A novel role for nitric oxide in the endogenous degradation of heparan sulfate during recycling of glypican-1 in vascular endothelial cells

Glycobiology

Volumn 10, Issue 6, 2000, Pages 577-586

  Mani, Katrin ^b   Jönsson, Mats ^b   Edgren, Gudrun ^b   Belting, Mattias ^b   Fransson, Lars Åke ^a,b  

^a Dept of Cell and Molec Biology 1 ^*  (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Brefeldin A; Glypican; Heparan sulfate; Nitric oxide; Suramin

Indexed keywords

BREFELDIN A; GLYPICAN; HEPARAN SULFATE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRITE; OLIGOSACCHARIDE; PROTEOGLYCAN; SURAMIN;

ARTICLE; DEGRADATION; DEPOLYMERIZATION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; VASCULAR ENDOTHELIUM;

EID: 0343729304     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/10.6.577     Document Type: Article

References (41)

1. Anderson, R.G.W. (1998) The caveolae membrane system. Annu. Rev. Biochem., 67, 199-225.
2. Bai, X., Bame, K.J., Habuchi, H., Kimata, K. and Esko, J.D. (1997) Turnover of heparan sulfate depends on 2-O-sulfation of uronic acids., J. Biol. Chem., 272, 23172-23179.
3. Belting, M., Persson, S. and Fransson, L.-Å. (1999) Proteoglycan involvement in polyamine uptake. Biochem. J., 338, 317-323.
4. Bernfield, M., Götte, M., Park, P.W., Reizes, O., Fitzgerald, M.L., Lincecum, J. and Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem., 68, 729-777.
5. Björnsson, S. (1993) Simultaneous preparation and quantitation of proteoglycans by precipitation with Alcian Blue. Anal. Biochem., 210, 282-291.
6. David, G. (1993) Integral membrane heparan-sulfate proteoglycans. FASEB J., 7, 1023-1030.
7. David, G., Lories, V., Decock, B., Marynen, P., Cassiman J.-J. and Van den Berghe, H. (1990) Molecular cloning of a phosphatidylinositol-anchored membrane heparan sulfate proteoglycan from human lung fibroblasts. J. Biol. Chem., 267, 4870-4877.
8. Edgren, G., Havsmark, B., Jönsson, M. and Fransson L.-Å. (1997) Glypican (heparan sulfate proteoglycan) is palmitoylated, deglycanated and reglycanated during recycling in skin fibroblasts. Glycobiology, 7, 103-112.
9. Feron, O., Saldana, F., Michel, J.B. and Michel, T. (1998) The endothelial nitricoxide synthase-caveolin regulatory cycle. J. Biol. Chem., 273, 3125-3128.
10. Fransson, L.-Å., Karlsson, P. and Schmidtchen, A. (1992) Effects of cycloheximide, brefeldin A, suramin, heparin and primaquine on proteoglycan and glycosaminoglycan biosynthesis in human embryonic skin fibroblasts. Biochim. Biophys. Acta, 1137, 287-297.
11. Fransson, L.-Å., Edgren, G., Havsmark, B. and Schmidtchen, A. (1995) Recycling of a glycosylphosphatidyl-inositol-anchored heparan sulfate proteoglycan (glypican) in skin fibroblasts. Glycobiology, 5, 407-415.
12. Fransson, L.-Å., Belting, M., Edgren, G., Jönsson, M., Mani, K., Schmidtchen, A. and Wiik, P. (1998) Degradation and reprocessing of heparan sulfate in recycling glypican (heparan sulfate proteoglycan). Trends Glycosci. Glycotechnol, 10, 81-94.
13. Garcia-Cardenas, G., Oh, P., Liu, J., Schnitzer, J.E. and Sessa, W.C. (1996) Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc. Natl. Arad. Sci. USA, 93, 6448-6453.
14. Godder, K., Vlodavsky, I., Eldor, A., Weksler, B.B., Haimovitz-Friedmann, A. and Fuks, Z. (1991) Heparanase activity in cultured endothelial cells. J. Cell Physiol., 148, 274-280.
15. Humphries, D.E., Sullivan, B.M., Aleixo, M.D. and Stow, J.L. (1997) Localization of human heparan glucosaminyl N-deacetylase/N-sulfotransferase to the trans-Golgi network. Biochem. J., 325, 351-357.
16. Hunziker, W., Whitney, A. and Mellman, I. (1991) Selective inhibition of transcytosis by BFA in MDCK cells. Cell, 67, 617-627.
17. Irokawa, M., Nishinaga, M., Ikeda, U., Shinoda, Y., Suematsu, M., Gouda, N., Ishimura, Y. and Shimada, K. (1997) Endothelial-derived nitric oxide preserves anticoagulant heparan sulfate expression in cultured porcine endothelial cells. Atherosclerosis, 135, 9-17.
18. Klausner, R.D., Donaldson, J.G. and Lippincott-Schwartz, J. (1992) BFA: insight into the control of membrane traffic and organelle structure, J. Cell Biol., 116, 1071-1080.
19. Lindahl, U., Bäckström, G., Jansson, L. and Hallén, A. (1973) Biosynthesis of heparin II. Formation of sulfamino groups. J. Biol. Chem., 248, 7234-7241.
