1887

Abstract

The role of glycoprotein C (gC) for binding of herpes simplex virus type 1 (HSV-1) to cell surface chondroitin sulfate (CS) and the consequences of this interaction for virus attachment and infectivity were studied. To this end, a panel of HSV-1 gC mutants, including a gC-negative (gC) variant, and mouse fibroblasts expressing either cell surface CS or heparan sulfate (HS) were used. Comparing gC-positive (gC) and gC viruses in terms of their attachment to and infection of CS-expressing cells indicated that gC was essential for both functions. Furthermore, purified gC bound efficiently to isolated CS chains. However, hypertonic NaCl disrupted this interaction more easily as compared to the binding of gC to HS. Also, native and selectively desulfated heparins were approximately 10 times more efficient at inhibiting gC binding to CS-expressing cells than binding to HS-expressing cells. Experiments with the HSV-1 gC mutants revealed that specific, positively charged and hydrophobic amino acids within the N-terminal part of the protein were responsible for efficient binding as well as infectivity in both CS- and HS-expressing cells. When the infectivity of the gC mutants in the two cell types was compared, it appeared that more residues contributed to the infection of CS-expressing cells than to infection of HS-expressing cells. Taken together, analysis of gC function in cell systems with limited expression of glycosaminoglycans revealed that gC could interact with either CS or HS and that these interactions exhibited subtle but definite differences as regards to the involved structural features of gC, ionic strength dependency as well as sensitivity to specifically desulfated heparin compounds.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-83-2-291
2002-02-01
2020-07-10
Loading full text...

Full text loading...

/deliver/fulltext/jgv/83/2/0830291a.html?itemId=/content/journal/jgv/10.1099/0022-1317-83-2-291&mimeType=html&fmt=ahah

