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

Volumn 21, Issue 5, 2011, Pages 565-574

  Akatsu, Chizuru ^a,c   Mizumoto, Shuji ^a   Kaneiwa, Tomoyuki ^a   MacCarana, Marco ^b   Malmström, Anders ^b   Yamada, Shuhei ^a   Sugahara, Kazuyuki ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b LUND UNIVERSITY   (Sweden)

^c MEIJI PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

brain development; chondroitin sulfate; dermatan sulfate; dermatan sulfate epimerase; proteoglycan

Indexed keywords

CHONDROITIN SULFATE; DERMATAN SULFATE; DERMATAN SULFATE EPIMERASE 1; DERMATAN SULFATE EPIMERASE 2; IDURONIC ACID; ISOENZYME; SULFUR 35; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BIOSYNTHESIS; BRAIN; BRAIN DEVELOPMENT; CARBOHYDRATE ANALYSIS; CEREBELLUM; EPIMERIZATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN SITU HYBRIDIZATION; MEDULLA OBLONGATA; MESENCEPHALON; MOUSE; NONHUMAN; OLFACTORY BULB; PONS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; BRAIN; CARBOHYDRATE EPIMERASES; CHONDROITIN SULFATES; DERMATAN SULFATE; DISACCHARIDASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IDURONIC ACID; IN SITU HYBRIDIZATION; ISOENZYMES; MICE; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 79953842941     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwq208     Document Type: Article

References (61)

