Mapping the binding region on the low density lipoprotein receptor for blood coagulation factor VIII

Journal of Biological Chemistry

Volumn 288, Issue 30, 2013, Pages 22033-22041

  Kurasawa, James H ^a   Shestopal, Svetlana A ^a   Karnaukhova, Elena ^a   Struble, Evi B ^a   Lee, Timothy K ^a   Sarafanov, Andrey G ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD COAGULATION; LOW DENSITY LIPOPROTEIN RECEPTORS; MACROGLOBULIN; RECEPTOR-ASSOCIATED PROTEINS;

BIOCHEMISTRY; BIOLOGY;

BINDING SITES;

ALPHA 2 MACROGLOBULIN; BLOOD CLOTTING FACTOR 8; LOW DENSITY LIPOPROTEIN RECEPTOR; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; TRYPTOPHAN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CATABOLISM; CIRCULAR DICHROISM; CONTROLLED STUDY; IN VITRO STUDY; LIGAND BINDING; LIGHT CHAIN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; SURFACE PLASMON RESONANCE;

BLOOD COAGULATION FACTORS; FACTOR VIII; HEMOPHILIA A; LIPOPROTEIN RECEPTOR; RECEPTOR STRUCTURE-FUNCTION; RECOMBINANT PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; BINDING SITES; BINDING, COMPETITIVE; CIRCULAR DICHROISM; FACTOR VIII; HUMANS; KINETICS; LDL-RECEPTOR RELATED PROTEIN-ASSOCIATED PROTEIN; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; RECEPTORS, LDL; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SURFACE PLASMON RESONANCE;

EID: 84881244787     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.468108     Document Type: Article

References (69)

