Herpes simplex virus type 2 glycoprotein G is targeted by the sulfated oligo- and polysaccharide inhibitors of virus attachment to cells

Journal of Virology

Volumn 81, Issue 24, 2007, Pages 13424-13434

  Adamiak, Beata ^a,c   Ekblad, Maria ^a   Bergström, Tomas ^a   Ferro, Vito ^b   Trybala, Edward ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b Progen Pharmaceuticals Limited   (Australia)

^c UNIVERSITY OF GDA SK   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; GLYCOPROTEIN D; GLYCOPROTEIN E; GLYCOPROTEIN K; GLYCOSAMINOGLYCAN; HEPARIN; MUCIN; OLIGOSACCHARIDE; POLYSACCHARIDE SULFATE; PROTEIN C; SULFATED OLIGOSACCHARIDE PI 88; THROMBOSPONDIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL SPREADING; FRAMESHIFT MUTATION; GENE; GLYCOPROTEIN G GENE; HERPES SIMPLEX VIRUS 2; INFECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; CELL LINE; DRUG RESISTANCE, VIRAL; FRAMESHIFT MUTATION; HERPESVIRUS 2, HUMAN; HUMANS; KIDNEY; MOLECULAR SEQUENCE DATA; OLIGOSACCHARIDES; PLAQUE ASSAY; POLYSACCHARIDES; SEQUENCE ANALYSIS, DNA; VIRAL ENVELOPE PROTEINS;

HUMAN HERPESVIRUS 2; SIMPLEXVIRUS;

EID: 37149049377     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01528-07     Document Type: Article

References (39)

