Bone and skin disorders caused by a disturbance in the biosynthesis of chondroitin sulfate and dermatan sulfate

Extracellular Matrix: Pathobiology and Signaling

Volumn , Issue , 2012, Pages 98-118

  Mizumoto, Shuji ^a   Sugahara, Kazuyuki ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

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EID: 85120294478     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (93)

1. Akatsu, C., Mizumoto, S., Kaneiwa, T., et al. (2011). Dermatan sulfate epimerase 2 is the predominant isozyme in the formation of the chondroitin sulfate/dermatan sulfate hybrid structure in postnatal developing mouse brain. Glycobiology 21, 565-574.
2. Almeida, R., Levery, S. B., Mandel, U., et al. (1999). Cloning and expression of a proteoglycan UDP-galactose: B-xylose ß1,4-galactosyltransferase I: aseventh member of the human ß4-galactosyltransferase gene family. J Biol Chem 274, 26165-26171.
3. Baasanjav, S., Al-Gazali, L., Hashiguchi, T., et al. (2011). Faulty initiation of proteoglycan synthesis causes cardiac and joint defects. Am J Hum Genet 89, 15-27.
4. 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 ß1,3-galactosyltransferase family (ß3GalT6). J Biol Chem 276, 48189-48195.
5. Bandah-Rozenfeld, D., Collin, R. W., Banin, E., et al. (2010). Mutations in IMPG2, encoding interphotoreceptor matrix proteoglycan 2, cause autosomal-recessive retinitis pigmentosa. Am J Hum Genet 87, 199-208.
6. Bao, X., Muramatsu, T., and Sugahara, K. (2005). Demonstration of the pleiotrophin-binding oligosaccharide sequences isolated from chondroitin sulfate/dermatan sulfate hybrid chains of embryonic pig brains. J Biol Chem 280, 35318-35328.
7. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007). Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037.
8. Bredrup, C., Knappskog, P. M., Majewski, J., Rødahl, E., and Boman, H. (2005). Congenital stromal dystrophy of the cornea caused by a mutation in the decorin gene. Invest Ophthalmol Vis Sci 46, 420-426.
9. Cabral, W. A., Chang, W., Barnes, A. M., et al. (2007). Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat Genet 39, 359-365.
10. Cichon, S., Muhleisen, T. W., Degenhardt, F. A., et al. (2011). Genome-wide association study identifies genetic variation in neurocan as a susceptibility factor for bipolar disorder. Am J Hum Genet 88, 372-381.
11. Dundar, M., Demiryilmaz, F., Demiryilmaz, I., et al. (1997). An autosomal recessive adducted thumb-club foot syndrome observed in Turkish cousins. Clin Genet 51, 61-64.
12. Dündar, M., Müller, T., Zhang, Q., et al. (2009). Loss of dermatan-4-sulfotransferase 1 function results in adducted thumb-clubfoot syndrome. Am J Hum Genet 85, 873-882.
13. 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.
14. Fukuta, M., Kobayashi, Y., Uchimura, K., Kimata, K., and Habuchi, O. (1998) Molecular cloning and expression of human chondroitin 6-sulfotransferase. Biochim Biophys Acta 1399, 57-61.
15. Gleghorn, L., Ramesar, R., Beighton, P., and Wallis, G. (2005). A mutation in the variable repeat region of the aggrecan gene (AGC1) causes a form of spondyloepiphyseal dysplasia associated with severe, premature osteoarthritis. Am J Hum Genet 77, 484-490.
16. Goossens, D., Van Gestel, S., Claes, S., et al. (2003). A novel CpG-associated brain-expressed candidate gene for chromosome 18q-linked bipolar disorder. Mol Psychiatry 8, 83-89.
17. Gotoh, M., Sato, T., Akashima, T., et al. (2002a). 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.
18. Gotoh, M., Yada, T., Sato, T., et al. (2002b). Molecular cloning and characterization of a novel chondroitin sulfate glucuronyltransferase that transfers glucuronic acid to N-acetylgalactosamine. J Biol Chem 277, 38179-38188.
