1887

Abstract

Binding of human respiratory syncytial virus (HRSV) to cultured cells was measured by flow cytometry. Using this assay and influenza virus as a control virus with a well-characterized receptor, a systematic search of cell surface molecules that might be implicated in HRSV binding was carried out. Treatment of cells with different enzymes or with other reagents suggested that heparin-like glycosaminoglycans (GAGs) were involved in attachment of HRSV, but not influenza virus, to host cells. This was further confirmed by a lack of binding of HRSV to CHO-K1 mutant cell lines deficient in glycosylation or GAGs biosynthesis and by an inhibition of binding after preincubation of virus with heparin and other GAGs. The degree of sulfation, more than the polysaccharide backbone of GAGs, seems to be critical for virus binding.

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2000-11-01
2019-10-20
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References

  1. Anderson, L. J., Bingham, P. & Hierholzer, J. ( 1988; ). Neutralization of respiratory syncytial virus by individual and mixtures of F and G protein monoclonal antibodies. Journal of Virology 62, 4232-4238.
    [Google Scholar]
  2. Apostolopoulos, V. & McKenzie, I. F. C. ( 1994; ). Cellular mucins: targets for immunotherapy. Critical Reviews in Immunology 14, 293-309.[CrossRef]
    [Google Scholar]
  3. Bächi, T., Deas, J. E. & Howe, C. (1997). In Virus Infection and the Cell Surface, pp. 83–128. Edited by G. Poste and G. L. Nicolson. Amsterdam: Elsevier.
  4. Bourgeois, C., Bour, J. B., Lidholt, K., Gauthray, C. & Pothier, P. ( 1998; ). Heparin-like structures on respiratory syncytial virus are involved in its infectivity in vitro. Journal of Virology 72, 7221-7227.
    [Google Scholar]
  5. Byrnes, A. P. & Griffin, D. E. ( 1998; ). Binding of Sindbis virus to cell surface heparan sulfate. Journal of Virology 72, 7349-7356.
    [Google Scholar]
  6. Chen, Y., Maguire, T., Hileman, R. E., Fromm, J. R., Esko, J. D., Linhardt, R. J. & Marks, R. M. ( 1997; ). Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nature Medicine 3, 866-871.[CrossRef]
    [Google Scholar]
  7. Collins, P. L. & Mottet, G. ( 1992; ). Oligomerization and post-translational processing of glycoprotein G of human respiratory syncytial virus: altered O-glycosylation in the presence of brefeldin A. Journal of General Virology 73, 849-863.[CrossRef]
    [Google Scholar]
  8. Collins, P. L., McIntosh, K. & Chanock, R. M. ( 1996; ). Respiratory syncytial virus. In Fields Virology, pp. 1313-1351. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia:Lippincott–Raven.
  9. Dalgleish, A. G., Beverley, P. C., Clapham, P. R., Crawford, D. H., Greaves, M. F. & Weiss, R. A. ( 1984; ). The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312, 763-767.[CrossRef]
    [Google Scholar]
  10. De Clercq, E. ( 1996; ). Perspectives for the chemotherapy of respiratory syncytial virus (RSV) infections. International Journal of Antimicrobial Agents 7, 193-202.[CrossRef]
    [Google Scholar]
  11. Doreleijers, J. F., Landegijk, J. P. M., Hard, K., Boelens, R., Rullman, J. A. C., Schaaper, W. M., van Oirschot, J. T. & Kaptein, R. ( 1996; ). Solution structure of the immunodominant region of protein G of bovine respiratory syncytial virus. Biochemistry 35, 14684-14688.[CrossRef]
    [Google Scholar]
  12. Esko, J. D., Stewart, T. E. & Taylor, W. H. ( 1985; ). Animal cell mutants defective in glycosaminoglycan biosynthesis. Proceedings of the National Academy of Sciences, USA 82, 3197-3201.[CrossRef]
    [Google Scholar]
  13. Feldman, S. A., Hendry, R. M. & Beeler, J. A. ( 1999; ). Identification of a linear heparin-binding domain for human respiratory syncytial virus attachment glycoprotein G. Journal of Virology 73, 6610-6617.
    [Google Scholar]
  14. Garcı́a-Barreno, B., Jorcano, J. L., Aukenbauer, T., López-Galı́ndez, C. & Melero, J. A. ( 1988; ). Participation of cytoskeletal intermediate filaments in the infectious cycle of human respiratory syncytial virus (RSV). Virus Research 9, 307-322.[CrossRef]
    [Google Scholar]
  15. Garcı́a-Barreno, B., Palomo, C., Peñas, C., Delgado, T., Perez-Breña, P. & Melero, J. A. ( 1989; ). Marked differences in the antigenic structure of human respiratory syncytial virus F and G glycoproteins. Journal of Virology 63, 925-932.
