Skip to main content

The importance of heparan sulfate in herpesvirus infection

Virologica Sinica volume 23, pages 383–393 (2008)Cite this article

Abstract

Herpes simplex virus type-1 (HSV-1) is one of many pathogens that use the cell surface glycosaminoglycan heparan sulfate as a receptor. Heparan sulfate is highly expressed on the surface and extracellular matrix of virtually all cell types making it an ideal receptor. Heparan sulfate interacts with HSV-1 envelope glycoproteins gB and gC during the initial attachment step during HSV-1 entry. In addition, a modified form of heparan sulfate, known as 3-O-sulfated heparan sulfate, interacts with HSV-1 gD to induce fusion between the viral envelope and host cell membrane. The 3-O-sulfation of heparan sulfate is a rare modification which occurs during the biosynthesis of heparan sulfate that is carried out by a family of enzymes known as 3-O-sulfotransferases. Due to its involvement in multiple steps of the infection process, heparan sulfate has been a prime target for the development of agents to inhibit HSV entry. Understanding how heparan sulfate functions during HSV-1 infection may not only be critical for inhibiting infection by this virus, but it may also be crucial in the fight against many other pathogens as well.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  1. Akula S M, Wang F Z, Vierira J,et al. 2001. Human herpesvirus 8 (HHV8/KSHV) infection of target cells involves interaction with heparan sulfate. Virology, 282(2): 245–255.

    PubMed  Article  CAS  Google Scholar 

  2. Andersen J H, Jenssen H, Gutteberg T J. 2003. Lactoferrin and lactoferricin inhibit herpes simplex 1 and 2 infection and exhibit synergy when combined with acyclovir. Antiviral Res, 58(3): 209–215.

    PubMed  Article  CAS  Google Scholar 

  3. Andersen, J H, Jenssen H, Sandvik K,et al. 2004. Anti-HSV activity of lactoferrin and lactoferricin is dependent on the presence of heparan sulphate at the cell surface. J Med Virol, 74(2): 262–271.

    PubMed  Article  CAS  Google Scholar 

  4. Bacon T H, Levin M J, Leary J L,et al. 2003. Herpes simplex virus resistance to acyclovir and penciclovir after two decades of antiviral therapy. Clin Microbiol Rev, 16(1): 114–128.

    PubMed  Article  CAS  Google Scholar 

  5. Barth H, Schafer C, Adah M I,et al. 2003. Cellular binding of hepatitis C virus envelope glycoprotein E2 requires cell surface heparan sulfate. J Biol Chem, 278(42): 41003–41012.

    PubMed  Article  CAS  Google Scholar 

  6. Brady R C, Bernstein D I. 2004. Treatment of herpes simplex virus infections. Antiviral Res, 61(2): 73–81.

    PubMed  Article  CAS  Google Scholar 

  7. Campadelli-Fiume G, Cocchi F, Menotti L,et al. 2000. The novel receptors that mediate the entry of herpes simplex viruses and animal alphaherpesviruses into cells. Rev Med Virol, 10(5): 305–319.

    PubMed  Article  CAS  Google Scholar 

  8. Carfi A, Willis S H, Whitbeck J C,et al. 2001. Herpes simplex virus glycoprotein D bound to the human receptor HveA. Mol Cell, 8(1): 169–179.

    PubMed  Article  CAS  Google Scholar 

  9. Chen J, Avci F Y, Munoz E M,et al. 2005. Enzymatically redesigning of biologically active heparan sulfate. J Biol Chem, 280(52): 42817–42825.

    PubMed  Article  CAS  Google Scholar 

  10. Chen Y, Maguire T, Hileman R E,et al. 1997. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat Med 3(8): 866–871

    PubMed  Article  CAS  Google Scholar 

  11. Clement C, Tiwari V, Scanlan P M,et al. 2006. A novel role for phagocytosis-like uptake in herpes simplex virus entry. J Cell Biol, 174(7): 1009–1021.

    PubMed  Article  CAS  Google Scholar 

  12. Compton T, Nowlin D M, Cooper N R. 1993. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology, 193(2): 834–841.

    PubMed  Article  CAS  Google Scholar 

  13. Copeland R, Balasubramaniam A, Tiwari V,et al. 2008. Using a 3-O-sulfated heparin octasaccharide to inhibit the entry of herpes simplex virus type 1. Biochemistry, 47(21): 5774–5783.

