1887

Abstract

Dendritic cells (DCs) are essential for the induction of specific immune responses against invading pathogens. Herpes simplex virus (HSV) is a common human pathogen that causes painful but mild infections of the skin and mucosa, and which results in latency and recurrent infections. Of the two HSV subtypes described, HSV-1 causes mainly oral–facial lesions, whilst HSV-2 is associated with genital herpes. DCs are involved in HSV-induced immune suppression, but little is known about the molecular interactions between DCs and HSV. This study demonstrated that HSV-1 and -2 both interact with the DC-specific C-type lectin DC-SIGN. Further analyses demonstrated that DC-SIGN interacts with the HSV glycoproteins gB and gC. Binding of HSV-1 to immature DCs depended on both DC-SIGN and heparan sulfate proteoglycans. Strikingly, HSV-1 infection of DCs was almost completely inhibited by blocking antibodies against DC-SIGN. Thus, DC-SIGN is an important attachment receptor for HSV-1 on immature DCs and enhances infection of DCs . In addition, DC-SIGN captures HSV-1 for transmission to permissive target cells. These data strongly suggest that DC-SIGN is a potential target to prevent HSV infection and virus dissemination. Further studies will show whether these interactions are involved in HSV-induced immune suppression.

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2008-10-01
2020-10-24
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References

  1. Altmann F., Staudacher E., Wilson I. B., Marz L. 1999; Insect cells as hosts for the expression of recombinant glycoproteins. Glycoconj J 16:109–123 [CrossRef]
    [Google Scholar]
  2. Barreca C., O'Hare P. 2004; Suppression of herpes simplex virus 1 in MDBK cells via the interferon pathway. J Virol 78:8641–8653 [CrossRef]
    [Google Scholar]
  3. Bergstrom T., Sjogren-Jansson E., Jeansson S., Lycke E. 1992; Mapping neuroinvasiveness of the herpes simplex virus type 1 encephalitis-inducing strain 2762 by the use of monoclonal antibodies. Mol Cell Probes 6:41–49 [CrossRef]
    [Google Scholar]
  4. Burleigh L., Lozach P. Y., Schiffer C., Staropoli I., Pezo V., Porrot F., Canque B., Virelizier J. L., Arenzana-Seisdedos F., Amara A. 2006; Infection of dendritic cells (DCs), not DC-SIGN-mediated internalization of human immunodeficiency virus, is required for long-term transfer of virus to T cells. J Virol 80:2949–2957 [CrossRef]
    [Google Scholar]
  5. Cai W. Z., Person S., Warner S. C., Zhou J. H., DeLuca N. A. 1987; Linker-insertion nonsense and restriction-site deletion mutations of the gB glycoprotein gene of herpes simplex virus type 1. J Virol 61:714–721
    [Google Scholar]
  6. Cai W. H., Gu B., Person S. 1988; Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. J Virol 62:2596–2604
    [Google Scholar]
  7. Cheshenko N., Herold B. C. 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
    [Google Scholar]
  8. Coffin R. S., Thomas S. K., Thomas N. S., Lilley C. E., Pizzey A. R., Griffiths C. H., Gibb B. J., Wagstaff M. J., Inges S. J. other authors 1998; Pure populations of transduced primary human cells can be produced using GFP expressing herpes virus vectors and flow cytometry. Gene Ther 5:718–722 [CrossRef]
    [Google Scholar]
  9. de Witte L., Abt M., Schneider-Schaulies S., van Kooyk Y., Geijtenbeek T. B. 2006; Measles virus targets DC-SIGN to enhance dendritic cell infection. J Virol 80:3477–3486 [CrossRef]
    [Google Scholar]
  10. de Witte L., Bobardt M., Chatterji U., Degeest G., David G., Geijtenbeek T. B., Gallay P. 2007; Syndecan-3 is a dendritic cell-specific attachment receptor for HIV-1. Proc Natl Acad Sci U S A 104:19464–19469 [CrossRef]
    [Google Scholar]
