Double belt structure of discoidal high density lipoproteins: Molecular basis for size heterogeneity

Journal of Molecular Biology

Volumn 343, Issue 5, 2004, Pages 1293-1311

  Li, Ling ^a,b   Chen, Jianguo ^a,b   Mishra, Vinod K ^a,b   Kurtz, Jennifer A ^a,b   Cao, Dongfeng ^a,b   Klon, Anthony E ^b   Harvey, Stephen C ^b   Anantharamaiah, G M ^a,b   Segrest, Jere P ^a,b  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

apolipoprotein A I; discoidal high density lipoprotein; double belt model; hairpin belt model; size heterogeneity

Indexed keywords

APOLIPOPROTEIN A1; HIGH DENSITY LIPOPROTEIN; MONOMER; PHOSPHORYLCHOLINE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; TANDEM REPEAT;

EID: 6344248642     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.09.017     Document Type: Article

References (62)

1. P.W. Wilson, R.D. Abbott, and W.P. Castelli High density lipoprotein cholesterol and mortality. The Framingham heart study Arteriosclerosis 8 1988 737 741
2. J.P. Segrest, and G.M. Anantharamaiah Pathogenesis of atherosclerosis Curr. Opin. Cardiol. 9 1994 404 410
3. C.H. Sloop, L. Dory, B.R. Krause, C. Castle, and P.S. Roheim Lipoproteins and apolipoproteins in peripheral lymph of normal and cholesterol-fed dogs Atherosclerosis 49 1983 9 21
4. A. Brooks-Wilson, M. Marcil, S.M. Clee, L.H. Zhang, K. Roomp, and M. van Dam Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency Nature Genet. 22 1999 336 345
5. M. Bodzioch, E. Orso, J. Klucken, T. Langmann, A. Bottcher, and W. Diederich The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease Nature Genet. 22 1999 347 351
6. S. Rust, M. Rosier, H. Funke, J. Real, Z. Amoura, and J.C. Piette Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1 Nature Genet. 22 1999 352 355
7. A.T. Remaley, S. Rust, M. Rosier, C. Knapper, L. Naudin, and C. Broccardo Human ATP-binding cassette transporter 1 (ABC1): genomic organization and identification of the genetic defect in the original Tangier disease kindred Proc. Natl Acad. Sci. USA 96 1999 12685 12690
8. R.M. Lawn, D.P. Wade, M.R. Garvin, X. Wang, K. Schwartz, and J.G. Porter The Tangier disease gene product ABC1 controls the cellular apolipoprotein- mediated lipid removal pathway [see comments] J. Clin. Invest. 104 1999 R25 R31
9. G.A. Francis, R.H. Knopp, and J.F. Oram Defective removal of cellular cholesterol and phospholipids by apolipoprotein A-I in Tangier disease J. Clin. Invest. 96 1995 78 87
10. J.P. Segrest, D.W. Garber, C.G. Brouillette, S.C. Harvey, and G.M. Anantharamaiah The amphipathic alpha helix: a multifunctional structural motif in plasma apolipoproteins Adv. Protein Chem. 45 1994 303 369
11. J.P. Segrest, R.L. Jackson, J.D. Morrisett, and A.M. Gotto Jr A molecular theory of lipid-protein interactions in the plasma lipoproteins FEBS Letters 38 1974 247 258
12. J.P. Segrest, M.K. Jones, H. De Loof, C.G. Brouillette, Y.V. Venkatachalapathi, and G.M. Anantharamaiah The amphipathic helix in the exchangeable apolipoproteins: a review of secondary structure and function J. Lipid Res. 33 1992 141 166
13. A. Wlodawer, J.P. Segrest, B.H. Chung, R. Chiovetti Jr, and J.N. Weinstein High-density lipoprotein recombinants: evidence for a bicycle tire micelle structure obtained by neutron scattering and electron microscopy FEBS Letters 104 1979 231 235
