The cell cholesterol exporter ABCA1 as a protector from cardiovascular disease and diabetes

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1791, Issue 7, 2009, Pages 563-572

  Tang, Chongren ^a   Oram, John F ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

ABCA1; Apolipoprotein A I; Cardiovascular disease; Cell cholesterol export; Diabetes; HDL; Inflammation; Macrophage

Indexed keywords

ABC TRANSPORTER A1; APOLIPOPROTEIN; HIGH DENSITY LIPOPROTEIN; STEROL;

ANTIINFLAMMATORY ACTIVITY; ATHEROGENESIS; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CELL SURFACE; CHOLESTEROL TRANSPORT; DIABETES MELLITUS; DRUG TARGETING; GENE MUTATION; GENETIC MANIPULATION; HUMAN; LIPOPROTEIN BLOOD LEVEL; LIPOPROTEIN DEFICIENCY; MACROPHAGE; METABOLIC REGULATION; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS FUNCTION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; CARDIOVASCULAR DISEASES; CHOLESTEROL; DIABETES MELLITUS, TYPE 2; HUMANS; MICE; MODELS, BIOLOGICAL; MUTANT PROTEINS; TRANSCRIPTION, GENETIC;

MUS;

EID: 67649262236     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2009.03.011     Document Type: Review

References (166)

1. Pike L.J. Lipid rafts: heterogeneity on the high seas. Biochem. J. 378 (2004) 281-292
2. Lewis P.M., Dunn M.P., McMahon J.A., Logan M., Martin J.F., St-Jacques B., and McMahon A.P. Cholesterol modification of sonic hedgehog is required for long-range signaling activity and effective modulation of signaling by Ptc1. Cell 105 (2001) 599-612
3. Feng B., Yao P.M., Li Y., Devlin C.M., Zhang D., Harding H.P., Sweeney M., Rong J.X., Kuriakose G., Fisher E.A., Marks A.R., Ron D., and Tabas I. The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat. Cell Biol. 5 (2003) 781-792
4. Guyton J.R., and Klemp K.F. Development of the lipid-rich core in human atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 16 (1996) 4-11
5. Wellington C.L. Cholesterol at the crossroads: Alzheimer's disease and lipid metabolism. Clin. Genet. 66 (2004) 1-16
6. Abrass C.K. Cellular lipid metabolism and the role of lipids in progressive renal disease. Am. J. Nephrol. 24 (2004) 46-53
7. Kees-Folts D., and Diamond J.R. Relationship between hyperlipidemia, lipid mediators, and progressive glomerulosclerosis in the nephrotic syndrome. Am. J. Nephrol. 13 (1993) 365-375
8. Fielding C.J., and Fielding P.E. Molecular physiology of reverse cholesterol transport. J. Lipid Res. 36 (1995) 211-228
9. Rothblat G.H., de la Llera-Moya M., Atger V., Kellner-Weibel G., Williams D.L., and Phillips M.C. Cell cholesterol efflux: integration of old and new observations provides new insights. J. Lipid Res. 40 (1999) 781-796
10. Dean M., Hamon Y., and Chimini G. The human ATP-binding cassette (ABC) transporter superfamily. J. Lipid Res. 42 (2001) 1007-1017
11. Oram J.F. HDL Apolipoproteins and ABCA1: partners in the removal of excess cellular cholesterol. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 720-727
12. Oram J.F., and Heinecke J.W. ATP-binding cassette transporter A1: a cell cholesterol exporter that protects against cardiovascular disease. Physiol. Rev. 85 (2005) 1343-1372
13. Tall A.R. ATVB in focus: role of ABCA1 in cellular cholesterol efflux and reverse cholesterol transport. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 710-711
14. Rothblat G.H., Mahlberg F.H., Johnson W.J., and Phillips M.C. Apolipoproteins, membrane cholesterol domains, and the regulation of cholesterol efflux. J. Lipid Res. 33 (1992) 1091-1097
15. Nakamura K., Kennedy M.A., Baldan A., Bojanic D.D., Lyons K., and Edwards P.A. Expression and regulation of multiple murine ATP-binding cassette transporter G1 mRNAs/isoforms that stimulate cellular cholesterol efflux to high density lipoprotein. J. Biol. Chem. 279 (2004) 45980-45989
16. Oldfield S., Lowry C., Ruddick J., and Lightman S. ABCG4: a novel human white family ABC-transporter expressed in the brain and eye. Biochim. Biophys. Acta 1591 (2002) 175-179
17. Schmitz G., Langmann T., and Heimerl S. Role of ABCG1 and other ABCG family members in lipid metabolism. J. Lipid Res. 42 (2001) 1513-1520
18. Wang N., Lan D., Chen W., Matsuura F., and Tall A.R. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 9774-9779
19. Vaughan A.M., and Oram J.F. ABCA1 and ABCG1 or ABCG4 act sequentially to remove cellular cholesterol and generate cholesterol-rich HDL. J. Lipid Res. 47 (2006) 2433-2443
20. Gelissen I.C., Harris M., Rye K.A., Quinn C., Brown A.J., Kockx M., Cartland S., Packianathan M., Kritharides L., and Jessup W. ABCA1 and ABCG1 synergize to mediate cholesterol export to apoA-I. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 534-540
21. Fitzgerald M.L., Mendez A.J., Moore K.J., Andersson L.P., Panjeton H.A., and Freeman M.W. ATP-binding cassette transporter A1 contains an NH2-terminal signal anchor sequence that translocates the protein's first hydrophilic domain to the exoplasmic space. J. Biol. Chem. 276 (2001) 15137-15145
