1887

Abstract

We examined a panel of monoclonal antibodies (MAbs) against bovine herpesvirus type 1 (BHV-1) glycoproteins gI, gIII and gIV for inhibition of virus attachment and interference with subsequent steps of infection. Attachment of radiolabelled virions was partially prevented by 600 to 700 µg/ml of IgM antibodies against gI and gIII and one IgG2A antibody against gIV, but not by the majority of MAbs against any of the three viral glycoproteins. Productive infection following attachment was prevented by lower concentrations of MAbs 5106 and 4807 against gI and by 0.7 to 5.5 µg/ml of all five MAbs against gIV. MAbs against gIV had almost the same activity whether added before or after BHV-1 was incubated with cells, suggesting that their principal activity is to prevent the penetration of virus through the cell membrane. The ability of polyethylene glycol to overcome neutralization by one anti-gIV MAb supported this concept, but an attempt to confirm this by direct electron microscopy failed. A bovine monospecific antiserum against gIV had approximately 10-fold more neutralizing activity against BHV-1 than did antisera against gI or gIII. Complement increased the activity of anti-gI and anti-gIII MAbs by 10- to 100-fold, but had little or no effect on neutralization by anti-gIV MAbs. Some antibodies against gI and gIV inhibited the enlargement of plaques in cell cultures. Taken together, these data suggest that MAbs against gIV are the principal agents of BHV-1 neutralization, and that these antibodies can be fully effective in areas such as the ocular and respiratory mucosae, from which complement is absent at the time of primary exposure to infection.

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1992-08-01
2022-08-13
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References

