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J Virol. Jan 1989; 63(1): 52–58.
PMCID: PMC247656

Initial interaction of herpes simplex virus with cells is binding to heparan sulfate.

Abstract

We have shown that cell surface heparan sulfate serves as the initial receptor for both serotypes of herpes simplex virus (HSV). We found that virions could bind to heparin, a related glycosaminoglycan, and that heparin blocked virus adsorption. Agents known to bind to cell surface heparan sulfate blocked viral adsorption and infection. Enzymatic digestion of cell surface heparan sulfate but not of dermatan sulfate or chondroitin sulfate concomitantly reduced the binding of virus to the cells and rendered the cells resistant to infection. Although cell surface heparan sulfate was required for infection by HSV types 1 and 2, the two serotypes may bind to heparan sulfate with different affinities or may recognize different structural features of heparan sulfate. Consistent with their broad host ranges, the two HSV serotypes use as primary receptors ubiquitous cell surface components known to participate in interactions with the extracellular matrix and with other cell surfaces.

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Selected References

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  • Addison C, Rixon FJ, Palfreyman JW, O'Hara M, Preston VG. Characterisation of a herpes simplex virus type 1 mutant which has a temperature-sensitive defect in penetration of cells and assembly of capsids. Virology. 1984 Oct 30;138(2):246–259. [PubMed]
  • Brown MS, Deuel TF, Basu SK, Goldstein JL. Inhibition of the binding of low-density lipoprotein to its cell surface receptor in human fibroblasts by positively charged proteins. J Supramol Struct. 1978;8(3):223–234. [PubMed]
  • Cai WH, Gu B, Person S. Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. J Virol. 1988 Aug;62(8):2596–2604. [PMC free article] [PubMed]
  • Cai WZ, Person S, Warner SC, Zhou JH, DeLuca NA. Linker-insertion nonsense and restriction-site deletion mutations of the gB glycoprotein gene of herpes simplex virus type 1. J Virol. 1987 Mar;61(3):714–721. [PMC free article] [PubMed]
  • Campadelli-Fiume G, Arsenakis M, Farabegoli F, Roizman B. Entry of herpes simplex virus 1 in BJ cells that constitutively express viral glycoprotein D is by endocytosis and results in degradation of the virus. J Virol. 1988 Jan;62(1):159–167. [PMC free article] [PubMed]
  • Cassai EN, Sarmiento M, Spear PG. Comparison of the virion proteins specified by herpes simplex virus types 1 and 2. J Virol. 1975 Nov;16(5):1327–1331. [PMC free article] [PubMed]
  • Cole GJ, Glaser L. A heparin-binding domain from N-CAM is involved in neural cell-substratum adhesion. J Cell Biol. 1986 Feb;102(2):403–412. [PMC free article] [PubMed]
  • Cole GJ, Loewy A, Glaser L. Neuronal cell-cell adhesion depends on interactions of N-CAM with heparin-like molecules. Nature. 1986 Apr 3;320(6061):445–447. [PubMed]
  • Cole GJ, Schubert D, Glaser L. Cell-substratum adhesion in chick neural retina depends upon protein-heparan sulfate interactions. J Cell Biol. 1985 Apr;100(4):1192–1199. [PMC free article] [PubMed]
  • Desai PJ, Schaffer PA, Minson AC. Excretion of non-infectious virus particles lacking glycoprotein H by a temperature-sensitive mutant of herpes simplex virus type 1: evidence that gH is essential for virion infectivity. J Gen Virol. 1988 Jun;69(Pt 6):1147–1156. [PubMed]
  • Draper KG, Costa RH, Lee GT, Spear PG, Wagner EK. Molecular basis of the glycoprotein-C-negative phenotype of herpes simplex virus type 1 macroplaque strain. J Virol. 1984 Sep;51(3):578–585. [PMC free article] [PubMed]
  • Ejercito PM, Kieff ED, Roizman B. Characterization of herpes simplex virus strains differing in their effects on social behaviour of infected cells. J Gen Virol. 1968 May;2(3):357–364. [PubMed]
  • Esko JD, Stewart TE, Taylor WH. Animal cell mutants defective in glycosaminoglycan biosynthesis. Proc Natl Acad Sci U S A. 1985 May;82(10):3197–3201. [PMC free article] [PubMed]
  • Esko JD, Weinke JL, Taylor WH, Ekborg G, Rodén L, Anantharamaiah G, Gawish A. Inhibition of chondroitin and heparan sulfate biosynthesis in Chinese hamster ovary cell mutants defective in galactosyltransferase I. J Biol Chem. 1987 Sep 5;262(25):12189–12195. [PubMed]
  • Fuller AO, Spear PG. Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virion-cell fusion at the cell surface. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5454–5458. [PMC free article] [PubMed]
  • Gill PJ, Silbert CK, Silbert JE. Effects of heparan sulfate removal on attachment and reattachment of fibroblasts and endothelial cells. Biochemistry. 1986 Jan 28;25(2):405–410. [PubMed]
