High density lipoprotein biogenesis, cholesterol efflux, and immune cell function

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 11, 2012, Pages 2561-2565

  Sorci Thomas, Mary G ^a   Thomas, Michael J ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Apolipoprotein A I; Atherosclerosis; Autoimmunity; Cholesterol efflux; Lipid rafts; Nascent high density lipoprotein; T cells; T regulatory cells (CD4+CD25+FoxP3)

Indexed keywords

ABC TRANSPORTER A1; APOLIPOPROTEIN A1; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; SPHINGOSINE 1 PHOSPHATE; ABC TRANSPORTER; DRUG DERIVATIVE; LYSOPHOSPHOLIPID; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE;

ARTICLE; ATHEROSCLEROSIS; AUTOIMMUNITY; BIOGENESIS; CARDIOVASCULAR DISEASE; CELL FUNCTION; CELL MEMBRANE; CHOLESTEROL TRANSPORT; CORONARY VASCULAR DISEASE; HOMEOSTASIS; HUMAN; IMMUNOCOMPETENT CELL; LIPID RAFT; LIPOPROTEIN BLOOD LEVEL; LIVER; NONHUMAN; PRIORITY JOURNAL; RISK; T LYMPHOCYTE ACTIVATION; ANIMAL; BIOSYNTHESIS; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE ACTIVATION; METABOLISM; REVIEW; T LYMPHOCYTE; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; APOLIPOPROTEIN A-I; ATHEROSCLEROSIS; ATP-BINDING CASSETTE TRANSPORTERS; AUTOIMMUNITY; BIOLOGICAL TRANSPORT; CHOLESTEROL; HOMEOSTASIS; HUMANS; INFLAMMATION; LIPOPROTEINS, HDL; LYMPHOCYTE ACTIVATION; LYSOPHOSPHOLIPIDS; MEMBRANE MICRODOMAINS; SPHINGOSINE; T-LYMPHOCYTES;

EID: 84871865547     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300135     Document Type: Article

References (85)

1. Castelli WP, Doyle JT, Gordon T, Hames CG, Hjortland MC, Hulley SB, Kagan A, Zukel WJ. HDL cholesterol and other lipids in coronary heart disease. The cooperative lipoprotein phenotyping study. Circulation. 1977;55:767-772.
2. Duffy D, Rader DJ. Update on strategies to increase HDL quantity and function. Nat Rev Cardiol. 2009;6:455-463.
3. Brown WV, Brewer HB, Rader DJ, Schaefer EJ. HDL as a treatment target. J Clin Lipidol. 2010;4:5-16.
4. 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 effux capacity, high-density lipopro-tein function, and atherosclerosis. N Engl J Med. 2011;364:127-135.
5. Francis GA. The complexity of HDL. Biochim Biophys Acta. 2010;1801: 1286-1293.
6. Oram JF, Heinecke JW. ATP-binding cassette transporter A1: a cell cholesterol exporter that protects against cardiovascular disease. Physiol Rev. 2005;85:1343-1372.
7. Timmins JM, Lee JY, Boudyguina E, Kluckman KD, Brunham LR, Mulya A, Gebre AK, Coutinho JM, Colvin PL, Smith TL, Hayden MR, Maeda N, Parks JS. Targeted inactivation of hepatic Abca1 causes profound hypoal-phalipoproteinemia and kidney hypercatabolism of apoA-I. J Clin Invest. 2005;115:1333-1342.
8. Brunham LR, Singaraja RR, Duong M, Timmins JM, Fievet C, Bissada N, Kang MH, Samra A, Fruchart JC, McManus B, Staels B, Parks JS, Hayden MR. Tissue-specifc roles of ABCA1 infuence susceptibility to atherosclerosis. Arterioscler Thromb Vasc Biol. 2009;29:548-554.
9. Wellington CL, Walker EK, Suarez A, Kwok A, Bissada N, Singaraja R, Yang YZ, Zhang LH, James E, Wilson JE, Francone O, McManus BM, Hayden MR. ABCA1 mRNA and protein distribution patterns predict multiple different roles and levels of regulation. Lab Invest. 2002;82:273-283.
10. Simons K, Sampaio JL. Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol. 2011;3:a004697.
11. Lingwood D, Simons K. Lipid rafts as a membrane-organizing principle. Science. 2010;327:46-50.
12. Fessler MB, Parks JS. Intracellular lipid fux and membrane microdo-mains as organizing principles in infammatory cell signaling. J Immunol. 2011;187:1529-1535.
13. Yvan-Charvet L, Wang N, Tall AR. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol effux and immune responses. Arterioscler Thromb Vasc Biol. 2010;30:139-143.