1. Fay, P. J. (2006) Factor VIII structure and function. Int. J. Hematol. 83, 103-108
2. Bovenschen, N., Mertens, K., Hu, L., Havekes, L. M., and van Vlijmen, B. J. (2005) LDL receptor cooperates with LDL receptor-related protein in regulating plasma levels of coagulation factor VIII in vivo. Blood 106, 906-912
3. Strickland, D. K., Ashcom, J. D., Williams, S., Battey, F., Behre, E., Mc-Tigue, K., Battey, J. F., and Argraves, W. S. (1991) Primary structure of2-macroglobulin receptor-associated protein. Human homologue of a Heymann nephritis antigen. J. Biol. Chem. 266, 13364-13369
4. Lazic, A., Dolmer, K., Strickland, D. K., and Gettins, P. G. (2003) Structural organization of the receptor associated protein. Biochemistry 42, 14913-14920
5. 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
6. Bovenschen, N., Herz, J., Grimbergen, J. M., Lenting, P. J., Havekes, L. M., Mertens, K., and van Vlijmen, B. J. (2003) Elevated plasma factor VIII in a mouse model of low-density lipoprotein receptor-related protein deficiency. Blood 101, 3933-3939
7. Martinelli, N., Girelli, D., Lunghi, B., Pinotti, M., Marchetti, G., Malerba, G., Pignatti, P. F., Corrocher, R., Olivieri, O., and Bernardi, F. (2010) Polymorphisms at LDLR locus may be associated with coronary artery disease through modulation of coagulation factor VIII activity and independently from lipid profile. Blood 116, 5688-5697
8. Mello, T. B., Siqueira, L. H., Montavão, S. A., Ozello, M. C., and Annichino-Bizzacchi, J. M. (2008) Low density lipoprotein receptor-related protein polymorphisms are not risk factors for venous thromboembolism. Thromb. Res. 121, 625-629
9. Pocathikorn, A., Granath, B., Thiry, E., Van Leuven, F., Taylor, R., and Mamotte, C. (2003) Influence of exonic polymorphisms in the gene for LDL receptor-related protein (LRP) on risk of coronary artery disease. Atherosclerosis 168, 115-121
10. Vormittag, R., Bencur, P., Ay, C., Tengler, T., Vukovich, T., Quehenberger, P., Mannhalter, C., and Pabinger, I. (2007) Low-density lipoprotein receptor-related protein 1 polymorphism 663 C3T affects clotting factor VIII activity and increases the risk of venous thromboembolism. J. Thromb. Haemost. 5, 497-502
11. Jeon, H., and Blacklow, S. C. (2005) Structure and physiologic function of the low-density lipoprotein receptor. Annu. Rev. Biochem. 74, 535-562
12. Strickland, D. K., and Ranganathan, S. (2003) Diverse role of LDL receptor-related protein in the clearance of proteases and in signaling. J. Thromb. Haemost. 1, 1663-1670
13. Ananyeva, N. M., Makogonenko, Y. M., Kouiavskaia, D. V., Ruiz, J., Limburg, V., Meijer, A. B., Khrenov, A. V., Shima, M., Strickland, D. K., and Saenko, E. L. (2008) The binding sites for the very low density lipoprotein receptor and low-density lipoprotein receptor-related protein are shared within coagulation factor VIII. Blood Coagul. Fibrinolysis 19, 166-177
14. Ananyeva, N. M., Makogonenko, Y. M., Sarafanov, A. G., Pechik, I. V., Gorlatova, N., Radtke, K. P., Shima, M., and Saenko, E. L. (2008) Interaction of coagulation factor VIII with members of the low-density lipoprotein receptor family follows common mechanism and involves consensus residues within the A2 binding site 484-509. Blood Coagul. Fibrinolysis 19, 543-555
15. Bovenschen, N., van Dijk, K. W., Havekes, L. M., Mertens, K., and van Vlijmen, B. J. (2004) Clearance of coagulation factor VIII in very lowdensity lipoprotein receptor knockout mice. Br. J. Haematol. 126, 722-725
16. Christensen, E. I., Birn, H., Storm, T., Weyer, K., and Nielsen, R. (2012) Endocytic receptors in the renal proximal tubule. Physiology (Bethesda) 27, 223-236
17. 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
18. 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
19. Daly, N. L., Scanlon, M. J., Djordjevic, J. T., Kroon, P. A., and Smith, R. (1995) Three-dimensional structure of a cysteine-rich repeat from the low-density lipoprotein receptor. Proc. Natl. Acad. Sci. U.S.A. 92, 6334-6338
20. Daly, N. L., Djordjevic, J. T., Kroon, P. A., and Smith, R. (1995) Threedimensional structure of the second cysteine-rich repeat from the human low-density lipoprotein receptor. Biochemistry 34, 14474-14481
21. North, C. L., and Blacklow, S. C. (2000) Solution structure of the sixth LDL-A module of the LDL receptor. Biochemistry 39, 2564-2571
22. 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
23. 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
24. 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
25. 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
26. Yasui, N., Nogi, T., and Takagi, J. (2010) Structural basis for specific recognition of reelin by its receptors. Structure 18, 320-331
