Chemoenzymatic synthesis and structural characterization of 2-O-sulfated glucuronic acid-containing heparan sulfate hexasaccharides

Glycobiology

Volumn 24, Issue 8, 2014, Pages 681-692

  Hsieh, Po Hung ^a   Xu, Yongmei ^a   Keire, David A ^b   Liu, Jian ^a  

^a University of North Carolina   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

Chemoenzymatic synthesis; Heparin; Heparin sulfate; Oligosaccharides; Sulfotransferase

Indexed keywords

ANTITHROMBIN; GLUCURONIC ACID; HEPARAN SULFATE; HEPARIN; OLIGOSACCHARIDE; POLYSACCHARIDE SULFATE; GLUCURONIC ACID 2-SULFATE; SULFOTRANSFERASE;

ANTICOAGULATION; ARTICLE; BINDING AFFINITY; CARBON NUCLEAR MAGNETIC RESONANCE; CHEMOENZYMATIC SYNTHESIS; DISSOCIATION CONSTANT; DRUG CONFORMATION; DRUG DETERMINATION; DRUG STRUCTURE; DRUG SULFATION; DRUG SYNTHESIS; EPIMERIZATION; HETERONUCLEAR MULTIPLE BOND CORRELATION; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ACTIVITY RELATION; BIOSYNTHESIS; CHEMISTRY; CONFORMATION; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

CARBOHYDRATE CONFORMATION; GLUCURONATES; HEPARITIN SULFATE; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; SULFOTRANSFERASES;

EID: 84903718332     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwu032     Document Type: Article

References (37)

