Decoding of lipoprotein-receptor interactions: Properties of ligand binding modules governing interactions with apolipoprotein E

Biochemistry

Volumn 49, Issue 6, 2010, Pages 1207-1216

  Guttman, Miklos ^a   Prieto, J Helena ^a   Croy, Johnny E ^a   Komives, Elizabeth A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY BINDING; APOLIPOPROTEIN E; BINDING AFFINITIES; CHOLESTEROL HOMEOSTASIS; CONSERVED RESIDUES; LARGE CLUSTERS; LIGAND BINDING; RECEPTOR BINDING; RECEPTOR INTERACTION; RECOGNITION PROCESS;

BINDING ENERGY;

LIGANDS;

APOLIPOPROTEIN E; CALCIUM; LOW DENSITY LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; VERY LOW DENSITY LIPOPROTEIN RECEPTOR;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CALCIUM BINDING; CONTROLLED STUDY; HUMAN; INDUCED MUTATION; LIGAND BINDING; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; APOLIPOPROTEINS E; HUMANS; LDL-RECEPTOR RELATED PROTEIN 1; LIGANDS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, LDL; SEQUENCE ALIGNMENT;

EID: 76749135871     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi9017208     Document Type: Article

References (58)

1. Blacklow, S. C. (2007) Versatility in ligand recognition by LDL receptor family proteins: advances and frontiers. Curr. Opin. Struct. Biol. 17, 419-426.
2. Brown, M. S., and Goldstein, J. L. (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232, 34-47.
3. Hui, D. Y., Innerarity, T. L., and Mahley, R. W. (1984) Defective hepatic lipoprotein receptor binding of B-very low density lipoproteins from type 111 hyperlipoproteinemic patients: importance of apolipoprotein E. J. Biol. Chem. 259, 860-869.
4. Kowal, R. C., Herz, J, Goldstein, J. L., Esser, V., and Brown, M. S. (1989) Low density receptor-related protein mediates uptake of cholesteryl esters derived from apolipoprotein E-enriched lipoproteins. Proc. Natl. Acad. Sci. U.S.A. 86, 5810-5814.
5. Hussain, M. M., Maxfield, F. R., Mas-Oliva, J., Tabas, I., Ji, Z. S., Innerarity, T. L., and Mahley, R. W. (1991) Clearance of chylomicron remnants by the low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J. Biol. Chem. 266, 13936-13940.
6. Tacken, P. J., Teusink, B., Jong, M. C., Harats, D., Havekes, L. M., van Dijk, K. W., and Hofker, M. H. (2000) LDL receptor deficiency unmasks altered VLDL triglyceride metabolism in VLDL receptor transgenic and knockout mice. J. Lipid Res. 41, 2055-2062.
7. Takahashi, S., Kawarabayasi, Y., Nakai, T., Sakai, J., and Yamamoto, T. (1992) Rabbit very low density lipoprotein receptor: a low density lipoprotein receptor-like protein with distinct ligand specificity. Proc. Natl. Acad. Sci. U.S.A. 89, 9252-9256.
8. Herz, J., and Strickland, D. K. (2001) LRP: a multifunctional scavenger and signaling receptor. J. Clin. Invest. 108, 779-784.
9. Willnow, T. E., Moehring, J. M., Inocencio, N. M., Moehring, T. J., and Herz, J. (1996) The low-density-lipoprotein receptor-related protein (LRP) is processed by furin in vivo and in vitro. Biochem. J. 313, 71-76.
10. Willnow, T. E., Armstrong, S. A., Hammer, R. E., and Herz, J. (1995) Functional expression of low density lipoprotein receptor-related protein is controlled by receptor-associated protein in vivo. Proc. Natl. Acad. Sci. U.S.A. 92, 4537-4541.
11. Bu, G., and Rennke, S. (1996) Receptor-associated protein is a folding chaperone for low density lipoprotein receptor-related protein. J. Biol. Chem. 271, 22218-22224.