14. D. Atkinson, D.M. Small, and G.G. Shipley X-ray and neutron scattering studies of plasma lipoproteins Ann. N Y Acad. Sci. 348 1980 284 298
15. J.P. Segrest Amphipathic helixes and plasma lipoproteins: thermodynamic and geometric considerations Chem. Phys. Lipids 18 1977 7 22
16. D.P. Rogers, C.G. Brouillette, J.A. Engler, S.W. Tendian, L. Roberts, and V.K. Mishra Truncation of the amino terminus of human apolipoprotein A-I substantially alters only the lipid-free conformation Biochemistry 36 1997 288 300
17. M.A. Tricerri, A.K. Behling Agree, S.A. Sanchez, J. Bronski, and A. Jonas Arrangement of apolipoprotein A-I in reconstituted high-density lipoprotein disks: an alternative model based on fluorescence resonance energy transfer experiments Biochemistry 40 2001 5065 5074
18. A.R. Tall, D.M. Small, R.J. Deckelbaum, and G.G. Shipley Structure and thermodynamic properties of high density lipoprotein recombinants J. Biol. Chem. 252 1977 4701 4711
19. D.W. Borhani, D.P. Rogers, J.A. Engler, and C.G. Brouillette Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation Proc. Natl Acad. Sci. USA 94 1997 12291 12296
20. J.P. Segrest, M.K. Jones, A.E. Klon, C.J. Sheldahl, M. Hellinger, H. De Loof, and S.C. Harvey A detailed molecular belt model for apolipoprotein A-I in discoidal high density lipoprotein J. Biol. Chem. 274 1999 31755 31758
21. V. Koppaka, L. Silvestro, J.A. Engler, C.G. Brouillette, and P.H. Axelsen The structure of human lipoprotein A-I. Evidence for the "belt" model J. Biol. Chem. 274 1999 14541 14544
22. J.N. Maiorano, and W.S. Davidson The orientation of helix 4 in apolipoprotein A-I-containing reconstituted high density lipoproteins J. Biol. Chem. 275 2000 17374 17380
23. S.E. Panagotopulos, E.M. Horace, J.N. Maiorano, and W.S. Davidson Apolipoprotein A-I adopts a belt-like orientation in reconstituted high density lipoproteins J. Biol. Chem. 276 2001 42965 42970
24. H. Li, D.S. Lyles, M.J. Thomas, W. Pan, and M.G. Sorci-Thomas Structural determination of lipid-bound ApoA-I using fluorescence resonance energy transfer J. Biol. Chem. 275 2000 37048 37054
25. H.H. Li, D.S. Lyles, W. Pan, E. Alexander, M.J. Thomas, and M.G. Sorci-Thomas ApoA-I structure on discs and spheres. Variable helix registry and conformational states J. Biol. Chem. 277 2002 39093 39101
26. W.S. Davidson, and G.M. Hilliard The spatial organization of apolipoprotein A-I on the edge of discoidal high density lipoprotein particles: a mass specrometry study J. Biol. Chem. 278 2003 27199 27207
27. M.N. Oda, T.M. Forte, R.O. Ryan, and J.C. Voss The C-terminal domain of apolipoprotein A-I contains a lipid-sensitive conformational trigger Nature Struct. Biol. 10 2003 455 460
28. C.G. Brouillette, J.L. Jones, T.C. Ng, H. Kercret, B.H. Chung, and J.P. Segrest Structural studies of apolipoprotein A-I/phosphatidylcholine recombinants by high-field proton NMR, nondenaturing gradient gel electrophoresis, and electron microscopy Biochemistry 23 1984 359 367
29. L. Calabresi, G. Tedeschi, C. Treu, S. Ronchi, D. Galbiati, and S. Airoldi Limited proteolysis of a disulfide-linked apoA-I dimer in reconstituted HDL J. Lipid Res. 42 2001 935 942
