Biosynthesis of chondroitin/dermatan sulfate

IUBMB Life

Volumn 54, Issue 4, 2002, Pages 177-186

  Silbert, Jeremiah E ^a,b   Sugumaran, Geetha ^a,b,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biosynthesis; Chondroitin sulfate; Dermatan sulfate

Indexed keywords

CHONDROITIN SULFATE; DERMATAN SULFATE; GLYCOSAMINOGLYCAN;

BIOSYNTHESIS; CELLULAR DISTRIBUTION; CONNECTIVE TISSUE; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HUMAN; MOLECULAR CLONING; NONHUMAN; PROTEIN PHOSPHORYLATION; REVIEW;

ANIMALS; CHONDROITIN SULFATES; DERMATAN SULFATE; HUMANS;

EID: 0036818369     PISSN: 15216543     EISSN: None     Source Type: Journal    
DOI: 10.1080/15216540214923     Document Type: Review

References (82)

1. Roden, L. (1980) Structure and metabolism of connective tissue proteoglycans. In The Biochemistry of Glycoproteins and Proteoglycans (Lennarz, W. J., ed.). pp. 267-371, Plenum Press, New York.
2. Silbert, J. E., Bernfield, M., and Kokenyesi, R. (1997) Proteoglycans: A special class of glycoproteins. In Glycoproteins II (Montreuil, J., Vliegenthart, J. F. G., and Schachter, H., eds.). pp. 1-31, Elsevier, New York.
3. Sugumaran, G., and Vertel, B. M. (2000) Biosynthesis of chondroitin sulfate and dermatan sulfate proteoglycans. In Oligosaccharides in Chemistry and Biology: A Comprehensive Handbook (Ernst, B., Hart, G., and Sinay, P., eds.). pp. 375-394, Wiley VCH.
4. Kjellen, L., and Lindahl, U. (1991) Proteoglycans: Structures and interactions. Annu. Rev. Biochem. 60, 443-475.
5. Wight, T. N., Heinegard, D. K., and Hascall, V. C. (1991) Proteoglycans: structure and function. In Cell Biology of the Extracellular Matrix, 2nd ed. (Hay, E. D., ed.). pp. 45-78, Plenum Press, New York.
6. Iozzo, R. V. (1998) Matrix proteoglycans: From molecular design to cellular function. Annu. Rev. Biochem. 67, 609-652.
7. 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. Ann. Rev. Cell Biol. 8, 365-393.
8. Stevens, R. L. (1987) Intracellular proteoglycans in cells of the immune system. In Biology of Proteoglycans (Wight T. N., and Mecham, R. P., eds.). pp. 367-387, Academic Press, Orlando.
9. Sugahara, K., and Kitagawa, H. (2002) Heparin and heparan sulfate biosynthesis. IUBMB Life 54, 163-175.
10. Lyle, S., Stanczak, J., Ng, K., and Schwartz, N. B. (1994) Rat chondrosarcoma ATP sulfurylase and adenosine 5′-phosphosulfate kinase reside on a single bifunctional protein. Biochemistry 33, 5920-5925.
11. Esko, J. D., Elgavish, A., Prasthofer, T., Taylor, W. H., and Weinke, J. L. (1986) Sulfate transport-deficient mutants of Chinese hamster ovary cells: Sulfation of glycosaminoglycans dependent on cysteine. J. Biol. Chem. 261, 15725-15733.
12. Humphries, D. E., Silbert, C. K., and Silbert, J. E. (1988) Sulphation by cultured cells: Cysteine, cysteinesulphinic acid, and sulphite as sources for proteoglycan sulphate. Biochem. J. 252, 305-308.
13. Silbert, C. K., Humphries, D. E., Palmer, M. E., and Silbert, J. E. (1991) Effects of sulfate deprivation on the production of chondroitin/dermatan sulfate by cultures of skin fibroblasts from normal and diabetic individuals. Arch. Biochem. Biophys. 285, 137-141.
14. 2- concentration. J. Biol. Chem. 257, 917-923.
15. Silbert, J. E., and DeLuca, S. (1967) The synthesis of uridine diphosphate xylose by cell-free preparations from mouse mast cell tumors. Biochim. Biophys. Acta 141, 193-196.
16. Kearns, A. E., Vertel, B. M., and Schwartz, N. B. (1993) Topography of glycosylation and UDP-xylose production. J. Biol. Chem. 268, 11097-11104.
