Identification of heparin-binding sites in proteins by selective labeling

Molecular and Cellular Proteomics

Volumn 8, Issue 10, 2009, Pages 2256-2265

  Ori, Alessandro ^a   Free, Paul ^a   Courty, José ^b   Wilkinson, Mark C ^a   Fernig, David G ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b Université Paris XII ^*  (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTIN; CARBOHYDRATE BINDING PROTEIN; FIBROBLAST GROWTH FACTOR 2; HEPARAN SULFATE; HEPARIN; LYSINE; N HYDROXYSUCCINIMIDE; PLEIOTROPHIN; THROMBOCYTE FACTOR 4;

ARTICLE; BINDING SITE; BIOTINYLATION; CELL FUNCTION; CHEMICAL MODIFICATION; ENZYME BINDING; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTECTION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN ISOLATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REGULATORY MECHANISM; WESTERN BLOTTING;

ACETATES; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; FIBROBLAST GROWTH FACTOR 2; HEPARAN SULFATE PROTEOGLYCANS; HEPARIN; LYSINE; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SUCCINIMIDES;

EID: 71049175228     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M900031-MCP200     Document Type: Article

References (43)

1. Medeiros, G. F., Mendes, A., Castro, R. A., Bau, E. C., Nader, H. B., and Dietrich, C. P. (2000) Distribution of sulfated glycosaminoglycans in the animal kingdom: widespread occurrence of heparin-like compounds in invertebrates. Biochim. Biophys. Acta 1475, 287-294
2. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037 (Pubitemid 46676065)
3. Rodgers, K. D., San Antonio, J. D., and Jacenko, O. (2008) Heparan sulfate proteoglycans: a GAGgle of skeletal-hematopoietic regulators. Dev. Dyn. 237, 2622-2642
4. Lin, X. (2004) Functions of heparan sulfate proteoglycans in cell signaling during development. Development 131, 6009-6021 (Pubitemid 40123916)
5. Häcker, U., Nybakken, K., and Perrimon, N. (2005) Heparan sulphate proteoglycans: the sweet side of development. Nat. Rev. Mol. Cell Biol. 6, 530-541
6. Bülow, H. E., and Hobert, O. (2006) The molecular diversity of glycosaminoglycans shapes animal development. Annu. Rev. Cell Dev. Biol. 22, 375-407
7. Parish, C. R. (2006) The role of heparan sulphate in inflammation. Nat. Rev. Immunol. 6, 633-643
8. Handel, T. M., Johnson, Z., Crown, S. E., Lau, E. K., and Proudfoot, A. E. (2005) Regulation of protein function by glycosaminoglycans - as exemplified by chemokines. Annu. Rev. Biochem. 74, 385-410
9. Fuster, M. M., and Esko, J. D. (2005) The sweet and sour of cancer: glycans as novel therapeutic targets. Nat. Rev. Cancer 5, 526-542
10. Ori, A., Wilkinson, M. C., and Fernig, D. G. (2008) The heparanome and regulation of cell function: structures, functions and challenges. Front. Biosci. 13, 4309-4338
11. Hileman, R. E., Fromm, J. R., Weiler, J. M., and Linhardt, R. J. (1998) Glycosaminoglycan-protein interactions: definition of consensus sites in glycosaminoglycan binding proteins. BioEssays 20, 156-167 (Pubitemid 28132111)
12. Powell, A. K., Yates, E. A., Femig, D. G., and Turnbull, J. E. (2004) Interactions of heparin/heparan sulfate with proteins: appraisal of structural factors and experimental approaches. Glycobiology 14, 17R-30R
13. Forster, M., and Mulloy, B. (2006) Computational approaches to the identification of heparin-binding sites on the surfaces of proteins. Biochem. Soc. Trans. 34, 431-434
