Biosynthesis and function of chondroitin sulfate

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 10, 2013, Pages 4719-4733

  Mikami, Tadahisa ^a   Kitagawa, Hiroshi ^a  

^a KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

Biosynthesis catabolism; Chondroitin sulfate; Glycosaminoglycan; Glycosyltransferase; Proteoglycan; Sulfotransferase

Indexed keywords

BETA1,3 GALACTOSYLTRANSFERASE II; BETA1,4 GALACTOSYLTRANSFERASE I; CARRIER PROTEIN; CHONDROITIN; CHONDROITIN 4 O SULFOTRANSFERASE 1; CHONDROITIN 4 O SULFOTRANSFERASE 2; CHONDROITIN 4 O SULFOTRANSFERASE 3; CHONDROITIN 6 O SULFOTRANSFERASE 1; CHONDROITIN ABC LYASE; CHONDROITIN N ACETYLGALACTOSAMINE TRANSFERASE 1; CHONDROITIN N ACETYLGALACTOSAMINE TRANSFERASE 2; CHONDROITIN SULFATE; CHONDROITIN SYNTHASE 1; DERMATAN 4 O SULFOTRANSFERASE 1; DERMATAN 4 O SULFOTRANSFERASE 3; GAG PROTEIN; GLUCURONIC ACID; N ACETYL BETA GLUCOSAMINIDASE; N ACETYLGALACTOSAMINE; N ACETYLGALACTOSAMINE 4 SULFATE 6 O SULFOTRANSFERASE; PHOSPHOTRANSFERASE; PROTEOCHONDROITIN SULFATE; SOLUTE CARRIER 35D1; SULFOTRANSFERASE; SYNTHETASE; TETRASACCHARIDE; TRANSFERASE; UNCLASSIFIED DRUG; UNINDEXED DRUG; URONYL 2 O SULFOTRANSFERASE; XYL KINASE;

ADDUCTED THUMB CLUBFOOT SYNDROME; ATHEROSCLEROSIS; BELL PALSY; BONE DEVELOPMENT; BONE DYSPLASIA; BRACHYDACTYLY; CARBOHYDRATE ANALYSIS; CARBOHYDRATE METABOLISM; CARBOHYDRATE SYNTHESIS; CATABOLISM; CELL DIFFERENTIATION; CELL DIVISION; CHGN 1 GENE; CHONDRODYSPLASIA; CHONDROITIN 6 O SULFOTRANSFERASE 1 DEFICIENCY; CONGENITAL BONE DISEASE; CONGENITAL JOINT DISLOCATION; DERMATAN 4 O SULFOTRANSFERASE 1 DEFICIENCY; DUCHENNE MUSCULAR DYSTROPHY; EHLERS DANLOS SYNDROME; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME REGULATION; EPIMERIZATION; EXTL2 GENE; FAM20B GENE; GENE; GENE INTERACTION; HEREDITARY MOTOR SENSORY NEUROPATHY; HUMAN; JOINT DISLOCATION; KYPHOSCOLIOSIS; LOSS OF FUNCTION MUTATION; LUNG METASTASIS; MALARIA; MISSENSE MUTATION; MUCOPOLYSACCHARIDOSIS; MUSCLE CELL; N ACETYLGALACTOSAMINE 4 SULFATE 6 O SULFOTRANSFERASE DEFICIENCY; NERVE CELL PLASTICITY; NERVE REGENERATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE PHOSPHORYLATION; PATHOPHYSIOLOGY; PERIPHERAL NEUROPATHY; PFC 1 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; RNA TRANSLATION; SIGNAL TRANSDUCTION; SPONDYLOEPIPHYSEAL DYSPLASIA; SQV 5 GENE; SULFATION; XYLT1 GENE;

Β1,3-GALACTOSYLTRANSFERASE-II; Β1,3-GLUCURONYLTRANSFERASE-I; Β1,4-GALACTOSYLTRANSFERASE-I; BIOSYNTHESIS/CATABOLISM; C4ST; C6ST; CHABC; CHGN; CHN; CHONDROITIN; CHONDROITIN 4-O-SULFOTRANSFERASE; CHONDROITIN 6-O-SULFOTRANSFERASE; CHONDROITIN GALNAC TRANSFERASE; CHONDROITIN POLYMERIZING FACTOR; CHONDROITIN SULFATE; CHONDROITIN SYNTHASE; CHONDROITINASE ABC; CHPF; CHSY; CS; D4ST; DERMATAN 4-O-SULFOTRANSFERASE; DERMATAN SULFATE; DS; DS-EPI; EXOSTOSIN; EXT; EXT-LIKE; EXTL; FAM; FAMILY WITH SEQUENCE SIMILARITY; GAG; GAL; GALACTOSE; GALNAC; GALNAC 4-SULFATE 6-O-SULFOTRANSFERASE; GALNAC TRANSFERASE; GALNAC4S-6ST; GALNACT; GALT-I; GALT-II; GLCA; GLCA C-5 EPIMERASE (DS EPIMERASE); GLCA TRANSFERASE-II; GLCAT-I; GLCAT-II; GLCNAC; GLCNAC TRANSFERASE; GLCNACT; GLUCURONIC ACID; GLYCOSAMINOGLYCAN; GLYCOSYLTRANSFERASE; HA; HEPARAN SULFATE; HERPES SIMPLEX VIRUS; HNK-1; HS; HSV; HUMAN NATURAL KILLER-1; HYAL; HYALURONAN; MAMMALIAN HYALURONIDASE; N-ACETYLGALACTOSAMINE; N-ACETYLGLUCOSAMINE; PG; PROTEOGLYCAN; SER; SERINE; SULFOTRANSFERASE; THROMBOMODULIN; TM; URONYL 2-O-SULFOTRANSFERASE; UST; XYL; XYLOSE; XYLOSYLTRANSFERASE; XYLT;

CHONDROITIN SULFATES; ENZYMES;

EID: 84879814568     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.06.006     Document Type: Review

References (188)

1. K. Sugahara, and H. Kitagawa Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans Curr. Opin. Struct. Biol. 10 2000 518 527
2. K. Sugahara, T. Mikami, T. Uyama, S. Mizuguchi, K. Nomura, and H. Kitagawa Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate Curr. Opin. Struct. Biol. 13 2003 612 620 (Pubitemid 37244117)
3. T. Uyama, H. Kitagawa, and K. Sugahara Biosynthesis of glycosaminoglycans and proteoglycans J.P. Kamerling, Comprehensive Glycoscience vol. 3 2007 Elsevier Amsterdam 79 104
4. J.E. Silbert, and G. Sugumaran Biosynthesis of chondroitin/dermatan sulfate IUBMB Life 54 2002 177 186 (Pubitemid 36008326)
5. C. Götting, J. Kuhn, R. Zahn, T. Brinkmann, and K. Kleesiek Molecular cloning and expression of human UDP-d-Xylose:proteoglycan core protein beta-d-xylosyltransferase and its first isoform XT-II J. Mol. Biol. 304 2000 517 528 (Pubitemid 32006187)
6. C. Götting, J. Kuhn, and K. Kleesiek Human xylosyltransferases in health and disease Cell. Mol. Life Sci. 64 2007 1498 1517 (Pubitemid 46954157)
7. T. Okajima, K. Yoshida, T. Kondo, and K. Furukawa 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 1999 22915 22918
8. R. Almeida, S.B. Levery, U. Mandel, H. Kresse, T. Schwientek, E.P. Bennett, and H. Clausen Cloning and expression of a proteoglycan UDP-galactose:beta-xylose beta1,4-galactosyltransferase I. A seventh member of the human beta4-galactosyltransferase gene family J. Biol. Chem. 274 1999 26165 26171
9. X. Bai, D. Zhou, J.R. Brown, B.E. Crawford, T. Hennet, and J.D. Esko Biosynthesis of the linkage region of glycosaminoglycans: cloning and activity of galactosyltransferase II, the sixth member of the beta 1,3- galactosyltransferase family (beta 3GalT6) J. Biol. Chem. 276 2001 48189 48195
10. H. Kitagawa, Y. Tone, J. Tamura, K.W. Neumann, T. Ogawa, S. Oka, T. Kawasaki, and K. Sugahara Molecular cloning and expression of glucuronyltransferase I involved in the biosynthesis of the glycosaminoglycan- protein linkage region of proteoglycans J. Biol. Chem. 273 1998 6615 6618 (Pubitemid 28160318)
11. G. Wei, X. Bai, A.K. Sarkar, and J.D. Esko Formation of HNK-1 determinants and the glycosaminoglycan tetrasaccharide linkage region by UDP-GlcUA:Galactose beta1, 3-glucuronosyltransferases J. Biol. Chem. 274 1999 7857 7864
12. X. Bai, G. Wei, A. Sinha, and J.D. Esko Chinese hamster ovary cell mutants defective in glycosaminoglycan assembly and glucuronosyltransferase I J. Biol. Chem. 274 1999 13017 13024
13. J.D. Esko, and S.B. Selleck Order out of chaos: assembly of ligand binding sites in heparan sulfate Annu. Rev. Biochem. 71 2002 435 471 (Pubitemid 34800227)