22. Attie A.D. ABCA1: at the nexus of cholesterol, HDL and atherosclerosis. Trends Biochem. Sci. 32 (2007) 172-179
23. Neufeld E.B., Remaley A.T., Demosky S.J., Stonik J.A., Cooney A.M., Comly M., Dwyer N.K., Zhang M., Blanchette-Mackie J., Santamarina-Fojo S., and Brewer Jr. H.B. Cellular localization and trafficking of the human ABCA1 transporter. J. Biol. Chem. 276 (2001) 27584-27590
24. Neufeld E.B., Stonik J.A., Demosky Jr. S.J., Knapper C.L., Combs C.A., Cooney A., Comly M., Dwyer N., Blanchette-Mackie J., Remaley A.T., Santamarina-Fojo S., and Brewer Jr. H.B. The ABCA1 transporter modulates late endocytic trafficking: insights from the correction of the genetic defect in Tangier disease. J. Biol. Chem. 279 (2004) 15571-15578
25. Chen W., Wang N., and Tall A.R. A PEST deletion mutant of ABCA1 shows impaired internalization and defective cholesterol efflux from late endosomes. J. Biol. Chem. 280 (2005) 29277-29281
26. Denis M., Landry Y.D., and 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. 283 (2008) 16178-16186
27. Faulkner L.E., Panagotopulos S.E., Johnson J.D., Woollett L.A., Hui D.Y., Witting S.R., Maiorano J.N., and Davidson W.S. An analysis of the role of a retroendocytosis pathway in ABCA1-mediated cholesterol efflux from macrophages. J. Lipid Res. 49 (2008) 1322-1332
28. Lu R., Arakawa R., Ito-Osumi C., Iwamoto N., and Yokoyama S. ApoA-I facilitates ABCA1 recycle/accumulation to cell surface by inhibiting its intracellular degradation and increases HDL generation. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 1820-1824
29. Denis M., Haidar B., Marcil M., Bouvier M., Krimbou L., and Genest J. Characterization of oligomeric human ATP binding cassette transporter A1. Potential implications for determining the structure of nascent high density lipoprotein particles. J. Biol. Chem. 279 (2004) 41529-41536
30. Trompier D., Alibert M., Davanture S., Hamon Y., Pierres M., and Chimini G. Transition from dimers to higher oligomeric forms occurs during the ATPase cycle of the ABCA1 transporter. J. Biol. Chem. (2006)
31. Vaughan A.M., and Oram J.F. ABCA1 redistributes membrane cholesterol independent of apolipoprotein interactions. J. Lipid. Res. 44 (2003) 1373-1380
32. Wang N., Silver D.L., Thiele C., and Tall A.R. ATP-binding cassette transporter A1 (ABCA1) functions as a cholesterol efflux regulatory protein. J. Biol. Chem. 276 (2001) 23742-23747
33. Fielding P.E., Nagao K., Hakamata H., Chimini G., and Fielding C.J. A two-step mechanism for free cholesterol and phospholipid efflux from human vascular cells to apolipoprotein A-1. Biochemistry 39 (2000) 14113-14120
34. Liu L., Bortnick A.E., Nickel M., Dhanasekaran P., Subbaiah P.V., Lund-Katz S., Rothblat G.H., and Phillips M.C. Effects of apolipoprotein A-I on ATP-binding cassette transporter A1-mediated efflux of macrophage phospholipid and cholesterol: formation of nascent high density lipoprotein particles. J. Biol. Chem. 278 (2003) 42976-42984
35. Chambenoit O., Hamon Y., Marguet D., Rigneault H., Rosseneu M., and Chimini G. Specific docking of apolipoprotein A-I at the cell surface requires a functional ABCA1 transporter. J. Biol. Chem. 276 (2001) 9955-9960
36. Hamon Y., Broccardo C., Chambenoit O., Luciani M.F., Toti F., Chaslin S., Freyssinet J.M., Devaux P.F., McNeish J., Marguet D., and Chimini G. ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat. Cell Biol. 2 (2000) 399-406
37. Combes V., Coltel N., Alibert M., van Eck M., Raymond C., Juhan-Vague I., Grau G.E., and Chimini G. ABCA1 gene deletion protects against cerebral malaria: potential pathogenic role of microparticles in neuropathology. Am. J. Pathol. 166 (2005) 295-302
38. Nandi S., Ma L., Denis M., Karwatsky J., Li Z., Jiang X.C., and Zha X. ABCA1-mediated cholesterol efflux generates microparticles in addition to HDL through processes governed by membrane rigidity. J. Lipid Res. (2008)
39. Duong P.T., Collins H.L., Nickel M., Lund-Katz S., Rothblat G.H., and Phillips M.C. Characterization of nascent HDL particles and microparticles formed by ABCA1-mediated efflux of cellular lipids to apoA-I. J. Lipid Res. 47 (2006) 832-843
40. Oram J.F., Vaughan A.M., and Stocker R. ATP-binding cassette transporter A1 mediates cellular secretion of alpha-tocopherol. J. Biol. Chem. 276 (2001) 39898-39902
41. Von Eckardstein A., Langer C., Engel T., Schaukal I., Cignarella A., Reinhardt J., Lorkowski S., Li Z., Zhou X., Cullen P., and Assmann G. ATP binding cassette transporter ABCA1 modulates the secretion of apolipoprotein E from human monocyte-derived macrophages. FASEB J. 15 (2001) 1555-1561
42. Zhou X., Engel T., Goepfert C., Erren M., Assmann G., and von Eckardstein A. The ATP binding cassette transporter A1 contributes to the secretion of interleukin 1beta from macrophages but not from monocytes. Biochem. Biophys. Res. Commun. 291 (2002) 598-604
