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Journal of Virology, July 2006, p. 6629-6636, Vol. 80, No. 13
0022-538X/06/$08.00+0     doi:10.1128/JVI.01988-05
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

N- and 6-O-Sulfated Heparan Sulfates Mediate Internalization of Coxsackievirus B3 Variant PD into CHO-K1 Cells

Andreas E. Zautner, Birgit Jahn, Elke Hammerschmidt, Peter Wutzler, and Michaela Schmidtke*

Institute of Virology and Antiviral Therapy, Medical Centre of the Friedrich Schiller University Jena, Hans Knoell Str. 2, PF, D-07740 Jena, Germany

Received 19 September 2005/ Accepted 3 April 2006

Recently, it was demonstrated that the coxsackievirus B3 variant PD (CVB3 PD) is able to infect coxsackievirus-adenovirus receptor (CAR)-lacking cells by using heparan sulfates (HS) as additional receptors (A. E. Zautner, U. Korner, A. Henke, C. Badorff, and M. Schmidtke, J. Virol. 77:10071-10077, 2003). For this study, competition experiments with growth factors binding to known HS sequences as well as with specifically desulfated heparins were performed with Chinese hamster ovary cells (CHO-K1) to determine the structural requirements of HS for interaction with CVB3. Hepatocyte growth factor interacting with HS sequences containing [IdUA-GlcNSO3(6OSO3)]n, but not basic fibroblast growth factor binding to [HexUA-GlcNSO3-HexUA-GlcNSO3-IdUA(2OSO3)]n, was shown to compete effectively with CVB3 PD for cell surface HS. Whereas unmodified heparin and 2-O-desulfated heparin strongly inhibited the CVB3 PD-induced cytopathic effect, the antiviral activity was markedly reduced after N-, O- and 6-O-desulfation of heparin. Taken together, these results indicate that 6-O- and N-sulfation of GlcNAc of HS is crucial for HS interaction with CVB3 PD and that the disaccharide [IdUA-GlcNSO3(6OSO3)]n is involved in viral binding. Results from experiments with various inhibitors of endocytic pathways suggest that HS-mediated virus internalization is pH dependent. Despite the fact that CVB3 PD initiates infection about four times slower by making use of HS as a receptor than by using CAR, the time required for a complete viral life cycle in Chinese hamster ovary cells was independent of the utilized receptor.

* Corresponding author. Mailing address: Institute of Virology and Antiviral Therapy, Medical Centre of the Friedrich Schiller University Jena, Hans-Knoell-Str. 2, D-07740 Jena, Germany. Phone: 49 3641 657222. Fax: 49 3641 657202. E-mail: michaela.schmidtke{at}med.uni-jena.de.

Journal of Virology, July 2006, p. 6629-6636, Vol. 80, No. 13
0022-538X/06/$08.00+0     doi:10.1128/JVI.01988-05
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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