Chemoenzymatic synthesis of heparan sulfate and heparin

Biocatalysis and Biotransformation

Volumn 30, Issue 3, 2012, Pages 296-308

  Zhou, Xianxuan ^a   O'Leary, Timothy R ^a   Xu, Yongmei ^a   Sheng, Juzheng ^a   Liu, Jian ^a  

^a University of North Carolina   (United States)

Author keywords

Chemoenzymatic synthesis; Heparan sulfate; Heparin; Sulfotransferase

Indexed keywords

CHEMICAL SYNTHESIS; CHEMO-ENZYMATIC SYNTHESIS; CHEMOENZYMATIC APPROACHES; GLYCOSYL TRANSFERASE; HEPARAN SULFATES; HEPARIN; PATHOPHYSIOLOGICAL; RECENT PROGRESS; SULFATED POLYSACCHARIDES; SULFOTRANSFERASE;

BIOCHEMISTRY; ENZYMES; OLIGOSACCHARIDES; SULFUR COMPOUNDS;

POLYSACCHARIDES;

EPIMERASE; GLYCOSYLTRANSFERASE; HEPARAN SULFATE; HEPARIN; SULFOTRANSFERASE;

BIOSYNTHESIS; CARBOHYDRATE ANALYSIS; CARBOHYDRATE SYNTHESIS; CHEMICAL REACTION; DRUG SYNTHESIS; ENZYME ANALYSIS; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; REVIEW;

EID: 84861749326     PISSN: 10242422     EISSN: 10292446     Source Type: Journal    
DOI: 10.3109/10242422.2012.681852     Document Type: Review

References (52)

