Structure-function relationships of apolipoprotein A-I: A flexible protein with dynamic lipid associations

Current Opinion in Lipidology

Volumn 14, Issue 2, 2003, Pages 151-157

  Marcel, Yves L ^a   Kiss, Robert S ^a  

^a UNIVERSITY OF OTTAWA HEART INSTITUTE   (Canada)

Author keywords

ABCA1; Apolipoprotein A I; HDL; Molecular models; Reverse cholesterol transport

Indexed keywords

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

BINDING SITE; CARBOXY TERMINAL SEQUENCE; CHOLESTEROL TRANSPORT; HUMAN; HYDROPHOBICITY; LIPID METABOLISM; LIPOPROTEIN METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; STRUCTURE ACTIVITY RELATION;

APOLIPOPROTEIN A-I; HUMANS; LIPID METABOLISM; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 0037398373     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/00041433-200304000-00006     Document Type: Review

References (75)

1. Frank PG, Marcel YL. Apolipoprotein A-I: structure-function relationships. J Lipid Res 2000; 41:853-872.
2. Segrest JP, Li L, Anantharamaiah GM, et al. Structure and function of apolipoprotein A-I and high-density lipoprotein. Curr Opin Lipidol 2000; 11:105-115.
3. Klon AE, Segrest JP, Harvey SC. Comparative models for human apolipoprotein A-I bound to lipid in discoidal high-density lipoprotein particles. Biochemistry 2002; 41:10895-10905.
4. Brouillette CG, Anantharamaiah GM, Engler JA, Borhani DW. Structural models of human apolipoprotein A-I: a critical analysis and review. Biochim Biophys Acta Mol Cell Biol Lipids 2001; 1531:4-46. This is a comprehensive review of the structure of apoA-I in the lipid-free and lipid-bound forms.
5. Rogers DP, Brouillette CG, Engler JA, et al. Truncation of the amino terminus of human apolipoprotein A-I substantially alters only the lipid-free conformation. Biochemistry 1997; 36:288-300.
6. Rogers DP, Roberts LM, Lebowitz J, et al. Structural analysis of apolipoprotein A-I: Effects of amino- and carboxy-terminal deletions on the lipid-free structure. Biochemistry 1998; 37:945-955.
7. Davidson WS, Arnvig-McGuire K, Kennedy A, et al. Structural organization of the N-terminal domain of apolipoprotein A-I: Studies of tryptophan mutants. Biochemistry 1999; 38:14387-14395.
8. Kiss RS, Kay CM, Ryan RO. Amphipathic alpha-helix bundle organization of lipid-free chicken apolipoprotein A-I. Biochemistry 1999; 38:4327-4334.
9. Borhani DW, Rogers DP, Engler JA, Brouillette CG. Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation. Proc Natl Acad Sci U S A 1997; 94:12291-12296.
10. Okon M, Frank PG, Marcel YL, Cushley RJ. Secondary structure of human apolipoprotein A-I(1-186) in lipid-mimetic solution. FEBS Lett 2001; 487:390-396. A nuclear magnetic resonance structure of apoA-I in lipid mimetic solvent confirmed the structure of apoA-I described in the Borhani paper, and describes the secondary structure of the N-terminus.
11. Okon M, Frank PG, Marcel YL, Cushley RJ. Heteronuclear NMR studies of human serum apolipoprotein A-I, Part I. Secondary structure in lipid-mimetic solution. FEBS Lett. 2002; 517:139-143.
12. Maiorano JN, Davidson WS. The orientation of helix 4 in apolipoprotein A-I-containing reconstituted high density lipoproteins. J Biol Chem 2000; 275:17374-17380.
13. Panagotopulos SE, Horace EM, Maiorano JN, Davidson WS. Apolipoprotein A-I adopts a belt-like orientation in reconstituted high density lipoproteins. J Biol Chem 2001; 276:42965-42970. This was a follow-up study to Ref. [12], which defined the orientation of the remaining helices.
