Chondroitin 4-O-sulfotransferase-1 is required for somitic muscle development and motor axon guidance in zebrafish

Biochemical Journal

Volumn 419, Issue 2, 2009, Pages 387-399

  Mizumoto, Shuji ^a,b   Mikami, Tadahisa ^a   Yasunaga, Daiki ^a   Kobayashi, Naoki ^a   Yamauchi, Hajime ^c   Miyake, Ayumi ^c   Itoh, Nobuyuki ^c   Kitagawa, Hiroshi ^a   Sugahara, Kazuyuki ^a,b  

^a KOBE PHARMACEUTICAL UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

Chondroitin sulfate; Embryogenesis; Glycos aminoglycan; Sulfation; Sulfotransferase; Zebrafish

Indexed keywords

CHONDROITIN SULFATE; EMBRYOGENESIS; GLYCOS-AMINOGLYCAN; SULFATION; SULFOTRANSFERASE; ZEBRAFISH;

MOTORS; OLIGONUCLEOTIDES; SULFUR COMPOUNDS;

MUSCLE;

CHONDROITIN; CHONDROITIN 4 O SULFOTRANSFERASE 1; CHONDROITIN SULFATE; ISOENZYME; MORPHOLINE; MYOD PROTEIN; N ACETYLGALACTOSAMINE; SULFOTRANSFERASE; UNCLASSIFIED DRUG; CHONDROITIN 4 SULFOTRANSFERASE; CHONDROITIN 4-SULFOTRANSFERASE; ZEBRAFISH PROTEIN;

ARTICLE; CHROMOSOME ABERRATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENZYME SPECIFICITY; GENE EXPRESSION; IN SITU HYBRIDIZATION; MORPHOLOGY; MUSCLE DEVELOPMENT; NERVE FIBER GROWTH; NONHUMAN; NOTOCHORD; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; SOMITE; SULFATION; ZEBRA FISH; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; METABOLISM; MOLECULAR GENETICS; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; PRENATAL DEVELOPMENT; PROTEIN BINDING;

DANIO RERIO; VERTEBRATA;

ANIMALS; CHONDROITIN SULFATES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; ISOENZYMES; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; NEUROGENESIS; PROTEIN BINDING; SUBSTRATE SPECIFICITY; SULFOTRANSFERASES; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 64249117496     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20081639     Document Type: Article

References (50)

