High affinity binding of the receptor-associated protein D1D2 domains with the low density lipoprotein receptorrelated protein (LRP1) Involves bivalent complex formation: Critical roles of lysines 60 and 191

Journal of Biological Chemistry

Volumn 291, Issue 35, 2016, Pages 18430-18439

  Prasad, Joni M ^a   Young, Patricia A ^a   Strickland, Dudley K ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SITES; BINS; BIOSYNTHESIS; CELL MEMBRANES; LIGANDS; MOLECULAR BIOLOGY; PROTEINS; SURFACE PLASMON RESONANCE;

CANONICAL MODELING; COMPLEX FORMATIONS; ENDOPLASMIC RETICULUM; HIGH AFFINITY BINDING; HIGH-AFFINITY BINDING SITES; LOW DENSITY LIPOPROTEINS; MOLECULAR CHAPERONES; RECEPTOR-ASSOCIATED PROTEINS;

AMINO ACIDS;

ALANINE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PEPTIDES AND PROTEINS; RECEPTOR ASSOCIATED PROTEIN D1D2; UNCLASSIFIED DRUG; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN ASSOCIATED PROTEIN; LRP1 PROTEIN, HUMAN; LYSINE; MULTIPROTEIN COMPLEX; PROTEIN BINDING;

ARTICLE; BINDING SITE; BIVALENT COMPLEX FORMATION; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; HUMAN; LIMIT OF QUANTITATION; MOLECULAR DOCKING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SURFACE PLASMON RESONANCE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR MODEL; PROTEIN DOMAIN;

HUMANS; LDL-RECEPTOR RELATED PROTEIN-ASSOCIATED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; LYSINE; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN DOMAINS;

EID: 84984680151     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.744904     Document Type: Article

References (52)

