Heparin mapping using heparin lyases and the generation of a novel low molecular weight heparin

Journal of Medicinal Chemistry

Volumn 54, Issue 2, 2011, Pages 603-610

  Xiao, Zhongping ^a,b   Tappen, Britney R ^c   Ly, Mellisa ^b   Zhao, Wenjing ^c   Canova, Lauren P ^c   Guan, Huashi ^a   Linhardt, Robert J ^b,c,d  

^a OCEAN UNIVERSITY OF CHINA   (China)

^b Research Rensselaer Polytechnic Institute   (United States)

^c RENSSELAER POLYTECHNIC INSTITUTE   (United States)

^d RENSSELAER POLYTECHNIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICOAGULANT AGENT; ANTITHROMBIN III; HEPARIN LYASE; LOW MOLECULAR WEIGHT HEPARIN; OLIGOSACCHARIDE; URONIC ACID;

ARTICLE; DRUG STRUCTURE; GENETIC LINKAGE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN;

ANTICOAGULANTS; HEPARIN; HEPARIN LYASE; HEPARIN, LOW-MOLECULAR-WEIGHT; OLIGOSACCHARIDES; SUBSTRATE SPECIFICITY;

EID: 78751655946     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm101381k     Document Type: Article

References (46)

1. Rabenstein, D. L. Heparin and heparan sulfate: structure and function Nat. Prod. Rep. 2002, 19, 312-331
2. Linhardt, R. J. Perspective: 2003 Claude S. Hudson Award Address in Carbohydrate Chemistry. Heparin: Structure and Activity J. Med. Chem. 2003, 46, 2551-2564
3. Toida, T.; Linhardt, R. J. Structure and bioactivity of sulfated polysaccharides Trends Glycosci. Glycobiol. 2003, 15, 29-46
4. Capila, I.; Linhardt, R. J. Heparin-protein interactions Angew. Chemie. Int. Ed. 2002, 41, 390-412
5. Petitou, M.; Casu, B.; Lindahl, U. 1976-1983, a critical period in the history of heparin: the discovery of the antithrombin binding site Biochimie 2003, 85, 83-89
6. Liu, H.; Zhang, Z.; Linhardt, R. J. Lessons learned from the contamination of heparin Nat. Prod. Rep. 2009, 26, 313-321
7. Yang, V. C.; Linhardt, R. J.; Bernstein, H.; Cooney, C. L.; Langer, R. Purification and characterization of heparinase from Flavobacterium heparinum J. Biol. Chem. 1985, 260, 1849-1857
8. Lohse, D. L.; Linhardt, R. J. Purification and characterization of heparin lyases from Flavobacterium heparinum J. Biol. Chem. 1992, 267, 24347-24355
9. Linhardt, R. J.; Galliher, P. M.; Cooney, C. L. Polysaccharide lyases Appl. Biochem. Biotechnol. 1986, 12, 135-177
10. Desai, U. R.; Wang, H.; Linhardt, R. J. Substrate specificity of the heparin lyases from Flavobacterium heparinum Arch. Biochem. Biophys. 1993, 306, 461-468 (Pubitemid 23314473)
11. Desai, U. R.; Wang, H. M.; Linhardt, R. J. Specificity studies of heparin lyases from Flavobacterium heparinum Biochemistry 1993, 32, 8140-8145
12. Dietrich, C. P.; Silva, M. E.; Michelacci, Y. M. Sequential degradation of heparin in Flavobacterium heparinum: purification and properties of five enzymes involved in heparin degradation J. Biol. Chem. 1973, 248, 6408-6415
13. 13C NMR spectroscopy J. Biol. Chem. 1990, 265, 16807-16813
14. Shaya, D.; Zhao, W.; Garron, M.-L.; Xiao, Z.; Cui, Q.; Zhang, F.; Sulea, J.; Linhardt, R. J.; Cygler, M. Catalytic mechanism of heparinase II revealed by site-directed multagenesis and the crystal structure with its substrate J. Biol. Chem. 2010, 285, 20051-20061
15. Shriver, Z.; Sundaram, M.; Venkataraman, G.; Fareed, J.; Linhardt, R. J.; Biemann, K.; Sasisekharan, R. Cleavage of the antithrombin III binding site in heparin by heparinases and its implication in the generation of low molecular weight heparin Proc. Natl. Acad. Sci. U. S. A. 2000, 97, 10365-10370