1. Iozzo, R. V. (1998) Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67, 609-652
2. 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
3. Sugahara, K. and Mikami, T. (2007) Chondroitin/dermatan sulfate in the central nervous system. Curr. Opin. Struct. Biol. 17, 536-545
4. Schwartz, N. B. and Domowicz, M. (2002) Chondrodysplasias due to proteoglycan defects. Glycobiology 12, 57R-68R
5. Uyama, T., Kitagawa, H. and Sugahara, K. (2007) Biosynthesis of glycosaminoglycans and proteoglycans. In Comprehensive Glycoscience, Volume 3 (Kamerling, J. P., ed.), pp. 79-104, Elsevier, Amsterdam
6. Mark, M. P., Baker, J. R., Kimata, K. and Ruch, J. V. (1990) Regulated changes in chondroitin sulfation during embryogenesis: an immunohistochemical approach. Int. J. Dev. Biol. 34, 191-204
7. Kitagawa, H., Tsutsumi, K., Tone, Y. and Sugahara, K. (1997) Developmental regulation of the sulfation profile of chondroitin sulfate chains in the chicken embryo development. J. Biol. Chem. 272, 31377-31381
8. Mitsunaga, C., Mikami, T., Mizumoto, S., Fukuda, J. and Sugahara, K. (2006) 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, 18942-18952
9. Mikami, T. and Sugahara, K. (2006) The biological importance of specific sulfation of chondroitin sulfate/dermatan sulfate in their functional expression. Trends Glycosci. Glycotechnol. 18, 165-183
10. Gama, C. I., Tully, S. E., Sotogaku, N., Clark, P. M., Rawat, M., Vaidehi, N., Goddard, III, W. A., Nishi, A. and Hsieh-Wilson, L. C. (2006) Sulfation patterns of glycosaminoglycans encode molecular recognition and activity. Nat. Chem. Biol. 2, 467-473
11. Kusche-Gullberg, M. and Kjellén, L. (2003) Sulfotransferase in glycosaminoglycan biosynthesis. Curr. Opin. Struct. Biol. 13, 605-611
12. Maccarana, M., Olander, B., Malmström, J., Tiedemann, K., Aebersold, R., Lindahl, U., Li, J. P. and Malmström, A. (2006) Biosynthesis of dermatan sulfate: chondroitin-glucuronate C5-epimerase is identical to SART2. J. Biol. Chem. 281, 11560-11568
13. Yamauchi, S., Mita, S., Matsubara, T., Fukuta, M., Habuchi, H., Kimata, K. and Habuchi, O. (2000) Molecular cloning and expression of chondroitin 4-sulfotransferase. J. Biol. Chem. 275, 8975-8981
14. 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
15. 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. J. Biol. Chem. 277, 34766-34772
16. 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
17. 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. J. Biol. Chem. 278, 36115-36127
18. Uyama, T., Ishida, M., Izumikawa, T., Trybala, E., Tufaro, F., Bergström, T., Sugahara, K. and Kitagawa, H. (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
19. Klüppel, M., Wight, T. N., Chan, C., Hinek, A. and Wrana, J. L. (2005) Maintenance of chondroitin sulfation balance by chondroitin-4-sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis. Development 132, 3989-4003
20. Nüsslein-Volhard, C., Gilmour, D. T. and Dahm, R. (2002) Introduction: zebrafish as a system to study development and organogenesis. In Zebrafish (Nüsslein-Volhard, C. and Dahm R., eds), pp. 1-5, Oxford University Press, New York
21. Grunwald, D. J. and Eisen, J. S. (2002) Headwaters of the zebrafish - emergence of a new model vertebrate. Nat. Rev. Genet. 3, 717-724
22. Bernhardt, R. R., Goerlinger, S., Roos, M. and Schachner, M. (1998) Anterior-posterior subdivision of the somite in embryonic zebrafish: implications for motor axon guidance. Dev. Dyn. 213, 334-347
23. Bernhardt, R. R. and Schachner, M. (2000) Chondroitin sulfates affect the formation of the segmental motor nerves in zebrafish embryos. Dev. Biol. 221, 206-219
24. Schneider, V. A. and Granato, M. (2003) Motor axon migration: a long way to go. Dev. Biol. 263, 1-11
25. Stickney, H. L., Barresi, M. J. and Devoto, S. H. (2000) Somite development in zebrafish. Dev. Dyn. 219, 287-303
26. Inohaya, K., Takano, Y. and Kudo, A. (2007) The teleost intervertebral region acts as a growth center of the centrum: in vivo visualization of osteoblasts and their progenitors in transgenic fish. Dev. Dyn. 236, 3031-3046
27. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995) Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310
28. Kitagawa, H., Egusa, N., Tamura, J., Kusche-Gullberg, M., Lindahl, U. and Sugahara, K. (2001) rib-2, a Caenorhabditis elegans homolog of the human tumor suppressor EXT genes encodes a novel alpha1,4-N-acetylglucosaminyltransferase involved in the biosynthetic initiation and elongation of heparan sulfate. J. Biol. Chem. 276, 4834-4838