    [Google Scholar]
  16. Garcı́a-Beato, R., Martı́nez, I., Francı́, C., Real, F. X., Garcı́a-Barreno, B. & Melero, J. A. ( 1996; ). Host cell effect upon glycosylation and antigenicity of human respiratory syncytial virus G glycoprotein. Virology 221, 301-309.[CrossRef]
    [Google Scholar]
  17. Gromm, J. R., Hileman, R. R., Caldwell, E. E. O., Weiler, J. M. & Lindhardt, R. J. ( 1995; ). Differences in the interaction of heparin with arginine and lysine and the importance of these basic amino acids in the binding of heparin to acidic fibroblast growth factor. Archives in Biochemistry and Biophysics 323, 279-287.[CrossRef]
    [Google Scholar]
  18. Gruber, C. & Levine, S. ( 1985; ). Respiratory syncytial virus polypeptides. IV. The oligosaccharides of the glycoproteins. Journal of General Virology 66, 417-432.[CrossRef]
    [Google Scholar]
  19. Jackson, T., Ellard, F. M., Abu, G. R., Brookes, S. M., Blakemore, W. E., Corteyn, A. H., Stuart, D. I., Newman, J. W. I. & King, A. M. Q. ( 1996; ). Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. Journal of Virology 70, 5282-5287.
    [Google Scholar]
  20. Johnson, P. R., Spriggs, M. K., Olmsted, R. A. & Collins, P. L. ( 1987; ). The G glycoprotein of human respiratory syncytial viruses of subgroups A and B: extensive sequence divergence between antigenically related proteins. Proceedings of the National Academy of Sciences, USA 84, 5625-5629.[CrossRef]
    [Google Scholar]
  21. Karron, R. A., Bounagurio, D. A., Georgius, A. F., Whitehead, S. S., Adamus, J. E., Clements-Mann, M. L., Harris, D. O., Randolph, V. B., Udem, S. A., Murphy, B. R. & Sidhu, M. S. ( 1997; ). Respiratory syncytial virus (RSV) SH and G proteins are not essential for viral replication in vitro: clinical evaluation and molecular characterization of a cold-passaged, attenuated RSV subgroup B mutant. Proceedings of the National Academy of Sciences, USA 94, 13961-13966.[CrossRef]
    [Google Scholar]
  22. Kingsley, D. M., Kozarsky, K. F., Hobbie, L. & Krieger, M. ( 1986; ). Reversible defects in O-linked glycosylation and LDL receptor expression in a UDP–Gal/UDP–GalNac 4-epimerase deficient mutant. Cell 44, 749-759.[CrossRef]
    [Google Scholar]
  23. Kjellén, L. & Lindahl, U. ( 1991; ). Proteoglycans: structures and interactions. Annual Review of Biochemistry 60, 443-475.[CrossRef]
    [Google Scholar]
  24. Klatzmann, D., Champagne, E., Chamaret, S., Gruest, J., Guetard, D., Hercend, T., Gluckman, J. C. & Montagnier, L. ( 1984; ). T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature 312, 767-768.[CrossRef]
    [Google Scholar]
  25. Krusat, T. & Streckert, H.-J. ( 1997; ). Heparin-dependent attachment of respiratory syncytial virus (RSV) to host cells. Archives of Virology 12, 1247-1254.
    [Google Scholar]
  26. Lamb, R. A. & Kolakofsky, D. ( 1996; ). Paramyxoviridae: the viruses and their replication. In Fields Virology, pp. 1177-1204. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia:Lippincott–Raven.
  27. LeVine, A. M., Gwozdz, J., Stark, J., Bruno, M., Whitsett, J. & Korfhagen, T. ( 1999; ). Surfactant protein-A enhances respiratory syncytial virus clearance in vivo. Journal of Clinical Investigation 103, 1015-1021.[CrossRef]
    [Google Scholar]
  28. Levine, S., Klaiber-Franco, R. & Paradiso, P. R. ( 1987; ). Demonstration that glycoprotein G is the attachment protein of respiratory syncytial virus. Journal of General Virology 68, 2521-2524.[CrossRef]
    [Google Scholar]
  29. Leyrer, S., Bitzer, M., Lauer, U., Kramer, J. & Neubert, W. J. ( 1998; ). Sendai virus-like particles devoid of haemagglutinin-neuraminidase protein infect cells via the human asialoglycoprotein receptor. Journal of General Virology 79, 683-687.
