The conformation of lipid-free human apolipoprotein A-I in solution

Biochemistry

Volumn 52, Issue 52, 2013, Pages 9470-9481

  Pollard, Ricquita D ^a   Fulp, Brian ^a   Samuel, Michael P ^a   Sorci Thomas, Mary G ^a   Thomas, Michael J ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN A-I (APOA-I); ATP-BINDING CASSETTE TRANSPORTERS; BIOPHYSICAL STUDIES; CHEMICAL CROSS-LINKING; DEGREE OF CONNECTIVITY; DISULFIDE CROSS-LINKING; HIGH DENSITY LIPOPROTEIN; TANDEM MASS SPECTROMETRY;

AMINO ACIDS; CROSSLINKING; LIPOPROTEINS; MASS SPECTROMETRY;

CONFORMATIONS;

AMINO ACID; APOLIPOPROTEIN A1; LIPID; LYSINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONTROLLED STUDY; MOLECULAR MODEL; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; TANDEM MASS SPECTROMETRY;

EID: 84891510210     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401080k     Document Type: Article

References (77)

1. Oram, J. F. and Vaughan, A. M. (2000) ABCA1-mediated transport of cellular cholesterol and phospholipids to HDL apolipoproteins Curr. Opin. Lipidol. 11, 253-260
2. Wang, N., Silver, D. L., Costet, P., and Tall, A. R. (2000) Specific binding of ApoA-I, enhanced cholesterol efflux, and altered plasma membrane morphology in cells expressing ABC1 J. Biol. Chem. 275, 33053-33058
3. Yancey, P. G., Bortnick, A. E., Kellner-Weibel, G., De La Llera-Moya, M., Phillips, M. C., and Rothblat, G. H. (2003) Importance of Different Pathways of Cellular Cholesterol Efflux Arterioscler. Thromb. Vasc. Biol. 23, 712-719
4. Libby, P. (2001) Managing the risk of atherosclerosis: The role of high-density lipoprotein Am. J. Cardiol. 88, 3N-8N
5. Rader, D. J. and Tall, A. R. (2012) The not-so-simple HDL story: Is it time to revise the HDL cholesterol hypothesis? Nat. Med. 18, 1344-1346
6. Yang, Y., Hoyt, D., and Wang, J. (2007) A complete NMR spectral assignment of the lipid-free mouse apolipoprotein A-I (apoAI) C-terminal truncation mutant, apoAI(1-216) Biomol. NMR Assignments 1, 109-111
7. Borhani, D. W., Rogers, D. P., Engler, J. A., and Brouillette, C. G. (1997) Crystal structure of truncated human apolipoprotein A-I suggests a lipid-bound conformation Proc. Natl. Acad. Sci. U. S. A. 94, 12291-12296
8. Krishna Murthy, H. M. (2013) Wikipedia.
9. Silva, R. A., Hilliard, G. M., Fang, J., Macha, S., and Davidson, W. S. (2005) A three-dimensional molecular model of lipid-free apolipoprotein A-I determined by cross-linking/mass spectrometry and sequence threading Biochemistry 44, 2759-2769
10. Forte, T., Norum, K. R., Glomset, J. A., and Nichols, A. V. (1971) Plasma lipoproteins in familial lecithin: cholesterol acyltransferase deficiency: Structure of low and high density lipoproteins as revealed by elctron microscopy J. Clin. Invest. 50, 1141-1148
11. Matz, C. E. and Jonas, A. (1982) Micellar complexes of human apolipoprotein A-I with phosphatidylcholines and cholesterol prepared from cholate-lipid dispersions J. Biol. Chem. 257, 4535-4540
12. Segrest, J. P., Jackson, R. L., Morrisett, J. D., and Gotto, A. M., Jr. (1974) A molecular theory of lipid-protein interactions in the plasma lipoproteins FEBS Lett. 38, 247-258
13. Wald, J. H., Coormaghtigh, E., De Meutter, J., Ruysschaert, J. M., and Jonas, A. (1990) Investigation of the lipid domains and apolipoprotein orientation in reconstituted high density lipoproteins by fluorescence and IR methods J. Biol. Chem. 265, 20044-20050
