Differences in the susceptibility of herpes simplex virus types 1 and 2 to modified heparin compounds suggest serotype differences in viral entry

Journal of Virology

Volumn 70, Issue 6, 1996, Pages 3461-3469

  Herold, Betsy C ^a   Gerber, Susan I ^a   Belval, Brian J ^a   Siston, Alicia M ^a   Shulman, Nancy ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPARIN; VIRUS RECEPTOR;

ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; HEP 2 CELL; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SEROTYPE; STRAIN DIFFERENCE; VERO CELL; VIRUS ADSORPTION;

EID: 0030000108     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.6.3461-3469.1996     Document Type: Article

References (62)

1. Bae, J., U. Desai, A. Pervin, E. Caldwell, J. Weiler, and R. J. Linhardt. 1994. Interaction of heparin with synthetic antithrombin III peptide analogues. Biochem. J. 301:121-129.
2. Brown, S. M., D. A. Ritchie, and J. H. Subak-Sharpe. 1973. Genetic studies with herpes simplex virus type 1. The isolation of temperature-sensitive mutants, their arrangement into complementation groups and recombination analysis leading to a linkage map. J. Gen. Virol. 18:329-346.
3. Campadelli-Fiume, G., D. Stirpe, A. Boscaro, E. Aritabile, L. Tomasi, D. Barker, and B. Roizman. 1940. Glycoprotein C-dependent attachment of herpes simplex virus to susceptible cells leading to productive infection. Virology 178:213-219.
4. Cassai, E. N., M. Sarmiento, and P. G. Spear. 1975. Comparison of the virion proteins specified by herpes simplex virus types 1 and 2. J. Virol. 16:1327-1331.
5. Compton, T., D. M. Nowlin, and N. R. Cooper. 1993. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 193:834-841.
6. Conley, A. J., D. M. Knipe, P. C. Jones, and B. Roizman. 1981. Molecular genetics of herpes simplex virus. VII. Characterization of a temperature-sensitive mutant produced by in vitro mutagenesis and defective in DNA synthesis and accumulation of γ polypeptides. J. Virol. 37:191-206.
7. David, G. 1993. Integral membrane heparan sulfate proteoglycans. FASEB J. 7:1023-1030.
8. Ejercito, P. M., E. D. Kieff, and B. Roizman. 1968. Characterization of herpes simplex virus strains differing in their effects on social behavior of infected cells. J. Gen. Virol. 2:357-364.
9. Fernandes, J., D. Tang, G. Leone, and P. Lee. 1994. Binding of reovirus to receptor leads to conformational changes in viral capsid proteins that are reversible upon virus detachment. J. Biol. Chem. 269:17043-17047.
10. Flynn, D. C., W. J. Meyer, J. M. MacKenzie, Jr., and R. E. Johnston. 1990. A conformational change in Sindbis virus glycoproteins E1 and E2 is detected at the plasma membrane as a consequence of early virus-cell interaction. J. Virol. 64:3643-3653.
11. Flynn, S. J., and P. Ryan. 1995. A heterologous heparin-binding domain can promote functional attachment of a pseudorabies virus gC mutant to cell surfaces. J. Virol. 69:834-839.
12. Fuller, A. O., and W.-C. Lee. 1992. Herpes simplex virus type 1 entry through a cascade of virus-cell interactions requires different roles of gD and gH in penetration. J. Virol. 66:5002-5012.
13. 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.
14. Gruenheid, S., L. Gatzke, H. Meadows, and F. Tufaro. 1993. Herpes simplex virus infection and propagation in a mouse L cell mutant lacking heparan sulfate proteoglycans. J. Virol. 67:93-100.
15. Habuchi, H., S. Suzuki, T. Saito, T. Tamura, T. Harada, K. Yoshida, and K. Kimata. 1992. Structure of a heparan sulfate oligosaccharide that binds to basic fibroblast growth factor. Biochem. J. 285:805-813.
16. Haywood, A. M. 1994. Virus receptors: binding, adhesion strengthening, and changes in viral structure. J. Virol. 68:1-5.
17. 16a.Herold, B. C. Unpublished data.
18. Herold, B. C., S. I. Gerber, T. Polonksy, B. J. Belval, P. N. Shaklee, and K. Holme. 1995. Identification of structural features of heparin required for inhibition of herpes simplex virus type I binding. Virology 206:1108-1116.