    PubMed  Article  CAS  Google Scholar 

  14. Corey L, Spear P G. 1986. Infections with herpes simplex viruses. N Engl J Med, 314(11): 686–691.

    PubMed  CAS  Article  Google Scholar 

  15. Dyer A P, Banfield B W, Martindale D,et al. 1997. Dextran sulfate can act as an artificial receptor to mediate a typespecific herpes simplex virus infection via glyco-protein B. J Virol, 71(1): 191–198.

    PubMed  CAS  Google Scholar 

  16. Eizuru Y. 2003. Development of new antivirals for herpes-viruses. Antivir Chem Chemother, 14(6): 299–308.

    PubMed  CAS  Google Scholar 

  17. Esko J D, Lindahl U. 2001. Molecular diversity of heparan sulfate. J Clin Invest, 108(2): 169–173.

    PubMed  CAS  Google Scholar 

  18. Feyzi E, Trybala E, Bergstrom T,et al. 1997. Structural requirement of heparan sulphate for interaction with herpes simplex virus type 1 virions and isolated glycoprotein C. J Biol Chem, 272(40): 24850–24857.

    PubMed  Article  CAS  Google Scholar 

  19. Friedman H M, Cohen G H, Eisenberg R J,et al. 1984. Glycoprotein C of herpes simplex virus type 1 acts as a receptor for C3b component of complement on infected cells. Nature, 309(5969): 633–635.

    PubMed  Article  CAS  Google Scholar 

  20. Geraghty R J, Krummenacher C, Cohen G H,et al. 1998. Entry of alphaherpesviruses mediated by poliovirus receptor-related protein 1 and poliovirus receptor. Science, 280(5369): 1618–1620.

    PubMed  Article  CAS  Google Scholar 

  21. Hasegawa K, Motsuchi W, Tanaka S,et al. 1994. Inhibition with lactoferrin of in vitro infection with human herpes virus. Jpn J Med Sci Biol, 47(2): 73–85.

    PubMed  CAS  Google Scholar 

  22. Hayashi T, Hayashi K, Maeda M,et al. 1996. Calcium spirulan, an inhibitor of enveloped virus replication, from a blue-green alga Spirulina platensis. J Nat Prod, 59(1): 83–87.

    PubMed  Article  CAS  Google Scholar 

  23. Herold B C, Gerber S I, Polonsky T,et al. 1995. Identification of structural features of heparin required for inhibition of herpes simplex virus type 1 binding. Virology, 206(2): 1108–1116.

    PubMed  Article  CAS  Google Scholar 

  24. Herold B C, Siston A, Bremer J,et al. 1997. Sulfated carbohydrate compounds prevent microbial adherence by sexually transmitted disease pathogens. Antimicrob. Agents Chemother, 41(12): 2776–2780.

    PubMed  CAS  Google Scholar 

  25. Herold B C, Visalli R J, Susmarski N,et al. 1994. Glycoprotein C-independent binding of herpes simplex virus to cells requires cell surface heparan sulphate and glycoprotein B. J Gen Virol, 75(Pt 6): 1211–1222.

    PubMed  Article  CAS  Google Scholar 

  26. Herold B C, WuDunn D, Soltys N,et al. 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(3): 1090–1098.

    PubMed  CAS  Google Scholar 

  27. Hutton R D, Ewert D L, French G R. 1973. Differentiation of types 1 and 2 of herpes simplex virus by plaque inhibition with sulfated polyanions. Proc Soc Exp Biol Med, 142(1): 27–29.

    PubMed  CAS  Google Scholar 

  28. Gerber S I, Belval B J, Herold B C. 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(1): 29–39.

    PubMed  Article  CAS  Google Scholar 

  29. Giroglou T, Florin L, Schafer F,et al. 2001. Human papillomavirus infection requires cell surface heparan sulfate. J Virol, 75(3): 1565–1570.

    PubMed  Article  CAS  Google Scholar 

  30. Gruenheid S, Gatzke L, Meadows H,et al. 1993. Herpes simplex virus infection and propagation in a mouse L cell mutant lacking heparan sulfate proteoglycans. J Virol, 67(1): 93–100.

    PubMed  CAS  Google Scholar 

  31. Jacquet A, Haumont M, Chellun D,et al. 1998. The varicella zoster virus glycoprotein B (gB) plays a role in virus binding to cell surface heparan sulfate proteoglycans. Virus Res, 53(2): 197–207.

