Crystal Structure of Δ(185-243)ApoA-I Suggests a Mechanistic Framework for the Protein Adaptation to the Changing Lipid Load in Good Cholesterol: From Flatland to Sphereland via Double Belt, Belt Buckle, Double Hairpin and Trefoil/Tetrafoil

Journal of Molecular Biology

Volumn 425, Issue 1, 2013, Pages 1-16

  Gursky, Olga ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

amphipathic helical repeats; cardiovascular disease; protein conformations on various HDLs; reverse cholesterol transport; structural models

Indexed keywords

APOLIPOPROTEIN A1; HIGH DENSITY LIPOPROTEIN;

CHOLESTEROL TRANSPORT; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ELECTRON SPIN RESONANCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; LIPID MEMBRANE; MASS SPECTROMETRY; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN METABOLISM; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW;

EID: 84871799222     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.09.027     Document Type: Review

References (69)

1. G.H. Rothblat, and M.C. Phillips High-density lipoprotein heterogeneity and function in reverse cholesterol transport Curr. Opin. Lipidol. 21 2010 229 238
2. B.F. Asztalos, M. Tani, and E.J. Schaefer Metabolic and functional relevance of HDL subspecies Curr. Opin. Lipidol. 22 2011 176 185
3. D. Duffy, and D.J. Rader Update on strategies to increase HDL quantity and function Nat. Rev. Cardiol. 6 2009 455 463
4. L. Yvan-Charvet, N. Wang, and A.R. Tall Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses Arterioscler. Thromb. Vasc. Biol. 30 2010 139 143
5. X. Gao, and S. Yuan High density lipoproteins-based therapies for cardiovascular disease J. Cardiovasc. Dis. Res. 1 2010 99 103
6. B.F. Voight, G.M. Peloso, M. Orho-Melander, R. Frikke-Schmidt, M. Barbalic, and M.K. Jensen Plasma HDL cholesterol and risk of myocardial infarction: a Mendelian randomisation study Lancet 380 2012 572 580
7. C.J. Fielding, and P.E. Fielding Molecular physiology of reverse cholesterol transport J. Lipid Res. 36 1995 211 228
8. S. Lund-Katz, and M.C. Phillips High density lipoprotein structure-function and role in reverse cholesterol transport Subcell. Biochem. 51 2010 183 227
9. R.S. Rosenson, H.B. Brewer Jr.; W.S. Davidson, Z.A. Fayad, V. Fuster, and J. Goldstein Cholesterol efflux and atheroprotection: advancing the concept of reverse cholesterol transport Circulation 125 2012 1905 1919
10. S.M. Gordon, S. Hofmann, D.S. Askew, and W.S. Davidson High density lipoprotein: it's not just about lipid transport anymore Trends Endocrinol. Metab. 22 2010 9 15
11. 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
12. R.T. Nolte, and D. Atkinson Conformational analysis of apolipoprotein A-I and E-3 based on primary sequence and circular dichroism Biophys. J. 63 1992 1221 1239
13. A. Mulya, J.Y. Lee, A.K. Gebre, E.Y. Boudyguina, S.K. Chung, and T.L. Smith Initial interaction of apoA-I with ABCA1 impacts in vivo metabolic fate of nascent HDL J. Lipid Res. 49 2008 2390 2401
14. P.J. Barter Hugh Sinclair lecture: the regulation and remodelling of HDL by plasma factors Atheroscler. Suppl. 3 2002 39 47
15. T. Liu, M. Krieger, H.Y. Kan, and V.I. Zannis The effects of mutations in helices 4 and 6 of ApoA-I on scavenger receptor class B type I (SR-BI)-mediated cholesterol efflux suggest that formation of a productive complex between reconstituted high density lipoprotein and SR-BI is required for efficient lipid transport J. Biol. Chem. 277 2002 21576 21584