19. Herold, B. C., and P. G. Spear. 1994. Neomycin inhibits glycoprotein C (gC)-dependent binding of herpes simplex virus type 1 to cells and also inhibits postbinding events in entry. Virology 203:166-171.
20. Herold, B. C., R. Visalli, N. Susmarksi, C. Brandt, and P. G. Spear. 1994. Glycoprotein C-independent binding of herpes simplex virus to cells requires cell surface HS and virion gB. J. Gen. Virol. 75:1211-1222.
21. 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.
22. Holland, T. C., R. M. Sandri-Goldin, L. E. Holland, S. D. Marlin, M. Levine, and J. Glorioso. 1983. Physical mapping of the mutation in an antigenic variant of herpes simplex virus type 1 by use of an immunoreactive plaque assay. J. Virol. 46:649-652.
23. Ishihara, M., P. N. Shaklee, Z. Yang, W. Liang, Z. Wei, R. J. Stack, and K. Holme. 1994. Structural features in heparin which modulate specific biological activities mediated by basic fibroblast growth factor. Glycobiology 4:451-458.
24. Jackson, R. L., S. J. Busch, and A. D. Cardin. 1991. Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol. Rev. 71:481-539.
25. Johnson, D. C., R. L. Burke, and T. Gregory. 1990. Soluble forms of herpes simplex virus glycoprotein D hind to a limited number of cell surface receptors and inhibit virus entry into cells. J. Virol. 64:2569-2576.
26. Johnson, D. C., and M. W. Ligas. 1988. Herpes simplex viruses lacking glycoprotein D are unable to inhibit virus penetration: quantitative evidence for virus-specific cell surface receptors. J. Virol. 62:4605-4612.
27. Karger, A., and T. C. Mettenleiter. 1993. Glycoproteins gIII and gp50 play dominant roles in the biphasic attachment of pseudorabies virus. Virology 194:654-664.
28. Kari, B., and R. Gehrz. 1992. A human cytomegalovirus glycoprotein complex designated gC-II is a major heparin-binding component of the envelope. J. Virol. 66:1761-1764.
29. Kari, B., and R. Gehrz. 1993. Structure, composition and heparin binding properties of a human cytomegalovirus glycoprotein complex designated gC-II. J. Gen. Virol. 74:255-264.
30. Kiefer, M. C., J. C. Stephans, K. Crawford, K. Okino, and P. J. Barr. 1990. Ligand-affinity cloning and structure of a cell surface heparan sulfate proteoglycan that binds basic fibroblast growth factor. Proc. Natl. Acad. Sci. USA 87:6985-6989.
31. Kieff, E. D., S. L. Bachenheimer, and B. Roizman. 1971. Size, composition, and structure of the deoxyribonucleic acid of herpes simplex virus subtypes 1 and 2. J. Virol. 8:125-132.
32. Kjellén, L., and U. Lindahl. 1991. Proteoglycans: structures and interactions. Annu. Rev. Biochem. 60:443-475.
33. Langeland, N., H. Holmsen, J. R. Lillehaug, and L. Haarr. 1987. Evidence that neomycin inhibits binding of herpes simplex virus type 1 to the cellular receptor. J. Virol. 61:3388-3393.
34. Langeland, N., L. J. Moore, H. Holsman, and L. Haarr. 1988. Interaction of polylysine with the cellular receptor for herpes simplex virus type 1. J. Gen. Virol. 69:1137-1145.
35. Langeland, N., A. M. Øyan, H. S. Marsden, A. Cross, J. C. Glorioso, L. J. Moore, and L. Haarr. 1990. Localization on the herpes simplex virus type 1 genome of a region encoding proteins involved in adsorption to the cellular receptor. J. Virol. 64:1271-1277.
36. Liang, X., L. A. Babiuk, S. van Drunen Littel-van den Hurk, D. R. Fitzpatrick, and T. J. Zamb. 1991. Bovine herpesvirus 1 attachment to permissive cells is mediated by its major glycoproteins gI, gIII, and gIV. J. Virol. 65:1124-1132.
37. Lindahl, U., and L. Kjellén. 1991. Heparin or heparan sulfate - what is the difference? Thromb. Haemostasis 66:44-48. (Letter.)
38. Lindahl, U., L. Thunberg, G. Backstrom, J. Riesenfild, K. Nording, and I. Bjork. 1984. Extension and structural variability of the antithrombin-binding sequence in heparin. J. Biol. Chem. 259:12368-12376.
39. Lycke, E., M. Johansson, B. Svennerholm, and U. Lindahl. 1991. Binding of herpes simplex virus to cellular heparan sulphate, an initial step in the adsorption process. J. Gen. Virol. 72:1131-1137.
