Solution NMR structure of a human FGF-1 monomer, activated by a hexasaccharide heparin-analogue

FEBS Journal

Volumn 273, Issue 20, 2006, Pages 4716-4727

  Canales, Angeles ^a   Lozano, Rosa ^a   López Méndez, Blanca ^a   Angulo, Jesús ^b   Ojeda, Rafael ^b   Nieto, Pedro M ^b   Martín Lomas, Manuel ^b   Giménez Gallego, Guillermo ^a   Jiménez Barbero, Jesús ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b INSTITUTO DE INVESTIGACIONES QUÍMICAS   (Spain)

Author keywords

Fibroblast growth factor; Heparin like hexasaccharide; Protein carbohydrate complex

Indexed keywords

CARBOHYDRATE DERIVATIVE; FIBROBLAST GROWTH FACTOR 1; GLYCOSAMINOGLYCAN; HEPARIN DERIVATIVE; MONOMER;

ARTICLE; BIOASSAY; CIS TRANS ISOMERISM; DIMERIZATION; MITOGENESIS; MOLECULAR INTERACTION; MOLECULAR WEIGHT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN STRUCTURE; STRUCTURAL PROTEOMICS;

BINDING SITES; CARBOHYDRATE SEQUENCE; DIMERIZATION; FIBROBLAST GROWTH FACTOR 1; HEPARIN; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; OLIGOSACCHARIDES; SOLUTIONS;

EID: 33749412368     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2006.05474.x     Document Type: Article

References (53)

1. Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M & Ornitz DM (2006) Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281, 15694-15700.
2. Itoh N & Ornitz DM (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet 20, 563-569.
3. Olsen SK, Garbi M, Zampieri N, Eliseenkova AV, Ornitz DM, Goldfarb M & Mohammadi M (2003) Fibroblast growth factor (FGF) homologous factors share structural but not functional homology with FGFs. J Biol Chem 278, 34226-34236.
4. White KE, Evans WE, O'Riordan JL, Speer MC, Econs MJ, Lorenz-Depiereux B, Grabowski M, Meitinger T & Strom TM (2000) Autosomal dominant hypophosphataemic rickets is associated with mutations in FGF23. Nat Genet 26, 345-348.
5. Gimenez-Gallego G & Cuevas P (1994) Fibroblast growth factors, proteins with a broad spectrum of biological activities. Neurol Res 16, 313-316.
6. Nishimura T, Nakatake Y, Konishi M & Itoh N (2000) Identification of a novel FGF, FGF-21, preferentially expressed in the liver. Biochim Biophys Acta 1492, 203-206.
7. Powers CJ, McLeskey SW & Wellstein A (2000) Fibroblast growth factors, their receptors and signalling. Endocr Relat Cancer 7, 165-197.
8. Zhu X, Komiya H, Chirino A, Faham S, Fox GM, Arakawa T, Hsu BT & Rees DC (1991) Three-dimensional structures of acidic and basic fibroblast growth factors. Science 251, 90-93.
9. Moy FJ, Seddon AP, Bohlen P & Powers R (1996) High-resolution solution structure of basic fibroblast growth factor determined by multidimensional heteronuclear magnetic resonance spectroscopy. Biochemistry 35, 13552-13561.
10. Ogura K, Nagata K, Hatanaka H, Habuchi H, Kimata K, Tate S, Ravera MW, Jaye M, Schlessinger J & Inagaki F (1999) Solution structure of human acidic fibroblast growth factor and interaction with heparin-derived hexasaccharide. J Biomol NMR 13, 11-24.
11. Bernett MJ, Somasundaram T & Blaber M (2004) An atomic resolution structure for human fibroblast growth factor 1. Proteins 57, 626-634.
12. McLachlan AD (1979) Three-fold structural pattern in the soybean trypsin inhibitor (Kunitz). J Mol Biol 133, 557-563.
13. Arunkumar AI, Srisailam S, Kumar TK, Kathir KM, Chi YH, Wang HM, Chang GG, Chiu I & C (2002) Structure and stability of an acidic fibroblast growth factor from Notophthalmus viridescens. J Biol Chem 277, 46424-46432.
14. Pineda-Lucena A, Jimenez MA, Nieto JL, Santoro J, Rico M & Gimenez-Gallego G (1994) 1H-NMR assignment and solution structure of human acidic fibroblast growth factor activated by inositol hexasulfate. J Mol Biol 242, 81-98.
15. Pineda-Lucena A, Jimeacute;nez MA, Lozano RM, Nieto JL, Santoro J, Rico M & Gimenez-Gallego G (1996) Three-dimensional structure of acidic fibroblast growth factor in solution: effects of binding to a heparin functional analog. J Mol Biol 264, 162-178.
16. 13CO assignments and secondary structure determination of basic fibroblast growth factor using 3D heteronuclear NMR spectroscopy. J Biomol NMR 6, 245-254.
17. Chi YH, Kumar TK, Kathir KM, Lin DH, Zhu G, Chiu IM & Yu C (2002) Investigation of the structural stability of the human acidic fibroblast growth factor by hydrogen-deuterium exchange. Biochemistry 41, 15350-15359.
18. Faham S, Linhardt RJ & Rees DC (1998) Diversity does make a difference: fibroblast growth factor-heparin interactions. Curr Opin Struct Biol 8, 578-586.
19. Capila I & Linhardt RJ (2002) Heparin-Protein interactions. Angew Chem Int Ed Engl 41, 391-412.
20. Conrad HE (1998) Heparin Binding Proteins. Academic Press, San Diego.
21. Ornitz DM, Yayon A, Flanagan JG, Svahn CM, Levi E & Leder P (1992) Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells. Mol Cell Biol 12, 240-247.
22. Yayon A, Klagsbrun M, Esko JD, Leder P & Ornitz DM (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64, 841-848.
23. Rapraeger AC, Krufka A & Olwin BB (1991) Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252, 1705-1708.
24. Venkataraman G, Shriver Z, Davis JC & Sasisekharan R (1999) Fibroblast growth factors 1 and 2 are distinct in oligomerization in the presence of heparin-like glycosaminoglycans. Proc Natl Acad Sci USA 96, 1892-1897.
25. Waksman G & Herr AB (1998) New insights into heparin-induced FGF oligomerization. Nat Struct Biol 5, 527-530.
26. Spivak-Kroizman T, Lemmon MA, Dikic I, Ladbury JE, Pinchasi D, Huang J, Jaye M, Crumley G, Schlessinger J & Lax I (1994) Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell 79, 1015-1024.
27. Faham S, Hileman RE, Fromm JR, Linhardt RJ & Rees DC (1996) Heparin structure and interactions with basic fibroblast growth factor. Science 271, 1116-1120.