12. Herz, J., Goldstein, J. L., Strickland, D. K., Ho, Y. K., and Brown, M. S. (1991) 39-kDa protein modulates binding of ligands to low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J. Biol. Chem. 266, 21232-21238.
13. Andersen, O. M., Schwarz, F. P., Eisenstein, E., Jacobsen, C., Moestrup, S. K., Etzerodt, M., and Thoegersen, H. C. (2001) Dominant thermodynamic role of the third independent receptor binding site in the receptor-associated protein RAP. Biochem. J. 40, 15408-15417.
14. Andersen, O. M., Christensen, L. L., Christensen, P. A., Soerensen, E. S., Jacobsen, C., Moestrup, S. K., Etzerodt, M., and Thogersen, H. C. (2000) Identification of the minimal functional unit in the low density lipoprotein receptor-related protein for binding the receptor-associated protein (RAP). A conserved acidic residue in the complement-type repeats is important for recognition of RAP. J. Biol. Chem. 275, 21017-21024.
15. Willnow, T. E., Orth, K., and Herz, J. (1994) Molecular dissection of ligand binding sites on the low density lipoprotein receptor-related protein. J. Biol. Chem. 269, 15827-15832.
16. Neels, J. G., van den Berg, B. M. M., Lookene, A., Olivecrona, G., Pannekoek, H., and van Zonneveld, A. J. (1999) The second and fourth cluster of class A cysteine-rich repeats of the low density lipoprotein receptor-related protein share ligand binding properties. J. Biol. Chem. 274, 31305-31311.
17. Horn, I. R., van den Berg, B. M., van der Meijden, P. Z., Pannekoek, H., and van Zonneveld, A. J. (1997) Molecular analysis of ligand binding to the second cluster of complement-type repeats of the low density lipoprotein receptor-related protein. Evidence for an allosteric component in receptor-associated protein-mediated inhibition of ligand binding. J. Biol. Chem. 272, 13608-13613.
18. Croy, J. E., Shin, W. D., Knauer, M. F., Knauer, D. J., and Komives, E. A. (2003) All three LDL receptor homology regions of the LDL receptor-related protein (LRP) bind multiple ligands. Biochemistry 42, 13049-13057.
19. Beisiegel, U., Weber, W., Ihrke, G., Herz, J., and Stanley, K. K. (1989) The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature 341, 162-164.
20. Mokuno, H., Yamada, N., Shimano, H., Ishibashi, S., Mori, N., Takahashi, K., Oka, T., Yoon, T. H., and Takaku, F. (1991) The enhanced cellular uptake of very-low-density lipoprotein enriched in apolipoprotein E. Biochim. Biophys. Acta 1082, 63-70.
21. Blacklow, S. C., and Kim, P. S. (1996) Protein folding and calcium binding defects arising from familial hypercholesterolemia mutations of the LDL receptor. Nat. Struct. Biol. 3, 758-762.
22. Rudenko, G., and Deisenhofer, J. (2003) The low-density lipoprotein receptor: ligands, debates and lore. Curr. Opin. Struct. Biol. 13, 683-689.
23. Huang, W., Dolmer, K., and Gettins, P. G. (1999) NMR solution structure of complement-like repeat CR8 from the low density lipoprotein receptor-related protein. J. Biol. Chem. 274, 14130-14136.
24. Rall, S. C. J., 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.
25. Innerarity, T. L., Friedlander, E. J., Rall, S. C. J., Weisgraber, K. H., and Mahley, R. W. (1983) The receptor binding domain of human apolipoprotein E. Binding of apolipoprotein E fragments. J. Biol. Chem. 258, 12341-12347.
26. Weisgraber, K. L., Innerarity, T. L., Harder, K. J., Mahley, R. W., Milne, R. W., Marcel, Y. L., and Sparrow, J. T. (1983) The receptor binding domain of human apolipoprotein E. J. Biol. Chem. 258, 12348-12354.
