Novel aspects of glypican glycobiology

Cellular and Molecular Life Sciences

Volumn 61, Issue 9, 2004, Pages 1016-1024

  Fransson, L A ^a   Cheng, F ^a   Jonsson M ^a   Mani, K ^a   Sandgren, S ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Caveolae; Development; Growth factors; Heparan sulfate; Nitric oxide; Polyamines; S nitrosylation

Indexed keywords

AMIDE; ASCORBIC ACID; CAVEOLIN; COPPER; CORE PROTEIN; CYSTEINE; GLUCOSAMINE; HEPARAN SULFATE; NITRIC OXIDE; POLYAMINE; PROTEIN GLYPICAN; PROTEOGLYCAN; UNCLASSIFIED DRUG;

ASCIDIACEA; BINDING SITE; CARBOXY TERMINAL SEQUENCE; DEAMINATION; DNA FLANKING REGION; ENZYME ACTIVITY; ENZYME DEGRADATION; GASTRULATION; GENE MUTATION; GROWTH CURVE; HUMAN; NITROSYLATION; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; WORM; ZEBRA FISH;

ANIMALS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; NITRIC OXIDE; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION;

ASCIDIACEA; DANIO RERIO;

EID: 2442656740     PISSN: 1420682X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00018-004-3445-0     Document Type: Review

References (88)