16. 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
17. S. Tian, and A. Jonas Structural and functional properties of apolipoprotein A-I mutants containing disulfide-linked cysteines at positions 124 or 232 Biochim. Biophys. Acta 1599 2002 56 64
18. L. Li, J. Chen, V.K. Mishra, J.A. Kurtz, D. Cao, and A.E. Klon Double belt structure of discoidal high density lipoproteins: molecular basis for size heterogeneity J. Mol. Biol. 343 2004 1293 1311
19. H. Saito, S. Lund-Katz, and M.C. Phillips Contributions of domain structure and lipid interaction to the functionality of exchangeable human apolipoproteins Prog. Lipid Res. 43 2004 350 380
20. J.N. Maiorano, R.J. Jandacek, E.M. Horace, and W.S. Davidson Identification and structural ramifications of a hinge domain in apolipoprotein A-I discoidal high-density lipoproteins of different size Biochemistry 43 2004 11717 11726
21. S. Bhat, M.G. Sorci-Thomas, E.T. Alexander, M.P. Samuel, and M.J. Thomas Intermolecular contact between globular N-terminal fold and C-terminal domain of ApoA-I stabilizes its lipid-bound conformation: studies employing chemical cross-linking and mass spectrometry J. Biol. Chem. 280 2005 33015 33025
22. D.D. Martin, M.S. Budamagunta, R.O. Ryan, J.C. Voss, and M.N. Oda Apolipoprotein A-I assumes a "looped belt" conformation on reconstituted high density lipoprotein J. Biol. Chem. 281 2006 20418 20426
23. S. Bhat, M.G. Sorci-Thomas, R. Tuladhar, M.P. Samuel, and M.J. Thomas Conformational adaptation of apolipoprotein A-I to discretely sized phospholipid complexes Biochemistry 46 2007 7811 7821
24. M. Kono, Y. Okumura, M. Tanaka, D. Nguyen, P. Dhanasekaran, and S. Lund-Katz Conformational flexibility of the N-terminal domain of apolipoprotein A-I bound to spherical lipid particles Biochemistry 47 2008 11340 11347
25. R.A. Silva, R. Huang, J. Morris, J. Fang, E.O. Gracheva, and G. Ren Structure of apolipoprotein A-I in spherical high density lipoproteins of different sizes Proc. Natl Acad. Sci. USA 105 2008 12176 12181
26. P.S. Chetty, L. Mayne, S. Lund-Katz, D. Stranz, S.W. Englander, and M.C. Phillips Helical structure and stability in human apolipoprotein A-I by hydrogen exchange and mass spectrometry Proc. Natl Acad. Sci. USA 106 2009 19005 19010
27. M. Koyama, M. Tanaka, P. Dhanasekaran, S. Lund-Katz, M.C. Phillips, and H. Saito Interaction between the N- and C-terminal domains modulates the stability and lipid binding of apolipoprotein A-I Biochemistry 48 2009 2529 2537
28. B. Chen, X. Ren, T. Neville, W.G. Jerome, D.W. Hoyt, and D. Sparks Apolipoprotein AI tertiary structures determine stability and phospholipid-binding activity of discoidal high-density lipoprotein particles of different sizes Protein Sci. 18 2009 921 935
29. F. Gu, M.K. Jones, J. Chen, J.C. Patterson, A. Catte, and W.G. Jerome Structures of discoidal high density lipoproteins: a combined computational-experimental approach J. Biol. Chem. 285 2010 4652 4665
30. J.O. Lagerstedt, G. Cavigiolio, M.S. Budamagunta, I. Pagani, J.C. Voss, and M.N. Oda Structure of apolipoprotein A-I's N-terminus on nascent high density lipoprotein J. Biol. Chem. 286 2011 2966 2975
31. C. Vedhachalam, P.S. Chetty, M. Nickel, P. Dhanasekaran, S. Lund-Katz, G.H. Rothblat, and M.C. Phillips Influence of apolipoprotein (Apo) A-I structure on nascent high density lipoprotein (HDL) particle size distribution J. Biol. Chem. 285 2010 31965 31973