14. K. Cuellar, H. Chuong, S.M. Hubbell, and M.E. Hinsdale Biosynthesis of chondroitin and heparan sulfate in Chinese hamster ovary cells depends on xylosyltransferase II J. Biol. Chem. 282 2007 5195 5200 (Erratum in: J. Biol. Chem. 282 (2007) 18660) (Pubitemid 47093751)
15. C. Pönighaus, M. Ambrosius, J.C. Casanova, C. Prante, J. Kuhn, J.D. Esko, K. Kleesiek, and C. Götting 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 2007 5201 5206 (Pubitemid 47093752)
16. S. Mizumoto, S. Ikegawa, and K. Sugahara Human genetic disorders caused by mutations in the genes encoding biosynthetic enzymes for sulfated glycosaminoglycans J. Biol. Chem. 288 2013 10953 10961
17. M. Kusche-Gullberg, and L. Kjellén Sulfotransferases in glycosaminoglycan biosynthesis Curr. Opin. Struct. Biol. 13 2003 605 611 (Pubitemid 37244116)
18. A. Malmström, B. Bartolini, M.A. Thelin, B. Pacheco, and M. Maccarana Iduronic acid in chondroitin/dermatan sulfate: biosynthesis and biological function J. Histochem. Cytochem. 60 2012 916 925
19. M. Maccarana, B. Olander, J. Malmström, K. Tiedemann, R. Aebersold, U. Lindahl, J.P. Li, and A. Malmström Biosynthesis of dermatan sulfate: chondroitin-glucuronate C5-epimerase is identical to SART2 J. Biol. Chem. 281 2006 11560 11568 (Pubitemid 43855412)
20. B. Pacheco, A. Malmström, and M. Maccarana Two dermatan sulfate epimerases form iduronic acid domains in dermatan sulfate J. Biol. Chem. 284 2009 9788 9795
21. H. Kitagawa, T. Uyama, and K. Sugahara Molecular cloning and expression of a human chondroitin synthase J. Biol. Chem. 276 2001 38721 38726
22. M. Gotoh, T. Yada, T. Sato, T. Akashima, H. Iwasaki, H. Mochizuki, N. Inaba, A. Togayachi, T. Kudo, H. Watanabe, K. Kimata, and H. Narimatsu Molecular cloning and characterization of a novel chondroitin sulfate glucuronyltransferase that transfers glucuronic acid to N-acetylgalactosamine J. Biol. Chem. 277 2002 38179 38188 (Pubitemid 35154671)
23. H. Kitagawa, T. Izumikawa, T. Uyama, and K. Sugahara Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization J. Biol. Chem. 278 2003 23666 23671 (Pubitemid 36833253)
24. T. Yada, M. Gotoh, T. Sato, M. Shionyu, M. Go, H. Kaseyama, H. Iwasaki, N. Kikuchi, Y.D. Kwon, A. Togayachi, T. Kudo, H. Watanabe, H. Narimatsu, and K. Kimata 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 2003 30235 30247 (Pubitemid 36962418)
25. T. Yada, T. Sato, H. Kaseyama, M. Gotoh, H. Iwasaki, N. Kikuchi, Y.D. Kwon, A. Togayachi, T. Kudo, H. Watanabe, H. Narimatsu, and K. Kimata Chondroitin Sulfate Synthase-3. Molecular Cloning and Characterization J. Biol. Chem. 278 2003 39711 39725 (Pubitemid 37248533)
26. T. Izumikawa, T. Uyama, Y. Okuura, K. Sugahara, and H. Kitagawa 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 2007 545 552 (Pubitemid 46706983)
27. T. Izumikawa, T. Koike, S. Shiozawa, K. Sugahara, J. Tamura, and H. Kitagawa 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 2008 11396 11406
28. T. Uyama, H. Kitagawa, J. Tamura, and K. Sugahara 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 2002 8841 8846 (Pubitemid 34952951)
29. M. Gotoh, T. Sato, T. Akashima, H. Iwasaki, A. Kameyama, H. Mochizuki, T. Yada, N. Inaba, Y. Zhang, N. Kikuchi, Y.D. Kwon, A. Togayachi, T. Kudo, S. Nishihara, H. Watanabe, K. Kimata, and H. Narimatsu 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 2002 38189 38196 (Pubitemid 35154672)
30. T. Sato, M. Gotoh, K. Kiyohara, T. Akashima, H. Iwasaki, A. Kameyama, H. Mochizuki, T. Yada, N. Inaba, A. Togayachi, T. Kudo, M. Asada, H. Watanabe, T. Imamura, K. Kimata, and H. Narimatsu 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 2003 3063 3071 (Pubitemid 36801215)
31. T. Uyama, H. Kitagawa, J. Tanaka, J. Tamura, T. Ogawa, and K. Sugahara Molecular cloning and expression of a second chondroitin N- acetylgalactosaminyltransferase involved in the initiation and elongation of chondroitin/dermatan sulfate J. Biol. Chem. 278 2003 3072 3078 (Pubitemid 36801216)
32. S. Yamada, I. Van Die, D.H. Van den Eijnden, A. Yokota, H. Kitagawa, and K. Sugahara Demonstration of glycosaminoglycans in Caenorhabditis elegans FEBS Lett. 459 1999 327 331 (Pubitemid 29467362)
33. H. Toyoda, A. Kinoshita-Toyoda, and S.B. Selleck Structural analysis of glycosaminoglycans in Drosophila and Caenorhabditis elegans and demonstration that tout-velu, a Drosophila gene related to EXT tumor suppressors, affects heparan sulfate in vivo J. Biol. Chem. 275 2000 2269 2275 (Pubitemid 30081981)
34. H.Y. Hwang, S.K. Olson, J.D. Esko, and H.R. Horvitz Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis Nature 423 2003 439 443 (Pubitemid 36626995)
35. S. Mizuguchi, T. Uyama, H. Kitagawa, K.H. Nomura, K. Dejima, K. Gengyo-Ando, S. Mitani, K. Sugahara, and K. Nomura Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans Nature 423 2003 443 448 (Pubitemid 36626996)
36. T. Herman, E. Hartwieg, and H.R. Horvitz sqv mutants of Caenorhabditis elegans are defective in vulval epithelial invagination Proc. Natl. Acad. Sci. U. S. A. 96 1999 968 973 (Pubitemid 29072167)
37. T. Herman, and H.R. Horvitz Three proteins involved in Caenorhabditis elegans vulval invagination are similar to components of a glycosylation pathway Proc. Natl. Acad. Sci. U. S. A. 96 1999 974 979 (Pubitemid 29072168)
38. D.A. Bulik, G. Wei, H. Toyoda, A. Kinoshita-Toyoda, W.R. Waldrip, J.D. Esko, P.W. Robbins, and S.B. Selleck sqv-3, -7, and -8, a set of genes affecting morphogenesis in Caenorhabditis elegans, encode enzymes required for glycosaminoglycan biosynthesis Proc. Natl. Acad. Sci. U. S. A. 97 2000 10838 10843
39. P. Berninsone, H.Y. Hwang, I. Zemtseva, H.R. Horvitz, and C.B. Hirschberg SQV-7, a protein involved in Caenorhabditis elegans epithelial invagination and early embryogenesis, transports UDP-glucuronic acid, UDP-N-acetylgalactosamine, and UDP-galactose Proc. Natl. Acad. Sci. U. S. A. 98 2001 3738 3743 (Pubitemid 32249841)
40. H.Y. Hwang, and H.R. Horvitz The SQV-1 UDP-glucuronic acid decarboxylase and the SQV-7 nucleotide-sugar transporter may act in the Golgi apparatus to affect Caenorhabditis elegans vulval morphogenesis and embryonic development Proc. Natl. Acad. Sci. U. S. A. 99 2002 14218 14223 (Pubitemid 35257652)
41. H.Y. Hwang, and H.R. Horvitz The Caenorhabditis elegans vulval morphogenesis gene sqv-4 encodes a UDP-glucose dehydrogenase that is temporally and spatially regulated Proc. Natl. Acad. Sci. U. S. A. 99 2002 14224 14229 (Pubitemid 35257653)
