Using sugar remodeling to study chondroitin sulfate function

Biological and Pharmaceutical Bulletin

Volumn 37, Issue 11, 2014, Pages 1705-1712

  Kitagawa, Hiroshi ^a  

^a KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

Chondroitin sulfate; Glycobiology; Glycosyltransferase; Proteoglycan; Sulfotransferase

Indexed keywords

ALPHA 1,3 GALACTOSYLTRANSFERASE; BETA 1,3 GALACTOSYLTRANSFERASE; CHONDROITIN SULFATE; CORE PROTEIN; GAG PROTEIN; GALACTOSE; GALACTOSYLTRANSFERASE; GLYCOSAMINOGLYCAN; GLYCOSYLTRANSFERASE; POLYSACCHARIDE; PROTEOGLYCAN; SERINE; SUGAR; TETRASACCHARIDE; UNCLASSIFIED DRUG; XYLOSE; PROTEOCHONDROITIN SULFATE; SULFOTRANSFERASE;

ANIMAL EXPERIMENT; BONE DEVELOPMENT; CAENORHABDITIS ELEGANS; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME SYNTHESIS; EXTRACELLULAR MATRIX; GENE MUTATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MORPHOGENESIS; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PROTEIN STRUCTURE; REVIEW; SPONDYLOEPIPHYSEAL DYSPLASIA; SULFATION; ANIMAL; CHEMISTRY; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; CHONDROITIN SULFATE PROTEOGLYCANS; CHONDROITIN SULFATES; GLYCOSYLTRANSFERASES; HUMANS; SIGNAL TRANSDUCTION; SULFOTRANSFERASES;

EID: 84910048673     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.b14-00613     Document Type: Review

References (65)

