Anticoagulant heparan sulfate: Structural specificity and biosynthesis

Applied Microbiology and Biotechnology

Volumn 74, Issue 2, 2007, Pages 263-272

  Liu, Jian ^a   Pedersen, Lars C ^b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Anticoagulant; Heparan sulfate; Heparin; Herpes simplex virus; Oligosaccharide; Sulfotransferase

Indexed keywords

BIOMEDICAL ENGINEERING; BIOSYNTHESIS; BLOOD VESSELS; COAGULATION; ORGANIC ACIDS; TISSUE;

ANTICOAGULANT; HEPARAN SULFATE; HEPARIN; HERPES SIMPLEX VIRUS; OLIGOSACCHARIDE; SULFOTRANSFERASE;

POLYSACCHARIDES;

ANTICOAGULANT AGENT; BACTERIAL POLYSACCHARIDE; BLOOD CLOTTING FACTOR; DRUG METABOLIZING ENZYME; HEPARAN SULFATE;

BACTERIUM; BLOOD; COAGULATION; DRUG DEVELOPMENT; ENZYME ACTIVITY; POLYSACCHARIDE;

ANTICOAGULATION; DRUG MECHANISM; DRUG SPECIFICITY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME SPECIFICITY; ENZYME SUBSTRATE; MOLECULAR INTERACTION; NONHUMAN; SHORT SURVEY; STRUCTURE ACTIVITY RELATION;

ANTICOAGULANTS; BIOTECHNOLOGY; CARBOHYDRATE CONFORMATION; HEPARITIN SULFATE; HUMANS; MODELS, MOLECULAR; POLYSACCHARIDES, BACTERIAL; SIMPLEXVIRUS; SULFOTRANSFERASES;

BACTERIA (MICROORGANISMS); SIMPLEXVIRUS;

EID: 33846850636     PISSN: 01757598     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00253-006-0722-x     Document Type: Short Survey

References (62)

