Quantitative dissection of the binding contributions of ligand lysines of the receptor-associated protein (RAP) to the low density lipoprotein receptor-related protein (LRP1)

Journal of Biological Chemistry

Volumn 288, Issue 33, 2013, Pages 24081-24090

  Dolmer, Klavs ^a   Campos, Andres ^a   Gettins, Peter G W ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH AFFINITY; HIGH AFFINITY BINDING; LOW DENSITY LIPOPROTEINS; PROTEIN LIGANDS; RECEPTOR-ASSOCIATED PROTEINS;

AMINO ACIDS; LIGANDS;

PROTEINS;

LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LYSINE; PLASMINOGEN ACTIVATOR INHIBITOR 1; RECEPTOR ASSOCIATED PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CALORIMETRY; CONTROLLED STUDY; ENTHALPY; ENTROPY; LIGAND BINDING; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

FLUORESCENCE; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; LIPOPROTEIN RECEPTOR; LIPOPROTEIN-LIKE RECEPTOR (LRP); LOW DENSITY LIPOPROTEIN (LDL); LYSINE; RECEPTOR STRUCTURE-FUNCTION; RECEPTOR-ASSOCIATED PROTEIN; THERMODYNAMICS;

AMINO ACID SEQUENCE; CALORIMETRY; CIRCULAR DICHROISM; FLUORESCENCE; LDL-RECEPTOR RELATED PROTEIN-ASSOCIATED PROTEIN; LIGANDS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; LYSINE; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; OSMOLAR CONCENTRATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS;

EID: 84882326084     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.473728     Document Type: Article

References (26)

1. Herz, J., and Strickland, D. K. (2001) LRP.Amultifunctional scavenger and signaling receptor. J. Clin. Invest. 108, 779-784
2. 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
3. Nielsen, K. L., Holtet, T. L., Etzerodt, M., Moestrup, S. K., Gliemann, J., Sottrup-Jensen, L., and Thogersen, H. C. (1996) Identification of residues in-macroglobulins important for binding to the α2-macroglobulin receptor/ Low density lipoprotein receptor-related protein. J. Biol. Chem. 271, 12909-12912
4. 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
5. Arandjelovic, S., Hall, B. D., and Gonias, S. L. (2005) Mutation of lysine 1370 in full-length human α2-macroglobulin blocks binding to the low density lipoprotein receptor-related protein-1. Arch. Biochem. Biophys. 438, 29-35
6. Sarafanov, A. G., Makogonenko, E. M., Pechik, I. V., Radtke, K.-P., Khrenov, A. V., Ananyeva, N. M., Strickland, D. K., and Saenko, E. L. (2006) Identification of coagulation factor VIII A2 domain residues forming the binding epitope for low-density lipoprotein receptor-related protein. Biochemistry 45, 1829-1840
7. Jensen, G. A., 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
8. Dolmer, K., and Gettins, P. G. (2006) Three complement-like repeats compose the completeα2-macroglobulin binding site in the second ligand binding cluster of the low density lipoprotein receptor-related protein. J. Biol. Chem. 281, 34189-34196
9. Yasui, N., Nogi, T., and Takagi, J. (2010) Structural basis for specific recognition of reelin by its receptors. Structure 18, 320-331
10. 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 endocytosis by low-density lipoprotein receptor-related protein. Int. J. Biochem. Cell Biol. 43, 431-440
11. Guttman, M., 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
12. Gettins, P. G., and Dolmer, K. (2012) A proximal pair of positive charges provides the dominant ligand-binding contribution to complement-like domains from the LRP (low-density lipoprotein receptor-related protein). Biochem. J. 443, 65-73
13. Horn, I. R., van den Berg, B. M., Moestrup, S. K., Pannekoek, H., and van Zonneveld, A. J. (1998) Plasminogen activator inhibitor 1 contains a cryptic high affinity receptor binding site that is exposed upon complex formation with tissue-type plasminogen activator. Thromb. Haemost. 80, 822-828
14. Fisher, C., Beglova, N., and Blacklow, S. C. (2006) Structure of an LDLRRAP complex reveals a general mode for ligand recognition by lipoprotein receptors. Mol. Cell 22, 277-283
15. 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
16. Beglova, N., North, C. L., and Blacklow, S. C. (2001) Backbone dynamics of a module pair from the ligand-binding domain of the LDL receptor. Biochemistry 40, 2808-2815
17. Jensen, J. K., Dolmer, K., Schar, C., and Gettins, P. G. (2009) Receptorassociated protein (RAP) has two high-affinity binding sites for the lowdensity lipoprotein receptor-related protein (LRP). Consequences for the chaperone functions of RAP. Biochem. J. 421, 273-282
18. 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
19. Andersen, O. M., Petersen, H. H., Jacobsen, C., Moestrup, S. K., Etzerodt, M., Andreasen, P. A., and Thøgersen, H. C. (2001) Analysis of a twodomain binding site for the urokinase-type plasminogen activator-plasminogen activator inhibitor-1 complex in low-density-lipoprotein-receptor-related protein. Biochem. J. 357, 289-296
20. Jensen, J. K., Dolmer, K., and Gettins, P. G. (2009) Specificity of binding of the low density lipoprotein receptor-related protein to different conformational states of the clade E serpins plasminogen activator inhibitor-1 and proteinase nexin-1. J. Biol. Chem. 284, 17989-17997
21. Lazic, A., Dolmer, K., Strickland, D. K., and Gettins, P. G. (2006) Dissection of RAP-LRP interactions. Binding of RAP and RAP fragments to complement-like repeats 7 and 8 from ligand binding cluster II of LRP. Arch. Biochem. Biophys. 450, 167-175
22. Guttman, M., and Komives, E. A. (2011) The structure, dynamics, and binding of the LA45 module pair of the low-density lipoprotein receptor suggest an important role for LA4 in ligand release. Biochemistry 50, 11001-11008
23. 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
24. Huang, W., Dolmer, K., and Gettins, P. G. (1999) NMR solution structure of complement-like repeat CR8 from the low density lipoprotein receptorrelated protein. J. Biol. Chem. 274, 14130-14136
25. Dolmer, K., Huang, W., and Gettins, P. G. (2000) NMR solution structure of complement-like repeat CR3 from the low density lipoprotein receptorrelated protein. Evidence for specific binding to the receptor binding domain of human α2-macroglobulin. J. Biol. Chem. 275, 3264-3269
26. Simonovic, M., Dolmer, K., Huang, W., Strickland, D. K., Volz, K., and Gettins, P. G. (2001) Calcium coordination and pH dependence of the calcium affinity of ligand-binding repeat CR7 from the LRP. Comparison with related domains from the LRP and the LDL receptor. Biochemistry 40, 15127-15134