1. Adams, Y., C. Freeman, R. Schwartz-Albiez, V. Ferro, C. R. Parish, and K. T. Andrews. 2006. Inhibition of Plasmodium falciparum growth in vitro and adhesion to chondroitin-4-sulfate by the heparan sulfate mimetic PI-88 and other sulfated oligosaccharides. Antimicrob. Agents Chemother. 50:2850-2852.
2. Balachandran, N., and L. M. Hutt-Fletcher. 1985. Synthesis and processing of glycoprotein gG of herpes simplex virus type 2. J. Virol. 54:825-832.
3. Boukamp, P., R. T. Petrussevska, D. Breitkreutz, J. Hornung, A. Markham, and N. E. Fusenig. 1988. Normal keratinization in a spontaneously immortalized aneuploid human keratinocyte cell line. J. Cell Biol. 106:761-771.
4. Carlucci, M. J., L. A. Scolaro, and E. B. Damonte. 2002. Herpes simplex virus type 1 variants arising after selection with an antiviral carageenan: lack of correlation between drug susceptibility and syn phenotype. J. Med. Virol. 68:92-98.
5. Cheshenko, N., and B. C. Herold. 2002. Glycoprotein B plays a predominant role in mediating herpes simplex virus type 2 attachment and is required for entry and cell-to-cell spread. J. Gen. Virol. 83:2247-2255.
6. Duff, R., and F. Rapp. 1971. Oncogenic transformation of hamster cells after exposure to herpes simplex virus type 2. Nat. New Biol. 233:48-50.
7. Ekblad, M., B. Adamiak, K. Bergefall, H. Nenonen, A. Roth, T. Bergström, V. Ferro, and E. Trybala. 2007. Molecular basis for resistance of herpes simplex virus type 1 mutants to the sulfated oligosaccharide inhibitor PI-88. Virology 367:244-252.
8. Ekblad, M., T. Bergström, M. G. Banwell, M. Bonnet, J. Renner, V. Ferro, and E. Trybala. 2006. Anti-herpes simplex virus activities of two novel disulphated cyclitols. Antivir. Chem. Chemother. 17:97-106.
9. Feldman, S. A., R. M. Hendry, and J. A. Beeler. 1999. Identification of a linear heparin binding domain for human respiratory syncytial virus attachment glycoprotein G. J. Virol. 73:6610-6617.
10. Geraghty, R. J., C. Krummenacher, G. H. Cohen, R. J. Eisenberg, and P. G. Spear. 1998. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science 280:1618- 1620.
11. Gerber, S. I., B. J. Belval, and B. C. Herold. 1995. Differences in the role of glycoprotein C of HSV-1 and HSV-2 in viral binding may contribute to serotype differences in cell tropism. Virology 214:29-39.
12. Goodman, J. L., and J. P. Engel. 1991. Altered pathogenesis in herpes simplex virus type 1 infection due to a syncytial mutation mapping to the carboxy terminus of glycoprotein B. J. Virol. 65:1770-1778.
13. Görander, S., B. Svennerholm, and J.-Å. Liljeqvist. 2003. Secreted portion of glycoprotein G of herpes simplex virus type 2 is a novel antigen for type-discriminating serology. J. Clin. Microbiol. 41:3681-3686.
14. Gunalp, A. 1965. Growth and cytopathic effect of rubella virus in a line of green monkey kidney cells. Proc. Soc. Exp. Biol. Med. 118:185-190.
15. Herold, B. C., D. WuDunn, N. Soltys, and P. G. Spear. 1991. Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectivity. J. Virol. 65:1090-1098.
16. Johnson, D. C., M. Webb, T. W. Wisner, and C. Brunetti. 2001. Herpes simplex virus gE/gI sorts nascent virions to epithelial cell junctions, promoting virus spread. J. Virol. 75:821-833.
17. Krusat, T., and H. J. Strecken. 1997. Heparin-dependent attachment of respiratory syncytial virus (RSV) to host cells. Arch. Virol. 142:1247-1254.
18. Lee, E., M. Pavy, N. Young, C. Freeman, and M. Lobigs. 2006. Antiviral effect of the heparan sulfate mimetic, PI-88, against dengue and encephalitic flaviviruses. Antivir. Res. 69:31-38.
19. Lee, F. K., R. M. Coleman, L. Pereira, P. D. Bailey, M. Tatsuno, and A. J. Nahmias. 1985. Detection of herpes simplex virus type 2-specific antibody with glycoprotein G. J. Clin. Microbiol. 22:641-644.
20. Liljeqvist, J.-Å., B. Svennerholm, and T. Bergström. 1999. Herpes simplex virus type 2 glycoprotein G-negative clinical isolates are generated by single frameshift mutations. J. Virol. 73:9796-9802.
21. Liljeqvist, J.-Å., E. Trybala, J. Hoebeke, B. Svennerholm, and T. Bergström. 2002. Monoclonal antibodies and human sera directed to the secreted glycoprotein G of herpes simplex virus type 2 recognize type-specific antigenic determinants. J. Gen. Virol. 83:157-165.
22. Mårdberg, K., E. Trybala, J. C. Glorioso, and T. Bergström. 2001. Mutational analysis of the major heparan sulfate-binding domain of herpes simplex virus type 1 glycoprotein C. J. Gen. Virol. 82:1941-1950.
23. Marsden, H. S., A. Buckmaster, J. W. Palfreyman, R. G. Hope, and A. C. Minson. 1984. Characterization of the 92,000-dalton glycoprotein induced by herpes simplex virus type 2. J. Virol. 50:547-554.
24. Mettenleiter, T. C., B. Lomniczi, N. Sugg, C. Schreurs, and T. Ben-Porat. 1988. Host cell-specific growth advantage of pseudorabies virus with a deletion in the genome sequences encoding a structural glycoprotein. J. Virol. 62:12-19.
25. Montgomery, R. I., M. S. Warner, B. J. Lum, and P. G. Spear. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87:427-436.
26. Neyts, J., and E. De Clercq. 1995. Effect of polyanionic compounds on intracutaneous and intravaginal herpesvirus infection in mice: impact on the search for vaginal microbicides with anti-HIV activity. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol. 10:8-12.
27. Nyberg, K., M. Ekblad, T. Bergström, C. Freeman, C. R. Parish, V. Ferro, and E. Trybala. 2004. The low molecular weight heparan sulfate-mimetic, PI-88, inhibits cell-to-cell spread of herpes simplex virus. Antivir. Res. 63: 15-24.
28. Oyan, A. M., K. E. Dolter, N. Langeland, W. F. Goins, J. C. Glorioso, L. Haarr, and C. S. Crumpacker. 1993. Resistance of herpes simplex virus type 2 to neomycin maps to the N-terminal portion of glycoprotein C. J. Virol. 67:2434-2441.
29. Pertel, P. E., and P. G. Spear. 1996. Modified entry and syncytium formation by herpes simplex virus type 1 mutants selected for resistance to heparin inhibition. Virology 226:22-33.
30. Shields, B., J. Mills, R. Ghildyal, P. Gooley, and J. Meanger. 2003. Multiple heparin binding domains of respiratory syncytial virus G mediate binding to mammalian cells. Arch. Virol. 148:1987-2003.
31. Shukla, D., J. Liu, P. Blaiklock, N. W. Shworak, X. Bai, J. D. Esko, G. H. Cohen, R. J. Eisenberg, R. D. Rosenberg, and P. G. Spear. 1999. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell 99:13-22.
32. r cleavage product. J. Virol. 61:1735-1737.
33. Su, H. K., J. D. Fetherston, M. E. Smith, and R. J. Courtney. 1993. Orientation of the cleavage site of the herpes simplex virus glycoprotein G-2. J. Virol. 67:2954-2959.
34. Tal-Singer, R., C. Peng, M. Ponce de Leon, W. R. Abrams, B. W. Banfield, F. Tufaro, G. H. Cohen, and R. J. Eisenberg. 1995. Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. J. Virol. 69:4471-4483.
35. Trybala, E., T. Bergström, B. Svennerholm, S. Jeansson, J. C. Gloriose, and S. Olofsson. 1994. Localization of a functional site on herpes simplex virus type 1 glycoprotein C involved in binding to cell surface heparan sulphate. J. Gen. Virol. 75:743-752.
36. Trybala, E., J.-Å. Liljeqvist, B. Svennerholm, and T. Bergström. 2000. Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. J. Virol. 74:9106-9114.
37. Vaheri, A. 1964. Heparin and related polyionic substances as virus inhibitors. Acta Pathol. Microbiol. Scand. Suppl. 171:1-98.
38. WuDunn, D., and P. G. Spear. 1989. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. J. Virol. 63:52-58.
39. Yu, G., N. S. Gunay, R. J. Linhardt, T. Toida, J. Fareed, D. A. Hoppensteadt, H. Shadid, V. Ferro, C. Li, K. Fewings, M. C. Palermo, and D. Podger. 2002. Preparation and anticoagulant activity of the phosphosulfomannan PI-88. Eur. J. Med. Chem. 37:783-791.