    PubMed  Article  CAS  Google Scholar 

  32. Jenssen H. 2005. Anti herpes simplex virus activity of lactoferrin/lactoferricin-an example of antiviral activity of antimicrobial protein/peptide. Cell Mol Life Sci, 62(24): 3002–3013.

    PubMed  Article  CAS  Google Scholar 

  33. Jenssen H, Andersen J H, Mantzilas D,et al. 2004. A wide range of medium-sized, highly cationic, alpha-helical peptides show antiviral activity against herpes simplex virus. Antiviral Res, 64(2): 119–126.

    PubMed  CAS  Google Scholar 

  34. Jenssen H, Andersen J H, Uhlin-Hansen L,et al. 2004. Anti-HSV activity of lactoferricin analogues is only partly related to their affinity for heparan sulfate. Antiviral Res, 61(2): 101–109.

    PubMed  Article  CAS  Google Scholar 

  35. Jenssen H, Hamill P, Hancock R E. 2006. Peptide antimicrobial agents. Clin Microbiol Rev, 19(3): 491–511.

    PubMed  Article  CAS  Google Scholar 

  36. Jenssen H, Sandvik K, Andersen J H,et al. 2008. Inhibition of HSV cell-to-cell spread by lactoferrin and lactoferricin. Antiviral Res, 79(3): 192–198.

    PubMed  Article  CAS  Google Scholar 

  37. Inatani M, Irie F, Plump A S,et al. 2003. Mammalian brain morphogenesis and midline axon guidance require heparan sulfate. Science, 302(5647): 1044–1046.

    PubMed  Article  CAS  Google Scholar 

  38. Kwon H, Bai Q, Baek H J,et al. 2006. Soluble V domain of Nectin-1/HveC enables entry of herpes simplex virus type 1 (HSV-1) into HSV-resistant cells by binding to viral glycoprotein D. J Virol, 80(1): 138–148.

    PubMed  Article  CAS  Google Scholar 

  39. Langeland N, Holmsen H, Lillehaug J R,et al. 1987. Evidence that neomycin inhibits binding of herpes simplex virus type 1 to the cellular receptor. J Virol, 61(11): 3388–3393.

    PubMed  CAS  Google Scholar 

  40. Langeland N, Moore L J, Holmsen H,et al. 1998. Interaction of polylysine with the cellular receptor for herpes simplex virus type 1. J Gen Virol, 69(Pt 6): 1137–1145.

    Google Scholar 

  41. Laquerre S, Argnani R, Anderson D B,et al. 1998. Heparan sulfate proteoglycan binding by herpes simplex virus type 1 glycoproteins B and C, which differ in their contributions to virus attachment, penetration, and cell-to-cell spread. J Virol, 72(7): 6119–6130.

    PubMed  CAS  Google Scholar 

  42. Lee J B, Hayashi K, Hashimoto M,et al. 2004. Novel antiviral fucoidan from sporophyll of Undaria pinnatifida (Mekabu). Chem Pharm Bull (Tokyo), 52(9): 1091–1094.

    Article  CAS  Google Scholar 

  43. Legrand D, Pierce A, Elass E,et al. 2008. Lactoferrin structure and functions. Adv Exp Med Biol, 606: 163–194.

    PubMed  Article  Google Scholar 

  44. Liang X, Babiuk L A, Zamb T J. 1993. Mapping of heparin-binding structures on bovine herpesvirus 1 and pseudorabies virus gIII glycoproteins. Virology, 194(1): 233–243.

    PubMed  Article  CAS  Google Scholar 

  45. Lindahl U, Kusche-Gullberg M, Kjellén L. 1998. Regulated diversity of heparan sulfate. J Biol Chem, 273(39): 24979–24982.

    PubMed  Article  CAS  Google Scholar 

  46. Liu J, Shriver Z, Pope R M,et al. 2002. Characterization of a heparan sulphate octasaccharide that binds to herpes simplex viral type 1 glycoprotein D. J Biol Chem, 277(36): 33456–33467.

    PubMed  Article  CAS  Google Scholar 

  47. Liu J, Shworak N W, Sinay P,et al. 1999. Expression of heparan sulphate D glucosaminyl 3-O sulphotransferase isoforms reveals novel substrate specificities. J Biol Chem, 274(8): 5185–5192.

