Dissociation of apolipoprotein e oligomers to monomer is required for high-affinity binding to phospholipid vesicles

Biochemistry

Volumn 50, Issue 13, 2011, Pages 2550-2558

  Garai, Kanchan ^a   Baban, Berevan ^a   Frieden, Carl ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY BINDING; ALZHEIMER'S DISEASE; APOLIPOPROTEIN E; APOLIPOPROTEINS; ASSOCIATION-DISSOCIATION PROCESS; BIOLOGICAL FUNCTIONS; CONFORMATIONAL CONVERSION; DIMYRISTOYL; ISOFORMS; KINETIC DATA; LIPID METABOLISMS; LIPIDATION; MICROMOLAR CONCENTRATION; PHOSPHOCHOLINE; PHOSPHOLIPID VESICLES; PRIOR KNOWLEDGE; RATE OF DISSOCIATION; RATE-LIMITING PROCESS; REACTION MODEL; RISK FACTORS; SELF-ASSOCIATION BEHAVIOR; SELF-ASSOCIATIONS; SMALL UNILAMELLAR VESICLE; TETRAMERS; TIME DEPENDENCE;

CONFORMATIONS; DIMERS; DISSOCIATION; LIPOSOMES; MOLECULAR WEIGHT; MONOMERS; PHOSPHOLIPIDS; RATE CONSTANTS; TURBIDITY;

ASSOCIATION REACTIONS;

APOLIPOPROTEIN E; DIMYRISTOYLPHOSPHATIDYLCHOLINE; OLIGOMER;

ARTICLE; BINDING AFFINITY; BINDING KINETICS; DISSOCIATION; MOLECULAR WEIGHT; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; TURBIDITY;

APOLIPOPROTEIN E4; APOLIPOPROTEINS E; CIRCULAR DICHROISM; DIMERIZATION; DIMYRISTOYLPHOSPHATIDYLCHOLINE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HUMANS; KINETICS; MUTANT PROTEINS; OSMOLAR CONCENTRATION; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN ISOFORMS; PROTEIN STABILITY; UNILAMELLAR LIPOSOMES;

EID: 79953225852     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1020106     Document Type: Article

References (54)

