N- and 6-O-sulfated heparan sulfates mediate internalization of coxsackievirus B3 variant PD into CHO-K1 cells

J Virol. 2006 Jul;80(13):6629-36. doi: 10.1128/JVI.01988-05.

Abstract

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-GlcNSO(3)(6OSO(3))](n), but not basic fibroblast growth factor binding to [HexUA-GlcNSO(3)-HexUA-GlcNSO(3)-IdUA(2OSO(3))](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-GlcNSO(3)(6OSO(3))](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.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anticoagulants / pharmacology
  • CHO Cells
  • Coxsackie and Adenovirus Receptor-Like Membrane Protein
  • Cricetinae
  • Cricetulus
  • Cytopathogenic Effect, Viral / drug effects
  • Drug Antagonism
  • Drug Synergism
  • Endocytosis / drug effects*
  • Enterovirus B, Human / metabolism*
  • Enterovirus Infections / metabolism*
  • Fibroblast Growth Factors / pharmacology
  • Heparin / pharmacology
  • Heparitin Sulfate / pharmacology*
  • Hepatocyte Growth Factor / pharmacology
  • Humans
  • Hydrogen-Ion Concentration
  • Receptors, Virus / deficiency
  • Time Factors

Substances

  • Anticoagulants
  • CLMP protein, human
  • Coxsackie and Adenovirus Receptor-Like Membrane Protein
  • Receptors, Virus
  • Fibroblast Growth Factors
  • Hepatocyte Growth Factor
  • Heparin
  • Heparitin Sulfate