    PubMed  Article  CAS  Google Scholar 

  48. Lycke E, Johansson M, Svennerholm B,et al. 1991. Binding of herpes simplex virus to cellular heparan sulphate, an initial step in the adsorption process. J Gen Virol, 72(Pt 5): 1131–1137.

    PubMed  Article  CAS  Google Scholar 

  49. Marchetti M, Longhi C, Conte M P,et al. 1996. Lactoferrin inhibits herpes simplex virus type1 adsorption to Vero cells. Antiviral Res, 29(2–3): 221–231.

    PubMed  Article  CAS  Google Scholar 

  50. Marchetti M, Pisani S, Antonini G,et al. 1998. Metal complexes of bovine lactoferrin inhibit in vitro replication of herpes simplex virus type 1 and 2. Biometals, 11(2): 89–94.

    PubMed  Article  CAS  Google Scholar 

  51. Mardberg K, Trybala E, Glorioso J C,et al. 2001. Mutational analysis of the major heparan sulfate-binding domain of herpes simplex virus type 1 glycoprotein C. J Gen Virol, 82(Pt 8): 1941–1950.

    PubMed  CAS  Google Scholar 

  52. McKeehan W L, Wu X, Kan M. 1999. Requirement for anticoagulant heparan sulfate in the fibroblast growth factor receptor complex. J Biol Chem, 274(31): 21511–21514.

    PubMed  Article  CAS  Google Scholar 

  53. Montgomery R I, Warner M S, Lum B J,et al. 1996. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell, 87(3): 427–436.

    PubMed  Article  CAS  Google Scholar 

  54. Nahmias A J, Kibrick S. 1964. Inhibitory effect of heparin on herpes simplex virus. J Bacteriol, 87(5): 1060–1066.

    PubMed  CAS  Google Scholar 

  55. Neyts J, Snoeck R, Schols D,et al. 1992. Sulfated polymers inhibit the interaction of human cytomegalovirus with cell surface heparan sulfate. Virology, 189(1): 48–58.

    PubMed  Article  CAS  Google Scholar 

  56. Nicola A V, McEvoy A M, Straus S E. 2003. Roles for endocytosis and low pH in herpes simplex virus entry into HeLa and Chinese hamster ovary cells. J Virol, 77(9): 5324–5332.

    PubMed  Article  CAS  Google Scholar 

  57. Nyberg K, Ekblad M, Bergstrom T,et al. 2004. The low molecular weight heparan sulfate-mimetic, PI-88, inhibits cell-to-cell spread of herpes simplex virus. Antiviral Res, 63(1): 15–24.

    PubMed  Article  CAS  Google Scholar 

  58. O’Donnell C D, Tiwari V, Oh M J,et al. 2006. A role for heparan sulfate 3-O sulfotransferase isoform 2 in herpes simplex virus type 1 entry and spread. Virology, 346(2): 452–459.

    PubMed  Article  CAS  Google Scholar 

  59. Pertel P E, Fridberg A, Parish M L,et al. 2001. Cell fusion induced by herpes simplex virus glycoproteins gB, gD, and gH-gL requires a gD receptor but not necessarily heparan sulfate. Virology, 279(1): 313–324.

    PubMed  Article  CAS  Google Scholar 

  60. Ponce N M, Pujol C A, Damonte E B,et al. 2003. Fucoidans from the brown seaweed Adenocystis utricularis: extraction methods, antiviral activity and structural studies. Carbohydr Res, 338(2): 153–165.

    PubMed  Article  CAS  Google Scholar 

  61. Preeprame S, Hayashi K, Lee J,et al. 2001. A novel antivirally active fucan sulfate derived from an edible brown alga, Sargassum horneri. Chem Pharm Bull (Tokyo), 49(4): 484–485.

    Article  CAS  Google Scholar 

  62. Raghuraman A, Tiwari V, Zhao Q,et al. 2007. Viral inhibition studies on sulfated lignin, a chemically modified biopolymer and a potential mimic of heparan sulfate. Biomacromolecules, 8(5): 1759–1763.

    PubMed  Article  CAS  Google Scholar 

  63. Rosenberg R D, Shworak N W, Liu J,et al. 1997. Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated? J Clin Invest, 99(9): 2062–2070.

    PubMed  Article  CAS  Google Scholar 

  64. Scanlan P M, Tiwari V, Bommireddy S,et al. 2005. Spinoculation of heparan sulfate deficient cells enhances HSV-1 entry, but does not abolish the need for essential glycoproteins in viral fusion. J Virol Methods, 128(1–2): 104–112.