1. Bao X, Muramatsu T, Sugahara K. 2005. Demonstration of the pleiotrophin-binding oligosaccharide sequences isolated from chondroitin sulfate/derma-tan sulfate hybrid chains of embryonic pig brains. J Biol Chem. 280:35318-35328. (Pubitemid 41532720)
2. Bao X, Nishimura S, Mikami T, Yamada S, Itoh N, Sugahara K. 2004. Chondroitin sulfate/dermatan sulfate hybrid chains from embryonic pig brain, which contain a higher proportion of L-iduronic acid than those from adult pig brain, exhibit neuritogenic and growth factor binding activities. J Biol Chem. 279:9765-9776. (Pubitemid 38372574)
3. Basappa, Murugan S, Sugahara KN, Lee CM, ten Dam GB, van Kuppevelt TH, Miyasaka M, Yamada S, Sugahara K. 2009. Involvement of chondroitin sulfate E in the liver tumor focal formation of murine osteosarcoma cells. Glycobiology. 19:735-742.
4. Bitter T, Muir HM. 1962. A modified uronic acid carbazole reaction. Anal Biochem. 4:330-334.
5. Casu B, Petitou M, Provasoli M, Sinaÿ P. 1988. Conformational flexibility: A new concept for explaining binding and biological properties of iduronic acid-containing glycosaminoglycans. Trends Biochem Sci. 13:221-225.
6. Clement AM, Nadanaka S, Masayama K, Mandl C, Sugahara K, Faissner A. 1998. The DSD-1 carbohydrate epitope depends on sulfation, correlates with chondroitin sulfate D motifs, and is sufficient to promote neurite outgrowth. J Biol Chem. 273:28444-28453. (Pubitemid 28496150)
7. Clement AM, Sugahara K, Faissner A. 1999. Chondroitin sulfate E promotes neurite outgrowth of rat embryonic day 18 hippocampal neurons. Neurosci Lett. 269:125-128. (Pubitemid 29317716)
8. Cöster L, Malmström A, Sjöberg I, Fransson LÅ. 1975. The co-polymeric structure of pig skin dermatan sulphate: Distribution of L-iduronic acid sulphate residues in co-polymeric chains. Biochem J. 145:379-389.
9. Dündar M, Müller T, Zhang Q, Pan J, Steinmann B, Vodopiutz J, Gruber R, Sonoda T, Krabichler B, Utermann G, et al. 2009. Loss of dermatan-4-sulfotransferase 1 function results in adducted thumb-clubfoot syndrome. Am J Hum Genet. 85:873-882.
10. Esko JD, Selleck SB. 2002. Order out of chaos: Assembly of ligand binding sites in heparan sulfate. Annu Rev Biochem. 71:435-471. (Pubitemid 34800227)
11. Faissner A, Clement A, Lochter A, Streit A, Mandl C, Schachner M. 1994. Isolation of a neural chondroitin sulfate proteoglycan with neurite outgrowth promoting properties. J Cell Biol. 126:783-799. (Pubitemid 24241390)
12. Ferro DR, Provasoli A, Ragazzi M, Casu B, Torri G, Bossennec V, Perly B, Sinaÿ P, Petitou M, Choay J. 1990. Conformer populations of L-iduronic acid residues in glycosaminoglycan sequences. Carbohydr Res. 195:157-167.
13. Fransson LÅ, Rodén L. 1967. Structure of dermatan sulfate: I. Degradation by testicular hyaluronidase. J Biol Chem. 242:4161-4169.
14. Goossens D, Van Gestel S, Claes S, De Rijk P, Souery D, Massat I, Van den Bossche D, Backhovens H, Mendlewicz J, Van Broeckhoven C, et al. 2003. A novel CpG-associated brain-expressed candidate gene for chromosome 18q-linked bipolar disorder. Mol Psychiatry. 8:83-89. (Pubitemid 36188576)
15. Habuchi H, Yamagata T, Iwata H, Suzuki S. 1973. The occurrence of a wide variety of dermatan sulfate-chondroitin sulfate copolymers in fibrous cartilage. J Biol Chem. 248:6019-6028.
16. Hikino M, Mikami T, Faissner A, Vilela-Silva ACES, Pavão MSG, Sugahara K. 2003. Oversulfated dermatan sulfate exhibits neurite outgrowth-promoting activity toward embryonic mouse hippocampal neurons: Implications of dermatan sulfate in neuritogenesis in the brain. J Biol Chem. 278:43744-43754. (Pubitemid 37346002)
17. Hiyama K, Okada S. 1975. Crystallization and some properties of chondroiti-nase from Arthrobacter aurescens. J Biol Chem. 250:1824-1828.
18. Ishii M, Maeda N. 2008. Spatiotemporal expression of chondroitin sulfate sul-fotransferases in the postnatal developing mouse cerebellum. Glycobiology. 18:602-614.
19. Izumikawa T, Koike T, Shiozawa S, Sugahara K, Tamura J, Kitagawa H. 2008. Identification of chondroitin sulfate glucuronyltransferase as chon-droitin 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.
20. Izumikawa T, Uyama T, Okuura Y, Sugahara K, Kitagawa H. 2007. Involvement of chondroitin sulfate synthase-3 (chondroitin synthase-2) in chondroitin polymerization through its interaction with chondroitin synthase-1 or chondroitin-polymerizing factor. Biochem J. 403:545-552. (Pubitemid 46706983)
