Involvement of chondroitin sulfate synthase-3 (chondroitin synthase-2) in chondroitin polymerization through its interaction with chondroitin synthase-1 or chondroitin-polymerizing factor

Biochemical Journal

Volumn 403, Issue 3, 2007, Pages 545-552

  Izumikawa, Tomomi ^a   Uyama, Toru ^a   Okuura, Yuka ^a   Sugahara, Kazuyuki ^a,b   Kitagawa, Hiroshi ^a  

^a KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Chondroitin polymerization; Chondroitin sulfate; Glycosaminoglycan; Glycosyltransferase; Protein interaction; Proteoglycan

Indexed keywords

CHONDROITIN POLYMERIZATION; CHONDROITIN SULFATE; GLYCOSAMINOGLYCAN; GLYCOSYLTRANSFERASE; PROTEIN INTERACTION; PROTEOGLYCAN;

BIOASSAY; CELLS; CLONING; GENE EXPRESSION; POLYMERIZATION;

ENZYMES;

CHONDROITIN; CHONDROITIN POLYMERIZING FACTOR; CHONDROITIN SULFATE; CHONDROITIN SULFATE SYNTHASE 3; CHONDROITIN SYNTHASE 1; CHONDROITIN SYNTHASE 2; GLUCURONOSYLTRANSFERASE; GLUCURONOSYLTRANSFERASE 2; GLYCOSYLTRANSFERASE; N ACETYLGALACTOSAMINYLTRANSFERASE; N ACETYLGALACTOSAMINYLTRANSFERASE 2; SYNTHETASE; UNCLASSIFIED DRUG; CHONDROITIN POLYMERIZING FACTOR, HUMAN; CHONDROITIN SULFATE SYNTHASE 2; CHONDROITIN SULFATE SYNTHASE 3, HUMAN; CHONDROITIN SULFATE SYNTHASE-2; CHONDROITIN SULFATE SYNTHASE-3, HUMAN; MEMBRANE PROTEIN;

ARTICLE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN POLYMERIZATION; PROTEIN SECRETION; PROTEOMICS; ANIMAL; CELL STRAIN COS1; CERCOPITHECUS; HELA CELL; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

ANIMALS; BASE SEQUENCE; CERCOPITHECUS AETHIOPS; COS CELLS; GLYCOSYLTRANSFERASES; HELA CELLS; HEXOSYLTRANSFERASES; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA;

EID: 34247880268     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20061876     Document Type: Article

References (36)