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 ß-D-xylosyltransferase and its first isoform XT-II. J Mol Biol 304, 517-528.
20. Gulberti, S., Lattard, V., Fondeur, M., et al. (2005). Phosphorylation and sulfation of oligosaccharide substrates critically influence the activity of human ß1,4-galactosyltransferase 7 (GalT-I) and ß1,3-glucuronosyltransferase I (GlcAT-I) involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans. J Biol Chem 280, 1417-1425.
21. Harroch, S., Palmeri, M., Rosenbluth, J., et al. (2000). No obvious abnormality in mice deficient in receptor protein tyrosine phosphatase ß. Mol Cell Biol 20, 7706-7715.
22. Hermanns, P., Unger, S., Rossi, A., et al. (2008). Congenital joint dislocations caused by carbohydrate sulfotransferase 3 deficiency in recessive Larsen syndrome and humero-spinal dysostosis. Am J Hum Genet 82, 1368-1374.
23. Hiraoka, 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.
24. Hiraoka, S., Furuichi, T., Nishimura, G., 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.
25. Izumikawa, T., Koike, T., Shiozawa, S., Sugahara, K., Tamura, 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.
26. 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.
27. Kamiyama, S., Suda, T., Ueda, R., et al. (2003). Molecular cloning and identification of 3'-phosphoadenosine 5'-phosphosulfate transporter. J Biol Chem 278, 25958-25963.
28. Kang, H. G., Evers, M. R., Xia, G., Baenziger, J. U., and Schachner, M. (2002). Molecular cloning and characterization of chondroitin-4-O-sulfotransferase-3: a novel member of the HNK-1 family of sulfotransferases. J Biol Chem 277, 34766-34772.
29. 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.
30. Kitagawa, H., Tone, Y., Tamura, J., et al. (1998). Molecular cloning and expression of glucuronyltransferase I involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans. J Biol Chem 273, 6615-6618.
31. Kitagawa, H., Tsutsumi, K., Ikegami-Kuzuhara, A., et al. (2008). Sulfation of the galactose residues in the glycosaminoglycan-protein linkage region by recombinant human chondroitin 6-O-sulfotransferase-1. J Biol Chem 283, 27438-27443.
32. Kitagawa, H., Uyama, T., and Sugahara, K. (2001). Molecular cloning and expression of a human chondroitin synthase. J Biol Chem 276, 38721-38726.
33. 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.
34. 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.
35. Li, F., ten Dam, G. B., Murugan, S., et al. (2008). Involvement of highly sulfated chondroitin sulfate in the metastasis of the Lewis lung carcinoma cells. J Biol Chem 283, 34294-34304.
36. Li, Y., Laue, K., Temtamy, S., et al. (2010). Temtamy preaxial brachydactyly syndrome is caused by loss-of-function mutations in chondroitin synthase 1, a potential target of BMP signaling. Am J Hum Genet 87, 757-767.
37. Maccarana, M., Olander, B., Malmström, J., et al. (2006). Biosynthesis of dermatan sulfate: chondroitin-glucuronate C5-epimerase is identical to SART2. J Biol Chem 281, 11560-11568.
38. Malfait, F., Syx, D., Vlummens, P., et al. (2010). Musculocontractural Ehlers-Danlos Syndrome (former EDS type VIB) and adducted thumb clubfoot syndrome (ATCS) represent a single clinical entity caused by mutations in the dermatan-4-sulfotransferase 1 encoding CHST14 gene. Hum Mutat 31, 1233-1239.
39. Malmstrom, A. (1984). Biosynthesis of dermatan sulfate. II. Substrate specificity of the C-5 uronosyl epimerase. J Biol Chem 259, 161-165.
40. Malmstrom, A., and Fransson, L. A. (1975). Biosynthesis of dermatan sulfate. I. Formation of L-iduronic acid residues. J Biol Chem 250, 3419-3425.