17. Abeijon, C., Mandon, E. C., and Hirschberg, C. B. (1997) Transporters of nucleotide sugars, nucleotide sulfate and ATP in the Golgi apparatus. Trends Biochem. Sci. 22, 203-207.
18. Toma, L., Pinhal, M. M., Dietrich C. P., Nader, H. B., and Hirschberg, C. B. (1996) Transport of UDP-galactose into the Golgi lumen regulates the biosynthesis of proteoglycans. J. Biol. Chem. 271, 3897-3906.
19. Esko, J. D., and Zhang, L. (1996) Influence of core protein sequence on glycosaminoglycan assembly. Curr. Opin. Struct. Biol. 6, 663-670.
20. Sobue, M., Habuchi, H., Ito, K., Yonekura, H., Oguri, K., Sakurai, K., Kamohara, S., Ueno, Y., Noyori, R., and Suzuki, S. (1987) β-D-Xylosides and their analogues as artificial initiators of glycosaminoglycan chain synthesis. A glycone-related variation in their effectiveness in vitro and in ovo. Biochem. J. 241, 591-601.
21. Robinson, J. A., and Robinson, H. C. (1981) Control of chondroitin sulphate biosynthesis. β-D-Xylopyranosides as substrates for UDP-galactose: D-xylose transferase from embryonic chicken cartilage. Biochem. J. 194, 839-846.
22. Sugumaran, G., Katsman, M., and Silbert, J. E. (1992) Effects ofbrefeldin A on the localization of chondroitin sulfate-synthesizing enzymes: Activities in subfractions of the Golgi from chick embryo epiphyseal cartilage. J. Biol. Chem. 267, 8802-8806.
23. Etchison, J. R., Srikrishna, G., and Freeze, H. H. (1995) A novel method to co-localize glycosaminoglycan-core oligosaccharide glycosyltransferases in rat liver Golgi. Co-localization of galactosyltransferase I with a sialyltransferase. J. Biol. Chem. 270, 756-764.
24. Wei, G., Bai, X., Sarkar, A., and Esko, J. D. (1999) Formation of HNK-1 determinants and the glycosaminoglycan tetrasaccharide linkage region by UDP-GlcUA: galactose β1,3-glucuronosyltransferases. J. Biol. Chem. 274, 7857-7864.
25. Sugumaran, G., Katsman, M., and Silbert, J. E. (1998) Subcellular colocalization and potential interaction of glucuronosyl transferases with nascent proteochondroitin sulphate at Golgi sites of chondroitin synthesis. Biochem. J. 329, 203-208.
26. 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. U.S.A. 98, 12984-12989.
27. Rohrmann, K., Niemann, R., and Buddecke, E. (1985) Two N-acetylgalactosaminyl-transferases are involved in the biosynthesis of chondroitin sulfate. Eur. J. Biochem. 148, 463-469.
28. Nadanaka, S., Kitagawa, H., Goto, F., Tamura, J., Neumann, K. W., Ogawa, T., and Sugahara, K. (1999) Involvement of the core protein in the first β-N-acetylgalactosamine transfer to the glycosaminoglycan protein linkage-region tetrasaccharide and in the subsequent polymerization: The critical determining step for chondroitin sulphate biosynthesis. Biochem. J. 340, 353-357.
29. 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 tetrasacccharide shared by heparin/heparan sulfate. J. Biol. Chem. 277, 8841-8846.
30. Silbert, J. E., and DeLuca, S. (1969) Biosynthesis of chondroitin sulfate: III. Formation of sulfated glycosaminoglycan with a microsomal preparation from chick cartilage. J. Biol. Chem. 244, 876-881.
31. Lewis, R. G., Spencer, A. F., and Silbert, J. E. (1973) Biosynthesis of glycosaminoglycans by microsomal preparations from cultured mastocytoma cells. Biochem. J. 134, 465-471.
32. Silbert, J. E., and Freilich, L. S., (1980) Biosynthesis of chondroitin sulfate by a Golgi-apparatus-enriched preparation from cultures of mouse mastocytoma cells. Biochem. J. 190, 307-313.