1. Ahsan A, Jeske W, Hoppensteadt D, Lormeau JC, Wolf H, Fareed J. 1995. Molecular profiling and weight determination of heparins and depolymerized heparins. J Pharm Sci. 84(6): 724-727
2. Bishop JR, Schuksz M, Esko JD. 2007. Heparan sulphate proteoglycans finetune mammalian physiology. Nature. 446(7139): 1030-1037. (Pubitemid 46676065
3. Carlsson P, Presto J, Spillmann D, Lindahl U, Kjellen L. 2008. Heparin/heparan sulfate biosynthesis: Processive formation of N-sulfated domains. J Biol Chem. 283(29): 20008-20014
4. Casu B. 1985. Structure and biological activity of heparin. Adv Carbohydr Chem Biochem. 43: 51-134
5. Das SK, Mallet JM, Esnault J, Driguez PA, Duchaussoy P, Sizun P, Herault JP, Herbert JM, Petitou M, Sinay P. 2001. Synthesis of conformationally locked L-iduronic acid derivatives: Direct evidence for a critical role of the skewboat 2S0 conformer in the activation of antithrombin by heparin. Chemistry. 7(22): 4821-4834
6. 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(6687): 812-817. (Pubitemid 28299496
7. Faham S, Hileman RE, Fromm JR, Linhardt RJ, Rees DC. 1996. Heparin structure and interactions with basic fibroblast growth factor. Science. 271 (5252): 1116-1120. (Pubitemid 26075225
8. 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 (2): 157-167
9. Feyerabend TB, Li JP, Lindahl U, Rodewald HR. 2006. Heparan sulfate C5-epimerase is essential for heparin biosynthesis in mast cells. Nat Chem Biol. 2(4): 195-196
10. Griffin CC, Linhardt RJ, Van Gorp CL, Toida T, Hileman RE, Schubert RL, 2nd, Brown SE. 1995. Isolation and characterization of heparan sulfate from crude porcine intestinal mucosal peptidoglycan heparin. Carbohydr Res. 276 (1): 183-197
11. Guerrini M, Elli S, Gaudesi D, Torri G, Casu B, Mourier P, Herman F, Boudier C, Lorenz M, Viskov C. 2010. 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. J Med Chem. 53(22): 8030-8040
12. Guerrini M, Elli S, Mourier P, Rudd TR, Gaudesi D, Casu B, Boudier C, Torri G, Viskov C. 2013. An unusual antithrombin-binding heparin octasaccharide with an additional 3-O-sulfated glucosamine in the active pentasaccharide sequence. Biochem J. 449(2): 343-351
13. Guerrini M, Guglieri S, Casu B, Torri G, Mourier P, Boudier C, Viskov C. 2008. Antithrombin-binding octasaccharides and role of extensions of the active pentasaccharide sequence in the specificity and strength of interaction. Evidence for very high affinity induced by an unusual glucuronic acid residue. J Biol Chem. 283(39): 26662-26675
14. Guerrini M, Torri G. 2008. Quantitative 2D NMR analysis of glycosaminoglycans. In: Holzgrabe U, Diehl B and Wawer I, editors. NMR Spectroscopy in Pharmaceutical Analysis. New York: Elsevier. p. 407-428
15. Guglier S, Hricovini 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(52): 13862-13869
16. Hricovini M, Guerrini M, Bisio A, Torri G, Petitou M, Casu B. 2001. Conformation of heparin pentasaccharide bound to antithrombin III. Biochem J. 359(Pt 2): 265-272. (Pubitemid 32999770
17. Jin L, Abrahams JP, Skinner R, Petitou M, Pike RN, Carrell RW. 1997. The anticoagulant activation of antithrombin by heparin. Proc Natl Acad Sci USA. 94 (26): 14683-14688. (Pubitemid 28041434
18. Keire DA, Buhse LF, Al-Hakim A. 2013. Characterization of currently marketed heparin products: Composition analysis by 2D-NMR. Anal Methods. 5 (12): 2984-2994
19. Kreuger J, Salmivirta M, Sturiale L, Gimenez-Gallego G, Lindahl U. 2001. Sequence analysis of heparan sulfate epitopes with graded affinities for fibroblast growth factors 1 and 2. J Biol Chem. 276(33): 30744-30752
20. Langeslay DJ, Young RP, Beni S, Beecher CN, Mueller LJ, Larive CK. 2012. Sulfamate proton solvent exchange in heparin oligosaccharides: Evidence for a persistent hydrogen bond in the antithrombin-binding pentasaccharide Arixtra. Glycobiology. 22(9): 1173-1182
21. Lee MK, Lander AD. 1991. Analysis of affinity and structural selectivity in the binding of proteins to glycosaminoglycans: Development of a sensitive electrophoretic approach. Proc Natl Acad Sci USA. 88(7): 2768-2772. (Pubitemid 21916500
22. Limtiaco JF, Beni S, Jones CJ, Langeslay DJ, Larive CK. 2011. The efficient structure elucidation of minor components in heparin digests using microcoil NMR. Carbohydr Res. 346(14): 2244-2254
23. Linhardt RJ. 2003. 2003 Claude S. Hudson Award address in carbohydrate chemistry. Heparin: Structure and activity. J Med Chem. 46(13): 2551-2564. (Pubitemid 36702523
24. Liu R, Xu Y, Chen M, Weiwer M, Zhou X, Bridges AS, DeAngelis PL, Zhang Q, Linhardt RJ, Liu J. 2010. Chemoenzymatic design of heparan sulfate oligosaccharides. J BiolChem. 285(44): 34240-34249
25. Liu H, Zhang Z, Linhardt RJ. 2009. Lessons learned from the contamination of heparin. Nat Prod Rep. 26(3): 313-321
26. McMahon AW, Pratt RG, Hammad TA, Kozlowski S, Zhou E, Lu S, Kulick CG, Mallick T, Dal Pan G. 2010. Description of hypersensitivity adverse events following administration of heparin that was potentially contaminated with oversulfated chondroitin sulfate in early 2008. Pharmacoepidemiol Drug Saf. 19(9): 921-933
27. Ozug J, Wudyka S, Gunay NS, Beccati D, Lansing J, Wang J, Capila I, Shriver Z, Kaundinya GV. 2012. Structural elucidation of the tetrasaccharide pool in enoxaparin sodium. Anal Bioanal Chem. 403(9): 2733-2744
28. Petitou M, van Boeckel CA. 1992. Chemical synthesis of heparin fragments and analogues. Fortschr Chem Org Naturst. 60: 143-210
29. Sattelle BM, Hansen SU, Gardiner J, Almond A. 2010. Free energy landscapes of iduronic acid and related monosaccharides. J Am Chem Soc. 132 (38): 13132-13134
30. Sommers CD, Ye H, Kolinski RE, Nasr M, Buhse LF, Al-Hakim A, Keire DA. 2011. Characterization of currently marketed heparin products: Analysis of molecular weight and heparinase-I digest patterns. Anal Bioanal Chem. 401 (8): 2445-2454
31. Victor XV, Nguyen TK, Ethirajan M, Tran VM, Nguyen KV, Kuberan B. 2009. Investigating the elusive mechanism of glycosaminoglycan biosynthesis. J Biol Chem. 284(38): 25842-25853
32. Xu Y, Masuko S, Takieddin M, Xu H, Liu R, Jing J, Mousa SA, Linhardt RJ, Liu J. 2011. Chemoenzymatic synthesis of homogeneous ultralow molecular weight heparins. Science. 334(6055): 498-501
33. Xu D, Moon AF, Song D, Pedersen LC, Liu J. 2008. Engineering sulfotransferases to modify heparan sulfate. Nat Chem Biol. 4(3): 200-202. (Pubitemid 351264127
34. Yamada S, Murakami T, Tsuda H, Yoshida K, Sugahara K. 1995. Isolation of the porcine heparin tetrasaccharides with glucuronate 2-o-sulfate Y heparinase cleaves glucuronate 2-O-sulfate-containing disaccharides in highly sulfated blocks in heparin. J Biol Chem. 270(15): 8696-8705
35. Zhang Z, McCallum SA, Xie J, Nieto L, Corzana F, Jimenez-Barbero J, Chen M, Liu J, Linhardt RJ. 2008. Solution structures of chemoenzymatically synthesized heparin and its precursors. J AmChem Soc. 130(39): 12998-13007
36. Zhao G, Guan W, Cai L, Wang PG. 2010. Enzymatic route to preparative-scale synthesis of UDP-GlcNAc/GalNAc, their analogues and GDP-fucose. Nat Protoc. 5(4): 636-646
37. Zhou X, Chandarajoti K, Pham TQ, Liu R, Liu J. 2011. Expression of heparan sulfate sulfotransferases in Kluyveromyces lactis and preparation of 3′-phosphoadenosine-5′-phosphosulfate. Glycobiology. 21(6): 771-780.