30. L.M. Roberts, M.J. Ray, T.W. Shih, E. Hayden, M.M. Reader, and C.G. Brouillette Structural analysis of apolipoprotein A-I: limited proteolysis of methionine-reduced and -oxidized lipid-free and lipid-bound human apo A-I Biochemistry 36 1997 7615 7624
31. J. Bergeron, P.G. Frank, D. Scales, Q.H. Meng, G. Castro, and Y.L. Marcel Apolipoprotein A-I conformation in reconstituted discoidal lipoproteins varying in phospholipid and cholesterol content J. Biol. Chem. 270 1995 27429 27438
32. L. Calabresi, G. Vecchio, F. Frigerio, L. Vavassori, C.R. Sirtori, and G. Franceschini Reconstituted high-density lipoproteins with a disulfide-linked apolipoprotein A-I dimer: evidence for restricted particle size heterogeneity Biochemistry 36 1997 12428 12433
33. M. Okon, P.G. Frank, Y.L. Marcel, and R.J. Cushley Heteronuclear NMR studies of human serum apolipoprotein A-I. Part I. Secondary structure in lipid-mimetic solution FEBS Letters 517 2002 139 143
34. B. Corsico, J.D. Toledo, and H.A. Garda 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. 276 2001 16978 16985
35. M.N. Palgunachari, V.K. Mishra, S. Lund-Katz, M.C. Phillips, S.O. Adeyeye, and S. Alluri 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. 16 1996 328 338
36. V.K. Mishra, M.N. Palgunachari, G. Datta, M.C. Phillips, S. Lund-Katz, and S.O. Adeyeye Studies of synthetic peptides of human apolipoprotein A-I containing tandem amphipathic alpha-helixes Biochemistry 37 1998 10313 10324
37. M. Sorci-Thomas, M.W. Kearns, and J.P. Lee Apolipoprotein A-I domains involved in lecithin-cholesterol acyltransferase activation. Structure:function relationships J. Biol. Chem. 268 1993 21403 21409
38. M. Laccotripe, S.C. Makrides, A. Jonas, and V.I. Zannis The carboxyl-terminal hydrophobic residues of apolipoprotein A-I affect its rate of phospholipid binding and its association with high density lipoprotein [published erratum appears in J. Biol. Chem. 1998 Jun 19;273(25):15878] J. Biol. Chem. 272 1997 17511 17522
39. J.W. Burgess, P.G. Frank, V. Franklin, P. Liang, D.C. McManus, and M. Desforges Deletion of the C-terminal domain of apolipoprotein A-I impairs cell surface binding and lipid efflux in macrophage Biochemistry 38 1999 14524 14533
40. A.E. Klon, J.P. Segrest, and S.C. Harvey Molecular dynamics simulations on discoidal HDL particles suggest a mechanism for rotation in the apo A-I belt model J. Mol. Biol. 324 2002 703 721
41. T. Blundell, D. Barlow, N. Borkakoti, and J. Thornton Solvent-induced distortions and the curvature of alpha-helices Nature 306 1983 281 283
42. L. Pauling, and R.B. Corey Atomic coordinates and structure factors for two helical configurations of polypeptide chains Proc. Natl Acad. Sci. USA 37 1951 235 240
43. R. Bussell Jr, and D. Eliezer A structural and functional role for 11-mer repeats in alpha-synuclein and other exchangeable lipid binding proteins J. Mol. Biol. 329 2003 763 778
44. C.C. Jao, A. Der-Sarkissian, J. Chen, and R. Langen From the cover: Structure of membrane-bound {alpha}-synuclein studied by site-directed spin labeling Proc. Natl Acad. Sci. USA 101 2004 8331 8336
45. Y.L. Marcel, P.R. Provost, H. Koa, E. Raffai, N.V. Dac, J.C. Fruchart, and E. Rassart The epitopes of apolipoprotein A-I define distinct structural domains including a mobile middle region J. Biol. Chem. 266 1991 3644 3653