16. Yu, G.; LeBrun, L.; Gunay, N. S.; Hoppensteadt, D.; Walenga, J.; Fareed, J.; Linhardt, R. J. Heparinase 1 acts on a synthetic heparin pentasaccharide corresponding to the antithrombin III binding site Thrombos. Res. 2000, 100, 549-556
17. Jandik, K. A.; Gu, K.; Linhardt, R. J. Action pattern of polysaccharide lyases on glycosaminoglycans Glycobiology 1994, 4, 289-296
18. Xiao, Z.; Zhao, W.; Yang, B.; Zhang, Z.; Guan, H.; Linhardt, R. J. Heparinase 1 selectivity for the 3,6-di- O -sulfo-2-deoxy-2-sulfamido-α- d -glucopyranose (1,4) 2- O -sulfo-α- l -idopyranosyluronic acid (GlcNS3S6SIdoA2S) linkages. Glycobiology 2011, 21, 13 - 22.
19. Turnbull, J. E.; Hopwood, J. J.; Gallagher, J. T. A strategy for rapid sequencing of heparan sulfate and heparin saccharides Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 2698-2703
20. Shriver, Z.; Raman, R.; Venkataraman, G.; Drummond, K.; Turnbull, J.; Toida, T.; Linhardt, R. J.; Biemann, K.; Sasisekharan, R. Sequencing of 3- O -sulfated containing heparin decasaccharides with a partial antithrombin III binding site Proc. Natl. Acad. Sci. U. S. A. 2000, 97, 10359-10364
21. Korir, A. K.; Limtiaco, F. K.; Gutierrez, S. M.; Larive, C. K. Ultra performance ion-pair liquid chromatography coupled to electrospray Time-of-flight mass spectrometry for compositional profiling and quantification of heparin and heparan sulfate Anal. Chem. 2008, 80, 1297-1306
22. Guerrini, M.; Naggi, A.; Guglieri, S.; Santarsiero, R.; Torri, G. Complex glycosaminoglycans: profiling substitution patterns by two-dimensional nuclear magnetic resonance spectroscopy Anal. Biochem. 2005, 337, 35-47
23. Linhardt, R. J.; Rice, K. G.; Kim, Y. S.; Lohse, D. L.; Wang, H. M.; Loganathan, D. Mapping and quantification of the major oligosaccharide components of heparin Biochem. J. 1988, 254, 781-787
24. Turnbull, J. E. Oligosaccharide mapping and sequence analysis of glycosaminoglycans. In Methods in Molecular Biology. Biomembrane Protocols I. Isolation and Analysis; Graham, J. M.; Higgins, J. A., Eds.; Humana Press Inc: Totowa, NJ, 1993; Vol. 19, pp 253 - 267.
25. Ly, M.; Laremore, T. N.; Linhardt, R. J. Proteoglycomics: Recent progress and future challenges Omics 2010, 14, 389-399
26. Sasisekharan, R.; Bulmer, M.; Moremen, K. W.; Cooney, C. L.; Langer, R. Cloning and expression of heparinase I gene from Flavobacterium heparinum Proc. Natl. Acad. Sci. U. S. A. 1993, 90, 3660-3664
27. Shaya, D.; Tocilj, A.; Li, Y.; Myette, J.; Venkataraman, G.; Sasisekharan, R.; Cygler, M. Crystal structure of heparinase II from Pedobacter heparinus and its complex with a disaccharide product J. Biol. Chem. 2006, 281, 15525-15535
28. Godavarti, R.; Davis, M.; Venkataraman, G.; Cooney, C.; Langer, R.; Sasisekharan, R. Heparinase III from Flavobacterium heparinum: cloning and recombinant expression in Escherichia coli Biochem. Biophys. Res. Commun. 1996, 225, 751-758 (Pubitemid 26319178)
29. Laremore, T. N.; Ly, M.; K.; Zagorevski, D. V.; Linhardt, R. J. High-resolution preparative separation of glycosaminoglycan oligosaccharides by polyacrylamide gel electrophoresis Anal. Biochem. 2010, 401, 236-241
30. Zhang, F.; Zhang, Z.; Thistle, R.; McKeen, L.; Hosoyama, S.; Toida, T.; Linhardt, R. J.; Page-McCaw, P. Structural characterization of glycosaminoglycans from zebrafish in different ages Glycoconjugate J. 2009, 26, 211-218
31. Cesaretti, M.; Luppi, E.; Maccari, F.; Volpi, N. A 96-well assay for uronic acid carbazole reaction Carbohydr. Polym. 2003, 54, 59-61
