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Originally published In Press as doi:10.1074/jbc.M204209200 on July 23, 2002

J. Biol. Chem., Vol. 277, Issue 40, 37912-37919, October 4, 2002
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Heparan Sulfate 3-O-Sulfotransferase Isoform 5 Generates Both an Antithrombin-binding Site and an Entry Receptor for Herpes Simplex Virus, Type 1*

Guoqing XiaDagger , Jinghua Chen§, Vaibhav Tiwari, Wujian Ju§, Jin-Ping Li||, Anders MalmströmDagger , Deepak Shukla, and Jian Liu§**

From the Dagger  Cell and Molecular Biology, Biomedical Center C13, Lund University, Lund S-22184, Sweden, the § Division of Medicinal Chemistry and Natural Products, University of North Carolina, School of Pharmacy, Chapel Hill, North Carolina 27599, the  Departments of Ophthalmology and Visual Sciences and Microbiology and Immunology, University of Illinois, Chicago, Illinois 60612, and the || Department of Medical Biochemistry and Microbiology, Uppsala University, S-75123 Uppsala, Sweden

Heparan sulfate 3-O-sulfotransferase transfers sulfate to the 3-OH position of a glucosamine residue of heparan sulfate (HS) to form 3-O-sulfated HS. The 3-O-sulfated glucosamine residue contributes to two important biological functions of HS: binding to antithrombin and thereby carrying anticoagulant activity, and binding to herpes simplex viral envelope glycoprotein D to serve as an entry receptor for herpes simplex virus 1. A total of five HS 3-O-sulfotransferase isoforms were reported previously. Here we report the isolation and characterization of a novel HS 3-O-sulfotransferase isoform, designated as HS 3-O-sulfotransferase isoform 5 (3-OST-5). 3-OST-5 cDNA was isolated from a human placenta cDNA library and expressed in COS-7 cells. The disaccharide analysis of 3-OST-5-modified HS revealed that 3-OST-5 generated at least three 3-O-sulfated disaccharides as follows: IdoUA2S-AnMan3S, GlcUA-AnMan3S6S, and IdoUA2S-AnMan3S6S. Transfection of the plasmid expressing 3-OST-5 rendered wild type Chinese hamster ovary cells susceptible to the infection by herpes simplex virus 1, suggesting that 3-OST-5-modified HS serves as an entry receptor for herpes simplex virus 1. In addition, 3-OST-5-modified HS bound to herpes simplex viral envelope protein glycoprotein D. Furthermore, we found that 3-OST-5-modified HS also bound to antithrombin, suggesting that 3-OST-5 also produces anticoagulant HS. In summary, our results indicate that a new member of 3-OST family generates both anticoagulant HS and an entry receptor for herpes simplex virus 1. These results provide a new insight regarding the mechanism for the biosynthesis of biologically active HS.

* This work was supported by National Institutes of Health Grants AI50050-01 (to J. L.) and AI053836-01 (to D. S.), a grant from Pharmacy Foundation of North Carolina (to J. L.), and a grant from Swedish Research Council 7479 (to A. M.).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.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBankTM/EBI Data Bank with accession number(s) AF503292.

** To whom correspondence and reprint requests should be addressed: Rm. 309, Beard Hall, CB7360, University of North Carolina, Chapel Hill, NC 27599. Tel.: 919-843-6511; Fax: 919-843-5432; E-mail: jian_liu@unc.edu.

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