Residual dipolar coupling investigation of a heparin tetrasaccharide confirms the limited effect of flexibility of the iduronic acid on the molecular shape of heparin

Glycobiology

Volumn 19, Issue 11, 2009, Pages 1185-1196

  Jin, Lan ^a,d   Hricovíni, Miloš ^b   Deakin, Jon A ^c   Lyon, Malcolm ^c   Uhrín, Dušan ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d SHANDONG UNIVERSITY   (China)

Author keywords

Conformation; Heparin; Iduronic acid; NMR spectroscopy; Residual dipolar couplings

Indexed keywords

DISACCHARIDE; GLYCOSAMINOGLYCAN; HEPARIN; HEXOSAMINE; IDURONIC ACID; TETRASACCHARIDE;

AB INITIO CALCULATION; ARTICLE; BINDING AFFINITY; CARBOHYDRATE ANALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CROSS LINKING; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN CARBOHYDRATE INTERACTION; PROTEIN CLEAVAGE; PROTON TRANSPORT; RESIDUAL DIPOLAR COUPLING; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

CARBOHYDRATE CONFORMATION; CARBON; COMPUTER SIMULATION; HEPARIN; IDURONIC ACID; MODELS, CHEMICAL; OLIGOSACCHARIDES; PROTONS; QUANTUM THEORY;

EID: 70349994805     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwp105     Document Type: Article

References (59)