42. H.Y. Hwang, S.K. Olson, J.R. Brown, J.D. Esko, and R. Horvitz The Caenorhabditis elegans genes sqv-2 and sqv-6, which are required for vulval morphogenesis, encode glycosaminoglycan galactosyltransferase II and xylosyltransferase J. Biol. Chem. 278 2003 11735 11738 (Pubitemid 36800140)
43. T. Izumikawa, H. Kitagawa, S. Mizuguchi, K.H. Nomura, K. Nomura, J. Tamura, K. Gengyo-Ando, S. Mitani, and K. Sugahara Nematode chondroitin polymerizing factor showing cell-/organ-specific expression is indispensable for chondroitin synthesis and embryonic cell division J. Biol. Chem. 279 2004 53755 53761 (Pubitemid 40051884)
44. T. Izumikawa, N. Kanagawa, Y. Watamoto, M. Okada, M. Saeki, M. Sakano, K. Sugahara, K. Sugihara, M. Asano, and H. Kitagawa Impairment of embryonic cell division and glycosaminoglycan biosynthesis in glucuronyltransferase-I-deficient mice J. Biol. Chem. 285 2010 12190 12196
45. D.G. Wilson, K. Phamluong, W.Y. Lin, K. Barck, R.A. Carano, L. Diehl, A.S. Peterson, F. Martin, and M.J. Solloway Chondroitin sulfate synthase 1 (Chsy1) is required for bone development and digit patterning Dev. Biol. 363 2012 413 425
46. H. Ogawa, S. Hatano, N. Sugiura, N. Nagai, T. Sato, K. Shimizu, K. Kimata, H. Narimatsu, and H. Watanabe Chondroitin sulfate synthase-2 is necessary for chain extension of chondroitin sulfate but not critical for skeletal development PLoS One 7 2012 e43806
47. Y. Watanabe, K. Takeuchi, S. Higa Onaga, M. Sato, M. Tsujita, M. Abe, R. Natsume, M. Li, T. Furuichi, M. Saeki, T. Izumikawa, A. Hasegawa, M. Yokoyama, S. Ikegawa, K. Sakimura, N. Amizuka, H. Kitagawa, and M. Igarashi Chondroitin sulfate N-acetylgalactosaminyltransferase-1 is required for normal cartilage development Biochem. J. 432 2010 47 55
48. T. Sato, T. Kudo, Y. Ikehara, H. Ogawa, T. Hirano, K. Kiyohara, K. Hagiwara, A. Togayachi, M. Ema, S. Takahashi, K. Kimata, H. Watanabe, and H. Narimatsu Chondroitin sulfate N-acetylgalactosaminyltransferase 1 is necessary for normal endochondral ossification and aggrecan metabolism J. Biol. Chem. 286 2011 5803 5812
49. K. Kurima, M.L. Warman, S. Krishnan, M. Domowicz, R.C. Krueger Jr., A. Deyrup, and N.B. Schwartz A member of a family of sulfate-activating enzymes causes murine brachymorphism Proc. Natl. Acad. Sci. U. S. A. 95 1998 8681 8685 (Erratum in: Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 12071)
50. A. Forlino, R. Piazza, C. Tiveron, S. Della Torre, L. Tatangelo, L. Bonafè, B. Gualeni, A. Romano, F. Pecora, A. Superti-Furga, G. Cetta, and A. Rossi A diastrophic dysplasia sulfate transporter (SLC26A2) mutant mouse: morphological and biochemical characterization of the resulting chondrodysplasia phenotype Hum. Mol. Genet. 14 2005 859 871 (Pubitemid 40403281)
51. B. Gualeni, M. Facchini, F. De Leonardis, R. Tenni, G. Cetta, M. Viola, A. Passi, A. Superti-Furga, A. Forlino, and A. Rossi Defective proteoglycan sulfation of the growth plate zones causes reduced chondrocyte proliferation via an altered Indian hedgehog signalling Matrix Biol. 29 2010 453 460
52. M. Klüppel, T.N. Wight, C. Chan, A. Hinek, and J.L. Wrana Maintenance of chondroitin sulfation balance by chondroitin-4-sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis Development 132 2005 3989 4003 (Pubitemid 41410261)
53. J. Tian, L. Ling, M. Shboul, H. Lee, B. O'Connor, B. Merriman, S.F. Nelson, S. Cool, O.H. Ababneh, A. Al-Hadidy, A. Masri, H. Hamamy, and B. Reversade Loss of CHSY1, a secreted FRINGE enzyme, causes syndromic brachydactyly in humans via increased NOTCH signaling Am. J. Hum. Genet. 87 2010 768 778
54. Y. Li, K. Laue, S. Temtamy, M. Aglan, L.D. Kotan, G. Yigit, H. Canan, B. Pawlik, G. Nürnberg, E.L. Wakeling, O.W. Quarrell, I. Baessmann, M.B. Lanktree, M. Yilmaz, R.A. Hegele, K. Amr, K.W. May, P. Nürnberg, A.K. Topaloglu, M. Hammerschmidt, and B. Wollnik 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 2010 757 767
55. K. Saigoh, T. Izumikawa, T. Koike, J. Shimizu, H. Kitagawa, and S. Kusunoki Chondroitin beta-1,4-N-acetylgalactosaminyltransferase-1 missense mutations are associated with neuropathies J. Hum. Genet. 56 2011 143 146
56. S. Yamauchi, S. Mita, T. Matsubara, M. Fukuta, H. Habuchi, K. Kimata, and O. Habuchi Molecular cloning and expression of chondroitin 4-sulfotransferase J. Biol. Chem. 275 2000 8975 8981 (Pubitemid 30180256)
57. N. Hiraoka, H. Nakagawa, E. Ong, T.O. Akama, M.N. Fukuda, and M. Fukuda 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 2000 20188 20196 (Pubitemid 30441630)
58. H.G. Kang, M.R. Evers, G. Xia, J.U. Baenziger, and M. Schachner Molecular cloning and characterization of chondroitin-4-O-sulfotransferase-3. A novel member of the HNK-1 family of sulfotransferases J. Biol. Chem. 277 2002 34766 34772
59. M.R. Evers, G. Xia, H.G. Kang, M. Schachner, and J.U. Baenziger Molecular cloning and characterization of a dermatan-specific N-acetylgalactosamine 4-O-sulfotransferase J. Biol. Chem. 276 2001 36344 36353
60. T. Mikami, S. Mizumoto, N. Kago, H. Kitagawa, and K. Sugahara 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 2003 36115 36127 (Pubitemid 37139933)
61. T. Uyama, M. Ishida, T. Izumikawa, E. Trybala, F. Tufaro, T. Bergström, K. Sugahara, and H. Kitagawa Chondroitin 4-O-sulfotransferase-1 regulates E disaccharide expression of chondroitin sulfate required for herpes simplex virus infectivity J. Biol. Chem. 281 2006 38668 38674 (Pubitemid 46041992)
62. S. Mizumoto, T. Mikami, D. Yasunaga, N. Kobayashi, H. Yamauchi, A. Miyake, N. Itoh, H. Kitagawa, and K. Sugahara Chondroitin 4-O-sulfotransferase-1 is required for somitic muscle development and motor axon guidance in zebrafish Biochem. J. 419 2009 387 399
63. T. Izumikawa, Y. Okuura, T. Koike, N. Sakoda, and H. Kitagawa Chondroitin 4-O-sulfotransferase-1 regulates the chain length of chondroitin sulfate in co-operation with chondroitin N-acetylgalactosaminyltransferase-2 Biochem. J. 434 2011 321 331
64. B. Pacheco, M. Maccarana, and A. Malmström Dermatan 4-O-sulfotransferase 1 is pivotal in the formation of iduronic acid blocks in dermatan sulfate Glycobiology 19 2009 1197 1203
65. M. Fukuta, Y. Kobayashi, K. Uchimura, K. Kimata, and O. Habuchi Molecular cloning and expression of human chondroitin 6-sulfotransferase Biochim. Biophys. Acta 1399 1998 57 61 (Pubitemid 28374916)
