Effects on molecular conformation and anticoagulant activities of 1,6-anhydrosugars at the reducing terminal of antithrombin-binding octasaccharides isolated from low-molecular-weight heparin enoxaparin

Journal of Medicinal Chemistry

Volumn 53, Issue 22, 2010, Pages 8030-8040

  Guerrini, Marco ^a   Elli, Stefano ^a   Gaudesi, Davide ^a   Torri, Giangiacomo ^a   Casu, Benito ^a   Mourier, Pierre ^b   Herman, Frederic ^b   Boudier, Christian ^c   Lorenz, Martin ^b   Viskov, Christian ^b  

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

^b SANOFI   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICOAGULANT AGENT; ANTITHROMBIN; BLOOD CLOTTING FACTOR 10A; CARBOHYDRATE DERIVATIVE; ENOXAPARIN; FONDAPARINUX; N SULFO 1,6 ANHYDRO DEXTRO GLUCOSAMINE; N SULFO 1,6 ANHYDRO DEXTRO MANNOSAMINE; UNCLASSIFIED DRUG;

ANTICOAGULATION; ARTICLE; BINDING AFFINITY; DRUG CONFORMATION; DRUG PROTEIN BINDING; DRUG STRUCTURE; HUMAN; PROTON NUCLEAR MAGNETIC RESONANCE;

ANTICOAGULANTS; ANTITHROMBIN PROTEINS; CARBOHYDRATE SEQUENCE; ENOXAPARIN; FACTOR XA; HEXOSAMINES; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 78649512935     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm100771s     Document Type: Article

References (38)

