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Originally published In Press as doi:10.1074/jbc.M201312200 on March 12, 2002

J. Biol. Chem., Vol. 277, Issue 20, 18182-18190, May 17, 2002
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Biosynthesis of HNK-1 Glycans on O-Linked Oligosaccharides Attached to the Neural Cell Adhesion Molecule (NCAM)
THE REQUIREMENT FOR CORE 2 beta 1,6-N-ACETYLGLUCOSAMINYLTRANSFERASE AND THE MUSCLE-SPECIFIC DOMAIN IN NCAM*

Edgar OngDagger , Misa Suzuki, Frederic Belot§, Jiunn-Chern Yeh, Isabelle Franceschini||, Kiyohiko Angata, Ole Hindsgaul, and Minoru Fukuda**

From the Glycobiology Program, Cancer Research Center, The Burnham Institute, La Jolla, California 92037

The HNK-1 glycan, sulforight-arrow3GlcAbeta 1right-arrow3Galbeta 1right-arrow4GlcNAcbeta 1right-arrowR, is highly expressed in neuronal cells and apparently plays critical roles in neuronal cell migration and axonal extension. The HNK-1 glycan synthesis is initiated by the addition of beta 1,3-linked GlcA to N-acetyllactosamine followed by sulfation of the C-3 position of GlcA. The cDNAs encoding beta 1,3-glucuronyltransferase (GlcAT-P) and HNK-1 sulfotransferase (HNK-1ST) have been recently cloned. Among various adhesion molecules, the neural cell adhesion molecule (NCAM) was shown to contain HNK-1 glycan on N-glycans. In the present study, we first demonstrated that NCAM also bears HNK-1 glycan attached to O-glycans when NCAM contains the O-glycan attachment scaffold, muscle-specific domain, and is synthesized in the presence of core 2 beta 1,6-N-acetylglucosaminyltransferase, GlcAT-P, and HNK-1ST. Structural analysis of the HNK-1 glycan revealed that the HNK-1 glycan is attached on core 2 branched O-glycans, sulforight-arrow3GlcAbeta 1right-arrow3Galbeta 1right-arrow4GlcNAcbeta 1right-arrow6(Galbeta 1right-arrow3)GalNAc. Using synthetic oligosaccharides as acceptors, we found that GlcAT-P and HNK-1ST almost equally act on oligosaccharides, mimicking N- and O-glycans. By contrast, HNK-1 glycan was much more efficiently added to N-glycans than O-glycans when NCAM was used as an acceptor. These results are consistent with our results showing that HNK-1 glycan is minimally attached to O-glycans of NCAM in fetal brain, heart, and the myoblast cell line, C2C12. These results combined together indicate that HNK-1 glycan can be synthesized on core 2 branched O-glycans but that the HNK-1 glycan is preferentially added on N-glycans over O-glycans of NCAM, probably because N-glycans are extended further than O-glycans attached to NCAM containing the muscle-specific domain.

* This work was supported by NCI, National Institutes of Health, Grants R37CA33000, RO1CA33895, and PO1CA71932.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger Present address: Corvas International Inc., San Diego, CA 92121.

§ Present address: Unite de Chimie Organique, Institute Pasteur, 75724 Paris cedex 15, France.

Present address: Genset Corp., San Diego, CA 92121.

|| Present address: Deptartment of Neuroscience, Institute Pasteur, 75724 Paris cedex 15, France.

** To whom correspondence should be addressed: The Burnham Institute, 10901 N. Torrey Pines Rd., La Jolla, CA 92037. Tel.: 858-646-3144; Fax: 858-646-3193; E-mail: minoru@burnham.org.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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