27. Lalazar, A., Weisgraber, K. H., Rall, S. C. J., Gilad, H., Innerarity, T. L., Levanon, A. Z., Boyles, J. K., Amit, B., Gorecki, M., Mahley, R. W., and Vogel, T. (1988) Site-specific mutagenesis of human apolipoprotein E. Receptor binding activity of variants with single amino acids substitutions. J. Biol. Chem. 263, 3542-3545.
28. Zaiou, M., Arnold, K. S., Newhouse, Y. M., Innerarity, T. L., Weisgraber, K. H., Segall, M. L., Phillips, M. C., and Lund-Katz, S. (2000) Apolipoprotein E; low density lipoprotein receptor interaction. Influences of basic residue and amphipathic alpha-helix organization in the ligand. J. Lipid Res. 41, 1087-1095.
29. Kiss, R. S., Weers, P. M., Narayanaswami, V., Cohen, J., Kay, C. M., and Ryan, R. O. (2003) Structure-guided protein engineering modulates helix bundle exchangeable apolipoprotein properties. J. Biol. Chem. 278, 21952-21959.
30. Mims, M. P., Darnule, A. T., Tovar, R. W., Pownall, H. J., Sparrow, D. A., Sparrow, J. T., Via, D. P., and Smith, L. C. (1994) A nonexchangeable apolipoprotein E peptide that mediates binding to the low density lipoprotein receptor. J. Biol. Chem. 269, 20539-20547.
31. Datta, G., Garber, D. W., Chung, B. H., Chaddha, M., Dashti, N., Bradley, W. A., Gianturco, S. H., and Anantharamaiah, G. M. (2001) Cationic domain 141-150 of apoE covalently linked to a class A amphipathic helix enhances atherogenic lipoprotein metabolism in vitro and in vivo. J. Lipid Res. 42, 959-966.
32. Croy, J. E., Brandon, T., and Komives, E. A. (2004) Two apolipoprotein E mimetic peptides, apoE(130-149) and apoE(141-155)2, bind to LRP1. Biochemistry 43, 7328-7335.
33. 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.
34. Fisher, C. A., and Ryan, R. O. (1999) Lipid binding-induced conformational changes in the N-terminal domain of human apolipoprotein E. J. Lipid Res. 40, 93-99.
35. Peters-Libeu, C. A., Newhouse, Y., Hatters, D. M., and Weisgraber, K. H. (2006) Model of biologically active apolipoprotein E bound to dipalmitoylphosphatidylcholine. J. Biol. Chem. 281, 1073-1079.
36. Peters-Libeu, C. A., Newhouse, Y., Hall, S. C., Witkowska, H. E., and Weisgraber, K. H. (2007) Apolipoprotein E3 dipalmitoylphosphatidylcholine particles are ellipsoidal in solution. J. Lipid Res. 48, 1035-1044.
37. Lund-Katz, S., Zaiou, M., Wehrli, S., Dhanasekaran, P., Baldwin, F., Weisgraber, K. H., and Phillips, M. C. (2000) Effects of lipid interaction on the lysine microenvironments in apolipoprotein E. J. Biol. Chem. 275, 34459-34464.
38. Lalazar, A., and Mahley, R. W. (1989) Human apolipoprotein E. Receptor binding activity of truncated variants with carboxyl-terminal deletions. J. Biol. Chem. 264, 8447-8450.
39. Morrow, J. A., Arnold, K. S., Dong, J., Balesta, M. E., and Innerarity, T. L. (2000) Effect of arginine 172 on the binding of apolipoprotein E to the low density lipoprotein receptor. J. Biol. Chem. 275, 2576-2580.
40. Gupta, V., Narayanaswami, V., Budamagunta, M. S., Yamamato, T., Voss, J. C., and Ryan, R. O. (2006) Lipid-induced extension of apolipoprotein E helix 4 correlates with low density lipoprotein receptor binding ability. J. Biol. Chem. 281, 39294-39299.
41. Fisher, C., Abdul-Aziz, D., and Blacklow, S. C. (2004) A two-module region of the low-density lipoprotein receptor sufficient for formation of complexeswith apolipoprotein E ligands. Biochem. J. 43, 1037-1044.
