Molecular basis for the differences in lipid and lipoprotein binding properties of human apolipoproteins E3 and E4

Biochemistry

Volumn 49, Issue 51, 2010, Pages 10881-10889

  Nguyen, David ^a   Dhanasekaran, Padmaja ^a   Nickel, Margaret ^a   Nakatani, Ryosuke ^b   Saito, Hiroyuki ^b   Phillips, Michael C ^a   Lund Katz, Sissel ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEINS; BINDING PROPERTIES; C-TERMINAL DOMAINS; HIGH-DENSITY LIPOPROTEINS; ISOFORMS; LIPID BINDING; LOW DENSITY LIPOPROTEINS; MOLECULAR BASIS; N-TERMINAL DOMAINS; N-TERMINAL HELIX; PARTICLE SURFACE; PLASMA CHOLESTEROL; TRIOLEIN EMULSION;

EMULSIFICATION; PHOSPHOLIPIDS;

BINDING ENERGY;

APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; HIGH DENSITY LIPOPROTEIN; LIPID EMULSION; PHOSPHOLIPID; TRIOLEIN; VERY LOW DENSITY LIPOPROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; GENE DELETION; GENE REARRANGEMENT; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN VARIANT;

APOLIPOPROTEIN E3; APOLIPOPROTEIN E4; ESCHERICHIA COLI; GENE EXPRESSION; HUMANS; LIPID METABOLISM; LIPOPROTEINS; LIPOPROTEINS, HDL; LIPOPROTEINS, VLDL; MUTATION; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY;

EID: 78650487051     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1017655     Document Type: Article

References (36)

