1887

Abstract

Pseudorabies virus first attaches to cells through an interaction between the envelope glycoprotein C (gC) and the cell surface heparan sulfate (HS) that is linked to proteoglycans (HSPGs). The HS-binding domain of gC is composed of three discrete heparin-binding domains (HBDs), designated HBD1, -2 and -3 for their proximity to the amino terminus of gC. Each HBD can independently mediate virus attachment to HS, yet each also exhibits a distinct binding preference for differentially sulfated derivatives of heparin. To demonstrate this, affinity columns composed of wild-type gC or mutant gC retaining a single HBD to capture several HSPGs from cultured pig and bovine kidney cells were used. The wild-type gC column bound all of the HSPGs well and, overall, bound more than 90% of the total sample applied to the column. Columns composed of either HBD2 or -3 bound intermediate amounts (40%) of the total sample applied, while the HBD1 column bound low amounts of HSPGs. HBD2 and -3 columns did not uniformly bind all of the HSPGs from bovine kidney cells, but the same HSPGs were bound with equal efficiency on each column. Thus, despite their different preferences for sulfation patterns on HS side-chains, HBD2 and -3 appear to bind the same proteoglycan cores. These results established a hierarchy of HBD2=HBD3>HBD1 in importance for HSPG binding. These -binding results correlated with the attachment phenotype of virus strains expressing gC with a single HBD in their envelopes.

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2002-02-01
2019-10-23
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References