1. 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. Cell Biol. 111: 3165-3176
2. Perrimon N. and Bernfield M. (2000) Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404: 725-728
3. Filmus J. and Selleck S. B. (2001) Glypicans: proteoglycans with a surprise. J. Clin. Invest. 108: 497-501
4. Esko J. D. and Selleck S. B. (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71: 435-471
5. Fransson L.-Å. (2003) Glypicans. Intern. J. Biochem. Cell Biol. 35: 125-129
6. Liang Y., Haring M., Roughley P. J., Margolis R. K. and Margolis R. U. (1997) Glypican and biglycan in the nuclei of neurons and glioma cells: presence of functional nuclear localization signals and dynamic changes in glypican during the cell cycle. J. Cell Biol. 139: 851-864
7. Litwack E. D., Ivins J. K., Kumbasar A., Paine-Saunders S., Stipp C. S. and Lander A. D. (1998) Expression of the heparan sulfate proteoglycan glypican-1 in the developing rodent. Dev. Dyn. 211: 72-87
8. Ivins J. K., Litwack E. D., Kumbasar A., Stipp C. S. and Lander A. D. (1997) Cerebroglycan, a developmentally regulated cell-surface heparan sulfate proteoglycan, is expressed on developing axons and growth cones. Dev. Biol. 184: 320-332
9. Syrrou M., Keymolen K., Devrient K., Holvoet M., Thoelen R., Verhofstadt K. et al. (2002) Glypican 1 gene: good candidate for brachydactyly type E. Am. J. Med. Genet. 108: 310-314
10. Farooq M., Hwang S. Y., Park M. K., Kim J. C., Kim M. K. and Sung Y. K. (2003) Blocking endogenous glypican-3 expression releases Hep 3B cells from G1 arrest. Mol. Cells 15: 356-360
11. Baeg G. H. and Perrimon N. (2000) Functional binding of secreted molecules to heparan sulfate proteoglycans in Drosophila. Curr. Opin. Cell Biol. 12: 575-580
12. Fujise M., Takeo S., Kamimura K., Matsuo T., Aigaki T., Izumi S. et al. (2003) Dally regulates Dpp morphogen gradient formation in the Drosophila wing. Development 130: 1515-1522
13. Topczewski J., Sepich D. S., Myers D. C., Walker C., Amores A., Lele Z. et al. (2001) The zebrafish glypican knypek controls cell polarity during gastrulation movements of convergent extension. Dev. Cell 1: 251-264
14. Matsuda K., Maruyama H., Guo F., Kleeff K., Itakura J., Matsumoto Y. et al. (2001) Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells. Cancer Res. 61: 5562-5569
15. Sung Y. K., Hwang S. Y., Park M. K., Farooq M., Han I. S., Bae H. I. et al. (2003) Glypican-3 is overexpressed in human hepatocellular carcinoma. Cancer Sci. 94: 259-262
16. Xiang Y. Y., Ladeda V. and Filmus J. (2001) Glypican-3 expression is silenced in human breast cancer. Oncogene 20: 7408-7412
17. Filmus J. (2001) Glypicans in growth control and cancer. Glycobiology 11: 19R-23R
18. Kleeff J., Wildi S., Kumbasar A., Friess H., Lander A. and Korc M. (1999) Stable transfection of a glypican-1 antisense construct decreases tumorigenicity in PANC-1 pancreatic carcinoma cells. Pancreas 19: 281-288
19. Ellgaard L. and Helenius A. (2003) Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell. Biol. 4: 181-191
20. Iozzo R. V. (1998) Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67: 609-652
21. Bernfield M., Götte M., Park P.-W., Reizes O., Fitzgerald M. L., Lincecum J. et al. (1999) Functions of cell-surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68: 729-777
22. Chen R. L. and Lander A. D. (2001) Mechanisms underlying preferential assembly of heparan sulfate on glypican-1. J. Biol. Chem. 276: 7507-7517
23. Kim B. T., Kitagawa H., Tamura J., Saito T., Kusche-Gullberg M., Lindahl U. et al. (2001) Human tumor suppressor EXT gene family members EXTL1 and EXTL3 encode alpha 1,4-N-acetylglucosaminyltransferases that likely are involved in heparan sulfate/heparin biosynthesis. Proc. Natl. Acad. Sci. USA 98: 7176-7181
24. McCormick C., Duncan G., Goutsos K. T. and Tufaro F. (2000) The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes synthesis of heparan sulfate. Proc. Natl. Acad. Sci. USA 97: 668-673
25. Senay C., Lind T., Muguruma K., Tone Y., Kitagawa H., Sugahara K. et al. (2000) The EXT1/EXT2 tumor suppressors: catalytic activities and role in heparan sulfate biosynthesis. EMBO Rep. 1: 282-286
