Combinatorial one-pot chemoenzymatic synthesis of heparin

Carbohydrate Polymers

Volumn 122, Issue , 2015, Pages 399-407

  Bhaskar, Ujjwal ^a,c   Li, Guoyun ^b,c   Fu, Li ^b,c   Onishi, Akihiro ^a,c   Suflita, Mathew ^a,c   Dordick, Jonathan S ^a,c   Linhardt, Robert J ^a,b,c  

^a RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^b Research Rensselaer Polytechnic Institute   (United States)

^c RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

Bioengineered heparin; Liquid chromatography mass spectrometry; Nuclear magnetic resonance spectroscopy; One pot synthesis; United States Pharmacopeia

Indexed keywords

ACETYLATION; CHROMATOGRAPHY; DRUG PRODUCTS; ENZYMES; GLUCOSE; LIQUID CHROMATOGRAPHY; LIQUIDS; MAGNETIC RESONANCE SPECTROMETERS; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SPECTROMETRY;

ACTIVE PHARMACEUTICAL INGREDIENTS; ANTICOAGULANT ACTIVITIES; BIOENGINEERED HEPARIN; CAPSULAR POLYSACCHARIDES; CHEMO-ENZYMATIC SYNTHESIS; LIQUID CHROMATOGRAPHY - MASS SPECTROMETRIES; ONE-POT SYNTHESIS; UNITED STATES PHARMACOPEIAS;

POLYSACCHARIDES;

ANIMALIA; BACTERIA (MICROORGANISMS);

ANTICOAGULANT AGENT; BLOOD CLOTTING FACTOR 10A; FACTOR IIA; HEPARIN; PROTHROMBIN; SULFOTRANSFERASE;

ANIMAL; ANTAGONISTS AND INHIBITORS; BIOENGINEERING; BIOSYNTHESIS; CHEMISTRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROCEDURES;

ANIMALS; ANTICOAGULANTS; BIOENGINEERING; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CHROMATOGRAPHY, LIQUID; FACTOR XA; HEPARIN; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; PROTHROMBIN; SULFOTRANSFERASES;

EID: 84925447095     PISSN: 01448617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.carbpol.2014.10.054     Document Type: Article

References (40)

