Heparan sulfate proteoglycans of the cardiovascular system: Specific structures emerge but how is synthesis regulated?

Journal of Clinical Investigation

Volumn 99, Issue 9, 1997, Pages 2062-2070

  Rosenberg, Robert D ^a,b   Shworak, Nicholas W ^a,b   Liu, Jian ^a   Schwartz, John J ^a   Zhang, Lijuan ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B; APOLIPOPROTEIN E; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; GAMMA INTERFERON; GLYPICAN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 3; LIPOPROTEIN LIPASE; PERLECAN; PROTEINASE INHIBITOR; PROTEOHEPARAN SULFATE; SYNDECAN; VASCULOTROPIN;

BLOOD CLOTTING; CARBOHYDRATE ANALYSIS; CARDIOVASCULAR SYSTEM; CELL ADHESION; EXTRACELLULAR MATRIX; HUMAN; LIPOPROTEIN METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEOGLYCAN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION;

EID: 0030973187     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119377     Document Type: Review

References (88)

1. Simionescu, M., N. Simionescu, J.E. Sibert, and G.E. Palade. 1981. Differentiated microdomains on the luminal surface of the capillary endothelium. II. Partial characterization of their anionic sites. J. Cell Biol. 90:614-621.
2. Conrad, H.E. 1989. Structure of heparan sulfate and dermatan sulfate. Ann. NY Acad. Sci. 556:18-28.
3. Yanagishita, M., and V.C. Hascall. 1992. Cell surface heparan sulfate proteoglycans. J. Biol. Chem. 267:9451-9454.
4. Nathan, A., M.A. Nugent, and E.R. Edelman. 1995. Tissue engineered perivascular endothelial cell implants regulate vascular injury. Proc. Natl. Acad. Sci. USA. 92:8130-8134.
5. Yost, H.J. 1992. Regulation of vertebrate left-right symmetries by extracellular matrix. Nature (Lond.). 357:158-161.
6. Sanderson, R.D., J.E. Turnbull, J.T. Gallagher, and A.D. Lander. 1994. Structure of heparan sulfate regulates proteoglycan function and cell behavior. J. Biol. Chem. 269:13100-13106.
7. Guyton, J.R., R.D. Rosenberg, A.W. Clowes, and M.J. Karnovsky. 1980. Inhibition of rat arterial smooth muscle cell proliferation by heparin. In vivo studies with anticoagulant and nonanticoagulant heparin. Circ. Res. 46:625-634
8. Itoh, K., and S.Y. Sokol. 1994. Heparan sulfate proteoglycans are required for mesoderm formation in Xenopus embryos. Development (Camb.). 120:2703-2711.
9. Nikkari, S.T., H.T. Jarvelainen, T.N. Wight, M. Ferguson, and A.W. Clowes. 1994. Smooth muscle cell expression of extracellular matrix genes after arterial injury. Am. J. Pathol. 144:1348-1356.
10. Bernfield, M., R. Kokenyesi, M. Kato, M.T. Hinkes, J. Spring, R.L. Gallo, and E.J. Lose. 1992. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell Biol. 8:365-393.
11. Asundi, V.K., and D.J. Carey. 1995. Self-association of N-syndecan (syndecan-3) core protein is mediated by a novel structural motif in the transmembrane domain and ectodomain flanking region. J. Biol. Chem. 270:26404-26410.
12. Oh, E.-S., A. Woods, and J.R. Couchman. 1997. Multimerization of the cytoplasmic domain of syndecan-4 is required for its ability to activate protein kinase C. J. Biol. Chem. In press.
13. Baciu, P.C., and P.F. Goetinck. 1995. Protein kinase C regulates the recruitment of syndecan-4 into focal contacts. Mol. Biol. Cell. 6:1503-1513.
14. Carey, D.J., K.M. Bendt, and R.C. Stahl. 1996. The cytoplasmic domain of syndecan-1 is required for cytoskeleton association but not detergent insolubility. Identification of essential cytoplasmic domain residues. J. Biol. Chem. 271:15253-15260.
15. Itano, N., K. Oguri, Y. Nagayasu, Y. Kusano, H. Nakanishi, G. David, and M. Okayama. 1996. Phosphorylation of a membrane-intercalated proteoglycan, syndecan-2, expressed in a stroma-inducing clone from a mouse Lewis lung carcinoma. Biochem. J. 315:925-930.