1. Kjellén, L. and Lindahl, U. (1991) Proteoglycans: structures and interactions. Annu. Rev. Biochem. 60, 443-475
2. Salmivirta, M., Lidholt, K. and Lindahl, U. (1996) Heparan sulfate: a piece of information. FASEB J. 10, 1270-1279
3. Perrimon, N. and Bernfield, M. (2000) Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404, 725-728
4. Lowe, J. B. and Marth, J. D. (2003) A genetic approach to mammalian glycan function. Annu. Rev. Biochem. 72, 643-691
5. Princivalle, M. and Agostini, A. D. (2002) Normal levels of anticoagulant heparan sulfate are not essential for normal hemostasis. Int. J. Dev. Biol. 46, 267-278
6. Sugahara, K., Mikami, T., Uyama, T., Mizuguchi, S., Nomura, K. and Kitagawa, H. (2003) Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol. 13, 612-620
7. Hwang, H.-Y., Olson, S. K., Esko, J. D. and Horvitz, R. H. (2003) Caenorhabditis elegans early embryogenesis and vulval morphogenesis reguire chondroitin biosynthesis. Nature 423, 439-443
8. Mizuguchi, S., Uyama, T., Kitagawa, H., Nomura, K., Dejima, K., Gengyo-Ando, K., Mitani, S., Sugahara, K. and Nomura, K. (2003) Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature 423, 443-448
9. Silbert, J. E. and Sugumaran, G. (2002) Biosynthesis of chondroitin/dermatan sulfate. IUBMB Life 54, 177-186
10. Kusche-Gullberg, M. and Kjellén, L. (2003) Sulfotransferases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 13, 605-611
11. Kitagawa, H., Uyama, T. and Sugahara, K. (2001) Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem. 276, 38721-38726
12. Uyama, T., Kitagawa, H., Tamura, J. and Sugahara, K. (2002) Molecular cloning and expression of human chondroitin N- acetylgalactosaminyltransferase: the key enzyme for chain initiation and elongation of chondroitin/dermatan sulfate on the protein linkage region tetrasaccharide shared by heparin/heparan sulfate. J. Biol. Chem. 277, 8841-8846
13. Gotoh, M., Sato, T., Akashima, T., Iwasaki, H., Kameyama, A., Mochizuki, H., Yada, T., Inaba, N., Zhang, Y., Kikuchi, N. et al. (2002) Enzymatic synthesis of chondroitin with a novel chondroitin sulfate N- acetylgalactosaminyltransferase that transfers N-acetylgalactosamine to glucuronic acid in initiation and elongation of chondroitin sulfate synthesis. J. Biol. Chem. 277, 38189-38196
14. Sato, T., Gotoh, M., Kiyohara, K., Akashima, T., Iwasaki, H., Kameyama, A., Mochizuki, H., Yada, T., Inaba, N., Togayachi, A. et al. (2003) Differential roles of two N-acetylgalactosaminyltransferases, CSGalNAcT-1, and a novel enzyme, CSGalNAcT-2. Initiation and elongation in synthesis of chondroitin sulfate. J. Biol. Chem. 278, 3063-3071
15. Uyama, T., Kitagawa, H., Tanaka, J., Tamura, J., Ogawa, T. and Sugahara, K. (2003) Molecular cloning and expression of a second chondroitin N-acetylgalactosaminyltransferase involved in the initiation and elongation of chondroitin/dermatan sulfate. J. Biol. Chem. 278, 3072-3078
16. Gotoh, M., Yada, T., Sato, T., Akashima, T., Iwasaki, H., Mochizuki, H., Inaba, N., Togayachi, A., Kudo, T., Watanabe, H. et al. (2002) Molecular cloning and characterization of a novel chondroitin sulfate glucuronyltransferase that transfers glucuronic acid to N-acetylgalactosamine. J. Biol. Chem. 277, 38179-38188
17. Kitagawa, H., Izumikawa, T., Uyama, T. and Sugahara, K. (2003) Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization. J. Biol. Chem. 278, 23666-23671
18. Yada, T., Gotoh, M., Sato, T., Shionyu, M., Go, M., Kaseyama, H., Iwasaki, H., Kikuchi, N., Kwon, Y.-D., Togayachi, A. et al. (2003) Chondroitin sulfate synthase-2. Molecular cloning and characterization of a novel human glycosyltransferase homologous to chondroitin sulfate glucuronyltransferase, which has dual enzymatic activities. J. Biol. Chem. 278, 30235-30247
19. Busse, M. and Kusche-Gullberg, M. (2003) In vitro polymerization of heparan sulfate backbone by the EXT proteins. J. Biol. Chem. 278, 41333-41337
