The interaction of ApoA-I and ABCA1 triggers signal transduction pathways to mediate efflux of cellular lipids

Molecular Medicine

Volumn 18, Issue 2, 2012, Pages 149-158

  Zhao, Guo Jun ^a   Yin, Kai ^a   Fu, Yu chang ^b   Tang, Chao Ke ^a  

^a UNIVERSITY OF SOUTH CHINA   (China)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER A1; APOLIPOPROTEIN A1; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; JANUS KINASE 2; LIPID; PROTEIN KINASE C; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

CELL TRANSPORT; HUMAN; LIPID TRANSPORT; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; APOLIPOPROTEIN A-I; ATP-BINDING CASSETTE TRANSPORTERS; BIOLOGICAL TRANSPORT; HUMANS; LIPID METABOLISM; SIGNAL TRANSDUCTION;

EID: 84858201901     PISSN: 10761551     EISSN: None     Source Type: Journal    
DOI: 10.2119/molmed.2011.00183     Document Type: Review

References (114)

1. Vergeer M, Holleboom AG, Kastelein JJ, Kuivenhoven JA. (2010) The HDL hypothesis: does high-density lipoprotein protect from atherosclerosis? J. Lipid Res. 51:2058-73.
2. Yang R, et al. (2010) A genome-wide linkage scan identifies multiple quantitative trait loci for HDL-cholesterol levels in families with premature CAD and MI. J. Lipid Res. 51:1442-51.
3. Fielding CJ, Fielding PE. (1995) Molecular physiology of reverse cholesterol transport. J. Lipid Res. 36:211-28.
4. Pieters MN, Schouten D, Van Berkel TJ. (1994) In vitro and in vivo evidence for the role of HDL in reverse cholesterol transport. Biochim. Biophys. Acta. 1225:125-34.
5. Duffy D, Rader DJ. (2006) Emerging therapies targeting high-density lipoprotein metabolism and reverse cholesterol transport. Circulation. 113:1140-50.
6. Niesor EJ, et al. 2010) Modulating cholesteryl ester transfer protein activity maintains efficient pre-beta-HDL formation and increases reverse cholesterol transport. J. Lipid Res. 51:3443-54.
7. Ye D, et al. (2010) ATP-binding cassette transporters A1 and G1, HDL metabolism, cholesterol efflux, and inflammation: important targets for the treatment of atherosclerosis. Curr. Drug Targets. 12:647-60.
8. Yancey PG, et al. (2003) Importance of different pathways of cellular cholesterol efflux. Arterioscler. Thromb. Vasc. Biol. 23:712-9.
9. Oram JF. (2003) HDL apolipoproteins and ABCA1: partners in the removal of excess cellular cholesterol. Arterioscler. Thromb. Vasc. Biol. 23:720-7.
10. Wang N, Tall AR. (2003) Regulation and mechanisms of ATP-binding cassette transporter A1-mediated cellular cholesterol efflux. Arterioscler. Thromb. Vasc. Biol. 23:1178-84.
11. Remaley AT, et al. (2001) Apolipoprotein specificity for lipid efflux by the human ABCAI transporter. Biochem. Biophys. Res. Commun. 280:818-23.
12. Yin K, Liao DF, Tang CK. (2010) ATP-binding membrane cassette transporter A1 (ABCA1): a possible link between inflammation and reverse cholesterol transport. Mol. Med. 16:438-49.
13. Navab M, Reddy ST, Van Lenten BJ, Fogelman AM. (2011) HDL and cardiovascular disease: atherogenic and atheroprotective mechanisms. Nat. Rev. Cardiol. 8:222-32.
14. Nandedkar SD, et al. (2011) D-4F, an apoA-1 mimetic, decreases airway hyperresponsiveness, inflammation, and oxidative stress in a murine model of asthma. J. Lipid Res. 52:499-508.
15. Fitzgerald ML, et al. (2004) ABCA1 and amphipathic apolipoproteins form high-affinity molecular complexes required for cholesterol efflux. J. Lipid Res. 45:287-94.
16. Oram JF, Wolfbauer G, Vaughan AM, Tang C, Albers JJ. (2003) Phospholipid transfer protein interacts with and stabilizes ATP-binding cassette transporter A1 and enhances cholesterol efflux from cells. J. Biol. Chem. 278:52379-85.
