QSulf1 remodels the 6-O sulfation states of cell surface heparan sulfate proteoglycans to promote Wnt signaling

Journal of Cell Biology

Volumn 162, Issue 2, 2003, Pages 341-351

  Ai, Xingbin ^a   Do, Anh Tri ^b   Lozynska, Olga ^a   Kusche Gullberg, Marion ^b   Lindahl, Ulf ^b   Emerson Jr , Charles P ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Endosulfatase; Glypican1; HSPG; QSulf1; Wnt signaling

Indexed keywords

DISACCHARIDE; FRIZZLED PROTEIN; GLYPICAN; HEPARIN; PROTEIN QSULF1; PROTEOHEPARAN SULFATE; RECEPTOR; SULFATASE; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL FUNCTION; CELL GROWTH; CELL SURFACE; CHO CELL; CONTROLLED STUDY; GOLGI COMPLEX; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SULFATION;

ANIMALS; BINDING, COMPETITIVE; CELL MEMBRANE; CELLS, CULTURED; CHO CELLS; CRICETINAE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GOLGI APPARATUS; HEPARAN SULFATE PROTEOGLYCANS; HEPARIN; HUMANS; MODELS, BIOLOGICAL; MUTATION; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; SULFATASES; TRANSFECTION; WNT PROTEINS; ZEBRAFISH PROTEINS;

ANIMALIA;

EID: 0041671071     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200212083     Document Type: Article

References (47)