66. K. Uchimura, K. Kadomatsu, H. Nishimura, H. Muramatsu, E. Nakamura, N. Kurosawa, O. Habuchi, F.M. El-Fasakhany, Y. Yoshikai, and T. Muramatsu Functional analysis of the chondroitin 6-sulfotransferase gene in relation to lymphocyte subpopulations, brain development, and oversulfated chondroitin sulfates J. Biol. Chem. 277 2002 1443 1450 (Pubitemid 34968899)
67. T. Yamada, S. Ohtake, M. Sato, and O. Habuchi Chondroitin 4-sulphotransferase-1 and chondroitin 6-sulphotransferase-1 are affected differently by uronic acid residues neighbouring the acceptor GalNAc residues Biochem. J. 384 2004 567 575 (Pubitemid 40018970)
68. S. Nadanaka, M. Fujita, and K. Sugahara 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 alpha1-3GalNAc beta1-4iduronic acid in dermatan sulfate FEBS Lett. 452 1999 185 189 (Pubitemid 29301741)
69. M. Kobayashi, G. Sugumaran, J. Liu, N.W. Shworak, J.E. Silbert, and R.D. Rosenberg Molecular cloning and characterization of a human uronyl 2-sulfotransferase that sulfates iduronyl and glucuronyl residues in dermatan/chondroitin sulfate J. Biol. Chem. 274 1999 10474 10480
70. S. Ohtake, Y. Ito, M. Fukuta, and O. Habuchi Human N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase cDNA is related to human B cell recombination activating gene-associated gene J. Biol. Chem. 276 2001 43894 43900
71. H. Thiele, M. Sakano, H. Kitagawa, K. Sugahara, A. Rajab, W. Höhne, H. Ritter, G. Leschik, P. Nürnberg, and S. Mundlos 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 2004 10155 10160 (Pubitemid 38891211)
72. M.H. van Roij, S. Mizumoto, S. Yamada, T. Morgan, M.B. Tan-Sindhunata, H. Meijers-Heijboer, J.I. Verbeke, D. Markie, K. Sugahara, and S.P. Robertson Spondyloepiphyseal dysplasia, Omani type: further definition of the phenotype Am. J. Med. Genet. A 146A 2008 2376 2384
73. B. Tuysuz, S. Mizumoto, K. Sugahara, A. Celebi, S. Mundlos, and S. Turkmen Omani-type spondyloepiphyseal dysplasia with cardiac involvement caused by a missense mutation in CHST3 Clin. Genet. 75 2009 375 383
74. P. Hermanns, S. Unger, A. Rossi, A. Perez-Aytes, H. Cortina, L. Bonafé, L. Boccone, V. Setzu, M. Dutoit, L. Sangiorgi, F. Pecora, K. Reicherter, G. Nishimura, J. Spranger, B. Zabel, and A. Superti-Furga Congenital joint dislocations caused by carbohydrate sulfotransferase 3 deficiency in recessive Larsen syndrome and humero-spinal dysostosis Am. J. Hum. Genet. 82 2008 1368 1374 (Erratum in: Am. J. Hum. Genet. 83 (2008) 293)
75. S. Unger, E. Lausch, A. Rossi, A. Mégarbané, D. Sillence, M. Alcausin, A. Aytes, R. Mendoza-Londono, S. Nampoothiri, B. Afroze, B. Hall, I.F. Lo, S.T. Lam, J. Hoefele, I. Rost, E. Wakeling, E. Mangold, K. Godbole, N. Vatanavicharn, L.M. Franco, K. Chandler, S. Hollander, T. Velten, K. Reicherter, J. Spranger, S. Robertson, L. Bonafé, B. Zabel, and A. Superti-Furga 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 2010 2543 2549
76. M. Dündar, T. Müller, Q. Zhang, J. Pan, B. Steinmann, J. Vodopiutz, R. Gruber, T. Sonoda, B. Krabichler, G. Utermann, J.U. Baenziger, L. Zhang, and A.R. Janecke Loss of dermatan-4-sulfotransferase 1 function results in adducted thumb-clubfoot syndrome Am. J. Hum. Genet. 85 2009 873 882
77. N. Miyake, T. Kosho, S. Mizumoto, T. Furuichi, A. Hatamochi, Y. Nagashima, E. Arai, K. Takahashi, R. Kawamura, K. Wakui, J. Takahashi, H. Kato, H. Yasui, T. Ishida, H. Ohashi, G. Nishimura, M. Shiina, H. Saitsu, Y. Tsurusaki, H. Doi, Y. Fukushima, S. Ikegawa, S. Yamada, K. Sugahara, and N. Matsumoto Loss-of-function mutations of CHST14 in a new type of Ehlers-Danlos syndrome Hum. Mutat. 31 2010 966 974
78. F. Malfait, D. Syx, P. Vlummens, S. Symoens, S. Nampoothiri, T. Hermanns-Lê, L. Van Laer, and A. De Paepe 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 2010 1233 1239
79. K. Shimizu, N. Okamoto, N. Miyake, K. Taira, Y. Sato, K. Matsuda, N. Akimaru, H. Ohashi, K. Wakui, Y. Fukushima, N. Matsumoto, and T. Kosho Delineation of dermatan 4-O-sulfotransferase 1 deficient Ehlers-Danlos syndrome: observation of two additional patients and comprehensive review of 20 reported patients Am. J. Med. Genet. A 155A 2011 1949 1958
80. N.C. Voermans, M. Kempers, M. Lammens, N. van Alfen, M.C. Janssen, C. Bönnemann, B.G. van Engelen, and B.C. Hamel Myopathy in a 20-year-old female patient with D4ST-1 deficient Ehlers-Danlos syndrome due to a homozygous CHST14 mutation Am. J. Med. Genet. A 158A 2012 850 855
81. R. Mendoza-Londono, D. Chitayat, W.H. Kahr, A. Hinek, S. Blaser, L. Dupuis, E. Goh, R. Badilla-Porras, A. Howard, L. Mittaz, A. Superti-Furga, S. Unger, G. Nishimura, and L. Bonafe Extracellular matrix and platelet function in patients with musculocontractural Ehlers-Danlos syndrome caused by mutations in the CHST14 gene Am. J. Med. Genet. A 158A 2012 1344 1354
82. N. Akyüz, S. Rost, A. Mehanna, S. Bian, G. Loers, I. Oezen, B. Mishra, K. Hoffmann, D. Guseva, E. Laczynska, A. Irintchev, I. Jakovcevski, and M. Schachner Dermatan 4-O-sulfotransferase1 ablation accelerates peripheral nerve regeneration Exp. Neurol. 2013 10.1016/j.expneurol.2013.01.025 (in press)
83. M. Maccarana, S. Kalamajski, M. Kongsgaard, S.P. Magnusson, A. Oldberg, and A. Malmström Dermatan sulfate epimerase 1-deficient mice have reduced content and changed distribution of iduronic acids in dermatan sulfate and an altered collagen structure in skin Mol. Cell. Biol. 29 2009 5517 5528
84. C. Akatsu, S. Mizumoto, T. Kaneiwa, M. Maccarana, A. Malmström, S. Yamada, and K. Sugahara 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 2011 565 574
85. D. Goossens, S. Van Gestel, S. Claes, P. De Rijk, D. Souery, I. Massat, D. Van den Bossche, H. Backhovens, J. Mendlewicz, C. Van Broeckhoven, and J. Del-Favero A novel CpG-associated brain-expressed candidate gene for chromosome 18q-linked bipolar disorder Mol. Psychiatry 8 2003 83 89 (Pubitemid 36188576)
86. H. Zayed, R. Chao, A. Moshrefi, N. Lopezjimenez, A. Delaney, J. Chen, G.M. Shaw, and A.M. Slavotinek A maternally inherited chromosome 18q22.1 deletion in a male with late-presenting diaphragmatic hernia and microphthalmia-evaluation of DSEL as a candidate gene for the diaphragmatic defect Am. J. Med. Genet. A 152A 2010 916 923
