Solution structure of the ligand binding domain of the fibroblast growth factor receptor: Role of heparin in the activation of the receptor

Biochemistry

Volumn 44, Issue 48, 2005, Pages 15787-15798

  Hung, Kuo Wei ^b   Kumar, Thallapuranam Krishnaswamy S ^a   Kathir, Karuppanan Muthusamy ^a   Xu, Ping ^c   Ni, Feng ^c   Ji, Hsiang Hui ^b   Chen, Mei Chi ^b   Yang, Chu Chi ^b   Lin, Fu Pang ^e   Chiu, Ing Ming ^d   Yu, Chin ^a,b  

^a UNIVERSITY OF ARKANSAS   (United States)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d OHIO STATE UNIVERSITY   (United States)

^e NATIONAL TAIWAN OCEAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CALORIMETRY; GROWTH KINETICS; NUCLEAR MAGNETIC RESONANCE; SEDIMENTATION; SOLUTIONS; SUGAR (SUCROSE); SULFUR COMPOUNDS; THREE DIMENSIONAL; TITRATION;

CONFORMATIONAL CHANGES; FIBROBLAST GROWTH FACTOR RECEPTORS (FGFR); SUCROSE OCTASULFATE (SOS); THREE-DIMENSIONSL SOLUTION STRUCTURE;

MOLECULAR STRUCTURE;

FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR RECEPTOR; HEPARIN; MONOMER; SUCROSE; SUCROSE OCTASULFATE; SULFATE; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; BINDING AFFINITY; BINDING SITE; COMPARATIVE STUDY; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; GEL PERMEATION CHROMATOGRAPHY; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; MOLECULAR STABILITY; NITROGEN NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; RECEPTOR UPREGULATION; SEDIMENTATION RATE; SIGNAL TRANSDUCTION;

BINDING SITES; ELECTRON SPIN RESONANCE SPECTROSCOPY; HEPARIN; HUMANS; LIGANDS; MODELS, MOLECULAR; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, FIBROBLAST GROWTH FACTOR; SUCROSE;

EID: 28544449351     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi051030n     Document Type: Article

References (48)