21. Kinoshita A, Sugahara K. 1999. Microanalysis of glycosaminoglycan-derived oligosaccharides labeled with a fluorophore 2-aminobenzamide by high-performance liquid chromatography: Application to disaccharide composition analysis and exosequencing of oligosaccharides. Anal Biochem. 269:367-378. (Pubitemid 29201038)
22. Kitagawa H, Izumikawa T, Uyama T, Sugahara K. 2003. Molecular cloning of a chondroitin polymerizing factor that cooperates with chondroitin synthase for chondroitin polymerization. J Biol Chem. 278:23666-23671. (Pubitemid 36833253)
23. Kitagawa H, Tsutsumi K, Tone Y, Sugahara K. 1997. Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo brain. J Biol Chem. 272:31377-31381. (Pubitemid 28013273)
24. Kitagawa H, Uyama T, Sugahara K. 2001. Molecular cloning and expression of a human chondroitin synthase. J Biol Chem. 276: 38721-38726.
25. Kobayashi M, Sugumaran G, Liu J, Shworak NW, Silbert JE, Rosenberg RD. 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.
26. Kusche-Gullberg M, Kjellén L. 2003. Sulfotransferases in glycosaminoglycan biosynthesis. Curr Opin Struct Biol. 13:605-611. (Pubitemid 37244116)
27. Li F, Nandini CD, Hattori T, Bao X, Murayama D, Nakamura T, Fukushima N, Sugahara K. 2010. Structure of pleiotrophin- and hepatocyte growth factor-binding sulfated hexasaccharide determined by biochemical and computational approaches. J Biol Chem. 285:27673-27685.
28. Li F, Shetty AK, Sugahara K. 2007. Neuritogenic activity of chondroitin/ dermatan sulfate hybrid chains of embryonic pig brain and their mimicry from shark liver: Involvement of the pleiotrophin and hepatocyte growth factor signaling pathways. J Biol Chem. 282:2956-2966. (Pubitemid 47084329)
29. Li F, ten Dam GB, Murugan S, Yamada S, Hashiguchi T, Mizumoto S, Oguri K, Okayama M, van Kuppevelt TH, Sugahara K. 2008. Involvement of highly sulfated chondroitin sulfate in the metastasis of the Lewis lung carcinoma cells. J Biol Chem. 283:34294-34304.
30. Linhardt RJ, Avci FY, Toida T, Kim YS, Cygler M. 2006. CS lyases: Structure, activity, and applications in analysis and the treatment of diseases. In: Volpi N, editor. Chondroitin Sulfate: Structure, Role and Pharmacological Activity. London (UK): Academic Press. p. 187-215.
31. Maccarana M, Kalamajski S, Kongsgaard M, Magnusson SP, Oldberg Å, Malmström A. 2009. 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. 29:5517-5528.
32. Maccarana M, Olander B, Malmström J, Tiedemann K, Aebersold R, Lindahl U, Li JP, Malmström A. 2006. Biosynthesis of dermatan sulfate: Chondroitin-glucuronate C5-epimerase is identical to SART2. J Biol Chem. 281:11560-11568. (Pubitemid 43855412)
33. Maimone MM, Tollefsen DM. 1990. Structure of a dermatan sulfate hexasac-charide that binds to heparin cofactor II with high affinity. J Biol Chem. 265:18263-18271.
34. Malmström A. 1984. Biosynthesis of dermatan sulfate: II. Substrate specificity of the C-5 uronosyl epimerase. J Biol Chem. 259:161-165. (Pubitemid 14177641)
35. McCormick C, Duncan G, Goutsos KT, Tufaro F. 2000. The putative tumor suppressors EXT1 and EXT2 form a stable complex that accumulates in the Golgi apparatus and catalyzes the synthesis of heparan sulfate. Proc Natl Acad Sci USA. 97:668-673. (Pubitemid 30070367)
36. Michelacci YM, Dietrich CP. 1974. Isolation and partial characterization of an induced chondroitinase B from Flavobacterium heparinum. Biochem Biophys Res Commun. 56:973-980.
37. Mikami T, Mizumoto S, Kago N, Kitagawa H, 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. (Pubitemid 37139933)
38. Mitsunaga C, Mikami T, Mizumoto S, Fukuda J, Sugahara K. 2006. Chondroitin sulfate/dermatan sulfate hybrid chains in the development of cerebellum: Spatiotemporal regulation of the expression of critical disul-fated disaccharides by specific sulfotransferases. J Biol Chem. 281:18942-18952. (Pubitemid 44035397)
39. Miyake N, Kosho T, Mizumoto S, Furuichi T, Hatamochi A, Nagashima Y, Arai E, Takahashi K, Kawamura R, Wakui K, et al. 2010. Loss-of-function mutations of CHST14 in a new type of Ehlers-Danlos syndrome. Hum Mutat. 31:966-974.
40. Nadanaka S, Clement AM, Masayama K, Faissner A, Sugahara K. 1998. Characteristic hexasaccharide sequences in octasaccharides derived from shark cartilage chondroitin sulfate D with a neurite outgrowth promoting activity. J Biol Chem. 273:3296-3307. (Pubitemid 28109743)
41. Nakao M, Shichijo S, Imaizumi T, Inoue Y, Matsunaga K, Yamada A, Kikuchi M, Tsuda N, Ohta K, Takamori S, et al. 2000. Identification of a gene coding for a new squamous cell carcinoma antigen recognized by the CTL. J Immunol. 164:2565-2574. (Pubitemid 30115487)