41. Mao, J. R., and Bristow, J. (2001). The Ehlers-Danlos syndrome: on beyond collagens. J Clin Invest 107, 1063-1069.
42. Marcelino, J., Carpten, J. D., Suwairi, W. M., et al. (1999). CACP, encoding a secreted proteoglycan, is mutated in camptodactyly-arthropathy-coxa vara-pericarditis syndrome. Nat Genet 23, 319-322.
43. Mikami, T., Mizumoto, S., Kago, N., Kitagawa, H., and Sugahara, K. (2003). Specificities of three distinct human chondroitin/dermatan N-acetylgalactosamine 4-O-sulfotransferases demonstrated using partially desulfated dermatan sulfate as an acceptor: implication of differential roles in dermatan sulfate biosynthesis. J Biol Chem 278, 36115-36127.
44. Miyake, N., Kosho, T., Mizumoto, S., et al. (2010). Loss-of-function mutations of CHST14 in a new type of Ehlers-Danlos syndrome. Hum Mutat 31, 966-974.
45. Miyamoto, T., Inoue, H., Sakamoto, Y., et al. (2005). Identification of a novel splice site mutation of the CSPG2 gene in a Japanese family with Wagner syndrome. Invest Ophthalmol Vis Sci 46, 2726-2735.
46. Mizumoto, S., Uyama, T., Mikami, T., Kitagawa, H., and Sugahara, K. (2005). Biosynthetic pathways for differential expression of functional chondroitin sulfate and heparan sulfate. In Handbook of Carbohydrate Engineering, Kevin J. Yarema, ed. Boca Raton, FL: CRC Press, Taylor & Francis Group, pp. 289-324.
47. Moriarity, J. L., Hurt, K. J., Resnick, A. C., et al. (2002). UDP-glucuronate decarboxylase, a key enzyme in proteoglycan synthesis. J Biol Chem 277, 16968-16975.
48. Moses, J., Oldberg, Å., Cheng, F., and Fransson, L. Å. (1997). Biosynthesis of the proteoglycan decorin: transient 2-phosphorylation of xylose during formation of the trisaccharide linkage region. Eur J Biochem 248, 521-526.
49. Nadanaka, S., Clement, A., Masayama, K., Faissner, A., and Sugahara, K. (1998). Characteristic hexasaccharide sequences in octasaccharides derived from shark cartilage chondroitin sulfate D with neurite outgrowth promoting activity. J Biol Chem 273, 3296-3307.
50. 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 recombination activating gene-associated gene. J Biol Chem 276, 43894-43900.
51. Okajima, T., Fukumoto, S., Furukawa, K., Urano, T., and Furukawa, K. (1999a). Molecular basis for the progeroid variant of Ehlers-Danlos syndrome: identification and characterization of two mutations in galactosyltransferase I gene. J Biol Chem 274, 28841-28844.
52. Okajima, T., Yoshida, K., Kondo, T., and Furukawa, K. (1999b). 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.
53. Pacheco, B., Malmstrom, A., and Maccarana, M. (2009) Two dermatan sulfate epimerases form iduronic acid domains in dermatan sulfate. J Biol Chem 284, 9788-9795.
54. Pedersen, L. C., Dong, J., Taniguchi, F., et al. (2003). Crystal structure of an A1, 4-N-acetylhexosaminyltransferase (EXTL2), a member of the exostosin gene family involved in heparan sulfate biosynthesis. J Biol Chem 278, 14420-14428.
55. Pedersen, L. C., Tsuchida, K., Kitagawa, H., Sugahara, K., and Negishi, M. (2000). Heparan/ chondroitin sulfate biosynthesis: structure and mechanism of human glucuronyltransferase I. J Biol Chem 275, 34580-34585.
56. Perrimon, N., and Bernfield, M. (2000). Specificities of heparan sulphate proteoglycans in developmental processes. Nature 404, 725-728.
