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J. Biol. Chem., Vol. 278, Issue 33, 31118-31127, August 15, 2003

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Heparan Sulfate 6-O-Sulfotransferase Is Essential for Muscle Development in Zebrafish^*

From the ^aHubrecht Laboratory, Netherlands Institute for Developmental Biology, Uppsalalaan 8, 3584 CT Utrecht, the Netherlands, the ^dInstitute for Molecular Science of Medicine, Aichi Medical University, Nagakute, Aichi 480-1195, Japan, the ^eDepartment of Anatomy and Developmental Biology, University College London, Gower Street, London WC1E 6BT, United Kingdom, and the ^hMax-Planck-Institut für Entwicklungsbiologie, Abteilung III-Genetik, Spemannstrasse 35, 72076 Tübingen, Germany

Heparan sulfate proteoglycans function in development and disease. They consist of a core protein with attached heparan sulfate chains that are altered by a series of carbohydrate-modifying enzymes and sulfotransferases. Here, we report on the identification and characterization of a gene encoding zebrafish heparan sulfate 6-O-sulfotransferase (hs6st) that shows high homology to other heparan sulfate 6-O-sulfotransferases. When expressed as a fusion protein in cultured cells, the protein shows specific 6-O-sulfotransferase activity and preferentially acts on the iduronosyl N-sulfoglycosamine. In the developing embryo, hs6st is expressed in the brain, the somites, and the fins; the same structures that were affected upon morpholino-mediated functional knockdown. Morpholino injections significantly inhibited 6-O- but not 2-O-sulfation as assessed by HPLC. Morphants display disturbed somite specification independent of the somite oscillator mechanism and have impaired muscle differentiation. In conclusion, our results show that transfer of sulfate to specific positions on glycosaminoglycans is essential for muscle development.

Received for publication, December 23, 2002 , and in revised form, May 28, 2003.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AJ505990.

^* This work was supported by the German Human Genome Project (DHGP Grant 01 KW 9919) and the National Institutes of Health (NIH Grant 1 R01 DK55377-01A1) (to R. G.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^b Present address: Netherlands Forensic Institute, Volmerlaan 17, 2288 GC Rijswijk, the Netherlands.

^c These authors contributed equally to the work.

^f Present address: Dept. of Molecular Cell Biology, University Utrecht, Padualaan 8, 3584 CH Utrecht, the Netherlands.

^g Present address: Pepscan Systems, Edelhertweg 15, 8219 PH Lelystad, the Netherlands.

ⁱ Present address: Dept. of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305.

^j To whom correspondence should be addressed. Tel.: 31-30-2121800; Fax: 31-30-2516464; E-mail: dana{at}niob.knaw.nl.

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