Chondroitin sulfate N-acetylgalactosaminyltransferase-1 is required for normal cartilage development

Biochemical Journal

Volumn 432, Issue 1, 2010, Pages 47-55

  Watanabe, Yumi ^a,b   Takeuchi, Kosei ^a,b   Higa Onaga, Susumu ^a   Sato, Michiko ^a   Tsujita, Mika ^b   Abe, Manabu ^b   Natsume, Rie ^b   Li, Minqi ^b,c   Furuichi, Tatsuya ^d,f   Saeki, Mika ^e   Izumikawa, Tomomi ^e   Hasegawa, Ayumi ^b   Yokoyama, Minesuke ^b   Ikegawa, Shiro ^d   Sakimura, Kenji ^b   Amizuka, Norio ^b,c   Kitagawa, Hiroshi ^e   Igarashi, Michihiro ^a,b  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d RIKEN   (Japan)

^e KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

^f JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cartilage; Chondroitin sulfate; Collagen fibre; Gene knockout; Glycosaminoglycan; N acetylgalactosaminyltransferase (GalNAcT)

Indexed keywords

CHONDROITIN SULFATES; COLLAGEN FIBRE; GENE KNOCKOUT; GLYCOSAMINOGLYCANS; N- ACETYLGALACTOSAMINYLTRANSFERASE (GALNACT);

COLLAGEN; GENES; LIGAMENTS; SULFUR COMPOUNDS;

CARTILAGE;

CHONDROITIN SULFATE; COLLAGEN TYPE 2; CYCLINE; GLYCOSYLTRANSFERASE; N ACETYLGALACTOSAMINYLTRANSFERASE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARTILAGE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EPIPHYSIS; FORELIMB; GENE INACTIVATION; LUMBAR SPINE; MOUSE; MOUSE MUTANT; MUSCULOSKELETAL DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PELVIC GIRDLE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SKULL; WILD TYPE;

ANIMALS; BLOTTING, WESTERN; CELL LINE; CELL PROLIFERATION; CHONDROCYTES; CHONDROGENESIS; CHONDROITIN SULFATES; COLLAGEN TYPE II; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GROWTH PLATE; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; N-ACETYLGALACTOSAMINYLTRANSFERASES; PROLIFERATING CELL NUCLEAR ANTIGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

MUS;

EID: 78649745551     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20100847     Document Type: Article

References (30)