87. J. Shi, J.B. Potash, J.A. Knowles, M.M. Weissman, W. Coryell, W.A. Scheftner, W.B. Lawson, J.R. DePaulo Jr., P.V. Gejman, A.R. Sanders, J.K. Johnson, P. Adams, S. Chaudhury, D. Jancic, O. Evgrafov, A. Zvinyatskovskiy, N. Ertman, M. Gladis, K. Neimanas, M. Goodell, N. Hale, N. Ney, R. Verma, D. Mirel, P. Holmans, and D.F. Levinson Genome-wide association study of recurrent early-onset major depressive disorder Mol. Psychiatry 16 2011 193 201
88. B. Bartolini, M.A. Thelin, U. Rauch, R. Feinstein, A. Oldberg, A. Malmström, and M. Maccarana Mouse development is not obviously affected by the absence of dermatan sulfate epimerase 2 in spite of a modified brain dermatan sulfate composition Glycobiology 22 2012 1007 1016
89. S. Ohtake-Niimi, S. Kondo, T. Ito, S. Kakehi, T. Ohta, H. Habuchi, K. Kimata, and O. Habuchi Mice deficient in N-acetylgalactosamine 4-sulfate 6-o-sulfotransferase are unable to synthesize chondroitin/dermatan sulfate containing N-acetylgalactosamine 4,6-bissulfate residues and exhibit decreased protease activity in bone marrow-derived mast cells J. Biol. Chem. 285 2010 20793 20805
90. S. Gruenheid, L. Gatzke, H. Meadows, and F. Tufaro Herpes simplex virus infection and propagation in a mouse L cell mutant lacking heparan sulfate proteoglycans J. Virol. 67 1993 93 100 (Pubitemid 23002968)
91. B.W. Banfield, Y. Leduc, L. Esford, K. Schubert, and F. Tufaro Sequential isolation of proteoglycan synthesis mutants by using herpes simplex virus as a selective agent: evidence for a proteoglycan-independent virus entry pathway J. Virol. 69 1995 3290 3298
92. S. Nadanaka, and H. Kitagawa Heparan sulphate biosynthesis and disease J. Biochem. 144 2008 7 14 (Pubitemid 351957475)
93. S. Hiraoka, T. Furuichi, G. Nishimura, S. Shibata, M. Yanagishita, D.L. Rimoin, A. Superti-Furga, P.G. Nikkels, M. Ogawa, K. Katsuyama, H. Toyoda, A. Kinoshita-Toyoda, N. Ishida, K. Isono, Y. Sanai, D.H. Cohn, H. Koseki, and S. Ikegawa Nucleotide-sugar transporter SLC35D1 is critical to chondroitin sulfate synthesis in cartilage and skeletal development in mouse and human Nat. Med. 13 2007 1363 1367 (Pubitemid 350080551)
94. P.J. Little, L. Tannock, K.L. Olin, A. Chait, and T.N. Wight Proteoglycans synthesized by arterial smooth muscle cells in the presence of transforming growth factor-beta1 exhibit increased binding to LDLs Arterioscler. Thromb. Vasc. Biol. 22 2002 55 60 (Pubitemid 34076232)
95. V.Y. Anggraeni, N. Emoto, K. Yagi, D.S. Mayasari, K. Nakayama, T. Izumikawa, H. Kitagawa, and K. Hirata Correlation of C4ST-1 and ChGn-2 expression with chondroitin sulfate chain elongation in atherosclerosis Biochem. Biophys. Res. Commun. 406 2011 36 41
96. E. Schönherr, H.T. Järveläinen, L.J. Sandell, and T.N. Wight Effects of platelet-derived growth factor and transforming growth factor-beta 1 on the synthesis of a large versican-like chondroitin sulfate proteoglycan by arterial smooth muscle cells J. Biol. Chem. 266 1991 17640 17647 (Pubitemid 21907985)
97. E. Schönherr, H.T. Järveläinen, M.G. Kinsella, L.J. Sandell, and T.N. Wight Platelet-derived growth factor and transforming growth factor-beta 1 differentially affect the synthesis of biglycan and decorin by monkey arterial smooth muscle cells Arterioscler. Thromb. 13 1993 1026 1036 (Pubitemid 23195805)
98. K. Sakai, K. Kimata, T. Sato, M. Gotoh, H. Narimatsu, K. Shinomiya, and H. Watanabe Chondroitin sulfate N-acetylgalactosaminyltransferase-1 plays a critical role in chondroitin sulfate synthesis in cartilage J. Biol. Chem. 282 2007 4152 4161 (Pubitemid 47084455)
99. T. Izumikawa, T. Koike, and H. Kitagawa Chondroitin 4-O-sulfotransferase- 2 regulates the number of chondroitin sulfate chains initiated by chondroitin N-acetylgalactosaminyltransferase-1 Biochem. J. 441 2012 697 705
100. N. Venkatesan, L. Barré, A. Benani, P. Netter, J. Magdalou, S. Fournel-Gigleux, and M. Ouzzine Stimulation of proteoglycan synthesis by glucuronosyltransferase-I gene delivery: a strategy to promote cartilage repair Proc. Natl. Acad. Sci. U. S. A. 101 2004 18087 18092 (Pubitemid 40054078)
101. S. Gulberti, V. Lattard, M. Fondeur, J.C. Jacquinet, G. Mulliert, P. Netter, J. Magdalou, M. Ouzzine, and S. Fournel-Gigleux Phosphorylation and sulfation of oligosaccharide substrates critically influence the activity of human beta1,4-galactosyltransferase 7 (GalT-I) and beta1,3- glucuronosyltransferase I (GlcAT-I) involved in the biosynthesis of the glycosaminoglycan-protein linkage region of proteoglycans J. Biol. Chem. 280 2005 1417 1425
102. Y. Tone, L.C. Pedersen, T. Yamamoto, T. Izumikawa, H. Kitagawa, J. Nishihara, J. Tamura, M. Negishi, and K. Sugahara 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 2008 16801 16807
103. H. Kitagawa, K. Tsutsumi, A. Ikegami-Kuzuhara, S. Nadanaka, F. Goto, T. Ogawa, and K. Sugahara Sulfation of the galactose residues in the glycosaminoglycan-protein linkage region by recombinant human chondroitin 6-O-sulfotransferase-1 J. Biol. Chem. 283 2008 27438 27443
104. T. Koike, T. Izumikawa, J. Tamura, and H. Kitagawa FAM20B is a kinase that phosphorylates xylose in the glycosaminoglycan-protein linkage region Biochem. J. 421 2009 157 162
105. T.R. Oegema Jr., E.L. Kraft, G.W. Jourdian, and T.R. Van Valen Phosphorylation of chondroitin sulfate in proteoglycans from the swarm rat chondrosarcoma J. Biol. Chem. 259 1984 1720 1726 (Pubitemid 14146558)
106. L.A. Fransson, I. Silverberg, and I. Carlstedt Structure of the heparan sulfate-protein linkage region. Demonstration of the sequence galactosyl-galactosyl-xylose-2-phosphate J. Biol. Chem. 260 1985 14722 14726
107. J. Moses, A. Oldberg, F. Cheng, and L.A. Fransson Biosynthesis of the proteoglycan decorin - transient 2-phosphorylation of xylose during formation of the trisaccharide linkage region Eur. J. Biochem. 248 1997 521 526 (Pubitemid 27387500)
108. J. Moses, A. Oldberg, and L.A. Fransson Initiation of galactosaminoglycan biosynthesis. Separate galactosylation and dephosphorylation pathways for phosphoxylosylated decorin protein and exogenous xyloside Eur. J. Biochem. 260 1999 879 884 (Pubitemid 29148656)
109. B.F. Eames, M.E. Swartz, and C.B. Kimmel Fam20b and xylosyltransferase1 (Xylt1) drive cartilage matrix production and inhibit perichondral bone during endochondral ossification Dev. Biol. 319 2008 480