16. Weksberg, R., J.A. Squire, and D.M. Templeton. 1996. Glypicans: a growing trend. Nat. Genet. 12:225-227.
17. Mertens, G., B. Van der Schueren, H. van den Berghe, and G. David. 1996. Heparan sulfate expression in polarized epithelial cells. The apical sorting of glypican (GPI-anchored proteoglycan) is inversely related to its heparan sulfate content. J. Cell Biol. 132:487-497.
18. Noonan, D.M., A. Fulle, P. Valente, S. Cai, E. Horigan, M. Sasaki, Y. Yamada, and J.R. Hassell. 1991. The complete sequence of perlecan, a basement membrane heparan sulfate proteoglycan. reveals extensive similarity with laminin A chain, low density lipoprotein-receptor, and the neural cell adhesin molecule. J. Biol. Chem. 266:22939-22947.
19. Murdoch, A.D., G.R. Dodge. I. Cohen, R.S. Tuan, and R.V. Iozzo. 1992. Primary structure of the human heparan sulfate proteoglycan from basement membrane (HSPG2/perlecan). A chimeric molecule with multiple domains homologous to the low density lipoprotein receptor, laminin, neural cell adhesion molecules, and epidermal growth factor. J. Biol. Chem. 267:8544-8557.
20. Sugahara, K., H. Tsuda, K. Yoshida, S. Yamada, T. de Beer, and J.F. Vliegenthart. 1995. Structure determination of the octa-and decasaccharide sequences isolated from the carbohydrate-protein linkage region of porcine intestinal heparin. J. Biol. Chem. 270:22914-22923.
21. Esko, J.D., and L. Zhang. 1996. Influence of core protein sequence on glycosaminoglycan assembly. Curr. Opin. Struct. Biol. 6:663-670.
22. David, G., V. Lories, B. Decock, P. Marynen, J.-J. Cassiman, and H. Van den Berghe. 1990. Molecular cloning of a phosphatidylinositol-anchored membrane heparan sulfate proteoglycan from human lung fibroblasts. J. Cell Biol. 111:3165-3176.
23. Dolan, M., T. Horchar, B. Rigatti, and J.R. Hassell. 1997. Identification of sites in domain I of perlecan that regulate heparan sulfate synthesis. J. Biol. Chem. 272:4316-4322.
24. Shworak, N.W., M. Shirakawa, R.C. Mulligan, and R.D. Rosenberg. 1994. Characterization of ryudocan glycosaminoglycan acceptor sites. J. Biol. Chem. 269:21204-21214.
25. Lindahl, U. 1989. Biosynthesis of heparin and related polysaccharides. In Heparin, Chemical and Biological Properties: Clinical Applications. D.A. Lane and U. Lindahl, editors. Edward Arnold. London. 159-191.
26. Lind, T., U. Lindahl, and K. Lidholt. 1993. Biosynthesis of heparin/ heparan sulfate. Identification of a 70-kDa protein catalyzing both the D-glucuronosyl-and the N-acetyl-D-glucosaminyltransferase reactions. J. Biol. Chem. 268:20706-20708.
27. Kobayashi, M., H. Habuchi, O. Habuchi, M. Saito, and K. Kimata. 1996. Purification and characterization of heparan sulfate 2-sulfotransferase from cultured Chinese hamster ovary cells. J. Biol. Chem. 271:7645-7653.
28. Habuchi, H., O. Habuchi, and K. Kimata. 1995. Purification and characterization of heparan sulfate 6-sulfotransferase from the culture medium of Chinese hamster ovary cells. J. Biol. Chem. 270:4172-4179.
29. Liu, J., N.W. Shworak, L.M.S. Fritze, J.M. Edelberg, and R.D. Rosenberg. 1996. Purification of heparan sulfate D-glucosaminyl 3-O-sulfotransferase. J. Biol. Chem. 271:27072-27082.
30. Orellana, A., C.B. Hirschberg, Z. Wei, S.J. Swiedler, and M. Ishihara. 1994. Molecular cloning and expression of a glycosaminoglycan N-acetylglucosaminyl N-deacetylase/N-sulfotransferase from a heparin-producing cell line. J. Biol. Chem. 269:2270-2276.
31. Hashimoto, Y., A. Orellana, G. Oil, and C.B. Hirschberg. 1992. Molecular cloning and expression of rat liver N-heparan sulfate sulfotransferase. J. Biol. Chem. 267:15744-15750.
32. Eriksson, I., D. Sandbäck, B. Ek, U. Lindahl, and L. Kjellén. 1994. cDNA cloning and sequencing of mouse mastocytoma glucosaminyl N-deacetylase/N-sulfotransferase, an enzyme involved in the biosynthesis of heparin. J. Biol. Chem. 269:10438-10443.