1. Aikawa J-i, Grobe K, Tsujimoto M, Esko JD. 2001. Multiple isozymes of heparan sulfates/heparin GlcNAc N-deacetylase/GlcN N-sulfotransferase: structure and activity of the fourth member, NDST4. J Biol Chem 276:5876-5882.
2. Arungundram S, Al-Mafraji K, Asong J, Leach III FE, Amster IJ, Venot A, Turnbull JE, Boons GJ. 2009. Modular synthesis of heparan sulfate oligosaccharides for structure-activity relatioship studies. J Am Chem Soc 131:17394-17405.
3. Babu P, Victor XV, Nelsen E, Nguyen TKN, Raman K, Kuberan B. 2011. Hydrogen/deuterium exchange-LC-MS approach to characterize the action of heparan sulfate C5-epimerase. Anal Bioanal Chem 401:237-244.
4. Balagurunathan K, Beeler DL, Lech M, Wu ZL, Rosenberg RD. 2003a. Chemoenzymatic Synthesis of Classical and Nonclassical Anticoagulant Heparan Sulfate Polysaccharides. J Biol Chem 278:52613-52621. (Pubitemid 38035858)
5. Balagurunathan K, Lech MZ, Beeler DL, Wu ZL, Rosenberg RD. 2003b. Enzymatic synthesis of antithrombin III-binding heparan sulfate pentasaccharide. Nat Biotechnol 21:1343-1346. (Pubitemid 37356620)
6. Bethea HN, Xu D, Liu J, Pedersen LC. 2008. Redirecting the substrate specifi city of heparan sulfate 2-O-sulfotransferase by structurally guided mutagenesis. Proc Natl Acad Sci USA 105:18724-18729.
7. Bishop J, Schuksz M, Esko JD. 2007. Heparan sulphate proteoglycans fi ne-tune mammalian physiology. Nature 446:1030-1037. (Pubitemid 46676065)
8. Burkart MD, Izumi M, Chapman E, Lin C, Wong C. 2000. Regeneration of PAPS for the enzymatic synthesis of sulfated oligosaccharides. J Org Chem 65:5565-5574.
9. Chen J, Avci FY, Mu A oz EM, McDowell LM, Chen M, Pedersen LC, et al. 2005. Enzymatically redesigning of biologically active heparan sulfate. J Biol Chem 280:42817-42825. (Pubitemid 43049243)
10. Chen J, Jones CL, Liu J. 2007. Using an enzymatic combinatorial approach to identify anticoagulant heparan sulfate structures. Chem Biol 14:986-993. (Pubitemid 47404901)
11. Chen M, Bridges A, Liu J. 2006. Substrate specifi cities of recombinant N-acetyl- D -glucosaminyl transferase (Kfi A). Biochemistry 45:12358-12365.
12. Copeland RJ, Balasubramaniam A, Tiwari V, Zhang F, Bridges A, Linhardt RJ, Shukla D, Liu J. 2008. Using a 3-O-sulfated heparin octasaccharide to inhibit the entry of herpes simplex virus 1. Biochemistry 47:5774-5783. (Pubitemid 351747056)
13. de Paz JL, Seeberger PH. 2008. Deciphering the glycosaminoglycan code with the help of microarrays. Mol Biosyst 4:707-711. (Pubitemid 351871754)
14. Duncan MB, Liu M, Fox C, Liu J. 2006. Characterization of the N -deacetylase domain from the heparan sulfate N -deacetylase/ N-sulfotransferase 2. Biochem Biophys Res Commun 339: 1232-1237. (Pubitemid 41790595)
15. Edavettal SC, Lee KA, Negishi M, Linhardt RJ, Liu J, Pedersen LC. 2004. Crystal structure and mutational analysis of heparan sulfate 3-O-sulfotransferase isoform 1. J Biol Chem 279: 25789-25797. (Pubitemid 38756843)
16. Esko JD, Selleck SB. 2002. Order out of chaos: Assembly of ligand binding sites in heparan sulfate. Ann Rev Biochem 71: 435-471. (Pubitemid 34800227)
17. Hagner-McWhirter A, Hannesson HH, Campbell P, Westley J, RodA n L, Lindahl U, Li JP. 2000. Biosynthesis of heparin/ heparan sulfate: kinetic studies of the glucuronyl C5-epimerase with N-sulfated derivatives of the Escherichia coli K5 capsular polysaccharide as substrates. Glycobiology 10:159-171. (Pubitemid 30193016)
18. Kakuta Y, Sueyoshi T, Negishi M, Pedersen LC. 1999. Crystal structure of the sulfotransferase domain of human heparan sulfate N-deacetylase/N- sulfotransferase 1. J Biol Chem 274: 10673-10676.
19. Kinnunen T, Huang Z, Townsend J, Gatdula MM, Brown JR, Esko JD, Turnbull JE. 2005. Heparan 2-O-sulfotransferase, hst-2, is essential for normal cell migration in Caenorhabditis elegans. Proc Natl Acad Sci USA 102:1507-1512. (Pubitemid 40209199)
20. Kobayashi M, Habuchi H, Yoneda M, Habuchi O, Kimata K. 1997. Molecular cloning and expression of Chinese hamster ovary cell heparan-sulfate 2-sulfotransferase. J Biol Chem 272:13980-13985. (Pubitemid 27224844)
21. Li J-P, Gong F, Darwish KE, Jalkanen M, Lindahl U. 2001. Characterization of the D-glucuronyl C5-epimerase involved in the biosynthesis of heparin and heparan sulfate. J Biol Chem 276:20069-20077.
22. Li J-P, Gong F, Hagner-McWhirter A, Forsberg E,Abrink M, Kisilevsky R, Zhang X, Lindahl U. 2003. Targeted disruption of a murine glucuronyl C5-epimerase gene results in heparan sulfate lacking L-iduronic acid and in neonatal lethality. J Biol Chem 278:28363-28366. (Pubitemid 36935735)
23. Li J-p, Hagner-McWhirter A, Kjellen L, Palgi J, Jalkanen M, Lindahl U. 1997. Biosynthesis of Heparin/Heparan Sulfate. cDNA cloning and expression of D-glucuronyl C5-epimerase from bovine lung. J Biol Chem 272:28158-28163. (Pubitemid 27473627)
24. Li K, Bethea HN, Liu J. 2010. Determining the activity of C5-epimerase using an engineered heparan sulfate 2-O-sulfotransferase. J Biol Chem 285:11106-11113.
25. Lindahl U, Backstrom G, Thunberg L, Leder IG. 1980. Evidence for a 3-O-sulfated D-glucosamine residue in the antithrombinbinding sequence of heparin. Proc Natl Acad Sci USA 77: 6551-6555. (Pubitemid 11219166)