1. Avnur, Z., and B. Geiger. 1984. Immunocytochemical localization of native chondroitin-sulfate in tissues and cultured cells using specific monoclonal antibody. Cell. 38:811-822.
2. Baeg, G.H., X. Lin, N. Khare, S. Baumgartner, and N. Perrimon. 2001. Heparan sulfate proteoglycans are critical for the organization of the extracellular distribution of Wingless. Development. 128:87-94.
3. Bai, X., K.J. Bame, H. Habuchi, K. Kimata, and J.D. Esko. 1997. Turnover of heparan sulfate depends on 2-O sulfation of uronic acids. J. Biol. Chem. 272:23172-23179.
4. Bai, X., G. Wei, A. Sinha, and J.D. Esko. 1999. Chinese hamster ovary cell mutants defective in glycosaminoglycan assembly and glucuronosyltransferase I. J. Biol. Chem. 274:13017-13024.
5. Bernfield, M., M. Gotte, P.W. Park, O. Reizes, M.L. Fitzgerald, J. Lincecum, and M. Zako. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68:729-777.
6. Brickman, Y.G., M.D. Ford, J.T. Gallagher , V. Nurcombe, P.F. Bartlett, and J.E. Turnbull. 1998. Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J. Biol. Chem. 273:4350-4359.
7. Chen, R.L., and A.D. Lander. 2001. Mechanisms underlying preferential assembly of heparan sulfate on glypican-1. J. Biol. Chem. 276:7507-7517.
8. Chong, J.M., A. Uren, J.S. Rubin, and D.W. Speicher. 2002. Disulfide bond assignments of secreted Frizzled-related protein-1 provide insights about Frizzled homology and netrin modules. J. Biol. Chem. 277:5134-5144.
9. David, G., B. Van der Schueren, P. Marynen, J.J. Cassiman, and H. van den Berghe. 1992. Molecular cloning of amphiglycan, a novel integral membrane heparan sulfate proteoglycan expressed by epithelial and fibroblastic cells. J. Cell Biol. 118:961-969.
10. Dhoot, G.K., M.K. Gustafsson, X. Ai, W. Sun, D.M. Standiford, and C.P. Emerson, Jr. 2001. Regulation of Wnt signaling and embryo patterning by an extracellular sulfatase. Science. 293:1663-1666.
11. Esko, J.D., and U. Lindahl. 2001. Molecular diversity of heparan sulfate. J. Clin. Invest. 108:169-173.
12. Giraldez, A.J., R.R. Copley, and S.M. Cohen. 2002. HSPG modification by the secreted enzyme Notum shapes the Wingless morphogen gradient. Dev. Cell. 2:667-676.
13. Gleeson, P.A., R.D. Teasdale, and J. Burke. 1994. Targeting of proteins to the Golgi apparatus. Glycoconj. J. 11:381-394.
14. He, W., Y.V. Voznyi, A.M. Boer, W.J. Kleijer, and O.P. van Diggelen. 1993. A fluorimetric enzyme assay for the diagnosis of Sanfilippo disease type D (MPS IIID). J. Inherit. Metab. Dis. 16:935-941.
15. Hsieh, J., A. Pattner, P.M. Smallwood, and J. Nathans. 1999. Biochemical characterization of Wnt-Frizzled interactions using a soluble, biologically active vertebrate Wnt protein. Proc. Natl. Acad. Sci. USA. 96:3546-3551.
16. Jayson, G.C., C. Vives, C. Paraskeva, K. Schofield, J. Courts, A. Fleetwood, and J.T. Gallagher. 1999. Coordinated modulation of the fibroblast growth factor dual receptor mechanism during transformation from human colon adenoma to carcinoma. Int. J. Cancer. 82:298-304.
17. Jemth, P., J. Kreuger, M. Kusche-Gullberg, L. Sturiale, G. Gimenez-Gallego, and U. Lindahl. 2002. Biosynthetic oligosaccharide libraries for identification of protein-binding heparan sulfate motifs. J. Biol. Chem. 277:30567-30573.
18. Kresse, H., E. Paschke, K. von Figura, W. Gilberg, and W. Fuchs. 1980. Sanfilippo disease type D: deficiency of N-acetylglucosamine-6-sulfate sulfatase required for heparan sulfate degradation. Proc. Natl. Acad. Sci. USA. 77:6822-6826.
19. Lin, X., and N. Perrimon. 1999. Dally cooperates with Drosophila Frizzled to transduce Wingless signaling. Nature. 400:281-284.
20. Lindahl, U., M. Kusche-Gullberg, and L. Kjellen. 1998. Regulated diversity of heparan sulfate. J. Biol. Chem. 273:24979-24982.
21. Lundin, L., H. Larsson, J. Kreuger, S. Kanda, U. Lindahl, M. Salmivirta, and L. Claesson-Welsh. 2000. Selectively desulfated heparin inhibits fibroblast growth factor-induced mitogenicity and angiogenesis. J. Biol. Chem. 275:24653-24660.
22. Merry, C.L., M. Lyon, J.A. Deakin, J.J. Hopwood, and J.T. Gallagher. 1999. Highly sensitive sequencing of the sulfated domains of heparan sulfate. J. Biol. Chem. 274:18455-18462.
23. Morimoto-Tomita, M., K. Uchimura, Z. Werb, S. Hemmerich, and S.D. Rosen. 2002. Cloning and characterization of two extracellular heparin-degrading endosulfatases in mouse and human. J. Biol. Chem. 277:49175-49185.