  11. Dolan A., Jamieson F. E., Cunningham C., Barnett B. C., McGeoch D. J. 1998; The genome sequence of herpes simplex virus type 2. J Virol 72:2010–2021
    [Google Scholar]
  12. Garcia-Vallejo J. J., , van het Hof B., Robben J., van Wijk J. A., van Die I., Joziasse D. H., van Dijk W. 2004; Approach for defining endogenous reference genes in gene expression experiments. Anal Biochem 329:293–299 [CrossRef]
    [Google Scholar]
  13. Geijtenbeek T. B., van Kooyk Y. 2003; DC-SIGN: a novel HIV receptor on DCs that mediates HIV-1 transmission. Curr Top Microbiol Immunol 276:31–54
    [Google Scholar]
  14. Geijtenbeek T. B., Torensma R., van Vliet S. J., van Duijnhoven G. C., Adema G. J., van Kooyk Y., Figdor C. G. 2000; Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100:575–585 [CrossRef]
    [Google Scholar]
  15. Geijtenbeek T. B., van Duijnhoven G. C., van Vliet S. J., Krieger E., Vriend G., Figdor C. G., van Kooyk Y. 2002; Identification of different binding sites in the dendritic cell-specific receptor DC-SIGN for intercellular adhesion molecule 3 and HIV-1. J Biol Chem 277:11314–11320 [CrossRef]
    [Google Scholar]
  16. Gringhuis S. I., den Dunnen J., Litjens M., , van't Hof B., van Kooyk Y., Geijtenbeek T. B. H. 2007; C-type lectin DC-SIGN modulates toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF- κ B. Immunity 26:605–616 [CrossRef]
    [Google Scholar]
  17. Halary F., Amara A., Lortat-Jacob H., Messerle M., Delaunay T., Houlès C., Fieschi F., Arenzana-Seisdedos F., Moreau J. F., Déchanet-Merville J. 2002; Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell trans -infection. Immunity 17:653–664 [CrossRef]
    [Google Scholar]
  18. Herold B. C., WuDunn D., Soltys N., Spear P. G. 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
    [Google Scholar]
  19. Hovius J. W. R., de Jong M. A. W. P., den Dunnen J., Litjens M., van der Poll T., Gringhuis S. I., Geijtenbeek T. B. H. 2008; Salp15 binding to DC-SIGN inhibits cytokine expression by impairing both nucleosome remodeling and mRNA stabilization. PloS Pathog 4:e31 [CrossRef]
    [Google Scholar]
  20. Kruse M., Rosorius O., Kratzer F., Bevec D., Kuhnt C., Steinkasserer A., Schuler G., Hauber J. 2000a; Inhibition of CD83 cell surface expression during dendritic cell maturation by interference with nuclear export of CD83 mRNA. J Exp Med 191:1581–1590 [CrossRef]
    [Google Scholar]
  21. Kruse M., Rosorius O., Kratzer F., Stelz G., Kuhnt C., Schuler G., Hauber J., Steinkasserer A. 2000b; Mature dendritic cells infected with herpes simplex virus type 1 exhibit inhibited T-cell stimulatory capacity. J Virol 74:7127–7136 [CrossRef]
    [Google Scholar]
  22. Kummer M., Turza N. M., Muhl-Zurbes P., Lechmann M., Boutell C., Coffin R. S., Everett R. D., Steinkasserer A., Prechtel A. T. 2007; Herpes simplex virus type 1 induces CD83 degradation in mature dendritic cells with immediate-early kinetics via the cellular proteasome. J Virol 81:6326–6338 [CrossRef]
    [Google Scholar]
  23. Lekkerkerker A. N., Ludwig I. S., van Vliet S. J., van Kooyk Y., Geijtenbeek T. B. 2004; Potency of HIV-1 envelope glycoprotein gp120 antibodies to inhibit the interaction of DC-SIGN with HIV-1 gp120. Virology 329:465–476 [CrossRef]
    [Google Scholar]
  24. Little S. P., Jofre J. T., Courtney R. J., Schaffer P. A. 1981; A virion-associated glycoprotein essential for infectivity of herpes simplex virus type 1. Virology 115:149–160 [CrossRef]
    [Google Scholar]
  25. Mikloska Z., Bosnjak L., Cunningham A. L. 2001; Immature monocyte-derived dendritic cells are productively infected with herpes simplex virus type 1. J Virol 75:5958–5964 [CrossRef]
    [Google Scholar]
  26. Morrison L. A. 2004; The Toll of herpes simplex virus infection. Trends Microbiol 12:353–356 [CrossRef]
    [Google Scholar]
