.
22. Vaughan AM, Oram JF, ABCG1 redistributes cell cholesterol to domains removable by high density lipoprotein but not by lipid-depleted apolipoproteins. J Biol Chem 2005; 280: 30150-30157. doi: 10.1074/jbc.M505368200.
23. Clay MA, Pyle DH, Rye KA, Barter PJ, Formation of spherical, reconstituted high density lipoproteins containing both apolipoproteins A-I and A-II is mediated by lecithin:cholesterol acyltransferase. J Biol Chem 2000 275 9019 9025
24. Barter PJ, Puranik R, Rye KA, New insights into the role of HDL as an anti-inflammatory agent in the prevention of cardiovascular disease. Curr Cardiol Rep 2007 9 493 498
25. Curtiss LK, Bonnet DJ, Rye KA, The conformation of apolipoprotein A-I in high-density lipoproteins is influenced by core lipid composition and particle size: a surface plasmon resonance study. Biochemistry 2000 39 5712 5721
26. Kockx M, Rye KA, Gaus K, Apolipoprotein A-I-stimulated apolipoprotein E secretion from human macrophages is independent of cholesterol efflux. J Biol Chem 2004; 279: 25966-25977. doi: 10.1074/jbc.M401177200.
27. Kontush A, Chantepie S, Chapman MJ, Small, dense HDL particles exert potent protection of atherogenic LDL against oxidative stress. Arterioscler Thromb Vasc Biol 2003; 23: 1881-1888. doi: 10.1161/01.ATV.0000091338.93223.E8.
28. Camont L, Lhomme M, Rached F, Le Goff W, Nègre-Salvayre A, Salvayre R, Calzada C, Lagarde M, Chapman MJ, Kontush A, Small, dense high-density lipoprotein-3 particles are enriched in negatively charged phospholipids: relevance to cellular cholesterol efflux, antioxidative, antithrombotic, anti-inflammatory, and antiapoptotic functionalities. Arterioscler Thromb Vasc Biol 2013; 33: 2715-2723. doi: 10.1161/ATVBAHA.113.301468.
29. Rye KA, Wee K, Curtiss LK, Bonnet DJ, Barter PJ, Apolipoprotein A-II inhibits high density lipoprotein remodeling and lipid-poor apolipoprotein A-I formation. J Biol Chem 2003; 278: 22530-22536. doi: 10.1074/jbc.M213250200.
30. Rothblat GH, de la Llera-Moya M, Favari E, Yancey PG, Kellner-Weibel G, Cellular cholesterol flux studies: methodological considerations. Atherosclerosis 2002 163 1 8
31. Vedhachalam C, Ghering AB, Davidson WS, Lund-Katz S, Rothblat GH, Phillips MC, ABCA1-induced cell surface binding sites for ApoA-I. Arterioscler Thromb Vasc Biol 2007; 27: 1603-1609. doi: 10.1161/ATVBAHA.107.145789.
32. Oram JF, Heinecke JW, ATP-binding cassette transporter A1: a cell cholesterol exporter that protects against cardiovascular disease. Physiol Rev 2005; 85: 1343-1372. doi: 10.1152/physrev.00005.2005.
33. Van Eck M, Singaraja RR, Ye D, Hildebrand RB, James ER, Hayden MR, Van Berkel TJ, Macrophage ATP-binding cassette transporter A1 overexpression inhibits atherosclerotic lesion progression in low-density lipoprotein receptor knockout mice. Arterioscler Thromb Vasc Biol 2006; 26: 929-934. doi: 10.1161/01.ATV.0000208364.22732.16.
34. Zheng P, Horwitz A, Waelde CA, Smith JD, Stably transfected ABCA1 antisense cell line has decreased ABCA1 mRNA and cAMP-induced cholesterol efflux to apolipoprotein AI and HDL. Biochim Biophys Acta 2001 1534 121 128
35. Huang R, Silva RA, Jerome WG, Kontush A, Chapman MJ, Curtiss LK, Hodges TJ, Davidson WS, Apolipoprotein A-I structural organization in high-density lipoproteins isolated from human plasma. Nat Struct Mol Biol 2011; 18: 416-422. doi: 10.1038/nsmb.2028.
36. Jonas A, Wald JH, Toohill KL, Krul ES, Kézdy KE, Apolipoprotein A-I structure and lipid properties in homogeneous, reconstituted spherical and discoidal high density lipoproteins. J Biol Chem 1990 265 22123 22129
37. Calabresi L, Tedeschi G, Treu C, Ronchi S, Galbiati D, Airoldi S, Sirtori CR, Marcel Y, Franceschini G, Limited proteolysis of a disulfide-linked apoA-I dimer in reconstituted HDL. J Lipid Res 2001 42 935 942
38. Vaughan AM, Tang C, Oram JF, ABCA1 mutants reveal an interdependency between lipid export function, apoA-I binding activity, and Janus kinase 2 activation. J Lipid Res 2009; 50: 285-292. doi: 10.1194/jlr.M800366-JLR200.
39. Sankaranarayanan S, Oram JF, Asztalos BF, Vaughan AM, Lund-Katz S, Adorni MP, Phillips MC, Rothblat GH, Effects of acceptor composition and mechanism of ABCG1-mediated cellular free cholesterol efflux. J Lipid Res 2009; 50: 275-284. doi: 10.1194/jlr.M800362-JLR200.
40. 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 U S A 2004; 101: 9774-9779. doi: 10.1073/pnas.0403506101.