14. Koppaka, V., Silvestro, L., Engler, J. A., Brouillette, C. G., and Axelsen, P. H. (1999) The structure of human lipoprotein A-I. Evidence for the ″belt″ model J. Biol. Chem. 274, 14541-14544
15. Segrest, J. P., Jones, M. K., Klon, A. E., Sheldahl, C. J., Hellinger, M., De Loof, H., and Harvey, S. C. (1999) A detailed molecular belt model for apolipoprotein A-I in discoidal high density lipoprotein J. Biol. Chem. 274, 31755-31758
16. Bhat, S., Sorci-Thomas, M. G., Alexander, E. T., Samuel, M. P., and Thomas, M. J. (2005) 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, 33015-33025
17. Davidson, W. S. and Hilliard, G. M. (2003) The spatial organization of apolipoprotein A-I on the edge of discoidal high density lipoprotein particles: a mass specrometry study J. Biol. Chem. 278, 27199-27207
18. Tricerri, M. A., Behling Agree, A. K., Sanchez, S. A., Bronski, J., and Jonas, A. (2001) Arrangement of apolipoprotein A-I in reconstituted high-density lipoprotein disks: An alternative model based on fluorescence resonance energy transfer experiments Biochemistry 40, 5065-5074
19. Li, H., Lyles, D. S., Thomas, M. J., Pan, W., and Sorci-Thomas, M. G. (2000) Structural determination of lipid-bound ApoA-I using fluorescence resonance energy transfer J. Biol. Chem. 275, 37048-37054
20. Bhat, S., Sorci-Thomas, M. G., Tuladhar, R., Samuel, M. P., and Thomas, M. J. (2007) Conformational adaptation of apolipoprotein A-I to discretely sized phospholipid complexes Biochemistry 46, 7811-7821
21. Thomas, M. J., Bhat, S., and Sorci-Thomas, M. G. (2008) Three-dimensional models of HDL apoA-I: Implications for its assembly and function J. Lipid Res. 49, 1875-1883
22. Sorci-Thomas, M. G., Owen, J. S., Fulp, B., Bhat, S., Zhu, X., Parks, J. S., Shah, D., Jerome, W. G., Gerelus, M., Zabalawi, M., and Thomas, M. J. (2012) Nascent high density lipoproteins formed by ABCA1 resemble lipid rafts and are structurally organized by three ApoA-I monomers J. Lipid Res. 53, 1890-1909
23. Gursky, O. (2013) Crystal structure of Delta(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 J. Mol. Biol. 425, 1-16
24. Norum, K. R., Glomset, J. A., Nichols, A. V., and Forte, T. (1971) Plasma lipoproteins in familial lecithin: Cholesterol acyltransferase deficiency: Physical and chemical studies of low and high density lipoproteins J. Clin. Invest. 50, 1131-1140
25. Mitchell, C. D., King, W. C., Applegate, K. R., Forte, T., Glomset, J. A., Norum, K. R., and Gjone, E. (1980) Characterization of apolipoprotein E-rich high density lipoproteins in familial lecithin:cholesterol acyltransferase deficiency J. Lipid Res. 21, 625-634
26. Glomset, J. A., Norum, K. R., and King, W. (1970) Plasma lipoproteins in familial lecithin: cholesterol acyltransferase deficiency: Lipid composition and reactivity in vitro J. Clin. Invest. 49, 1827-1837
27. Lowry, O. J., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent J. Biol. Chem. 19, 265-275
28. Owen, J. S., Bharadwaj, M. S., Thomas, M. J., Bhat, S., Samuel, M. P., and Sorci-Thomas, M. G. (2007) Ratio determination of plasma wild-type and L159R apoA-I using mass spectrometry: tools for studying apoA-IFin J. Lipid Res. 48, 226-234
29. Bhat, S., Zabalawi, M., Willingham, M. C., Shelness, G. S., Thomas, M. J., and Sorci-Thomas, M. G. (2004) Quality control in the apoA-I secretory pathway: deletion of apoA-I helix 6 leads to the formation of cytosolic phospholipid inclusions J. Lipid Res. 45, 1207-1220