28. DiGabriele AD, Lax I, Chen DI, Svahn CM, Jaye M, Schlessinger J & Hendrickson WA (1998) Structure of a heparin-linked biologically active dimer of fibroblast growth factor. Nature 393, 812-817.
29. Stauber DJ, DiGabriele AD & Hendrickson WA (2000) Structural interactions of fibroblast growth factor receptor with its ligands. Proc Natl Acad Sci USA 97, 49-54.
30. Pellegrini L, Burke DF, von Delft F, Mulloy B & Blundell TL (2000) Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature 407, 1029-1034.
31. Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ & 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.
32. Mohammadi M, Olsen SK & Goetz R (2005) A protein canyon in the FGF-FGF receptor dimer selects from an a la carte menu of heparan sulfate motifs. Curr Opin Struct Biol 15, 506-516.
33. Angulo J, Ojeda R, de Paz JL, Lucas R, Nieto PM, Lozano RM, Redondo-Horcajo M, Gimenez-Gallego G & 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.
34. Chi Y, Kumar TK, Chiu IM & C (2000) 15N NMR relaxation studies of free and ligand-bound human acidic fibroblast growth factor. J Biol Chem 275, 39444-39450.
35. Canales A, Angulo J, Ojeda R, Bruix M, Fayos R, Lozano R, Gimenez-Gallego G, Martin-Lomas M, Nieto PM & 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.
36. Canales A, Fayos R, Angulo J, Ojeda R, Martín-Pastor M, Nieto PM, Martín-Lomas M, Giménez-Gallego G & Jiménez Barbero J (2006) Backbone dynamics of a biologically active human FGF-1 monomomer, complexed to a hexasaccharide heparin-analogue, by 15N NMR relaxation methods. J Biomol NMR 35, 225-239.
37. Guntert P, Braun W & Wuthrich K (1991) Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J Mol Biol 217, 517-530.
38. Goodsell DS & Olson AJ (1990) Automated docking of substrates to proteins by simulated annealing. Proteins 8, 195-202.
39. Morris GM, Goodsell DS, Halliday RS, Huey R, Hart WE, Belew RK & Olson AJ (1998) Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. J Comp Chem 19, 1639-1662.
40. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R & Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8, 477-486.
41. Lozano RM, Pineda-Lucena A, Gonzalez C, Angeles Jimenez M, Cuevas P, Redondo-Horcajo M, Sanz JM, Rico M & Gimenez-Gallego G (2000) 1H NMR structural characterization of a nonmitogenic, vasodilatory, ischemia-protector and neuromodulatory acidic fibroblast growth factor. Biochemistry 39, 4982-4993.
42. Pellegrini L (2001) Role of heparan sulfate in fibroblast growth factor signalling: a structural view. Curr Opin Struct Biol 11, 629-634.
43. Ojeda R, Angulo J, Nieto PM & Martín Lomas M (2002) The activation of fibroblast growth factors by heparin: Synthesis and structural study of rationally modified heparin-like oligosaccharides. Can J Chem 80, 917-936.
44. Peränen J, Rikkonen M, Hyvönen M & Kääriä nien L (1996) T7 Vectors with a modified T7lac promoter for expression of proteins in E. coli. Anal Biochem 236, 371-373.
45. Marley J, Lu M & Bracken C (2001) A method for efficient isotopic labeling of recombinant proteins. J Biomol NMR 20, 71-75.
46. Cavanagh J, Fairbrother WJ, PalmerAG III & Skelton NJ (1996) Protein NMR Spectroscopy. Principles and Practice. Academic Press, Inc, San Diego.
47. Guntert P, Mumenthaler C & Wuthrich K (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol 273, 283-298.
48. Scheek RM, van Gunsteren WF & Kaptein R (1989) Molecular dynamics simulation techniques for determination of molecular structures from nuclear magnetic resonance data. Methods Enzymol 177, 204-218.
49. Pearlman DA, Case DA, Caldwell JW, Ross WS, Cheatham TEI, DeBolt S, Ferguson D, Seibel G & Kollman P (1995) AMBER, a package of computer programs for applying molecular mechanics, nomal mode anylisis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comp Phys Commun 91, 1-41.
50. Angulo J, Nieto PM & Martín Lomas M (2003) A molecular dynamics description of the conformational flexibility of the 1-iduronate ring in glycosaminoglycans. Chem Commun 13, 1512-1513.
51. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A & Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81, 3684-3690.
52. Sadir R, Baleux F, Grosdidier A, Imberty A & Lortat-Jacob H (2001) Characterization of the stromal cell-derived factor-1alpha-heparin complex. J Biol Chem 276, 8288-8296.
53. Imberty A, Bettler E, Karababa M, Mazeau K, Petrova P & Pérez S (1999) PIM Parameters, Perspectives in Structural Biology (Vijayan M, Yathindra N & Kolaskar AS, eds) pp. 392-409. Indian Academy of Sciences and Universities Press, Hyderabad, India.