57. Pönighaus, C., Ambrosius, M., Casanova, J. C., et al. (2007). Human xylosyltransferase II is involved in the biosynthesis of the uniform tetrasaccharide linkage region in chondroitin sulfate and heparan sulfate proteoglycans. J Biol Chem 282, 5201-5206.
58. Quentin, E., Gladen, A., Roden, L., and Kresse, H. (1990). A genetic defect in the biosynthesis of dermatan sulfate proteoglycan: galactosyltransferase I deficiency in fibroblasts from a patient with a progeroid syndrome. Proc Natl Acad Sci U S A 87, 1342-1346.
59. Reed, C. C., and Iozzo, R. V. (2002). The role of decorin in collagen fibrillogenesis and skin homeostasis. Glycoconj J 19, 249-255.
60. Rossi, A., van der Harten, H. J., Beemer, F. A., et al. (1996). Phenotypic and genotypic overlap between atelosteogenesis type 2 and diastrophic dysplasia. Hum Genet 98, 657-661.
61. Saigoh, K., Izumikawa, T., Koike, T., Shimizu, J., Kitagawa, H., and Kusunoki, S. (2011). Chondroitin beta-1,4-N-acetylgalactosaminyltransferase-1 missense mutations are associated with neuropathies. J Hum Genet 56, 143-146.
62. Sato, T., Gotoh, M., Kiyohara, K., 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.
63. Schwartz, N. B., Lyle, S., Ozeran, J. D., et al. (1998). Sulfate activation and transport in mammals: system components and mechanisms. Chem Biol Interact 109, 143-151.
64. Seidler, D. G., Faiyaz-Ul-Haque, M., Hansen, U., et al. (2006). Defective glycosylation of decorin and biglycan, altered collagen structure, and abnormal phenotype of the skin fibroblasts of an Ehlers-Danlos syndrome patient carrying the novel Arg270Cys substitution in galactosyltransferase I (beta4GalT-7). J Mol Med 84, 583-594.
65. Seno, N., and Murakami, K. (1982). Structure of disulfated disaccharides from chondroitin polysulfates, chondroitin sulfate D and K. Carbohydr Res 103, 190-194.
66. Shi, J., Potash, J. B., Knowles, J. A., et al. (2011). Genome-wide association study of recurrent early-onset major depressive disorder. Mol Psychiatry 16, 193-201.
67. Sonoda, T., and Kouno, K. (2000). Two brothers with distal arthrogryposis, peculiar facial appearance, cleft palate, short stature, hydronephrosis, retentio testis, and normal intelligence: a new type of distal arthrogryposis? Am J Med Genet 91, 280-285.
68. Spicer, A. P., Kaback, L. A., Smith, T. J., and Seldin, M. F. (1998). Molecular cloning and characterization of the human and mouse UDP-glucose dehydrogenase genes. J Biol Chem 273, 25117-25124.
69. Stattin, E.-L., Wiklund, F., Lindblom, K., et al. (2010). A missense mutation in the aggrecan C-type lectin domain disrupts extracellular matrix interactions and causes dominant familial osteochondritis dissecans. Am J Hum Genet 86, 126-137.
70. 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.
71. Sugahara, K., and Mikami, T. (2007). Chondroitin/dermatan sulfate in the central nervous system. Curr Opin Struct Biol 17, 536-545.
72. 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.
73. Sugahara, K., and Schwartz, N. B. (1979). Defect in 3'-phosphoadenosine 5'-phosphosulfate formation in brachymorphic mice. Proc Natl Acad Sci U S A 76, 6615-6618.
74. Superti-Furga, A., Hastbacka, J., Wilcox, W. R., et al. (1996). Achondrogenesis type IB is caused by mutations in the diastrophic dysplasia sulphate transporter gene. Nat Genet 12, 100-102.
75. Tamura, H., Fukada, M., Fujikawa, A., and Noda, M. (2006). Protein tyrosine phosphatase receptor type Z is involved in hippocampus-dependent memory formation through dephosphorylation at Y1105 on p190 RhoGAP. Neurosci Lett 399, 33-38.