42. Russell, D. W., Brown, M. S., and Goldstein, J. L. (1989) Different combinations of cysteine-rich repeats mediate binding of lowdensity lipoprotein receptor to two different proteins. J. Biol. Chem. 264, 21682-21688.
43. 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.
44. Nicholas, K. B., Nicholas, H. B., Jr., and Deerfield, D. W., II. (1997) GeneDoc: Analysis and visualization of genetic variation. EMBnet. NEWS 4, 14.
45. White, C. E., Hunter, M. J., Meininger, D. P., White, L. R., and Komives, E. A. (1995) Large-scale expression, purification and characterization of small fragments of thrombomodulin: the roles of the sixth domain and of methionine 388. Protein Eng. 8, 1177-1187.
46. Fass, D., Blacklow, S., Kim, P. S., and Berger, J. M. (1997) Molecular basis of familial hypercholesterolaemia from structure of LDL receptor module. Nature 388, 691-693.
47. Clackson, T., Detlef, G., and Jones, P. (1991) PCR, a Practical Approach (McPherson, M., Quirke, P., and Taylor, G., Eds.) p 202, IRL Press, Oxford.
48. Jez, M., J., Ferrer, J., Bowman, M., E., Dixon, R., A., and Noel, J., P. (2000) Dissection of malonyl-coenzyme A decarboxylation from polyketide formation in the reaction mechanism of a plant polyketide synthase. Biochemistry 39, 890-902.
49. Hoffman, R. M. B., Li, M. X., and Sykes, B. D. (2005) The binding of W7, an inhibitor of striated muscle contraction, to cardiac troponin C. Biochemistry 44, 15750-15759.
50. 2+ binding tocomplement-type repeat domains 5 and 6 fromthe lowdensity lipoprotein receptor-related protein. BMC Biochem. 4, 7.
51. Simonovic, M., Dolmer, K., Huang, W., Strickland, D. K., Volz, K., and Gettins, P. G. W. (2001) Calcuim coordination and pH dependence of the calcium affinity of ligand-binding repeat CR7 from the LRP. Comparision with related domains from the LRP and the LDL receptor. Biochemistry 40, 15127-15134.
52. Rudenko, G., Henry, L., Henderson, K., Ichtchenko, K., Brown, M. S., Goldstein, J. L., and Deisenhofer, J. (2002) Structure of the LDL receptor extracellular domain at endosomal pH. Science 298, 2353-2358.
53. Verdaguer, N., Fita, I., Reithmayer, M., Moser, R., and Blaas, D. (2004) X-ray structure of aminor group human rhinovirus bound to a fragment of its cellular receptor protein. Nat. Struct. Mol. Biol. 11, 429-434.
54. Fisher, C., Beglova, N., and Blacklow, S. C. (2006) Structure of an LDLR-RAP complex reveals a general mode for ligand recognition by lipoprotein receptors. Mol. Cell 22, 277-283.
55. Prévost, M., and Raussens, V. (2004) Apolipoprotein E-low density lipoprotein receptor binding: study of protein-protein interaction in rationally selected docked complexes. Proteins 55, 874-884.
56. Mahley, R. W., Innerarity, T. L., Rall, S. C., and Weisgraber, K. H. (1984) Plasma lipoproteins: apolipoprotein structure and function. J. Lipid Res. 25, 1277-1294.
57. Pitas, R. E., Innerarity, T. L., and Mahley, R. W. (1980) Cell surface receptor binding of phospholipid • protein complexes containing different ratios of receptor-active and -inactive E apoprotein. J. Biol. Chem. 255, 5454-5460.
58. Abdul-Aziz, D., Fisher, C., Beglova, N., and Blacklow, S. C. (2005) Folding and binding integrity of variants of a prototype ligand-binding module from the LDL receptor possessing multiple alanine substitutions. Biochem. J. 44, 5075-5085.