Stem domains of heparan sulfate 6-O-sulfotransferase are required for Golgi localization, oligomer formation and enzyme activity

Journal of Cell Science

Volumn 117, Issue 15, 2004, Pages 3331-3341

  Nagai, Naoko ^a   Habuchi, Hiroko ^a   Esko, Jeffrey D ^b   Kimata, Koji ^a  

^a AICHI MEDICAL UNIVERSITY   (Japan)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Enzyme complex; Golgi; Heparan sulfate; Stem region; Sulfotransferase

Indexed keywords

EPIMERASE; ISOENZYME; OLIGOMER; PROTEOHEPARAN SULFATE; SULFOTRANSFERASE;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL CULTURE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME MECHANISM; EXPRESSION VECTOR; GENETIC TRANSFECTION; GOLGI COMPLEX; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SULFONATION;

ANIMALS; BINDING SITES; BREFELDIN A; CATALYSIS; CELLS, CULTURED; CHO CELLS; CHROMATOGRAPHY, GEL; CRICETINAE; CYCLOHEXIMIDE; DNA PRIMERS; DNA, COMPLEMENTARY; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; GENE DELETION; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; GROWTH SUBSTANCES; LIGANDS; MICE; MICROSCOPY, FLUORESCENCE; MODELS, GENETIC; NOCODAZOLE; PLASMIDS; PROTEIN CONFORMATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTEIN SYNTHESIS INHIBITORS; SIGNAL TRANSDUCTION; SULFOTRANSFERASES; TRANSFECTION;

ANIMALIA; VECTORS;

EID: 4344632972     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01191     Document Type: Article

References (50)