    PubMed  Article  CAS  Google Scholar 

  65. Shieh M T, WuDunn D, Montgomery R I,et al. 1992. Cell surface receptors for herpes simplex virus are heparan sulphate proteoglycans. J Cell Biol, 116(5): 1273–1281.

    PubMed  Article  CAS  Google Scholar 

  66. Shukla D, Liu J, Blaiklock P,et al. 1999. A novel role for 3-O-sulfated heparan sulfate in herpes simplex virus 1 entry. Cell, 99(1): 13–22.

    PubMed  Article  CAS  Google Scholar 

  67. Shukla D, Spear P G. 2001. Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J Clin Invest, 108(4): 503–510.

    PubMed  CAS  Google Scholar 

  68. Shworak N W, Liu J, Petros L M,et al. 1999. Multiple isoforms of heparan sulfate D glucosaminyl 3-O-sulfotrans-ferase. Isolation, characterization, and expression of human cDNAs and identification of distinct genomic loci. J Biol Chem, 274(8): 5170–5184.

    PubMed  Article  CAS  Google Scholar 

  69. Shworak N W, HajMohammadi S, de Agostini A I,et al. 2002. Mice deficient in heparan sulfate 3-O-sulfotrans-ferase-1: normal hemostasis with unexpected perinatal phenotypes. Glycoconj J, 19(4–5): 355–361.

    PubMed  Article  CAS  Google Scholar 

  70. Skrincosky D, Hocknell P, Whetter L,et al. 2000. Identification and analysis of a novel heparin-binding glycoprotein encoded by human herpesvirus 7. J Virol, 74(10): 4530–4540.

    PubMed  Article  CAS  Google Scholar 

  71. Spear P G, Longnecker R. 2003. Herpesvirus entry: an update. J Virol, 77(19): 10179–10185.

    PubMed  Article  CAS  Google Scholar 

  72. Spear P G, Shieh M T, Herold B C,et al. 1992. Heparan sulfate glycosaminoglycans as primary cell surface receptors for herpes simplex virus. Adv Exp Med Biol, 313: 341–353.

    PubMed  CAS  Google Scholar 

  73. Svennerholm B, Jeansson S, Vahlne A,et al. 1991. Involvement of glycoprotein C (gC) in adsorption of herpes simplex virus type 1 (HSV-1) to the cell. Arch Virol, 120(3–4): 273–279.

    PubMed  Article  CAS  Google Scholar 

  74. Tal-Singer R, Peng C, Ponce De Leon M,et al. 1995. Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. J Virol, 69(7): 4471–4483.

    PubMed  CAS  Google Scholar 

  75. Tiwari V, Clement C, Duncan M B,et al. 2004. A role for 3-O-sulphated heparan sulphate in cell fusion induced by herpes simplex virus type 1. J Gen Virol, 85(Pt 4): 805–809.

    PubMed  Article  CAS  Google Scholar 

  76. Tiwari V, O’Donnell C D, Oh M J,et al. 2005. A role for 3-O-sulfotransferase isoform-4 in assisting HSV-1 entry and spread. Biochem Biophys Res Commun, 338(2): 930–937.

    PubMed  Article  CAS  Google Scholar 

  77. Tiwari V, O’Donnell, C, Copeland R J,et al. 2007. Soluble 3-O-sulfated heparan sulfate can trigger herpes simplex virus type 1 entry into resistant Chinese hamster ovary (CHO-K1) cells. J Gen Virol, 88:1075–1079.

    PubMed  Article  CAS  Google Scholar 

  78. Tiwari V, ten Dam G B, Yue B Y,et al. 2007. Role of 3-O-sulfated heparan sulfate in virus-induced polykary-ocyte formation. FEBS Lett, 581(23): 4468–4472.

    PubMed  Article  CAS  Google Scholar 

  79. Trybala E, Bergstrom T, Svennerholm B,et al. 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( Pt 4): 743–752.

    PubMed  Article  CAS  Google Scholar 

  80. Trybala E, Bergstrom T, Spillmann D,et al. 1998. Interaction between pseudorabies virus and heparin/heparan sulfate. Pseudorabies virus mutants differ in their interaction with heparin/heparan sulfate when altered for specific glycoprotein C heparin-binding domain. J Biol Chem, 273(9): 5047–5052.