43. Hamon Y., Luciani M.F., Becq F., Verrier B., Rubartelli A., and Chimini G. Interleukin-1beta secretion is impaired by inhibitors of the Atp binding cassette transporter, ABC1. Blood 90 (1997) 2911-2915
44. Duong P.T., Weibel G.L., Lund-Katz S., Rothblat G.H., and Phillips M.C. Characterization and properties of pre beta-HDL particles formed by ABCA1-mediated cellular lipid efflux to apoA-I. J. Lipid Res. 49 (2008) 1006-1014
45. Mulya A., Lee J.Y., Gebre A.K., Thomas M.J., Colvin P.L., and Parks J.S. Minimal lipidation of pre-beta HDL by ABCA1 results in reduced ability to interact with ABCA1. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 1828-1836
46. Remaley A.T., Stonik J.A., Demosky S.J., Neufeld E.B., Bocharov A.V., Vishnyakova T.G., Eggerman T.L., Patterson A.P., Duverger N.J., Santamarina-Fojo S., and Brewer Jr. H.B. Apolipoprotein specificity for lipid efflux by the human ABCAI transporter. Biochem. Biophys. Res. Commun. 280 (2001) 818-823
47. Segrest J.P., Jones M.K., De Loof H., Brouillette C.G., Venkatachalapathi Y.V., and Anantharamaiah G.M. The amphipathic helix in the exchangeable apolipoproteins: a review of secondary structure and function. J. Lipid Res. 33 (1992) 141-166
48. Mendez A.J., Anantharamaiah G.M., Segrest J.P., and Oram J.F. Synthetic amphipathic helical peptides that mimic apolipoprotein A-I in clearing cellular cholesterol. J. Clin. Invest. 94 (1994) 1698-1705
49. Remaley A.T., Thomas F., Stonik J.A., Demosky S.J., Bark S.E., Neufeld E.B., Bocharov A.V., Vishnyakova T.G., Patterson A.P., Eggerman T.L., Santamarina-Fojo S., and Brewer H.B. Synthetic amphipathic helical peptides promote lipid efflux from cells by an ABCA1-dependent and an ABCA1-independent pathway. J. Lipid Res. 44 (2003) 828-836
50. Tang C., Vaughan A.M., Anantharamaiah G.M., and Oram J.F. Janus kinase 2 modulates the lipid-removing but not protein-stabilizing interactions of amphipathic helices with ABCA1. J. Lipid Res. 47 (2006) 107-114
51. Yancey P.G., Bielicki J.K., Johnson W.J., Lund-Katz S., Palgunachari M.N., Anantharamaiah G.M., Segrest J.P., Phillips M.C., and Rothblat G.H. Efflux of cellular cholesterol and phospholipid to lipid-free apolipoproteins and class A amphipathic peptides. Biochemistry 34 (1995) 7955-7965
52. Arakawa R., and Yokoyama S. Helical apolipoproteins stabilize ATP-binding cassette transporter A1 by protecting it from thiol protease-mediated degradation. J. Biol. Chem. 277 (2002) 22426-22429
53. Oram J.F., Wolfbauer G., Vaughan A.M., Tang C., and Albers J.J. Phospholipid transfer protein interacts with and stabilizes ATP-binding cassette transporter A1 and enhances cholesterol efflux from cells. J. Biol. Chem. 278 (2003) 52379-52385
54. Oram J.F., Wolfbauer G., Tang C., Davidson W.S., and Albers J.J. An amphipathic helical region of the N-terminal barrel of phospholipid transfer protein is critical for ABCA1-dependent cholesterol efflux. J. Biol. Chem. 283 (2008) 11541-11549
55. Stonik J.A., Remaley A.T., Demosky S.J., Neufeld E.B., Bocharov A., and Brewer H.B. Serum amyloid A promotes ABCA1-dependent and ABCA1-independent lipid efflux from cells. Biochem. Biophys. Res. Commun. 321 (2004) 936-941
56. Hoffman J.S., and Benditt E.P. Changes in high density lipoprotein content following endotoxin administration in the mouse. Formation of serum amyloid protein-rich subfractions. J. Biol. Chem. 257 (1982) 10510-10517
57. Langmann T., Klucken J., Reil M., Liebisch G., Luciani M.F., Chimini G., Kaminski W.E., and Schmitz G. Molecular cloning of the human ATP-binding cassette transporter 1 (hABC1): evidence for sterol-dependent regulation in macrophages. Biochem. Biophys. Res. Commun. 257 (1999) 29-33
58. Lawn R.M., Wade D.P., Garvin M.R., Wang X., Schwartz K., Porter J.G., Seilhamer J.J., Vaughan A.M., and Oram J.F. The Tangier disease gene product ABC1 controls the cellular apolipoprotein-mediated lipid removal pathway. J. Clin. Invest. 104 (1999) R25-31
59. Schwartz K., Lawn R.M., and Wade D.P. ABC1 gene expression and ApoA-I-mediated cholesterol efflux are regulated by LXR. Biochem. Biophys. Res. Commun. 274 (2000) 794-802
60. Costet P., Luo Y., Wang N., and Tall A.R. Sterol-dependent transactivation of the ABC1 promoter by the liver X receptor/retinoid X receptor. J. Biol. Chem. 275 (2000) 28240-28245
61. Repa J.J., and Mangelsdorf D.J. Nuclear receptor regulation of cholesterol and bile acid metabolism. Curr. Opin. Biotechnol. 10 (1999) 557-563
62. Janowski B.A., Grogan M.J., Jones S.A., Wisely G.B., Kliewer S.A., Corey E.J., and Mangelsdorf D.J. Structural requirements of ligands for the oxysterol liver X receptors LXRalpha and LXRbeta. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 266-271
63. Fu X., Menke J.G., Chen Y., Zhou G., MacNaul K.L., Wright S.D., Sparrow C.P., and Lund E.G. 27-hydroxycholesterol is an endogenous ligand for liver X receptor in cholesterol-loaded cells. J. Biol. Chem. 276 (2001) 38378-38387