26. Liu J, Rosenberg RD. 2002. Handbook of glycosyltransferases and their related genes. Tokyo: Springer-Verlag.
27. Liu R, Liu J. 2011. Enzymatical placement of 6-O-sulfo groups in heparan sulfate. Biochemistry 50:4382-4391.
28. Liu R, Xu Y, Chen M, We awer M, Zhou X, Bridges AS, et al. 2010. Chemoenzymatic design of heparan sulfate oligosaccharides. J Biol Chem 285:34240-34249.
29. Lundin L, Larsson H, Kreuger J, Kanda S, Lindahl U, Salmivirta M, Claesson-Welsh L. 2000. Selectively desulfated heparin inhibits fi broblast growth factor-induced mitogenicity and angiogenesis. J Biol Chem 275:24653-24660. (Pubitemid 30626565)
30. McDowell LM, Frazier B, Studelska DR, Giljum K, Chen J, Liu J, et al. 2006. Inhibition or activation of Apert syndrome FGFRs (S252W) signaling by specifi c glycosaminoglycans. J Biol Chem 281:6924-6930. (Pubitemid 43847454)
31. Moon A, Edavettal SC, Krahn JX, Munoz EM, Negishi M, Linhardt RJ, Liu J, Pedersen LC. 2004. Structural analysis of the sulfotransferase (3-OST-3) involved in the biosynthesis of an entry receptor of herpes simplex virus 1. J Biol Chem 279:45185-45193. (Pubitemid 39430934)
32. Mu A oz E, Xu D, Avci F, Kemp M, Liu J, Linhardt RJ. 2006. Enzymatic synthesis of heparin related polysaccharides on sensor chips: Rapis screening of heparin-protein interactions. Biochem Biophys Res Commun 339:597-602. (Pubitemid 41739709)
33. Peterson SB, Liu J. 2010. Unraveling the specifi city of heparanase utilizing synthetic substrates. J Biol Chem 285:14504-14513.
34. Peterson SP, Frick A, Liu J. 2009. Designing of biologically active heparan sulfate and heparin using an enzyme-based approach. Nat Prod Rep 26:61-627.
35. Petitou M, van Boeckel CAA. 2004. A synthetic antithrombin III binding pentasaccharide is now a drug! What comes next? Angew Chem Int Ed 43:3118-3133. (Pubitemid 39257600)
36. Renosto F, Seubert PA, Segel IH. 1984. Adenosine 5 α- phosphosulfate kinase from Penicillium chrysogenum: purifi cation and kinetic characterization. J Biol Chem 259:2113-2123. (Pubitemid 14190318)
37. Rong J, Habuchi H, Kimata K, Lindahl U, Kusche-Gullberg M. 2001. Substrate specifi city of the heparan sulfate hexuronic acid 2- O -sulfotransferase. Biochemistry 40: 5548-5555. (Pubitemid 32458257)
38. Saribas AS, Mobasseri A, Pristatsky P, Chen X, Barthelson R, Hakes D, Wang J. 2004. Production of N-sulfated polysaccharides using yeast expressed N-deacetylase/N-sulfotransferase-1 (NDST-1). Glycobiology 14:1217-1228. (Pubitemid 39585356)
39. Sheng Z, Liu R, Xu Y, Liu J. 2011. Determination of the substrate specifi city of heparan sulfate N-deacetylase/N-sulfotransferase. J Biol Chem 286:19768-19776.
40. Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, et al. 1999. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13-22. (Pubitemid 29468626)
41. Sismey-Ragatz AE, Green DE, Otto NJ, Rejzek M, Field RA, Deangelis PL. 2007. Chemoenzymatic Synthesis with Distinct Pasteurella Heparosan Synthases. J Biol Chem 282:28321-28327.
42. Smeds E, Habuchi H, Do A-T, Hjertson E, Grundberg H, Kimata K, Lindahl U, Kusche-Gullberg M. 2003. Substrate specifi cities of mouse heparan sulphate glucosaminyl 6-O-sulfotransferases. Biochem J 372:371-380. (Pubitemid 36723882)
43. Sugahara K, Kitagawa H. 2000. Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr Opin Struct Biol 10:518-527.
44. Wang L, Brown JR, Varki A, Esko JD. 2002. Heparin's antiinfl ammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L- and P-selectins. J Clin Invest 110:127-136. (Pubitemid 34743473)
45. Wang Z, Xu Y, Yang B, Tiruchinapally G, Sun B, Liu R, et al. 2010. Preactivation-based one-pot combinatorial synthesis of heparin-like hexasaccharides for the analysis of heparin-protein interactions. Chem Eur J 16:8365-8375.
46. Wang Z, Yang B, Zhang Z, Ly M, Takieddin M, Mousa SA, et al. 2011. Control of the heparosan N-deacetylation leads to an improved bioengineered heparin. Appl Biochem Biotech 91:91-99.
47. Xia G, Chen J, Tiwari V, Ju W, Li J-P, Malmstr am A, Shukla D, Liu J. 2002. Heparan sulfate 3-O-sulfotransferase isoform 5 generates both an antithrombin-binding site and an entry receptor for herpes simplex virus, type 1. J Biol Chem 277:37912-37919.
48. Xu D, Moon A, Song D, Pedersen LC, Liu J. 2008. Engineering sulfotransferases to modify heparan sulfate. Nat Chem Biol 4:200-202. (Pubitemid 351264127)
49. Xu D, Tiwari V, Xia G, Clement C, Shukla D, Liu J. 2005. Characterization of Heparan Sulfate 3-O-Sulfotransferase Isoform 6 and Its Role in Assisting the Entry of Herpes Simplex Virus, Type 1. Biochem J 385:451-459. (Pubitemid 40165078)
50. Xu Y, Masuko S, Takieddin M, Xu H, Liu R, Jing J, et al. 2011. Chemoenzymatic synthesis of homogeneous ultralow molecular weight heparins. Science 334:498-501.
51. Zhang Z, McCallum SA, Xie J, Nieto L, Corzana F, JimA nez- Barbero J, et al. 2008. Solution structure of chemoenzymatically synthesized heparin and its precursors. J Am Chem Soc 130:12998-13007.
52. Zhou X, Chandarajoti K, Pham TQ, Liu R, Liu J. 2011. Expression of heparan sulfate sulfotransferases in Kluyveromyces lactis and preparation of 3 α-phosphoadenosine-5 α-phosphosulfate. Glycobiology 21:771-780.