14. Kaminski WE, Piehler A, Wenzel JJ. ABC A-subfamily transporters: structure, function and disease. Biochim Biophys Acta. 2006;1762:510-524.
15. Voloshyna I, Reiss AB. The ABC transporters in lipid fux and atherosclerosis. Prog Lipid Res. 2011;50:213-224.
16. 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.
17. Rosenson RS, Brewer HB Jr, Davidson WS, Fayad ZA, Fuster V, Goldstein J, Hellerstein M, Jiang XC, Phillips MC, Rader DJ, Remaley AT, Rothblat GH, Tall AR, Yvan-Charvet L. Cholesterol effux and atheroprotection: advancing the concept of reverse cholesterol transport. Circulation. 2012;125:1905-1919.
18. 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.
19. Repa JJ, Turley SD, Lobaccaro JA, Medina J, Li L, Lustig K, Shan B, Heyman RA, Dietschy JM, Mangelsdorf DJ. Regulation of absorption and ABC1-mediated effux of cholesterol by RXR heterodimers. Science. 2000;289:1524-1529.
20. Venkateswaran A, Lafftte BA, Joseph SB, Mak PA, Wilpitz DC, Edwards PA, Tontonoz P. Control of cellular cholesterol effux by the nuclear oxys-terol receptor LXR alpha. Proc Natl Acad Sci USA. 2000;97:12097-12102.
21. Sabol SL, Brewer HB Jr, Santamarina-Fojo S. The human ABCG1 gene: identifcation of LXR response elements that modulate expression in mac-rophages and liver. J Lipid Res. 2005;46:2151-2167.
22. Tangirala RK, Bischoff ED, Joseph SB, Wagner BL, Walczak R, Lafftte BA, Daige CL, Thomas D, Heyman RA, Mangelsdorf DJ, Wang X, Lusis AJ, Tontonoz P, Schulman IG. Identifcation of macrophage liver X receptors as inhibitors of atherosclerosis. Proc Natl Acad Sci USA. 2002;99:11896-11901.
23. Lehmann JM, Kliewer SA, Moore LB, Smith-Oliver TA, Oliver BB, Su JL, Sundseth SS, Winegar DA, Blanchard DE, Spencer TA, Willson TM. Activation of the nuclear receptor LXR by oxysterols defnes a new hormone response pathway. J Biol Chem. 1997;272:3137-3140.
24. Peet DJ, Turley SD, Ma W, Janowski BA, Lobaccaro JM, Hammer RE, Mangelsdorf DJ. Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha. Cell. 1998;93:693-704.
25. Huuskonen J, Vishnu M, Chau P, Fielding PE, Fielding CJ. Liver X receptor inhibits the synthesis and secretion of apolipoprotein A1 by human liver-derived cells. Biochemistry. 2006;45:15068-15074.
26. Mogilenko DA, Dizhe EB, Shavva VS, Lapikov IA, Orlov SV, Perevozchikov AP. Role of the nuclear receptors HNF4 alpha, PPAR alpha, and LXRs in the TNF alpha-mediated inhibition of human apolipoprotein A-I gene expression in HepG2 cells. Biochemistry. 2009;48:11950-11960.
27. Hamon Y, Broccardo C, Chambenoit O, Luciani MF, Toti F, Chaslin S, Freyssinet JM, Devaux PF, McNeish J, Marguet D, Chimini G. ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat Cell Biol. 2000;2:399-406.
28. Krimbou L, Hajj Hassan H, Blain S, Rashid S, Denis M, Marcil M, Genest J. Biogenesis and speciation of nascent apoA-I-containing particles in various cell lines. J Lipid Res. 2005;46:1668-1677.
29. Luciani MF, Chimini G. The ATP binding cassette transporter ABC1, is required for the engulfment of corpses generated by apoptotic cell death. EMBO J. 1996;15:226-235.
30. Mulya A, Lee JY, Gebre AK, Thomas MJ, Colvin PL, Parks JS. Minimal lipidation of pre-beta HDL by ABCA1 results in reduced ability to interact with ABCA1. Arterioscler Thromb Vasc Biol. 2007;27:1828-1836.
31. Liu L, Bortnick AE, Nickel M, Dhanasekaran P, Subbaiah PV, Lund-Katz S, Rothblat GH, Phillips MC. Effects of apolipoprotein A-I on ATP-binding cassette transporter A1-mediated effux of macrophage phos-pholipid and cholesterol: formation of nascent high density lipoprotein particles. J Biol Chem. 2003;278:42976-42984.