64. Wellington C.L., Walker E.K., Suarez A., Kwok A., Bissada N., Singaraja R., Yang Y.Z., Zhang L.H., James E., Wilson J.E., Francone O., McManus B.M., and Hayden M.R. ABCA1 mRNA and protein distribution patterns predict multiple different roles and levels of regulation. Lab. Invest. 82 (2002) 273-283
65. Oram J.F., Lawn R.M., Garvin M.R., and Wade D.P. ABCA1 is the cAMP-inducible apolipoprotein receptor that mediates cholesterol secretion from macrophages. J. Biol. Chem. 275 (2000) 34508-34511
66. Wang N., Chen W., Linsel-Nitschke P., Martinez L.O., Agerholm-Larsen B., Silver D.L., and Tall A.R. A PEST sequence in ABCA1 regulates degradation by calpain protease and stabilization of ABCA1 by apoA-I. J. Clin. Invest. 111 (2003) 99-107
67. Wang Y., and Oram J.F. Unsaturated fatty acids inhibit cholesterol efflux from macrophages by increasing degradation of ATP-binding cassette transporter A1. J. Biol. Chem. 277 (2002) 5692-5697
68. Alfaro Leon M.L., Evans G.F., Farmen M.W., and Zuckerman S.H. Post-transcriptional regulation of macrophage ABCA1, an early response gene to IFN-gamma. Biochem. Biophys. Res. Commun. 333 (2005) 596-602
69. Wang Y., Kurdi-Haidar B., and Oram J.F. LXR-mediated activation of macrophage stearoyl-CoA desaturase generates unsaturated fatty acids that destabilize ABCA1. J. Lipid Res. 45 (2004) 972-980
70. Wang Y., and Oram J.F. Unsaturated fatty acids phosphorylate and destabilize ABCA1 through a phospholipase D2 pathway. J. Biol. Chem. 280 (2005) 35896-35903
71. Wang Y., and Oram J.F. Unsaturated fatty acids phosphorylate and destabilize ABCA1 through a protein kinase C delta pathway. J. Lipid Res. 48 (2007) 1062-1068
72. Chroni A., Liu T., Fitzgerald M.L., Freeman M.W., and Zannis V.I. Cross-linking and lipid efflux properties of apoA-I mutants suggest direct association between apoA-I helices and ABCA1. Biochemistry 43 (2004) 2126-2139
73. Fitzgerald M.L., Morris A.L., Chroni A., Mendez A.J., Zannis V.I., and Freeman M.W. ABCA1 and amphipathic apolipoproteins form high-affinity molecular complexes required for cholesterol efflux. J. Lipid Res. 45 (2004) 287-294
74. Tang C., Vaughan A.M., and Oram J.F. Janus kinase 2 modulates the apolipoprotein interactions with ABCA1 required for removing cellular cholesterol. J. Biol. Chem. 279 (2005) 7622-7628
75. Y. Yamauchi, M. Hayashi, S. Abe-Dohmae, S. Yokoyama, ApoA-I activates PKCalpha signaling to phosphorylate and stabilize ABCA1 for the HDL assemblym, J. Biol. Chem. (On line) (in press).
76. Nofer J.R., Remaley A.T., Feuerborn R., Wolinnska I., Engel T., von Eckardstein A., and Assmann G. Apolipoprotein A-I activates Cdc42 signaling through the ABCA1 transporter. J. Lipid Res. 47 (2006) 794-803
77. Kerr I.M., Costa-Pereira A.P., Lillemeier B.F., and Strobl B. Of JAKs, STATs, blind watchmakers, jeeps and trains. FEBS Lett. 546 (2003) 1-5
78. Vaughan A.M., Tang C., and Oram J.F. ABCA1 mutants reveal an interdependency between lipid export function, apoA-I binding activity, and Janus kinase 2 activation. J. Lipid Res. 50 (2009) 285-292
79. Tang C., and Oram J.F. ApoA-I activates both JAK2 and STAT3 through ABCA1, but only JAK2 regulates cholesterol export from cells. Arterioscler. Thromb. Vasc. Biol. 26 (2006) e56
80. Zhu X., Lee J.Y., Timmins J.M., Brown J.M., Boudyguina E., Mulya A., Gebre A.K., Willingham M.C., Hiltbold E.M., Mishra N., Maeda N., and Parks J.S. Increased cellular free cholesterol in macrophage-specific Abca1 knock-out mice enhances pro-inflammatory response of macrophages. J. Biol. Chem. 283 (2008) 22930-22941
81. Koseki M., Hirano K., Masuda D., Ikegami C., Tanaka M., Ota A., Sandoval J.C., Nakagawa-Toyama Y., Sato S.B., Kobayashi T., Shimada Y., Ohno-Iwashita Y., Matsuura F., Shimomura I., and Yamashita S. Increased lipid rafts and accelerated lipopolysaccharide-induced tumor necrosis factor-alpha secretion in Abca1-deficient macrophages. J. Lipid Res. 48 (2007) 299-306
82. Wolf Z., Orso E., Werner T., Klunemann H.H., and Schmitz G. Monocyte cholesterol homeostasis correlates with the presence of detergent resistant membrane microdomains. Cytometry A 71 (2007) 486-494
83. Yvan-Charvet L., Welch C., Pagler T.A., Ranalletta M., Lamkanfi M., Han S., Ishibashi M., Li R., Wang N., and Tall A.R. Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation 118 (2008) 1837-1847
84. Murphy A.J., Woollard K.J., Hoang A., Mukhamedova N., Stirzaker R.A., McCormick S.P., Remaley A.T., Sviridov D., and Chin-Dusting J. High-density lipoprotein reduces the human monocyte inflammatory response. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 2071-2077
85. Tellier E., Canault M., Poggi M., Bonardo B., Nicolay A., Alessi M.C., Nalbone G., and Peiretti F. HDLs activate ADAM17-dependent shedding. J. Cell. Physiol. 214 (2008) 687-693