1. Adeyeye J, Azurmendi HF, Stroop CJM, Sozhamannan S, Williams AL, Adetumbi AM, Johnson JA, Bush CA. 2003. Conformation of the hexasaccharide repeating subunit from the Vibrio cholerae O139 capsular polysaccharide. Biochemistry. 42:3979-3988.
2. Almond A, Axelsen JB. 2002. Physical interpretation of residual dipolar couplings in neutral aligned media. J Am Chem Soc. 124:9986-9987.
3. Almond A, Bunkenborg J, Franch T, Gotfredsen CH, Duus JO. 2001. Comparison of aqueous molecular dynamics with NMR relaxation and residual dipolar couplings favors internal motion in a mannose oligosaccharide. J Am Chem Soc. 123:4792-4802.
4. 2+: A model study with a synthetic heparin-like hexasaccharide. Isr J Chem. 40:289-299.
5. Azurmendi HF, Bush CA. 2002. Tracking alignment from the moment of inertia tensor (TRAMITE) of biomolecules in neutral dilute liquid crystal solutions. J Am Chem Soc. 124:2426-2427.
6. 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.
7. Capila I, Linhardt RJ. 2002. Heparin-protein interactions. Angew Chem Int Ed. 41:391-412.
8. Case DA, Pearlman DA, Caldwell JW, Cheatham TE III, Wang J, Ross WS, Simmerling CL, Darden TA, Merz KM, Stanton RV, et al. 2002. AMBER 7 San Francisco: University of California.
9. Casu B, Lindahl U. 2001. Structure and biological interactions of heparin and heparan sulfate. Adv Carbohydr Chem Biochem. 57:159-206.
10. Catlow KR, Deakin JA, Wei Z, Delehedde M, Fernig DG, Gherardi E, Gallagher JT, Pavao MSG, Lyon M. 2008. Interactions of hepatocyte growth factor/scatter factor with various glycosaminoglycans reveal an important interplay between the presence of iduronate and sulfate density. J Biol Chem. 283:5235-5248.
11. 2+ interaction: The influence of the O-sulfation pattern on binding. Carbohydr Res. 339:975-983.
12. de Paz JL, Angulo J, Lassaletta JM, Nieto PM, Redondo-Horcajo M, Lozano RM, Gimenez-Gallego G, 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.
13. Ernst S, Venkataraman G, Sasisekharan V, Langer R, Cooney CL, Sasisekharan R. 1998. Pyranose ring flexibility. Mapping of physical data for iduronate in continuous conformational space. J Am Chem Soc 120:2099-2107.
14. Faham S, Hileman RE, Fromm JR, Linhardt RJ, Rees DC. 1996. Heparin structure and interactions with basic fibroblast growth factor. Science. 271:1116-1120.
15. Ferro DR, Provasoli A, Ragazzi M, Casu B, Torri G, Bossennec V, Perly B, Sinay P, Petitou M, Choay J. 1990. Conformer populations of L-iduronic acid residues in glycosaminoglycan sequences. Carbohydr Res. 195:157-167.
16. Ferro DR, Provasoli A, Ragazzi M, Torri G, Casu B, Gatti G, Jacquinet JC, Sinay P, Petitou M, Choay J. 1986. Evidence for conformational equilibrium of the sulfated L-iduronate residue in heparin and in synthetic heparin monosaccharides and oligosaccharides - NMR and force-field studies. J Am Chem Soc. 108:6773-6778.
17. Forster MJ, Mulloy B. 1993. Molecular-dynamics study of iduronate ring conformation. Biopolymers. 33:575-588.
18. Guerrini M, Guglieri S, Beccati D, Torri G, Viskov C, Mourier P. 2006. Conformational transitions induced in heparin octasaccharides by binding with antithrombin III. Biochem J. 399:191-198.
19. Guerrini M, Hricovíni M, Torri G. 2007. Interaction of heparins with fibroblast growth factors: Conformational aspects. Curr Pharm Des. 13:2045-2056.
20. Guglieri S, Hricovíni M, Raman R, Polito L, Torri G, Casu B, Sasisekharan R, Guerrini M. 2008. Minimum FGF2 binding structural requirements of heparin and heparan sulfate oligosaccharides as determined by NMR spectroscopy. Biochemistry. 47:13862-13869.
21. Haasnoot CAG, Deleeuw F, Altona C. 1980. The relationship between protonproton NMR coupling-constants and substituent electronegativities: 1. An empirical generalization of the Karplus equation. Tetrahedron 36:2783-2792.
22. Hricovíni M. 2006. B3LYP/6-311++G** study of structure and spin-spin coupling constant in methyl 2-O-sulfo-alpha-L-iduronate. Carbohydr Res. 341:2575-2580.
23. Hricovíni M, Bízik F. 2007. Relationship between structure and three-bond proton-proton coupling constants in glycosaminoglycans. Carbohydr Res. 342:779-783.
24. Hricovíni M, Guerrini M, Bisio A, Torri G, Petitou M, Casu B. 2001. Conformation of heparin pentasaccharide bound to antithrombin III. Biochem J. 359:265-272.
25. Hricovíni M, Nieto PM, Torri G. 2002. NMR of sulfated oligo- and polysaccharides. In: Jimenéz-Barbero J, Peters T, editors. NMR Spectroscopy of Glycoconjugates. Weinham: Wiley-VCH. p. 325-334.
26. Hricovíni M, Scholtzova E, Bízik F. 2007. B3LYP/6-31 1++G** study of structure and spin-spin coupling constant in heparin disaccharide. Carbohydr Res. 342:1350-1356.
27. Huige CJM, Altona C. 1995. Force-field parameters for sulfates and sulfamates based on ab-initio calculations - Extensions of amber and CHARMM fields. J Comput Chem. 16:56-79.
28. Imberty A, Lortat-Jacob H, Perez S. 2007. Structural view of glycosaminoglycan-protein interactions. Carbohydr Res. 342:430-439.
29. JAGUAR 3.5, Schrodinger, Inc., Portland, 1998.