30. Li, H. H., Thomas, M. J., Pan, W., Alexander, E., Samuel, M., and Sorci-Thomas, M. G. (2001) Preparation and incorporation of probe-labeled apoA-I for fluorescence resonance energy transfer studies of rHDL J. Lipid Res. 42, 2084-2091
31. Li, H. H., Lyles, D. S., Pan, W., Alexander, E., Thomas, M. J., and Sorci-Thomas, M. G. (2002) ApoA-I structure on discs and spheres. Variable helix registry and conformational states J. Biol. Chem. 277, 39093-39101
32. Bhat, S., Sorci-Thomas, M. G., Calabresi, L., Samuel, M. P., and Thomas, M. J. (2010) Conformation of dimeric apolipoprotein A-I milano on recombinant lipoprotein particles Biochemistry 49, 5213-5224
33. Alexander, E. T., Bhat, S., Thomas, M. J., Weinberg, R. B., Cook, V. R., Bharadwaj, M. S., and Sorci-Thomas, M. (2005) Apolipoprotein A-I helix 6 negatively charged residues attenuate lecithin-cholesterol acyltransferase (LCAT) reactivity Biochemistry 44, 5409-5419
34. Mei, X. and Atkinson, D. (2011) Crystal structure of C-terminal truncated apolipoprotein A-I reveals the assembly of high density lipoprotein (HDL) by dimerization J. Biol. Chem. 286, 38570-38582
35. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD: Visual molecular dynamics J. Mol. Graphics 14, 33-38
36. Vitello, L. B. and Scanu, A. M. (1976) Studies on human serum high density lipoproteins. Self-association of apolipoprotein A-I in aqueous solutions J. Biol. Chem. 251, 1131-1136
37. Teng, T. L., Edelstein, C., Barbeau, D. L., and Scanu, A. M. (1977) An ultracentrifugal study of the self-association of canine apolipoprotein A-I in solution J. Biol. Chem. 252, 8634-8638
38. Barbeau, D. L., Jonas, A., Teng, T., and Scanu, A. M. (1979) Asymmetry of apolipoprotein A-I in solution as assessed from ultracentrifugal, viscometric, and fluorescence polarization studies Biochemistry 18, 362-369
39. Roberts, L. M., Ray, M. J., Shih, T. W., Hayden, E., Reader, M. M., and Brouillette, C. G. (1997) Structural analysis of apolipoprotein A-I: limited proteolysis of methionine-reduced and -oxidized lipid-free and lipid-bound human apo A-I Biochemistry 36, 7615-7624
40. Rogers, D. P., Roberts, L. M., Lebowitz, J., Datta, G., Anantharamaiah, G. M., Engler, J. A., and Brouillette, C. G. (1998) The lipid-free structure of apolipoprotein A-I: effects of amino-terminal deletions Biochemistry 37, 11714-11725
41. Rogers, D. P., Roberts, L. M., Lebowitz, J., Engler, J. A., and Brouillette, C. G. (1998) Structural analysis of apolipoprotein A-I: Effects of amino- and carboxy-terminal deletions on the lipid-free structure Biochemistry 37, 945-955
42. Saito, H., Dhanasekaran, P., Nguyen, D., Holvoet, P., Lund-Katz, S., and Phillips, M. C. (2003) Domain structure and lipid interaction in human apolipoproteins A-I and E, a general model J. Biol. Chem. 278, 23227-23232
43. Rogers, D. P., Brouillette, C. G., Engler, J. A., Tendian, S. W., Roberts, L., Mishra, V. K., Anantharamaiah, G. M., Lund-Katz, S., Phillips, M. C., and Ray, M. J. (1997) Truncation of the amino terminus of human apolipoprotien A-I substantially alters only the lipid-free conformation Biochemistry 36, 288-300
44. Chetty, P. S., Mayne, L., Lund-Katz, S., Stranz, D., Englander, S. W., and Phillips, M. C. (2009) Helical structure and stability in human apolipoprotein A-I by hydrogen exchange and mass spectrometry Proc. Natl. Acad. Sci. U. S. A. 106, 19005-19010