14. Li H, Lyles DS, Thomas MJ, et al. Structural determination of lipid-bound ApoA-I using fluorescence resonance energy transfer. J Biol Chem 2000; 275:37048-37054.
15. Tricerri MA, Agree AKB, Sanchez SA, et al. Arrangement of apolipoprotein A-I in reconstituted high-density lipoprotein disks: An alternative model based on fluorescence resonance energy transfer experiments. Biochemistry 2001; 40:5065-5074. The use of FRET defined the intermolecular conformations of apoA-I.
16. Li HH, Lyles DS, Pan W, et al. ApoA-I structure on discs and spheres. Variable helix registry and conformational states. Structural determination of lipid-bound ApoA-I using fluorescence resonance energy transfer. J Biol Chem 2002; 277:39093-39101. This paper introduced the concept of variable registry for the pairing of apoA-I helices in discoidal lipoproteins.
17. Tricerri MA, Sanchez SA, Arnulphi C, et al. Interaction of apolipoprotein A-I in three different conformations with palmitoyl oleoyl phosphatidylcholine vesicles. J Lipid Res 2002; 43:187-197.
18. Segrest JP, Jones MK, Klon AE, et al. A detailed molecular belt model for apolipoprotein A-I in discoidal high density lipoprotein. J Biol Chem 1999; 274:31755-31758.
19. Li HH, Thomas MJ, Pan W, et al. Preparation and incorporation of probe-labeled apoA-I for fluorescence resonance energy transfer studies of rHDL. J Lipid Res 2001; 42:2084-2091.
20. Sparks DL, Lund-Katz S, Phillips MC. The charge and structural stability of apolipoprotein A-I in discoidal and spherical recombinant High Density Lipoproteins particles. J Biol Chem 1992; 267:25839-25847.
21. Palgunachari MN, Mishra VK, Lund-Katz S, et al. Only the two end helixes of eight tandem amphipathic helical domains of human apo A-I have significant lipid affinity: Implications for HDL assembly. Arterioscler Thromb Vasc Biol 1996; 16:328-338.
22. Scott BR, McManus DC, Franklin V, et al. The N-terminal globular domain and the first class A amphipathic helix of apolipoprotein A-I important for lecithin: cholesterol acyltransferase activation and the maturation of high density lipoprotein in vivo. J Biol Chem 2001; 276:48716-48724. This complete study combined in-vitro characterization and in-vivo physiological relevance to define the role of the N-terminus in apoA-I.
23. Reardon CA, Kan HY, Cabana V, et al. In vivo studies of HDL assembly and metabolism using adenovirus-mediated transfer of apoA-I mutants in apoA-I-deficient mice. Biochemistry 2001; 40:13670-13680. In vivo studies of C-terminal mutations of apoA-I defined the role of different regions of the C-terminus.
24. McManus DC, Scott BR, Frank PG, et al. Distinct central amphipathic α-helices in apolipoprotein A-I contribute to the in vivo maturation of high density lipoprotein by either activating lecithin-cholesterol acyltransferase or binding lipids. J Biol Chem 2000; 275:5043-5051.
25. Sorci-Thomas MG, Thomas M, Curtiss L, Landrum M. Single repeat deletion in ApoA-I blocks cholesterol esterification and results in rapid catabolism of delta6 and wild-type ApoA-I in transgenic mice. J Biol Chem 2000; 275:12156-12163.
26. Cho KH, Durbin DM, Jonas A. Role of individual amino acids of apolipoprotein A-I in the activation of lecithin:cholesterol acyltransferase and in HDL rearrangements. J Lipid Res 2001; 42:379-389.
27. Roosbeek S, Vanloo B, Duverger N, et al. Three arginine residues in apolipoprotein A-I are critical for activation of lecithin:cholesterol acyltransferase. J Lipid Res 2001; 42:31-40.