110. B.F. Eames, Y.L. Yan, M.E. Swartz, D.S. Levic, E.W. Knapik, J.H. Postlethwait, and C.B. Kimmel Mutation in fam20b and xylt1 reveal that cartilage matrix controls timing of endochondral ossification by inhibiting chondrocyte maturation PLoS Genet. 7 2011 e1002246
111. D. Nalbant, H. Youn, S.I. Nalbant, S. Sharma, E. Cobos, E.G. Beale, Y. Du, and S.C. Williams FAM20: an evolutionarily conserved family of secreted proteins expressed in hematopoietic cells BMC Genomics 6 2005 11
112. J. O'Sullivan, C.C. Bitu, S.B. Daly, J.E. Urquhart, M.J. Barron, S.S. Bhaskar, H. Martelli-Júnior, P.E. dos Santos Neto, M.A. Mansilla, J.C. Murray, R.D. Coletta, G.C. Black, and M.J. Dixon Whole-Exome sequencing identifies FAM20A mutations as a cause of amelogenesis imperfecta and gingival hyperplasia syndrome Am. J. Hum. Genet. 88 2011 616 620
113. S.H. Cho, F. Seymen, K.E. Lee, S.K. Lee, Y.S. Kweon, K.J. Kim, S.E. Jung, S.J. Song, M. Yildirim, M. Bayram, E.B. Tuna, K. Gencay, and J.W. Kim Novel FAM20A mutations in hypoplastic amelogenesis imperfecta Hum. Mutat. 33 2012 91 94
114. G. Jaureguiberry, M. De la Dure-Molla, D. Parry, M. Quentric, N. Himmerkus, T. Koike, J. Poulter, E. Klootwijk, S.L. Robinette, A.J. Howie, V. Patel, M.L. Figueres, H.C. Stanescu, N. Issler, J.K. Nicholson, D. Bockenhauer, C. Laing, S.B. Walsh, D.A. McCredie, S. Povey, A. Asselin, A. Picard, A. Coulomb, A.J. Medlar, I. Bailleul-Forestier, A. Verloes, C. Le Caignec, G. Roussey, J. Guiol, B. Isidor, C. Logan, R. Shore, C. Johnson, C. Inglehearn, S. Al-Bahlani, M. Schmittbuhl, F. Clauss, M. Huckert, V. Laugel, E. Ginglinger, S. Pajarola, G. Spartà, D. Bartholdi, A. Rauch, M.C. Addor, P.M. Yamaguti, H.P. Safatle, A.C. Acevedo, H. Martelli-Júnior, P.E. Dos Santos Netos, R.D. Coletta, S. Gruessel, C. Sandmann, D. Ruehmann, C.B. Langman, S.J. Scheinman, D. Ozdemir-Ozenen, T.C. Hart, P.S. Hart, U. Neugebauer, E. Schlatter, P. Houillier, W.A. Gahl, M. Vikkula, A. Bloch-Zupan, M. Bleich, H. Kitagawa, R.J. Unwin, A. Mighell, A. Berdal, and R. Kleta Nephrocalcinosis (enamel renal syndrome) caused by autosomal recessive FAM20A mutations Nephron Physiol. 122 2012 1 6
115. M.A. Simpson, R. Hsu, L.S. Keir, J. Hao, G. Sivapalan, L.M. Ernst, E.H. Zackai, L.I. Al-Gazali, G. Hulskamp, H.M. Kingston, T.E. Prescott, A. Ion, M.A. Patton, V. Murday, A. George, and A.H. Crosby Mutations in FAM20C are associated with lethal osteosclerotic bone dysplasia (Raine syndrome), highlighting a crucial molecule in bone development Am. J. Hum. Genet. 81 2007 906 912 (Pubitemid 47580245)
116. M.A. Simpson, A. Scheuerle, J. Hurst, M.A. Patton, H. Stewart, and A.H. Crosby Mutations in FAM20C also identified in non-lethal osteosclerotic bone dysplasia Clin. Genet. 75 2009 271 276
117. S. Gulberti, J.C. Jacquinet, M. Chabel, N. Ramalanjaona, J. Magdalou, P. Netter, M.W. Coughtrie, M. Ouzzine, and S. Fournel-Gigleux Chondroitin sulfate N-acetylgalactosaminyltransferase-1 (CSGalNAcT-1) involved in chondroitin sulfate initiation: impact of sulfation on activity and specificity Glycobiology 22 2012 561 571
118. H. Kitagawa, H. Shimakawa, and K. Sugahara The tumor suppressor EXT-like gene EXTL2 encodes an alpha1, 4-N-acetylhexosaminyltransferase that transfers N-acetylgalactosamine and N-acetylglucosamine to the common glycosaminoglycan- protein linkage region. The key enzyme for the chain initiation of heparan sulfate J. Biol. Chem. 274 1999 13933 13937
119. H. Kitagawa, Y. Kano, H. Shimakawa, F. Goto, T. Ogawa, H. Okabe, and K. Sugahara Identification and characterization of a novel UDP-GalNAc:GlcAbeta-R alpha1,4-N-acetylgalactosaminyltransferase from a human sarcoma cell line Glycobiology 9 1999 697 703 (Pubitemid 29329013)
120. S. Nadanaka, S. Zhou, S. Kagiyama, N. Shoji, K. Sugahara, K. Sugihara, M. Asano, and H. Kitagawa EXTL2, a member of EXT family of tumor suppressors, controls glycosaminoglycan biosynthesis in a xylose kinase-dependent manner J. Biol. Chem. 288 2013 9321 9333
121. L.Å. Fransson Structure and function of cell-associated proteoglycans Trends Biochem. Sci. 12 1987 406 411
122. S. Nadanaka, H. Kitagawa, and K. Sugahara Demonstration of the immature glycosaminoglycan tetrasaccharide sequence GlcAβ1-3Galβ1-3Galβ1- 4Xyl on recombinant soluble human α-thrombomodulin. A possible mechanism generating 'part-time' proteoglycan J. Biol. Chem. 273 1998 33728 33734
123. 4- 3GlcAβ1-3Galβ1-3(+/- Siaα2-6)Galβ1-4Xyl J. Biol. Chem. 274 1999 5436 5442 (Pubitemid 29109189)
124. T. Hashiguchi, S. Mizumoto, Y. Nishimura, J. Tamura, S. Yamada, and K. Sugahara Involvement of human natural killer-1 (HNK-1) sulfotransferase in the biosynthesis of the GlcUA(3-O-sulfate)-Gal-Gal-Xyl tetrasaccharide found in α-thrombomodulin from human urine J. Biol. Chem. 286 2011 33003 33011
125. N. Nakagawa, T. Izumikawa, H. Kitagawa, and S. Oka Sulfation of glucuronic acid in the linkage tetrasaccharide by HNK-1 sulfotransferase is an inhibitory signal for the expression of a chondroitin sulfate chain on thrombomodulin Biochem. Biophys. Res. Commun. 415 2011 109 113
126. R.J. Midura, A. Calabro, M. Yanagishita, and V.C. Hascall Nonreducing end structures of chondroitin sulfate chains on aggrecan isolated from Swarm rat chondrosarcoma cultures J. Biol. Chem. 270 1995 8009 8015
127. A.H. Plaas, S. Wong-Palms, P.J. Roughley, R.J. Midura, and V.C. Hascall Chemical and immunological assay of the nonreducing terminal residues of chondroitin sulfate from human aggrecan J. Biol. Chem. 272 1997 20603 20610 (Pubitemid 27355619)
128. S. Ohtake, S. Kondo, T. Morisaki, K. Matsumura, K. Kimata, and O. Habuchi Expression of sulfotransferases involved in the biosynthesis of chondroitin sulfate E in the bone marrow derived mast cells Biochim. Biophys. Acta 1780 2008 687 695
129. S. Ohtake, K. Kimata, and O. Habuchi A unique nonreducing terminal modification of chondroitin sulfate by N-acetylgalactosamine 4-sulfate 6-o-sulfotransferase J. Biol. Chem. 278 2003 38443 38452 (Pubitemid 37221738)
130. V. Prabhakar, and R. Sasisekharan The biosynthesis and catabolism of galactosaminoglycans Adv. Pharmacol. 53 2006 69 115
131. R. Lawrence, J.R. Brown, K. Al-Mafraji, W.C. Lamanna, J.R. Beitel, G.J. Boons, J.D. Esko, and B.E. Crawford Disease-specific non-reducing end carbohydrate biomarkers for mucopolysaccharidoses Nat. Chem. Biol. 8 2012 197 204
