Generation of a potent low density lipoprotein receptor-related protein 1 (LRP1) antagonist by engineering a stable form of the receptor-associated protein (RAP) D3 domain

Journal of Biological Chemistry

Volumn 290, Issue 28, 2015, Pages 17262-17268

  Prasad, Joni M ^a   Migliorini, Mary ^a   Galisteo, Rebeca ^a   Strickland, Dudley K ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; COVALENT BONDS; DISSOCIATION; LIPOPROTEINS; MOLECULAR BIOLOGY; MOLECULES; PROTEINS;

ACIDIC ENVIRONMENT; ENDOPLASMIC RETICULUM; HISTIDINE RESIDUES; INDUCED DISSOCIATION; LOW DENSITY LIPOPROTEIN RECEPTORS; MOLECULAR CHAPERONES; PATHOLOGICAL PROCESS; RECEPTOR-ASSOCIATED PROTEINS;

CELL MEMBRANES;

CHAPERONE; HISTIDINE; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; PROTEIN INHIBITOR; RECEPTOR ASSOCIATED PROTEIN; UNCLASSIFIED DRUG; LOW DENSITY LIPOPROTEIN RECEPTOR; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN ASSOCIATED PROTEIN; LRP1 PROTEIN, HUMAN; LRP1 PROTEIN, MOUSE; PEPTIDE FRAGMENT; PROTEIN BINDING; TUMOR SUPPRESSOR PROTEIN;

ACIDITY; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BIOENGINEERING; CONTROLLED STUDY; DISULFIDE BOND; DRUG STABILITY; DRUG SYNTHESIS; ENDOCYTOSIS; ENDOSOME; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTON TRANSPORT; THERMOSTABILITY; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; PROTEIN ENGINEERING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SITE DIRECTED MUTAGENESIS;

ANIMALS; CELL LINE; HUMANS; HYDROGEN-ION CONCENTRATION; LDL-RECEPTOR RELATED PROTEIN-ASSOCIATED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MICE; MICE, INBRED C57BL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, LDL; TUMOR SUPPRESSOR PROTEINS;

EID: 84940055362     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.660084     Document Type: Article

References (31)

1. Herz, J., and Strickland, D. K. (2001) LRP: a multifunctional scavenger and signaling receptor. J. Clin. Investig. 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. 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
4. Strickland, D. K., 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
5. Strickland, D. K., Ashcom, J. D., Williams, S., Battey, F., Behre, E., McTigue, K., Battey, J. F., and Argraves, W. S. (1991) Primary structure of α2-macroglobulin receptor-associated protein. Human homologue of a Heymann nephritis antigen. J. Biol. Chem. 266, 13364-13369
6. 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/α2-macroglobulin receptor. J. Biol. Chem. 266, 21232-21238
7. Williams, S. E., Ashcom, J. D., Argraves, W. S., and Strickland, D. K. (1992) A novel mechanism for controlling the activity of α2-macroglobulin receptor/low density lipoprotein receptor-related protein. Multiple regulatory sites for 39-kDa receptor-associated protein. J. Biol. Chem. 267, 9035-9040
8. Willnow, T. E., Rohlmann, A., Horton, J., Otani, H., 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
9. 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
10. Lee, D., 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
11. Estrada, K., Fisher, C., and Blacklow, S. C. (2008) Unfolding of the RAP-D3 helical bundle facilitates dissociation of RAP-receptor complexes. Biochemistry 47, 1532-1539
12. Kounnas, M. Z., Argraves, W. S., and Strickland, D. K. (1992) The 39-kDa receptor-associated protein interacts with two members of the low density lipoprotein receptor family, α2-macroglobulin receptor and glycoprotein 330. J. Biol. Chem. 267, 21162-21166
13. Battey, F. D., Gåfvels, M. E., FitzGerald, D. J., Argraves, W. S., Chappell, D. A., Strauss, J. F., 3rd, and Strickland, D. K. (1994) The 39-kDa receptor-associated protein regulates ligand binding by the very low density lipoprotein receptor. J. Biol. Chem. 269, 23268-23273
14. Andersen, O. M., Benhayon, D., Curran, T., and Willnow, T. E. (2003) Differential binding of ligands to the apolipoprotein E receptor 2. Biochemistry 42, 9355-9364
15. Polavarapu, R., Gongora, M. C., Yi, H., Ranganthan, S., Lawrence, D. A., Strickland, D., and Yepes, M. (2007) Tissue-type plasminogen activator-mediated shedding of astrocytic low-density lipoprotein receptor-related protein increases the permeability of the neurovascular unit. Blood 109, 3270-3278
16. Saenko, E. L., Yakhyaev, A. V., Mikhailenko, I., Strickland, D. K., and Sarafanov, A. G. (1999) Role of the low density lipoprotein-related protein receptor in mediation of factor VIII catabolism. J. Biol. Chem. 274, 37685-37692
17. Josephson, N. (2013) The hemophilias and their clinical management. Hematology Am. Soc. Hematol. Educ. Program 2013, 261-267
18. Medved, L. V., Migliorini, M., Mikhailenko, I., Barrientos, L. G., Llinás, M., and Strickland, D. K. (1999) Domain organization of the 39-kDa receptor-associated protein. J. Biol. Chem. 274, 717-727
19. Riddles, P. W., Blakeley, R. L., and Zerner, B. (1983) Reassessment of Ellman's reagent. Methods Enzymol. 91, 49-60
20. Migliorini, M. M., Behre, E. H., Brew, S., Ingham, K. C., and Strickland, D. K. (2003) Allosteric modulation of ligand binding to low density lipoprotein receptor-related protein by the receptor-associated protein requires critical lysine residues within its carboxyl-terminal domain. J. Biol. Chem. 278, 17986-17992
21. Perry, L. J., and Wetzel, R. (1984) Disulfide bond engineered into T4 lysozyme: stabilization of the protein toward thermal inactivation. Science 226, 555-557
22. Sauer, R. T., Hehir, K., Stearman, R. S., Weiss, M. A., Jeitler-Nilsson, A., Suchanek, E. G., and Pabo, C. O. (1986) An engineered intersubunit disulfide enhances the stability and DNA binding of the N-terminal domain of λ repressor. Biochemistry 25, 5992-5998
23. 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
24. Dani, V. S., Ramakrishnan, C., and Varadarajan, R. (2003) MODIP revisited: re-evaluation and refinement of an automated procedure for modeling of disulfide bonds in proteins. Protein Eng. 16, 187-193
25. Rall, S. C., Jr., Ye, P., Bu, G., and Wardell, M. R. (1998) The domain structure of human receptor-associated protein. Protease sensitivity and guanidine HCl denaturation. J. Biol. Chem. 273, 24152-24157
26. Wei, Y., Thyparambil, A. A., and Latour, R. A. (2014) Protein helical structure determination using CD spectroscopy for solutions with strong background absorbance from 190 to 230 nm. Biochim. Biophys. Acta 1844, 2331-2337
27. Yepes, M., Sandkvist, M., Moore, E. G., Bugge, T. H., Strickland, D. K., and Lawrence, D. A. (2003) Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J. Clin. Investig. 112, 1533-1540
28. Bu, G., 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
29. 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
30. Savonen, R., Obermoeller, L. M., Trausch-Azar, J. S., Schwartz, A. L., and Bu, G. (1999) The carboxyl-terminal domain of receptor-associated protein facilitates proper folding and trafficking of the very low density lipoprotein receptor by interaction with the three amino-terminal ligand-binding repeats of the receptor. J. Biol. Chem. 274, 25877-25882
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