1. Mahley, R. W., Weisgraber, K. H., and Huang, Y. (2009) Apolipoprotein E: Structure determines function-from atherosclerosis to Alzheimers disease to AIDS J. Lipid Res. 50, S183-S188
2. 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, S156-S161
3. Curtiss, L. K. and Boisvert, W. A. (2000) Apolipoprotein E and atherosclerosis Curr. Opin. Lipidol. 11, 243-251
4. Weisgraber, K. H. (1994) Apolipoprotein E: Structure-function relationships Adv. Protein Chem. 45, 249-302
5. Mahley, R. W., Huang, Y., and Rall, S. C. (1999) Pathogenesis of type III hyperlipoproteinemia (dysbetalipoproteinemia): Questions, quandaries, and paradoxes J. Lipid Res. 40, 1933-1949
6. Davignon, J., Gregg, R. E., and Sing, C. F. (1988) Apolipoprotein E polymorphism and atherosclerosis Arteriosclerosis 8, 1-21
7. Lahoz, C., Schaefer, E. J., Cupples, L. A., Wilson, P. W., Levy, D., Osgood, D., Parpos, S., Pedro-Botet, J., Daly, J. A., and Ordovas, J. M. (2001) Apolipoprotein E genotype and cardiovascular disease in the Framingham Heart Study Atherosclerosis 154, 529-537
8. 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
9. Steinmetz, A., Jakobs, C., Motzny, S., and Kaffarnik, H. (1989) Differential distribution of apolipoprotein E isoforms in human plasma lipoproteins Arteriosclerosis 9, 405-411
10. 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
11. 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
12. Morrow, J. A., Hatters, D. M., Lu, B., Hocht, P., Oberg, K. A., Rupp, B., and Weisgraber, K. H. (2002) Apolipoprotein E4 forms a molten globule J. Biol. Chem. 277, 50380-50385
13. Dong, L. M., Wilson, C., Wardell, M. R., Simmons, T., Mahley, R. W., Weisgraber, K. H., and Agard, D. A. (1994) Human apolipoprotein E. Role of arginine 61 in mediating the lipoprotein preferences of the E3 and E4 isoforms J. Biol. Chem. 269, 22358-22365
14. Dong, L. M. and Weisgraber, K. H. (1996) Human apolipoprotein E4 domain interaction. Arginine 61 and glutamic acid 255 interact to direct the preference for very low density lipoproteins J. Biol. Chem. 271, 19053-19057
15. Drury, J. and Narayanaswami, V. (2005) Examination of lipid-bound conformation of apolipoprotein E4 by pyrene excimer fluorescence J. Biol. Chem. 280, 14605-14610
16. 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
17. Sakamoto, T., Tanaka, M., Vedhachalam, C., Nickel, M., Nguyen, D., Dhanasekaran, P., Phillips, M. C., Lund-Katz, S., and Saito, H. (2008) Contributions of the carboxyl-terminal helical segment to the self-association and lipoprotein preferences of human apolipoprotein E3 and E4 isoforms Biochemistry 47, 2968-2977
18. Saito, H., Dhanasekaran, P., Baldwin, F., Weisgraber, K. H., Phillips, M. C., and Lund-Katz, S. (2003) Effects of polymorphism on the lipid interaction of human apolipoprotein E J. Biol. Chem. 278, 40723-40729
19. 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
20. Tanaka, M., Vedhachalam, C., Sakamoto, T., Dhanasekaran, P., Phillips, M. C., Lund-Katz, S., and Saito, H. (2006) Effect of carboxyl-terminal truncation on structure and lipid interaction of human apolipoprotein E4 Biochemistry 45, 4240-4247
21. Chroni, A., Pyrpassopoulos, S., Thanassoulas, A., Nounesis, G., Zannis, V. I., and Stratikos, E. (2008) Biophysical analysis of progressive C-terminal truncations of human apolipoprotein E4: Insights into secondary structure and unfolding properties Biochemistry 47, 9071-9080
22. Morrow, J. A., Arnold, K. S., and Weisgraber, K. H. (1999) Functional characterization of apolipoprotein E isoforms overexpressed in Escherichia coli Protein Expression Purif. 16, 224-230
23. Saito, H., Dhanasekaran, P., Baldwin, F., Weisgraber, K., Lund-Katz, S., and Phillips, M. C. (2001) Lipid binding-induced conformational change in human apolipoprotein E J. Biol. Chem. 276, 40949-40954
24. Saito, H., Dhanasekaran, P., Nguyen, D., Baldwin, F., Weisgraber, K. H., Wehrli, S., Phillips, M. C., and Lund-Katz, S. (2003) Characterization of the heparin binding sites in human apolipoprotein E J. Biol. Chem. 278, 14782-14787
25. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the folin phenol reagent J. Biol. Chem. 193, 265-275
26. 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
27. Segall, M. L., Dhanasekaran, P., Baldwin, F., Anantharamaiah, G. M., Weisgraber, K., 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
28. 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
29. 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
30. 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
31. Saito, H., Lund-Katz, S., and Phillips, M. C. (2004) Contributions of domain structure and lipid interaction to the functionality of exchangeable human apolipoproteins Prog. Lipid Res. 43, 350-380
32. Shen, B. W., Scanu, A. M., and Kezdy, F. J. (1977) Structure of human serum lipoproteins inferred from compositional analysis Proc. Natl. Acad. Sci. U.S.A. 74, 837-841
33. Ibdah, J. A., Lund-Katz, S., and Phillips, M. C. (1989) Molecular packing of high-density and low-density lipoprotein surface lipids and apolipoprotein A-I binding Biochemistry 28, 1126-1133
34. Phillips, M. C. and Krebs, K. E. (1986) Studies of apolipoproteins at the air-water interface Methods Enzymol. 128, 387-403
35. Narayanaswami, V. and Ryan, R. O. (2000) Molecular basis of exchangeable apolipoprotein function Biochim. Biophys. Acta 1483, 15-36
36. Lund-Katz, S., Nguyen, D., Dhanasekaran, P., Kono, M., Nickel, M., Saito, H., and Phillips, M. C. (2010) Surface plasmon resonance analysis of the mechanism of binding of apoA-I to high density lipoprotein particles J. Lipid Res. 51, 606-617