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J. Biol. Chem., Vol. 279, Issue 9, 8219-8229, February 27, 2004

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Distinctive Expression Patterns of Heparan Sulfate O-Sulfotransferases and Regional Differences in Heparan Sulfate Structure in Chick Limb Buds^*

Ken Nogami, Hiroaki Suzuki¶, Hiroko Habuchi¶, Naoki Ishiguro, Hisashi Iwata, and Koji Kimata¶||

From the ^¶Institute for Molecular Science of Medicine, Aichi Medical University, Yazako, Nagakute, Aichi 480-1195 and the Department of Orthopaedic Surgery, Nagoya University School of Medicine, 65 Tsurumai-Cho, Showa-Ku, Nagoya 466-8550, Japan

The skeletal tissue development and patterning in chick limb buds are known to be under the spacio-temporal control of various heparin-binding cell growth factors such as fibroblast growth factors and bone morphogenetic proteins. Different structural regions on heparan sulfate (HS) chains of proteoglycans could be implicated in regional differences in the binding capacities of these cell growth factors, by which they could selectively interact with targeted cells and regulate their signaling in those processes. In this study we first demonstrated by cDNA cloning that one heparan sulfate 2-O-sulfotransferase (HS2ST) and two isoforms of heparan sulfate 6-O-sulfotransferase (HS6ST-1 and -2) occurred in chick embryos and had different substrate specificities each other. We next showed by whole mount in situ hybridization that the HS6ST-1 and HS6ST-2 transcripts were preferentially localized to the anterior proximal region and at the posterior proximal region of the limb bud, respectively, whereas the HS2ST transcript was distributed rather uniformly throughout the bud. Analyses of the structures of HS from different regions of the wing buds have shown variation in that 6-O-sulfated residues are more abundant in the proximal than distal region, whereas iduronosyl 6-O-sulfated residues are abundant in the anterior proximal region and glucuronosyl 6-O-sulfated residues in the posterior proximal region. These results suggest that HS with different sulfation patterns created with multiple sulfotransferase activities provides an appropriate extracellular environment for morphogenetic signal transduction.

Received for publication, July 8, 2003 , and in revised form, December 1, 2003.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AB093515 (chick HS2ST mRNA), AB093516 (chick HS6ST-1 mRNA), and AB071190 (chick HS6ST-2 mRNA).

^* This work was supported by Grant-in-aid for Scientific Research on Priority Areas (14082206) from the Ministry of Education, Culture, Sports, Science and Technology of Japan; by a Grant-in-Aid for Scientific Research (B) from the Japan Society for the Promotion of Science; by the preparatory grant for the research at the Matrix Glycoconjugate Group, Research Center for Infectious Disease, Aichi Medical University; and by a special research fund from Seikagaku Corporation. 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.

Both authors contributed equally to this work.

^|| To whom correspondence should be addressed. Tel.: 81-52-264-4811; Fax: 81-561-63-3532; E-mail: kimata{at}amugw.aichi-med-u.ac.jp.

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