17. Wang N, Silver DL, Costet P, Tall AR. (2000) Specific binding of ApoA-I, enhanced cholesterol efflux, and altered plasma membrane morphology in cells expressing ABC1. J. Biol. Chem. 275:33053-8.
18. Chambenoit O, et al. (2001) Specific docking of apolipoprotein A-I at the cell surface requires a functional ABCA1 transporter. J. Biol. Chem. 276:9955-60.
19. Smith JD, Waelde C, Horwitz A, Zheng P. (2002) Evaluation of the role of phosphatidylserine translocase activity in ABCA1-mediated lipid efflux. J. Biol. Chem. 277:17797-803.
20. Wang N, Silver DL, Thiele C, Tall AR. (2001) ATP-binding cassette transporter A1 (ABCA1) functions as a cholesterol efflux regulatory protein. J. Biol. Chem. 276:23742-7.
21. Chroni A, Liu T, Fitzgerald ML, Freeman MW, Zannis VI. (2004) Cross-linking and lipid efflux properties of apoA-I mutants suggest direct association between apoA-I helices and ABCA1. Biochemistry. 43:2126-39.
22. Hassan HH, et al. (2007) 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: 2428-42.
23. Vedhachalam C, et al. (2007) ABCA1-induced cell surface binding sites for ApoA-I. Arterioscler. Thromb. Vasc. Biol. 27:1603-9.
24. Okuhira K, et al. (2010) Binding of PDZ-RhoGEF to ATP-binding cassette transporter A1 (ABCA1) induces cholesterol efflux through RhoA activatranstion and prevention of transporter degradation. J. Biol. Chem. 285:16369-77.
25. Vaughan AM, Tang C, Oram JF. (2009) ABCA1 mutants reveal an interdependency between lipid export function, apoA-I binding activity, and Janus kinase 2 activation. J. Lipid Res. 50:285-92.
26. Denis M, Landry YD, Zha X. (2008) ATP-binding cassette A1-mediated lipidation of apolipoprotein A-I occurs at the plasma membrane and not in the endocytic compartments. J. Biol. Chem. 283:16178-86.
27. Neufeld EB, et al. (2001) Cellular localization and trafficking of the human ABCA1 transporter. J. Biol. Chem. 276:27584-90.
28. Takahashi Y, Smith JD. (1999) Cholesterol efflux to apolipoprotein AI involves endocytosis and resecretion in a calcium-dependent pathway. Proc. Natl. Acad. Sci. U. S. A. 96:11358-63.
29. Heeren J, Weber W, Beisiegel U. (1999) Intracellular processing of endocytosed triglyceride-rich lipoproteins comprises both recycling and degradation. J. Cell Sci. 112 (Pt 3): 349-59.
30. Neufeld EB, et al. (2004) The ABCA1 transporter modulates late endocytic trafficking: insights from the correction of the genetic defect in Tangier disease. J. Biol. i. 279:15571-8.
31. Lorenzi I, von Eckardstein A, Cavelier C, Radosavljevic S, Rohrer L. (2008) Apolipoprotein A-I but not high-density lipoproteins are internalised by RAW macrophages: roles of ATPbinding cassette transporter A1 and scavenger receptor BI. J Mol. Med. 86:171-83.
32. Hassan HH, et al. (2008) Quantitative analysis of ABCA1-dependent compartmentalization and trafficking of apolipoprotein A-I: implications for determining cellular kinetics of nascent high density lipoprotein biogenesis. J. Biol. Chem. 283:11164-75.
33. Singaraja RR, et al. (2009) Palmitoylation of ATPbinding cassette transporter A1 is essential for its trafficking and function. Circ. Res. 105:138-47.
34. Faulkner LE, et al. (2008) An analysis of the role of a retroendocytosis pathway in ABCA1-mediated cholesterol efflux from macrophages. J. Lipid Res. 49:1322-32.
35. Tang CK, et al. (2004) Effect of apolipoprotein A-I on ATP binding cassette transporter A1 degradation and cholesterol efflux in THP-1 macrophagederived foam cells. Acta. Biochim. Biophys. Sin. Shanghai. 36:218-26.
36. Wang N, et al. (2003) A PEST sequence in ABCA1 regulates degradation by calpain protease and stabilization of ABCA1 by apoA-I. J. Clin. Invest. 111:99-107.