33. Nelson, R.M., A. Venot, M.P. Bevilacqua, R.J. Linhardt, and I. Stamenkovic. 1995. Carbohydrate-protein interactions in vascular biology. Annu. Rev. Cell Dev. Biol. 11:601-631.
34. Olwin, B.B., and A. Rapraeger. 1992. Repression of myogenic differentiation by aFGF, bFGF, and K-FGF is dependent on cellular heparan sulfate. J. Cell Biol. 118:631-639.
35. Ornitz, D.M., and P. Leder. 1992. Ligand specificity and heparin dependence of fibroblast growth factor receptors 1 and 3. J. Biol. Chem. 267:16305-16311.
36. Faham, S., R.E. Hileman, J.R. Fromm, R.J. Linhardt, and D.C. Rees. 1996. Heparin structure and interactions with basic fibroblast growth factor. Science (Wash. DC). 271:1116-1120.
37. Ornitz, D.M., A.B. Herr, M. Nilsson, J. Westman, C.-M. Svahn, and G. Waksman. 1995. FGF binding and FGF receptor activation by synthetic heparan-derived di-and trisaccharides. Science (Wash. DC). 268:432-436.
38. Yayon, A., M. Klagsbrun, J.D. Esko, P. Leder, and D.M. Ornitz. 1991. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell. 64:841-848.
39. Kan, M., F. Wang, J. Xu, J.W. Crabb, J. Hou, and W.L. McKeehan. 1993. An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science (Wash. DC). 259:1918-1921.
40. Brickman, Y.G., M.D. Ford, D.H. Small, P.F. Bartlet, and V. Nurcombe. 1995. Heparan sulfates mediate the binding of basic fibroblast growth factor to a specific receptor on neural precursor cells. J. Biol. Chem. 270:24941-24948.
41. Habuchi, H., S. Suzuki, T. Saito, T. Tamura, T. Harada, K. Yoshida, and K. Kimata. 1992. Structure of a heparan sulphate oligosaccharide that binds to basic fibroblast growth factor. Biochem. J. 285:805-813.
42. Maccarana, M., B. Casu, and U. Lindahl. 1993. Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor. J. Biol. Chem. 268:23898-23905.
43. Turnbull, J.E., D.G. Fernig, Y. Ke, M.C. Wilkinson, and J.T. Gallagher. 1992. Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J. Biol. Chem. 267:10337-10341.
44. Bai, X., and J.D. Esko. 1996. Mutant defective in heparan sulfate hexuronic acid 2-O-sulfation. J. Biol. Chem. 271:17711-17717.
45. Guimond, S., M. Maccarana, B.B. Olwin, U. Lindahl, and A.C. Rapraeger. 1993. Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4. J. Biol. Chem. 268:23906-23914.
46. Krufka, A., S. Guimond, and A.C. Rapraeger. 1996. Two hierarchies of FGF-2 signaling in heparin: mitogenic stimulation and high-affinity binding/receptor transphosphorylation. Biochemistry. 35:11131-11141.
47. Ueno, H., M. Gunn, K. Dell, A.J. Tseng, and L. Williams. 1992. A truncated form of fibroblast growth factor receptor 1 inhibits signal transduction by multiple types of fibroblast growth factor receptor. J. Biol. Chem. 267:1470-1476.
48. Aviezer, D., D. Hecht, M. Safran, M. Eisinger, G. David, and A. Yayon. 1994. Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell. 79:1005-1013.
49. Perrimon, N. 1996. Serpentine proteins slither into the wingless and hedgehog fields. Cell. 86:513-516.
50. Reichsman, F., L. Smith, and S. Cumberledge. 1996. Glycosaminoglycans can modulate extracellular localization of the wingless protein and promote signal transduction. J. Cell Biol. 135:819-827.
51. Lin, X., U. Haecker, and N. Perrimon. 1996. Mutations in the synthesis of heparan sulfate result in defects of wg signaling. Wnt meeting 1996, Stanford University.
52. Nakato, H., T.A. Futch, and S.B. Selleck. 1995. The division abnormally delayed (dally) gene: a putative integral membrane proteoglycan required for cell division patterning during postembryonic development of the nervous system in Drosophila. Development (Camb.). 121:3687-3702.
53. Cheng, C.F., A. Oosta, A. Bensadoun, and R.D. Rosenberg. 1981. Binding of lipoprotein lipase to endothelial cells in culture. J. Biol. Chem. 256: 12893-12896.