1. Sugahara K, Kitagawa H. Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans. Curr. Opin. Struct. Biol., 10, 518-527 (2000).
2. Sugahara K, Mikami T, Uyama T, Mizuguchi S, Nomura K, Kitagawa H. Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate. Curr. Opin. Struct. Biol., 13, 612-620 (2003).
3. Nadanaka S, Kitagawa H. Heparan sulphate biosynthesis and disease. J. Biochem., 144, 7-14 (2008).
4. Mikami T, Kitagawa H. Biosynthesis and function of chondroitin sulfate. Biochim. Biophys. Acta, 1830, 4719-4733 (2013).
5. Kitagawa H, Uyama T, Sugahara K. Molecular cloning and expression of a human chondroitin synthase. J. Biol. Chem., 276, 38721-38726 (2001).
6. Gotoh M, Yada T, Sato T, Akashima T, Iwasaki H, Mochizuki H, Inaba N, Togayachi A, Kudo T, Watanabe H, Kimata K, Narimatsu H. Molecular cloning and characterization of a novel chondroitin sulfate glucuronyltransferase that transfers glucuronic acid to N-acetylgalactosamine. J. Biol. Chem., 277, 38179-38188 (2002).
7. Kitagawa H, Izumikawa T, Uyama T, Sugahara K. Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization. J. Biol. Chem., 278, 23666-23671 (2003).
8. Yada T, Gotoh M, Sato T, Shionyu M, Go M, Kaseyama H, Iwasaki H, Kikuchi N, Kwon YD, Togayachi A, Kudo T, Watanabe H, Narimatsu H, Kimata K. 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 (2003).
9. Yada T, Sato T, Kaseyama H, Gotoh M, Iwasaki H, Kikuchi N, Kwon YD, Togayachi A, Kudo T, Watanabe H, Narimatsu H, Kimata K. Chondroitin sulfate synthase-3. Molecular cloning and characterization. J. Biol. Chem., 278, 39711-39725 (2003).
10. Izumikawa T, Uyama T, Okuura Y, Sugahara K, Kitagawa H. 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 (2007).
11. Izumikawa T, Koike T, Shiozawa S, Sugahara K, Tamura J, Kitagawa H. 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 (2008).
12. Uyama T, Kitagawa H, Tamura J, Sugahara K. 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 (2002).
13. Gotoh M, Sato T, Akashima T, Iwasaki H, Kameyama A, Mochizuki H, Yada T, Inaba N, Zhang Y, Kikuchi N, Kwon YD, Togayachi A, Kudo T, Nishihara S, Watanabe H, Kimata K, Narimatsu H. 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 (2002).
14. Sato T, Gotoh M, Kiyohara K, Akashima T, Iwasaki H, Kameyama A, Mochizuki H, Yada T, Inaba N, Togayachi A, Kudo T, Asada M, Watanabe H, Imamura T, Kimata K, Narimatsu H. 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 (2003).
15. Uyama T, Kitagawa H, Tanaka J, Tamura J, Ogawa T, Sugahara K. 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 (2003).
16. Nadanaka S, Kitagawa H, Sugahara K. 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, 33728-33734 (1998).
17. Izumikawa T, Okuura Y, Koike T, Sakoda N, Kitagawa H. Chondroitin 4-O-sulfotransferase-1 regulates the chain length of chondroitin sulfate in co-operation with chondroitin N-acetylgalactos-aminyltransferase-2. Biochem. J., 434, 321-331 (2011).
18. Izumikawa T, Koike T, Kitagawa H. Chondroitin 4-O-sulfotransferase-2 regulates the number of chondroitin sulfate chains initiated by chondroitin N-acetylgalactosaminyltransferase-1. Biochem. J., 441, 697-705 (2012).
19. Yamada S, Van Die I, Van den Eijnden DH, Yokota A, Kitagawa H, Sugahara K. Demonstration of glycosaminoglycans in Caenorhabditis elegans. FEBS Lett., 459, 327-331 (1999).
20. Toyoda H, Kinoshita-Toyoda A, Selleck SB. 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, 2269-2275 (2000).
21. Hwang HY, Olson SK, Esko JD, Horvitz HR. Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis. Nature, 423, 439-443 (2003).
22. Mizuguchi S, Uyama T, Kitagawa H, Nomura KH, Dejima K, Gengyo-Ando K, Mitani S, Sugahara K, Nomura K. Chondroitin proteoglycans are involved in cell division of Caenorhabditis elegans. Nature, 423, 443-448 (2003).
23. Izumikawa T, Kitagawa H, Mizuguchi S, Nomura KH, Nomura K, Tamura J, Gengyo-Ando K, Mitani S, Sugahara K. Nematode chondroitin polymerizing factor showing cell-/organ-specific expression is indispensable for chondroitin synthesis and embryonic cell division. J. Biol. Chem., 279, 53755-53761 (2004).