    [Google Scholar]
  30. Lidholt, K., Weinke, J. L., Kiser, C. S., Lugemwa, F. N., Bame, K. J., Cheifetz, S., Massagué, J., Lindahl, U. & Esko, J. D. ( 1992; ). A single mutation affects both N-acetylglucosaminyltransferase and glucuronosyltransferase activities in a Chinese hamster ovary cell mutant defective in heparan sulfate biosynthesis. Proceedings of the National Academy of Sciences, USA 89, 2267-2271.[CrossRef]
    [Google Scholar]
  31. Linhardt, R. J., Turnbull, J. E., Wang, H. M., Loganathan, D. & Gallagher, J. T. ( 1990; ). Examination of the substrate specificity of heparin and heparan sulfate lyases. Biochemistry 29, 2611-2617.[CrossRef]
    [Google Scholar]
  32. López, J. A., Guillén, M., Sanchez-Fauquier, A. & Melero, J. A. ( 1986; ). An antigen-binding assay to determine the specificity of monoclonal antibodies against influenza virus and mapping of epitopes. Journal of Virological Methods 13, 255-264.[CrossRef]
    [Google Scholar]
  33. Lycke, E., Johansson, M., Svennerholm, B. & Lindahl, U. ( 1991; ). Binding of herpes simplex virus to cellular heparan sulphate, an initial step in the adsorption process. Journal of General Virology 72, 1131-1137.[CrossRef]
    [Google Scholar]
  34. Martı́nez, I. & Melero, J. A. ( 1998; ). Enhanced neutralization of human respiratory syncytial virus by mixtures of monoclonal antibodies to the attachment (G) glycoprotein. Journal of General Virology 79, 2215-2220.
    [Google Scholar]
  35. Martı́nez, I., Dopazo, J. & Melero, J. A. ( 1997; ). Antigenic structure of the human respiratory syncytial virus G glycoprotein and relevance of hypermutation events for the generation of antigenic variants. Journal of General Virology 78, 2419-2429.
    [Google Scholar]
  36. Mondor, I., Ugolini, S. & Sattentau, Q. J. ( 1998; ). Human immunodeficiency virus type 1 attachment to HeLa CD4 cells is CD4 independent and gp120 dependent and requires cell surface heparans. Journal of Virology 72, 3623-3634.
    [Google Scholar]
  37. Montgomery, R. I., Warner, M. S., Lum, B. J. & Spear, P. G. ( 1996; ). Herpes simplex virus type 1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 87, 427-436.[CrossRef]
    [Google Scholar]
  38. Patel, M., Yanagishita, M., Roderiquez, G., Bou-Habbib, D. C., Oravecz, T., Hascall, V. C. & Norcross, M. A. ( 1993; ). Cell-surface heparan sulfate proteoglycan mediates HIV-1 infection of T cell lines. AIDS Research and Human Retroviruses 9, 167-174.[CrossRef]
    [Google Scholar]
  39. Rostand, K. S. & Esko, J. D. ( 1997; ). Microbial adherence to and invasion through proteoglycans. Infection and Immunity 65, 1-8.
    [Google Scholar]
  40. Simoes, E. A. ( 1999; ). Respiratory syncytial virus infection. Lancet 354, 847-852.[CrossRef]
    [Google Scholar]
  41. Wang, K.-S., Kuhn, R. J., Strauss, E. G., Ou, S. & Strauss, J. H. ( 1992; ). High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. Journal of Virology 66, 4992-5001.
    [Google Scholar]
  42. Wertz, G. W., Collins, P. L., Huang, Y., Gruber, C., Levine, S. & Ball, L. A. ( 1985; ). Nucleotide sequence of the G protein of human respiratory syncytial virus reveals an unusual type of viral membrane protein. Proceedings of the National Academy of Sciences, USA 82, 4075-4079.[CrossRef]
    [Google Scholar]
  43. Wertz, G. W., Krieger, M. & Ball, L. A. ( 1989; ). Structure and cell surface maturation of the attachment glycoprotein of human respiratory syncytial virus in a cell line deficient in O-glycosylation. Journal of Virology 63, 4767-4776.
    [Google Scholar]
  44. WuDunn, D. & Spear, P. G. ( 1989; ). Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. Journal of Virology 63, 52-58.
    [Google Scholar]
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