28. Corsico B, Toledo JD, Garda HA. Evidence for a central apolipoprotein A-I domain loosely bound to lipids in discoidal lipoproteins that is capable of penetrating the bilayer of phospholipid vesicles. J Biol Chem 2001; 276:16978-16985. This study provided novel evidence for a hinge domain in apoA-I with intermediate lipid binding properties.
29. Calabresi L, Meng Q-H, Castro GR, Marcel YL. Apolipoprotein A-I conformation in discoidal particles: Evidence for alternate structures. Biochemistry 1993; 32:6477-6484.
30. Calabresi L, Tedeschi G, Treu C, et al. Limited proteolysis of a disulfide-linked apoA-I dimer in reconstituted HDL. J Lipid Res 2001; 42:935-942.
31. Brouillette CG, Anantharamaiah GM. Structural models of human apolipoprotein A-I. Biochim Biophys Acta 1995; 1256:103-129.
32. Liadaki KN, Liu T, Xu SZ, et al. Binding of high density lipoprotein (HDL) and discoidal reconstituted HDL to the HDL receptor scavenger receptor class B type I: Effect of lipid association and APOA-I mutations on receptor binding. J Biol Chem 2000; 275:21262-21271.
33. Miettinen HE, Rayburn H, Krieger M. Abnormal lipoprotein metabolism and reversible female infertility in HDL receptor (SR-BI)-deficient mice. J Clin Invest 2001; 108:1717-1722.
34. Temel RE, Parks JS, Williams DL. Enhancement of SR-BI-mediated selective cholesteryl ester uptake from ApoA-I-/- HDL by ApoA-I requires HDL reorganization by LCAT. J Biol Chem (in press).
35. Temel RE, Walzem RL, Banka CL, Williams DL. Apolipoprotein A-I is necessary for the in vivo formation of high density lipoprotein competent for scavenger receptor BI-mediated cholesteryl ester-selective uptake. J Biol Chem 2002; 277:26565-26572.
36. Li XP, Kan HY, Lavrentiadou S, et al. Reconstituted discoidal ApoE-phospholipid particles are ligands for the scavennger receptor BI - The amino-terminal 1-165 domain of ApoE suffices for receptor binding. J Biol Chem 2002; 277:21149-21157.
37. Hammad SM, Barth JL, Knaak C, Argraves WS. Megalin acts in concert with cubilin to mediate endocytosis of high density lipoproteins. J Biol Chem 2000; 275:12003-12008.
38. Hammad SM, Stefansson S, Twal WO, et al. Cubilin, the endocytic receptor for intrinsic factor-vitamin B(12) complex, mediates high-density lipoprotein holoparticle endocytosis. Proc Natl Acad Sci U S A 1999; 96:10158-10163.
39. Fidge NH. High density lipoprotein receptors, binding proteins, and ligands. J Lipid Res 1999; 40:187-201.
40. Martinez LO, Georgeaud V, Rolland C, et al. Characterization of two high-density lipoprotein binding sites on porcine hepatocyte plasma membranes: Contribution of scavenger receptor class B type I (SR-BI) to the low-affinity component. Biochemistry 2000; 39:1076-1082.
41. Moestrup SK, Kozyraki R, Cubilin, a high-density lipoprotein receptor. Curr Opin Lipidol 2000; 11:133-140.
42. Katoh H, Ping GY, Tsuda T, Hayashi S. High density lipoprotein binding protein of eel (Anguilla japonica) liver with specificity of binding to apoAI as a ligand. Comp Biochem Physiol B Biochem Mol Biol 2001; 129:843-852.
43. Bocharov AV, Vishnyakova TG, Baranova IN, et al. Characterization of a 95 kDa high affinity human high density lipoprotein-binding protein. Biochemistry 2001; 40:4407-4416.
44. Ritter M, Buechler C, Boettcher A, et al. Cloning and characterization of a novel apolipoprotein A-I binding protein, AI-BP, secreted by cells of the kidney proximal tubules in response to HDL or ApoA-I. Genomics 2002; 79:693-702.