54. Saxena, U., M.G. Klein, and I.J. Goldberg. 1991. Identification and characterization of the endothelial cell surface lipoprotein lipase receptor. J. Biol. Chem. 266:17516-17521.
55. Lookene, A., O. Chevreuil, P. Ostergaard, and G. Olivecrona. 1996. Interaction of lipoprotein lipase with heparin fragments and with heparan sulfate: stoichiometry, stabilization, and kinetics. Biochemistry. 35:12155-12163.
56. Goldberg, I.J. 1996. Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J. Lipid Res. 37:693-707.
57. Saxena, U., M.G. Klein, and I.J. Goldberg. 1991. Transport of lipoprotein lipase across endothelial cells. Proc. Natl. Acad. Sci. USA. 88:2254-2258.
58. Eisenberg, S., E. Sehayek, T. Olivecrona, and I. Vlodavsky. 1992. Lipoprotein lipase enhances binding of lipoproteins to heparan sulfate on cell surfaces and extracellular matrix. J. Clin. Invest. 90:2013-2021.
59. Ji, Z.S., S. Fazio, and R.W. Mahley. 1994. Variable heparan sulfate proteoglycan binding of apolipoprotein E variants may modulate the expression of type III hyperlipoproteinemia. J. Biol. Chem. 269:13421-13428.
60. Obunike, J.C., I.J. Edwards, S.C. Rumsey, L.K. Curtiss, W.D. Wagner, R.J. Deckelbaum, and I.J. Goldberg. 1994. Cellular differences in lipoprotein lipase-mediated uptake of low density lipoproteins. J. Biol. Chem. 269:13129-13135.
61. Fernandez-Borja, M., D. Bellido, E. Vilella, G. Olivecrona, and S. Vilaro. 1996. Lipoprotein lipase-mediated uptake of lipoprotein in human fibroblasts: evidence for an LDL receptor-independent internalization pathway. J. Lipid Res. 37:464-481.
62. van Tilbeurgh, H., A. Roussel, J.M. Lalouel, and C. Cambillau. 1994. Lipoprotein lipase. Molecular model based on the pancreatic lipase x-ray structure: consequences for heparin binding and catalysis. J. Biol. Chem. 269:4626-4633.
63. Cardin, A.C., and H.R.J. Weintraub. 1989. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis. 9:21-32.
64. Hata, A., D.N. Ridinger, S. Sutherland, M. Emi, Z. Shuhua, R.L. Myers, K. Ren, T. Cheng, I. Inoue, D.E. Wilson, P.-H. Iverius, and J.-M. Lalouel. 1993. Binding of lipoprotein lipase to heparin. Identification of five critical residues in two distinct segments of the amino-terminal domain. J. Biol. Chem. 268: 8447-8457.
65. Nielsen, M.S., J. Brejning, R. García, H. Zhang, M.R. Hayden, S. Vilaró, and J. Gliemann. 1997. Segments in the C-terminal folding domain of lipoprotein lipase important for binding to the low density lipoprotein receptor-related protein and to heparan sulfate proteoglycans. J. Biol. Chem. 272:5821-5827.
66. Hoogewerf, A.J., L.A. Cisar, D.C. Evans, and A. Bensadoun. 1991. Effect of chlorate on the sulfation of lipoprotein lipase and heparan sulfate proteoglycans. Sulfation of heparan sulfate proteoglycans affects lipoprotein lipase degradation. J. Biol. Chem. 266:16564-16571.
67. Parthasarathy, N., I.J. Goldberg, P. Sivaram, B. Mulloy, D.M. Flory, and W.D. Wagner. 1994. Oligosaccharide sequences of endothelial cell surface heparan sulfate proteoglycan with affinity for lipoprotein lipase. J. Biol. Chem. 269:22391-22396.
68. Larnkjær, A., A. Nykjær, G. Olivecrona, H. Thogersen, and P.B. Østergaard. 1995. Structure of heparin fragments with high affinity for lipoprotein lipase and inhibition of lipoprotein lipase binding to alpha 2-macroglobulin-receptor/low-density-lipoprotein-receptor-related protein by heparin fragments. Biochem. J. 307:205-214.
69. Rosenberg, R.D., and P.S. Damus. 1973. The purification and mechanism of action of human antithrombin-heparin cofactor. J. Biol. Chem. 248: 6490-6505.
70. Carrell, R.W., P.E. Stein, G. Fermi, and M.R. Wardell. 1994. Biological implications of a 3 Å structure of dimeric antithrombin. Structure (Lond.). 2: 257-270.