1. Ashikari-Hada, S., Habuchi, H., Itoh, N., Reddi, A. H. and Kimata, K. (2004). Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library. J. Biol. Chem. 279, 12346-12354.
2. Bai, X. and Esko, J. D. (1996). An animal cell mutant defective in heparan sulfate hexuronic acid 2-O-sulfation. J. Biol. Chem. 271, 17711-17717.
3. Bernfield, M., Kokenyesi, R., Kato, M., Hinkes, M. T., Spring, J., Gallo, R. L. and Lose, E. J. (1992). Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu. Rev. Cell Biol. 8, 365-393.
4. Blackball, F. H., Merry, C. L., Lyon, M., Jayson, G. C., Folkman, J., Javaherian, K. and Gallagher, J. T. (2003). Binding of endostatin to endothelial heparan sulphate shows a differential requirement for specific sulphates. Biochem. J. 375, 131-139.
5. Brickman, Y. G., Ford, M. D., Gallagher, J. T., Nurcombe, V., Bartlett, P. F. and Turnbull, J. E. (1998). Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J. Biol. Chem. 273, 4350-4359.
6. Bullock, S. L., Fletcher, J. M., Beddington, R. S. and Wilson, V. A. (1998). Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev. 12, 1894-1906.
7. Chen, C., Ma, J., Lazic, A., Backovic, M. and Colley, K. J. (2000). Formation of insoluble oligomers correlates with ST6Gal I stable localization in the golgi. J. Biol. Chem. 275, 13819-13826.
8. Colley, K. J. (1997). Golgi localization of glycosyltransferases: more questions than answers. Glycobiology 7, 1-13.
9. Crawford, B. E., Olson, S. K., Esko, J. D. and Pinhal, M. A. (2001). Cloning, golgi localization, and enzyme activity of the full-length heparin/heparan sulfate-glucuronic acid c5-epimerase. J. Biol. Chem. 276, 21538-21543.
10. Delehedde, M., Seve, M., Sergeant, N., Wartelle, I., Lyon, M., Rudland, P. S. and Fernig, D. G. (2000). Fibroblast growth factor-2 stimulation of p42/44MAPK phosphorylation and IkappaB degradation is regulated by heparan sulfate/heparin in rat mammary fibroblasts. J. Biol. Chem. 275, 33905-33910.
11. Ellgaard, L. and Helenius, A. (2003). Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4, 181-191.
12. Esko, J. D. and Lindahl, U. (2001). Molecular diversity of heparan sulfate. J. Clin. Invest. 108, 169-173.
13. Fan, G., Xiao, L., Cheng, L., Wang, X., Sun, B. and Hu, G. (2000). Targeted disruption of NDST-1 gene leads to pulmonary hypoplasia and neonatal respiratory distress in mice. FEBS Lett. 467, 7-11.
14. Ford-Perriss, M., Guimond, S. E., Greferath, U., Kita, M., Grobe, K., Habuchi, H., Kimata, K., Esko, J. D., Murphy, M. and Turnbull, J. E. (2002). Variant heparan sulfates synthesized in developing mouse brain differentially regulate FGF signaling. Glycobiology 12, 721-727.
15. Forsberg, E. and Kjellen, L. (2001). Heparan sulfate: lessons from knockout mice. J. Clin. Invest. 108, 175-180.
16. Giraldez, A. J., Copley, R. R. and Cohen, S. M. (2002). HSPG modification by the secreted enzyme Notum shapes the Wingless morphogen gradient. Dev. Cell 2, 667-676.
17. Habuchi, H., Suzuki, S., Saito, T., Tamura, T., Harada, T., Yoshida, K. and Kimata, K. (1992). Structure of a heparan sulphate oligosaccharide that binds to basic fibroblast growth factor. Biochem. J. 285, 805-813.
18. Habuchi, H., Habuchi, O. and Kimata, K. (1995). Purification and characterization of heparan sulfate 6-sulfotransferase from the culture medium of Chinese hamster ovary cells. J. Biol. Chem. 270, 4172-4179.
19. Habuchi, H., Tanaka, M., Habuchi, O., Yoshida, K., Suzuki, H., Ban, K. and Kimata, K. (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.
20. Habuchi, H., Miyake, G., Nogami, K., Kuroiwa, A., Matsuda, Y., Kusche-Gullberg, M., Habuchi, O., Tanaka, M. and Kimata, K. (2003). Biosynthesis of heparan sulphate with diverse structures and functions: two alternatively spliced forms of human heparan sulphate 6-O-sulphotransferase-2 having different expression patterns and properties. Biochem. J. 371, 131-142.
21. Habuchi, O., Matsui, Y., Kotoya, Y., Aoyama, Y., Yasuda, Y. and Noda, M. (1993). Purification of chondroitin 6-sulfotransferase secreted from cultured chick embryo chondrocytes. J. Biol. Chem. 268, 21968-21974.
22. Hampton, R. Y. (2002). ER-associated degradation in protein quality control and cellular regulation. Curr. Opin. Cell Biol. 14, 476-482.
23. Humphries, D. E., Sullivan, B. M., Aleixo, M. D. and Stow, J. L. (1997). Localization of human heparan glucosaminyl N-deacetylase/N-sulphotransferase to the trans-Golgi network. Biochem. J. 325, 351-357.
24. Kamimura, K., Fujise, M., Villa, F., Izumi, S., Habuchi, H., Kimata, K. and Nakato, H. (2001). Drosophila heparan sulfate 6-O-sulfotransferase (dHS6ST) gene. Structure, expression, and function in the formation of the tracheal system. J. Biol. Chem. 276, 17014-17021.
25. Kan, M., Wang, F., Xu, J., Crabb, J. W., Hou, J. and McKeehan, W. L. (1993). An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science 259, 1918-1921.
26. Kjellen, L. and Lindahl, U. (1991). Proteoglycans: structures and interactions. Annu. Rev. Biochem. 60, 443-475.