32. Mulya A, Lee JY, Gebre AK, Boudyguina EY, Chung SK, Smith TL, Colvin PL, Jiang XC, Parks JS. Initial interaction of apoA-I with ABCA1 impacts in vivo metabolic fate of nascent HDL. J Lipid Res. 2008;49:2390-2401.
33. Sorci-Thomas MG, Owen JS, Fulp B, Bhat S, Zhu X, Parks JS, Shah D, Jerome WG, Gerelus M, Zabalawi M, Thomas MJ. Nascent high density lipoproteins formed by ABCA1 resemble lipid rafts and are structurally organized by three apoA-I monomers. J Lipid Res. 2012;53:1890-1909.
34. Norum KR, Glomset JA, Nichols AV, Forte T. Plasma lipoproteins in familial lecithin: cholesterol acyltransferase defciency: physical and chemical studies of low and high density lipoproteins. J Clin Invest. 1971;50: 1131-1140.
35. Mitchell CD, King WC, Applegate KR, Forte T, Glomset JA, Norum KR, Gjone E. Characterization of apolipoprotein E-rich high density lipopro-teins in familial lecithin:cholesterol acyltransferase defciency. J Lipid Res. 1980;21:625-634.
36. Simons K, Ikonen E. Functional rafts in cell membranes. Nature. 1997;387:569-572.
37. Landry YD, Denis M, Nandi S, Bell S, Vaughan AM, Zha X. ATP-binding cassette transporter A1 expression disrupts raft membrane microdomains through its ATPase-related functions. J Biol Chem. 2006; 281:36091-36101.
38. Mendez AJ, Lin G, Wade DP, Lawn RM, Oram JF. Membrane lipid domains distinct from cholesterol/sphingomyelin-rich rafts are involved in the ABCA1-mediated lipid secretory pathway. J Biol Chem. 2001; 276:3158-3166.
39. Kobayashi A, Takanezawa Y, Hirata T, Shimizu Y, Misasa K, Kioka N, Arai H, Ueda K, Matsuo M. Effux of sphingomyelin, cholesterol, and phosphatidylcholine by ABCG1. J Lipid Res. 2006;47:1791-1802.
40. Sano O, Kobayashi A, Nagao K, Kumagai K, Kioka N, Hanada K, Ueda K, Matsuo M. Sphingomyelin-dependence of cholesterol effux mediated by ABCG1. J Lipid Res. 2007;48:2377-2384.
41. Nagao K, Takahashi K, Hanada K, Kioka N, Matsuo M, Ueda K. Enhanced apoA-I-dependent cholesterol effux by ABCA1 from sphingomyelin-defcient Chinese hamster ovary cells. J Biol Chem. 2007;282:14868-14874.
42. Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol. 2011;12:204-212.
43. Lange Y. Disposition of intracellular cholesterol in human fbroblasts. J Lipid Res. 1991;32:329-339.
44. Owen DM, Magenau A, Williamson D, Gaus K. The lipid raft hypothesis revisited-New insights on raft composition and function from super-resolution fuorescence microscopy. Bioessays. 2012;34:739-747.
45. Staubach S, Hanisch FG. Lipid rafts: signaling and sorting platforms of cells and their roles in cancer. Expert Rev Proteomics. 2011;8:263-277.
46. James JR, Vale RD. Biophysical mechanism of T-cell receptor triggering in a reconstituted system. Nature. 2012;487:64-69.
47. Simons K, Gerl MJ. Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol. 2010;11:688-699.
48. Surls J, Nazarov-Stoica C, Kehl M, Olsen C, Casares S, Brumeanu TD. Increased membrane cholesterol in lymphocytes diverts T-cells toward an infammatory response. PLoS ONE. 2012;7:e38733.
49. Dong L, Watanabe K, Itoh M, et al. CD4+ T-cell dysfunctions through the impaired lipid rafts ameliorate concanavalin A-induced hepatitis in sphin-gomyelin synthase 1-knockout mice. Int Immunol. 2012;24:327-337.
50. Yin K, Chen WJ, Zhou ZG, Zhao GJ, Lv YC, Ouyang XP, Yu XH, Fu Y, Jiang ZS, Tang CK. Apolipoprotein A-I inhibits CD40 proinfammatory signaling via ATP-binding cassette transporter A1-mediated modulation of lipid raft in macrophages. J Atheroscler Thromb. 2012;19:823-836.
51. Cheng AM, Handa P, Tateya S, Schwartz J, Tang C, Mitra P, Oram JF, Chait A, Kim F. Apolipoprotein A-I attenuates palmitate-mediated NF-?B activation by reducing Toll-like receptor-4 recruitment into lipid rafts. PLoS ONE. 2012;7:e33917.