46. L. Calabresi, Q.H. Meng, G.R. Castro, and Y.L. Marcel Apolipoprotein A-I conformation in discoidal particles: evidence for alternate structures Biochemistry 32 1993 6477 6484
47. L.K. Curtiss, D.J. Bonnet, and K.A. Rye The conformation of apolipoprotein A-I in high-density lipoproteins is influenced by core lipid composition and particle size: a surface plasmon resonance study Biochemistry 39 2000 5712 5721
48. P.B. Moore, C.F. Lopez, and M.L. Klein Dynamical properties of a hydrated lipid bilayer from a multinanosecond molecular dynamics simulation Biophys. J. 81 2001 2484 2494
49. H.I. Petrache, S. Tristram-Nagle, and J.F. Nagle Fluid phase structure of EPC and DMPC bilayers Chem. Phys. Lipids 95 1998 83 94
50. R. Mehta, D.L. Gantz, and O. Gursky Human plasma high-density lipoproteins are stabilized by kinetic factors J. Mol. Biol. 328 2003 183 192
51. H. Saito, P. Dhanasekaran, D. Nguyen, E. Deridder, P. Holvoet, S. Lund-Katz, and M.C. Phillips {alpha}-Helix formation is required for high affinity binding of human apolipoprotein A-I to lipids J. Biol. Chem. 279 2004 20974 20981
52. A.E. Klon, M.K. Jones, J.P. Segrest, and S.C. Harvey Molecular belt models for the apolipoprotein A-I Paris and Milano mutations Biophys. J. 79 2000 1679 1685
53. G.M. Anantharamaiah, Y.V. Venkatachalapathi, C.G. Brouillette, and J.P. Segrest Use of synthetic peptide analogues to localize lecithin:cholesterol acyltransferase activating domain in apolipoprotein A-I Arteriosclerosis 10 1990 95 105
54. B.R. Scott, D.C. McManus, V. Franklin, A.G. McKenzie, T. Neville, D.L. Sparks, and Y.L. Marcel The N-terminal globular domain and the first class A amphipathic helix of apolipoprotein A-I are important for lecithin:cholesterol acyltransferase activation and the maturation of high density lipoprotein in vivo J. Biol. Chem. 276 2001 48716 48724
55. A. Chroni, T. Liu, I. Gorshkova, H.Y. Kan, Y. Uehara, A. Von Eckardstein, and V.I. Zannis 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 2003 6719 6730
56. J.P. Segrest, M.K. Jones, V.K. Mishra, G.M. Anantharamaiah, and D.W. Garber apoB-100 has a pentapartite structure composed of three amphipathic alpha-helical domains alternating with two amphipathic beta-strand domains. Detection by the computer program LOCATE Arterioscler. Thromb. 14 1994 1674 1685
57. J.B. Hazelrig, M.K. Jones, and J.P. Segrest A mathematically defined motif for the radial distribution of charged residues on apolipoprotein amphipathic alpha helixes Biophys. J. 64 1993 1827 1832
58. A. Jonas Reconstitution of high-density lipoproteins Methods Enzymol. 128 1986 553 582
59. M.A. Markwell, S.M. Haas, L.L. Bieber, and N.E. Tolbert A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples Anal. Biochem. 87 1978 206 210
60. J.D. Morrisett, J.T. Sparrow, H.F. Hoff, and A.M. Gotto Jr Methods for studying lipid-protein interactions Cardiovasc. Res. Cent. Bull. 12 1973 39 51
61. V.K. Mishra, and M.N. Palgunachari Interaction of model class A1, class A2, and class Y amphipathic helical peptides with membranes Biochemistry 35 1996 11210 11220
62. R.A. Sayle, and E.J. Milner-White RASMOL: biomolecular graphics for all Trends Biochem. Sci. 20 1995 374