Minimum FGF2 binding structural requirements of heparin and heparan sulfate oligosaccharides as determined by NMR spectroscopy

Biochemistry

Volumn 47, Issue 52, 2008, Pages 13862-13869

  Guglieri, Sara ^a   Hricovíni, Miloš ^b   Raman, Rahul ^c   Polito, Laura ^d   Torri, Giangiacomo ^a   Casu, Benito ^a   Sasisekharan, Ram ^c   Guerrini, Marco ^a  

^a Istituto di Ricerche Chimiche e Biochimiche G Ronzoni   (Italy)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING MOTIF; BIOCHEMICAL STUDIES; BIOLOGICAL PROCESS; COCRYSTAL STRUCTURE; FIBROBLAST GROWTH FACTOR; FREE STATE; GLYCOSAMINOGLYCANS; HEPARAN SULFATES; NMR SPECTROSCOPY; PROTEIN BINDING; PROTEIN INTERACTION; STRUCTURAL REQUIREMENTS; SULFATE GROUPS; SULFATED POLYSACCHARIDES; TETRASACCHARIDES;

BIOCHEMISTRY; CELL CULTURE; NUCLEAR MAGNETIC RESONANCE; OLIGOSACCHARIDES; POLYSACCHARIDES; PROTEINS; STRUCTURAL ANALYSIS;

NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

ALPHA LEVO IDURONIC ACID; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; HEPARIN AND HEPARAN SULFATE GLYCOSAMINOGLYCANS; IDURONIC ACID; POLYSACCHARIDE; PROTON; TETRASACCHARIDE; TRISACCHARIDE; UNCLASSIFIED DRUG; HEPARAN SULFATE; HEPARIN; OLIGOSACCHARIDE;

ARTICLE; BINDING SITE; BIOCHEMISTRY; CHEMICAL STRUCTURE; CRYSTAL STRUCTURE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION; STRUCTURE ANALYSIS; SULFATION; CHEMISTRY; METABOLISM; STRUCTURE ACTIVITY RELATION;

FIBROBLAST GROWTH FACTOR 2; HEPARIN; HEPARITIN SULFATE; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR STRUCTURE; OLIGOSACCHARIDES; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 58849156045     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi801007p     Document Type: Article

References (54)