References

  1. Akula S. M., Wang F. Z., Vieira J., Chandran B.. 2001; Human herpesvirus 8 interaction with target cells involves heparan sulfate. Virology282:245–255
    [Google Scholar]
  2. Banfield B. W., Leduc Y., Esford L., Schubert K., Tufaro F.. 1995a; Sequential isolation of proteoglycan synthesis mutants by using herpes simplex virus as a selective agent: evidence for a proteoglycan-independent virus entry pathway. Journal of Virology69:3290–3298
    [Google Scholar]
  3. Banfield B. W., Leduc Y., Esford L., Visalli R. J., Brandt C. R., Tufaro F.. 1995b; Evidence for an interaction of herpes simplex virus with chondroitin sulfate proteoglycans during infection. Virology208:531–539
    [Google Scholar]
  4. Bode-Lesniewska B., Dours-Zimmermann M. T., Odermatt B. F., Briner J., Heitz P. U., Zimmermann D. R.. 1996; Distribution of the large aggregating proteoglycan versican in adult human tissues. Journal of Histochemistry and Cytochemistry44:303–312
    [Google Scholar]
  5. Bovolenta P., Fernaud-Espinosa I.. 2000; Nervous system proteoglycans as modulators of neurite outgrowth. Progress in Neurobiology61:113–132
    [Google Scholar]
  6. Bruett L., Barber S. A., Clements J. E.. 2000; Characterization of a membrane-associated protein implicated in visna virus binding and infection. Virology271:132–141
    [Google Scholar]
  7. Feyzi E., Trybala E., Bergström T., Lindahl U., Spillmann D.. 1997; Structural requirement of heparan sulfate for interaction with herpes simplex virus type 1 virions and isolated glycoprotein C. Journal of Biological Chemistry272:24850–24857
    [Google Scholar]
  8. Griffiths A., Renfrey S., Minson T.. 1998; Glycoprotein C-deficient mutants of two strains of herpes simplex virus type 1 exhibit unaltered adsorption characteristics on polarized or non-polarized cells. Journal of General Virology79:807–812
    [Google Scholar]
  9. Gruenheid S., Gatzke L., Meadows H., Tufaro F.. 1993; Herpes simplex virus infection and propagation in a mouse L cell mutant lacking heparan sulfate proteoglycans. Journal of Virology67:93–100
    [Google Scholar]
  10. 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. Journal of Virology65:1090–1098
    [Google Scholar]
  11. Holland T. C., Homa F. L., Marlin S. D., Levine M., Glorioso J.. 1984; Herpes simplex virus type 1 glycoprotein C-negative mutants exhibit multiple phenotypes, including secretion of truncated glycoproteins. Journal of Virology52:566–574
    [Google Scholar]
  12. Hsiao J. C., Chung C. S., Chang W.. 1999; Vaccinia virus envelope D8L protein binds to cell surface chondroitin sulfate and mediates the adsorption of intracellular mature virions to cells. Journal of Virology73:8750–8761
    [Google Scholar]
  13. Huff J. C., Krueger G. G., Overall J. C., Copeland J. Jr, Spruance S. L.. 1981; The histopathologic evolution of recurrent herpes simplex labialis. Journal of American Academy of Dermatology5:550–557
    [Google Scholar]
  14. Karger A., Saalmuller A., Tufaro F., Banfield B. W., Mettenleiter T. C.. 1995; Cell surface proteoglycans are not essential for infection by pseudorabies virus. Journal of Virology69:3482–3489
    [Google Scholar]
  15. Kari B., Gehrz R.. 1992; A human cytomegalovirus glycoprotein complex designated gC-II is a major heparin-binding component of the envelope. Journal of Virology66:1761–1764
    [Google Scholar]
  16. Kolset S. O., Vuong T. T., Prydz K.. 1999; Apical secretion of chondroitin sulphate in polarized Madin–Darby canine kidney (MDCK) cells. Journal of Cell Science112:1797–1801
    [Google Scholar]
  17. Laquerre S., Argnani R., Anderson D. B., Zucchini S., Manservigi R., Glorioso J. C.. 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. Journal of Virology72:6119–6130
    [Google Scholar]
  18. Lind T., Tufaro F., McCormick C., Lindahl U., Lidholt K.. 1998; The putative tumor suppressors EXT1 and EXT2 are glycosyltransferases required for the biosynthesis of heparan sulfate. Journal of Biological Chemistry273:26265–26268
    [Google Scholar]
  19. Lyon M., Deakin J. A., Mizuno K., Nakamura T., Gallagher J. T.. 1994; Interaction of hepatocyte growth factor with heparan sulfate. Elucidation of the major heparan sulfate structural determinants. Journal of Biological Chemistry269:11216–11223
    [Google Scholar]
  20. McCormick C., Leduc Y., Martindale D., Mattison K., Esford L. E., Dyer A. P., Tufaro F.. 1998; The putative tumour suppressor EXT1 alters the expression of cell-surface heparan sulfate. Nature Genetics19:158–161
    [Google Scholar]
  21. Mårdberg K., Trybala E., Glorioso J. C., Bergström T.. 2001; Mutational analysis of the major heparan sulfate-binding domain of herpes simplex virus type 1 glycoprotein C. Journal of General Virology82:1941–1950
    [Google Scholar]
  22. Moffat J. F., Zerboni L., Kinchington P. R., Grose C., Kaneshima H., Arvin A. M.. 1998; Attenuation of the vaccine Oka strain of varicella-zoster virus and role of glycoprotein C in alphaherpesvirus virulence demonstrated in the SCID-hu mouse. Journal of Virology72:965–974
    [Google Scholar]
  23. Murdoch A. D., Liu B., Schwarting R., Tuan R. S., Iozzo R. V.. 1994; Widespread expression of perlecan proteoglycan in basement membranes and extracellular matrices of human tissues as detected by a novel monoclonal antibody against domain III and by in situ hybridization. Journal of Histochemistry and Cytochemistry42:239–249
    [Google Scholar]
  24. Petersen F., Brandt E., Lindahl U., Spillmann D.. 1999; Characterization of a neutrophil cell surface glycosaminoglycan that mediates binding of platelet factor 4. Journal of Biological Chemistry274:12376–12382
    [Google Scholar]
  25. Sears A. E., McGwire B. S., Roizman B.. 1991; Infection of polarized MDCK cells with herpes simplex virus 1: two asymmetrically distributed cell receptors interact with different viral proteins. Proceedings of the National Academy of Sciences, USA88:5087–5091
    [Google Scholar]
  26. Secchiero P., Sun D., De Vico A. L., Crowley R. W., Reitz M. S. Jr, Zauli G., Lusso P., Gallo R. C.. 1997; Role of the extracellular domain of human herpesvirus 7 glycoprotein B in virus binding to cell surface heparan sulfate proteoglycans. Journal of Virology71:4571–4580
    [Google Scholar]
  27. Sorrell J. M., Carrino D. A., Baber M. A., Asselineau D., Caplan A. I.. 1999; A monoclonal antibody which recognizes a glycosaminoglycan epitope in both dermatan sulfate and chondroitin sulfate proteoglycans of human skin. Histochemical Journal31:549–558
    [Google Scholar]
  28. Svennerholm B., Jeansson S., Vahlne A., Lycke E.. 1991; Involvement of glycoprotein C (gC) in adsorption of herpes simplex virus type 1 (HSV-1) to the cell. Archives of Virology120:273–279
    [Google Scholar]
  29. Tal-Singer R., Peng C., Ponce De Leon M., Abrams W. R., Banfield B. W., Tufaro F., Cohen G. H., Eisenberg R. J.. 1995; Interaction of herpes simplex virus glycoprotein gC with mammalian cell surface molecules. Journal of Virology69:4471–4483
    [Google Scholar]
  30. Tollefsen D. M.. 1994; The interaction of glycosaminoglycans with heparin cofactor II. Annals of the New York Academy of Sciences714:21–31
    [Google Scholar]
  31. Trybala E., Bergström T., Svennerholm B., Jeansson S., Glorioso J. C., Olofsson S.. 1994; Localization of a functional site on herpes simplex virus type 1 glycoprotein C involved in binding to cell surface heparan sulphate. Journal of General Virology75:743–752
    [Google Scholar]
  32. Trybala E., Bergström T., Spillmann D., Svennerholm B., Flynn S. J., Ryan P.. 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. Journal of Biological Chemistry273:5047–5052
    [Google Scholar]
  33. Trybala E., Liljeqvist J. A., Svennerholm B., Bergström T.. 2000; Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. Journal of Virology74:9106–9114
    [Google Scholar]
  34. WuDunn D., Spear P. G.. 1989; Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. Journal of Virology63:52–58
    [Google Scholar]
  35. Zhu Z., Gershon M. D., Gabel C., Sherman D., Ambron R., Gershon A.. 1995; Entry and egress of varicella-zoster virus: role of mannose 6-phosphate, heparan sulfate proteoglycan, and signal sequences in targeting virions and viral glycoproteins. Neurology45:S15–S17
    [Google Scholar]
  36. Zimmermann D. R., Dours-Zimmermann M. T., Schubert M., Bruckner-Tuderman L.. 1994; Versican is expressed in the proliferating zone in the epidermis and in association with the elastic network of the dermis. Journal of Cell Biology124:817–825
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-83-2-291
Loading
/content/journal/jgv/10.1099/0022-1317-83-2-291
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error