132. A.B. Csoka, G.I. Frost, and R. Stern The six hyaluronidase-like genes in the human and mouse genomes Matrix Biol. 20 2001 499 508 (Pubitemid 33109098)
133. R. Stern, and M.J. Jedrzejas Hyaluronidases: their genomics, structures, and mechanisms of action Chem. Rev. 106 2006 818 839
134. T. Kaneiwa, S. Yamada, S. Mizumoto, A.M. Montaño, S. Mitani, and K. Sugahara Identification of a novel chondroitin hydrolase in Caenorhabditis elegans J. Biol. Chem. 283 2008 14971 14979
135. T. Kaneiwa, S. Mizumoto, K. Sugahara, and S. Yamada Identification of human hyaluronidase-4 as a novel chondroitin sulfate hydrolase that preferentially cleaves the galactosaminidic linkage in the trisulfated tetrasaccharide sequence Glycobiology 20 2010 300 309
136. T. Kaneiwa, A. Miyazaki, R. Kogawa, S. Mizumoto, K. Sugahara, and S. Yamada Identification of amino acid residues required for the substrate specificity of human and mouse chondroitin sulfate hydrolase (conventional hyaluronidase-4) J. Biol. Chem. 287 2012 42119 42128
137. A.B. Csóka, S.W. Scherer, and R. Stern Expression analysis of six paralogous human hyaluronidase genes clustered on chromosomes 3p21 and 7q31 Genomics 60 1999 356 361 (Pubitemid 29471502)
138. L. Gushulak, R. Hemming, D. Martin, V. Seyrantepe, A. Pshezhetsky, and B. Triggs-Raine Hyaluronidase 1 and β-hexosaminidase have redundant functions in hyaluronan and chondroitin sulfate degradation J. Biol. Chem. 287 2012 16689 16697
139. T. Mikami, S. Koyama, Y. Yabuta, and H. Kitagawa Chondroitin sulfate is a crucial determinant for skeletal muscle development/regeneration and improvement of muscular dystrophies J. Biol. Chem. 287 2012 38531 38542
140. T. Honda, T. Kaneiwa, S. Mizumoto, K. Sugahara, and S. Yamada Hyaluronidases have strong hydrolytic activity toward chondroitin 4-sulfate comparable to that for hyaluronan Biomolecules 2 2012 549 563
141. R. Raman, V. Sasisekharan, and R. Sasisekharan Structural insights into biological roles of protein-glycosaminoglycan interactions Chem. Biol. 12 2005 267 277 (Pubitemid 40406273)
142. J.R. Bishop, M. Schuksz, and J.D. Esko Heparan sulphate proteoglycans fine-tune mammalian physiology Nature 446 2007 1030 1037 (Pubitemid 46676065)
143. A. Purushothaman, K. Sugahara, and A. Faissner Chondroitin sulfate "wobble motifs" modulate maintenance and differentiation of neural stem cells and their progeny J. Biol. Chem. 287 2012 2935 2942
144. D.C. Gowda Role of chondroitin-4-sulfate in pregnancy-associated malaria. Role of chondroitin-4-sulfate in pregnancy-associated malaria Adv. Pharmacol. 53 2006 375 400
145. K. Bergefall, E. Trybala, M. Johansson, T. Uyama, S. Naito, S. Yamada, H. Kitagawa, K. Sugahara, and T. Bergström Chondroitin sulfate characterized by the E-disaccharide unit is a potent inhibitor of herpes simplex virus infectivity and provides the virus binding sites on gro2C cells J. Biol. Chem. 280 2005 32193 32199 (Pubitemid 41361826)
146. K. Sugahara, and T. Mikami Chondroitin/dermatan sulfate in the central nervous system Curr. Opin. Struct. Biol. 17 2007 536 545 (Pubitemid 350019013)
147. C.I. Gama, S.E. Tully, N. Sotogaku, P.M. Clark, M. Rawat, N. Vaidehi, W.A. Goddard III, A. Nishi, and L.C. Hsieh-Wilson Sulfation patterns of glycosaminoglycans encode molecular recognition and activity Nat. Chem. Biol. 2 2006 467 473 (Pubitemid 44266308)
148. M. Ida, T. Shuo, K. Hirano, Y. Tokita, K. Nakanishi, F. Matsui, S. Aono, H. Fujita, Y. Fujiwara, T. Kaji, and A. Oohira Identification and functions of chondroitin sulfate in the milieu of neural stem cells J. Biol. Chem. 281 2006 5982 5991 (Pubitemid 43847699)
149. K. Akita, A. von Holst, Y. Furukawa, T. Mikami, K. Sugahara, and A. Faissner Expression of multiple chondroitin/dermatan sulfotransferases in the neurogenic regions of the embryonic and adult central nervous system implies that complex chondroitin sulfates have a role in neural stem cell maintenance Stem Cells 26 2008 798 809
150. S. Nadanaka, M. Ishida, M. Ikegami, and H. Kitagawa Chondroitin 4-O-sulfotransferase-1 modulates Wnt-3a signaling through control of E disaccharide expression of chondroitin sulfate J. Biol. Chem. 283 2008 27333 27343
151. S. Nadanaka, H. Kinouchi, K. Taniguchi-Morita, J. Tamura, and H. Kitagawa Down-regulation of chondroitin 4-O-sulfotransferase-1 by Wnt signaling triggers diffusion of Wnt-3a J. Biol. Chem. 286 2011 4199 4208
152. H.H. Schmidt, V.G. Dyomin, N. Palanisamy, T. Itoyama, G. Nanjangud, H. Pirc-Danoewinata, O.A. Haas, and R.S. Chaganti Deregulation of the carbohydrate (chondroitin 4) sulfotransferase 11 (CHST11) gene in a B-cell chronic lymphocytic leukemia with a t(12;14)(q23;q32) Oncogene 23 2004 6991 6996 (Pubitemid 39280000)
153. D. Kalathas, D.A. Theocharis, D. Bounias, D. Kyriakopoulou, N. Papageorgakopoulou, M.S. Stavropoulos, and D.H. Vynios Alterations of glycosaminoglycan disaccharide content and composition in colorectal cancer: structural and expressional studies Oncol. Rep. 22 2009 369 375
154. M. Klüppel, P. Samavarchi-Tehrani, K. Liu, J.L. Wrana, and A. Hinek C4ST-1/CHST11-controlled chondroitin sulfation interferes with oncogenic HRAS signaling in Costello syndrome Eur. J. Hum. Genet. 20 2012 870 877
155. C.M. Willis, and M. Klüppel Inhibition by chondroitin sulfate E can specify functional Wnt/β-catenin signaling thresholds in NIH3T3 fibroblasts J. Biol. Chem. 287 2012 37042 37056
156. C.M. Galtrey, and J.W. Fawcett The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system Brain Res. Rev. 54 2007 1 18 (Pubitemid 46498163)
157. E.J. Bradbury, L.D. Moon, R.J. Popat, V.R. King, G.S. Bennett, P.N. Patel, J.W. Fawcett, and S.B. McMahon Chondroitinase ABC promotes functional recovery after spinal cord injury Nature 416 2002 636 640 (Pubitemid 34406764)
158. J. Silver, and J.H. Miller Regeneration beyond the glial scar Nat. Rev. Neurosci. 5 2004 146 156 (Pubitemid 38160289)
159. J.M. Brown, J. Xia, B. Zhuang, K.S. Cho, C.J. Rogers, C.I. Gama, M. Rawat, S.E. Tully, N. Uetani, D.E. Mason, M.L. Tremblay, E.C. Peters, O. Habuchi, D.F. Chen, and L.C. Hsieh-Wilson A sulfated carbohydrate epitope inhibits axon regeneration after injury Proc. Natl. Acad. Sci. U. S. A. 109 2012 4768 4773
160. H. Wang, Y. Katagiri, T.E. McCann, E. Unsworth, P. Goldsmith, Z.X. Yu, F. Tan, L. Santiago, E.M. Mills, Y. Wang, A.J. Symes, and H.M. Geller Chondroitin-4-sulfation negatively regulates axonal guidance and growth J. Cell Sci. 121 2008 3083 3091