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. Ashikari-Hada S, Habuchi H, Kariya Y, Itoh N, Reddi AH, Kimata K (2004) Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library. J Biol Chem 279:12346-12354
3. Atha DH, Lormeau J-C, Petitou M, Rosenberg RD, Choay J (1985) Contribution of monosaccharide residues in heparin binding to antithrombin III. Biochemistry 24:6723-6729
4. Avci FY, Karst NA, Linhardt RJ (2003) Synthetic oligosaccharides as heparin-mimetics displaying anticoagulant properties. Curr Pharm Des 9:2323-2335
5. Balagurunathan K, Beeler DL, Lech M, Wu ZL, Rosenberg RD (2003a) Chemoenzymatic synthesis of classical and non-classical anticoagulant heparan sulfate polysaccharides. J Biol Chem 278:52613-52621
6. 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
7. Becker RC (2004) Optimizing heparin compounds: a working construct for future antithrombotic drug development. J Thromb Thrombolysis 18:55-58
8. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M (1999) Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729-777
9. 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
10. Chen J, Duncan MB, Carrick K, Pope M, Liu J (2003) Biosynthesis of 3-O-sulfated heparan sulfate: unique substrate specificity of heparan sulfate 3-O-sulfotransferase isoform 5. Glycobiology 13:785-794
11. Chen J, Avci FY, Muñoz EM, McDowell LM, Chen M, Pedersen LC, Zhang L, Linhardt RJ, Liu J (2005) Enzymatically redesigning of biologically active heparan sulfate. J Biol Chem 280:42817-42825
12. Coombe DR, Kett WC (2005) Heparan sulfate-protein interactions: therapeutic potential through structure-function insights. Cell Mol Life Sci 62:410-424
13. Das S, Mallet J, Esnault J, Driguez P, Duchaussoy P, Sizun P, Herault J, Herbert J, Petitou M, Sinay P (2001) Synthesis of conformationally locked L-iduronic acid derivatives: direct evidence for a critical role of the skew-boat 2S0 conformer in the activation of antithrombin by heparin. Chemistry 7:4821-4834
14. de Paz JL, Noti C, Seeberger PH (2006) Microarrays of synthetic heparin oligosaccharides. J Am Chem Soc 128:2766-2767
15. Dementiev A, Petitou M, Herbert J-M, Gettins PG (2004) The ternary complex of antithrombin-anhydrothrombin-heparin reveals the basis of inhibitor specificity. Nat Struct Biol 11:867-863
16. Duncan MB, Chen J, Krise JP, Liu J (2004) The biosynthesis of anticoagulant heparan sulphate by the heparan sulphate 3-Osulphotransferase isoform 5. Biochim Biophys Acta 1671:34-43
17. 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
18. Esko JD, Selleck SB (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem 71:435-471
19. Ferro V, Don R (2003) The development of the novel angiogenesis inhibitor PI-88 as an anticancer drug. Australas Biotechnol 13:38-39
20. Gettins PG (2002) Serpin structure, mechanism, and function. Chem Rev 102:4751-4803
21. Habuchi H, Habuchi O, Kimata K (1995) Purification and characterization of heparan sulfate 6-sulfotransferase from the culture medium of Chinese hamster ovary cells. J Biol Chem 270:4172
22. Habuchi H, Tanaka M, Habuchi O, Yoshida K, Suzuki H, Ban K, Kimata K (2000) The occurrence of three isoforms of heparan sulfate 6-O-sulfotransferase having different specificities for hexuronic acid adjacent to the targeted N-sulfoglucosamine. J Biol Chem 275:2859-2868
23. Hacker U, Nybakken K, Perrimon N (2005) Heparan sulfate proteoglycans: the sweet side of development. Nat Rev Mol Cell Biol 6:530-541
24. HajMohammadi S, Enjyoji K, Princivalle M, Christi P, Lech M, Beeler DL, Rayburn H, Schwartz JJ, Barzegar S, de Agostini AI, Post MJ, Rosenberg RD, Shworak NW (2003) Normal levels of anticoagulant heparan sulfate are not essential for normal hemostasis. J Clin Invest 111:989-999
25. Herbert JM, Herault JP, Bernat A, Savi P, Schaeffer P, Driguez PA, Duchaussov P, Petitou M (2001) SR 123781A, a synthetic heparin mimetic. Thromb Haemost 85:852-860
26. Hirsh J, O'Donnell M, Weitz JI (2005) New anticoagulants. Blood 105:453-463
27. Ishihara M, Guo Y, Wei Z, Yang Z, Swiedler SJ, Orellana A, Hirschberg CB (1993) Regulation of biosynthesis of the basic fibroblast growth factor binding domains of heparan sulfate by heparan sulfate-N-deacetylase/N- sulfotransferase expression. J Biol Chem 268:20091-20095
28. Jin L, Abrahams P, Skinner R, Petitou M, Pike RN, Carrell RW (1997) The anticoagulant activation of antithrombin by heparin. Proc Natl Acad Sci USA 94:14683-14688
29. Kelton JG (2002) Heparin-induced thrombocytopenia: an overview. Blood Rev 16:77-80
30. Kobayashi M, Habuchi H, Habuchi O, Saito M, Kimata K (1996) Purification and characterization of heparan sulfate 2-sulfotransferase from cultured Chinese hamster ovary cells. J Biol Chem 271:7645-7653
31. Kraulis PJ (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24:946-950