32. M. Tanaka, P. Dhanasekaran, D. Nguyen, M. Nickel, Y. Takechi, and S. Lund-Katz Influence of N-terminal helix bundle stability on the lipid-binding properties of human apolipoprotein A-I Biochim. Biophys. Acta 1811 2011 25 30
33. D. Bashtovyy, M.K. Jones, G.M. Anantharamaiah, and J.P. Segrest Analyses of sequence conservation of apolipoprotein A-I afford novel insights into HDL structure-function J. Lipid Res. 52 2011 435 450
34. P. Sevugan Chetty, L. Mayne, Z.Y. Kan, S. Lund-Katz, S.W. Englander, and M.C. Phillips Apolipoprotein A-I helical structure and stability in discoidal high-density lipoprotein (HDL) particles by hydrogen exchange and mass spectrometry Proc. Natl Acad. Sci. USA 109 2012 11687 11692
35. 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
36. D.P. Rogers, L.M. Roberts, J. Lebowitz, G. Datta, G.M. Anantharamaiah, J.A. Engler, and C.G. Brouillette The lipid-free structure of apolipoprotein A-I: effects of amino-terminal deletions Biochemistry 37 1998 11714 11725
37. 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
38. 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 J. Biol. Chem. 277 2002 39093 39101
39. M.G. Sorci-Thomas, J.S. Owen, B. Fulp, S. Bhat, X. Zhu, and J.S. Parks Nascent high density lipoproteins formed by ABCA1 resemble lipid rafts and are structurally organized by three apoA-I monomers J. Lipid Res. 53 2012 1890 1909
40. 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
41. 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
42. C.G. Brouillette, G.M. Anantharamaiah, J.A. Engler, and D.W. Borhani Structural models of human apolipoprotein A-I: a critical analysis and review Biochim. Biophys. Acta 1531 2001 4 46
43. X. Mei, and D. Atkinson Crystal structure of C-terminal truncated apolipoprotein A-I reveals the assembly of HDL by dimerization J. Biol. Chem. 286 2011 38570 38582
44. S. Jayaraman, G. Cavigiolio, and O. Gursky Folded functional lipid-poor apolipoprotein A-I obtained by heating of high-density lipoproteins: relevance to HDL biogenesis Biochem. J. 442 2012 703 712
45. Segrest, J. P.; Jones, M. K.; Catte, A. & Thirumuruganandham, S. P. (2012). Validation of previous computer models and MD simulations of discoidal HDL by a recent crystal structure of apoA-I. J. Lipid Res. (In press).
46. O. Gursky, X. Mei, and D. Atkinson The crystal structure of the C-terminal truncated apolipoprotein A-I sheds new light on the amyloid formation by the N-terminal segment Biochemistry 51 2012 10 18
47. W.S. Davidson, and T.B. Thompson The structure of apolipoprotein A-I in high density lipoproteins J. Biol. Chem. 282 2007 22249 22253
48. M.J. Thomas, S. Bhat, and M.G. Sorci-Thomas Three-dimensional models of HDL apoA-I: implications for its assembly and function J. Lipid Res. 49 2008 1875 1883
49. M.G. Sorci-Thomas, S. Bhat, and M.J. Thomas Activation of lecithin:cholesterol acyltransferase by HDL apoA-I central helices Clin. Lipidol. 4 2009 113 124
50. M.K. Jones, A. Catte, L. Li, and J.P. Segrest Dynamics of activation of lecithin:cholesterol acyltransferase by apolipoprotein A-I Biochemistry 48 2009 11196 11210
51. R. Huang, R.A.G.D. Silva, W.G. Jerome, A. Kontush, M.J. Chapman, and L.K. Curtiss Apolipoprotein A-I structural organization in high-density lipoproteins isolated from human plasma Nat. Struct. Mol. Biol. 18 2011 416 422
52. A. Catte, J.C. Patterson, D. Bashtovyy, M.K. Jones, F. Gu, and L. Li Structure of spheroidal HDL particles revealed by combined atomistic and coarse-grained simulations Biophys. J. 94 2008 2306 2319