37. Martinez LO, Agerholm-Larsen B, Wang N, Chen W, Tall AR. (2003) Phosphorylation of a pest sequence in ABCA1 promotes calpain degradation and is reversed by ApoA-I. J. Biol. Chem. 278: 37368-74.
38. Kasza I, et al. (2009) Model system for the analysis of cell surface expression of human ABCA1. BMC Cell Biol. 10:93.
39. Imajoh S, Kawasaki H, Suzuki K. (1986) The amino-terminal hydrophobic region of the small subunit of calcium-activated neutral protease (CANP) is essential for its activation by phosphatidylinositol. J. Biochem. 99:1281-4.
40. Arakawa R, Yokoyama S. (2002) Helical apo-lipoproteins stabilize ATP-binding cassette transporter A1 by protecting it from thiol protease-mediated degradation. J. Biol. Chem. 277:22426-9.
41. Lu R, Arakawa R, Ito-Osumi C, Iwamoto N, Yokoyama S. (2008) ApoA-I facilitates ABCA1 recycle/accumulation to cell surface by inhibiting its intracellular degradation and increases HDL generation. Arterioscler. Thromb. Vasc. Biol. 28: 1820-4.
42. Francis GA, Knopp RH, Oram JF. (1995) Defective removal of cellular cholesterol and phospholipids by apolipoprotein A-I in Tangier Disease. J. Clin. Invest. 96:78-87.
43. Delgado-Lista J, et al. (2010) ABCA1 gene variants regulate postprandial lipid metabolism in healthy men. Arterioscler. Thromb. Vasc. Biol. 30:1051-7.
44. Mulya A, et al. (2008) Initial interaction of apoA-I with ABCA1 impacts in vivo metabolic fate of nascent HDL. J. Lipid Res. 49:2390-401.
45. Cavelier C, Rohrer L, von Eckardstein A. (2006) ATP-Binding cassette transporter A1 modulates apolipoprotein A-I transcytosis through aortic endothelial cells. Circ. Res. 99:1060-6.
46. Abe-Dohmae S, et al. (2000) Characterization of apolipoprotein-mediated HDL generation induced by cAMP in a murine macrophage cell line. Biochemistry. 39:11092-9.
47. Oram JF, Lawn RM, Garvin MR, Wade DP. (2000) ABCA1 is the cAMP-inducible apolipoprotein receptor that mediates cholesterol secretion from macrophages. J. Biol. Chem. 275:34508-11.
48. Bortnick AE, et al. (2000) The correlation of ATPbinding cassette 1 mRNA levels with cholesterol efflux from various cell lines. J. Biol. Chem. 275: 28634-40.
49. Haidar B, Denis M, Marcil M, Krimbou L, Genest J Jr. (2004) Apolipoprotein A-I activates cellular cAMP signaling through the ABCA1 transporter. J. Biol. Chem. 279:9963-9.
50. Haidar B, Denis M, Krimbou L, Marcil M, Genest J Jr. (2002) cAMP induces ABCA1 phosphorylation activity and promotes cholesterol efflux from fibroblasts. J. Lipid Res. 43:2087-94.
51. See RH, et al. (2002) Protein kinase A site-specific phosphorylation regulates ATP-binding cassette A1 (ABCA1)-mediated phospholipid efflux. J. Biol. Chem. 277:41835-42.
52. Yang J, et al. (2007) Effect of apolipoproteinA-I on expression and function of ATP-binding cassette transporter A1 through PKA signaling. Prog. Biochem. Biophys. 34:611-9.
53. Yamauchi Y, Hayashi M, Abe-Dohmae S, Yokoyama S. (2003) Apolipoprotein A-I activates protein kinase C alpha signaling to phosphorylate and stabilize ATP binding cassette tranporter A1 for the high density lipoprotein assembly. J. Biol. Chem. 278:47890-7.
54. Delvecchio CJ, Capone JP. (2008) Protein kinase C alpha modulates liver X receptor alpha transactivation. J. Endocrinol. 197:121-30.
55. Tang C, Vaughan AM, Oram JF. (2004) Janus kinase 2 modulates the apolipoprotein interactions with ABCA1 required for removing cellular cholesterol. J. Biol. Chem. 279:7622-8.
56. Tang C, Vaughan AM, Anantharamaiah GM, Oram JF. (2006) Janus kinase 2 modulates the lipid-removing but not protein-stabilizing interactions of amphipathic helices with ABCA1. J. Lipid Res. 47:107-14.
