The Activities of Heparan Sulfate and its Analogue Heparin are Dictated by Biosynthesis, Sequence, and Conformation

REFERENCES

• Turnbull J., Powell A., Guimond S. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell. Biol. 2001; 11: 75–82
   PubMed Web of Science ®Google Scholar
• Warner R.G., Hundt C., Weiss S., Turnbull J.E. Identification of the heparan sulfate binding sites in the cellular prion protein. J. Biol. Chem. 2002; 277: 18421–18430
   PubMed Web of Science ®Google Scholar
• Snow A.D., Mar H., Nochlin D., Kimata K., Kato M., Suzuki S., Hassell J., Wight T.N. The presence of heparan sulfate proteoglycans in the neuritic plaques and congophilic angiopathy in Alzheimer's disease. Am. J. Pathol. 1988; 133: 456–463
   PubMed Web of Science ®Google Scholar
• Patel M., Yanagishita M., Roderiquez G., Bou-Habib D.C., Oravecz T., Hascall V.C., Norcross M.A. Cell-surface heparan sulfate proteoglycan mediates HIV-1 infection of T-cell lines. AIDS Res. Hum Retrovir. 1993; 9: 167–174
   PubMed Web of Science ®Google Scholar
• Pancake S.J., Holt G.D., Mellouk S., Hoffman S.L. Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. J. Cell Biol. 1992; 117: 1351–1357
   PubMed Web of Science ®Google Scholar
• Scarselli M., Serruto D., Montanari P., Capecchi B., Adu-Bobie J., Veggi D., Rappuoli R., Pizza M., Arico B. Neisseria meningitidis NhhA is a multifunctional trimeric autotransporter adhesin. Mol. Microbiol. 2006; 61: 631–644
   PubMed Web of Science ®Google Scholar
• Lin Y.L., Lei H.Y., Lin Y.S., Yeh T.M., Chen S.H., Liu H.S. Heparin inhibits dengue-2 virus infection of five human liver cell lines. Antiviral. Res. 2002; 56: 93–96
   PubMed Web of Science ®Google Scholar
• Patey S.J., Edwards E.A., Yates E.A., Turnbull J.E. Heparin derivatives as inhibitors of BACE-1, the Alzheimer's beta-secretase, with reduced activity against factor Xa and other proteases. J. Med. Chem. 2006; 49: 6129–6132
   PubMed Web of Science ®Google Scholar
• Rabenstein D.L. Heparin and heparan sulfate: structure and function. Nat. Prod. Rep. 2002; 19: 312–331
   PubMed Web of Science ®Google Scholar
• Aikawa J., Esko J.D. Molecular cloning and expression of a third member of the heparan sulfate/heparin GlcNAc N-deacetylase/N-sulfotransferase family. J. Biol. Chem. 1999; 274: 2690–2695
   PubMed Web of Science ®Google Scholar
• Habuchi H., Tanaka M., Habuchi O., Yoshida K., Suzuki H., Ban K., Kimata K. 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. 2000; 275: 2859–2868
   PubMed Web of Science ®Google Scholar
• Shworak N.W., Liu J., Petros L.M., Zhang L., Kobayashi M., Copeland N.G., Jenkins N.A., Rosenberg R.D. Multiple isoforms of heparan sulfate D-glucosaminyl 3-O-sulfotransferase. Isolation, characterization, and expression of human cdnas and identification of distinct genomic loci. J. Biol. Chem. 1999; 274: 5170–5184
   PubMed Web of Science ®Google Scholar
• Kobayashi M., Habuchi H., Yoneda M., Habuchi O., Kimata K. Molecular cloning and expression of Chinese hamster ovary cell heparan-sulfate 2-sulfotransferase. J. Biol. Chem. 1997; 272: 13980–13985
   Google Scholar
• Li J., Hagner-McWhirter A., Kjellen L., Palgi J., Jalkanen M., Lindahl U. Biosynthesis of heparin/heparan sulfate. cDNA cloning and expression of D-glucuronyl C5-epimerase from bovine lung. J. Biol. Chem. 1997; 272: 28158–28163
   PubMed Web of Science ®Google Scholar
• Allen B.L., Rapraeger A.C. Spatial and temporal expression of heparan sulfate in mouse development regulates FGF and FGF receptor assembly. J. Cell Biol. 2003; 163: 637–648
   PubMed Web of Science ®Google Scholar
• Jayson G.C., Lyon M., Paraskeva C., Turnbull J.E., Deakin J.A., Gallagher J.T. Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro. J. Biol. Chem. 1998; 273: 51–57
   PubMed Web of Science ®Google Scholar
• Kato M., Wang H., Bernfield M., Gallagher J.T., Turnbull J.E. Cell surface syndecan-1 on distinct cell types differs in fine structure and ligand binding of its heparan sulfate chains. J. Biol. Chem. 1994; 269: 18881–18890
   PubMed Web of Science ®Google Scholar
• Turnbull J.E., Gallagher J.T. Distribution of iduronate 2-sulphate residues in heparan sulphate. Evidence for an ordered polymeric structure. Biochem. J. 1991; 273(Pt 3)553–559
   PubMedGoogle Scholar