45. Martinez LO, Jacquet S, Esteve JP, et al. Ectopic beta-chain of ATP synthase is an apolipoprotein A-I receptor in hepatic HDL endocytosis. Nature 2003; 421:75-79. This is an extremely interesting paper that identifies a novel apoA-I receptor that mediates holo-HDL endocytosis. It may have important implications for apoA-I metabolism.
46. Wang N, Silver DL, Thiele C, Tall AR. ATP-binding cassette transporter A1 (ABCA1) functions as a cholesterol efflux regulatory protein. J Biol Chem 2001; 276:23742-23747. This very good paper describes the specificity of interactions of apoA-I with ABCA1.
47. Remaley AT, Stonik JA, Demosky SJ, et al. Apolipoprotein specificity for lipid efflux by the human ABCAI transporter. Biochem Biophys Res Commun 2001; 280:818-823. This is an important paper that shows that ABCA1 binding is not limited to apoA-I, but also other exchangeable apolipoproteins.
48. Burgess JW, Frank PG, Franklin V, et al. Deletion of the C-terminal domain of apolipoprotein A-I impairs cell surface binding and lipid efflux in macrophage. Biochemistry 1999; 38:14524-14533.
49. Chroni A, Liu T, Gorshkova I, et al. The central helices of APOA-I can promote ABCA1-mediated lipid efflux: amino acid residues 220-231 of the wild-type APOA-I are required for lipid efflux in vitro and HDL formation in vivo. J Biol Chem (in press).
50. Favari E, Bernini F, Tarugi P, et al. The C-terminal domain of apolipoprotein A-I is involved in ABCA1-driven phospholipid and cholesterol efflux. Biochem Biophys Res Commun 2002; 299:801-805.
51. Panagotopulos SE, Witting SR, Horace EM, et al. The role of apolipoprotein A-I helix 10 in apolipoprotein-mediated cholesterol efflux via the ATP-binding cassette transporter ABCA1. J Biol Chem 2002; 277:39477-39484. This study correlated binding of apoA-I via its C-terminus to ABCA1 to cholesterol efflux.
52. 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.
53. Fitzgerald ML, Morris AL, Rhee JS, et al. Naturally occurring mutations in the largest extracellular loops of ABCA1 can disrupt its direct interaction with apolipoprotein A-I. J Biol Chem 2002; 277:33178-33187. After the existence of a large extracellular loop of ABCA1 was identified, this study clearly demonstrated the importance of this region in interacting with apoA-I to mediate efflux.
54. Hamon Y, Broccardo C, Chambenoit O, et al. ABC1 promotes engulfment of apoptotic cells and transbilayer redistribution of phosphatidylserine. Nat Cell Biol 2000; 2:399-406.
55. Chambenoit O, Hamon Y, Marguet D, et al. Specific docking of apolipoprotein A-I at the cell surface requires a functional ABCA1 transporter. J Biol Chem 2001; 276:9955-9960. Using mutations of ABCA1, these authors demonstrated that apoA-I binding to ABCA1 required a fully functional ABCA1.
56. Narayanaswami V, Wang J, Schieve D, et al. A molecular trigger of lipid binding-induced opening of a helix bundle exchangeable apolipoprotein. Proc Natl Acad Sci U S A 1999; 96:4366-4371.
57. Wang JJ Sykes BD, Ryan RO. Structura basis for the conformational adaptability of apolipophorin III, a helix-bundle exchangeable apolipoprotein. Proc Natl Acad Sci U S A 2002; 99:1188-1193.
58. Rigot V, Hamon Y, Chambenoit O, et al. Distinct sites on ABCA1 control distinct steps required for cellular release of phospholipids. J Lipid Res 2002; 43:2077-2086. This study emphasized the complex nature of apoA-I interactions with ABCA1, where binding and efflux require the active transporter.
59. Szakacs G, Langmann T, Ozvegy C, et al. Characterization of the ATPase cycle of human ABCA1: implications for its function as a regulator rather than an active transporter. Biochem Biophys Res Commun 2001; 288:1258-1264.