53. M.K. Jones, L. Zhang, A. Catte, L. Li, M.N. Oda, G. Ren, and J.P. Segrest Assessment of the validity of the double superhelix model for reconstituted high density lipoproteins: a combined computational-experimental approach J. Biol. Chem. 285 2010 41161 41171
54. 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
55. M. Guha, X. Gao, S. Jayaraman, and O. Gursky Correlation of structural stability with functional remodeling of high-density lipoproteins: the importance of being disordered Biochemistry 47 2008 11393 11397
56. I. Visiers, B.B. Braunheim, and H. Weinstein Prokink: a protocol for numerical evaluation of helix distortions by proline Protein Eng. 13 2000 603 606
57. M. Tanaka, P. Dhanasekaran, D. Nguyen, S. Ohta, S. Lund-Katz, M.C. Phillips, and H. Saito Contributions of the N- and C-terminal helical segments to the lipid-free structure and lipid interaction of apolipoprotein A-I Biochemistry 45 2006 10351 10358
58. H.L. Zhu, and D. Atkinson Conformation and lipid binding of a C-terminal (198-243) peptide of human apolipoprotein A-I Biochemistry 46 2007 1624 1634
59. O. Gursky, and D. Atkinson Thermal unfolding of human high-density apolipoprotein A-1: implications for a lipid-free molten globular state Proc. Natl Acad. Sci. USA 93 1996 2991 2995
60. M.K. Jones, F. Gu, A. Catte, L. Li, and J.P. Segrest "Sticky" and "promiscuous", the yin and yang of apolipoprotein A-I termini in discoidal high-density lipoproteins: a combined computational-experimental approach Biochemistry 50 2011 2249 2263
61. X. Gao, S. Yuan, S. Jayaraman, and O. Gursky Differential stability of high-density lipoprotein subclasses: effects of particle size and protein composition J. Mol. Biol. 387 2009 628 638
62. X. Gao, S. Yuan, S. Jayaraman, and O. Gursky Effect of apolipoprotein A-II on the structure and stability of human high-density lipoprotein: implications for the role of apoA-II in HDL metabolism Biochemistry 51 2012 4633 4641
63. D.J. Reijngoud, and M.C. Phillips Mechanism of dissociation of human apolipoprotein A-I from complexes with dimyristoylphosphatidylcholine as studied by guanidine hydrochloride denaturation Biochemistry 21 1982 2969 2976
64. S. Jayaraman, D.L. Gantz, and O. Gursky Effects of salt on the thermal stability of human plasma high-density lipoprotein Biochemistry 45 2006 4620 4628
65. K. Gauthamadasa, C. Rosales, H.J. Pownall, S. Macha, W.G. Jerome, R. Huang, and R.A. Silva Speciated human high-density lipoprotein protein proximity profiles Biochemistry 49 2010 10656 10665
66. B. Lu, J.A. Morrow, and K.H. Weisgraber Conformational reorganization of the four-helix bundle of human apolipoprotein E in binding to phospholipid J. Biol. Chem. 275 2000 20775 20781
67. G. Cavigiolio, B. Shao, E.G. Geier, G. Ren, J.W. Heinecke, and M.N. Oda The interplay between size, morphology, stability, and functionality of high-density lipoprotein subclasses Biochemistry 47 2008 4770 4779
68. A.N. Hoofnagle, and J.W. Heinecke Lipoproteomics: using mass spectrometry-based proteomics to explore the assembly, structure, and function of lipoproteins J. Lipid Res. 50 2009 1967 1975
69. W.S. Davidson, R.A. Silva, S. Chantepie, W.R. Lagor, M.J. Chapman, and A. Kontush Proteomic analysis of defined HDL subpopulations reveals particle-specific protein clusters: relevance to antioxidative function Arterioscler. Thromb. Vasc. Biol. 29 2009 870 876