• Lindahl U., Kusche-Gullberg M., Kjellen L. Regulated diversity of heparan sulfate. J. Biol. Chem. 1998; 273: 24979–24982
   PubMed Web of Science ®Google Scholar
• Nugent M.A. Heparin sequencing brings structure to the function of complex oligosaccharides. Proc. Natl. Acad. Sci. USA 2000; 97: 10301–10303
   PubMed Web of Science ®Google Scholar
• Rapraeger A.C., Guimond S., Krufka A., Olwin B.B. Regulation by heparan sulfate in fibroblast growth factor signaling. Methods Enzymol. 1994; 245: 219–240
   PubMed Web of Science ®Google Scholar
• Rapraeger A.C., Krufka A., Olwin B.B. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 1991; 252: 1705–1708
   PubMed Web of Science ®Google Scholar
• Zhang L., Lawrence R., Frazier B.A., Esko J.D. CHO glycosylation mutants: proteoglycans. Methods Enzymol. 2006; 416: 205–221
   PubMedGoogle Scholar
• Ornitz D.M., Xu J., Colvin J.S., McEwen D.G., MacArthur C.A., Coulier F., Gao G., Goldfarb M. Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 1996; 271: 15292–15297
   PubMed Web of Science ®Google Scholar
• Nieduszynski I.A., Atkins E.D. Conformation of the mucopolysaccharides. X-ray fibre diffraction of heparin. Biochem. J. 1973; 135: 729–733
   PubMed Web of Science ®Google Scholar
• Mulloy B., Forster M.J., Jones C., Davies D.B. N m.r.and molecular-modelling studies of the solution conformation of heparin. Biochem. J. 1993; 293(Pt 3)849–858
   PubMedGoogle Scholar
• Hricovini M., Guerrini M., Torri G., Piani S., Ungarelli F. Conformational analysis of heparin epoxide in aqueous solution. An NMR relaxation study. Carbohydr. Res. 1995; 277: 11–23
   PubMed Web of Science ®Google Scholar
• Hricovini M., Guerrini M., Torri G., Casu B. Motional properties of E. coli polysaccharide K5 in aqueous solution analyzed by NMR relaxation measurements. Carbohydr. Res. 1997; 300: 69–76
   PubMed Web of Science ®Google Scholar
• Mackie W., Yates E.A., Lamba D. Structural studies of O-sulfated D-glucosamines - the crystal and molecular-structures of 2-amino-2-deoxy-alpha/beta-D-glucopyranose 3-sulfate (free acid) and 2-amino-2-deoxy-beta-D-glucopyranose 6-sulfate (free-base). Carbohydr. Res. 1995; 266: 65–74
   Web of Science ®Google Scholar
• Yates E.A., Mackie W., Lamba D. The crystal and molecular structure of 2-sulfamino-2-deoxy-alpha-D-glucopyranose sodium salt.2H2O (glucosamine 2-sulfate). Int. J. Biol. Macromol. 1995; 17: 219–226
   PubMed Web of Science ®Google Scholar
• Ayotte L., Perlin A.S. N.m.r. spectroscopic observations related to the function of sulfate groups in heparin. Calcium binding vs. biological activity. Carbohydr. Res. 1986; 145: 267–277
   PubMed Web of Science ®Google Scholar
• Rabenstein D.L., Robert J.M., Peng J. Multinuclear magnetic resonance studies of the interaction of inorganic cations with heparin. Carbohydr. Res. 1995; 278: 239–256
   PubMed Web of Science ®Google Scholar
• Angulo J., De Paz J.L., Nieto P.M., Martin-Lomas M. Interaction of heparin with Ca2+. A model study with synthetic heparin-like hexasaccharide. Isr. J. Chem. 2000; 40: 289–299
   Web of Science ®Google Scholar
• Yates E.A., Santini F., De Cristofano B., Payre N., Cosentino C., Guerrini M., Naggi A., Torri G., Hricovini M. Effect of substitution pattern on 1H, 13C NMR chemical shifts and 1J(CH) coupling constants in heparin derivatives. Carbohydr. Res. 2000; 329: 239–247
   PubMed Web of Science ®Google Scholar
• Yates E.A., Santini F., Guerrini M., Naggi A., Torri G., Casu B. 1H and 13C NMR spectral assignments of the major sequences of twelve systematically modified heparin derivatives. Carbohydr. Res. 1996; 294: 15–27
   PubMed Web of Science ®Google Scholar
• Morris E.R., Rees D.A., Sanderson G.R., Thom D. Conformation and Circular-Dichroism of Uronic Acid Residues in Glycosides and Polysaccharides. J. Chem. Soc. Perkin Transactions. 1975; 2: 1418–1425
   Google Scholar
• Rudd T.R., Guimond S.E., Skidmore M.A., Duchesne L., Guerrini M., Torri G., Cosentino C., Brown A., Clarke D.T., Turnbull J.E., Fernig D.G., Yates E.A. Influence of substitution pattern and cation binding on conformation and activity in heparin derivatives. Glycobiology 2007; 17: 983–993
   PubMed Web of Science ®Google Scholar
• Almond A., Sheehan J.K. Predicting the molecular shape of polysaccharides from dynamic interactions with water. Glycobiology 2003; 13: 255–264
   PubMed Web of Science ®Google Scholar