27. Kobayashi, S., Morimoto, K., Shimizu, T., Takahashi, M., Kurosawa, H. and Shirasawa, T. (2000). Association of EXT1 and EXT2, hereditary multiple exostoses gene products, in Golgi apparatus. Biochem. Biophys. Res. Commun. 268, 860-867.
28. Lin, X., Wei, G., Shi, Z., Dryer, L., Esko, J. D., Wells, D. E. and Matzuk, M. M. (2000). Disruption of gastrulation and heparan sulfate biosynthesis in EXT1-deficient mice. Dev. Biol. 224, 299-311.
29. Lippincott-Schwartz, J., Yuan, L. C., Bonafacino, J. S. and Klausner, R. D. (1989). Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER. Cell 56, 801-813.
30. Lippincott-Schwartz, J., Donaldson, J. G., Schweizer, A., Berger, E. G., Hauri, H. P., Yuan, L. C. and Klausner, R. D. (1990). Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 60, 821-836.
31. Liu, J., Shworak, N. W., Fritze, L. M., Edelberg, J. M. and Rosenberg, R. D. (1996). Purification of heparan sulfate D-glucosaminyl 3-O-sulfotransferase. J. Biol. Chem. 271, 27072-27082.
32. Masibay, A. S., Balaji, P. V., Boeggeman, E. E. and Qasba, P, K. (1993). Mutational analysis of the Golgi retention signal of bovine beta-1,4-galactosyltransferase. J. Biol. Chem. 268, 9908-9916.
33. 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 the synthesis of heparan sulfate. Proc. Natl. Acad. Sci. USA 97, 668-673.
34. Merry, C. L., Bullock, S. L., Swan, D. C., Backen, A. C., Lyon, M., Beddington, R. S., Wilson, V. A. and Gallagher, J. T. (2001). The molecular phenotype of heparan sulfate in the Hs2st-/- mutant mouse. J. Biol. Chem. 276, 35429-35434.
35. Milland, J., Russell, S. M., Dodson, H. C., McKenzie, I. F. and Sandrin, M. S. (2002). The cytoplasmic tail of alpha 1,3-galactosyltransferase inhibits Golgi localization of the full-length enzyme. J. Biol. Chem. 277, 10374-10378.
36. Nakamura, N., Rabouille, C., Watson, R., Nilsson, T., Hui, N., Slusarewicz, P., Kreis, T. E. and Warren, G. (1995). Characterization of a cis-Golgi matrix protein, GM130. J. Cell Biol. 6, 1715-1726.
37. Nilsson, T., Hoe, M. H., Slusarewicz, P., Rabouille, C., Watson, R., Hunte, F., Watzele, G., Berger, E. G. and Warren, G. (1994). Kin recognition between medial Golgi enzymes in HeLa cells. EMBO J. 13, 562-574.
38. Nilsson, T., Rabouille, C., Hui, N., Watson, R. and Warren, G. (1996). The role of the membrane-spanning domain and stalk region of N-acetylglucosaminyltransferase I in retention, kin recognition and structural maintenance of the Golgi apparatus in HeLa cells. J. Cell Sci. 109, 1975-1989.
39. Opat, A. S., Houghton, F. and Gleeson, P. A. (2000). Medial Golgi but not late Golgi glycosyltransferases exist as high molecular weight complexes. Role of luminal domain in complex formation and localization. J. Biol. Chem. 275, 11836-11845.
40. Pennica, D., Nedwin, G. E., Hayflick, J. S., Seeburg, P. H., Derymck, R., Palladino, M. A., Kohr, W. J., Aggarwal, B. B. and Goeddel, D. V. (1984). Human tumor necrosis factor: precursor structure, expression and homology to lymphotoxin. Nature 312, 724-729.
41. Pinhal, M. A., Smith, B., Olson, S., Aikawa, J., 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.
42. Ringvall, M., Ledin, J., Holmborn, K., van Kuppevelt, T., Ellin, F., Eriksson, I., Olofsson, A. M., Kjellen, L. and Forsberg, E. (2000). Defective heparan sulfate biosynthesis and neonatal lethality in mice lacking N-Deacetylase/N-sulfotransferase-1. J. Biol. Chem. 275, 25926-25930.
43. Saraste, J. and Svensson, K. (1991). Distribution of the intermediate elements operating in ER to Golgi transport. J. Cell Sci. 100, 415-430.
44. Sasai, K., Ikeda, Y., Tsuda, T., Ihara, H., Korekane, H., Shiota, K. and Taniguchi, N. (2001). The critical role of the stem region as a functional domain responsible for the oligomerization and Golgi localization of N-acetylglucosaminyltransferase V. The involvement of a domain homophilic interaction. J. Biol. Chem. 276, 759-765.
45. Smeds, E., Habuchi, H., Do, A. T., Hjertson, E., Grundberg, H., Kimata, K., Lindahl, U. and Kusche-Gullberg, M. (2003). Substrate specificities of mouse heparan sulphate glucosaminyl 6-O-sulphotransferases. Biochem. J. 372, 371-380.
46. Teasdale, R. D., D'Agostaro, G. and Gleeson, P. A. (1992). The signal for Golgi retention of bovine beta 1,4-galactosyltransferase is in the transmembrane domain. J. Biol. Chem. 267, 4084-4096.
47. Teasdale, R. D., Matheson, F. and Gleeson, P. A. (1994). Post-translational modifications distinguish cell surface from Golgi-retained beta 1,4 galactosyltransferase molecules. Golgi localization involves active retention. Glycobiology 4, 917-928.
48. Turnbull, J., Powell, A. and Guimond, S. (2001). Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol. 11, 75-82.
49. Utsumi, T., Akimaru, K. Kawabata, Z., Levitan, A., Tokunaga, T., Tang, P., Ide, A., Hung, M. C. and Klostergaard, J. (1995). Human pro-tumor necrosis factor: molecular determinants of membrane translocation, sorting, and maturation. Mol. Cell. Biol. 15, 6398-6405.
50. Yang, W. and Storrie, B. (1998). Scattered Golgi elements during microtubule disruption are initially enriched in trans-Golgi proteins. Mol. Biol. Cell 9, 191-207