  • Goldstein JL, Basu SK, Brunschede GY, Brown MS. Release of low density lipoprotein from its cell surface receptor by sulfated glycosaminoglycans. Cell. 1976 Jan;7(1):85–95. [PubMed]
  • Highlander SL, Cai WH, Person S, Levine M, Glorioso JC. Monoclonal antibodies define a domain on herpes simplex virus glycoprotein B involved in virus penetration. J Virol. 1988 Jun;62(6):1881–1888. [PMC free article] [PubMed]
  • Highlander SL, Sutherland SL, Gage PJ, Johnson DC, Levine M, Glorioso JC. Neutralizing monoclonal antibodies specific for herpes simplex virus glycoprotein D inhibit virus penetration. J Virol. 1987 Nov;61(11):3356–3364. [PMC free article] [PubMed]
  • Homa FL, Purifoy DJ, Glorioso JC, Levine M. Molecular basis of the glycoprotein C-negative phenotypes of herpes simplex virus type 1 mutants selected with a virus-neutralizing monoclonal antibody. J Virol. 1986 May;58(2):281–289. [PMC free article] [PubMed]
  • Hök M, Kjellén L, Johansson S. Cell-surface glycosaminoglycans. Annu Rev Biochem. 1984;53:847–869. [PubMed]
  • Kjellén L, Pettersson I, Hök M. Cell-surface heparan sulfate: an intercalated membrane proteoglycan. Proc Natl Acad Sci U S A. 1981 Sep;78(9):5371–5375. [PMC free article] [PubMed]
  • Laterra J, Silbert JE, Culp LA. Cell surface heparan sulfate mediates some adhesive responses to glycosaminoglycan-binding matrices, including fibronectin. J Cell Biol. 1983 Jan;96(1):112–123. [PMC free article] [PubMed]
  • Ligas MW, Johnson DC. A herpes simplex virus mutant in which glycoprotein D sequences are replaced by beta-galactosidase sequences binds to but is unable to penetrate into cells. J Virol. 1988 May;62(5):1486–1494. [PMC free article] [PubMed]
  • Little SP, Jofre JT, Courtney RJ, Schaffer PA. A virion-associated glycoprotein essential for infectivity of herpes simplex virus type 1. Virology. 1981 Nov;115(1):149–160. [PubMed]
  • Longnecker R, Roizman B. Clustering of genes dispensable for growth in culture in the S component of the HSV-1 genome. Science. 1987 May 1;236(4801):573–576. [PubMed]
  • Markwell MA, Fredman P, Svennerholm L. Receptor ganglioside content of three hosts for Sendai virus. MDBK, HeLa, and MDCK cells. Biochim Biophys Acta. 1984 Aug 8;775(1):7–16. [PubMed]
  • Mitsuya H, Looney DJ, Kuno S, Ueno R, Wong-Staal F, Broder S. Dextran sulfate suppression of viruses in the HIV family: inhibition of virion binding to CD4+ cells. Science. 1988 Apr 29;240(4852):646–649. [PubMed]
  • Morgan C, Rose HM, Mednis B. Electron microscopy of herpes simplex virus. I. Entry. J Virol. 1968 May;2(5):507–516. [PMC free article] [PubMed]
  • Nahmias AJ, Kibrick S. Inhibitory effect of heparin on herpes simplex virus. J Bacteriol. 1964 May;87(5):1060–1066. [PMC free article] [PubMed]
  • Neidhardt H, Schröder CH, Kaerner HC. Herpes simplex virus type 1 glycoprotein E is not indispensable for viral infectivity. J Virol. 1987 Feb;61(2):600–603. [PMC free article] [PubMed]
  • Para MF, Baucke RB, Spear PG. Immunoglobulin G(Fc)-binding receptors on virions of herpes simplex virus type 1 and transfer of these receptors to the cell surface by infection. J Virol. 1980 May;34(2):512–520. [PMC free article] [PubMed]
  • Rapraeger A, Bernfield M. Cell surface proteoglycan of mammary epithelial cells. Protease releases a heparan sulfate-rich ectodomain from a putative membrane-anchored domain. J Biol Chem. 1985 Apr 10;260(7):4103–4109. [PubMed]
  • Sarmiento M, Haffey M, Spear PG. Membrane proteins specified by herpes simplex viruses. III. Role of glycoprotein VP7(B2) in virion infectivity. J Virol. 1979 Mar;29(3):1149–1158. [PMC free article] [PubMed]
  • Spear PG, Roizman B. Proteins specified by herpes simplex virus. V. Purification and structural proteins of the herpesvirion. J Virol. 1972 Jan;9(1):143–159. [PMC free article] [PubMed]
  • Stannard LM, Fuller AO, Spear PG. Herpes simplex virus glycoproteins associated with different morphological entities projecting from the virion envelope. J Gen Virol. 1987 Mar;68(Pt 3):715–725. [PubMed]
  • TAKEMOTO KK, FABISCH P. INHIBITION OF HERPES VIRUS BY NATURAL AND SYNTHETIC ACID POLYSACCHARIDES. Proc Soc Exp Biol Med. 1964 May;116:140–144. [PubMed]
  • Vahlne A, Svennerholm B, Lycke E. Evidence for herpes simplex virus type-selective receptors on cellular plasma membranes. J Gen Virol. 1979 Jul;44(1):217–225. [PubMed]
  • Vahlne A, Svennerholm B, Sandberg M, Hamberger A, Lycke E. Differences in attachment between herpes simplex type 1 and type 2 viruses to neurons and glial cells. Infect Immun. 1980 Jun;28(3):675–680. [PMC free article] [PubMed]

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