52. Wilhelm AJ, Zabalawi M, Owen JS, Shah D, Grayson JM, Major AS, Bhat S, Gibbs DP Jr, Thomas MJ, Sorci-Thomas MG. Apolipoprotein A-I modulates regulatory T cells in autoimmune LDLr-/-, ApoA-I-/-mice. J Biol Chem. 2010;285:36158- 36169.
53. Wilhelm AJ, Zabalawi M, Grayson JM, Weant AE, Major AS, Owen J, Bharadwaj M, Walzem R, Chan L, Oka K, Thomas MJ, Sorci-Thomas MG. Apolipoprotein A-I and its role in lymphocyte cholesterol homeosta-sis and autoimmunity. Arterioscler Thromb Vasc Biol. 2009;29:843-849.
54. Zabalawi M, Bharadwaj M, Horton H, Cline M, Willingham M, Thomas MJ, Sorci-Thomas MG. Infammation and skin cholesterol in LDLr-/-, apoA-I-/-mice: link between cholesterol homeostasis and self-tolerance? J Lipid Res. 2007;48:52-65.
55. Zabalawi M, Bhat S, Loughlin T, Thomas MJ, Alexander E, Cline M, Bullock B, Willingham M, Sorci-Thomas MG. Induction of fatal infam-mation in LDL receptor and ApoA-I double-knockout mice fed dietary fat and cholesterol. Am J Pathol. 2003;163:1201-1213.
56. Coutinho JM, Singaraja RR, Kang M, Arenillas DJ, Bertram LN, Bissada N, Staels B, Fruchart JC, Fievet C, Joseph-George AM, Wasserman WW, Hayden MR. Complete functional rescue of the ABCA1-/-mouse by human BAC transgenesis. J Lipid Res. 2005;46:1113-1123.
57. Yvan-Charvet L, Ranalletta M, Wang N, Han S, Terasaka N, Li R, Welch C, Tall AR. Combined defciency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J Clin Invest. 2007;117:3900-3908.
58. Aiello RJ, Brees D, Bourassa PA, Royer L, Lindsey S, Coskran T, Haghpassand M, Francone OL. Increased atherosclerosis in hyperlip-idemic mice with inactivation of ABCA1 in macrophages. Arterioscler Thromb Vasc Biol. 2002;22:630-637.
59. Sherer Y, Shoenfeld Y. Mechanisms of disease: atherosclerosis in autoimmune diseases. Nat Clin Pract Rheumatol. 2006;2:99-106.
60. Shoenfeld Y, Harats D, Wick G. Atherosclerosis and Autoimmunity. New York, NY: Elsevier; 2001.
61. Narshi CB, Giles IP, Rahman A. The endothelium: an interface between autoimmunity and atherosclerosis in systemic lupus erythematosus? Lupus. 2011;20:5-13.
62. Shoenfeld Y, Gerli R, Doria A, Matsuura E, Cerinic MM, Ronda N, Jara LJ, Abu-Shakra M, Meroni PL, Sherer Y. Accelerated atherosclerosis in autoimmune rheumatic diseases. Circulation. 2005;112:3337-3347.
63. Norata GD, Pirillo A, Ammirati E, Catapano AL. Emerging role of high density lipoproteins as a player in the immune system. Atherosclerosis. 2012;220:11-21.
64. Haraba R, Antohe F. T cells are active participants in the progression of atherosclerotic plaques. Dig J Nanomater Bios. 2011;6:1529-1534.
65. Taleb S, Tedgui A, Mallat Z. Adaptive T cell immune responses and atherogenesis. Curr Opin Pharmacol. 2010;10:197-202.
66. Lichtman AH. T cell costimulatory and coinhibitory pathways in vascular infammatory diseases. Front Physiol. 2012;3:18.
67. Lahoute C, Herbin O, Mallat Z, Tedgui A. Adaptive immunity in atherosclerosis: mechanisms and future therapeutic targets. Nat Rev Cardiol. 2011;8:348-358.
68. Peng Y, Laouar Y, Li MO, Green EA, Flavell RA. TGF-beta regulates in vivo expansion of Foxp3-expressing CD4+CD25+ regulatory T cells responsible for protection against diabetes. Proc Natl Acad Sci USA. 2004;101:4572-4577.
69. Morgan ME, Flierman R, van Duivenvoorde LM, Witteveen HJ, van Ewijk W, van Laar JM, de Vries RR, Toes RE. Effective treatment of collagen-induced arthritis by adoptive transfer of CD25+ regulatory T cells. Arthritis Rheum. 2005;52:2212-2221.