1. Gandhi, N. S. and Mancera, R. L. (2008) The structure of glycosaminoglycans and their interactions with proteins. Chem. Biol. Drug Des. 72, 455-492
2. Kitagawa, H., Uyama, T. and Sugahara, K. (2001) Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem. 276, 38721-38726
3. 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
4. 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
5. 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
6. Gotoh, M., Yada, T., Sato, T., Akashima, T., Iwasaki, H., Mochizuki, H., Inaba, N., Togayachi, A., Kudo, T., Watanabe, H. 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, 38179-38188
7. Sato, T., Gotoh, M., Kiyohara, K., Akashima, T., Iwasaki, H., Kameyama, A., Mochizuki, H., Yada, T., Inaba, N., Togayachi, A. et al. (2003) Molecular cloning and characterization of a novel human β1,4-N- acetylgalactosaminyltransferase, β4GalNAc-T3, responsible for the synthesis of N,N′-diacetyllactosediamine, GalNAcβ1-4GlcNAc. J. Biol. Chem. 278, 3063-3071
8. Izumikawa, T., Uyama, T., Okuura, Y., Sugahara, K. and Kitagawa, H. (2007) Involvement of chondroitin sulfate synthase-3 (chondroitin synthase-2) in chondroitin polymerization through its interaction with chondroitin synthase-1 or chondroitin-polymerizing factor. Biochem. J. 403, 545-552 (Pubitemid 46706983)
9. Izumikawa, T., Koike, T., Shiozawa, S., Sugahara, K., Tamaura, J. and Kitagawa, H. (2008) Identification of chondroitin sulfate glucuronyltransferase as chondroitin synthase-3 involved in chondroitin polymerization, chondroitin polymerization is achieved by multiple enzyme complexes consisting of chondroitin synthase family members. J. Biol. Chem. 283, 11396-11406
10. 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
11. Burdan, F., Szumilo, J., Korobowicz, A., Farooquee, R., Patel, S., Patel, A., Dave, A., Szumiko, M., Solecki, M., Klepacz, R. and Dudka, J. (2009) Morphology and physiology of the epiphyseal growth plate. Folia Histochem. Cytobiol. 47, 5-16
12. Quintana, L. M. S., zur Nieden, N. I. and Semino, C. E. (2009) Morphogenetic and regulatory mechanisms during developmental chondrogenesis, new paradigms for cartilage tissue engineering. Tissue Eng. B. 15, 29-41
13. Kiani, C., Chen, L., Wu, Y. J., Yee, A. J. and Yang, B. B. (2002) Roles of aggrecan domains in biosynthesis, modification by glycosaminoglycans and product secretion. Cell Res. 12, 19-32
14. Sakai, K., Kimata, K., Sato, T., Gotoh, M., Narimatsu, H., Shinomiya, K. and Watanabe, H. (2007) Chondroitin sulfate N-acetylgalactosaminyltransferase-1 plays a critical role in chondroitin sulfate synthesis in cartilage. J. Biol. Chem. 282, 4152-4161
15. Mishina, M. and Sakimura, K. (2007) Conditional gene targeting on the pure C57BL/6 genetic background. Neurosci. Res. 58, 105-112
16. Takeuchi, T., Nomura, T., Tsujita, M., Suzuki, M., Fuse, T., Mori, H. and Mishina, M. (2002) Flp recombinase transgenic mice of C57BL/6 strain for conditional gene targeting. Biochem. Biophys. Res. Commun. 293, 953-957
17. Kitayama, K., Abe, M., Kakizaki, T., Honma, D., Natsume, R., Fukaya, M., Watanabe, M., Miyazaki, J., Mishina, M. and Sakimura, K. (2001) Purkinje cell-specific and inducible gene recombination system generated from C57BL/6 mouse ES cells. Biochem. Biophys. Res. Commun. 281, 1134-1140
18. Nakamura, K., Manabe, T., Watanabe, M., Mamiya, T., Ichikawa, R., Kiyama, Y., Sanbo, M., Yagi, T., Inoue, Y., Nabeshima, T. et al. (2001) Enhancement of hippocampal LTP, reference memory and sensorimotor gating in mutant mice lacking a telencephalon-specific cell adhesion molecule. Eur. J. Neurosci. 13, 179-189
19. Fuse, T., Kanai, Y., Kanai-Azuma, M., Suzuki, M., Nakamura, K., Mori, H., Hayashi, Y. and Mishina, M. (2004) Conditional activation of RhoA suppresses the epithelial to mesenchymal transition at the primitive streak during mouse gastrulation. Biochem. Biophys. Res. Commun. 318, 665-672
20. Tsujita, M., Mori, H., Watanabe, M., Suzuki, M., Miyazaki, J. and Mishina, M. (1999) Cerebellar granule cell-specific and inducible expression of Cre recombinase in the mouse. J. Neurosci. 19, 10318-10323 (Pubitemid 30228039)
21. Rodriguez, E., Roland, S. K., Plaas, A. and Roughley, P. J. (2006) The glycosaminoglycan attachment regions of human aggrecan. J. Biol. Chem. 281, 18444-18450
22. Kinoshita, A. and Sugahara, K. (1999) Microanalysis of glycosaminoglycan-derived oligosaccharides labeled with a fluorophore 2-aminobenzamide by high-performance liquid chromatography: application to disaccharide composition analysis and exosequencing of oligosaccharides. Anal. Biochem. 269, 367-378
23. Koike, T., Izumikawa, T., Tamura, J. and Kitagawa, H. (2009) FAM20B is a kinase that phosphorylates xylose in the glycosaminoglycan-protein linkage region. Biochem. J. 421, 157-162
24. Amizuka, N., Davidson, D., Liu, H., Valverde-Franco, G., Chai, S., Maeda, T., Ozawa, H., Hammond, V., Ornitz, D. M., Goltzman, D. and Henderson, J. E. (2004) Signalling by fibroblast growth factor receptor 3 and parathyroid hormone-related peptide coordinate cartilage and bone development. Bone 34, 13-25
25. Breton, C., Bettler, E., Joziasse, D. H., Geremia, R. A. and Imberty, A. (1998) Sequence-function relationships of prokaryotic and eukaryotic galactosyltransferases. J. Biochem. 123, 1000-1009 (Pubitemid 28305979)
26. Qasba, P. K., Ramakrishnan, B. and Boeggeman, E (2005) Substrate-induced conformational changes in glycosyltransferases. Trends Biochem. Sci. 30, 53-62
27. Lairson, L. L., Henrissat, B., Davies, G. J. and Withers, S. G. (2008) Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521-555
28. Hiraoka, S., Furuichi, T., Nishimura, G., Shibata, S., Yanagishita, M., Rimoin, D. L., Superti-Furga, A., Nikkels, P. G., Ogawa, M., Katsuyama, K. et al. (2007) Nucleotide-sugar transporter SLC35D1 is critical to chondroitin sulfate synthesis in cartilage and skeletal development in mouse and human. Nat. Med. 13, 1363-1367
29. Cortes, M., Baria, A. T. and Schwartz, N. B. (2009) Sulfation of chondroitin sulfate proteoglycans is necessary for proper Indian hedgehog signaling in the developing growth plate. Development 136, 1697-1706
30. Schwartz, N. B. and Domowicz, M. (2002) Chondrodysplasias due to proteoglycan defects. Glycobiology 12, 57R-68R