33. Silbert, J. E., and Reppucci, A. C., Jr. (1976) Biosynthesis of chondroitin sulfate: Independent addition of glucuronic acid and Nacetylgalactosamine to oligosaccharides. J. Biol. Chem. 251, 3942-3947.
34. Sugumaran, G., and Silbert, J. E. (1991) Subfractionation of chick embryo epiphyseal cartilage Golgi: localization of enzymes involved in the synthesis of the polysaccharide portion of proteochondroitin sulfate. J. Biol. Chem. 266, 9565-9569.
35. Velasco, A., Hidalgo, J., Perez-Vilar, J., Garcia-Herdrigo, G., and Navas, P. (1988) Detection of glycosaminoglycans in the Golgi complex of chondrocytes. Eur. J. Cell Biol. 47, 241-250.
36. Sugumaran, G., Katsman, M., and Silbert, J. E. (1992) Effects of brefeldin A on the synthesis of chondroitin 4-sulfate by cultures of mouse mastocytoma cells. Biochem. Biophys. Res. Commun. 183, 357-361.
37. Uhlin-Hansen, L., Kusche-Gullberg, M., Berg, E., Eriksson, I., and Kjellen, L. (1997) Mouse mastocytoma cells synthesize undersulfated heparin and chondroitin sulfate in the presence of brefeldin A. J. Biol. Chem. 272, 3200-3206.
38. Sugumaran, G., Katsman, M., Sunthankar, P., and Drake, R. R. (1997) Purification of glucuronosyl transferase II and use of photoaffinity labeling for characterization of the enzyme as an 80-kDa protein. J. Biol. Chem. 272, 14399-14403.
39. Kitagawa, H., Uyama, T., and Sugahara, K. (2001) Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem. 276, 38721-38726.
40. DeAngelis, P. L., and Padgett-McCue, A. J. (2000) Identification and molecular cloning of a chondroitin synthase from Pasteurella multocida type F. J. Biol. Chem. 275, 24124-24129.
41. Ninomiya, T., Sugiura, N., Tawada, A., Sugimoto, K., Watanabe, H., and Kimata, K. (2002) Molecular cloning and characterization of chondroitin polymerase from Escherichia coli strain K4. J. Biol. Chem. 277, 21567-21575.
42. Oegema, T. R. J., Kraft, E. L., Jourdian, G. W., and VanValen, T. R. (1984) Phosphorylation of chondroitin sulfate in proteoglycans from the Swarm rat chondrosarcoma. J. Biol. Chem. 259, 1720-1726.
43. Lohmander, L. S., Hascall, V. C., Yanagishita, M., Kuettner, K. E., and Kimura, J. H. (1986) Post-translational events in proteoglycan synthesis: Kinetics of synthesis of chondroitin sulfate and oligosaccharides on the core protein. Arch. Biochem. Biophys. 250, 211-227.
44. Moses, J., Oldberg, A., Cheng, F., and Fransson, L.-A. (1997) Biosynthesis of the proteoglycan decorin - Transient 2-phosphorylation of xylose during formation of the trisaccharide linkage region. Eur. J. Biochem. 248, 521-526.
45. 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.
46. Ueno, M., Yamada, S., Zako, M., Bernfield, M., and Sugahara, K. (2001) Structural characterization of heparan sulfate and chondroitin sulfate of syndecan-1 purified from normal routine mammary gland epithelial cells. Common phosphorylation of xylose and differential sulfation of galactose in the protein linkage region tetrasaccharide sequence. J. Biol. Chem. 276, 29134-29140.
47. Funderburgh, J. L. (2002) Keratan sulfate biosynthesis. IUBMB Life 54, 187-194.
48. Saito, H., Yamagata, T., and Suzuki, S. (1968) Enzymatic methods for the determination of small quantities of isomeric chondroitin sulfates. J. Biol. Chem. 243, 1530-1542.
49. Ernst, S., Langer, R., Cooney, S. L., and Sasisekharan, R. (1995) Enzymatic degradation of glycosaminoglycans. Crit. Rev. Biochem. Mol. Biol. 30, 387-444.
50. Cheng, F., Yoshida, K., Heinegard, D., and Fransson, L.-A. (1992) A new method for sequence analysis of glycosaminoglycans from heavily substituted proteoglycans reveals non-random positioning of 4- and 6-O-sulphated N-acetylgalactosamine in aggrecan-derived chondroitin sulphate. Glycobiology 2, 553-561.