1. Conrad, H. E. (1998) Heparin-Binding Proteins, Academic Press, San Diego.
2. Casu, B., and Lindahl, U. (2001) Structure and biological interactions of heparin and heparan sulfate. Adv. Carbohydr. Chem. Biochem. 57, 159-206.
3. Esko, J. D., and Selleck, S. B. (2002) Order out of chaos: Assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435-471.
4. Lindahl, U., Kusche-Gullberg, M., and Kjellén, L. (1998) Regulated diversity of heparan sulfate. J. Biol. Chem. 273, 24979-24982.
5. Tumova, S., Woods, A., and Couchman, J. R. (2000) Heparan sulfate proteoglycans on the cell surface: Versatile coordinators of cellular functions. Int. J. Biochem. Cell Biol. 32, 269-288.
6. Capila, I., and Linhardt, R. J. (2002) Heparin-protein interactions. Angew. Chem., Int. Ed. 41, 391-412.
7. Sasisekharan, R., Raman, R., and Prabhakar, V. (2006) Glycomics approach to structure-function relationships of glycosaminoglycans. Annu. Rev. Biomed. Eng. 8, 181-231.
8. Lin, X. (2004) Functions of heparan sulfate proteoglycans in cell signaling during development. Development 131, 6009-6021.
9. Perrimon, N., and Bernfield, M. (2000) Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404, 725-728.
10. Yayon, A., Klagsbrun, M., Esko, J. D., Leder, P., and Ornitz, D. M. (1991) Cell surface, heparin-like molecules are required for binding basic fibroblast growth factor to its high affinity receptor. Cell 64, 841-848.
11. Venkataraman, C., Raman, R., Sasisekharan, V., and Sasisekharan, R. (1999) Molecular characteristics of fibroblast growth factorfibroblast growth factor receptor-heparin-like glycosaminoglycan complex. Proc. Natl. Acad. Sci. U.S.A. 96, 3658-3663.
12. Sasisekharan, R., Shriver, Z., Venkataraman, G., and Narayanasami, U. (2002) Roles of heparan sulfate glycosaminoglycans in cancer. Nat. Rev. Cancer 2, 521-528.
13. Humphries, D. E., Wong, G. W., Friend, D. S., Gurish, M. F., Qiu, W. T., Huang, C., Sharpe, A. H., and Stevens, R. L. (1999) Heparin is essential, for the storage of specific granule proteases in mast cells. Nature 400, 769-772.
14. Iozzo, R. V., and San Antonio, J. D. (2001) Heparan sulfate proteoglycans: Heavy hitters in the angiogenesis arena. J. Clin. Invest. 108, 349-355.
15. Delehedde, M., Lyon, M., Gallagher, J. T., Rudland, P. S., and Ferning, D. G. (2002) Fibroblast growth factor-2 binds to small heparin-derived oligosaccharides and stimulates a sustained phosphorylation of p42/44 mitogen-activated protein kinase and proliferation of rat mammary fibroblasts. Biochem. J. 366, 235-244.
16. Mohammadi, M., Olsen, S. K., and Ibrahimi, O. A. (2005) Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev. 16, 107-137.
17. Pellegrini, L. (2001) Role of heparan sulfate in fibroblast growth factor signaling: A structural view. Curr. Opin. Struct. Biol. 11, 629-634.
18. Canales, A., Angulo, J., Ojeda, R., Bruix, M., Fayos, R., Lozano, R., Gimenez-Gallego, G., Martin-Lomas, M., Nieto, P. M., and Jimenez-Barbero, J. (2005) Conformational flexibility of a synthetic glycosylaminoglycan bound to a fibroblast growth factor. FGF-1 recognizes both the C-1 (4) and S-2 (0) conformations of a bioactive heparin-like hexasaccharide. J. Am. Chem. Soc. 127, 5778-5779.
19. Canales, A., Lozano, R., Lopez-Mendez, B., Angulo, J., Ojeda, R., Nieto, P. M., Martin-Lomas, M., Gimenez-Gallego, G., and Jimenez-Barbero, J. (2006) Solution NMR structure of a human FGF-1 monomer, activated by a hexasaccharide heparin-analogue. FEBS J. 20, 4116-4121.
20. Coltrini, D., Rusnati, M., Zoppetti, G., Oreste, P., Isacchi, A., Caceia, P., Bergonzoni, L., and Presta, M. (1993) Biochemical bases of the interaction of human fibroblast growth factor with glycosaminoglycans. Eur. J. Biochem. 214, 51-58.
21. Venkataraman, G., Shriver, Z., Davis, J. C., and Sasisekharan, R. (1999) Fibroblast growth factors 1 and 2 are distinct in oligomerization in the presence of heparin-like glycosaminoglycans. Proc. Natl. Acad. Sci. U.S.A. 96, 1892-1897.
22. Coltrini, D., Rusnati, M., Zoppetti, G., Oreste, P., Grazioli, G., Naggi, A., and Presta, M. (1994) Different effects of mucosal, bovine lung and chemically modified heparin on selected biological properties of basic fibroblast growth factor. Biochem. J. 303, 583-590.
23. Mulloy, B., and Forster, M. J. (2000) Conformation and dynamics of heparin and heparan sulfate. Glycobiology 10, 1147-1156.
24. Nieduszynski, I. A. (1985) Connective tissue polysaccharides. In Polysaccharides: Topics in structure and morphology (Atkins, E. D. T., Ed.) pp 107-139, McMillian, London.
25. Casu, B., Choay, J., Ferro, D. R., Gatti, G., Jacquinet, J. G., Petitou, M., Provasoli, A., Ragazzi, M., Sinay, P., and Torri, G. (1986) Controversial glycosaminoglycan conformations. Nature 322, 215-216.
26. Ferro, D. R., Provasoli, A., Ragazzi, M., Casu, B., Torri, G., Bossennec, V., Perly, B., Sinay, P., Petitou, M., and Choay, J. (1990) Conformer populations of L-iduronic acid residues in glycosaminoglycan sequences. Carbohydr. Res. 195, 157-167.
27. Raman, R., Venkataraman, G., Ernst, S., Sasisekharan, V., and Sasisekharan, R. (2003) Structural specificity of heparin binding in the fibroblast growth, factor family of proteins. Proc. Natl. Acad. Sci. U.S.A. 100, 2357-2362.