1. Gray, E.; Mulloy, B.; Barrowcliffe, T. W. Heparin and low-molecular-weight heparin Thromb. Haemostasis 2008, 99, 807-818
2. Linhardt, R. J. Heparin: Structure and Activity J. Med. Chem. 2003, 46, 2551-2554
3. Mousa, S. A. Heparin and low molecular weight heparin in thrombosis and inflammation: emerging link. In Chemistry and Biology of Heparin and Heparan Sulfate; Garg, H. G.; Linhardt, R. J.; Hales, C. A., Eds; Elsevier Ltd.: New York, 2005; pp 571 - 581.
4. Casu, B.; Lindahl, U. Structure and biological interactions of heparin and heparan sulfate Adv. Carbohydr. Chem. Biochem. 2001, 57, 159-206
5. Loganathan, D.; Wang, H. M.; Mallis, L. M.; Linhardt, R. J. Structural variation in the antithrombin III binding site region and its occurrence in heparin from different sources Biochemistry 1990, 29, 4362-4368
6. Viskov, C.; Just, M.; Laux, V.; Mourier, P.; Lorenz, M. Description of the chemical and pharmacological characteristics of a new hemisynthetic ultra-low-molecular-weight heparin, AVE5026 J. Thromb. Haemostasis 2009, 7, 1143-1151
7. Bisio, A.; Vecchietti, D.; Citterio, L.; Guerrini, M.; Raman, R.; Bertini, S.; Eisele, G.; Naggi, A.; Sasisekharan, R.; Torri, G. Structural features of low-molecular-weight heparins affecting their affinity to antithrombin Thromb. Haemostasis 2009, 102, 865-873
8. Zang, Z.; Weiwer, M.; Li, B.; Kemp, M. M.; Daman, T. H.; Linhardt, R. J. Oversulfated chondroitin sulfate: impact of heparin impurity, associated with adverse events, on low-molecular-weight heparin preparation J. Med. Chem. 2008, 51, 5498-5501
9. Lane, D. A.; Denton, J.; Flynn, A. M.; Thunberg, L.; Lindahl, U. Anticoagulant activities of heparin oligosaccharides and their neutralization by platelet factor 4 Biochem. J. 1984, 218, 725-732
10. Petitou, M.; van Boeckel, C. A. A synthetic antithrombin III binding pentasaccharide is now a drug! What comes next? Angew. Chem., Int. Ed. 2004, 43, 3118-3133
11. Hricovini, M.; Guerrini, M.; Bisio, A.; Torri, G.; Petitou, M.; Casu, B. Conformation of heparin pentasaccharide bound to antithrombin III Biochem. J. 2001, 359, 265-272
12. Chen, J.; Jones, C. L.; Liu, J. Using an enzymatic combinatorial approach to identify anticoagulant heparan sulfate structures Chem. Biol. 2007, 14, 986-993
13. van Boeckel, C. A. A.; Petitou, M. The unique antithrombin III binding domain of heparin: a lead to new synthetic antithrombotics Angew. Chem., Int. Ed. 1993, 32, 1671-1818
14. Guerrini, M.; Guglieri, S.; Beccati, D.; Torri, G.; Viskov, C.; Mourier, P. Conformational transitions induced in heparin octasaccharides by binding with antithrombin III Biochem. J. 2006, 399, 191-198
15. Ferro, D. R.; Provasoli, A.; Ragazzi, M.; Casu, B.; Torri, G.; Bossennec, V.; Perly, B.; Sinaÿ, P.; Petitou, M.; Choay, J. Conformer populations of l -iduronic acid residues in glycosaminoglycan sequences Carbohydr. Res. 1990, 195, 157-167
16. Linhardt, R. J.; Gunay, N. S. Production and chemical processing of low molecular weight heparins Semin. Thromb. Hemostasis 1999, 25 (Suppl 3) 5-16
17. Guerrini, M.; Guglieri, S.; Naggi, A.; Sasisekharan, R.; Torri, G. Low molecular weight heparins: structural differentiation by bidimensional nuclear magnetic resonance spectroscopy Semin. Thromb. Hemostasis 2007, 33, 478-487
18. Mourier, P.; Viskov, C. US Patent 2005/0119477 A1, 2005
19. Chem. Abstr. 2005, 142, 89363.
20. Guerrini, M.; Guglieri, S.; Casu, B.; Torri, G.; Mourier, P.; Boudier, C.; Viskov, C. Antithrombin-binding octasaccharides and role of extensions of the active pentasaccharide sequence in the specificity and strength of interaction J. Biol. Chem. 2008, 283, 26662-26675
21. Mourier, P. A. J.; Viskov, C. Chromatographic analysis and sequencing approach of heparin oligosaccharides using cetyltrimethylammonium dynamically coated stationary phases Anal. Biochem. 2004, 332, 299-313
22. Höök, M.; Björk, I.; Hopwood, J.; Lindahl, U. Anticoagulant activity of heparin: separation of high-activity and low-activity heparin species by affinity chromatography on immobilized antithrombin FEBS Lett. 1976, 66, 90-93
23. Low molecular mass heparin. European Pharmacopoeia 01/2008:0828, 6.0 ed.; European Directorate for the Quality of Medicine & HealthCare: Strasbourg, January, 2008.
24. Herbert, J. M.; Hérault, J. P.; Bernat, A.; Van Amsterdam, R. G. M.; Vogel, G. M. T.; Lormeau, J. C.; Petitou, M.; Meuleman, D. G. Biochemical and pharmacological properties of SANORG3232701 Circ. Res. 1996, 79 (3) 590-600
25. Mascellani, G.; Guerrini, M.; Torri, G.; Liverani, L.; Spelta, F.; Bianchini, P. Characterization of di- and monosulfated, unsaturated heparin disaccharides with terminal N -sulfated 1,6-anhydro-β- d -glucosamine or N -sulfated 1,6-anhydro-β- d -mannosamine residues Carbohydr. Res. 2007, 342, 835-842
26. 13C-NMR spectra of deoxy derivatives of 2-amino-1,6-anhydro-2-deoxy- d -glucose and 2-amino-1,6-anhydro-2-deoxy- d -mannose Carbohydr. Res. 1984, 130, 103-114
27. Ferro, D. R.; Provasoli, A.; Ragazzi, M.; Torri, G.; Casu, B.; Gatti, G.; Jacquinet, J. C.; Sinay, P.; Petitou, M.; Choay, J. Evidence for conformational equilibrium of the sulphated l -iduronate residue in heparin and in synthetic heparin mono- and oligosaccharides: NMR and force-field studies J. Am. Chem. Soc. 1986, 108, 6773-6778
28. Mayer, M.; Meyer, B. Group epitope mapping by saturation transfer difference NMR to identify segments of a ligand in direct contact with a protein receptor J. Am. Chem. Soc. 2001, 123, 6108-6117
29. Moseley, H. N.; Curto, E. V.; Krishna, N. R. Complete relaxation and conformational exchange matrix (CORCEMA) analysis of NOESY spectra of interacting systems; two-dimensional transferred NOESY. J. Magn. Reson., Ser. B 1995, 108, 243 - 261.
30. Jin, L.; Abrahams, J. P.; Skinner, R.; Petitou, M.; Pike, R. N.; Carrell, R. W. The anticoagulant activation of antithrombin by heparin Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 14683-14688
31. Lindahl, U.; Li, J.P. Interaction between heparan sulfate and proteins-design and functional implications Int. Rev. Cell Biol. 2009, 276, 105-159
32. Deakin, J. A.; Blaum, B. S.; Gallagher, J. T.; Uhrín, D.; Lyon, M. The binding properties of minimal oligosaccharides reveal a common heparan sulfate/dermatan sulfate-binding site in hepatocyte growth factor/scatter factor that can accommodate a wide variety of sulfation patterns J. Biol. Chem. 2009, 284, 6311-6321
33. Jeske, W. P.; Neville, B.; Ma, Q.; Hoppensteadt, D. A.; Fareed, J. Effect of 1,6-anhydro bicyclic ring structure on the pharmacokinetic and pharmacodynamic behavior of low molecular weight heparin. Blood (ASH Annual Meeting Abstracts) 2004, 104, abstract 1868.
34. Forster, M; Mulloy, B. Computational approaches to the identification of heparin-binding sites on the surfaces of proteins Biochem. Soc. Trans. 2006, 34, 431-434
35. Petitou, M.; Jaurand, G.; Derrien, M.; Duchaussoy, P.; Choay, J. A new, highly potent, heparin-like pentasaccharide fragment containing a glucose residue instead of a glucosamine Bioorg. Med. Chem. Lett. 1991, 1, 95-98
36. Mulloy, B.; Forster, M. J.; Jones, C.; Davies, D. B. NMR molecular modeling studies of the solution conformation of heparin Biochem. J. 1993, 293, 849-858
37. Gasteiger, J.; Marsili, M. Iterative partial equalization of orbital electronegativity-a rapid access to atomic charges Tetrahedron 1980, 30, 3219-3228
38. Angulo, J.; Hricovini, M.; Gairi, M.; Guerrini, M.; de Paz, J. L.; Ojeda, R.; Martín-Lomas, M.; Nieto, P. Dynamic properties of biologically active synthetic heparin-like hexasaccharides Glycobiology 2005, 15, 1008-1015