24. Wilson DG, Phamluong K, Lin WY, Barck K, Carano RA, Diehl L, Peterson AS, Martin F, Solloway MJ. Chondroitin sulfate synthase 1 (Chsy1) is required for bone development and digit patterning. Dev. Biol., 363, 413-425 (2012).
25. Ogawa H, Hatano S, Sugiura N, Nagai N, Sato T, Shimizu K, Kimata K, Narimatsu H, Watanabe H. Chondroitin sulfate synthase-2 is necessary for chain extension of chondroitin sulfate but not critical for skeletal development. PLoS ONE, 7, e43806 (2012).
26. Watanabe Y, Takeuchi K, Higa Onaga S, Sato M, Tsujita M, Abe M, Natsume R, Li M, Furuichi T, Saeki M, Izumikawa T, Hasegawa A, Yokoyama M, Ikegawa S, Sakimura K, Amizuka N, Kitagawa H, Igarashi M. Chondroitin sulfate N-acetylgalactosaminyltransferase-1 is required for normal cartilage development. Biochem. J., 432, 47-55 (2010).
27. Sato T, Kudo T, Ikehara Y, Ogawa H, Hirano T, Kiyohara K, Hagiwara K, Togayachi A, Ema M, Takahashi S, Kimata K, Watanabe H, Narimatsu H. Chondroitin sulfate N-acetylgalactosaminyltransferase 1 is necessary for normal endochondral ossification and aggrecan metabolism. J. Biol. Chem., 286, 5803-5812 (2011).
28. Kitagawa H, Tone Y, Tamura J, Neumann KW, Ogawa T, Oka S, Kawasaki T, Sugahara K. 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 (1998).
29. Wei G, Bai X, Sarkar AK, Esko JD. Formation of HNK-1 determinants and the glycosaminoglycan tetrasaccharide linkage region by UDP-GlcUA:Galactose beta1, 3-glucuronosyltransferases. J. Biol. Chem., 274, 7857-7864 (1999).
30. Izumikawa T, Kanagawa N, Watamoto Y, Okada M, Saeki M, Sakano M, Sugahara K, Sugihara K, Asano M, Kitagawa H. Impairment of embryonic cell division and glycosaminoglycan biosynthesis in glucuronyltransferase-I-deficient mice. J. Biol. Chem., 285, 12190-12196 (2010).
31. Izumikawa T, Sato B, Kitagawa H. Chondroitin sulfate is indispensable for pluripotency and differentiation of mouse embryonic stem cells. Sci. Rep., 4, 3701 (2014).
32. Rochlin K, Yu S, Roy S, Baylies MK. Myoblast fusion: when it takes more to make one. Dev. Biol., 341, 66-83 (2010).
33. Pavlath GK. Spatial and functional restriction of regulatory molecules during mammalian myoblast fusion. Exp. Cell Res., 316, 3067-3072 (2010).
34. Mikami T, Koyama S, Yabuta Y, Kitagawa H. Chondroitin sulfate is a crucial determinant for skeletal muscle development/regeneration and improvement of muscular dystrophies. J. Biol. Chem., 287, 38531-38542 (2012).
35. Kitagawa H, Shimakawa H, Sugahara K. The tumor suppressor EXT-like gene EXTL2 encodes an α1,4-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, 13933-13937 (1999).
36. Kitagawa H, Kano Y, Shimakawa H, Goto F, Ogawa T, Okabe H, Sugahara K. Identification and characterization of a novel UDPGalNAc:GlcAbeta-R alpha1,4-N-acetylgalactosaminyltransferase from a human sarcoma cell line. Glycobiology, 9, 697-703 (1999).
37. Nadanaka S, Zhou S, Kagiyama S, Shoji N, Sugahara K, Sugihara K, Asano M, Kitagawa H. EXTL2, a member of EXT family of tumor suppressors, controls glycosaminoglycan biosynthesis in a xylose kinase-dependent manner. J. Biol. Chem., 288, 9321-9333 (2013).
38. Koike T, Izumikawa T, Tamura J, Kitagawa H. FAM20B is a kinase that phosphorylates xylose in the glycosaminoglycan-protein linkage region. Biochem. J., 421, 157-162 (2009).
39. Nadanaka S, Kagiyama S, Kitagawa H. Roles of EXTL2, a member of the EXT family of tumour suppressors, in liver injury and regeneration processes. Biochem. J., 454, 133-145 (2013).
40. Purnomo E, Emoto N, Nugrahaningsih DAA, Nakayama K, Yagi K, Heiden S, Nadanaka S, Kitagawa H, Hirata K. Glycosaminoglycan overproduction in the aorta increases aortic calcification in murine chronic kidney disease. J. Am. Heart Assoc., 2, e000405 (2013).
41. Nadanaka S, Kitagawa H. EXTL2 controls liver regeneration and aortic calcification through xylose kinase-dependent regulation of glycosaminoglycan biosynthesis. Matrix Biol., 35, 18-24 (2014).
42. Saigoh K, Izumikawa T, Koike T, Shimizu J, Kitagawa H, Kusunoki S. Chondroitin beta-1,4-N-acetylgalactosaminyltransferase-1 missense mutations are associated with neuropathies. J. Hum. Genet., 56, 143-146 (2011).