14. Yu, W., and Hill, J. S. (2006) Mapping the heparin-binding domain of human hepatic lipase. Biochem. Biophys. Res. Commun. 343, 659-665
15. Imberty, A., Lortat-Jacob, H., and Pérez, S. (2007) Structural view of glycosaminoglycan-protein interactions. Carbohydr. Res. 342, 430-439
16. Fang, J., Dong, Y., Salamat-Miller, N., and Middaugh, C. R. (2008) DB-PABP: a database of polyanion-binding proteins. Nucleic Acids Res. 36, D303-D306
17. Cardin, A. D., and Weintraub, H. J. (1989) Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9, 21-32 (Pubitemid 19046087)
18. Lortat-Jacob, H., Grosdidier, A., and Imberty, A. (2002) Structural diversity of heparan sulfate binding domains in chemokines. Proc. Natl. Acad. Sci. U.S.A 99, 1229-1234
19. Faham, S., Hileman, R. E., Fromm, J. R., Linhardt, R. J., and Rees, D. C. (1996) Heparin structure and interactions with basic fibroblast growth factor. Science 271, 1116-1120 (Pubitemid 26075225)
20. Jin, L., Abrahams, J. P., Skinner, R., Petitou, M., Pike, R. N., and Carrell, R. W. (1997) The anticoagulant activation of antithrombin by heparin. Proc. Natl. Acad. Sci. U.S.A. 94, 14683-14688
21. Mayo, K. H., Ilyina, E., Roongta, V., Dundas, M., Joseph, J., Lai, C. K., Maione, T., and Daly, T. J. (1995) Heparin binding to platelet factor-4. An NMR and site-directed mutagenesis study: arginine residues are crucial for binding. Biochem. J. 312, 357-365
22. Thompson, L. D., Pantoliano, M. W., and Springer, B. A. (1994) Energetic characterization of the basic fibroblast growth factor-heparin interaction: identification of the heparin binding domain. Biochemistry 33, 3831-3840
23. Kinsella, L., Chen, H. L., Smith, J. A., Rudland, P. S., and Fernig, D. G. (1998) Interactions of putative heparin-binding domains of basic fibroblast growth factor and its receptor, FGFR-1, with heparin using synthetic peptides. Glycoconj. J. 15, 419-422 (Pubitemid 28193051)
24. Chang, J. Y. (1989) Binding of heparin to human antithrombin III activates selective chemical modification at lysine 236. Lys-107, Lys-125, and Lys-136 are situated within the heparin-binding site of antithrombin III. J. Biol. Chem. 264, 3111-3115
25. Duchesne, L., Gentili, D., Comes-Franchini, M., and Fernig, D. G. (2008) Robust ligand shells for biological applications of gold nanoparticles. Langmuir 24, 13572-13580
26. Delbé, J., Vacherot, F., Laaroubi, K., Barritault, D., and Courty, J. (1995) Effect of heparin on bovine epithelial lens cell-proliferation induced by heparin affin regulatory peptide. J. Cell. Physiol. 164, 47-54
27. Heukeshoven, J., and Dernick, R. (1985) Simplified method for silver staining of proteins in polyacrylamide gels and the mechanism of silver staining. Electrophoresis 6, 103-112 (Pubitemid 15148654)
28. Vivès, R. R., Crublet, E., Andrieu, J. P., Gagnon, J., Rousselle, P., and Lortat-Jacob, H. (2004) A novel strategy for defining critical amino acid residues involved in protein/glycosaminoglycan interactions. J. Biol. Chem. 279, 54327-54333
29. Smith, J. S., Miller, B. T., Knock, S. L., and Kurosky, A. (1991) Biotinylated peptides/proteins. I. Determination of stoichiometry of derivatization. Anal. Biochem. 197, 247-253
30. Smith, G. P. (2006) Kinetics of amine modification of proteins. Bioconjug. Chem. 17, 501-506