60. Wang Y, Oram JF. Unsaturated fatty acids inhibit cholesterol efflux from macrophages by increasing degradation of ATP-binding cassette transporter A1. J Biol Chem 2002; 277:5692-5697.
61. Arakawa R, Yokoyama S. Helical apolipoproteins stabilize ATP-binding cassette transporter A1 by protecting it from thiol protease-mediated degradation. J Biol Chem 2002; 277:22426-22429. Upon binding of apolipoproteins, ABCA1 is prevented from leaving the cell surface, and thereby protected from intracellular degradation.
62. Wang N, Chen W, Linsel-Nitschke P, et al. A PEST sequence in ABCA1 regulates degradation by calpain protease and stabilization of ABCA1 by apoA-I. J Clin Invest 2003; 111:99-107. This study identified a PEST internalization and degradation signal in ABCA1 that mediates calpain proteolytic degradation. This degradation can be prevented by apoA-I binding of cell surface ABCA1.
63. Burgess JW, Kiss RS, Zheng H, et al. Trypsin-sensitive and lipid-containing sites of the macrophage extracellular matrix bind apolipoprotein A-I and participate in ABCA1-dependent cholesterol efflux. J Biol Chem 2002; 277:31318-31326. This study identified and characterized a novel apoA-I binding site on the extracellular matrix of macrophages that facilitates ABCA1-mediated efflux.
64. Basso F, Freeman L, Knapper C, et al. Role of the hepatic ABCA1 transporter in modulating intrahepatic cholesterol and plasma HDL-cholesterol concentrations. J Lipid Res (in press).
65. Kiss RS, McManus DC, Franklin V, et al. The lipidation by hepatocytes of human apolipoprotein A-I occurs by both ABCA1 dependent and independent pathways. J Biol Chem (in press).
66. Fielding PE, Nagao K, Hakamata H, et al. A two-step mechanism for free cholesterol and phospholipid efflux from human vascular cells to apolipoprotein A-I. Biochemistry 2000; 39:14113-14120. This paper was the first to provide evidence for the concept of a two-step lipidation of apoA-I. First, phospholipid is transferred to apoA-I by ABCA1, then free cholesterol is transferred to the apoA-I:phospholipid complex by a less well defined pathway.
67. Liu P, Rudick M, Anderson RG. Multiple functions of caveolin-1. J Biol Chem 2002; 277:41295-41298.
68. Fielding PE, Fielding CJ. Plasma membrane caveolae mediate the efflux of cellular free cholesterol. Biochemistry 1995; 34:14288-14292.
69. Sviridov D, Fidge N, Beaumier-Gallon G, Fielding C. Apolipoprotein A-I stimulates the transport of intracellular cholesterol to cell-surface cholesterol-rich domains (caveolae). Biochem J 2001; 358:79-86.
70. Ito J, Nagayasu Y, Kato K, et al. Apolipoprotein A-I induces translocation of cholesterol, phospholipid, and caveolin-1 to cytosol in rat astrocytes. J Biol Chem 2002; 277:7929-7935.
71. Uittenbogaard A, Smart EJ. Palmitoylation of caveolin-1 is required for cholesterol binding, chaperone complex formation, and rapid transport of cholesterol to caveolae. J Biol Chem 2000; 275:25595-25599.
72. Brown DA, London E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J Biol Chem 2000; 275:17221-17224.
73. Simons K, Ikonen E. Functional rafts in cell membranes. Nature 1997; 387:569-572.
74. Gargalovic P, Dory L. Caveolins and macrophage lipid metabolism. J Lipid Res 2003; 44:11-21. This review highlights evidence that cholesterol as part of caveolae is a poor substrate for cholesterol efflux.
75. Aussenac F, Tavares M, Dufourc EJ. Cholesterol dynamics in membranes of raft composition: a molecular point of view from 2H and 31P solid-state NMR. Biochemistry (in press).