1. H.N. Bethea, D. Xu, J. Liu, and L.C. Pedersen Redirecting the substrate specificity of heparan sulfate 2-O-sulfotransferase by structurally guided mutagenesis Proceedings of the National Academy of Sciences of the United States of America 105 48 2008 18724 18729
2. U. Bhaskar, E. Sterner, A.M. Hickey, A. Onishi, F. Zhang, and J.S. Dordick Engineering of routes to heparin and related polysaccharides Applied Microbiology and Biotechnology 93 1 2012 1 16
3. M.D. Burkart, M. Izumi, E. Chapman, C.-H. Lin, and C.-H. Wong Regeneration of PAPS for the enzymatic synthesis of sulfated oligosaccharides Journal of Organic Chemistry 65 18 2000 5565 5574
4. I. Capila, and R.J. Linhardt Heparin-protein interactions Angewandte Chemie International Edition 41 3 2002 391 412
5. J. Chen, F.Y. Avci, E.M. Muñoz, L.M. McDowell, M. Chen, and L.C. Pedersen Enzymatic redesigning of biologically active heparan sulfate The Journal of Biological Chemistry 280 52 2005 42817 42825
6. J. Chen, C.L. Jones, and J. Liu Using an enzymatic combinatorial approach to identify anticoagulant heparan sulfate structures Chemistry and Biology 14 9 2007 986 993
7. P.L. DeAngelis, J. Liu, and R.J. Linhardt Chemoenzymatic synthesis of glycosaminoglycans: Re-creating, re-modeling and re-designing nature's longest or most complex carbohydrate chains Glycobiology 23 7 2013 764 777
8. P.-A. Driguez, P. Potier, and P. Trouilleux Synthetic oligosaccharides as active pharmaceutical ingredients: Lessons learned from the full synthesis of one heparin derivative on a large scale Natural Product Reports 31 8 2014 980 989
9. T. Feizi Carbohydrate microarrays - A new set of technologies at the frontiers of glycomics Current Opinion in Structural Biology 13 5 2003 637 645
10. L. Fu, G. Li, B. Yang, A. Onishi, and L. Li Structural characterization of pharmaceutical heparins prepared from different animal tissues Journal of Pharmaceutical Sciences 102 5 2013 1447 1457
11. L. Fu, F. Zhang, G. Li, A. Onishi, U. Bhaskar, and P. Sun Structure and activity of a new low-molecular-weight heparin produced by enzymatic ultrafiltration Journal of Pharmaceutical Sciences 103 5 2014 1375 1383
12. M. Guerrini, D. Beccati, Z. Shriver, A. Naggi, K. Viswanathan, and A. Bisio Oversulfated chondroitin sulfate is a contaminant in heparin associated with adverse clinical events Nature Biotechnology 26 6 2008 669 675
13. H. Habuchi, G. Miyake, K. Nogami, A. Kuroiwa, Y. Matsuda, and M. Kusche-Gullberg Biosynthesis of heparan sulphate with diverse structures and functions: two alternatively spliced forms of human heparan sulphate 6-O-sulphotransferase-2 having different expression patterns and properties Biochemical Journal 371 2003 131 142
14. A.M. Hickey, U. Bhaskar, R.J. Linhardt, and J.S. Dordick Effect of eliminase gene (elmA) deletion on heparosan production and shedding in Escherichia coli K5 Journal of Biotechnology 165 3 2013 175 177
15. K. Higashi, M. Ly, Z. Wang, S. Masuko, U. Bhaskar, and E. Sterner Controlled photochemical depolymerization of K5 heparosan, a bioengineered heparin precursor Carbohydrate Polymers 86 3 2011 1365 1370
16. E. Holmer, K. Kurachi, and G. Soderstrom The molecular-weight dependence of the rate-enhancing effect of heparin on the inhibition of thrombin, factor Xa, factor IXa, factor XIa, factor XIIa and kallikrein by antithrombin Biochemical Journal 193 1981 395 400
17. K.M. Koeller, and C.-H. Wong Synthesis of complex carbohydrates and glycoconjugates: Enzyme-based and programmable one-pot strategies Chemical Reviews 100 12 2000 4465 4494
18. G. Li, B. Yang, L. Li, F. Zhang, C. Xue, and R.J. Linhardt Analysis of 3-O-sulfo group-containing heparin tetrasaccharides in heparin by liquid chromatography-mass spectrometry Analytical Biochemistry 455 2014 3 9
19. R.J. Linhardt, and N.S. Gunay Production and chemical processing of low molecular weight heparins Seminars in Thrombosis and Hemostasis 25 1999 5 16
20. H. Liu, Z. Zhang, and R.J. Linhardt Lessons learned from the contamination of heparin Natural Product Reports 26 2009 313 321
21. B. Mulloy, A. Heath, Z. Shriver, F. Jameison, A. Al Hakim, and T.S. Morris USP compendial methods for analysis of heparin: Chromatographic determination of molecular weight distributions for heparin sodium Analytical and Bioanalytical Chemistry 406 20 2014 4815 4823