31. Abello, N., Kerstjens, H. A., Postma, D. S., and Bischoff, R. (2007) Selective acylation of primary amines in peptides and proteins. J. Proteome Res. 6, 4770-4776
32. Kim, J. Y., Kim, K. W., Kwon, H. J., Lee, D. W., and Yoo, J. S. (2002) Probing lysine acetylation with a modification-specific marker ion using high-performance liquid chromatography/electrospray-mass spectrometry with collision-induced dissociation. Anal. Chem. 74, 5443-5449
33. Kilpelainen, I., Kaksonen, M., Kinnunen, T., Avikainen, H., Fath, M., Linhardt, R. J., Raulo, E., and Rauvala, H. (2000) Heparin-binding growth-associated molecule contains two heparin-binding beta-sheet domains that are homologous to the thrombospondin type I repeat. J. Biol. Chem. 275, 13564-13570
34. Zhang, J. D., Cousens, L. S., Barr, P. J., and Sprang, S. R. (1991) Three-dimensional structure of human basic fibroblast growth factor, a structural homolog of interleukin 1 beta. Proc. Natl. Acad. Sci. U.S.A. 88, 3446-3450
35. Li, L. Y., Safran, M., Aviezer, D., Böhlen, P., Seddon, A. P., and Yayon, A. (1994) Diminished heparin binding of a basic fibroblast growth factor mutant is associated with reduced receptor binding, mitogenesis, plasminogen activator induction, and in vitro angiogenesis. Biochemistry 33, 10999-11007 (Pubitemid 24296355)
36. Baird, A., Schubert, D., Ling, N., and Guillemin, R. (1988) Receptor- and heparin-binding domains of basic fibroblast growth factor. Proc. Natl. Acad. Sci. U.S.A. 85, 2324-2328
37. Moy, F. J., Safran, M., Seddon, A. P., Kitchen, D., Böhlen, P., Aviezer, D., Yayon, A., and Powers, R. (1997) Properly oriented heparin-decasaccharide-induced dimers are the biologically active form of basic fibroblast growth factor. Biochemistry 36, 4782-4791 (Pubitemid 27180959)
38. Hamma-Kourbali, Y., Bernard-Pierrot, I., Herault, M., Dalle, S., Caruelle, D., Milhiet, P. E., Fernig, D. G., Delbé, J., and Courty, J. (2008) Inhibition of the mitogenic, angiogenic and tumorigenic activities of pleiotrophin by a synthetic peptide corresponding to its C-thrombospondin repeat-I domain. J. Cell. Physiol. 214, 250-259
39. Seno, M., Sasada, R., Kurokawa, T., and Igarashi, K. (1990) Carboxylterminal structure of basic fibroblast growth factor significantly contributes to its affinity for heparin. Eur. J. Biochem. 188, 239-245
40. Springer, B. A., Pantoliano, M. W., Barbera, F. A., Gunyuzlu, P. L., Thompson, L. D., Herblin, W. F., Rosenfeld, S. A., and Book, G. W. (1994) Identification and concerted function of two receptor binding surfaces on basic fibroblast growth factor required for mitogenesis. J. Biol. Chem. 269, 26879-26884
41. Moy, F. J., Seddon, A. P., Campbell, E. B., Böhlen, P., and Powers, R. (1995) 1H, 15N, 13C and 13CO assignments and secondary structure determination of basic fibroblast growth factor using 3D heteronuclear NMR spectroscopy. J. Biomol. NMR 6, 245-254
42. Crublet, E., Andrieu, J. P., Vivès, R. R., and Lortat-Jacob, H. (2008) The HIV-1 envelope glycoprotein gp120 features four heparan sulfate binding domains, including the co-receptor binding site. J. Biol. Chem. 283, 15193-15200
43. Zhang, Q., Crosland, E., and Fabris, D. (2008) Nested Arg-specific bifunctional crosslinkers for MS-based structural analysis of proteins and protein assemblies. Anal. Chim. Acta 627, 117-128