1. Lindner, V., and Maciag, T. (2001) The putative convergent and divergent natures of angiogenesis and arteriogenesis, Circ. Res. 89, 747-749.
2. Angulo, J., Ojeda, R., de Paz, J. L., Lucas, R., Nieto, P. M., Lozano, R. M., Redondo-Horcajo, M., Gimenez-Gallego, G., and Martin-Lomas, M. (2004) The activation of fibroblast growth factors (FGFs) by glycosaminoglycans: Influence of the sulfation pattern on the biological activity of FGF-1, ChemBioChem 5, 55-61.
3. Itoh, N., and Ornitz, D. M. (2004) Evolution of the Fgf and Fgfr gene families, Trends Genet. 20, 563-569.
4. Schlessinger, J. (2004) Common and distinct elements in cellular signaling via EGF and FGF receptors, Science 306, 1506-1507.
5. Arunkumar, A. I., Srisailam, S., Kumar, T. K., Kathir, K. M., Chi, Y. H., Wang, H. M., Chang, G. G., Chiu, I., and Yu, C. (2002) Structure and stability of an acidic fibroblast growth factor from Notophthalmus viridescens, J. Biol. Chem. 277, 46424-46432.
6. Ibrahimi, O. A., Zhang, F., Hrstka, S. C., Mohammadi, M., and Linhardt, R. J. (2004) Kinetic model for FGF, FGFR, and proteoglycan signal transduction complex assembly, Biochemistry 43, 4724-4730.
7. Sher, I., Yeh, B. K., Mohammadi, M., Adir, N., and Ron, D. (2003) Structure-based mutational analyses in FGF7 identify new residues involved in specific interaction with FGFR2IIIb, FEBS Lett. 552, 150-154.
8. Robson-Dixon, N. D., and Garcia-Blanco, M. A. (2004) MAZ elements alter transcription elongation and silencing of the fibroblast growth factor receptor 2 exon IIIb, J. Biol. Chem. 279, 29075-29084.
9. Yeh, B. K., Igarashi, M., Eliseenkova, A. V., Plotnikov, A. N., Sher, I., Ron, D., Aaronson, S. A., and Mohammadi, M. (2003) Structural basis by which alternative splicing confers specificity in fibroblast growth factor receptors, Proc. Natl. Acad. Sci. U.S.A. 100, 2266-2271.
10. Olsen, S. K., Ibrahimi, O. A., Raucci, A., Zhang, F., Eliseenkova, A. V., Yayon, A., Basilico, C., Linhardt, R. J., Schlessinger, J., and Mohammadi, M. (2004) Insights into the molecular basis for fibroblast growth factor receptor autoinhibition and ligand-binding promiscuity, Proc. Natl. Acad. Sci. U.S.A. 101, 935-940.
11. Chellaiah, A., Yuan, W., Chellaiah, M., and Ornitz, D. M. (1999) Mapping ligand binding domains in chimeric fibroblast growth factor receptor molecules. Multiple regions determine ligand binding specificity, J. Biol. Chem. 274, 34785-34794.
12. Wang, F., McKeehan, K., Yu, C., and McKeehan, W. L. (2002) Fibroblast growth factor receptor 1 phosphotyrosine 766: Molecular target for prevention of progression of prostate tumors to malignancy, Cancer Res. 62, 1898-1903.
13. Hung, K. W., Kumar, T. K. S., Chi, Y. H., Chiu, I. M., and Yu, C. (2004) Molecular cloning, overexpression, and characterization of the ligand-binding D2 domain of fibroblast growth factor receptor, Biochem. Biophys. Res. Commun. 317, 253-258.
14. Plotnikov, A. N., Schlessinger, J., Hubbard, S. R., and Mohammadi, M. (1999) Structural basis for FGF receptor dimerization and activation, Cell 98, 641-650.
15. Yeh, B. K., Eliseenkova, A. V., Plotnikov, A. N., Green, D., Pinnell, J., Polat, T., Gritli-Linde, A., Linhardt, R. J., and Mohammadi, M. (2002) Structural basis for activation of fibroblast growth factor signaling by sucrose octasulfate, Mol. Cell. Biol. 22, 7184-7192.
16. 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.
17. Harmer, N. J., Ilag, L. L., Mulloy, B., Pellegrini, L., Robinson, C. V., and Blundell, T. L. (2004) Towards a resolution of the stoichiometry of the fibroblast growth factor (FGF)-FGF receptor-heparin complex, J. Mol. Biol. 339, 821-834.
18. Plotnikov, A. N., Hubbard, S. R., Schlessinger, J., and Mohammadi, M. (2000) Crystal structures of two FGF-FGFR complexes reveal the determinants of ligand-receptor specificity, Cell 101, 413-424.
19. Schlessinger, J., Plotnikov, A. N., Ibrahimi, O. A., Eliseenkova, A. V., Yeh, B. K., Yayon, A., Linhardt, R. J., and Mohammadi, M. (2000) Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization, Mol. Cell 6, 743-750.
20. Stauber, D. J., DiGabriele, A. D., and Hendrickson, W. A. (2000) Structural interactions of fibroblast growth factor receptor with its ligands, Proc. Natl. Acad. Sci. U.S.A. 97, 49-54.
21. Pellegrini, L., Burke, D. F., von Delft, F., Mulloy, B., and Blundell, T. L. (2000) Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin, Nature 407, 1029-1034.
22. Pellegrini, L. (2001) Role of heparan sulfate in fibroblast growth factor signalling: A structural view, Curr. Opin. Struct. Biol. 11, 629-634.
23. Sasisekharan, R., Ernst, S., and Venkataraman, G. (1997) On the regulation of fibroblast growth factor activity by heparin-like glycosaminoglycans, Angiogenesis 1, 45-54.
24. Ashikari-Hada, S., Habuchi, H., Kariya, Y., Itoh, N., Reddi, A. H., and Kimata, K. (2004) Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library, J. Biol. Chem. 279, 12346-12354.