1. Weisgraber, K. H., Innerarity, T. L., and Mahley, R. W. (1982) Abnormal lipoprotein receptor-binding activity of the human E apoprotein due to cysteine-arginine interchange at a single site J. Biol. Chem. 257, 2518-2521
2. Rall, S. C., Jr., Weisgraber, K. H., Innerarity, T. L., and Mahley, R. W. (1982) Structural basis for receptor binding heterogeneity of apolipoprotein E from type III hyperlipoproteinemic subjects Proc. Natl. Acad. Sci. U.S.A. 79, 4696-4700
3. Davignon, J., Gregg, R. E., and Sing, C. F. (1988) Apolipoprotein E polymorphism and atherosclerosis Arteriosclerosis 8, 1-21 (Pubitemid 18049171)
4. Weisgraber, K. H. (1990) Apolipoprotein E distribution among human plasma lipoproteins: role of the cysteine-arginine interchange at residue 112 J. Lipid Res. 31, 1503-1511 (Pubitemid 20261914)
5. Mahley, R. W., Huang, Y., and Rall, S. C., Jr. (1999) Pathogenesis of type III hyperlipoproteinemia (dysbetalipoproteinemia). Questions, quandaries, and paradoxes J. Lipid Res. 40, 1933-1949 (Pubitemid 29523420)
6. Getz, G. S. and Reardon, C. A. (2009) Apoprotein E as a lipid transport and signaling protein in the blood, liver, and artery wall J. Lipid Res. 50 (Suppl.) S156-S161
7. Mahley, R. W., Weisgraber, K. H., and Huang, Y. (2009) Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimer's disease to AIDS J. Lipid Res. 50 (Suppl.) S183-S188
8. Heide, S., Manfred, K., Glaser, C., and Schulz, S. (2009) Apolipoprotein E (apoE) polymorphism: a risk factor for fatal coronary sclerosis? Forensic Sci. Int. 192, 62-66
9. Vaisi-Raygani, A., Rahimi, Z., Nomani, H., Tavilani, H., and Pourmotabbed, T. (2007) The presence of apolipoprotein epsilon4 and epsilon2 alleles augments the risk of coronary artery disease in type 2 diabetic patients Clin. Biochem. 40, 1150-1156 (Pubitemid 47379326)
10. Winkler, K., Hoffmann, M. M., Krane, V., Marz, W., Drechsler, C., and Wanner, C. (2010) Apolipoprotein E genotype predicts cardiovascular endpoints in dialysis patients with type 2 diabetes mellitus Atherosclerosis 208, 197-202
11. Bennet, A. M., Di Angelantonio, E., Ye, Z., Wensley, F., Dahlin, A., Ahlbom, A., Keavney, B., Collins, R., Wiman, B., de Faire, U., and Danesh, J. (2007) Association of apolipoprotein E genotypes with lipid levels and coronary risk J. Am. Med. Assoc. 298, 1300-1311 (Pubitemid 47443344)
12. Anuurad, E., Lu, G., Rubin, J., Pearson, T. A., and Berglund, L. (2007) ApoE genotype affects allele-specific apo[a] levels for large apo[a] sizes in African Americans: the Harlem-Basset study J. Lipid Res. 48, 693-698 (Pubitemid 46397472)
13. Wagle, J., Farner, L., Flekkoy, K., Wyller, T. B., Sandvik, L., Eiklid, K. L., Fure, B., Stensrod, B., and Engedal, K. (2009) Association between ApoE epsilon4 and cognitive impairment after stroke Dementia Geriatr. Cognit. Disord. 27, 525-533
14. Corder, E. H., Saunders, A. M., Strittmatter, W. J., Schmechel, D. E., Gaskell, P. C., Small, G. W., Roses, A. D., Haines, J. L., and Pericak-Vance, M. A. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families Science 261, 921-923 (Pubitemid 23275809)
15. Drzezga, A., Grimmer, T., Henriksen, G., Muhlau, M., Perneczky, R., Miederer, I., Praus, C., Sorg, C., Wohlschlager, A., Riemenschneider, M., Wester, H. J., Foerstl, H., Schwaiger, M., and Kurz, A. (2009) Effect of APOE genotype on amyloid plaque load and gray matter volume in Alzheimer disease Neurology 72, 1487-1494
16. Farrer, L. A., Cupples, L. A., Haines, J. L., Hyman, B., Kukull, W. A., Mayeux, R., Myers, R. H., Pericak-Vance, M. A., Risch, N., and van Duijn, C. M. (1997) Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. APOE and Alzheimer Disease Meta Analysis Consortium J. Am. Med. Assoc. 278, 1349-1356 (Pubitemid 27449696)
17. Alberts, M. J., Graffagnino, C., McClenny, C., DeLong, D., Strittmatter, W., Saunders, A. M., and Roses, A. D. (1995) ApoE genotype and survival from intracerebral haemorrhage Lancet 346, 575
18. Hatters, D. M., Peters-Libeu, C. A., and Weisgraber, K. H. (2006) Apolipoprotein E structure: insights into function Trends Biochem. Sci. 31, 445-454 (Pubitemid 44108662)