161. R. Lin, T.W. Rosahl, P.J. Whiting, J.W. Fawcett, and J.C. Kwok 6-Sulphated chondroitins have a positive influence on axonal regeneration PLoS One 6 2011 e21499
162. F. Properzi, D. Carulli, R.A. Asher, E. Muir, L.M. Camargo, T.H. van Kuppevelt, G.B. ten Dam, Y. Furukawa, T. Mikami, K. Sugahara, T. Toida, H.M. Geller, and J.W. Fawcett Chondroitin 6-sulphate synthesis is up-regulated in injured CNS, induced by injury-related cytokines and enhanced in axon-growth inhibitory glia Eur. J. Neurosci. 21 2005 378 390 (Pubitemid 40204241)
163. J. Liu, C.H. Chau, H. Liu, B.R. Jang, X. Li, Y.S. Chan, and D.K. Shum Upregulation of chondroitin 6-sulphotransferase-1 facilitates Schwann cell migration during axonal growth J. Cell Sci. 119 2006 933 942
164. D. Carulli, T. Laabs, H.M. Geller, and J.W. Fawcett Chondroitin sulfate proteoglycans in neural development and regeneration Curr. Opin. Neurobiol. 15 2005 116 120 (Erratum in; Curr. Opin. Neurobiol. 15, 2005, 252) (Pubitemid 40249970)
165. T. Mikami, D. Yasunaga, and H. Kitagawa Contactin-1 is a functional receptor for neuroregulatory chondroitin sulfate-E J. Biol. Chem. 284 2009 4494 4499
166. Y. Shen, A.P. Tenney, S.A. Busch, K.P. Horn, F.X. Cuascut, K. Liu, Z. He, J. Silver, and J.G. Flanagan PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration Science 326 2009 592 596
167. A.R. Aricescu, I.W. McKinnell, W. Halfter, and A.W. Stoker Heparan sulfate proteoglycans are ligands for receptor protein tyrosine phosphatase sigma Mol. Cell. Biol. 22 2002 1881 1892 (Pubitemid 34175003)
168. A.N. Fox, and K. Zinn The heparan sulfate proteoglycan syndecan is an in vivo ligand for the Drosophila LAR receptor tyrosine phosphatase Curr. Biol. 15 2005 1701 1711 (Pubitemid 41415626)
169. K.G. Johnson, A.P. Tenney, A. Ghose, A.M. Duckworth, M.E. Higashi, K. Parfitt, O. Marcu, T.R. Heslip, J.L. Marsh, T.L. Schwarz, J.G. Flanagan, and D. Van Vactor The HSPGs Syndecan and Dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development Neuron 49 2006 517 531 (Pubitemid 43221888)
170. C.H. Coles, Y. Shen, A.P. Tenney, C. Siebold, G.C. Sutton, W. Lu, J.T. Gallagher, E.Y. Jones, J.G. Flanagan, and A.R. Aricescu Proteoglycan-specific molecular switch for RPTPσ clustering and neuronal extension Science 332 2011 484 488
171. D. Fisher, B. Xing, J. Dill, H. Li, H.H. Hoang, Z. Zhao, X.L. Yang, R. Bachoo, S. Cannon, F.M. Longo, M. Sheng, J. Silver, and S. Li Leukocyte common antigen-related phosphatase is a functional receptor for chondroitin sulfate proteoglycan axon growth inhibitors J. Neurosci. 31 2011 14051 14066
172. T.L. Dickendesher, K.T. Baldwin, Y.A. Mironova, Y. Koriyama, S.J. Raiker, K.L. Askew, A. Wood, C.G. Geoffroy, B. Zheng, C.D. Liepmann, Y. Katagiri, L.I. Benowitz, H.M. Geller, and R.J. Giger NgR1 and NgR3 are receptors for chondroitin sulfate proteoglycans Nat. Neurosci. 15 2012 703 712
173. S.L. Cheng, C.S. Shin, D.A. Towler, and R. Civitelli A dominant negative cadherin inhibits osteoblast differentiation J. Bone Miner. Res. 15 2000 2362 2370
174. I. Kii, N. Amizuka, J. Shimomura, Y. Saga, and A. Kudo Cell-cell interaction mediated by cadherin-11 directly regulates the differentiation of mesenchymal cells into the cells of the osteo-lineage and the chondro-lineage J. Bone Miner. Res. 19 2004 1840 1849 (Pubitemid 41103436)
175. T. Koike, T. Izumikawa, J. Tamura, and H. Kitagawa Chondroitin sulfate-E fine-tunes osteoblast differentiation via ERK1/2, Smad3 and Smad1/5/8 signaling by binding to N-cadherin and cadherin-11 Biochem. Biophys. Res. Commun. 420 2012 523 529
176. T. Miyazaki, S. Miyauchi, A. Tawada, T. Anada, S. Matsuzaka, and O. Suzuki Oversulfated chondroitin sulfate-E binds to BMP-4 and enhances osteoblast differentiation J. Cell. Physiol. 217 2008 769 777
177. F. Li, G.B. Ten Dam, S. Murugan, S. Yamada, T. Hashiguchi, S. Mizumoto, K. Oguri, M. Okayama, T.H. van Kuppevelt, and K. Sugahara Involvement of highly sulfated chondroitin sulfate in the metastasis of the Lewis lung carcinoma cells J. Biol. Chem. 283 2008 34294 34304
178. S. Mizumoto, M. Watanabe, and K. Sugahara Expression of N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase involved in chodroitin sulfate synthesis is responsible for pulmonary metastasis BioMed Res. Int. 2013 2013 656319
179. S. Mizumoto, J. Takahashi, and K. Sugahara Receptor for advanced glycation end products (RAGE) functions as receptor for specific sulfated glycosaminoglycans, and anti-RAGE antibody or sulfated glycosaminoglycans delivered in vivo inhibit pulmonary metastasis of tumor cells J. Biol. Chem. 287 2012 18985 18994
180. T. Pizzorusso, P. Medini, N. Berardi, S. Chierzi, J.W. Fawcett, and L. Maffei Reactivation of ocular dominance plasticity in the adult visual cortex Science 298 2002 1248 1251 (Pubitemid 35285495)
181. N. Gogolla, P. Caroni, A. Lüthi, and C. Herry Perineuronal nets protect fear memories from erasure Science 325 2009 1258 1261
182. H. Kitagawa, K. Tsutsumi, Y. Tone, and K. Sugahara Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain J. Biol. Chem. 272 1997 31377 31381 (Pubitemid 28013273)
183. C. Mitsunaga, T. Mikami, S. Mizumoto, J. Fukuda, and K. Sugahara Chondroitin sulfate/dermatan sulfate hybrid chains in the development of cerebellum. Spatiotemporal regulation of the expression of critical disulfated disaccharides by specific sulfotransferases J. Biol. Chem. 281 2006 18942 18952 (Pubitemid 44035397)
184. S. Miyata, Y. Komatsu, Y. Yoshimura, C. Taya, and H. Kitagawa Persistent cortical plasticity by upregulation of chondroitin 6-sulfation Nat. Neurosci. 15 2012 414 422
185. S. Sugiyama, A.A. Di Nardo, S. Aizawa, I. Matsuo, M. Volovitch, A. Prochiantz, and T.K. Hensch Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity Cell 134 2008 508 520
186. M. Beurdeley, J. Spatazza, H.H. Lee, S. Sugiyama, C. Bernard, A.A. Di Nardo, T.K. Hensch, and A. Prochiantz Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex J. Neurosci. 32 2012 9429 9437
187. K. Rochlin, S. Yu, S. Roy, and M.K. Baylies Myoblast fusion: when it takes more to make one Dev. Biol. 341 2010 66 83
188. G.K. Pavlath Spatial and functional restriction of regulatory molecules during mammalian myoblast fusion Exp. Cell Res. 316 2010 3067 3072