20. Lindahl, U., Kusche-Gullberg, M. and Kjellén, L. (1998) Regulated diversity of heparan sulfate. J. Biol. Chem., 273, 24979-24982.
21. Lindblom, A. (1991) Structure of endothelial cell proteoglycans. Characterization of biosynthetic and degradative components in tissue culture. Ph. D. thesis, Lund University, Sweden.
22. Lindblom, A., Carlstedt, I. and Fransson, L.-Å. (1989) Identification of the core proteins in proteoglycans synthesized by vascular endothelial cells. Biochem. J. 261, 145-153.
23. Mertens, G., Cassiman, J.-J., Van den Berghe, H., Vermylen, J. and David, G. (1992) Cell surface heparan sulfate proteoglycan from human vascular endothelial cells. J. Biol. Chem., 267, 20435-20443.
24. Misra, K.B., Kim, K.C. Cho, S.Y., Low, M.G. and Bensadoun, A. (1994) Purification and characterization of adipocyte heparan sulfate proteoglycans with affinity for lipoprotein lipase. J. Biol. Chem., 269, 23838-23844.
25. Nakajima, M., DeChavigny, A., Johnson, C.E., Hamada, J., Stein, C.A. and Nicolson, G.L. (1991) Suramin. A potent inhibitor of melanoma heparanase and invasion. J. Biol. Chem., 266, 9661-9666.
26. Norgard-Sumnicht, K. and Varki, A. (1995) Endothelial heparan sulfate proteoglycans that bind to L-selectin have glucosamine residues with unsubstituted amino groups. J. Biol. Chem., 270, 12012-12024.
27. Prabhakar, P., Thatte, H.S., Goetz, R.M., Cho, M.R., Golan, D.E. and Michel, T. (1998) Receptor-regulated translocation of endothelial nitric-oxide synthase. J. Biol. Chem., 273, 27383-27388.
28. Sandbäck-Pikas, D., Li, J.-P., Vlodavsky, I. and Lindahl, U. (1998) Substrate specificity of heparanases from human hepatoma and platelets. J. Biol. Chem., 273, 18770-18777.
29. Schmidtchen, A. and Fransson, L.-Å. (1994) Analysis of heparan sulfate chains and oligosaccharides from proliferating and quiescent fibroblasts. A proposed model for endoheparanase activity. Eur. J. Biochem., 223, 211-221.
30. Schmidtchen, A., Sundler, R. and Fransson, L.-Å. (1990) A fibroblast heparan sulfate proteoglycan with a 70 kDa core protein is linked to membrane phosphatidylinositol. Glycoconjugate J., 7, 563-572.
31. Seidenbecher, C.I., Richter, K., Rauch, U., Fässler, R., Garner, C.C. and Gundelfinger, E.D. (1995) Brevican, a chondroitin sulfate proteoglycan of rat brain, occurs as secreted and cell surface glycosylphosphatidylinositol-anchored isoforms. J. Biol. Chem., 270, 27206-27212.
32. Shaul, P.W., Smart, E.J., Robinson, L.J., German, Z., Yuhanna, I.S., Ying, Y. Anderson, R.G.W. and Michel, T. (1996) Acylation targets endothelial nitric-oxide synthase to plasmalemmal caveolae. J. Biol. Chem., 271, 6518-6522.
33. Shukla, D., Liu, J., Blaiklock, P., Shworak, N.W., Bai, X., Esko, J.D., Cohen, G.H., Eisenberg, R.J., Rosenberg, R.D. and Spear, P.G. (1999) A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell, 99, 13-22.
34. Smart, E.J., Ying, Y.S., Conrad, P.A. and Anderson, R.G. (1994) Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J. Cell Biol., 127, 1185-1197.
35. Taipale, J. and Keski-Oja, J. (1997) Growth factors in the extracellular matrix. FASEB J., 11, 51-59.
36. van den Born, J., Gunnarsson, K., Bakker, M.A.H., Kjellén, L., Kusche-Gullberg, M., Maccarana, M., Berden, J.H.M. and Lindahl, U. (1995) Presence of N-unsubstituted glucosamine units in native heparan sulfate revealed by a monoclonal antibody. J. Biol. Chem., 270, 31303-31309.
37. Vilar, R.E., Ghael, D., Li, M., Bhagat, D.D., Arrigo, L.M., Cowman, M.K., Dweck, H.S. and Rosenfeld, L. (1997) Nitric oxide degradation of heparin and heparan sulfate. Biochem. J., 324, 473-479.
38. Voogd, T.E., Vansterkenburg, L.M., Wilting, J. and Janssen, L.H.M. (1993) Recent research on the biological activity of suramin. Pharmacol. Rev., 45, 177-203.
39. Williams, D.L.H. (1996) S-Nitrosothiols and role of metal ions in decomposition to nitric oxide. Methods Enzymol., 268, 299-308.
40. Wink, D.A., Grisham, M.B., Mitchell, J.B. and Ford, P.C. (1996) Direct and indirect effects of nitric oxide in chemical reactions relevant to biology. Methods Enzymol., 268, 12-31.
41. Yanagashita, M. and Hascall, V.C. (1992) Cell surface heparan sulfate proteoglycans. J. Biol. Chem., 267, 9451-9454.