26. Busse M. and Kusche-Gullberg M. (2003) In vitro polymerization of heparan sulfate backbone by the EXT proteins. J. Biol. Chem. 278: 41333-41337
27. Kim B.-T., Kitagawa H., Tanaka J., Tamura J.-I. and Sugahara K. (2003) J. Biol. Chem. 10.1074/jbc.M304831200
28. Lin X., Wei G., Shi Z., Dryer L., Esko J. D., Wells D. E. et al. (2000) Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev. Biol. 224: 299-311
29. Zak B. M., Crawford B. E. and Esko J. D. (2002) Hereditary multiple exostoses and heparan sulfate polymerization. Biochim. Biophys. Acta 1573: 346-355
30. Pinhal M. A. S., Smith B., Olson S., Aikawa J.-I., Kimata K. and Esko J. D. (2001) Enzyme interactions in heparan sulfate biosynthesis: uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo. Proc. Natl. Acad. Sci. USA 98: 12984-12989
31. Liu J., Shriver Z., Blaiklock P., Yoshida K., Sasisekharan R. and Rosenberg R. D. (1999) Heparan sulfate D-glucosaminyl 3-O-sulfotransferase-3A sulfates N-unsubstituted glucosamine residues. J. Biol. Chem. 274: 38155-38162
32. Habuchi H., Tanaka M., Habuchi O., Yoshida K., Suzuki H., Ban K. et al. (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
33. Xia G., Chen J., Tiwari V., Ju W., Li J.-P., Malmström A. et al. (2002) Heparan sulfate 3-O-sulfotransferase isoform 5 generates both an antithrombin-binding site and an entry receptor for herpes simplex virus-1. J. Biol. Chem. 277: 37912-37919
34. Jemth P., Smeds E., Do A. T., Habuchi H., Kimata K., Lindahl U. et al. (2003) Oligosaccharide library-based assessment of heparan sulfate 6-O-sulfotransferase substrate specificity. J. Biol. Chem. 278: 24371-24376
35. Mertens G., Van der Schueren B., van den Berghe H. and David G. (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
36. Nabi I. R. and Le P. U. (2003) Caveolae/raft-dependent endocytosis. J. Cell Biol. 161: 673-677
37. Pelkmans L. and Helenius A. (2002) Endocytosis via caveolae. Traffic 3: 311-320
38. Fransson L.-Å., Carlstedt I., Cöster L. and Malmström A. (1983) Proteoheparan sulfate from human skin fibroblasts. Evidence for self-interaction via the heparan sulfate side-chains. J. Biol. Chem. 258: 14342-14345
39. Dinter A. and Berger E. G. (1998) Golgi-disturbing agents. Histochem. Cell Biol. 109: 571-590
40. Hunziker W., Whitney J. A. and Mellman I. (1992) Brefeldin A and the endocytotic pathway. Possible implications for membrane traffic and sorting. FEBS Lett. 307: 93-96
41. Fransson L.-Å., Edgren G., Havsmark B. and Schmidtchen A. (1995) Recycling of a glycosylphosphatidylinositol-anchored heparan sulfate proteoglycan (glypican) in skin fibroblasts. Glycobiology 5: 407-415
42. 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
43. Fransson L.-Å., Belting M., Edgren G., Jönsson M., Mani K., Schmidtchen A. et al. (1998) Degradation and reprocessing of heparan sulphate in recycling glypican (heparan sulphate proteoglycan). Trends Glycosci. & Glycotech. 10: 81-94
44. Mani K., Jönsson M., Edgren G., Belting M. and Fransson L.-Å. (2000) A novel role for nitric oxide in the endogenous degradation of heparan sulphate during recycling of glypican-1 in vascular endothelial cells. Glycobiology 10: 577-586
45. Ding K., Jönsson M., Mani K., Sandgren S., Belting M. and Fransson L.-Å. (2001) N-unsubstituted glucosamine in heparan sulfate of recycling glypican-1 from suramin-treated and nitrite-deprived endothelial cells. Mapping of nitric oxide/nitrite-susceptible glucosamine residues to clustered sites near the core protein. J. Biol. Chem. 276: 3885-3894
46. Westling C. and Lindahl U. (2002) Location of N-unsubstituted glucosamine residues in heparan sulfate. J. Biol. Chem. 277: 49247-49255
47. Ding K., Sandgren S., Mani K., Belting M. and Fransson L.-Å. (2001) Modulations of glypican-1 heparan sulfate structure by inhibition of endogenous polyamine synthesis. Mapping of spermine-binding sites and heparanase, heparin lyase and nitric oxide/nitrite cleavage sites. J. Biol. Chem. 276: 46779-46791