19. 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 (Pubitemid 21917100)
20. Sivashanmugam, A. and Wang, J. (2009) A unified scheme for initiation and conformational adaptation of human apolipoprotein E N-terminal domain upon lipoprotein binding and for receptor binding activity J. Biol. Chem. 284, 14657-14666
21. Aggerbeck, L. P., Wetterau, J. R., Weisgraber, K. H., Wu, C. S., and Lindgren, F. T. (1988) Human apolipoprotein E3 in aqueous solution. II. Properties of the amino- and carboxyl-terminal domains J. Biol. Chem. 263, 6249-6258
22. Westerlund, J. A. and Weisgraber, K. H. (1993) Discrete carboxyl-terminal segments of apolipoprotein E mediate lipoprotein association and protein oligomerization J. Biol. Chem. 268, 15745-15750 (Pubitemid 23222075)
23. Patel, A. B., Khumsupan, P., and Narayanaswami, V. (2010) Pyrene fluorescence analysis offers new insights into the conformation of the lipoprotein-binding domain of human apolipoprotein E Biochemistry 49, 1766-1775
24. Narayanaswami, V., Szeto, S. S., and Ryan, R. O. (2001) Lipid association-induced N- and C-terminal domain reorganization in human apolipoprotein E3 J. Biol. Chem. 276, 37853-37860
25. Hatters, D. M., Budamagunta, M. S., Voss, J. C., and Weisgraber, K. H. (2005) Modulation of apolipoprotein E structure by domain interaction: differences in lipid-bound and lipid-free forms J. Biol. Chem. 280, 34288-34295 (Pubitemid 41443154)
26. Zhang, Y., Chen, J., and Wang, J. (2008) A complete backbone spectral assignment of lipid-free human apolipoprotein E (apoE) Biomol. NMR Assign. 2, 207-210
27. Garai, K., Mustafi, S. M., Baban, B., and Frieden, C. (2010) Structural differences between apolipoprotein E3 and E4 as measured by (19)F NMR Protein Sci. 19, 66-74
28. Peters-Libeu, C. A., Newhouse, Y., Hall, S. C., Witkowska, H. E., and Weisgraber, K. H. (2007) Apolipoprotein E*dipalmitoylphosphatidylcholine particles are ellipsoidal in solution J. Lipid Res. 48, 1035-1044 (Pubitemid 46708670)
29. Schneeweis, L. A., Koppaka, V., Lund-Katz, S., Phillips, M. C., and Axelsen, P. H. (2005) Structural analysis of lipoprotein E particles Biochemistry 44, 12525-12534 (Pubitemid 41324343)
30. Segall, M. L., Dhanasekaran, P., Baldwin, F., Anantharamaiah, G. M., Weisgraber, K. H., Phillips, M. C., and Lund-Katz, S. (2002) Influence of apoE domain structure and polymorphism on the kinetics of phospholipid vesicle solubilization J. Lipid Res. 43, 1688-1700 (Pubitemid 35168283)
31. Massey, J. B., Gotto, A. M., Jr., and Pownall, H. J. (1981) Human plasma high density apolipoprotein A-I: effect of protein-protein interactions on the spontaneous formation of a lipid-protein recombinant Biochem. Biophys. Res. Commun. 99, 466-474 (Pubitemid 12195968)
32. Choy, N., Raussens, V., and Narayanaswami, V. (2003) Inter-molecular coiled-coil formation in human apolipoprotein E C-terminal domain J. Mol. Biol. 334, 527-539 (Pubitemid 37386352)
33. Lund-Katz, S. and Phillips, M. C. (0000) High density lipoprotein structure-function and role in reverse cholesterol transport Subcell. Biochem. 51, 183-227
34. Zhang, Y., Vasudevan, S., Sojitrawala, R., Zhao, W., Cui, C., Xu, C., Fan, D., Newhouse, Y., Balestra, R., Jerome, W. G., Weisgraber, K., Li, Q., and Wang, J. (2007) A monomeric, biologically active, full-length human apolipoprotein E Biochemistry 46, 10722-10732 (Pubitemid 47417264)
35. Garai, K. and Frieden, C. (2010) The association-dissociation behavior of the apoE proteins: kinetic and equilibrium studies Biochemistry 49, 9533-9541
36. Selvin, P. R. and Ha, T. (2008) Single-molecule techniques: a laboratory manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Santoro, M. M. and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants Biochemistry 27, 8063-8068
38. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) Global kinetic explorer: a new computer program for dynamic simulation and fitting of kinetic data Anal. Biochem. 387, 20-29
