SOX9 transduction increases chondroitin sulfate synthesis in cultured human articular chondrocytes without altering glycosyltransferase and sulfotransferase transcription

Biochemical Journal

Volumn 414, Issue 2, 2008, Pages 231-236

  Tew, Simon R ^a   Pothacharoen, Peraphan ^b   Katopodi, Theoni ^c   Hardingham, Timothy E ^c  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b Faculty of Medicine Chiang Mai University   (Thailand)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Chondrocyte; Glycosaminoglycan; Glycosyltransferase; Proteoglycan; Sry type high mobility group box 9 (SOX9); Sulfotransferase

Indexed keywords

BACTERIOPHAGES; BIOACTIVITY; BIOCHEMICAL ENGINEERING; BIOCHEMISTRY; BIOSYNTHESIS; BODY FLUIDS; CELL CULTURE; CONTROL THEORY; ELECTRON ENERGY LEVELS; ENZYME ACTIVITY; ENZYMES; FLUID DYNAMICS; FLUID MECHANICS; GENE EXPRESSION; HYDROGELS; PROTEINS; SULFUR COMPOUNDS; TISSUE; TRANSCRIPTION; TRANSCRIPTION FACTORS;

CHONDROCYTE; GLYCOSAMINOGLYCAN; GLYCOSYLTRANSFERASE; PROTEOGLYCAN; SRY-TYPE HIGH-MOBILITY-GROUP BOX 9 (SOX9); SULFOTRANSFERASE;

ORGANIC POLYMERS;

AGGRECAN; DERMATAN SULFATE; GLYCOSAMINOGLYCAN; GLYCOSYLTRANSFERASE; SULFOTRANSFERASE; TRANSCRIPTION FACTOR SOX9; XYLAN 1,4 BETA XYLOSIDASE;

ARTICLE; CARTILAGE CELL; CELL AGGREGATION; CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SYNTHESIS; GENE EXPRESSION; HUMAN; HUMAN CELL; HYDRODYNAMICS; MONOLAYER CULTURE; PRIORITY JOURNAL; PROTEIN PROCESSING; RETROVIRUS; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; TRANSCRIPTION REGULATION;

AGGRECANS; CARTILAGE, ARTICULAR; CELLS, CULTURED; CHONDROCYTES; CHONDROITIN SULFATES; GLYCOSAMINOGLYCANS; GLYCOSYLTRANSFERASES; HIGH MOBILITY GROUP PROTEINS; HUMANS; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SULFOTRANSFERASES; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSDUCTION, GENETIC;

EID: 50949114221     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20080262     Document Type: Article

References (34)