27. Fisher, C., Abdul-Aziz, D., and Blacklow, S. C. (2004) A two-module region of the low-density lipoprotein receptor sufficient for formation of complexes with apolipoprotein E ligands. Biochemistry 43, 1037-1044
28. Russell, D. W., Brown, M. S., and Goldstein, J. L. (1989) Different combinations of cysteine-rich repeats mediate binding of low density lipoprotein receptor to two different proteins. J. Biol. Chem. 264, 21682-21688
29. Andersen, O. M., Christensen, L. L., Christensen, P. A., Sørensen, 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
30. 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
31. Meijer, A. B., Rohlena, J., van der Zwaan, C., van Zonneveld, A. J., Boertjes, R. C., Lenting, P. J., and Mertens, K. (2007) Functional duplication of ligand-binding domains within low-density lipoprotein receptor-related protein for interaction with receptor associated protein,2-macroglobulin, factor IXa, and factor VIII. Biochim. Biophys. Acta 1774, 714-722
32. Neels, J. G., van Den Berg, B. 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
33. Lenting, P. J., Neels, J. G., van den Berg, B. M., Clijsters, P. P., Meijerman, D. W., Pannekoek, H., van Mourik, J. A., Mertens, K., and van Zonneveld, A. J. (1999) The light chain of factor VIII comprises a binding site for low density lipoprotein receptor-related protein. J. Biol. Chem. 274, 23734-23739
34. Sarafanov, A. G., Ananyeva, N. M., Shima, M., and Saenko, E. L. (2001) Cell surface heparan sulfate proteoglycans participate in factor VIII catabolism mediated by low density lipoprotein receptor-related protein. J. Biol. Chem. 276, 11970-11979
35. Saenko, E. L., Shima, M., Gilbert, G. E., and Scandella, D. (1996) Slowed release of thrombin-cleaved factor VIII from von Willebrand factor by a monoclonal and a human antibody is a novel mechanism for factor VIII inhibition. J. Biol. Chem. 271, 27424-27431
36. Kurasawa, J. H., Shestopal, S. A., Jha, N. K., Ovanesov, M. V., Lee, T. K., and Sarafanov, A. G. (2013) Insect cell-based expression and characterization of a single-chain variable antibody fragment directed against blood coagulation factor VIII. Protein. Expr. Purif. 88, 201-206
37. Sarafanov, A. G., Makogonenko, E. M., Andersen, O. M., Mikhailenko, I. A., Ananyeva, N. M., Khrenov, A. V., Shima, M., Strickland, D. K., and Saenko, E. L. (2007) Localization of the low-density lipoprotein receptorrelated protein regions involved in binding to the A2 domain of coagulation factor VIII. Thromb. Haemost. 98, 1170-1181
38. Sarafanov, A., and Saenko, E. (2004) High-throughput optimization of protein expression in the baculovirus system based on determination of relative expression efficiency of viral stocks. Anal. Biochem. 328, 98-100
39. Orlando, R. A., Exner, M., Czekay, R. P., Yamazaki, H., Saito, A., Ullrich, R., Kerjaschki, D., and Farquhar, M. G. (1997) Identification of the second cluster of ligand-binding repeats in megalin as a site for receptor-ligand interactions. Proc. Natl. Acad. Sci. U.S.A. 94, 2368-2373
40. Sato, A., Shimada, Y., Herz, J., Yamamoto, T., and Jingami, H. (1999) 39-kDa receptor-associated protein (RAP) facilitates secretion and ligand binding of extracellular region of very-low-density-lipoprotein receptor: implications for a distinct pathway from low-density-lipoprotein receptor. Biochem. J. 341, 377-383
41. Christiansen, M. L., Balling, K. W., Persson, E., Hilden, I., Bagger-Sørensen, A., Sørensen, B. B., Viuff, D., Segel, S., Klausen, N. K., Ezban, M., Lethagen, S., Steenstrup, T. D., and Kjalke, M. (2010) Functional characteristics of N8, a new recombinant FVIII. Haemophilia 16, 878-887
42. Butenas, S., Parhami-Seren, B., Gissel, M. T., Gomperts, E. D., Fass, D. N., and Mann, K. G. (2009) Potency and mass of factor VIII in FVIII products. Haemophilia 15, 63-72
43. Lin, Y., Yang, X., Chevrier, M. C., Craven, S., Barrowcliffe, T. W., Lemieux, R., and Ofosu, F. A. (2004) Relationships between factor VIII:Ag and factor VIII in recombinant and plasma-derived factor VIII concentrates. Haemophilia 10, 459-469
44. Ofosu, F. A., Tse, H., Naqvi, A., Bhakta, H., and Song, Y. (2012) The fraction of recombinant factor VIII:Ag unable to bind von Willebrand factor has no FVIII coagulant activity: studies in vitro. Haemophilia 18, 917-925
45. Pahl, S., Pavlova, A., Driesen, J., Müller, J., Pötzsch, B., and Oldenburg, J. (2013) In vitro characterization of recombinant factor VIII concentrates reveals significant differences in protein content, activity, and thrombin activation profile. Haemophilia 19, 392-398
46. Limburg, V., van der Zwaan, C., Boertjes, R. C., Bovenschen, N., Mertens, K., and Meijer, A. (2005) An antibody fragment against factor VIII that inhibits factor VIII assembly with von Willebrand factor and LDL receptor family members. J. Thromb. Haemost. 3, Suppl. 1, OR162