70. Zhang L, Bertucci AM, Ramsey-Goldman R, Burt RK, Datta SK. Regulatory T cell (Treg) subsets return in patients with refractory lupus following stem cell transplantation, and TGF-beta-producing CD8+ Treg cells are associated with immunological remission of lupus. J Immunol. 2009;183:6346-6358.
71. Foks AC, Frodermann V, ter Borg M, Habets KL, Bot I, Zhao Y, van Eck M, van Berkel TJ, Kuiper J, van Puijvelde GH. Differential effects of regulatory T cells on the initiation and regression of atherosclerosis. Atherosclerosis. 2011;218:53-60.
72. Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdy P, Zoll J, Merval R, Esposito B, Cohen JL, Fisson S, Flavell RA, Hansson GK, Klatzmann D, Tedgui A, Mallat Z. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med. 2006;12: 178-180.
73. Maganto-García E, Tarrio ML, Grabie N, Bu DX, Lichtman AH. Dynamic changes in regulatory T cells are linked to levels of diet-induced hypercho-lesterolemia. Circulation. 2011;124:185-195.
74. van Es T, van Puijvelde GH, Foks AC, Habets KL, Bot I, Gilboa E, Van Berkel TJ, Kuiper J. Vaccination against Foxp3(+) regulatory T cells aggravates atherosclerosis. Atherosclerosis. 2010;209:74-80.
75. Argraves KM, Argraves WS. HDL serves as a S1P signaling platform mediating a multitude of cardiovascular effects. J Lipid Res. 2007; 48:2325-2333.
76. Bolick DT, Srinivasan S, Kim KW, Hatley ME, Clemens JJ, Whetzel A, Ferger N, Macdonald TL, Davis MD, Tsao PS, Lynch KR, Hedrick CC. Sphingosine-1- phosphate prevents tumor necrosis factor-{alpha}-mediated monocyte adhesion to aortic endothelium in mice. Arterioscler Thromb Vasc Biol. 2005;25:976-981.
77. Hughes JE, Srinivasan S, Lynch KR, Proia RL, Ferdek P, Hedrick CC. Sphingosine-1-phosphate induces an antiinfammatory phenotype in macrophages. Circ Res. 2008;102:950-958.
78. Hammad SM, Pierce JS, Soodavar F, Smith KJ, Al Gadban MM, Rembiesa B, Klein RL, Hannun YA, Bielawski J, Bielawska A. Blood sphingolipido-mics in healthy humans: impact of sample collection methodology. J Lipid Res. 2010;51:3074-3087.
79. Christoffersen C, Obinata H, Kumaraswamy SB, Galvani S, Ahnström J, Sevvana M, Egerer-Sieber C, Muller YA, Hla T, Nielsen LB, Dahlbäck B. Endothelium-protective sphingosine-1-phosphate provided by HDL-associated apolipoprotein M. Proc Natl Acad Sci USA. 2011;108:9613-9618.
80. Karuna R, Park R, Othman A, Holleboom AG, Motazacker MM, Sutter I, Kuivenhoven JA, Rohrer L, Matile H, Hornemann T, Stoffel M, Rentsch KM, von Eckardstein A. Plasma levels of sphingosine-1-phosphate and apolipoprotein M in patients with monogenic disorders of HDL metabolism. Atherosclerosis. 2011;219:855-863.
81. Sato K, Okajima F. Role of sphingosine 1-phosphate in anti-atherogenic actions of high-density lipoprotein. World J Biol Chem. 2010;1:327-337.
82. Kobayashi N, Kobayashi N, Yamaguchi A, Nishi T. Characterization of the ATP-dependent sphingosine 1-phosphate transporter in rat erythrocytes. J Biol Chem. 2009;284:21192-21200.
83. Sato K, Malchinkhuu E, Horiuchi Y, Mogi C, Tomura H, Tosaka M, Yoshimoto Y, Kuwabara A, Okajima F. Critical role of ABCA1 transporter in sphingosine 1-phosphate release from astrocytes. J Neurochem. 2007;103:2610-2619.
84. Liu G, Yang K, Burns S, Shrestha S, Chi H. The S1P(1)-mTOR axis directs the reciprocal differentiation of T(H)1 and T(reg) cells. Nat Immunol. 2010;11:1047-1056.
85. Kappos L, Radue EW, O'Connor P, Polman C, Hohlfeld R, Calabresi P, Selmaj K, Agoropoulou C, Leyk M, Zhang-Auberson L, Burtin P; FREEDOMS Study Group. A placebo-controlled trial of oral fngolimod in relapsing multiple sclerosis. N Engl J Med. 2010;362:387-401.