51. Shibata, S., Midura, R. J., and Hascall, V. C. (1992) Structural analysis of the linkage region oligosaccharides and unsaturated disaccharides from chondroitin sulfate using CarboPac PAC1. J. Biol. Chem. 267, 6548-6455.
52. Humphries, D. E., Silbert, C. K., and Silbert, J. E. (1986) Glycosaminoglycan production by bovine aortic endothelial cells cultured in sulfate-depleted medium. J. Biol. Chem. 261, 9122-9127.
53. Humphries, D. E., Sugumaran, G., and Silbert, J. E. (1989) Techniques for decreasing the sulfation of proteoglycans produced by cultured cells. Methods Enzymol. 179, 428-434.
54. Sugumaran, G., and Silbert, J. E. (1990) Relationship of sulfation to ongoing chondroitin polymerization during biosynthesis of chondroitin 4-sulfate by microsomal preparations from cultured mouse mastocytoma cells. J. Biol. Chem. 265, 18284-18288.
55. DeLuca, S., Richmond, M. E., and Silbert, J. E. (1973) Biosynthesis of chondroitin sulfate: Sulfation of the polysaccharide chain. Biochemistry 12, 3911-3915.
56. Sugumaran, G., and Silbert, J. E. (1988) Sulfation of chondroitin: Specificity, degree of sulfation, and detergent effects with 4-sulfating and 6-sulfating microsomal systems. J. Biol. Chem. 263, 4673-4678.
57. Sugumaran, G., and Silbert, J. E. (1992) Effects of detergent on the sulphation of chondroitin by cell-free preparations from chick embryo epiphyseal cartilage. Biochem. J. 285, 577-583.
58. Silbert, J. E., Sugumaran, G., and Cogburn, J. N. (1993) Sulfation of proteochondroitin and 4-methylumbelliferyl β-D-xyloside-chondroitin formed by mouse mastocytoma cells cultured in sulfate-deficient medium. Biochem. J. 296, 119-126.
59. 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.
60. Fukuta, M., Uchimura, K., Nakashima, K., Kato, M., Kimata, K., Shinomura, T., and Habuchi, O. (1995) Molecular cloning and expression of chick chondrocyte chondroitin 6-sulfotransferase. J. Biol. Chem. 270, 18575-18580.
61. Sugumaran, G., Katsman, M., and Drake, R. R. (1995) Purification, photoaftinity labeling, and characterization of a single enzyme for 6-sulfation of both chondroitin sulfate and keratan sulfate. J. Biol. Chem. 270, 22483-22487.
62. Habuchi, O. (1998) Diversity and functions of glycosaminoglycan sulfotransferases. Biochim. Biophys. Acta 1474, 115-127.
63. Ohtake, S., Ito, Y., Fukuta, M., and Habuchi, O. (2001) Human N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase cDNA is related to human B cell RAG-associated gene. J. Biol. Chem. 276, 43894-43900.
64. Nadanaka, S., Fujita, M., and Sugahara, K. (1999) Demonstration of a novel sulfotransferase in fetal bovine serum, which transfers sulfate to the C6 position of the GalNAc residue in the sequence iduronic acid α1-3GalNAc β1-4iduronic acid in dermatan sulfate. FEBS Lett. 452, 185-189.
65. Uchimura, K., Kadomatsu, K., Nishimura, H., Muramatsu, H., Nakamura, E., Kurosawa, N., Habuchi, O., El-Fasakhany, F. M., Yoshikai, Y., and Muramatsu, T. (2002) Functional analysis of the chondroitin 6-sulfotransferase gene in relation to lymphocyte subpopulations, brain development and oversulfated chondroitin sulfate. J. Biol. Chem. 277, 1443-1450.
66. Yamauchi, S., Mita, S., Matsubara, T., Fukuta, M., Habuchi, H., Kimata, K., and Habuchi, O. (2000) Molecular cloning and expression of chondroitin 4-sulfotransferase. J. Biol. Chem. 275, 8975-8978.