86. Williams L.M., Sarma U., Willets K., Smallie T., Brennan F., and Foxwell B.M. Expression of constitutively active STAT3 can replicate the cytokine-suppressive activity of interleukin-10 in human primary macrophages. J. Biol. Chem. 282 (2007) 6965-6975
87. Murray P.J. Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 6 (2006) 379-386
88. Levy D.E., and Lee C.K. What does Stat3 do?. J. Clin. Invest. 109 (2002) 1143-1148
89. Rosenberg M.F., Callaghan R., Ford R.C., and Higgins C.F. Structure of the multidrug resistance P-glycoprotein to 2.5 nm resolution determined by electron microscopy and image analysis. J. Biol. Chem. 272 (1997) 10685-10694
90. Ward A., Reyes C.L., Yu J., Roth C.B., and Chang G. Flexibility in the ABC transporter MsbA: alternating access with a twist. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 19005-19010
91. Dawson R.J., and Locher K.P. Structure of a bacterial multidrug ABC transporter. Nature 443 (2006) 180-185
92. Lin G., and Oram J.F. Apolipoprotein binding to protruding membrane domains during removal of excess cellular cholesterol. Atherosclerosis 149 (2000) 359-370
93. Vedhachalam C., Duong P.T., Nickel M., Nguyen D., Dhanasekaran P., Saito H., Rothblat G.H., Lund-Katz S., and Phillips M.C. 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. 282 (2007) 25123-25130
94. Hassan H.H., Denis M., Lee D.Y., Iatan I., Nyholt D., Ruel I., Krimbou L., and Genest J. Identification of an ABCA1-dependent phospholipid-rich plasma membrane apolipoprotein A-I binding site for nascent HDL formation: implications for current models of HDL biogenesis. J. Lipid Res. 48 (2007) 2428-2442
95. Vedhachalam C., Ghering A.B., Davidson W.S., Lund-Katz S., Rothblat G.H., and Phillips M.C. ABCA1-induced cell surface binding sites for ApoA-I. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 1603-1609
96. Singaraja R.R., Brunham L.R., Visscher H., Kastelein J.J., and Hayden M.R. Efflux and atherosclerosis: the clinical and biochemical impact of variations in the ABCA1 gene. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 1322-1332
97. Cohen J.C., Kiss R.S., Pertsemlidis A., Marcel Y.L., McPherson R., and Hobbs H.H. Multiple rare alleles contribute to low plasma levels of HDL cholesterol. Science 305 (2004) 869-872
98. Frikke-Schmidt R., Nordestgaard B.G., Jensen G.B., and Tybjaerg-Hansen A. Genetic variation in ABC transporter A1 contributes to HDL cholesterol in the general population. J. Clin. Invest. 114 (2004) 1343-1353
99. Brunham L.R., Singaraja R.R., and Hayden M.R. Variations on a gene: rare and common variants in ABCA1 and their impact on HDL cholesterol levels and atherosclerosis. Annu. Rev. Nutr. (2006)
100. Clee S.M., Kastelein J.J., van Dam M., Marcil M., Roomp K., Zwarts K.Y., Collins J.A., Roelants R., Tamasawa N., Stulc T., Suda T., Ceska R., Boucher B., Rondeau C., DeSouich C., Brooks-Wilson A., Molhuizen H.O., Frohlich J., Genest Jr. J., and Hayden M.R. Age and residual cholesterol efflux affect HDL cholesterol levels and coronary artery disease in ABCA1 heterozygotes. J. Clin. Invest. 106 (2000) 1263-1270
101. Singaraja R.R., Visscher H., James E.R., Chroni A., Coutinho J.M., Brunham L.R., Kang M.H., Zannis V.I., Chimini G., and Hayden M.R. Specific mutations in ABCA1 have discrete effects on ABCA1 function and lipid phenotypes both in vivo and in vitro. Circ. Res. 99 (2006) 389-397
102. van Dam M.J., de Groot E., Clee S.M., Hovingh G.K., Roelants R., Brooks-Wilson A., Zwinderman A.H., Smit A.J., Smelt A.H., Groen A.K., Hayden M.R., and Kastelein J.J. Association between increased arterial-wall thickness and impairment in ABCA1-driven cholesterol efflux: an observational study. Lancet 359 (2002) 37-42
103. Aiello R.J., Brees D., and Francone O.L. ABCA1-deficient mice: insights into the role of monocyte lipid efflux in HDL formation and inflammation. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 972-980
104. Joyce C., Freeman L., Brewer Jr. H.B., and Santamarina-Fojo S. Study of ABCA1 function in transgenic mice. Arterioscler. Thromb. Vasc. Biol. 23 (2003) 965-971
105. Wellington C.L., Brunham L.R., Zhou S., Singaraja R.R., Visscher H., Gelfer A., Ross C., James E., Liu G., Huber M.T., Yang Y.Z., Parks R.J., Groen A., Fruchart-Najib J., and Hayden M.R. Alterations of plasma lipids in mice via adenoviral-mediated hepatic overexpression of human ABCA1. J. Lipid Res. 44 (2003) 1470-1480
106. Singaraja R.R., Fievet C., Castro G., James E.R., Hennuyer N., Clee S.M., Bissada N., Choy J.C., Fruchart J.C., McManus B.M., Staels B., and Hayden M.R. Increased ABCA1 activity protects against atherosclerosis. J. Clin. Invest. 110 (2002) 35-42
107. Wellington C.L., Brunham L.R., Zhou S., Singaraja R.R., Visscher H., Gelfer A., Ross C., James E., Liu G., Huber M.T., Yang Y.Z., Parks R.J., Groen A., Fruchart-Najib J., and Hayden M.R. Alterations of plasma lipids in mice via adenoviral mediated hepatic overexpression of human ABCA1. J. Lipid Res. (2003)