47. Meijer. A., Limburg, V., van der Zwaan, C., and Mertens, K. (2007) The factor VIII C1 domain contributes to efficient LRP/LDL receptor binding. J. Thromb. Haemost. 5, Suppl. 2, P-M-040
48. Meems, H., Meijer, A. B., Cullinan, D. B., Mertens, K., and Gilbert, G. E. (2009) Factor VIII C1 domain residues Lys 2092 and Phe 2093 contribute to membrane binding and cofactor activity. Blood 114, 3938-3946
49. Bieri, S., Atkins, A. R., Lee, H. T., Winzor, D. J., Smith, R., and Kroon, P. A. (1998) Folding, calcium binding, and structural characterization of a concatemer of the first and second ligand-binding modules of the low-density lipoprotein receptor. Biochemistry 37, 10994-11002
50. Atkins, A. R., Brereton, I. M., Kroon, P. A., Lee, H. T., and Smith, R. (1998) Calcium is essential for the structural integrity of the cysteine-rich, ligandbinding repeat of the low-density lipoprotein receptor. Biochemistry 37, 1662-1670
51. 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
52. 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
53. 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 human2-macroglobulin. J. Biol. Chem. 275, 3264-3269
54. Guo, Y., Yu, X., Rihani, K., Wang, Q. Y., and Rong, L. (2004) The role of a conserved acidic residue in calcium-dependent protein folding for a low density lipoprotein (LDL)-A module: implications in structure and function for the LDL receptor superfamily. J. Biol. Chem. 279, 16629-16637
55. 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
56. 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
57. Medh, J. D., Fry, G. L., Bowen, S. L., Pladet, M. W., Strickland, D. K., and Chappell, D. A. (1995) The 39-kDa receptor-associated protein modulates lipoprotein catabolism by binding to LDL receptors. J. Biol. Chem. 270, 536-540
58. Strickland, D. K., Ashcom, J. D., Williams, S., Burgess, W. H., Migliorini, M., and Argraves, W. S. (1990) Sequence identity between the2-macroglobulin receptor and low density lipoprotein receptor-related protein suggests that this molecule is a multifunctional receptor. J. Biol. Chem. 265, 17401-17404
59. Battey, F. D., GAfvels, M. E., FitzGerald, D. J., Argraves, W. S., Chappell, D. A., Strauss, J. F., 3rd, and Strickland, D. K. (1994) The 39-kDa receptorassociated protein regulates ligand binding by the very low density lipoprotein receptor. J. Biol. Chem. 269, 23268-23273
60. 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,2-macroglobulin receptor and glycoprotein 330. J. Biol. Chem. 267, 21162-21166
61. Dolmer, K., and Gettins, P. G. (2006) Three complement-like repeats compose the complete2-macroglobulin binding site in the second ligand binding cluster of the low density lipoprotein receptor-related protein. J. Biol. Chem. 281, 34189-34196
62. Esser, V., Limbird, L. E., Brown, M. S., Goldstein, J. L., and Russell, D. W. (1988) Mutational analysis of the ligand binding domain of the low density lipoprotein receptor. J. Biol. Chem. 263, 13282-13290
63. Zhang, D. W., Garuti, R., Tang, W. J., Cohen, J. C., and Hobbs, H. H. (2008) Structural requirements for PCSK9-mediated degradation of the low-density lipoprotein receptor. Proc. Natl. Acad. Sci. U.S.A. 105, 13045-13050
64. Lenting, P. J., Donath, M. J., van Mourik, J. A., and Mertens, K. (1994) Identification of a binding site for blood coagulation factor IXa on the light chain of human factor VIII. J. Biol. Chem. 269, 7150-7155
65. Bovenschen, N., Boertjes, R. C., van Stempvoort, G., Voorberg, J., Lenting, P. J., Meijer, A. B., and Mertens, K. (2003) Low density lipoprotein receptor-related protein and factor IXa share structural requirements for binding to the A3 domain of coagulation factor VIII. J. Biol. Chem. 278, 9370-9377
66. Bovenschen, N., van Stempvoort, G., Voorberg, J., Mertens, K., and Meijer, A. B. (2006) Proteolytic cleavage of factor VIII heavy chain is required to expose the binding-site for low-density lipoprotein receptor-related protein within the A2 domain. J. Thromb. Haemost. 4, 1487-1493
67. Meems, H., van den Biggelaar, M., Rondaij, M., van der Zwaan, C., Mertens, K., and Meijer, A. B. (2011) C1 domain residues Lys 2092 and Phe 2093 are of major importance for the endocytic uptake of coagulation factor VIII. Int. J. Biochem. Cell Biol. 43, 1114-1121
68. van den Biggelaar, M., van der Zwaan, C., Mertens, K., and Meijer, A. (2011) Low density lipoprotein receptor-related protein (LRP) cluster II interacts with the factor VIII light chain via an extended surface comprising multiple lysine residues. J. Thromb. Haemost. 9, Suppl. 2, 821
69. van den Brink, E. N., Turenhout, E. A., Bovenschen, N., Heijnen, B. G., Mertens, K., Peters, M., and Voorberg, J. (2001) Multiple VH genes are used to assemble human antibodies directed toward the A3-C1 domains of factor VIII. Blood 97, 966-972