40. McClain, D. S., and A. O. Fuller. 1994. Cell-specific kinetics and efficiency of herpes simplex virus type 1 entry are determined by two distinct phases of attachment. Virology 198:690-702.
41. Mettenleiter, T. C., L. Zsak, F. Zuckermann, N. Sugg, H. Kern, and T. Ben-Porat. 1990. Interaction of glycoprotein gIII with a cellular heparinlike substance mediates adsorption of pseudorabies virus. J. Virol. 64:278-286.
42. Neyts, J., R. Snoeck, D. Schols, J. Balzarini, J. D. Esko, A. Van Schepdael, and E. De Clercq. 1992. Sulfated polymers inhibit the interaction of human cytomegalovirus with cell surface heparan sulfate. Virology 189:48-58.
43. Okazaki, K., T. Matsuzaki, Y. Sugahara, J. Okada, M. Hasebe, Y. Iwamura, M. Ohnishi, T. Kanno, M. Shimizu, and E. Honda. 1991. BHV-1 adsorption is mediated by the interaction of glycoprotein gIII with heparinlike moiety on the cell surface. Virology 181:666-670.
44. Øyan, 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.
45. Sawitsky, D., H. Hampl, and K. O. Habermehl. 1990. Comparison of heparin-sensitive attachment of pseudorabies virus (PRV) and herpes simplex virus type 1 and identification of heparin-binding PRV glycoproteins. J. Gen. Virol. 71:1221-1225.
46. Schreurs, C., T. C. Mettenleiter, F. Zuckermann, N. Sugg, and T. Ben-Porat. 1988. Glycoprotein gIII of pseudorabies virus is multifunctional. J. Virol. 62:2251-2257.
47. Sears, A. E., B. S. McGwire, and B. Roizman. 1991. Infection of polarized MDCK cells with herpes simplex virus 1 : two asymmetrically distributed cell receptors interact with different viral proteins. Proc. Natl. Acad. Sci. USA 88:5087-5091.
48. Shieh, M.-T., and P. G. Spear. 1994. Herpesvirus-induced cell fusion that is dependent on cell surface heparan sulfate or soluble heparin. J. Virol. 68:1224-1228.
49. Shieh, M. T., D. WuDunn, R. I. Montgomery, J. D. Esko, and P. G. Spear. 1992. Cell surface receptors for herpes simplex virus are HS proteoglycans. J. Cell Biol. 116:1273-1281.
50. Smith, K. O. 1964. Relationships between the envelope and the infectivity of herpes simplex virus. Proc. Soc. Exp. Biol. Med. 115:814-819.
51. Spear, P. G. 1993. Entry of alphaherpesviruses into cells. Semin. Virol. 4:167-180.
52. Spivak-Kroizman, T., M. A. Lemmon, I. Dikic, J. E. Ladbury, D. Pinchasi, J. Huang, M. Jaye, G. Crumley, J. Schlessinger, and I. Lax. 1994. Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell 79:1015-1024.
53. Svennerholm, B., S. Jeansson, A. Vahlne, and E. Lycke. 1991. Involvement of glycoprotein C (gC) in adsorption of herpes simplex virus type 1 (HSV-1) to the cell. Arch. Virol. 120:273-279.
54. Swain, M. A., R. W. Peel, and D. A. Galloway. 1985. Characterization of the gene encoding herpes simplex virus type 2 glycoprotein C and comparison with the type 1 counterpart. J. Virol. 53:561-569.
55. 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.
56. Turnball, J. E., D. G. Fernig, Y. Ke, M. C. Wilkinson, and J. T. Gallagher. 1992. Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J. Biol. Chem. 267:10337-10341.
57. Vahlne, A., B. Svennerholm, M. Sandberg, A. Hamberger, and E. Lycke. 1979. Evidence for herpes simplex virus type-selective receptors on cellular plasma membranes. J. Gen. Virol. 4:217-225.
58. Vahlne, A., B. Svennerholm, M. Sandberg, A. Hamberger, and E. Lycke. 1980. Differences in attachment between herpes simplex type 1 and type 2 viruses to neurons and glial cells. Infect. Immun. 28:675-680.
59. 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.
60. Yayon, A., M. Klagsburn, J. D. Esko, P. Leder, and D. M. Ornitz. 1991. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64:841-848.
61. Zsak, L., N. Sugg, T. Ben-Porat, A. K. Robbins, M. E. Whealy, and L. W. Enquist. 1991. The gIII glycoprotein of pseudorabies virus is involved in two distinct steps of virus attachment. J. Virol. 65:4317-4324.
62. Zuckermann, F., L. Zsak, L. Reilly, N. Sugg, and T. Ben-Porat. 1989. Early interactions of pseudorabies virus with host cells: functions of glycoprotein gIII. J. Virol. 63:3323-3329.