30. Jia J, Maccarana M, Zhang X, Bespalov M, Lindahl U, Li JP. 2009. Lack of L-iduronic acid in heparan sulfate affects interaction with growth factors and cell signaling. J Biol Chem. 284:15942-15950.
31. Jin L, Barran PE, Deakin JA, Lyon M, Uhrín D. 2005. Conformation of glycosaminoglycans by ion mobility mass spectrometry and molecular modelling. Phys Chem Chem Phys. 7:3464-3471.
32. Jin L, Pham TN, Uhrín D. 2007. Measurement of H-1-H-1 residual dipolar coupling constants for structural studies of medium size molecules. Chemphyschem. 8:1228-1235.
33. Konrat R, Burghardt I, Bodenhausen G. 1991. Coherence transfer in nuclearmagnetic- resonance by selective homonuclear Hartmann-Hahn correlation spectroscopy. J Am Chem Soc. 113:9135-9140.
34. Landersjo C, Hoog C, Maliniak A, Widmalm G. 2000. NMR investigation of a tetrasaccharide using residual dipolar couplings in dilute liquid crystalline media: Effect of the environment. J Phys Chem. B 104:5618-5624.
35. Lee CT, Yang WT, Parr RG. 1988. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron-density. Phys Rev. B 37:785-789.
36. Losonczi JA, Andrec M, Fischer MWF, Prestegard JH. 1999. Order matrix analysis of residual dipolar couplings using singular value decomposition. J Magn Reson. 138:334-342.
37. Lycknert K, Maliniak A, Widmalm G. 2001. Analysis of oligosaccharide conformation by NMR spectroscopy utilizing H-1,H-1 and H-1,C-13 residual dipolar couplings in a dilute liquid crystalline phase. J Phys Chem A 105:5119-5122.
38. Mikhailov D, Linhardt RJ, Mayo KH. 1997. NMR solution conformation of heparin-derived hexasaccharide. Biochem J. 328:51-61.
39. Mikhailov D, Mayo KH, Vlahov IR, Toida T, Pervin A, Linhardt RJ. 1996. NMR solution conformation of heparin-derived tetrasaccharide. Biochem J. 318:93-102.
40. Mulloy B, Forster MJ. 2000. Conformation and dynamics of heparin and heparan sulfate. Glycobiology. 10:1147-1156.
41. Mulloy B, Forster MJ, Jones C, Davies DB. 1993.NMRand molecular-modeling studies of the solution conformation of heparin. Biochem J. 293:849-858.
42. Mulloy B, Linhardt RJ. 2001. Order out of complexity - Protein structures that interact with heparin. Curr Opin Struct Biol. 11:623-628.
43. Neuhaus D, Williamson MP. 2000. The Nuclear Overhauser Effect in Structural and Conformational Analysis. 2nd ed. New York: Willey-VCH.
44. Nieduszynski IA, Gardner KH, Atkins EDT. 1977. Cellulose Chemistry and Technology. ACS Symp. Ser. 2nd ed. Vol. 48. Washington (DC): American Chemical Society. p. 73-80.
45. Pham TN, Hinchley SL, Rankin DWH, Liptaj T, Uhrín D. 2004. Determination of sugar structures in solution from residual dipolar coupling constants: Methodology and application to methyl beta-D-xylopyranoside. J Am Chem Soc. 126:13100-13110.
46. Pham TN, Liptaj T, Barlow PN, Uhrín D. 2002. J-Modulated 1D directed COSY for precise measurement of proton-proton residual dipolar coupling constants of oligosaccharides. Magn Reson Chem. 40:729-732.
47. Pol-Fachin L, Verli H. 2008. Depiction of the forces participating in the 2-Osulfo- alpha-L-iduronic acid conformational preference in heparin sequences in aqueous solutions. Carbohydr Res. 343:1435-1445.
48. Powell AK, Yates EA, Fernig DG, Turnbull JE. 2004. Interactions of heparin/heparan sulfate with proteins: Appraisal of structural factors and epxerimental approaches. Glycobiology. 14:17R-30R.
49. Rabenstein DL, Robert JM, Peng J. 1995. Multinuclear magnetic resonance studies of the interaction of inorganic cations with heparin. Carbohydr Res. 278:239-256.
50. Robinson PT, Pham TN, Uhrín D. 2004. In phase selective excitation of overlapping multiplets by gradient-enhanced chemical shift selective filters. J Magn Reson. 170:97-103.
51. Ruckert M, Otting G. 2000. Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J Am Chem Soc. 122:7793-7797.
52. Saupe A. 1968. Recent results in field of liquid crystals. Angew Chem Int Ed. 7:97-118.
53. Silipo A, Zhang ZQ, Canada FJ, Molinaro A, Linhardt RJ, Jimenez-Barbero J. 2008. Conformational analysis of a dermatan sulfate-derived tetrasaccharide by NMR, molecular modeling, and residual dipolar couplings. Chembiochem. 9:240-252.
54. Tjandra N, Bax A. 1997. Direct measurement of distances and angles in biomolecules by NMR in a dilute liquid crystalline medium. Science 278:1111-1114.
55. Tian F, Al-Hashimi HM, Craighead JL, Prestegard JH. 2001. Conformational analysis of a flexible oligosaccharide using residual dipolar couplings. J Am Chem Soc. 123:485-492.
56. Tvaroška I,HricovíniM, Petráková E. 1989. An attempt to derive a newKarplustype equation of vicinal proton carbon coupling-constants for C-O-C-H segments of bonded atoms. Carbohydr Res. 189:359-362.
57. Valafar H, Prestegard JH. 2004. REDCAT: A residual dipolar coupling analysis tool. J Magn Reson. 167:228-241.
58. Zhang ZQ, McCallum SA, Xie J, Nieto L, Corzana F, Jimenez-Barbero J, Chen M, Liu J, Linhardtt RJ. 2008. Solution structures of chemoenzymatically synthesized heparin and its precursors. J Am Chem Soc. 130:12998-13007.
59. Zweckstetter M, Bax A. 2000. Prediction of sterically induced alignment in a dilute liquid crystalline phase: Aid to protein structure determination by NMR. J Am Chem Soc. 122:3791-3792.