  27. Novak N., Peng W. M. 2005; Dancing with the enemy: the interplay of herpes simplex virus with dendritic cells. Clin Exp Immunol 142:405–410
    [Google Scholar]
  28. Nystrom K., Biller M., Grahn A., Lindh M., Larson G., Olofsson S. 2004; Real time PCR for monitoring regulation of host gene expression in herpes simplex virus type 1-infected human diploid cells. J Virol Methods 118:83–94 [CrossRef]
    [Google Scholar]
  29. Olofsson S., Khanna B., Lycke E. 1980; Altered kinetic properties of sialyl and galactosyl transferases associated with herpes simplex virus infection of GMK and BHK cells. J Gen Virol 47:1–9 [CrossRef]
    [Google Scholar]
  30. Pepose J. S., Keadle T. L., Morrison L. A. 2006; Ocular herpes simplex: changing epidemiology, emerging disease patterns, and the potential of vaccine prevention and therapy. Am J Ophthalmol 141:547–557 [CrossRef]
    [Google Scholar]
  31. Pollara G., Speidel K., Samady L., Rajpopat M., McGrath Y., Ledermann J., Coffin R. S., Katz D. R., Chain B. 2003; Herpes simplex virus infection of dendritic cells: balance among activation, inhibition, and immunity. J Infect Dis 187:165–178 [CrossRef]
    [Google Scholar]
  32. Raftery M. J., Winau F., Kaufmann S. H., Schaible U. E., Schonrich G. 2006; CD1 antigen presentation by human dendritic cells as a target for herpes simplex virus immune evasion. J Immunol 177:6207–6214 [CrossRef]
    [Google Scholar]
  33. Roizman D., Knipe D., Whitley R. 2007; Herpes simplex viruses. In Fields Virology , 5th edn. pp 2501–2601Edited by Knipe D. M., Howley D., Griffin D. E., Lamb R., Martin. Philadelphia, PA: Lippincott Williams and Wilkins;
    [Google Scholar]
  34. Salio M., Cella M., Suter M., Lanzavecchia A. 1999; Inhibition of dendritic cell maturation by herpes simplex virus. Eur J Immunol 29:3245–3253 [CrossRef]
    [Google Scholar]
  35. Sallusto F., Lanzavecchia A. 1994; Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 179:1109–1118 [CrossRef]
    [Google Scholar]
  36. Sarmiento M., Haffey M., Spear P. G. 1979; Membrane proteins specified by herpes simplex viruses. III. Role of glycoprotein VP7(B2) in virion infectivity. J Virol 29:1149–1158
    [Google Scholar]
  37. Satoh T., Arii J., Suenaga T., Wang J., Kogure A., Uehori J., Arase N., Shiratori I., Tanaka S. other authors 2008; PILR α is a herpes simplex virus-1 entry coreceptor that associates with glycoprotein B. Cell 132:935–944 [CrossRef]
    [Google Scholar]
  38. Spear P. G. 2004; Herpes simplex virus: receptors and ligands for cell entry. Cell Microbiol 6:401–410 [CrossRef]
    [Google Scholar]
  39. Taylor T. J., Brockman M. A., McNamee E. E., Knipe D. M. 2002; Herpes simplex virus. Front Biosci 7:d752–d764 [CrossRef]
    [Google Scholar]
  40. Theodoridis A. A., Prechtel A. T., Turza N. M., Zenke M., Steinkasserer A. 2007; Infection of human dendritic cells with herpes simplex virus type 1 dramatically diminishes the mRNA levels of the prostaglandin E2 receptors EP2 and EP4. Immunobiology 212:827–838
    [Google Scholar]
  41. Trybala E., Liljeqvist J. A., Svennerholm B., Bergstrom T. 2000; Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. J Virol 74:9106–9114 [CrossRef]
    [Google Scholar]
  42. van Gisbergen K. P., Aarnoudse C. A., Meijer G. A., Geijtenbeek T. B., van Kooyk Y. 2005a; Dendritic cells recognize tumor-specific glycosylation of carcinoembryonic antigen on colorectal cancer cells through dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin. Cancer Res 65:5935–5944 [CrossRef]
    [Google Scholar]
  43. van Gisbergen K. P., Ludwig I. S., Geijtenbeek T. B., van Kooyk Y. 2005b; Interactions of DC-SIGN with Mac-1 and CEACAM1 regulate contact between dendritic cells and neutrophils. FEBS Lett 579:6159–6168 [CrossRef]
    [Google Scholar]
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