43. Izumikawa T, Saigoh K, Shimizu J, Tsuji S, Kusunoki S, Kitagawa H. Chondroitin synthase-1 (ChSy-1) missense mutation in a patient with neuropathy impairs the elongation of chondroitin sulfate chains initiated by chondroitin N-acetylgalactosaminyltransferase-1. Biochim. Biophys. Acta, 1830, 4806-4812 (2013).
44. Uyama T, Ishida M, Izumikawa T, Trybala E, Tufaro F, Bergström T, Sugahara K, Kitagawa H. Chondroitin 4-O-sulfotransferase-1 regulates E disaccharide expression of chondroitin sulfate required for herpes simplex virus infectivity. J. Biol. Chem., 281, 38668-38674 (2006).
45. Bergefall K, Trybala E, Johansson M, Uyama T, Naito S, Yamada S, Kitagawa H, Sugahara K, Bergström T. 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, 32193-32199 (2005).
46. Nadanaka S, Ishida M, Ikegami M, Kitagawa H. Chondroitin 4-O-sulfotransferase-1 modulates Wnt-3a signaling through control of E disaccharide expression of chondroitin sulfate. J. Biol. Chem., 283, 27333-27343 (2008).
47. Nadanaka S, Kinouchi H, Taniguchi-Morita K, Tamura J, Kitagawa H. Down-regulation of chondroitin 4-O-sulfotransferase-1 by Wnt signaling triggers diffusion of Wnt-3a. J. Biol. Chem., 286, 4199-4208 (2011).
48. Thiele H, Sakano M, Kitagawa H, Sugahara K, Rajab A, Höhne W, Ritter H, Leschik G, Nürnberg P, Mundlos S. 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 (2004).
49. Kitagawa H, Fujita M, Ito N, Sugahara K. Molecular cloning and expression of a novel chondroitin 6-O-sulfotransferase. J. Biol. Chem., 275, 21075-21080 (2000).
50. Galtrey CM, Fawcett JW. The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system. Brain Res. Rev., 54, 1-18 (2007).
51. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L. Reactivation of ocular dominance plasticity in the adult visual cortex. Science, 298, 1248-1251 (2002).
52. Kitagawa H, Tsutsumi K, Tone Y, Sugahara K. Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain. J. Biol. Chem., 272, 31377-31381 (1997).
53. Miyata S, Komatsu Y, Yoshimura Y, Taya C, Kitagawa H. Persistent cortical plasticity by upregulation of chondroitin 6-sulfation. Nat. Neurosci., 15, 414-422, S1-S2 (2012).
54. Sugiyama S, Di Nardo AA, Aizawa S, Matsuo I, Volovitch M, Prochiantz A, Hensch TK. Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell, 134, 508-520 (2008).
55. Lewis DA, Hashimoto T, Volk DW. Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci., 6, 312-324 (2005).
56. Bradbury EJ, Moon LD, Popat RJ, King VR, Bennett GS, Patel PN, Fawcett JW, McMahon SB. Chondroitinase ABC promotes functional recovery after spinal cord injury. Nature, 416, 636-640 (2002).
57. Silver J, Miller JH. Regeneration beyond the glial scar. Nat. Rev. Neurosci., 5, 146-156 (2004).
58. Gama CI, Tully SE, Sotogaku N, Clark PM, Rawat M, Vaidehi N, Goddard WA 3rd, Nishi A, Hsieh-Wilson LC. Sulfation patterns of glycosaminoglycans encode molecular recognition and activity. Nat. Chem. Biol., 2, 467-473 (2006).
59. Purushothaman A, Fukuda J, Mizumoto S, ten Dam GB, van Kuppevelt TH, Kitagawa H, Mikami T, Sugahara K. Functions of chondroitin sulfate/dermatan sulfate chains in brain development: critical roles of E and iE disaccharide units recognized by a single chain antibody GD3G7. J. Biol. Chem., 282, 19442-19452 (2007).
60. Mikami T, Yasunaga D, Kitagawa H. Contactin-1 is a functional receptor for neuroregulatory chondroitin sulfate-E. J. Biol. Chem., 284, 4494-4499 (2009).
61. Cheng SL, Shin CS, Towler DA, Civitelli R. A dominant negative cadherin inhibits osteoblast differentiation. J. Bone Miner. Res., 15, 2362-2370 (2000).
62. Kii I, Amizuka N, Shimomura J, Saga Y, Kudo A. 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, 1840-1849 (2004).
63. Koike T, Izumikawa T, Tamura J, Kitagawa H. 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, 523-529 (2012).
64. Miyazaki T, Miyauchi S, Tawada A, Anada T, Matsuzaka S, Suzuki O. Oversulfated chondroitin sulfate-E binds to BMP-4 and enhances osteoblast differentiation. J. Cell. Physiol., 217, 769-777 (2008).
65. Koike T, Izumikawa T, Sato B, Kitagawa H. Identification of phosphatase that dephosphorylates xylose in the glycosaminoglycan-protein linkage region of proteoglycans. J. Biol. Chem., 289, 6695-6708 (2014).