1. Herz, J., and Strickland, D. K. (2001) LRP: a multifunctional scavenger and signaling receptor. J. Clin. Invest. 108, 779-784
2. Lillis, A. P., Van Duyn, L. B., Murphy-Ullrich, J. E., and Strickland, D. K. (2008) LDL receptor-related protein 1: unique tissue-specific functions revealed by selective gene knockout studies. Physiol. Rev. 88, 887-918
3. Mantuano, E., Brifault, C, and Lam., M. S., Azmoon, P., Gilder, A. S., and Gonias, S. L. (2016) LDL receptor-related protein-1 regulates NFκB and microRNA-155 in macrophages to control the inflammatory response. Proc. Natl. Acad. Sci. U.S.A. 113, 1369-1374
4. Ashcom, J. D., and Tiller., S. E., Dickerson, K., Cravens, J. L., and Argraves., W. S., and Strickland, D. K. (1990) The human α2-macroglobulin receptor: identification of a 420-kD cell surface glycoprotein specific for the activated conformation of α2-macroglobulin. J. Cell Biol. 110, 1041-1048
5. May, P., Herz, J., and Bock, H. H. (2005) Molecular mechanisms of lipoprotein receptor signalling. Cell. Mol. Life Sci. 62, 2325-2338
6. Boucher, P., and Herz, J. (2011) Signaling through LRP1: Protection from atherosclerosis and beyond. Biochem. Pharmacol. 81, 1-5
7. Hahn-Dantona, E., Ruiz, J. F., Bornstein, P., and Strickland, D. K. (2001) The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism. J. Biol. Chem. 276, 15498-15503
8. Rozanov, D. V., Hahn-Dantona, E., Strickland, D. K., and Strongin, A. Y. (2004) The low density lipoprotein receptor-related protein LRP is regulated by membrane type-1 matrix metalloproteinase (MT1-MMP) proteolysis in malignant cells. J. Biol. Chem. 279, 4260-4268
9. Yang, Z., and Strickland., D. K., and Bornstein, P. (2001) Extracellular MMP2 levels are regulated by the LRP scavenger receptor and thrombospondin 2. J. Biol. Chem. 276, 8403-8408
10. Yamamoto, K., Owen, K., Parker, A. E., and Scilabra., S. D., Dudhia, J., Strickland, D. K., Troeberg, L., and Nagase, H. (2014) Low density lipoprotein receptor-related protein 1 (LRP1)-mediated endocytic clearance of a disintegrin and metalloproteinase with thrombospondin motifs-4 (ADAMTS-4): functional differences of non-catalytic domains of ADAMTS-4 and ADAMTS-5 in LRP1 binding. J. Biol. Chem. 289, 6462-6474
11. Muratoglu, S. C., Belgrave, S., Hampton, B., Migliorini, M., Coksaygan, T., Chen, L., Mikhailenko, I., and Strickland, D. K. (2013) LRP1 protects the vasculature by regulating levels of connective tissue growth factor and HtrA1. Arterioscler. Thromb. Vasc. Biol. 33, 2137-2146
12. Herz, J., and Couthier., D. E., and Hammer, R. E. (1993) Correction: LDL receptor-related protein internalizes and degrades uPA-PAI-1 complexes and is essential for embryo implantation. Cell. 73, 428
13. Nakajima, C, Haffner, P., Goerke, S. M., Zurhove, K., Adelmann, G., Frotscher, M., Herz, J., and Bock., H. H., and May, P. (2014) The lipoprotein receptor LRP1 modulates sphingosine-1-phosphate signaling and is essential for vascular development. Development 141, 4513-4525
14. Boucher, P., Gotthardt, M., Li, W. P., and Anderson., R. G., and Herz, J. (2003) LRP: Role in vascular wall integrity and protection from atherosclerosis. Science 300, 329-332
15. Basford, J. E., and Moore., Z. W., Zhou, L., Herz, J., and Hui, D. Y. (2009) Smooth muscle LDL receptor-related protein-1 inactivation reduces vascular reactivity and promotes injury-induced neointima formation. Arterioscler. Thromb. Vasc. Biol. 29, 1772-1778
16. Boucher, P., and Li., W. P., Matz, R. L., Takayama, Y., Auwerx, J., and Anderson., R. G., and Herz, J. (2007) LRP1 functions as an atheroprotective integrator of TGFβ and PDFG signals in the vascular wall: implications for Marfan syndrome. PLoS ONE. 2, e448
17. Strickland, D. K., and Ashcom., J. D., Williams, S., Burgess, W. H, Migliorini, M., and Argraves, W. S. (1990) Sequence identity between the α2-macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J. Biol. Chem. 265, 17401-17404
18. 2-macroglobulin receptor-associated protein. Human homologue of a Heymann nephritis antigen. J. Biol. Chem. 266, 13364-13369
19. 2-macroglobulin receptor/low density lipoprotein receptor-related protein. Multiple regulatory sites for 39-kDa receptor-associated protein. J. Biol. Chem. 267, 9035-9040
20. 2-macroglobulin receptor. J. Biol. Chem. 266, 21232-21238
21. Willnow, T. E., Rohlmann, A., Horton, J., Otani, H., and Braun., J. R., Hammer, R. E., and Herz, J. (1996) RAP, a specialized chaperone, prevents ligand-induced ER retention and degradation of LDL receptor-related endocytic receptors. EMBO J. 15, 2632-2639
22. Willnow, T. E., and 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
23. 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
24. Bu, G., and Geuze., H. J., Strous, G. J., and Schwartz, A. L. (1995) 39-kDa receptor-associated protein is an ER resident protein and molecular chaperone for LDL receptor-related protein. EMBO J. 14, 2269-2280
25. Lee, D., and Walsh., J. D., Mikhailenko, I., Yu, P., Migliorini, M., Wu, Y., Krueger, S., Curtis, J. E., Harris, B., Lockett, S., Blacklow, S. C, Strickland, D. K., and Wang, Y.-X. (2006) RAP uses a histidine switch to regulate its interaction with LRP in the ER and Golgi. Mol. Cell 22, 423-430
26. Bu, G., Rennke, S., and Geuze, H. J. (1997) ERD2 proteins mediate ER retention of the HNEL signal of LRP's receptor-associated protein (RAP). J. Cell Sci. 110, 65-73
27. Obermoeller, L. M., Warshawsky, I., Wardell, M. R., and Bu, G. (1997) Differential functions of triplicated repeats suggest two independent roles for the receptor-associated protein as a molecular chaperone. J. Biol. Chem. 272, 10761-10768
28. Lee, D., and Walsh., J. D., Migliorini, M., Yu, P., Cai, T., and Schwieters., C. D., Krueger, S., Strickland DK, and Wang, Y.-X. (2007) The structure of receptor-associated protein (RAP). Protein Sci. 16, 1628-1640