42. Nandini CD, Itoh N, Sugahara K. 2005. Novel 70-kDa chondroitin sulfate/der-matan sulfate hybrid chains with a unique heterogeneous sulfation pattern from shark skin, which exhibit neuritogenic activity and binding activities for growth factors and neurotrophic factors. J Biol Chem. 280:4058-4069. (Pubitemid 40288569)
43. Nandini CD, Mikami T, Ohta M, Itoh N, Akiyama-Nambu F, Sugahara K. 2004. Structural and functional characterization of oversulfated chondroitin sulfate/dermatan sulfate hybrid chains from the notochord of hagfish: Neuritogenic and binding activities for growth factors and neurotrophic factors. J Biol Chem. 279:50799-50809. (Pubitemid 40017818)
44. Ohtake S, Kimata K, Habuchi O. 2003. A unique nonreducing terminal modification of chondroitin sulfate by N-acetylgalactosamine 4-sulfate 6-O-sulfotransferase. J Biol Chem. 278:38443-38452. (Pubitemid 37221738)
45. Pacheco B, Maccarana M, Malmström A. 2009a. Dermatan 4-O-sulfotransferase 1 is pivotal in the formation of iduronic acid blocks in dermatan sulfate. Glycobiology. 19:1197-1203.
46. Pacheco B, Malmström A, Maccarana M. 2009b. Two dermatan sulfate epi-merases form iduronic acid domains in dermatan sulfate. J Biol Chem. 284:9788-9795.
47. Penc SF, Pomahac B, Winkler T, Dorschner RA, Eriksson E, Herndon M, Gallo RL. 1998. Dermatan sulfate released after injury is a potent promoter of fibroblast growth factor-2 function. J Biol Chem. 273:28116-28121. (Pubitemid 28496107)
48. Petit E, Delattre C, Papy-Garcia D, Michaud P. 2006. Chondroitin sulfate lyases: Applications in analysis and glycobiology. In: Volpi N, editor. Chondroitin Sulfate: Structure, Role and Pharmacological Activity. London (UK): Academic Press. p. 167-186.
49. Pinhal MAS, Smith B, Olson S, Aikawa J, Kimata K, Esko JD. 2001. Enzyme interactions in heparan sulfate biosynthesis: Uronosyl 5-epimerase and 2-O-sulfotransferase interact in vivo. Proc Natl Acad Sci USA. 98:12984-12989. (Pubitemid 33054083)
50. Presto J, Thuveson M, Carlsson P, Busse M, Wilén M, Eriksson I, Kusche-Gullberg M, Kjellén L. 2008. Heparan sulfate biosynthesis enzymes EXT1 and EXT2 affect NDST1 expression and heparan sulfate sulfation. Proc Natl Acad Sci USA. 105:4751-4756. (Pubitemid 351753818)
51. Rodier PM. 1977. Correlations between prenatally-induced alterations in CNS cell populations and postnatal function. Teratology. 16:235-246. (Pubitemid 8215240)
52. Senay C, Lind T, Muguruma K, Tone Y, Kitagawa H, Sugahara K, Lidholt K, Lindahl U, Kusche-Gullberg M. 2000. The EXT1/EXT2 tumor suppressors: Catalytic activities and role in heparan sulfate biosynthesis. EMBO Rep. 1:282-286.
53. Shors TJ. 2009. Saving new brain cells. Sci Am. 300:46-54.
54. Sugahara K, Mikami T. 2007. Chondroitin/dermatan sulfate in the central nervous system. Curr Opin Struct Biol. 17:536-545. (Pubitemid 350019013)
55. Thiele H, Sakano M, Kitagawa H, Sugahara K, Rajab A, Höhne W, Ritter H, Leschik G, Nürnberg P, Mundlos S. 2004. Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement. Proc Natl Acad Sci USA. 101:10155-10160. (Pubitemid 38891211)
56. Trowbridge JM, Rudisill JA, Ron D, Gallo RL. 2002. Dermatan sulfate binds and potentiates activity of keratinocyte growth factor (FGF-7). J Biol Chem. 277:42815-42820. (Pubitemid 35285657)
57. Tuysuz B, Mizumoto S, Sugahara K, Çelebi A, Mundlos S, Turkmen S. 2009. Omani-type spondyloepiphyseal dysplasia with cardiac involvement caused by a missense mutation in CHST3. Clin Genet. 75:375-383.
58. van Roij MHH, Mizumoto S, Yamada S, Morgan T, Tan-Sindhunata MB, Meijers-Heijboer H, Verbeke JILM, Markie D, Sugahara K, Robertson SP. 2008. Spondyloepiphyseal dysplasia, Omani type: Further definition of the phenotype. Am J Med Genet A. 146A:2376-2384.
59. Yamada S, Sugahara K. 2008. Potential therapeutic application of chondroitin sulfate/dermatan sulfate. Curr Drug Discov Technol. 5:289-301.
60. Yamagata T, Saito H, Habuchi O, Suzuki S. 1968. Purification and properties of bacterial chondroitinases and chondrosulfatases. J Biol Chem. 243:1523-1535.
61. Yoshida K, Arai M, Kohno Y, Maeyama K, Miyazono H, Kikuchi H, Morikawa K, Tawada A, Suzuki S. 1993. Activity of bacterial eliminases towards der-matan sulphates and dermatan sulphate proteoglycan. In: Scott JE, editor. Dermatan Sulphate Proteoglycans. London (UK): Portland Press. p. 55-70.