29. Roelink, H., Augsburger, A., Heemskerk, J., Korzh, V., Norlin, S., Ruiz i Altaba, A., Tanabe, Y., Placzek, M., Edlund, T., Jessell, T. M. and Dodd, J. (1994) Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761-775
30. Weinberg, E. S., Allende, M. L., Kelly, C. S., Abdelhamid, A., Murakami, T., Andermann, P., Doerre, O. G., Grunwald, D. J. and Riggleman, B. (1996) Developmental regulation of zebrafish MyoD in wild-type, no tail and spadetail embryos. Development 122, 271-280
31. Schlte-Merker, S. (2002) Looking at embryos. In Zebrafish (Nüsslein-Volhard, C. and Dahm, R., eds), pp. 39-58, Oxford University Press, New York
32. Nasevicius, A. and Ekker, S. C. (2000) Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26, 216-220
33. Yamada, S., Okada, Y., Ueno, M., Iwata, S., Deepa, S. S., Nishimura, S., Fujita, M., Van Die, I., Hirabayashi, Y. and Sugahara, K. (2002) Determination of the glycosaminoglycan-protein linkage region oligosaccharide structures of proteoglycans from Drosophila melanogaster and Caenorhabditis elegans. J. Biol. Chem. 277, 31877-31886
34. Kinoshita, A. and 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
35. Souza, A. R., Kozlowski, E. O., Cerqueira, V. R., Castelo-Branco, M. T., Costa, M. L. and Pavão, M. S. (2007) Chondroitin sulfate and keratan sulfate are the major glycosaminoglycans present in the adult zebrafish Danio rerio (Chordata-Cyprinidae). Glycoconj. J. 24, 521-530
36. Stemple, D. L., Solnica-Krezel, L., Zwartkruis, F., Neuhauss, S. C. F., Schier, A. F., Malicki, J., Stainier, D. Y. R., Abdelilah, S., Rangini, Z., Mountcastle-Shah, E. and Driever, W. (1996) Mutations affecting development of the notochord in zebrafish. Development 123, 117-128
37. Asakura, A., Hirai, H., Kablar, B., Morita, S., Ishibashi, J., Piras, B. A., Christ, A. J., Verma, M., Vineretsky, K. A. and Rudnicki, M. A. (2007) Increased survival of muscle stem cells lacking the MyoD gene after transplantation into regenerating skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 104, 16552-16557
38. Bink, R. J., Habuchi, H., Lele, Z., Dolk, E., Joore, J., Rauch, G. J., Geisler, R., Wilson, S. W., den Hertog, J., Kimata, K. and Zivkovic, D. (2003) Heparan sulfate 6-O-sulfotransferase is essential for muscle development in zebrafish. J. Biol. Chem. 278, 31118-31127
39. Chen, E., Stringer, S. E., Rusch, M. A., Selleck, S. B. and Ekker, S. C. (2005) A unique role for 6-O sulfation modification in zebrafish vascular development. Dev. Biol. 284, 364-376
40. Esko, J. D. and Selleck, S. B. (2002) Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435-471
41. Raman, R., Sasisekharan, V. and Sasisekharan, R. (2005) Structural insights into biological roles of protein-glycosaminoglycan interactions. Chem. Biol. 12, 267-277
42. Feng, X., Adiarte, E. G. and Devoto, S. H. (2006) Hedgehog acts directly on the zebrafish dermomyotome to promote myogenic differentiation. Dev. Biol. 300, 736-746
43. Pownall, M. E., Gustafsson, M. K. and Emerson, Jr, C. P. (2002) Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 18, 747-783
44. Nadanaka, S., Ishida, M., Ikegami, M. and Kitagawa, H. (2008) Chondroitin 4-O-sulfotransferase-1 modulates Wnt-3a signaling through control of E disaccharide expression of chondroitin sulfate. J. Biol. Chem. 283, 27333-27343
45. Klüppel, M., Vallis, K. A. and Wrana, J. L. (2002) A high-throughput induction gene trap approach defines C4ST as a target of BMP signaling. Mech. Dev. 118, 77-89
46. Mullins, M. C., Hammerschmidt, M., Kane, D. A., Odenthal, J., Brand, M., van Eeden, F. J., Furutani-Seiki, M., Granato, M., Haffter, P., Heisenberg, C. P. et al. (1996) Genes establishing dorsoventral pattern formation in the zebrafish embryo: the ventral specifying genes. Development 123, 81-93
47. Zhang, I., Lefebvre, J. L., Zhao, S. and Granato, M. (2004) Zebrafish unplugged reveals a role for muscle-specific kinase homologs in axonal pathway choice. Nat. Neurosci. 7, 1303-1309
48. Kantor, D. B., Chivatakarn, O., Peer, K. L., Oster, S. F., Inatani, M., Hansen, M. J., Flanagan, J. G., Yamaguchi, Y., Sretavan, D. W., Giger, R. J. and Kolodkin, A. L. (2004) Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44, 961-975
49. 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
50. 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