108. Lee J.Y., and Parks J.S. ATP-binding cassette transporter AI and its role in HDL formation. Curr. Opin. Lipidol. 16 (2005) 19-25
109. Brunham L.R., Kruit J.K., Iqbal J., Fievet C., Timmins J.M., Pape T.D., Coburn B.A., Bissada N., Staels B., Groen A.K., Hussain M.M., Parks J.S., Kuipers F., and Hayden M.R. Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. J. Clin. Invest. 116 (2006) 1052-1062
110. Timmins J.M., Lee J.Y., Boudyguina E., Kluckman K.D., Brunham L.R., Mulya A., Gebre A.K., Coutinho J.M., Colvin P.L., Smith T.L., Hayden M.R., Maeda N., and Parks J.S. Targeted inactivation of hepatic Abca1 causes profound hypoalphalipoproteinemia and kidney hypercatabolism of apoA-I. J. Clin. Invest. 115 (2005) 1333-1342
111. Serfaty-Lacrosniere C., Civeira F., Lanzberg A., Isaia P., Berg J., Janus E.D., Smith Jr. M.P., Pritchard P.H., Frohlich J., Lees R.S., Barnard G.F., Ordovas J.M., and Schaefer E.J. Homozygous Tangier disease and cardiovascular disease. Atherosclerosis 107 (1994) 85-98
112. Frikke-Schmidt R., Nordestgaard B.G., Jensen G.B., Steffensen R., and Tybjaerg-Hansen A. Genetic variation in ABCA1 predicts ischemic heart disease in the general population. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 180-186
113. Frikke-Schmidt R., Nordestgaard B.G., Stene M.C., Sethi A.A., Remaley A.T., Schnohr P., Grande P., and Tybjaerg-Hansen A. Association of loss-of-function mutations in the ABCA1 gene with high-density lipoprotein cholesterol levels and risk of ischemic heart disease. JAMA 299 (2008) 2524-2532
114. Clee S.M., Zwinderman A.H., Engert J.C., Zwarts K.Y., Molhuizen H.O., Roomp K., Jukema J.W., van Wijland M., van Dam M., Hudson T.J., Brooks-Wilson A., Genest Jr. J., Kastelein J.J., and Hayden M.R. Common genetic variation in abca1 is associated with altered lipoprotein levels and a modified risk for coronary artery disease. Circulation 103 (2001) 1198-1205
115. Joyce C.W., Amar M.J., Lambert G., Vaisman B.L., Paigen B., Najib-Fruchart J., Hoyt Jr. R.F., Neufeld E.D., Remaley A.T., Fredrickson D.S., Brewer Jr. H.B., and Santamarina-Fojo S. The ATP binding cassette transporter A1 (ABCA1) modulates the development of aortic atherosclerosis in C57BL/6 and apoE-knockout mice. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 407-412
116. Aiello R.J., Brees D., Bourassa P.A., Royer L., Lindsey S., Coskran T., Haghpassand M., and Francone O.L. Increased atherosclerosis in hyperlipidemic mice with inactivation of ABCA1 in macrophages. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 630-637
117. van Eck M., Bos I.S., Kaminski W.E., Orso E., Rothe G., Twisk J., Bottcher A., Van Amersfoort E.S., Christiansen-Weber T.A., Fung-Leung W.P., Van Berkel T.J., and Schmitz G. Leukocyte ABCA1 controls susceptibility to atherosclerosis and macrophage recruitment into tissues. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 6298-6303
118. Van Eck M., Singaraja R.R., Ye D., Hildebrand R.B., James E.R., Hayden M.R., and Van Berkel T.J. Macrophage ATP-binding cassette transporter A1 overexpression inhibits atherosclerotic lesion progression in low-density lipoprotein receptor knockout mice. Arterioscler. Thromb. Vasc. Biol. 26 (2006) 929-934
119. Brunham L.R., Kruit J.K., Verchere C.B., and Hayden M.R. Cholesterol in islet dysfunction and type 2 diabetes. J. Clin. Invest. 118 (2008) 403-408
120. Brunham L.R., Kruit J.K., Pape T.D., Timmins J.M., Reuwer A.Q., Vasanji Z., Marsh B.J., Rodrigues B., Johnson J.D., Parks J.S., Verchere C.B., and Hayden M.R. Beta-cell ABCA1 influences insulin secretion, glucose homeostasis and response to thiazolidinedione treatment. Nat. Med. 13 (2007) 340-347
121. Gerstein H.C., Yusuf S., Bosch J., Pogue J., Sheridan P., Dinccag N., Hanefeld M., Hoogwerf B., Laakso M., Mohan V., Shaw J., Zinman B., and Holman R.R. Effect of rosiglitazone on the frequency of diabetes in patients with impaired glucose tolerance or impaired fasting glucose: a randomised controlled trial. Lancet 368 (2006) 1096-1105
122. Lehmann J.M., Moore L.B., Smith-Oliver T.A., Wilkison W.O., Willson T.M., and Kliewer S.A. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J. Biol. Chem. 270 (1995) 12953-12956
123. Chawla A., Boisvert W.A., Lee C.H., Laffitte B.A., Barak Y., Joseph S.B., Liao D., Nagy L., Edwards P.A., Curtiss L.K., Evans R.M., and Tontonoz P. A PPAR gamma-LXR-ABCA1 pathway in macrophages is involved in cholesterol efflux and atherogenesis. Mol. Cell 7 (2001) 161-171
124. Chinetti G., Lestavel S., Bocher V., Remaley A.T., Neve B., Torra I.P., Teissier E., Minnich A., Jaye M., Duverger N., Brewer H.B., Fruchart J.C., Clavey V., and Staels B. PPAR-alpha and PPAR-gamma activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat. Med. 7 (2001) 53-58