67. Evers, M. R., Xia, G., Kang, H. G., Schachner, M., and Baenziger, J. U. (2001) Molecular cloning and characterization of a dermatan-specific N-acetylgalactosamine 4-O-sulfotransferase. J. Biol. Chem. 276, 36344-36353.
68. Silbert, J. E., Palmer, M. E., Humphries, D. E., and Silbert, C. K. (1986) Formation of dermatan sulfate by cultured human skin fibroblasts: Effects of sulfate concentration on proportions of dermatan/chondroitin. J. Biol. Chem. 261, 13397-13400.
69. Silbert, J. E., Silbert, C. K., Humphries, D. E., and Sugumaran, G. (1993) Role of sulphation in dermatan formation. In Dermatan Sulphate Proteoglycans: Chemistry, Biology, and Chemical Pathology (Scott J. E., ed.). pp. 147-158, Portland Press, London.
70. Kobayashi, M., Sugumaran, G., Liu, J., Shworak, N. W., Silbert, J. E., and Rosenberg, R. D. (1999) Molecular cloning and characterization of a human uronyl 2-sulfotransferase that sulfates iduronyl and glucuronyl residues in dermatan/chondroitin sulfate. J. Biol. Chem. 274, 10474-10480.
71. Kitagawa, H., Tanaka, Y., Yamada, S., Seno, N., Haslam, S. M., Morris, H. R., Dell, A., and Sugahara, K. (1997) A novel pentasaccharide sequence GlcA(3-sulfate)(β1-3)GalNAc(4-sulfate)(β1-4)(Fucα1-3) GlcA(1-3)GalNAc(4-sulfate) in the oligosaccharides isolated from king crab cartilage chondroitin sulfate K and its differential susceptibility to chondroitinases and hyaluronidase. Biochemistry 36, 3998-4008.
72. Malmstrom, A., Fransson, L.-A., Hook, M., and Lindahl, U. (1975) Biosynthesis of dermatan sulfate. 1. Formation of L-iduronic acid residues. J. Biol. Chem. 250, 3419-3425.
73. Hoppe, U., Glossl, J., and Kresse, H. (1985) Influence of monensin on biosynthesis, processing and secretion of proteodermatan sulfate by skin fibroblasts. Eur. J. Biochem. 152, 91-97.
74. Silbert, J. E. (1978) Biosynthesis of chondroitin sulfate: chain termination. J. Biol. Chem. 253, 6888-6892.
75. Otsu, K., Inoue, H., Tsuzuki, Y., Yonekura, H., Nakanishi, Y., and Suzuki, S. (1985) A distinct terminal structure in newly synthesized chondroitin sulphate chains. Biochem. J. 227, 37-48.
76. Cogburn, J. N., and Silbert, J. E. (1986) The effect of penultimate N-acetylgalactosamine 4-sulfate on chondroitin chain elongation. Carbohyd. Res. 151, 207-212.
77. Sugumaran, G., Cogburn, J. N., and Silbert, J. E. (1986) Simultaneous sulfation of endogenous chondroitin sulfate and chondroitin-derived oligosaccharides: Studies with separate 4-sulfating and 6-sulfating microsomal systems. J. Biol. Chem. 261, 12659-12664.
78. Nakanishi, Y., Shimizu, M., Otsu, S., Tsuji, M., and Suzuki, S. (1981) A terminal 6-sulfotransferase catalyzing a synthesis of N-acetylgalactosamine 4,6-bisulfate residue at the nonreducing terminal position of chondroitin sulfate. J. Biol. Chem. 256, 5443-5449.
79. Otsu, K., Inoue, H., Nakanishi, Y., Kato, S., Tsuji, M., and Suzuki, S. (1984) A sulfotransferase-sulfatase system in avian oviduct which catalyzes a conversion of UDP-N-acetylgalactosamine 4-sulfate to the 6-sulfate isomer. J. Biol. Chem. 259, 6403-6410.
80. Midura, R.J., Calabro, A., Yanagishita, M., and Hascall,V. C. (1995) Nonreducing end structures of chondroitin sulfate chains on aggrecan isolated from Swarm rat chondrosarcoma cultures. J. Biol. Chem. 270, 8009-8015.
81. Kokenyesi, R., and Silbert, J. E. (1997) Immortalized cloned mouse chondrocytes (MC 615) produce three different matrix proteoglycans with core protein-specific chondroitin/dermatan sulphate structures. Biochem. J. 327, 831-839.
82. Silbert, J. E. (1967) Biosynthesis of heparin: IV. N-Deacetylation of a precursor glycosaminoglycan. J. Biol. Chem. 242, 5146-5152.