45. Lagerstedt, J. O., Budamagunta, M. S., Liu, G. S., Devalle, N. C., Voss, J. C., and Oda, M. N. (2012) The "beta-clasp" model of apolipoprotein A-I-A lipid-free solution structure determined by electron paramagnetic resonance spectroscopy Biochim. Biophys. Acta 1821, 448-455
46. Brouillette, C. G., Dong, W.-J., Yang, Z. W., Ray, M. J., Protasevich, I. I., Cheung, H. C., and Engler, J. A. (2005) Forster resonance energy transfer measurements are consistent with a helical bundle model for lipid-free apolipoprotein A-I Biochemistry 44, 16413-16425
47. Wu, Z., Wagner, M. A., Zheng, L., Parks, J. S., Shy, J. M., 3rd, Smith, J. D., Gogonea, V., and Hazen, S. L. (2007) The refined structure of nascent HDL reveals a key functional domain for particle maturation and dysfunction Nat. Struct Mol. Biol. 14, 861-868
48. Nat. Struct Mol. Biol. 2008, 15, 2330.
49. Mayne, L., Kan, Z. Y., Chetty, P. S., Ricciuti, A., Walters, B. T., and Englander, S. W. (2011) Many overlapping peptides for protein hydrogen exchange experiments by the fragment separation-mass spectrometry method J. Am. Soc. Mass Spectrom. 22, 1898-1905
50. Fass, D. (2012) Disulfide bonding in protein biophysics Annu. Rev. Biophys 41, 63-79
51. Leroy, A. and Jonas, A. (1994) Native-like structure and self-association behavior of apolipoprotein A-I in a water/n-propanol solution Biochim. Biophys. Acta 1212, 285-294
52. Reijngoud, D. J. and Phillips, M. C. (1982) Mechanism of dissociation of human apolipoprotein A-I from complexes with dimyristoylphosphatidylcholine as studied by guanidine hydrochloride denaturation Biochemistry 21, 2969-2976
53. Saito, H., Dhanasekaran, P., Nguyen, D., Deridder, E., Holvoet, P., Lund-Katz, S., and Phillips, M. C. (2004) Alpha-helix formation is required for high affinity binding of human apolipoprotein A-I to lipids J. Biol. Chem. 279, 20974-20981
54. Chen, J., Wang, J., and Yang, Y. (2012) Monomeric mouse apoAI(1-216), In Protein Data Bank, p 2LEM, RCSB.
55. Wilson, C., Wardell, M. R., Weisgraber, K. H., Mahley, R. W., and Agard, D. A. (1991) Three-dimensional structure of the LDL receptor-binding domain of human apolipoprotein E Science 252, 1817-1822
56. Gursky, O., Mei, X., and Atkinson, D. (2012) The crystal structure of the C-terminal truncated apolipoprotein a-I sheds new light on amyloid formation by the N-terminal fragment Biochemistry 51, 10-18
57. Davidson, W. S. and Silva, R. A. (2005) Apolipoprotein structural organization in high density lipoproteins: Belts, bundles, hinges and hairpins Curr. Opin Lipidol. 16, 295-300
58. Sparks, D. L., Frank, P. G., Braschi, S., Neville, T. A., and Marcel, Y. L. (1999) Effect of apolipoprotein A-I lipidation on the formation and function of pre-beta and alpha-migrating LpA-I particles Biochemistry 38, 1727-1735
59. Jayaraman, S., Abe-Dohmae, S., Yokoyama, S., and Cavigiolio, G. (2011) Impact of self-association on function of apolipoprotein A-I J. Biol. Chem. 286, 35610-35623
60. Asztalos, B. F., Roheim, P. S., Milani, R. L., Lefevre, M., McNamara, J. R., Horvath, K. V., and Schaefer, E. J. (2000) Distribution of apoA-I-containing HDL subpopulations in patients with coronary heart disease Arterioscler., Thromb., Vasc. Biol. 20, 2670-2676
61. Schonfeld, G. and Pfleger, B. (1974) The structure of human high density lipoprotein and the levels of apolipoprotein A-I in plasma as determined by radioimmunoassay J. Clin. Invest. 54, 236-246