48. Ding K., Mani K., Cheng F., Belting M. and Fransson L.-Å. (2002) Copper-dependent autocleavage of glypican-1 heparan sulfate by nitric oxide derived from intrinsic nitrosothiols. J. Biol. Chem. 277: 33353-33360
49. Cheng F., Mani K., van den Born J., Ding K., Belting M. and Fransson L.-Å. (2002) Nitric oxide-dependent processing of heparan sulfate in recycling S-nitrosylated glypican-1 takes place in caveolin-1 containing endosomes. J. Biol. Chem. 277: 44431-44439
50. Berger U. V., Lu X. C., Liu W., Tang Z., Slusher B. S. and Hediger M. A. (2003) Effect of middle cerebral artery occlusion on mRNA expression for the sodium-coupled vitamin C transporter SVCT2 in rat brain. J. Neurochem. 86: 896-906
51. Peters P. J., Mironov A. Jr, Peretz D., Van Donselaar E., Leclerc E., Erpel S. et al. (2003) Trafficking of prion proteins through a caveolae-mediated endosomal pathway. J. Cell Biol. 162: 703-717
52. Mani K., Cheng F., Havsmark B., Jönsson M., Belting M. and Fransson L.-Å. (2003) Prion, amyloid-β-derived Cu(II) ions or free Zn(II) ions support S-nitroso-dependent autocleavage of glypican-1 heparan sulfate. J. Biol. Chem. 278: 38956-38965
53. Gow A. J., Chen Q., Hess D. T., Day B. J., Ischiropoulos H. and Stamler J. (2002) Basal and stimulated protein S-nitrosylation in multiple cell types and tissues. J. Biol. Chem. 277: 9637-9640
54. Bush A. I. and Tanzi R. E. (2002) The galvanization of β-amyloid in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 99: 7317-7319
55. Woods A. (2001) Syndecans: transmembrane modulators of adhesion and matrix assembly. J. Clin. Invest. 107: 935-941
56. Gallagher J. T. (2001) Heparan sulfate: growth control with a restricted sequence menu. J. Clin. Invest. 108: 357-361
57. Fitzgerald M. L., Wang Z., Park P. W., Murphy G. and Bernfield M. (2000) Shedding of syndecan-1 and -4 ectodomains is regulated by signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase. J. Cell Biol. 148: 811-824
58. Ishihara M., Fedarko N. S. and Conrad H. E. (1987) Involvement of phosphatidylinositol and insulin in the coordinate regulation of proteoheparan sulfate metabolism and hepatocyte growth. J. Biol. Chem. 262: 4708-4716
59. Mertens G., Cassiman J.-J., van den Berghe H., Vermylen J. and David G. (1992) Cell surface heparan sulfate proteoglycans from vascular endothelial cells. Core protein characterization and antithrombin III binding properties, J. Biol. Chem. 267: 20435-20443
60. Schlessinger J., Plotnikov A.N., Ibrahimi O. A., Eliseenkova A. V., Yeh B. K., Yayon A. et al. (2000) Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell 3: 743-750
61. Qiao D., Meyer K., Mundhenke C., Drew S. A. and Friedl A. (2003) Heparan sulfate proteoglycans as regulators of FGF2 signaling in brain endothelial cells - specific role for glypican-1 in glioma angiogenesis. J. Biol. Chem. 278: 16045-16053
62. Gengrinovitch S., Berman B., David G., Witte L., Neufeld G. and Ron D. (1999) Glypican-1 is a VEGF165 binding proteoglycan that acts as an extracellular chaperone for VEGF165. J. Biol. Chem. 274: 10816-10822
63. Hagihara K., Watanabe K., Chun J. and Yamaguchi Y. (2000) Glypican-4 is an FGF2-binding heparan sulfate proteoglycan expressed in neural precursor cells. Dev. Dyn. 219: 353-367
64. Williamson T. G., Mok S. S., Henry A., Cappai R., Lander A. D., Nurcombe V. et al. (1996) Secreted glypican binds to the amyloid precursor protein of Alzheimer's disease (APP) and inhibits APP-induced neunte outgrowth. J. Biol. Chem. 271: 31215-31221
65. Karumanchi S. A., Jha V., Ramchandran R., Karihaloo A., Tsiokas L., Chan B. et al. (2001) Cell surface glypicans are low-affinity endostatin receptors. Mol. Cell 7: 811-822
66. Belting M. (2003) Heparan sulfate proteoglycan as a plasma membrane carrier. Trends Biochem. Sci. 28: 145-151
67. Thomas T. and Thomas T. J. (2001) Polyamines in cell growth and cell death: molecular mechanisms and therapeutic applications. CMLS Cell. Mol. Life Sci. 58: 244-258
68. Belting M., Havsmark B., Jönsson M., Persson S. and Fransson L.-Å. (1996) Heparan sulphate/heparin glycosaminoglycans with strong affinity for the growth-promoter spermine have high antiproliferative activity. Glycobiology 6: 121-129