125. Villarreal-Molina M.T., Aguilar-Salinas C.A., Rodriguez-Cruz M., Riano D., Villalobos-Comparan M., Coral-Vazquez R., Menjivar M., Yescas-Gomez P., Konigsoerg-Fainstein M., Romero-Hidalgo S., Tusie-Luna M.T., and Canizales-Quinteros S. The ATP-binding cassette transporter A1 R230C variant affects HDL cholesterol levels and BMI in the Mexican population: association with obesity and obesity-related comorbidities. Diabetes 56 (2007) 1881-1887
126. Villarreal-Molina M.T., Flores-Dorantes M.T., Arellano-Campos O., Villalobos-Comparan M., Rodriguez-Cruz M., Miliar-Garcia A., Huertas-Vazquez A., Menjivar M., Romero-Hidalgo S., Wacher N.H., Tusie-Luna M.T., Cruz M., Aguilar-Salinas C.A., and Canizales-Quinteros S. Association of the ATP-binding cassette transporter A1 R230C variant with early-onset type 2 diabetes in a Mexican population. Diabetes 57 (2008) 509-513
127. Harris S.B., Gittelsohn J., Hanley A., Barnie A., Wolever T.M., Gao J., Logan A., and Zinman B. The prevalence of NIDDM and associated risk factors in native Canadians. Diabetes Care 20 (1997) 185-187
128. Salinas C.A., Cruz-Bautista I., Mehta R., Villarreal-Molina M.T., Perez F.J., Tusie-Luna M.T., and Canizales-Quinteros S. The ATP-binding cassette transporter subfamily A member 1 (ABC-A1) and type 2 diabetes: an association beyond HDL cholesterol. Curr. Diabetes Rev. 3 (2007) 264-267
129. Bierman E.L. George Lyman Duff Memorial Lecture. Atherogenesis in diabetes. Arterioscler. Thromb. 12 (1992) 647-656
130. Kannel W.B., and McGee D.L. Diabetes and cardiovascular risk factors: the Framingham study. Circulation 59 (1979) 8-13
131. Nathan D.M., Lachin J., Cleary P., Orchard T., Brillon D.J., Backlund J.Y., O'Leary D.H., and Genuth S. Intensive diabetes therapy and carotid intima-media thickness in type 1 diabetes mellitus. N. Engl. J. Med. 348 (2003) 2294-2303
132. Ruderman N.B., Williamson J.R., and Brownlee M. Glucose and diabetic vascular disease. FASEB J. 6 (1992) 2905-2914
133. Ginsberg H.N. Lipoprotein physiology in nondiabetic and diabetic states. Relationship to atherogenesis. Diabetes Care 14 (1991) 839-855
134. Hayden J.M., and Reaven P.D. Cardiovascular disease in diabetes mellitus type 2: a potential role for novel cardiovascular risk factors. Curr. Opin. Lipidol. 11 (2000) 519-528
135. Zimmet P., Magliano D., Matsuzawa Y., Alberti G., and Shaw J. The metabolic syndrome: a global public health problem and a new definition. J. Atheroscler. Thromb. 12 (2005) 295-300
136. Haffner S.M. Risk constellations in patients with the metabolic syndrome: epidemiology, diagnosis, and treatment patterns. Am. J. Med. 119 (2006) S3-S9
137. Jenkins A.J., Lyons T.J., Zheng D., Otvos J.D., Lackland D.T., McGee D., Garvey W.T., and Klein R.L. Serum lipoproteins in the diabetes control and complications trial/epidemiology of diabetes intervention and complications cohort: associations with gender and glycemia. Diabetes Care 26 (2003) 810-818
138. Reaven G.M., Hollenbeck C., Jeng C.Y., Wu M.S., and Chen Y.D. Measurement of plasma glucose, free fatty acid, lactate, and insulin for 24 h in patients with NIDDM. Diabetes 37 (1988) 1020-1024
139. Seigneur M., Freyburger G., Gin H., Claverie M., Lardeau D., Lacape G., Le Moigne F., Crockett R., and Boisseau M.R. Serum fatty acid profiles in type I and type II diabetes: metabolic alterations of fatty acids of the main serum lipids. Diabetes Res. Clin. Pract. 23 (1994) 169-177
140. Baynes J.W., and Thorpe S.R. Glycoxidation and lipoxidation in atherogenesis. Free Radic. Biol. Med. 28 (2000) 1708-1716
141. Brownlee M., Cerami A., and Vlassara H. Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N. Engl. J. Med. 318 (1988) 1315-1321
142. Thornalley P.J., Langborg A., and Minhas H.S. Formation of glyoxal, methylglyoxal and 3-deoxyglucosone in the glycation of proteins by glucose. Biochem. J. 344 Pt 1 (1999) 109-116
143. Passarelli M., and Oram J.F. Cellular glycoxidation impairs the ABCA1-mediated lipid secretory pathway. Circulation 102 (2000) II-312
144. Passarelli M., Tang C., McDonald T.O., O'Brien K.D., Gerrity R.G., Heinecke J.W., and Oram J.F. Advanced glycation end product precursors impair ABCA1-dependent cholesterol removal from cells. Diabetes 54 (2005) 2198-2205
145. Tang C., McMillen T., Kanter J.E., Bornfeldt K.E., LeBoeuf R.C., and Oram J.F. Expression of ABCA1 is selectively impaired in macrophages and kidneys in diabetic mice. Arterioscler. Thromb. Vasc. Biol. 25 (2005) e93
146. Laffitte B.A., Repa J.J., Joseph S.B., Wilpitz D.C., Kast H.R., Mangelsdorf D.J., and Tontonoz P. LXRs control lipid-inducible expression of the apolipoprotein E gene in macrophages and adipocytes. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 507-512
147. Huang Z.H., Lin C.Y., Oram J.F., and Mazzone T. Sterol efflux mediated by endogenous macrophage ApoE expression is independent of ABCA1. Arterioscler. Thromb. Vasc. Biol. 21 (2001) 2019-2025
148. Repa J.J., Berge K.E., Pomajzl C., Richardson J.A., Hobbs H., and Mangelsdorf D.J. Regulation of ATP-binding cassette sterol transporters ABCG5 and ABCG8 by the liver X receptors alpha and beta. J. Biol. Chem. 277 (2002) 18793-18800