57. Tang C, Liu Y, Kessler PS, Vaughan AM, Oram JF. (2009) The macrophage cholesterol exporter ABCA1 functions as an anti-inflammatory receptor. J. Biol. Chem. 284:32336-43.
58. Nofer JR, et al. (2006) Apolipoprotein A-I activates Cdc42 signaling through the ABCA1 transporter. J. Lipid Res. 47:794-803.
59. Nofer JR, et al. (2003) Involvement of Cdc42 signaling in apoA-I-induced cholesterol efflux. J. Biol. Chem. 278:53055-62.
60. Tsukamoto K, et al. (2002) Retarded intracellular lipid transport associated with reduced expression of Cdc42, a member of Rho-GTPases, in human aged skin fibroblasts: a possible function of Cdc42 in mediating intracellular lipid transport. Arterioscler. Thromb. Vasc. Biol. 22:1899-904.
61. Iwamoto N, Lu R, Tanaka N, Abe-Dohmae S, Yokoyama S. (2010) Calmodulin interacts with ATP binding cassette transporter A1 to protect from calpain-mediated degradation and upregulates high-density lipoprotein generation. Arterioscler. Thromb. Vasc. Biol. 30:1446-52.
62. Karwatsky J, Ma L, Dong F, Zha X. (2010) Cholesterol efflux to apoA-I in ABCA1-expressing cells is regulated by Ca2+-dependent calcineurin signaling. J. Lipid Res. 51:1144-56.
63. Jeon KI, et al. (2010) Ca2+/calmodulin-stimulated PDE1 regulates the beta-catenin/TCF signaling through PP2A B56 gamma subunit in proliferating vascular smooth muscle cells. FEBS J. 277:5026-39.
64. Hu YW, et al. (2009) Eicosapentaenoic acid reduces ABCA1 serine phosphorylation and impairs ABCA1-dependent cholesterol efflux through cyclic AMP/protein kinase A signaling pathway in THP-1 macrophage-derived foam cells. Atherosclerosis. 204:e35-43.
65. Ma L, et al. (2011) Ht31, a protein kinase A anchoring inhibitor, induces robust cholesterol efflux and reverses macrophage foam cell formation through ATP-binding cassette transporter A1. J. Biol. Chem. 286:3370-8.
66. Yamauchi Y, et al. (2004) Intracellular cholesterol mobilization involved in the ABCA1/apolipoprotein-mediated assembly of high density lipoprotein in fibroblasts. J. Lipid Res. 45:1943-51.
67. Thymiakou E, Zannis VI, Kardassis D. (2007) Physical and functional interactions between liver X receptor/retinoid X receptor and Sp1 modulate the transcriptional induction of the human ATP binding cassette transporter A1 gene by oxysterols and retinoids. Biochemistry. 46:11473-83.
68. Chen X, et al. (2011) Transcriptional regulation of ATP-binding cassette transporter A1 expression by a novel signaling pathway. J. Biol. Chem. 286:8917-23.
69. Williams LM, et al. (2007) Expression of constitutively active STAT3 can replicate the cytokinesuppressive activity of interleukin-10 in human primary macrophages. J. Biol. Chem. 282:6965-75.
70. Murray PJ. (2006) Understanding and exploiting the endogenous interleukin-10/STAT3-mediated anti-inflammatory response. Curr. Opin. Pharmacol. 6:379-86.
71. Hao XR, et al. (2009) IFN-gamma down-regulates ABCA1 expression by inhibiting LXRalpha in a JAK/STAT signaling pathway-dependent manner. Atherosclerosis. 203:417-28.
72. Wool GD, et al. (2011)4F Peptide reduces nascent atherosclerosis and induces natural antibody production in apolipoprotein E-null mice. Faseb J. 25:290-300.
73. Yin K, et al. (2011) Tristetraprolin-dependent posttranscriptional regulation of inflammatory cytokines mRNA expression by apolipoprotein A-I: role of ATP-binding membrane cassette transporter A1 and signal transducer and activator of transcription 3. J. Biol. Chem. 286:13834-45.
74. Matsunaga T, et al. (1991) Apolipoprotein A-I deficiency due to a codon 84 nonsense mutation of the apolipoprotein A-I gene. Proc. Natl. Acad. Sci. U. S. A. 88:2793-7.