24. Munro, S., and H.R. Pelham. 1987. A C-terminal signal prevents secretion of luminal ER proteins. Cell. 48:899-907.
25. Nybakken, K., and N. Perrimon. 2002. Heparan sulfate proteoglycan modulation of developmental signaling in Drosophila. Biochim. Biophys. Acta. 1573:280-291.
26. Ohto, T., H. Uchida, H. Yamazaki, K. Keino-Masu, A. Matsui, and M. Masayuki. 2002. Identification of a novel nonlysosomal sulphatase expressed in the floor plate, choroid plexus and cartilage. Genes Cells. 7:173-185.
27. Piccolo, S., E. Agius, L. Leyns, S. Bhattacharyya, H. Grunz, T. Bouwmeester, and E.M. De Robertis. 1999. The head inducer Cerberus is a multifunctional antagonist of nodal, BMP and Wnt signals. Nature. 397:707-710.
28. Prydz, K., and K.T. Dalen. 2000. Synthesis and sorting of proteoglycans. J. Cell Sci. 113:193-205.
29. Pye, D.A., R.R. Vives, P. Hyde, and J.T. Gallagher. 2000. Regulation of FGF-1 mitogenic activity by heparan sulfate oligosaccharides is dependent on specific structural features: differential requirement for the modulation of FGF-1 and FGF-2. Glycobiology. 10:1183-1192.
30. Raman, R., J.R. Myette, Z. Shriver, K. Pojasek, G. Venkataraman, and R. Sasisekharan. 2003. The heparin/heparan sulfate 2-O sulfatase from Flavobacterium heparinum. J. Biol. Chem. 278:12167-12174.
31. Rapraeger, A.C. 2002. Heparan sulfate-growth factor interactions. Methods Cell Biol. 69:83-109.
32. 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.
33. Reissig, J.L., J.L. Strominger, and L.F. Leloir. 1955. A modified colorimetric method for the estimation of N-acetylamino sugars. J. Biol. Chem. 217:959-966.
34. Rong, J., H. Habuchi, K. Kimata, U. Lindahl, and M. Kusche-Gullberg. 2001. Substrate specificity of the heparan sulfate hexuronic acid 2-O-sulfotransferase. Biochemistry. 40:5548-5555.
35. Safaiyan, F., S.O. Kolset, K. Prydz, E. Gottgridsson, U. Lindahl, and M. Salmivirta. 1999. Selective effects of sodium chlorate treatment on the sulfation of heparan sulfate. J. Biol. Chem. 274:36267-36273.
36. Safaiyan, F., U. Lindahl, and M. Salmivirta. 2000. Structural diversity of N-sulfated heparan sulfate domains: distinct modes of glucoronyl C5 epimerization, iduronic acid 2-O-sulfation, and glucosamine 6-O-sulfation. Biochemistry. 39:10823-10830.
37. Sasaki, T., H. Larsson, J. Kreuger, M. Salmivirta, L. Claesson-Welsh, U. Lindahl, E. Hohenester, and R. Timpl. 1999. Structural basis and potential role of heparin/heparan sulfate binding to the angiogenesis inhibitor endostatin. EMBO J. 18:6240-6248.
38. Schlessinger, J., A.N. Plotnikov, O.A. Ibrahimi, A.V. Eliseenkova, B.K. Yeh, A. Yayon, R. Linhardt, and M. Mohammadi. 2000. Crystal structure of a ternary FGF-FGFR-heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol. Cell. 6:743-750.
39. Schmidt, B., T. Selmer, A. Ingendoh, and K. von Figura. 1995. A novel amino acid modification in sulfatases that is defective in multiple sulfatase deficiency. Cell. 82:271-278.
40. Selva, E.M., and N. Perrimon. 2001. Role of heparan sulfate proteoglycans in cell signaling and cancer. Adv. Cancer Res. 83:67-80.
41. Shively, J.E., and H.E. Conrad. 1976. Formation of anhydrosugars in the chemical depolymerization of heparin. Biochemistry. 15:3932-3942.
42. Toyoda, H., A. Kinoshita-Toyoda, B. Fox, and S.C. Selleck. 2000. Structural analysis of glycosaminoglycans in animals bearing mutations in sugarless, sulfateless, and tout-velu. J. Biol. Chem. 275:21856-21861.
43. Tsuda, M., K. Kamimura, H. Nakato, M. Archer, W. Staaz, B. Fox, M. Humphrey, S. Olson, T. Futch, V. Kaluza, et al. 1999. The cell-surface proteoglycan Dally regulates Wingless signaling in Drosophila. Nature. 400:276-280.
44. Vives, R.R., D.A. Pye, M. Salmivirta, J.J. Hopwood, U. Lindahl, and J.T. Gallagher. 1999. Sequence analysis of heparan sulphate and heparin oligosaccharides. 1999. Biochem. J. 339:767-773.
45. Wu, C., and R. Nusse. 2002. Ligand receptor interactions in the Wnt signaling pathway in Drosophila. J. Biol. Chem. 277:41762-41769.
46. Yanagishita, M., and V.C. Hascall. 1992. Cell surface heparan sulfate proteoglycans. J. Biol. Chem. 267:9451-9454.
47. Yip, G.W., P. Ferreti, and A.J. Copp. 2002. Heparan sulfate proteoglycans and spinal neurulation in the mouse embryo. Development. 129:2109-2119.