69. Belting M., Persson S. and Fransson L.-Å. (1999) Proteoglycan involvement in polyamine uptake. Biochem. J. 338: 317-323
70. Belting M., Borsig L., Fuster M. M., Brown J. R., Persson L., Fransson L.-Å. et al. (2002) Tumor attenuation by combined heparan sulfate and polyamine depletion. Proc. Natl. Acad. Sci. USA 99: 371-376
71. Belting M., Mani K., Jönsson M., Cheng F., Sandgren S., Jonsson S. et al. (2003) Glypican-1 is a vehicle for polyamine uptake in mammalian cells. A pivotal role for nitrosothiol-derived nitric oxide. J. Biol. Chem. 278: 47181-47189
72. Sandgren S., Cheng F. and Belting M. (2002) Nuclear targeting of macromolecular polyanions by an HIV-Tat derived peptide. J. Biol. Chem. 277: 38877-38883
73. Mouillet-Richard S., Ermonval M., Chebasier C., Laplanche J. L., Lehmann S., Launay J. M. et al. (2000) Science 289: 1925-1928
74. Galli A., Rourc A., Zeller R. and Dono R. (2003) Glypican 4 modulates FGF signalling and regulates dorsoventral forebrain patterning inXenopus embryos. Development 130: 4919-4929
75. Malave C., Villegas G. M., Hernandez M., Martinez J. C. Castillo C., Suarez de Mata Z. et al. (2003) Role of glypican-1 in the trophic activity on PC 12 cells induced by cultured sciatic nerve conditioned medium: identification of a glypican-1-neuregulin complex. Brain Res. 983: 74-83
76. van Horssen J., Wesseling P., van den Heuvel L. P. W. J., de Waal R. and Verbeek M. (2003) Heparan sulfate proteoglycans in Alzheimer's disease and amyloid-related disorders. Lancet Neurol. 2: 482-492
77. Peters M. G., Farias E., Colombo L., Filmus J., Puricelli L. and Bal de Kier Joffe E. (2003) Inhibition of invasion and metastasis by glypican-3 in a syngeneic breast cancer model. Breast Cancer Res. Treat. 80: 221-232
78. Hagino S., Iseki K., Mori T., Zhang Y., Sakai N., Yokoya S. et al. (2003) Expression pattern of glypican-1 mRNA after brain injury in mice. Neurosci. Lett. 349: 29-32
79. Mast A. E., Higuchi D. A., Huang Z.-F., Warshawsky I., Schwartz A. L. and Broze G. J. (1997) Glypican-3 is a binding protein on the HepG2 cell surface for tissue factor pathway inhibitor. Biochem. J. 327: 577-583
80. Siebertz B., Stöcker G., Drzeniek Z., Handt S., Just U. and Haubeck H.-D. (1999) Expression of glypican-4 in haematopoietic-progenitor and bone-marrow-stromal cells. Biochem. J. 344: 937-943
81. 2 with the glycosylphosphatidylinositol-anchored heparan sulfate proteoglycan in the cyclooxygenase-2-mediated delayed prostanoid-biosynthetic pathway. J. Biol. Chem. 274: 29927-29936
82. Okada Y., Yamada S., Toyoshima M., Dong J., Nakajima M. and Sugahara K. (2002) Structural recognition by recombinant human heparanase that plays critical roles in tumor metastasis. Hierachical sulfate groups with differential effects and the essential target disulfated trisaccharide sequence. J. Biol. Chem. 277: 42488-42495
83. Lee J. Y., Chang M. Y., Park C. H., Kim H. Y., Kim J. H., Son H. et al. (2003) Ascorbate-induced differentiation of embryonic cortical precursors into neurons and astrocytes. J. Neurosci. Res. 73: 156-165
84. Bauer P. M., Buga G. M., Fukuto J. M., Pegg A. E. and Ignarro L. J. (2001) Nitric oxide inhibits ornithine decarboxylase via S-nitrosylation of cysteine 360 in the active site of the enzyme. J. Biol. Chem. 276: 34458-34464
85. Hu J., Mahmoud M. I. and el-Fakahany E. E. (1994) Polyamines inhibit nitric oxide synthase in rat cerebellum. Neurosci. Lett. 175: 41-45
86. Blachier F., Mignon A. and Soubrane O. (1997) Polyamines inhibit lipopolysaccharide-induced nitric oxide synthase activity in rat liver cytosol. Nitric Oxide 1: 268-272
87. Schmidtchen A., Carlstedt I., Malmström A. and Fransson L.-Å. (1990) Inventory of human skin fibroblast proteoglycans. Identification of multiple heparan and chondroitin/dermatan sulfate proteoglycans. Biochem. J. 265: 289-300
88. De Cat B., Muyldermans S. Y., Coomans C., Degeest G., Vanderscheuren B., Creemers J. et al. (2003) Processing by proprotein convertases is required for glypican-3 modulation of cell survival, Wnt signalling and gastrulation movements. J. Cell Biol. 163: 625-635