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J. Biol. Chem., Vol. 280, Issue 21, 20516-20523, May 27, 2005

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Novel Heparan Sulfate Structures Revealed by Monoclonal Antibodies^*

Jacob van den Born, Katriina Salmivirta¶, Tiina Henttinen||, Nina Östman||, Takeshi Ishimaru**, Shuichi Miyaura**, Keiichi Yoshida**, and Markku Salmivirta||

From the Department of Molecular Cell Biology and Immunology, Vrije Universiteit Medical Center, Amsterdam 1007 MB, The Netherlands, the Department of Animal Physiology, Uppsala University, Uppsala SE-75123, Sweden, the ^¶MediCity Research Laboratory, University of Turku and National Public Health Institute, Turku FIN-20520, Finland, the ^||Turku Centre for Biotechnology, University of Turku and Åbo Akademi University, Turku FIN-20520, Finland, and the ^**Seikagaku Corporation, Central Research Laboratories, Tokyo 207-0021, Japan

The sulfated glycosaminoglycan heparan sulfate (HS) is found ubiquitously on cell surfaces, in the extracellular matrix, and intracellularly as HS proteoglycans. Because of the structural heterogeneity of HS, tissue-derived HS preparations represent a mixture of HS chains originating from different cell types and tissue loci. Monoclonal anti-HS antibodies have been employed to detect the localization of specific HS epitopes in tissues, but limited information has been available on the saccharide structures recognized by the antibodies. We have studied the saccharide epitope structures of four anti-HS antibodies, HepSS1, JM13, JM403, and 10E4, which all recognize distinct HS species as demonstrated by different patterns of immunoreactivity upon staining of embryonic rat and adult human tissues. The epitopes recognized by JM13 and HepSS1 were found almost exclusively in basement membrane HS, whereas JM403 and 10E4 reacted also with cell-associated HS species. The binding of HepSS1, JM403, and 10E4 to HS was dependent on the GlcN N-substitution of the polysaccharide rather than O-sulfation. HepSS1 thus interacted with N-sulfated HS domains, JM403 binding was critically dependent on N-unsubstituted GlcN residues, and 10E4 bound to "mixed" HS domains containing both N-acetylated and N-sulfated disaccharide units. By contrast, JM13 binding seemed to require the presence of 2-O-sulfated glucuronic acid residues.

Received for publication, February 23, 2005

^* This work was supported by the Academy of Finland Grants 78400 and 20688, the Sigrid Jusélius Foundation, Finnish cancer organizations, K. Albin Johanssons Stiftelse, Polysackaridforskning AB, and the Mizutani Foundation for Glycoscience. 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.

To whom correspondence should be addressed: Turku Centre for Biotechnology, University of Turku and Åbo Akademi University, Tykistökatu 6, FIN-20520 Turku, Finland. Tel.: 358-2-333-8649; Fax: 358-2-333-8000; E-mail: markku.salmivirta{at}btk.fi.

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