    PubMed  Article  CAS  Google Scholar 

  81. Trybala E, Liljeqvist J A, Svennerholm B,et al. 2000. Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. J Virol, 74(19): 9106–9114.

    PubMed  Article  CAS  Google Scholar 

  82. Trybala E, Olofsson S, Mardberg K,et al. 2004. Structural and functional features of the polycationic peptide required for inhibition of herpes simplex virus invasion of cells. Antiviral Res, 62(3): 125–134.

    PubMed  Article  CAS  Google Scholar 

  83. Tyagi M, Rusnati M, Presta M,et al. 2001. Internali-zation of HIV-1 Tat requires cell surface heparan sulfate proteoglycans. J Biol Chem, 276(5): 3254–3261.

    PubMed  Article  CAS  Google Scholar 

  84. Vanderplasschen A, Bublot, M, Dubuisson J,et al. 1993. Attachment of the gammaherpesvirus bovine herpesvirus 4 is mediated by the interaction of gp8 glycoprotein with heparinlike moieties on the cell surface. Virology, 196(1): 232–240.

    PubMed  Article  CAS  Google Scholar 

  85. Wang F Z, Akula S M, Pramod N P,et al. 2001. Human herpesvirus 8 envelope glycoprotein K8.1 A interaction with the target cells involves heparan sulfate. J Virol, 75(16): 7517–7527.

    PubMed  Article  CAS  Google Scholar 

  86. WuDunn D, Spear P G. 1989. Initial interaction of herpes simplex virus with cells is binding to heparan sulphate. J Virol, 63(1): 52–58.

    PubMed  CAS  Google Scholar 

  87. Xia G, Chen J, Tiwari V,et al. 2002. Heparan sulfate 3-O-sulfotransferase isoform 5 generates both an anti-thrombin-binding site and an entry receptor for herpes simplex virus, type 1. J Biol Chem, 277(40): 37912–37919.

    PubMed  Article  CAS  Google Scholar 

  88. Xu D, Moon A, Song D,et al. 2008. Engineering sulfotransferases to modify heparan sulfate. Nat Chem Biol, 4(3): 200–202.

    PubMed  Article  CAS  Google Scholar 

  89. Xu D, Tiwari V, Xia G,et al. 2005. Characterization of heparan sulphate 3-O sulphotransferase isoform 6 and its role in assisting the entry of herpes simplex virus type 1. Biochem J, 385(Pt 2): 451–459.

    PubMed  CAS  Google Scholar 

  90. Yabe T, Shukla D, Spear P G,et al. 2001. Portable sulphotransferase domain determines sequence specificity of heparan sulphate 3-O-sulphotransferases. Biochem J, 359(Pt 1): 235–241.

    PubMed  Article  CAS  Google Scholar 

  91. Yamaguchi Y. 2001. Heparan sulfate proteoglycans in the nervous system: their diverse roles in neurogenesis, axon guidance, and synaptogenesis. Semin Cell Dev Biol, 12: 99–106.

    PubMed  Article  CAS  Google Scholar 

  92. Yoon M, Zago A, Shukla D,et al. 2003. Mutations in the N-termini of herpes simplex virus type 1 and 2 gDs alter functional interactions with the entry/fusion receptors HVEM, Nectin-2, and 3-O-sulphated heparan sulphate but not with Nectin-1. J Virol, 77(17): 9221–9231.

    PubMed  Article  CAS  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Microbiology and Immunology, College of Medicine, University of Illinois at Chicago, Chicago, IL, 60612, USA

    Christopher D. O’Donnell & Deepak Shukla

  2. Department of Ophthalmology and Visual Sciences, College of Medicine, University of Illinois at Chicago, Chicago, IL, 60612, USA

    Christopher D. O’Donnell & Deepak Shukla

Authors
  1. Christopher D. O’Donnell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Deepak Shukla
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Deepak Shukla.

Additional information

Foundation item: NIH grant (AI 057860 to D.S)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

O’Donnell, C.D., Shukla, D. The importance of heparan sulfate in herpesvirus infection. Virol. Sin. 23, 383–393 (2008). https://doi.org/10.1007/s12250-008-2992-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12250-008-2992-1

Key words

  • Heparan sulfate (HS)
  • Herpesviruses
  • Herpes simplex virus type-1 (HSV-1)
  • 3-O-sulfotransferases
  • Viral entry

CLC number

  • Q786