32. Kuberan B, Beeler DL, Lawrence R, Lech M, Rosenberg R (2003) Rapid two-step synthesis of mitrin from heparosan: a replacement for heparin. J Am Chem Soc 125:12424-12425
33. Lee JC, Lu XA, Kulkarni SS, Wen YS, Hung SC (2004) Synthesis of heparin oligosaccharides. J Am Chem Soc 126:476-477
34. Li W, Johnson DJ, Esmon CT, Huntington JA (2004) Structure of the antithrombin-thrombin-heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat Struct Mol Biol 11:857-862
35. Lind T, Tufaro F, McCormick C, Lindahl U, Lidholt K (1998) The putative tumor suppressors EXT1 and EXT2 are glycosyltransferases required for the biosynthesis of heparan sulfate. J Biol Chem 273:26265-26268
36. Lindahl U, Kusche-Gullberg M, Kjellen L (1998) Regulated diversity of heparan sulfate. J Biol Chem 273:24979-24982
37. Lindahl U, Li J, Kusche-Gullberg M, Salmivirta M, Alaranta S, Veromaa T, Emies J, Roberts I, Taylor C, Oreste P et al (2005) Generation of "neoheparin" from E. Coli K5 capsular polysaccharide. J Med Chem 48:349-352
38. Liu J, Rosenberg RD (2002) Heparan sulfate D-glucosaminyl 3-O-sulfotransferase. In: N Taniguchi, M Fukuda (eds) Handbook of glycosyltransferases and their related genes. Springer, Berlin Heidelberg New York, pp 475-483
39. Liu J, Thorp SC (2002) Heparan sulfate and the roles in assisting viral infections. Med Res Rev 22:1-25
40. Liu J, Shworak NW, Fritze LMS, Edelberg JM, Rosenberg RD (1996) Purification of heparan sulfate D-glucosaminyl 3-O-sulfotransferase. J Biol Chem 271:27072-27082
41. Liu J, Shworak NW, Sinaÿ P, Schwartz JJ, Zhang L, Fritze LMS, Rosenberg RD (1999) Expression of heparan sulfate D-glucosaminyl 3-O-sulfotransferase isoforms reveals novel substrate specificities. J Biol Chem 274:5185-5192
42. McCormick C, Leduc Y, Martindale D, Mattison K, Esford LE, Dyer AP, Tufaro F (1998) The putative tumour suppressor EXT1 alters the expression of cell-surface heparan sulfate. Nat Genet 19:158-161
43. Merritt EA, Bacon DJ (1997) Raster3D: photorealistic molecular graphics. Methods Enzymol 277:505-524
44. 13C-NMR relaxation study of heparin-disaccharide interactions with tripeptide GRG and GKG. Biochem J 315:447-454
45. 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
46. Mulloy B, Forster M (2000) Conformation and dynamics of heparin and heparan sulfate. Glycobiology 10:1147-1156
47. Nyberg K, Ekblad M, Bergstrom T, Freeman C, Parish CR, Ferro V, Trybala E (2004) The low molecular weight heparan sulfate-mimetic, PI-88, inhibits cell-to-cell spread of herpes simplex virus. Antiviral Res 63:15-24
48. Oosta GM, Gardner WT, Beeler DL, Rosenberg R (1981) Multiple functional domains of the heparin molecule. Proc Natl Acad Sci USA 78:829-833
49. Petitou M, van Boeckel CAA (1992) Chemical synthesis of heparin fragments and analogues. Fortschr Chem Org Naturst 60:143-210
50. 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
51. Petitou M, Herault L-P, Bernat A, Driguez P-A, Duchaussoy P, Lormeau J-C, Herbert J-M (1999) Synthesis of thrombininhibiting heparin mimetics without side effects. Nature 398:417-422
52. Raman R, Sasisekharan V, Sasisekharan R (2005) Structural insights into biological roles of protein-glycosaminoglycan interactions. Chem Biol 12:267-277
53. Rosenberg RD, Showrak NW, Liu J, Schwartz JJ, Zhang L (1997) Heparan sulfate proteoglycans of the cardiovascular system: specific structures emerge but how is synthesis regulated? J Clin Invest 99:2062-2070
54. Sanderson RD, Yang Y, Suva LJ, Kelly T (2004) Heparan sulfate proteglycans and heparanase - partners in osteolytic tumor growth and metastasis. Matrix Biol 23:341-352
55. Sasisekharan R, Shriver Z, Venkataraman G, Narayanasami U (2002) Roles of heparin-sulphate glycosaminoglycans in cancer. Nat Rev Cancer 2:521-528
56. Shukla D, Liu J, Blaiklock P, Shworak NW, Bai X, Esko JD, Cohen GH, Eisenberg RJ, Rosenberg RD, Spear PG (1999) A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13-22
57. Shworak NW, Liu J, Fritze LMS, Schwartz JJ, Zhang L, Logeart D, Rosenberg RD (1997) Molecular cloning and expression of mouse and human cDNAs encoding heparan sulfate D-glucosaminyl 3-O-sulfotransferase. J Biol Chem 272:28008-28019
58. Shworak NW, Liu J, Petros LM, Zhang L, Kobayashi M, Copeland NG, Jenkins NA, Rosenberg RD (1999) Diversity of the extensive heparan sulfate D-glucosaminyl 3-O-sulfotransferase (3-OST) multigene family. J Biol Chem 274:5170-5184
59. Smeds E, Habuchi H, Do A-T, Hjertson E, Grundberg H, Kimata K, Lindahl U, Kusche-Gullberg M (2003) Substrate specificities of mouse heparan sulphate glucosaminyl 6-O-sulfotransferases. Biochem J 372(Pt 2):371-380
60. Taylor KR, Gallo RL (2006) Glycosaminoglycans and their proteoglycans: host-associated molecular patterns for initiation and modulation of inflammation. FASEB J 20:9-22
61. Xia G, Chen J, Tiwari V, Ju W, Li J-P, Malmström 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
62. 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