  1. Barkalow, F. J. B. & Schwarzbauer, J. E. ( 1991; ). Localization of the major heparin-binding site in fibronectin. Journal of Biological Chemistry 266, 7812-7818.
    [Google Scholar]
  2. Bernfield, M., Kokenyesi, R., Kato, M., Hinkes, M. T., Spring, J., Gallo, R. L. & Lose, E. J. ( 1992; ). Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annual Review of Cell Biology 8, 365-393.[CrossRef]
    [Google Scholar]
  3. Bernfield, M., Götte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J. & Zako, M. ( 1999; ). Functions of cell surface heparan sulfate proteoglycans. Annual Review of Biochemistry 68, 729-777.[CrossRef]
    [Google Scholar]
  4. Cardin, A. D. & Weintraub, H. J. R. ( 1989; ). Molecular modeling of protein–glycosaminoglycan interactions. Arteriosclerosis 9, 21-32.[CrossRef]
    [Google Scholar]
  5. Carey, D. J. ( 1997; ). Syndecans: multifunctional cell-surface co-receptors. Biochemical Journal 327, 1-16.
    [Google Scholar]
  6. David, G., van der Schueren, B., Marynen, P., Cassiman, J.-J. & van den Berghe, H. ( 1992; ). Molecular cloning of amphiglycan, a novel integral membrane heparan sulfate proteoglycan expressed by epithelial and fibroblastic cells. Journal of Cell Biology 118, 961-969.[CrossRef]
    [Google Scholar]
  7. Flynn, S. J. & Ryan, P. ( 1996; ). The receptor-binding domain of pseudorabies virus glycoprotein gC is composed of multiple discrete units that are functionally redundant. Journal of Virology 70, 1355-1364.
    [Google Scholar]
  8. Flynn, S. J., Burgett, B. L., Stein, D. S., Wilkinson, K. S. & Ryan, P. ( 1993; ). The amino-terminal one-third of pseudorabies virus glycoprotein gIII contains a functional attachment domain, but this domain is not required for the efficient penetration of Vero cells. Journal of Virology 67, 2646-2654.
    [Google Scholar]
  9. Hampl, H., Ben-Porat, T., Ehrlicher, L., Habermehl, K.-O. & Kaplan, A. S. ( 1984; ). Characterization of the envelope proteins of pseudorabies virus. Journal of Virology 52, 583-590.
    [Google Scholar]
  10. Holland, T. C., Sandri-Goldin, R. M., Holland, L. E., Marlin, S. D., Levine, M. & Glorioso, J. C. ( 1983; ). Physical mapping of the mutation in an antigenic variant of herpes simplex virus type 1 by use of an immunoreactive plaque assay. Journal of Virology 46, 649-652.
    [Google Scholar]
  11. Karger, A. & Mettenleiter, T. C. ( 1996; ). Identification of cell surface molecules that interact with pseudorabies virus. Journal of Virology 70, 2138-2145.
    [Google Scholar]
  12. 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 Virology 69, 3482-3489.
    [Google Scholar]
  13. Kim, C. W., Goldberger, O. A., Gallo, R. L. & Bernfield, M. ( 1994; ). Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns. Molecular Biology of the Cell 5, 797-805.[CrossRef]
    [Google Scholar]
  14. Klupp, B. G., Nixdorf, R. & Mettenleiter, T. C. ( 2000; ). Pseudorabies virus glycoprotein M inhibits membrane fusion. Journal of Virology 74, 6760-6768.[CrossRef]
    [Google Scholar]
  15. Lindahl, U., Kusche-Gullberg, M. & Kjellén, L. ( 1998; ). Regulated diversity of heparan sulfate. Journal of Biological Chemistry 273, 24979-24982.[CrossRef]
    [Google Scholar]
  16. Lories, V., Cassiman, J.-J., van den Berghe, H. & David, G. ( 1989; ). Multiple distinct membrane heparan sulfate proteoglycans in human lung fibroblasts. Journal of Biological Chemistry 264, 7009-7016.
    [Google Scholar]
  17. Mettenleiter, T. C. ( 1989; ). Glycoprotein gIII deletion mutants of pseudorabies virus are impaired in virus entry. Virology 171, 623-625.[CrossRef]
    [Google Scholar]
  18. Mettenleiter, T. C., Zsak, L., Zuckermann, F., Sugg, N., Kern, H. & Ben-Porat, T. ( 1990; ). Interaction of glycoprotein gIII with a cellular heparinlike substance mediates adsorption of pseudorabies virus. Journal of Virology 64, 278-286.
    [Google Scholar]
  19. Rapraeger, A. C. & Ott, V. L. ( 1998; ). Molecular interactions of the syndecan core proteins. Current Opinion in Cell Biology 10, 620-628.[CrossRef]
    [Google Scholar]
  20. Robbins, A. K., Whealy, M. E., Watson, R. J. & Enquist, L. W. ( 1986; ). Pseudorabies virus gene encoding glycoprotein gIII is not essential for growth in tissue culture. Journal of Virology 59, 635-645.
    [Google Scholar]
  21. Roizman, B. ( 1990; ). Herpesviridae: a brief introduction. In Fields Virology , pp. 1787-1793. Edited by B. N. Fields & D. M. Knipe. New York:Raven Press.
  22. Rostand, K. S. & Esko, J. D. ( 1997; ). Microbial adherence to and invasion through proteoglycans. Infection and Immunity 65, 1-8.
    [Google Scholar]
  23. Ryan, J. P., Whealy, M. E., Robbins, A. K. & Enquist, L. W. ( 1987; ). Analysis of pseudorabies virus glycoprotein gIII localization and modification by using novel infectious viral mutants carrying unique EcoRI sites. Journal of Virology 61, 2962-2972.
    [Google Scholar]
  24. Saunders, S., Jalkanen, M., O’Farrell, S. & Bernfield, M. ( 1989; ). Molecular cloning of syndecan, an integral membrane proteoglycan. Journal of Cell Biology 108, 1547-1556.[CrossRef]
    [Google Scholar]
  25. Spear, P. G., Eisenberg, R. J. & Cohen, G. H. ( 2000; ). Three classes of cell surface receptors for alphaherpesvirus entry. Virology 275, 1-8.[CrossRef]
    [Google Scholar]
  26. Trybala, E., Bergström, T., Spillmann, D., Svennerholm, B., Flynn, S. J. & Ryan, P. ( 1998; ). Interaction between pseudorabies virus and heparin/heparan sulfate. Journal of Biological Chemistry 273, 5047-5052.[CrossRef]
    [Google Scholar]
  27. Trybala, E., Liljeqvist, J.-Å., Svennerholm, B. & Bergström, T. ( 2000; ). Herpes simplex virus types 1 and 2 differ in their interaction with heparan sulfate. Journal of Virology 74, 9106-9114.[CrossRef]
    [Google Scholar]
  28. Turner, A., Bruun, B., Minson, T. & Browne, H. ( 1998; ). Glycoproteins gB, gD, and gHgL of herpes simplex virus type 1 are necessary and sufficient to mediate membrane fusion in a Cos cell transfection system. Journal of Virology 72, 873-875.
    [Google Scholar]
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