75. Takai Y, Sasaki T, Matozaki T. (2001) Small GTPbinding proteins. Physiol. Rev. 81:153-208.
76. Hirano K, et al. (2000) Decreased expression of a member of the Rho GTPase family, Cdc42Hs, in cells from Tangier disease-the small G protein may play a role in cholesterol efflux. FEBS Lett. 484:275-9.
77. Tsukamoto K, et al. (2001) ATP-binding cassette transporter-1 induces rearrangement of actin cytoskeletons possibly through Cdc42/N-WASP. Biochem. Biophys. Res. Commun. 287:757-65.
78. Utech M, et al. (2001) Accumulation of RhoA, RhoB, RhoG, and Rac1 in fibroblasts from Tangier disease subjects suggests a regulatory role of Rho family proteins in cholesterol efflux. Biochem. Biophys. Res. Commun. 280:229-36.
79. Li J, et al. (2010) Exendin-4 regulates pancreatic ABCA1 transcription via CaMKK/CaMKIV pathway. J. Cell Mol. Med. 14:1083-7.
80. Mulay V, Wood P, Rentero C, Enrich C, Grewal T. (2011) Signal transduction pathways provide opportunities to enhance HDL and apoAIdependent reverse cholesterol transport. Curr. Pharm. Biotechnol. 2011, Apr 6 [Epub ahead of print].
81. Nakaya K, et al. (2010) Cilostazol enhances macrophage reverse cholesterol transport in vitro and in vivo. Atherosclerosis. 213:135-41.
82. Tall AR. (2008) Cholesterol efflux pathways and other potential mechanisms involved in the athero-protective effect of high density lipoproteins. J. Intern. Med. 263:256-73.
83. Nagao K, et al. (2007) Enhanced apoA-Idependent cholesterol efflux by ABCA1 from sphingomyelin-deficient Chinese hamster ovary cells. J. Biol. Chem. 282:14868-74.
84. Rosenberg MF, Callaghan R, Ford RC, Higgins CF. (1997) Structure of the multidrug resistance P-glycoprotein to 2.5 nm resolution determined by electron microscopy and image analysis. J. Biol. Chem. 272:10685-94.
85. Ward A, Reyes CL, Yu J, Roth CB, Chang G. (2007) Flexibility in the ABC transporter MsbA: Alternating access with a twist. Proc. Natl. Acad. Sci. U. S. A. 104:19005-10.
86. Dawson RJ, Locher KP. (2006) Structure of a bacterial multidrug ABC transporter. Nature. 443: 180-5.
87. Vedhachalam C, et al. (2004) Influence of ApoA-I structure on the ABCA1-mediated efflux of cellular lipids. J. Biol. Chem. 279:49931-9.
88. Lapicka-Bodzioch K, et al. (2001) Homogeneous assay based on 52 primer sets to scan for mutations of the ABCA1 gene and its application in genetic analysis of a new patient with familial high-density lipoprotein deficiency syndrome. Biochim. Biophys. Acta. 1537:42-8.
89. Vaughan AM, Oram JF. (2003) ABCA1 redistributes membrane cholesterol independent of apo-lipoprotein interactions. J. Lipid Res. 44:1373-80.
90. Lin G, Oram JF. (2000) Apolipoprotein binding to protruding membrane domains during removal of excess cellular cholesterol. Atherosclerosis. 149: 359-70.
91. Vedhachalam C, et al. (2007) Mechanism of ATPbinding cassette transporter A1-mediated cellular lipid efflux to apolipoprotein A-I and formation of high density lipoprotein particles. J. Biol. Chem. 282:25123-30.
92. Vedhachalam C, et al. (2010) Influence of apo-lipoprotein (Apo) A-I structure on nascent high density lipoprotein HDL) particle size distribution. J. Biol. Chem. 285:31965-73.
93. Santamarina-Fojo S, Remaley AT, Neufeld EB, Brewer HB Jr. (2001) Regulation and intracellular trafficking of the ABCA1 transporter. J. Lipid Res. 42:1339-45.
94. Forte TM, Bielicki JK, Knoff L, McCall MR. (1996) Structural relationships between nascent apoA-Icontaining particles that are extracellularly assembled in cell culture. J. Lipid Res. 37:1076-85.