62. Davidson, W. S., Hazlett, T., Mantulin, W. W., and Jonas, A. (1996) The role of apolipoprotein AI domains in lipid binding Proc. Natl. Acad. Sci. U. S. A. 93, 13605-13610
63. Gwynne, J., Brewer, B., Jr., and Edelhoch, H. (1974) The molecular properties of ApoA-I from human high density lipoprotein J. Biol. Chem. 249, 2411-2416
64. Willard, L., Ranjan, A., Zhang, H., Monzavi, H., Boyko, R. F., Sykes, B. D., and Wishart, D. S. (2003) VADAR: A web server for quantitative evaluation of protein structure quality Nucleic Acids Res. 31, 3316-3319
65. Voss, N. R. and Gerstein, M. (2010) 3V: Cavity, channel and cleft volume calculator and extractor Nucleic Acids Res. 38, W555-562
66. Gursky, O. and Atkinson, D. (1996) Thermal unfolding of human high-density apolipoprotein A-1: implications for a lipid-free molten globular state Proc. Natl. Acad. Sci. U. S. A. 93, 2991-2995
67. Young, M. M., Tang, N., Hempel, J. C., Oshiro, C. M., Taylor, E. W., Kuntz, I. D., Gibson, B. W., and Dollinger, G. (2000) High throughput protein fold identification by using experimental constraints derived from intramolecular cross-links and mass spectrometry Proc. Natl. Acad. Sci. U. S. A. 97, 5802-5806
68. Leitner, A., Reischl, R., Walzthoeni, T., Herzog, F., Bohn, S., Forster, F., and Aebersold, R. (2012) Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography Mol. Cell Proteomics 11, M111-014126
69. Huang, B. X., Kim, H. Y., and Dass, C. (2004) Probing three-dimensional structure of bovine serum albumin by chemical cross-linking and mass spectrometry J. Am. Soc. Mass Spectrom. 15, 1237-1247
70. Huang, B. X., Dass, C., and Kim, H. Y. (2005) Probing conformational changes of human serum albumin due to unsaturated fatty acid binding by chemical cross-linking and mass spectrometry Biochem. J. 387, 695-702
71. Jacobsen, R. B., Sale, K. L., Ayson, M. J., Novak, P., Hong, J., Lane, P., Wood, N. L., Kruppa, G. H., Young, M. M., and Schoeniger, J. S. (2006) Structure and dynamics of dark-state bovine rhodopsin revealed by chemical cross-linking and high-resolution mass spectrometry Protein Sci. 15, 1303-1317
72. Kalisman, N., Adams, C. M., and Levitt, M. (2012) Subunit order of eukaryotic TRiC/CCT chaperonin by cross-linking, mass spectrometry, and combinatorial homology modeling Proc. Natl. Acad. Sci. U. S. A. 109, 2884-2889
73. Leitner, A., Walzthoeni, T., Kahraman, A., Herzog, F., Rinner, O., Beck, M., and Aebersold, R. (2010) Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics Mol. Cell Proteomics 9, 1634-1649
74. Chen, Z. A., Jawhari, A., Fischer, L., Buchen, C., Tahir, S., Kamenski, T., Rasmussen, M., Lariviere, L., Bukowski-Wills, J. C., Nilges, M., Cramer, P., and Rappsilber, J. (2010) Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry EMBO J. 29, 717-726
75. Seebacher, J., Mallick, P., Zhang, N., Eddes, J. S., Aebersold, R., and Gelb, M. H. (2006) Protein cross-linking analysis using mass spectrometry, isotope-coded cross-linkers, and integrated computational data processing J. Proteome Res. 5, 2270-2282
76. Green, N. S., Reisler, E., and Houk, K. N. (2001) Quantitative evaluation of the lengths of homobifunctional protein cross-linking reagents used as molecular rulers Protein Sci. 10, 1293-1304
77. Lu, B., Morrow, J. A., and Weisgraber, K. H. (2000) Conformational reorganization of the four-helix bundle of human apolipoprotein E in binding to phospholipid J. Biol. Chem. 275, 20775-20781-20781