76. Thiele, H., Sakano, M., Kitagawa, H., et al. (2004). Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement. Proc Natl Acad Sci U S A 101, 10155-10160.
77. Tian, J., Ling, L., Shboul, M., et al. (2010). Loss of CHSY1, a secreted FRINGE enzyme, causes syndromic brachydactyly in humans via increased NOTCH signaling. Am J Hum Genet 87, 768-78.
78. Tompson, S. W., Merriman, B., Funari, V. A., et al. (2009). A recessive skeletal dysplasia, SEMD aggrecan type, results from a missense mutation affecting the C-type lectin domain of aggrecan. Am J Hum Genet 84, 72-79.
79. Tone, Y., Pedersen, L. C., Yamamoto, T., et al. (2008). 2-O-phosphorylation of xylose and 6-O-sulfation of galactose in the protein linkage region of glycosaminoglycans influence the glucuronyltransferase-I activity involved in the linkage region synthesis. J Biol Chem 283, 16801-16807.
80. Tuysuz, B., Mizumoto, S., Sugahara, K., Celebi, A., Mundlos, S., and Turkmen, S. (2009). Omani-type spondyloepiphyseal dysplasia with cardiac involvement caused by a missense mutation in CHST3. Clin Genet 75, 375-383.
81. ul Haque, M. F., King, L. M., Krakow, D., et al. (1998). Mutations in orthologous genes in human spondyloepimetaphyseal dysplasia and the brachymorphic mouse. Nat Genet 20, 157-162.
82. Unger, S., Lausch, E., Rossi, A., et al. (2010). Phenotypic features of carbohydrate sulfotransferase 3 (CHST3) deficiency in 24 patients: congenital dislocations and vertebral changes as principal diagnostic features. Am J Med Genet A 152A, 2543-2549.
83. Uyama, T., Ishida, M., Izumikawa, T., et al. (2006). Chondroitin 4-O-sulfotransferase-1 regulates E disaccharide expression of chondroitin sulfate required for herpes simplex virus infectivity. J Biol Chem 281, 38668-38674.
84. 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.
85. 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.
86. van Roij, M. H. H., Mizumoto, S., Yamada, S., et al. (2008). Spondyloepiphyseal dysplasia, Omani type: further definition of the phenotype. Am J Med Genet 146A, 2376-2384.
87. Vissers, L. E., Lausch, E., Unger, S., et al. (2011). Chondrodysplasia and abnormal joint development associated with mutations in IMPAD1, encoding the Golgi-resident nucleotide phosphatase, gPAPP. Am J Hum Genet 88, 608-615.
88. Wei, G., Bai, X., and Esko, J. D. (2004). Temperature-sensitive glycosaminoglycan biosynthesis in a Chinese hamster ovary cell mutant containing a point mutation in glucuronyltransferase I. J Biol Chem 279, 5693-5698.
89. Wiggins, C. A. R., and Munro, S. (1998). Activity of the yeast MNN1 a-1,3-mannosyltransferase requires a motif conserved in many other families of glycosyltransferases. Proc Natl Acad Sci U S A 95, 7945-7950.
90. Yada, T., Gotoh, M., Sato, T., et al. (2003a). 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.
91. Yada, T., Sato, T., Kaseyama, H., et al. (2003b). Chondroitin sulfate synthase-3: molecular cloning and characterization. J Biol Chem 278, 39711-39725.
92. Yamauchi, S., Mita, S., Matsubara, T., et al. (2000). Molecular cloning and expression of chondroitin 4-sulfotransferase. J Biol Chem 275, 8975-8981.
93. Zayed, H., Chao, R., Moshrefi, A., et al. (2010). A maternally inherited chromosome 18q22.1 deletion in a male with late-presenting diaphragmatic hernia and microphthalmiaevaluation of DSEL as a candidate gene for the diaphragmatic defect. Am J Med Genet A 152A, 916-923.