1. Hardingham, T. E. and Fosang, A. J. (1992) Proteoglycans: many forms and many functions. FASEB J. 6, 861-870
2. Stokes, D. G., Liu, G., Dharmavaram, R., Hawkins, D., Piera-Velazquez, S. and Jimenez. S. A. (2001) Regulation of type-II collagen gene expression during human chondrocyte de-differentiation and recovery of chondrocyte-specific phenotype in culture involves Sry-type high-mobility-group box (SOX) transcription factors. Blochem. J. 360, 461-470
3. Bell, D. M., Leung, K. K., Wheatley, S. C., Ng, L. J., Zhou, S., Ling, K. W., Sham, M. H.. Koopman, P, Tam, P. P. and Cheah, K. S. (1997) SOX9 directly regulates the type-II collagen gene. Nat. Genet. 16, 174-178
4. Sekiya, I., Tsuji, K., Koopman, R, Watanabe, H., Yamada, Y, Shinomiya, K., Nifuji, A. and Noda. M. (2000) SOX9 enhances aggrecan gene promoter/ enhancer activity and is up-regulated by retinoic acid in a cartilage-derived cell line, TC6. J. Biol. Chem, 275, 10738-10744
5. Kou, I. and Ikegawa, S. (2004) SOX9-dependent and -independent transcriptional regulation of human cartilage link protein. J. Biol. Chem. 279, 50942-50948
6. Wagner, T., Wirth, J., Meyer, J., Zabel, B., Held, M., Zimmer, J., Pasantes, J., Bricarelli, F D,, Keutel, J., Hustert, E. et al. (1994) Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79, 1111-1120
7. Kusche-Gullberg, M. and Kjellen. L. (2003) Sulfotransterases in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 13, 605-611
8. Sugahara, K. and Kitagawa, H. (2000) Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr. Opin. Struct. Biol. 10, 518-527
9. Tew. S. R., Li, Y, Pothacharoen, P. Tweats, L. M., Hawkins, R. E. and Hardingham, T. E. (2005) Retroviral transduction with SOX9 enhances re-expression of the chondrocyte phenotype in passaged osteoarthritic human articular. chondrocytes. Osteoarthritis Cartilage 13, 80-89
10. Li, Y., Tew, S. R., Russell. A. M.. Gonzalez, K., Hardingham, T. E. and Hawkins, R. E. (2004) Transduction of human articular chondrocytes with adenoviral, retroviral and lentiviral vectors and the effects of enhanced expression of SOX9. Tissue Eng. 10, 575-584
11. Kimura, J. H., Hardingham, T. E. and Hascall, V. C. (1980) Assembly of newly synthesized proteoglycan and link protein into aggregates in cultures of chondrosarcoma chondrocytes. J. Blol. Chem. 255, 7134-7143
12. Martin, I., Jakob, M., Schafer, D., Dick, W., Spagnoli, G. and Heberer, M. (2001) Quantitative analysis of gene expression in human articular cartilage from normal and osteoarthritic joints. Osteoarthritis Cartilage 9, 112-118
13. Fritz, T. A. and Esko, J. D. (2001) Xyloside priming of glycosaminoglycan biosynthesis and inhibition of proteoglycan assembly. In Proteoglycan Protocols (lozzo, R. V, ed.), pp. 317-323, Humana Press, Totowa, NJ
14. Mitchell, D. and Hardingham, T. (1982) Monensin inhibits synthesis of proteoglycan, but not of hyaluronate, in chondrocytes. Biochem. J. 202. 249-254
15. Ratcliffe, A., Fryer, P. R. and Hardingham, T. E. (1985) Proteoglycan biosynthesis in chondrocytes: Protein A-gold localization of proteoglycan protein core and chondroitin sulfate within Golgi subcompartments. J. Cell Biol. 101, 2355-2365
16. de Graftenried, C, L. and Bertozzi, C. R. (2003) Golgi localization of carbohydrate sultotransferases is a determinant Of L-selectin ligand biosynthesis. J. Biol. Chem. 278. 40282-40295
17. 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, U.S.A. 97, 668-673
18. Pinhal. M. A., Smith, B., Olson, S., Ailkawa, J., Kimata, K. and Esko, J. D. (2001) Enzyme interactions in heparan sulfate biosynthesis: uronosyl 5-epimerase and 2-O-sultotransferase interact in vivo. Proc. Natl. Acad. Sci. U.S.A. 98, 12984-12989
19. Gotting, C., Kuhn, J.. Zahn, R., Brinkmann, T and Kleesiek, K. (2000) Molecular cloning and expression of human UDP-D-Xylose:proteoglycan core protein β-D-xylosyl-transferase and its first isoform XT-II. J. Mol. Biol. 304, 517-528
20. Okajima, T, Yoshida, K., Kondo, T, and Furukawa, K, (1999) Human homolog of Caenorhabditis elegans sqv-3 gene is galactosyltransferase I involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans. J. Biol. Chem. 274, 22915-22918
21. Almeida, R., Levery, S, B., Mandel, U., Kresse, H., Schwientek, T., Bennett, E. P. and Clausen, H. (1999) Cloning and expression of a proteoglycan UDP-galactose:β-xylose β1,4-galactosyltransterase I. A seventh member of the human 2b4-galactosyltransterase gene family. J. Biol. Chem. 274, 26165-26171
22. Bai, X., Zhou, D., Brown, J. R., Crawford. B. E,. Hennet, T. and Esko, J. D. (2001) Biosynthesis of the linkage region of glycosaminoglycans: cloning and activity of galactosyltransferase II, the sixth member of the β 1,3-galactosyltransferase family (β 3GaIT6). J. Biol. Chem. 276, 48189-48195
23. Kitagawa. H., Tone, Y, Tamura, J., Neumann, K. W., Ogawa, T, Oka, S., Kawasaki, T. and Sugahara, K. (1998) Molecular cloning and expression of glucuronyltransferase I involved in the biasynthesis of the glycosaminoglycan-protein linkage region of proteoglycans. J. Biol. Chem. 273, 6615-6618
24. Kitagawa, H., Taoka, M., Tone, Y. and Sugahara, K. (2001) Human glycosaminoglycan glucuronyltransferase I gene and a related processed pseudogene: genomic structure, chromosomal mapping and characterization. Biochem. J. 358, 539-546
25. Uyama, T, Kitagawa, H., Tamura, J.-I. 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 tetrasacchadde shared by hepatin/heparan sulfate. J. Blol. Chem. 277, 8841-8846
26. Uyama. T, Kitagawa, H., Tanaka, J., Tamura, J., Ogawa, T. and Sugahara, K. (2003) Molecular cloning and expression of a second chondioitin N-acetylgalactosaminyltransferase involved in the initiation and elongation of chondroitin/dermatan sulfate. J. Biol. Chem. 278, 3072-3078
27. 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
28. 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
29. Tsutsumi, K., Shimakawa, H., Kitagawa, H. and Sugahara, K. (1998) Functional expression and genomic structure of human chondroitin 6-sulfotransferase. FEBS Lett. 441, 235-241
30. Kitagawa, H., Fujita, M., Ito, N. and Sugahara. K. (2000) Molecular cloning and expression of a novel chondroitin 6-O-sulfotransferase. J. Biol. Chem. 275, 21075-21080
31. Hlraolka, N., Nakagawa, H., Ong, E., Akama, T. O., Fukuda, M. N, and Fukuda, M. (2000) Molecular cloning and expression of two distinct human chondroitin 4-O-sulfotransferases that belong to the HNK-1 sulfotransferase gene family. J. Biol. Chem. 275, 20188-20196
32. Hiraoka, A., Yano Ki, K., Kagami, N., Takeshige, K., Mio, H., Anazawa, H. and Sugimoto. S. (2001) Stem cell growth factor: in situ hybridization analysis on the gene expression, molecular characterization and in vitro proliferative activity of a recombinant preparation on primitive hematopoietic progenitor cells. Hematol. J. 2, 307-315
33. Ohtake, S., Ito, Y., Fukuta, M. and Habuchi, O. (2001) Human N-acetylgalactosamine 4-sultate 6-O-sulfotransferase cDNA is related to human B cell recombination activating gene-associated gene. J. Biol. Chem. 276, 43894-43900
34. Rong, J., Habuchi, H.. Kimata, K., Lindahl, U. and Kusche-Gullberg, M. (2000) Expression of heparan sulphate L-iduronyl 2-O-sulphotransferase in human kidney 293 cells results in increased D-glucuronyl 2-O-sulphation. Biochem. J. 346, 463-468