20. Kim, B.-T., Kitagawa, H., Tanaka, J., Tamura, J. and Sugahara, K. (2003) In vitro heparan sulfate polymerization: crucial roles of core protein moieties of primer substrates in addition to the EXT1-EXT2 interaction. J. Biol. Chem. 278, 41618-41623
21. Yada, T., Sato, T., Kaseyama, H., Gotoh, M., Iwasaki, H., Kikuchi, N., Kwon, Y.-D., Togayachi, A., Kudo, T., Watanabe, H. et al. (2003) Chondroitin sulfate synthase-3. Molecular cloning and characterization. J. Biol. Chem. 278, 39711-39725
22. Nawa, K., Sakano, K., Fujiwara, H., Sato, Y., Sugiyama, N., Teruuchi, T., Iwamoto, M. and Marumoto, Y. (1990) Presence and function of chondroitin-4-sulfate on recombinant human soluble thrombomodulin. Biochem. Biophys. Res. Commun. 171, 729-737
23. Nadanaka, S., Kitagawa, H. and Sugahara, K. (1998) Demonstration of the immature glycosaminoglycan tetrasaccharide sequence GlcAβ1-3Galβ1- 3Galβ1-4Xyl on recombinant soluble human α-thrombomodulin. An oligosaccharide structure on a 'part-time' proteoglycan. J. Biol. Chem. 273, 33728-33734
24. Kitagawa, H. and Paulson, J. C. (1994) Cloning of a novel α2,3-sialyltransferase that sialylates glycoprotein and glycolipid carbohydrate groups. J. Biol. Chem. 269, 1394-1401
25. Mizushima, S. and Nagata, S. (1990) pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18, 5322
26. Kitagawa, H., Tsutsumi, K., Ujikawa, M., Goto, F., Tamura, J., Neumann, K. W., Ogawa, T. and Sugahara, K. (1997) Regulation of chondroitin sulfate biosynthesis by specific sulfation: acceptor specificity of serum β-GalNAc transferase revealed by structurally defined oligosaccharides. Glycobiology 7, 531-537
27. Kitagawa, H., Ujikawa, M., Tsutsumi, K., Tamura, J., Neumann, K. W., Ogawa, T. and Sugahara, K. (1997) Characterization of serum β- glucuronyltransferase involved in chondroitin sulfate biosynthesis. Glycobiology 7, 905-911
28. Sugahara, K., Shigeno, K., Masuda, M., Fujii, N., Kurosaka, A. and Takeda, K. (1994) Structural studies on the chondroitinase ABC-resistant sulfated tetrasaccharides isolated from various chondroitin sulfate isomers. Carbohydr. Res. 255, 145-163
29. Sugahara, K., Ohkita, Y., Shibata, Y., Yoshida, K. and Ikegami, A. (1995) Structural studies on the hexasaccharide alditols isolated from the carbohydrate-protein linkage region of dermatan sulfate proteoglycans of bovine aorta. Demonstration of iduronic acid-containing components. J. Biol. Chem. 270, 7204-7212
30. Kinoshita, A. and Sugahara, K. (1999) Microanalysis of glycosaminoglycan-derived oligosaccharides labeled with a fluorophore 2-aminobenzamide by high-performance liguid chromatography: application to disaccharide composition analysis and exoseguencing of oligosaccharides. Anal. Biochem. 269, 367-378
31. Senay, C., Lind, T., Muguruma, K., Tone, Y., Kitagawa, H., Sugahara, K., Lidholt, K., Lindahl, U. and Kusche-Gullberg, M. (2000) The EXT1/EXT2 tumor suppressors: catalytic activities and role in heparan sulfate biosynthesis. EMBO Rep. 1, 282-286
32. Itano, N. and Kimata, K. (2002) Mammalian hyaluronan synthases. IUBMB Life 54, 195-199
33. Itano, N., Sawa, T., Yoshida, M., Lenas, P., Yamada, Y., Imagawa, M., Shinomura, T., Hamaguchi, M., Yoshida, Y., Ohnuki, Y. et al. (1999) Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J. Biol. Chem. 274, 25085-25092
34. Michele, D. E. and Campbell, K. P. (2003) Dystrophin-glycoprotein complex: post-translational processing and dystroglycan function. J. Biol. Chem. 278, 15457-15460
35. Manya, H., Chiba, A., Yoshida, A., Wang, X., Chiba, Y., Jigami, Y., Margolis, R. U. and Endo, T. (2004) Demonstration of mammalian protein O-mannosyltransferase activity: coexpression of POMT1 and POMT2 reguired for enzymatic activity. Proc. Natl. Acad. Sci. U.S.A. 101, 500-505
36. Izumikawa, T., Kitagawa, H., Mizuguchi, S., Nomura, K. H., Nomura, K., Tamura, J., Gengyo-Angyo, K., Mitani, S. and Sugahara, K., (2004) Nematode chondroitin polymerizing factor showing cell-/organ-specific expression is indispensable for chondroitin synthesis and embryonic cell division. J. Biol. Chem. 279, 53755-53761