De novo synthesis of a narrow size distribution low-molecular-weight heparin.

Heparin, a commonly used anticoagulant drug, is a mixture of highly sulfated polysaccharides with various molecular weights (MWs). The unique sulfation pattern dictates the anticoagulant activity of heparin. Commercial heparins are categorized into three forms according to their average MW: unfractionated heparin (UFH, MWavg 14,000), low-MW heparin (LMWH, MWavg 3500-6500) and the synthetic pentasaccharide (fondaparinux, MW 1508.3). UFH is isolated from porcine intestine while LMWH is derived from UFH by various methods of depolymerization, which generate a wide range of oligosaccharide chain lengths. Different degradation methods result in structurally distinct LMWH products, displaying different pharmacological and pharmacokinetic properties. In this report, we utilized a chemoenzymatic method to synthesize LMWH with the emphasis on controlling the size distribution of the oligosaccharides. A tetrasaccharide primer and a controlled enzyme-based polymerization were employed to build a narrow size oligosaccharide backbone. The oligosaccharide backbones were further modified by a series of sulfation and epimerization steps in order to obtain a full anticoagulation activity. Determination of the anticoagulation activity in vitro and ex vivo indicated that the synthetic LMWH has higher potency than enoxaparin, a commercial LMWH drug in clinical usage.

[1]  Jian Liu,et al.  Use of biosynthetic enzymes in heparin and heparan sulfate synthesis. , 2013, Bioorganic & medicinal chemistry.

[2]  Yongmei Xu,et al.  Investigation of the substrate specificity of K5 lyase A from K5A bacteriophage. , 2013, Glycobiology.

[3]  Yongmei Xu,et al.  Chemoenzymatic Synthesis of Heparin Oligosaccharides with both Anti-factor Xa and Anti-factor IIa Activities* , 2012, The Journal of Biological Chemistry.

[4]  E. Harris,et al.  Probing Structural Selectivity of Synthetic Heparin Binding to Stabilin Protein Receptors* , 2012, The Journal of Biological Chemistry.

[5]  Yongmei Xu,et al.  Uncovering Biphasic Catalytic Mode of C5-epimerase in Heparan Sulfate Biosynthesis* , 2012, The Journal of Biological Chemistry.

[6]  R. Linhardt,et al.  Synthetic heparin. , 2012, Current opinion in pharmacology.

[7]  R. Linhardt,et al.  Dissecting the substrate recognition of 3-O-sulfotransferase for the biosynthesis of anticoagulant heparin , 2012, Proceedings of the National Academy of Sciences.

[8]  R. Linhardt,et al.  Structure/Function Analysis of Pasteurella multocida Heparosan Synthases , 2012, The Journal of Biological Chemistry.

[9]  S. Mousa,et al.  Chemoenzymatic Synthesis of Homogeneous Ultralow Molecular Weight Heparins , 2011, Science.

[10]  Jian Liu,et al.  Expression of heparan sulfate sulfotransferases in Kluyveromyces lactis and preparation of 3'-phosphoadenosine-5'-phosphosulfate. , 2011, Glycobiology.

[11]  C. Boeriu,et al.  Analysis of the Polymerization Initiation and Activity of Pasteurella multocida Heparosan Synthase PmHS2, an Enzyme with Glycosyltransferase and UDP-sugar Hydrolase Activity* , 2010, The Journal of Biological Chemistry.

[12]  R. Linhardt,et al.  Chemoenzymatic Design of Heparan Sulfate Oligosaccharides* , 2010, The Journal of Biological Chemistry.

[13]  Peng George Wang,et al.  Enzymatic route to preparative-scale synthesis of UDP–GlcNAc/GalNAc, their analogues and GDP–fucose , 2010, Nature Protocols.

[14]  G. Merli,et al.  Pharmacological and clinical differences between low-molecular-weight heparins: implications for prescribing practice and therapeutic interchange. , 2010, P & T : a peer-reviewed journal for formulary management.

[15]  R. Sasisekharan,et al.  Structural features of low-molecular-weight heparins affecting their affinity to antithrombin , 2009, Thrombosis and Haemostasis.

[16]  C. Boeriu,et al.  BIOTECHNOLOGICALLY RELEVANT ENZYMES AND PROTEINS In vitro synthesis of heparosan using recombinant Pasteurella multocida heparosan synthase PmHS2 , 2009 .

[17]  Jian Liu,et al.  Design of Biologically Active Heparan Sulfate and Heparin Using an Enzyme‐Based Approach , 2009 .

[18]  Zhenqing Zhang,et al.  Oversulfated chondroitin sulfate: impact of a heparin impurity, associated with adverse clinical events, on low-molecular-weight heparin preparation. , 2008, Journal of medicinal chemistry.

[19]  M. Rejžek,et al.  Chemoenzymatic Synthesis with Distinct Pasteurella Heparosan Synthases , 2007, Journal of Biological Chemistry.

[20]  Jian Liu,et al.  Using an enzymatic combinatorial approach to identify anticoagulant heparan sulfate structures. , 2007, Chemistry & biology.

[21]  Jian Liu,et al.  Determination of the substrate specificities of N-acetyl-d-glucosaminyltransferase. , 2006, Biochemistry.

[22]  Jian Liu,et al.  Characterization of the N-deacetylase domain from the heparan sulfate N-deacetylase/N-sulfotransferase 2. , 2006, Biochemical and biophysical research communications.

[23]  W. Jing,et al.  Synchronized Chemoenzymatic Synthesis of Monodisperse Hyaluronan Polymers* , 2004, Journal of Biological Chemistry.

[24]  J. Hirsh,et al.  Heparin and low-molecular-weight heparin: the Seventh ACCP Conference on Antithrombotic and Thrombolytic Therapy. , 2004, Chest.

[25]  Jian Liu,et al.  The biosynthesis of anticoagulant heparan sulfate by the heparan sulfate 3-O-sulfotransferase isoform 5. , 2004, Biochimica et biophysica acta.

[26]  G. Gravlee,et al.  The Clinical Onset of Heparin Is Rapid , 2001, Anesthesia and analgesia.

[27]  K. Biemann,et al.  Cleavage of the antithrombin III binding site in heparin by heparinases and its implication in the generation of low molecular weight heparin. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Herbert,et al.  Synthesis of thrombin-inhibiting heparin mimetics without side effects , 1999, Nature.

[29]  R. Linhardt,et al.  Production and chemical processing of low molecular weight heparins. , 1999, Seminars in thrombosis and hemostasis.

[30]  E. Ohman,et al.  Heparin and low-molecular-weight heparin: mechanisms of action, pharmacokinetics, dosing considerations, monitoring, efficacy, and safety. , 1998, Chest.

[31]  D. Hoppensteadt,et al.  Low-molecular-weight heparins: pharmacologic profile and product differentiation. , 1998, The American journal of cardiology.

[32]  Jian Liu,et al.  Purification of Heparan Sulfate D-Glucosaminyl 3-O-Sulfotransferase* , 1996, The Journal of Biological Chemistry.

[33]  S. Nightingale Appropriate Use of Low-Molecular-Weight Heparins (LMWHs) , 1993 .

[34]  J. Hirsh Heparin and low-molecular weight heparins , 1992 .

[35]  M. Petitou,et al.  Chemical synthesis of glycosaminoglycans: new approaches to antithrombotic drugs. , 1991, Nature.

[36]  G. Pejler,et al.  Location of the antithrombin-binding sequence in the heparin chain. , 1989, The Journal of biological chemistry.

[37]  J. Shively,et al.  Formation of anhydrosugars in the chemical depolymerization of heparin. , 1976, Biochemistry.