149. Yu L., Gupta S., Xu F., Liverman A.D., Moschetta A., Mangelsdorf D.J., Repa J.J., Hobbs H.H., and Cohen J.C. Expression of ABCG5 and ABCG8 is required for regulation of biliary cholesterol secretion. J. Biol. Chem. 280 (2005) 8742-8747
150. Tontonoz P., and Mangelsdorf D.J. Liver x receptor signaling pathways in cardiovascular disease. Mol. Endocrinol. 17 (2003) 985-993
151. Joseph S.B., McKilligin E., Pei L., Watson M.A., Collins A.R., Laffitte B.A., Chen M., Noh G., Goodman J., Hagger G.N., Tran J., Tippin T.K., Wang X., Lusis A.J., Hsueh W.A., Law R.E., Collins J.L., Willson T.M., and Tontonoz P. Synthetic LXR ligand inhibits the development of atherosclerosis in mice. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 7604-7609
152. Miao B., Zondlo S., Gibbs S., Cromley D., Hosagrahara V.P., Kirchgessner T.G., Billheimer J., and Mukherjee R. Raising HDL cholesterol without inducing hepatic steatosis and hypertriglyceridemia by a selective LXR modulator. J. Lipid Res. 45 (2004) 1410-1417
153. Repa J.J., Liang G., Ou J., Bashmakov Y., Lobaccaro J.M., Shimomura I., Shan B., Brown M.S., Goldstein J.L., and Mangelsdorf D.J. Regulation of mouse sterol regulatory element-binding protein-1c gene (SREBP-1c) by oxysterol receptors, LXRalpha and LXRbeta. Genes Dev. 14 (2000) 2819-2830
154. Schultz J.R., Tu H., Luk A., Repa J.J., Medina J.C., Li L., Schwendner S., Wang S., Thoolen M., Mangelsdorf D.J., Lustig K.D., and Shan B. Role of LXRs in control of lipogenesis. Genes Dev. 14 (2000) 2831-2838
155. Osborne T.F. Sterol regulatory element-binding proteins (SREBPs): key regulators of nutritional homeostasis and insulin action. J. Biol. Chem. 275 (2000) 32379-32382
156. Claudel T., Leibowitz M.D., Fievet C., Tailleux A., Wagner B., Repa J.J., Torpier G., Lobaccaro J.M., Paterniti J.R., Mangelsdorf D.J., Heyman R.A., and Auwerx J. Reduction of atherosclerosis in apolipoprotein E knockout mice by activation of the retinoid X receptor. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 2610-2615
157. Costet P., Lalanne F., Gerbod-Giannone M.C., Molina J.R., Fu X., Lund E.G., Gudas L.J., and Tall A.R. Retinoic acid receptor-mediated induction of ABCA1 in macrophages. Mol. Cell. Biol. 23 (2003) 7756-7766
158. Peterson S.J., Drummond G., Kim D.H., Li M., Kruger A.L., Ikehara S., and Abraham N.G. L-4F treatment reduces adiposity, increases adiponectin levels, and improves insulin sensitivity in obese mice. J. Lipid Res. 49 (2008) 1658-1669
159. Navab M., Anantharamaiah G.M., Reddy S.T., Hama S., Hough G., Grijalva V.R., Yu N., Ansell B.J., Datta G., Garber D.W., and Fogelman A.M. Apolipoprotein A-I mimetic peptides. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1325-1331
160. Navab M., Anantharamaiah G.M., Hama S., Garber D.W., Chaddha M., Hough G., Lallone R., and Fogelman A.M. Oral administration of an Apo A-I mimetic peptide synthesized from D-amino acids dramatically reduces atherosclerosis in mice independent of plasma cholesterol. Circulation 105 (2002) 290-292
161. Navab M., Anantharamaiah G.M., Reddy S.T., Van Lenten B.J., Datta G., Garber D., and Fogelman A.M. Human apolipoprotein A-I and A-I mimetic peptides: potential for atherosclerosis reversal. Curr. Opin. Lipidol. 15 (2004) 645-649
162. Gupta H., Dai L., Datta G., Garber D.W., Grenett H., Li Y., Mishra V., Palgunachari M.N., Handattu S., Gianturco S.H., Bradley W.A., Anantharamaiah G.M., and White C.R. Inhibition of lipopolysaccharide-induced inflammatory responses by an apolipoprotein AI mimetic peptide. Circ. Res. 97 (2005) 236-243
163. Ou J., Wang J., Xu H., Ou Z., Sorci-Thomas M.G., Jones D.W., Signorino P., Densmore J.C., Kaul S., Oldham K.T., and Pritchard Jr. K.A. Effects of D-4F on vasodilation and vessel wall thickness in hypercholesterolemic LDL receptor-null and LDL receptor/apolipoprotein A-I double-knockout mice on Western diet. Circ. Res. 97 (2005) 1190-1197
164. Shao B., Oda M.N., Oram J.F., and Heinecke J.W. Myeloperoxidase: an inflammatory enzyme for generating dysfunctional high density lipoprotein. Curr. Opin. Cardiol. 21 (2006) 322-328
165. Zheng L., Nukuna B., Brennan M.L., Sun M., Goormastic M., Settle M., Schmitt D., Fu X., Thomson L., Fox P.L., Ischiropoulos H., Smith J.D., Kinter M., and Hazen S.L. Apolipoprotein A-I is a selective target for myeloperoxidase-catalyzed oxidation and functional impairment in subjects with cardiovascular disease. J. Clin. Invest. 114 (2004) 529-541
166. Sethi A.A., Stonik J.A., Thomas F., Demosky S.J., Amar M., Neufeld E., Brewer H.B., Davidson W.S., D'Souza W., Sviridov D., and Remaley A.T. Asymmetry in the lipid affinity of bihelical amphipathic peptides. A structural determinant for the specificity of ABCA1-dependent cholesterol efflux by peptides. J. Biol. Chem. 283 (2008) 32273-32282