28. DiGabriele, A. D., Lax, I., Chen, D. I., Svahn, C. M., Jaye, M., Schlessinger, J., and Hendrickson, W. A. (1998) Structure of a heparin-linked biologically active dimer of fibroblast growth factor. Nature 393, 812-817.
29. 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.
30. Kreuger, J., Salmivirta, M., Sturiale, L., Gimenez-Gallego, G., and Lindahl, U. (2001) Sequence analysis of heparan sulfate epitopes with graded affinities for fibroblast growth factors 1 and 2. J. Biol. Chem. 276, 30744-30752.
31. Mikhailov, D., Linhardt, R. J., and Mayo, K. H. (1997) NMR solution conformation of heparin-derived hexasaccharide. Biochem. J. 328, 51-61.
32. Poletti, L., Lay, L., Fleischer, M., Vogel, C., Guerrini, M., Torri, G., and Russo, G. A. (2001) Rational approach to heparin-related fragments. Synthesis of differently sulfated tetrasaccharides as potential ligands toward fibroblast growth factors. Eur. J. Org. Chem. 14, 2727-2734.
33. Guerrini, M., Agulles, T., Bisio, A., Hricovini, M., Lay, L., Naggi, A., Poletti, L., Sturiale, L., Torri, G., and Casu, B. (2002) Minimal heparin/heparan sulfate sequences for binding fibroblast growth factor 1. Biochem. Biophys. Res. Commun. 292, 222-230.
34. Homans, S. W. (1990) A molecular mechanical force field for the conformational analysis of oligosaccharides: Comparison of theoretical and crystal structures of Man-α1,3-Man-β1,4-GlcNAc. Biochemistry 29, 9110-9118.
35. Still, W. C., Tempczyk, A., Hawley, R. C., and Hendrickson, T. (1990) A general treatment of solvation for molecular mechanics. J. Am. Chem. Soc. 112, 6127-6129.
36. Mulloy, B., Forster, M. J., Jones, C., and Davies, D. B. (1993) N.M.R. and molecular-modelling studies of the solution conformation of heparin. Biochem. J. 293, 849-858.
37. Chang, G., Guida, W. C., and Still, W. C. (1989) An internalcoordinate Monte Carlo method for searching conformational space. J Am. Chem. Soc. 111, 4379-4386.
38. Goodman, J. M., and Still, W. C. (1991) An unbounded systematic search of conformational space. J. Comput. Chem. 12, 1110-1117.
39. Cros, S., Petitou, M., Sizun, P., Perez, S., and Imberty, A. (1997) Combined NMR and molecular modeling study of an iduronic acidcontaining trisaccharide related to antithrombotic heparin fragments. Bioorg. Med. Chem. 5, 1301-1309.
40. Ragazzi, M., Ferro, D. R., Perly, B., Sinay, P., Petitou, M., and Choay, J. (1990) Conformation of the pentasaccharide corresponding to the binding site of heparin for antithrombin III. Carbohydr. Res. 195, 169-185.
41. Moseley, H. N., Curto, E. V., and Krishna, N. R. (1995) Complete relaxation and conformational exchange matrix (CORCEMA) analysis of NOESY spectra of interacting systems; two-dimensional transferred NOESY. J. Magn. Reson., Ser. B 108, 243-261.
42. Moy, F. J., Safran, M., Seddon, A. P., Kitchen, D., Bohlen, 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.
43. Ferro, D. R., Provasoli, A., Ragazzi, M., Torri, G., Casu, B., Gatti, G., Jacquinet, J. C., Sinay, P., Petitou, M., and Choay, J. (1986) Evidence for conformational equilibrium of the sulfated L-iduronate residue in heparin and in synthetic mono- and oligosaccharides. J. Am. Chem. Soc. 108, 6773-6778.
44. Hricovini, M., and Bizik, F. (2007) Relationship between structure and three-bond proton-proton coupling constants in glycosaminoglycans. Carbohydr. Res. 342, 779-783.
45. Hricovini, M. (2006) B3LYP/6-311++G** study of structure and spin-spin coupling constant in methyl 2-O-sulfo-α-L-iduronate. Carbohydr. Res. 341, 2575-2580.
46. Guerrini, M., Hricovini, M., and Torri, G. (2007) Interaction of heparins with fibroblast growth factors: Conformational aspects. Curr. Pharm. Des. 13, 2045-2056.
47. Hricovini, M., Guerrini, M., Bisio, A., Torri, G., Petitou, M., and Casu, B. (2001) Conformation of heparin pentasaccharide bound to antithrombin III. Biochem. J. 359, 265-272.
48. Turnbull, J. E., Fernig, D. G., Ke, Y., Wilkinson, M. C., and Gallagher, J. T. (1992) Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J. Biol. Chem. 267, 10337-10341.
49. Wang, F., Kan, M., McKeehan, K., Jang, J. H., Feng, S., and McKeehan, W. L. (1997) A homeo-interaction sequence in the ectodomain of the fibroblast growth factor receptor. J. Biol. Chem. 272 (38), 23887-23895.
50. Maccarana, M., Casu, B., and Lindahl, U. (1993) Minimal sequence in heparin-heparan sulfate required for binding of basic fibroblast growth factor. J. Biol. Chem. 268, 23898-23905.
51. Pye, D. A., Vives, R. R., Hyde, P., and Gallagher, J. T. (2000) Regulation of FGF-1 mitogenic activity by heparan sulfate oligosaccharides is dependent on specific structural features: Differential requirements for the modulation of FGF-1 and FGF-2. Glycobiology 10, 1183-1192.
52. Guimond, S., Maccarana, M., Olvin, B. B., Lindahl, U., and Rapraeger, A. C. (1993) Activating and inhibitory heparin sequences for FGF-2 (basic FGF). J. Biol. Chem. 268, 23906-23914.
53. Faham, S., Linhardt, R. J., and Rees, D. C. (1998) Diversity does make a difference: Fibroblast growth factor-heparin interactions. Curr. Opin. Struct. Biol. 8, 578-586.
54. Dai, Y., Yang, Y., MacLeod, V., Yue, X., Rapraeger, A. C., Shriver, Z., Venkataraman, G., Sasisekharan, R., and Sanderson, R. D. (2005) Hsulf-1 and Hsulf-2 are potent inhibitors of myeloma tumor growth in vivo. J. Biol. Chem. 280, 40066-40073.