71. Gettins, P.G.W., B. Fan, B.C. Crews, and I.V. Turko. 1993. Transmission of conformational change from the heparin binding site to the reactive center of antithrombin. Biochemistry. 32:8385-8389.
72. Shworak, N.W., and R.D. Rosenberg. 1995. Antithrombotic defence potential of the blood vessel wall: the heparan sulfate-antithrombin pathway. In The Endothelial Cell in Health and Disease. J.R. Vane, G.V.R. Born, and D. Welzel, editors. Schattauer, Stuttgart. 119-146.
73. Olson, S.T., and I. Bjork. 1994. Regulation of thrombin activity by anti-thrombin and heparin. Semin. Thromb. Hemostasis. 20:373-409.
74. Lam, L.H., J.E. Silbert, and R.D. Rosenberg. 1976. The separation of active and inactive forms of heparin. Biochem. Biophys. Res. Commun. 69: 570-577.
75. Rosenberg, R.D., and L. Lam. 1979. Correlation between structure and function of heparin. Proc. Natl. Acad. Sci. USA. 76:1218-1222.
76. Lindahl, U., G. Bäckström, L. Thunberg, and I.G. Leder. 1980. Evidence for a 3-O-sulfated D-glucosamine residue in the antithrombin-binding sequence of heparin. Proc. Natl. Acad. Sci. USA. 77:6551-6555.
77. Choay, J., M. Petitou, J.C. Lormeau, P. Sinaÿ, B. Casu, and G. Gatti. 1983. Structure-activity relationship in heparin: a synthetic pentasaccharide with high affinity for antithrombin III and eliciting high anti-factor Xa activity. Biochem. Biophys. Res. Commun. 116:492-499.
78. Atha, D.H., J.C. Lormeau, M. Petitou, R.D. Rosenberg, and J. Choay. 1985. Contribution of monosaccharide residues in heparin binding to anti-thrombin III. Biochemistry. 24:6723-6729.
79. Atha, D.H., J.C. Lormeau, M. Petitou, R.D. Rosenberg, and J. Choay. 1987. Contribution of 3-O-and 6-O-sulfated glucosamine residues in the heparin-induced conformational change in antithrombin III. Biochemistry. 26: 6454-6461.
80. Casu, B. 1985. Structure and biological activity of heparin. Adv. Carbohydr. Chem. Biochem. 43:51-134.
81. Marcum, J.A., and R.D. Rosenberg. 1989. The biochemistry, cell biology, and pathophysiology of anticoagulantly active heparin-like molecules of the vessel wall. In Heparin. Chemical and Biological Properties: Clinical Applications. D.A. Lane and U. Lindahl, editors. Edward Arnold, London. 275-294.
82. Shworak, N.W., M. Shirakawa, S. Colliec-Jouault, J. Liu, R.C. Mulligan, L.K. Birinyi, and R.D. Rosenberg. 1994. Pathway-specific regulation of the synthesis of anticoagulantly active heparan sulfate. J. Biol. Chem. 269:24941-24952.
83. Colliec-Jouault, S., N.W. Shworak, J. Liu, A.I. de Agostini, and R.D. Rosenberg. 1994. Characterization of a cell mutant specifically defective in the synthesis of anticoagulantly active heparan sulfate. J. Biol. Chem. 269:24953-24958.
84. Shworak, N.W., L.M.S. Fritze, J. Liu, L.D. Butler, and R.D. Rosenberg. 1996. Cell-free synthesis of anticoagulant heparan sulfate reveals a limiting activity which modifies a nonlimiting precursor pool. J. Biol. Chem. 271:27063-27071.
85. Edge, A.S., and R.G. Spiro. 1990. Characterization of novel sequences containing 3-O-sulfated glucosamine in glomerular basement membrane heparan sulfate and localization of sulfated disaccharides to a peripheral domain. J. Biol. Chem. 265:15874-15881.
86. Kanwar, Y.S., A. Linker, and M.G. Farquhar. 1980. Increased permeability of the glomerular basement membrane to ferritin after removal of glycosaminoglycans (heparan sulfate) by enzyme digestion. J. Cell Biol. 86:688-693.
87. Ishihara, M., Y. Guo, Z. Wei, Z. Yang, S.J. Swiedler, A. Orellana, and C.B. Hirschberg. 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.
88. Cheung, W.-F., I. Eriksson, M. Kusche-Gullberg, U. Lindahl, and L. Kjellén. 1996. Expression of the mouse mastocytoma glucosaminyl N-deacetylase/N-sulfotransferase in human kidney 293 cells results in increased N-sulfation of heparan sulfate. Biochemistry. 35:5250-5256.