29. Nielsen, P. R., Ellgaard, L., Etzerodt, M., Thogersen, H. C, and Poulsen, F. M. (1997) The solution structure of the N-terminal domain of α2macroglobulin receptor-associated protein. Proc. Natl. Acad. Sci. U.S.A. 94, 7521-7525
30. Medved, L. V., Migliorini, M., Mikhailenko, I., Barrientos, L. G., Llinás, M., and Strickland, D.K. (1999) Domain organization of the 39-kDa receptorassociated protein. J. Biol. Chem. 274, 717-727
31. Jensen, J. K., Dolmer, K., Schar, C, and Gettins, P. G. (2009) Receptor associated protein (RAP) has two high-affinity binding sites for the low-density lipoprotein receptor-related protein (LRP): consequences for the chaperone functions of RAP. Biochem. J. 421, 273-282
32. Migliorini, M. M., Behre, E. H, Brew, S., Ingham, K. C, and Strickland, D. K. (2003) Allosteric modulation of the ligand binding properties of LRP by the receptor associated protein (RAP) requires critical lysine residues within its carboxyl-terminal domain. J. Biol. Chem. 278, 17986-17992
33. 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
34. Rudenko, G., Henry, L., Henderson, K., Ichtchenko, K., and Brown., M. S., Goldstein, J. L., and Deisenhofer, J. (2002) Structure of the LDL receptor extracellular domain at endosomal pH. Science 298, 2353-2358
35. Yasui, N, Nogi, T., Kitao, T., Nakano, Y., Hattori, M., and Takagi, J. (2007) Structure of a receptor-binding fragment of reelin and mutational analysis reveal a recognition mechanism similar to endocytic receptors. Proc. Natl. Acad. Sci. U.S.A. 104, 9988-9993
36. Verdaguer, N, Fita, I., Reithmayer, M., Moser, R., and Blaas, D. (2004) X-ray structure of a minor group human rhinovirus bound to a fragment of its cellular receptor protein. Nat Struct. Mol. Biol 11, 429-434
37. Jensen, G. A., and Andersen., O. M., Bonvin, A. M., Bjerrum-Bohr, I., Etzerodt, M., Thøgersen, H. C, O'Shea, C, Poulsen, F. M., and Kragelund, B. B. (2006) Binding site structure of one LRP-RAP complex: implications for a common ligand-receptor binding motif. J. Mol. Biol. 362, 700-716
38. Lee, C. J., De Biasio, A., and Beglova, N (2010) Mode of interaction between β2GPI and lipoprotein receptors suggests mutually exclusive binding of β2GPI to the receptors and anionic phospholipids. Structure 18, 366-376
39. Guttman, M., and Prieto., J. H., Handel, T. M., Domaille, P.J., and Komives, E. A. (2010) Structure of the minimal interface between ApoE and LRP. J. Mol. Biol. 398, 306-319
40. Dagil, R., O'Shea, C, Nykjær, A., Bonvin, A. M, and Kragelund, B. B. (2013) Gentamicin binds to the megalin receptor as a competitive inhibitor using the common ligand binding motif of complement type repeats: insight from the NMR structure of the 10th complement type repeat domain alone and in complex with gentamicin. J. Biol. Chem. 288, 4424-4435
41. Andersen, O. M., and Schwarz., F. P., Eisenstein, E., Jacobsen, C., Moestrup, S. K., Etzerodt, M., and Thøgersen, H. C. (2001) Dominant thermodynamic role of the third independent receptor binding site in the receptor-associated protein RAP. Biochemistry 40, 15408-15417
42. Bloem, E., and Ebberink., E. H., van den Biggelaar, M., van der Zwaan, C., Mertens, K., and Meijer, A. B. (2015) A novel chemical footprinting approach identifies critical lysine residues involved in the binding of receptor-associated protein to cluster II of LDL receptor-related protein. Biochem. J. 468, 65-72
43. Dolmer, K., Campos, A., and Gettins, P. G. (2013) Quantitative dissection of the binding contributions of ligand lysines of the receptor-associated protein (RAP) to the low density lipoprotein receptor-related protein (LRP1). J. Biol. Chem. 288, 24081-24090
44. van den Biggelaar, M., Sellink, E., Klein Gebbinck, J. W., Mertens, K., and Meijer, A. B. (2011) A single lysine of the two-lysine recognition motif of the D3 domain of receptor-associated protein is sufficient to mediate en-docytosis by low-density lipoprotein receptor-related protein. Int. J. Biochem. Cell Biol. 43, 431-440
45. 2-macroglobulin receptor low density lipoprotein receptor-related protein. J. Biol. Chem. 271, 12909-12912
46. Arandjelovic, S., and Hall., B. D., and Gonias, S. L. (2005) Mutation of lysine 1370 in full-length human α-macroglobulin blocks binding to the low density lipoprotein receptor-related protein-1. Arch. Biochem. Biophys. 438, 29-35
47. 2-macroglobulin-protein-ase complex is achieved by binding to adjacent receptors. J. Biol. Chem. 266, 14011-14017
48. Mikhailenko, I., and Battey., F. D., Migliorini, M., Ruiz, J. F., Argraves, K., Moayeri, M., and Strickland, D. K. (2001) Recognition of α2-macroglob-ulin by the low density lipoprotein receptor-related protein requires the cooperation of two ligand binding cluster regions. J. Biol. Chem. 276, 39484-39491
49. Xiao, T., and DeCamp., D. L., and Sprang, S. R. (2000) Structure of a rat α(1)-macroglobulin receptor-binding domain dimer. Protein Sci. 9, 1889-1897
50. van den Biggelaar, M., Madsen, J.J., and Faber., J. H., Zuurveld, M. G., van der Zwaan, C, Olsen, O. H., Stennicke, H. R., Mertens, K., and Meijer, A. B. (2015) Factor VIII interacts with the endocytic receptor low-density lipoprotein receptor-related protein 1 via an extended surface comprising "Hot-Spot" lysine residues. J. Biol. Chem. 290, 16463-16476
51. Krauss, G., Riesner, D., and Maass, G. (1976) Mechanism of discrimination between cognate and non-cognate tRNAs by phenylalanyl-tRNA synthetase from yeast. Eur. J. Biochem. 68, 81-93
52. Riesner, D., Pingoud, A., Boehme, D., Peters, F., and Maass, G. (1976) Distinct steps in the specific binding of tRNA to aminoacyl-tRNA synthetase. Temperature-jump studies on the serine-specific system from yeast and the tyrosine-specific system from Escherichia coli. Eur. J. Biochem. 68, 71-80