32. Edens, R. E.; Al-Hakim, A.; Weiler, J. M.; Rethwisch, D. G.; Fareed, J.; Linhardt, R. J. Gradient polyacrylamide gel electrophoresis for determination of molecular weights of heparin preparations and low-molecular-weight heparin derivatives J. Pharm. Sci. 1992, 81, 823-827
33. Ly, M.; Wang, Z.; Laremore, T. N.; Zhang, F.; Zhong, W.; Pu, D.; Zagorevski, D. V.; Dordick, J. S.; Linhardt, R. J. Analysis of E. coli K5 capsular polysaccharide heparosan. Anal. Bioanal. Chem. 2010, in press.
34. Mousa, S. A.; Zhang, F.; Aljada, A.; Chaturvedi, S.; Takieddin, M.; Zhang, H.; Chi, L.; Castelli, M. C.; Friedman, K.; Goldberg, M. M.; Linhardt, R. J. Pharmacokinetics and pharmacodynamics of oral heparin solid dosage form in healthy human subjects J. Clin. Pharmacol. 2007, 47, 1508-1520
35. Rice, K. G.; Rottink, M. K.; Linhardt, R. J. Fractionation of heparin-derived oligosaccharides by gradient polyacrylamide-gel electrophoresis Biochem. J. 1987, 244, 515-522
36. Rhomberg, A. J.; Shriver, Z.; Biemann, K.; Sasisekharan, R. Mass spectrometric evidence for the enzymatic mechanism of the depolymerization of heparin-like glycosaminoglycans by heparinase II Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 12232-12237 (Pubitemid 28483748)
37. Liu, J.; Desai, U. R.; Han, X.; Toida, T.; Linhardt, R. J. Strategy for the sequence analysis of heparin Glycobiology 1995, 5, 765-774
38. Shibata, S.; Midura, R. J.; Hascall, V. C. Structural analysis of the linkage region oligosaccharides and unsaturated disaccharides from chondroitin sulfate using CarboPac PA1 J. Biol. Chem. 1992, 267, 6548-6555
39. Sugahara, K.; Tsuda, H.; Yoshida, K.; Yamada, S.; Beer, T.; Vliegenthart, J. F. G. Structure determination of the octa- and decasaccharide sequences isolated from the carbohydrate-protein linkage region of porcine intestinal heparin J. Biol. Chem. 1995, 270, 22914-22923
40. Kuberan, B.; Babu, P. Fluorescent-tagged heparan sulfate precursor oligosaccharides to probe the enzymatic action of heparintinase I Anal. Biochem. 2010, 396, 124-132
41. Linhardt, R. J.; Fitzgerald, G. L.; Cooney, C. L.; Langer, R. Mode of action of heparin lyase on heparin Biochim. Biophys. Acta 1982, 702, 197-203
42. Ernst, S.; Rhomberg, A. J.; Biemann, K.; Sasisekharan, R. Direct evidence for a predominantly exolytic processive mechanism for depolymerization of heparin-like glycosaminoglycans by heparinase I Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 4182-4187 (Pubitemid 28207885)
43. Linhardt, R. J.; Loganathan, D.; Hakim, A. A.; Wang, H.; Walenga, J. M.; Hoppensteadt, D.; Fareed, J. Oligosaccharide mapping of low molecular weight heparins: structure and activity differences J. Med. Chem. 1990, 33, 1639-1645
44. Venkataraman, G.; Shriver, Z.; Raman, R.; Sasisekharan, R. Sequencing complex polysaccharides Science 1999, 286, 537-542
45. Yamada, S.; Yamane, Y.; Tsuda, H.; Yoshida, K.; Sugahara, K. A major common trisulfated hexasaccharide core sequence, hexuronic acid (2-sulfate)-glucosamine (N -sulfate)-iduronic acid-N -acetylglucosamine- glucuronic acid-glucosamine (N -sulfate), isolated from the low sulfated irregular region of porcine intestinal heparin J. Biol. Chem. 1998, 273, 1863-1871
46. Yamada, S.; Sakamoto, K.; Tsuda, H.; Yoshida, K.; Sugiura, M.; Sugahara, K. Structural studies of octasaccharides derived from the low-sulfated repeating disaccharide region and octasaccharide serines derived from the protein linkage region of porcine intestinal heparin Biochemistry 1999, 38, 838-847