39. Morjana, N. A., McKeone, B. J., and Gilbert, H. F. (1993) Guanidine hydrochloride stabilization of a partially unfolded intermediate during the reversible denaturation of protein disulfide isomerase Proc. Natl. Acad. Sci. U.S.A. 90, 2107-2111 (Pubitemid 23078574)
40. Pownall, H., Pao, Q., Hickson, D., Sparrow, J. T., Kusserow, S. K., and Massey, J. B. (1981) Kinetics and mechanism of association of human plasma apolipoproteins with dimyristoylphosphatidylcholine: effect of protein structure and lipid clusters on reaction rates Biochemistry 20, 6630-6635 (Pubitemid 12186513)
41. Jonas, A. and Drengler, S. M. (1980) Kinetics and mechanism of apolipoprotein A-I interaction with l -alpha-dimyristoylphosphatidylcholine vesicles J. Biol. Chem. 255, 2190-2194
42. Jonas, A., Drengler, S. M., and Patterson, B. W. (1980) Two types of complexes formed by the interaction of apolipoprotein A-I with vesicles of l -alpha-dimyristoylphosphatidylcholine J. Biol. Chem. 255, 2183-2189
43. Nguyen, D., Dhanasekaran, P., Phillips, M. C., and Lund-Katz, S. (2009) Molecular mechanism of apolipoprotein E binding to lipoprotein particles Biochemistry 48, 3025-3032
44. Morrow, J. A., Segall, M. L., Lund-Katz, S., Phillips, M. C., Knapp, M., Rupp, B., and Weisgraber, K. H. (2000) Differences in stability among the human apolipoprotein E isoforms determined by the amino-terminal domain Biochemistry 39, 11657-11666
45. Langer, C., Huang, Y., Cullen, P., Wiesenhutter, B., Mahley, R. W., Assmann, G., and von Eckardstein, A. (2000) Endogenous apolipoprotein E modulates cholesterol efflux and cholesteryl ester hydrolysis mediated by high-density lipoprotein-3 and lipid-free apolipoproteins in mouse peritoneal macrophages J. Mol. Med. 78, 217-227 (Pubitemid 30432012)
46. LaDu, M. J., Stine, W. B., Narita, M., Getz, G. S., Reardon, C. A., and Bu, G. (2006) Self-assembly of HEK cell-secreted apoE particles resembles apoE enrichment of lipoproteins as a ligand for the LDL receptor-related protein Biochemistry 45, 381-390 (Pubitemid 43100405)
47. Krimbou, L., Denis, M., Haidar, B., Carrier, M., Marcil, M., and Genest, J. (2004) Molecular interactions between apoE and ABCA1 J. Lipid Res. 45, 839-848
48. Weisgraber, K. H., Rall, S. C., Mahley, R. W., Milne, R. W., Marcel, Y. L., and Sparrow, J. T. (1986) Human apolipoprotein E. Determination of the heparin binding sites of apolipoprotein E3 J. Biol. Chem. 261, 2068-2076 (Pubitemid 17205129)
49. Lin, C.-Y., Duan, H., and Mazzone, T. (1999) Apolipoprotein E-dependent cholesterol efflux from macrophages: kinetic study and divergent mechanisms for endogenous versus exogenous apolipoprotein E J. Lipid Res. 40, 1618-1626 (Pubitemid 29418702)
50. Bultel-Brienne, S. P., Lestavel, S., Pilon, A., Laffont, I., Tailleux, A., Fruchart, J.-C., Siest, G. R., and Clavey, V. R. (2002) Lipid free apolipoprotein E binds to the class B type I scavenger receptor I (SR-BI) and enhances cholesteryl ester uptake from lipoproteins J. Biol. Chem. 277, 36092-36099
51. Narita, M., Holtzman, D. M., Fagan, A. M., LaDu, M. J., Yu, L., Han, X., Gross, R. W., Bu, G., and Schwartz, A. L. (2002) Cellular catabolism of lipid poor apolipoprotein E via cell surface LDL receptor-related protein J. Biochem. 132, 743-749 (Pubitemid 35408497)
52. Ruiz, J., Kouiavskaia, D., Migliorini, M., Robinson, S., Saenko, E. L., Gorlatova, N., Li, D., Lawrence, D., Hyman, B. T., Weisgraber, K. H., and Strickland, D. K. (2005) The apoE isoform binding properties of the VLDL receptor reveal marked differences from LRP and the LDL receptor J. Lipid Res. 46, 1721-1731 (Pubitemid 41099339)
53. Yamauchi, Y., Deguchi, N., Takagi, C., Tanaka, M., Dhanasekaran, P., Nakano, M., Handa, T., Phillips, M. C., Lund-Katz, S., and Saito, H. (2008) Role of the N- and C-terminal domains in binding of apolipoprotein E isoforms to heparan sulfate and dermatan sulfate: a surface plasmon resonance study Biochemistry 47, 6702-6710 (Pubitemid 351874297)
54. Neyen, C., Pluddemann, A., Roversi, P., Thomas, B., Cai, L., van der Westhuyzen, D. R., Sim, R. B., and Gordon, S. (2009) Macrophage scavenger receptor a mediates adhesion to apolipoproteins A-I and E Biochemistry 48, 11858-11871