95. Bielicki JK, McCall MR, Forte TM. (1999) Apolipoprotein A-I promotes cholesterol release and apolipoprotein E recruitment from THP-1 macrophage-like foam cells. J. Lipid Res. 40:85-92.
96. Liu L, et al. (2003) 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. 278:42976-84.
97. Fielding PE, Nagao K, Hakamata H, Chimini G, Fielding CJ. (2000) A two-step mechanism for free cholesterol and phospholipid efflux from human vascular cells to apolipoprotein A-1. Biochemistry. 39:14113-20.
98. Sun Y, et al. (2003) Stearoyl-CoA desaturase inhibits ATP-binding cassette transporter A1-mediated cholesterol efflux and modulates membrane domain structure. J Biol. Chem. 278:5813-20.
99. Tsai JY, et al. (2010) EGb761 ameliorates the formation of foam cells by regulating the expression of SR-A and ABCA1: role of haem oxygenase-1. Cardiovasc. Res. 88:415-23.
100. Arakawa R, et al. (2009) Pharmacological inhibition of ABCA1 degradation increases HDL biogenesis and exhibits antiatherogenesis. J. Lipid Res. 50:2299-305.
101. Wu CA, Tsujita M, Hayashi M, Yokoyama S. (2004) Probucol inactivates ABCA1 in the plasma membrane with respect to its mediation of apolipoprotein binding and high density lipoprotein assembly and to its proteolytic degradation. J. Biol. Chem. 279:30168-74.
102. Le Goff W, et al. (2004) Cyclosporin A traps ABCA1 at the plasma membrane and inhibits ABCA1-mediated lipid efflux to apolipoprotein A-I. Arterioscler. Thromb. Vasc. Biol. 24:2155-61.
103. Feng B, Tabas I. (2002) ABCA1-mediated cholesterol efflux is defective in free cholesterolloaded macrophages. Mechanism involves enhanced ABCA1 degradation in a process requiring full NPC1 activity. J. Biol. Chem. 277:43271-80.
104. Passarelli M, et al. (2005) Advanced glycation end product precursors impair ABCA1-dependent cholesterol removal from cells. Diabetes. 54:2198-205.
105. Fitzgerald ML, et al. (2002) Naturally occurring mutations in the largest extracellular loops of ABCA1 can disrupt its direct interaction with apolipoprotein A-I. J. Biol. Chem. 277:33178-87.
106. Tanaka AR, et al. (2003) Effects of mutations of ABCA1 in the first extracellular domain on subcellular trafficking and ATP binding/hydro-lysis. J. Biol. Chem. 278:8815-9.
107. Clee SM, et al. (2000) Age and residual cholesterol efflux affect HDL cholesterol levels and coronary artery disease in ABCA1 heterozygotes. J. Clin. Invest. 106:1263-70.
108. Fitzgerald ML, et al. (2004) ATP-binding cassette transporter A1 contains a novel C-terminal VFVNFA motif that is required for its cholesterol efflux and ApoA-I binding activities. J. Biol. Chem. 279:48477-85.
109. Chroni A, et al. (2003) The central helices of ApoA-I can promote ATP-binding cassette transporter A1 (ABCA1)-mediated lipid efflux. Amino acid residues 220-231 of the wild-type ApoA-I are required for lipid efflux in vitro and high density lipoprotein formation in vivo. J. Biol. Chem. 278:6719-30.
110. Panagotopulos SE, et al. (2002) The role of apolipoprotein A-I helix 10 in apolipoproteinmediated cholesterol efflux via the ATP-binding cassette transporter ABCA1. J. Biol. Chem. 277:39477-84.
111. Chiesa G, et al. (2002) Recombinant apolipoprotein A-I(Milano) infusion into rabbit carotid artery rapidly removes lipid from fatty streaks. Circ. Res. 90:974-80.
112. Shah PK, et al. (2001) High-dose recombinant apolipoprotein A-I(Milano) mobilizes tissue cholesterol and rapidly reduces plaque lipid and macrophage content in apolipoprotein E-deficient mice. Potential implications for acute plaque stabilization. Circulation. 103:3047-50.
113. Nissen SE, et al. (2003) Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes: a randomized controlled trial. JAMA. 290:2292-300.
114. Alexander ET, et al. (2009) Macrophage reverse cholesterol transport in mice expressing ApoA-I Milano. Arterioscler. Thromb. Vasc. Biol. 29:1496-501.