25. Arunkumar, A. I., Kumar, T. K., Kathir, K. M., Srisailam, S., Wang, H. M., Leena, P. S., Chi, Y. H., Chen, H. C., Wu, C. H., Wu, R. T., Chang, G. G., Chiu, I. M., and Yu, C. (2002) Oligomerization of acidic fibroblast growth factor is not a prerequisite for its cell proliferation activity, Protein Sci. 11, 1050-1061.
26. Prakash, V., and Timasheff, S. N. (1985) Vincristine-induced self-association of calf brain tubulin, Biochemistry 24, 5004-5010.
27. Noe, V., Willems, J., Vandekerchlove, J., Roy, F. V., Bryoneel, E., and Mareel, M. (1999) Inhibition of adhesion and induction of epithelial cell invasion by HAV-containing E-cadherin-specific peptides, J. Cell Sci. 112, 127-135.
28. Hajduk, P. J., Meadows, R. P., and Fesik, S. W. (1999) NMR-based screening in drug discovery, Q. Rev. Biophys. 32, 211-240.
29. de Paz, J. L., Angulo, J., Lassaletta, J. M., Nieto, P. M., Redondo-Horcajo, M., Lozano, R. M., Gimenez-Gallego, G., and Martin-Lomas, M. (2001) The activation of fibroblast growth factors by heparin: Synthesis, structure, and biological activity of heparin-like oligosaccharides, ChemBioChem 2, 673-685.
30. Wu, Z. L., Zhang, L., Yabe, T., Kuberan, B., Beeler, D. L., Love, A., and Rosenberg, R. D. (2003) The involvement of heparan sulfate (HS) in FGF1/HS/FGFR1 signaling complex, J. Biol. Chem. 278, 17121-17129.
31. Roghani, M., Mansukhani, A., Dell'Era, P., Bellosta, P., Basilico, C., Rifkin, D. B., and Moscatelli, D. (1994) Heparin increases the affinity of basic fibroblast growth factor for its receptor but is not required for binding, J. Biol. Chem. 269, 3976-3984.
32. Delehedde, M., Seve, M., Sergeant, N., Wartelle, I., Lyon, M., Rudland, P. S., and Fernig, D. G. (2000) Fibroblast growth factor-2 stimulation of p42/44MAPK phosphorylation and IκB degradation is regulated by heparan sulfate/heparin in rat mammary fibroblasts, J. Biol. Chem. 275, 33905-33910.
33. Shireman, P. K., Xue, L., Maddox, E., Burgess, W. H., and Greisler, H. P. (2000) The S130K fibroblast growth factor-1 mutant induces heparin-independent proliferation and is resistant to thrombin degradation in fibrin glue, J. Vasc. Surg. 31, 382-390.
34. Brych, S. R., Dubey, V. K., Bienkiewicz, E., Lee, J., Logan, T. M., and Blaber, M. (2004) Symmetric primary and tertiary structure mutations within a symmetric superfold: A solution, not a constraint, to achieve a foldable polypeptide, J. Mol. Biol. 344, 769-780.
35. Turnbull, W. B., and Daranas, A. H. (2003) On the value of c: Can low affinity systems be studied by isothermal titration calorimetry? J. Am. Chem. Soc. 125, 14859-14866.
36. Zhang, T., and Johansson, J. S. (2003) An isothermal titration calorimetry study on the binding of four volatile general anesthetics to the hydrophobic core of a four-α-helix bundle protein, Biophys. J. 85, 3279-3285.
37. Pantoliano, M. W., Horlick, R. A., Springer, B. A., Van Dyk, D. E., Tobery, T., Wetmore, D. R., Lear, J. D., Nahapetian, A. T., Bradley, J. D., and Sisk, W. P. (1994) Multivalent ligand-receptor binding interactions in the fibroblast growth factor system produce a cooperative growth factor and heparin mechanism for receptor dimerization, Biochemistry 33, 10229-10248.
38. Chi, Y. H., Kumar, T, K. S., Kathir, K. M., Lin, D. H., Zhu, G., Chiu, I. M., and Yu, C. (2002) Investigation of the structural stability of the human acidic fibroblast growth factor by hydrogen-deuterium exchange, Biochemistry 41, 15350-15339.
39. Tugarinov, V., Hwang, P. M., and Kay, L. E. (2004) Nuclear magnetic resonance spectroscopy of high-molecular-weight proteins, Annu. Rev. Biochem. 73, 107-146.
40. Bax, A., and Grzesiek, S. (1993) Methodological advances in protein NMR, Acc. Chem. Res. 26, 130-138.
41. Cornilescu, G., Delaglio, F., and Bax, A. (1999) Protein backbone angle restraints from searching a database for chemical shift and sequence homology, J. Biomol. NMR 13, 289-302.
42. Markley, J. L., Bax, A., Arata, Y., Hilbers, C. W., Kaptein, R., Sykes, B. D., Wright, P. E., and Wuthrich, K. (1998) Recommendations for the presentation of NMR structures of proteins and nucleic acids: IUPAC-IUBMB-IUPAB Inter-Union Task Group on the standardization of data bases of protein and nucleic acid structures determined by NMR spectroscopy, Eur. J. Biochem. 256, 1-15.
43. Goddard, T. D., and Kneller, D. G. (2004) SPARKY 3, University of California, San Francisco.
44. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
45. Laskowski, R. A., Moss, D. S., and Thornton, J. M. (1993) Main-chain bond lengths and bond angles in protein structures, J. Mol. Biol. 231, 1049-1067.
46. Korardi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: A program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-55.
47. 1H coupling constants in the protein backbone, J. Magn. Reson. 140, 259-263.
48. Farrow, N. A., Muhandiram, R., Singer, A. U., Pascal, S. M., Kay, C. M., Gish, G., Shoelson, S. E., Pawson, T., Forman-Kay, J. D., and Kay, L. E. (1994) Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation, Biochemistry 33, 5984-6003.