22. J.R. Myette, Z. Shriver, J. Liu, G. Venkataraman, R. Rosenberg, and R. Sasisekharan Expression in Escherichia coli, purification and kinetic characterization of human heparan sulfate 3-O-sulfotransferase-1 Biochemical and Biophysical Research Communications 290 4 2002 1206 1213
23. C. Noti, J.L. de Paz, L. Polito, and P.H. Seeberger Preparation and use of microarrays containing synthetic heparin oligosaccharides for the rapid analysis of heparin-protein interactions Chemistry: A European Journal 12 34 2006 8664 8686
24. C.R. Parish The role of heparan sulphate in inflammation Nature Reviews Immunology 6 9 2006 633 643
25. M. Petitou, P. Duchaussoy, I. Lederman, J. Choay, J.-C. Jacquinet, and P. Sinaÿ Synthesis of heparin fragments: A methyl α-pentaoside with high affinity for antithrombin III Carbohydrate Research 167 1987 67 75
26. M.A. Pinhal, B. Smith, S. Olson, J. Aikawa, K. Kimata, and J.D. Esko Enzyme interactions in heparan sulfate biosynthesis: Uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo Proceedings of the National Academy of Sciences of the United States of America 98 23 2001 12984 12989
27. T. Polat, and C.-H. Wong Anomeric reactivity-based one-pot synthesis of heparin-like oligosaccharides Journal of the American Chemical Society 129 42 2007 12795 12800
28. O.F. Restaino, U. Bhaskar, P. Paul, L. Li, M. De Rosa, and J.S. Dordick High cell density cultivation of a recombinant E. coli strain expressing a key enzyme in bioengineered heparin production Applied Microbiology and Biotechnology 97 9 2013 3893 3900
29. J. Sheng, Y. Xu, S.B. Dulaney, X. Huang, and J. Liu Uncovering biphasic catalytic mode of C5-epimerase in heparan sulfate biosynthesis The Journal of Biological Chemistry 287 25 2012 20996 21002
30. E. Sterner, L. Li, P. Paul, J.M. Beaudet, J. Liu, and R.J. Linhardt Assays for determining heparan sulfate and heparin O-sulfotransferase activity and specificity Analytical and Bioanalytical Chemistry 406 2 2014 525 536
31. L. Wang, J.R. Brown, A. Varki, and J.D. Esko Heparin's anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of l- and p-selectins Journal of Clinical Investigation 110 1 2002 127 136
32. Z. Wang, Y. Xu, B. Yang, G. Tiruchinapally, B. Sun, and R. Liu Preactivation-based, one-pot combinatorial synthesis of heparin-like hexasaccharides for the analysis of heparin-protein interactions Chemistry: A European Journal 16 28 2010 8365 8375
33. Z. Wang, B. Yang, Z. Zhang, M. Ly, M. Takieddin, and S. Mousa Control of the heparosan N-deacetylation leads to an improved bioengineered heparin Applied Microbiology and Biotechnology 91 1 2011 91 99
34. J.W. Wilesmith, G.A. Wells, M.P. Cranwell, and J.B. Ryan Bovine spongiform encephalopathy: Epidemiological studies The Veterinary Record 123 25 1988 638 644
35. J. Xiong, U. Bhaskar, G. Li, L. Fu, L. Li, and F. Zhang Immobilized enzymes to convert N-sulfo, N-acetyl heparosan to a critical intermediate in the production of bioengineered heparin Journal of Biotechnology 167 3 2013 241 247
36. Y. Xu, S. Masuko, M. Takieddin, H. Xu, R. Liu, and J. Jing Chemoenzymatic synthesis of homogeneous ultralow molecular weight heparins Science 334 6055 2011 498 501
37. B. Yang, Y. Chang, A.M. Weyers, E. Sterner, and R.J. Linhardt Disaccharide analysis of glycosaminoglycan mixtures by ultra-high-performance liquid chromatography-mass spectrometry Journal of Chromatography A 1225 2012 91 98
38. F. Zhang, B. Yang, M. Ly, K. Solakyildirim, Z. Xiao, and Z. Wang Structural characterization of heparins from different commercial sources Analytical and Bioanalytical Chemistry 401 9 2011 2793 2803
39. L. Zhang, D.L. Beeler, R. Lawrence, M. Lech, J. Liu, and J.C. Davis 6-O-sulfotransferase-1 represents a critical enzyme in the anticoagulant heparan sulfate biosynthetic pathway The Journal of Biological Chemistry 276 45 2001 42311 42321
40. Z. Zhang, S.A. McCallum, J. Xie, L. Nieto, F. Corzana, and J. Jiménez-Barbero Solution structures of chemoenzymatically synthesized heparin and its precursors Journal of the American Chemical Society 130 39 2008 12998 13007