  1. Ali M., Bucher M., Ghosh H. 1987; Expression and nuclear envelope localization of biologically active fusion glycoprotein B of herpes simplex virus in mammalian cells using cloned DNA. Proceedings of the National Academy of Sciences, U.S.A. 84:5675–5679
    [Google Scholar]
  2. Babiuk L. A., L’Italien J., van Drunen Littel-van den Hurk S., Zamb T., Lawman M. J. P., Hughes G., Gifford G. A. 1987; Protection of cattle from bovine herpesvirus type 1 (BHV1) infection by immunization with individual viral glycoproteins. Virology 159:57–66
    [Google Scholar]
  3. Cai W., Gu B., Person S. 1988; Role of glycoprotein B of herpes simplex virus type 1 in viral entry and cell fusion. Journal of Virology 62:2596–2604
    [Google Scholar]
  4. Chang L. W. S., Zee Y. C., Pritchett R. F., Ardans A. A. 1986; Neutralizing monoclonal antibodies directed to infectious bovine rhinotracheitis virus. Archives of Virology 88:203–215
    [Google Scholar]
  5. Chase C. C., Carter-Allen K., Lohff C., Letchworth G. J. III 1990; Bovine cells expressing bovine herpesvirus 1 (BHV-1) glycoprotein IV resist infection by BHV-1, herpes simplex virus, and pseudorabies virus. Journal of Virology 64:4866–4872
    [Google Scholar]
  6. Collins J. K., Butcher A. C., Riegel C. A., McGrane V., Blair C. D., Teramoto Y. A., Winston S. 1984; Neutralizing determinants defined by monoclonal antibodies on polypeptides specified by bovine herpesvirus 1. Journal of Virology 52:403–409
    [Google Scholar]
  7. Cooper N. R., Nemerrow G. R. 1984; The role of antibody and complement in the control of viral infections. Journal of Investigative Dermatology 83:121s–127s
    [Google Scholar]
  8. Dimmock N. J. 1984; Mechanisms of neutralization of animal viruses. Journal of General Virology 65:1015–1022
    [Google Scholar]
  9. Dimmock N. J. 1987; Multiple mechanisms of neutralization of animal viruses. Trends in Biochemical Sciences 12:70–75
    [Google Scholar]
  10. Fitzpatrick D. R., Zamb T., Parker M. D., van Drunen Littel-van den Hurk S., Babiuk L. A. 1988; Expression of bovine herpesvirus 1 glycoproteins gI and gIII in transfected murine cells. Journal of Virology 62:4239–4248
    [Google Scholar]
  11. Fitzpatrick D. R., Babiuk L. A., Zamb T. 1989; Nucleotide sequence of bovine herpesvirus type 1 glycoprotein gIII, a structural model for gIII as a new member of the immunoglobulin superfamily, and implications for the homologous glycoproteins of other herpesviruses. Virology 173:46–57
    [Google Scholar]
  12. Fitzpatrick D. R., Zamb T. J., Babiuk L. A. 1990; Expression of bovine herpesvirus type 1 glycoprotein gI in transfected bovine cells induces spontaneous cell fusion. Journal of General Virology 71:1215–1219
    [Google Scholar]
  13. Fuller O. A., Spear P. G. 1985; Specificities of monoclonal and polyclonal antibodies that inhibit adsorption of herpes simplex virus to cells and lack of inhibition by potent neutralizing antibodies. Journal of Virology 55:475–482
    [Google Scholar]
  14. Fuller O. A., Spear P. G. 1987; Anti-glycoprotein D antibodies that permit adsorption but block infection by herpes simplex virus 1 prevent virion-cell fusion at the cell surface. Proceedings of the National Academy of Sciences, U.S.A. 84:5454–5458
    [Google Scholar]
  15. Fuller O. A., Santos R. E., Spear P. G. 1989; Neutralizing antibodies specific for glycoprotein H of herpes simplex virus permit viral attachment to cells but prevent penetration. Journal of Virology 63:3435–3443
    [Google Scholar]
  16. Gibbs E. P. J., Rweyemamu M. M. 1977; Bovine herpesviruses. Part I. Bovine herpesvirus 1. Veterinary Bulletin 47:317–342
    [Google Scholar]
  17. Gollins S. W., Porterfield J. S. 1986; A new mechanism for the neutralization of enveloped viruses by antiviral antibody. Nature, London 321:244–246
    [Google Scholar]
  18. Herold B. C., Wu Dunn 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 Virology 65:1090–1098
    [Google Scholar]
  19. Highlander S. L., Sutherland S. L., Gage P. J., Johnson D. C., Levine M., Glorioso J. C. 1987; Neutralizing monoclonal antibodies for herpes simplex virus glycoprotein D inhibit virus penetration. Journal of Virology 61:3356–3364
    [Google Scholar]
  20. Highlander S. L., Gai W., Person S., Levine M., Glorioso J. C. 1988; Monoclonal antibodies define a domain on herpes simplex virus glycoprotein B involved in virus penetration. Journal of Virology 62:1881–1888
    [Google Scholar]
  21. Ho D. D., Kaplan J. C., Rackauskas I. E., Gurney M. E. 1988; Second conserved domain of gp120 is important for HIV infectivity and antibody neutralization. Science 239:1021–1023
    [Google Scholar]
  22. Hughes G., Babiuk L. A., van Drunen littel-van den Hurk S. 1988; Functional and topographical analysis of epitopes on bovine herpesvirus type 1 glycoprotein IV. Archives of Virology 103:47–60
    [Google Scholar]
  23. Iorio R. M. 1988; Mechanisms of neutralization of animal viruses: monoclonal antibodies provide a new perspective. Microbial Pathogenesis 5:1–7
    [Google Scholar]
  24. Israel B. A., Marshall R. L., Letchworth G. J. III 1988; Epitope specificity and protective efficacy of bovine immune response to bovine herpesvirus 1 glycoprotein vaccines. Vaccine 6:349–356
    [Google Scholar]
  25. Israel B. A., Herber R., Gao Y., Letchworth G. J. 1992; Induction of a mucosal barrier to bovine herpesvirus 1 replication in cattle. Virology 188:256–264
    [Google Scholar]
  26. Johnson D. C., Burke R. L., Gregory T. 1990; Soluble forms of herpes simplex virus glycoprotein D bind to a limited number of cell surface receptors and inhibit virus entry into cells. Journal of Virology 63:2569–2576
    [Google Scholar]
  27. Kennedy-Stoskopf S., Narayan O. 1986; Neutralizing antibodies to visna lentivirus: mechanism of action and possible role in virus persistence. Journal of Virology 59:37–44
    [Google Scholar]
  28. Kühn J. E., Kramer M. D., Willenbacher W., Wieland U., Lorentzen E. U., Braun R. W. 1990; Identification of herpes simplex virus type 1 glycoproteins interacting with the cell surface. Journal of Virology 64:2491–2497
    [Google Scholar]
  29. Langeland N., Yan A. M., Marsden H. S., Cross A., Glorioso J. C., Moore L. J., Haarr L. 1990; Localization on the herpes simplex virus type 1 genome of a region encoding proteins involved in adsorption to the cellular receptor. Journal of Virology 64:1271–1277
    [Google Scholar]
  30. Liang X., Babiuk L. A., van Drunen Littel-van den Hurk S., Fitzpatrick D. R., Zamb T. J. 1991; Bovine herpesvirus 1 attachment to permissive cells is mediated by its major glycoproteins gI, gIII, and gIV. Journal of Virology 65:1124–1132
    [Google Scholar]
  31. Ligas M. W., Johnson D. C. 1988; A herpes simplex virus mutant in which glycoprotein D sequences are replaced by α-galactosidase sequences binds to but is unable to penetrate into cells. Journal of Virology 62:1486–1494
    [Google Scholar]
  32. 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
    [Google Scholar]
  33. Ludwig H. 1982; Bovine herpesviruses. In The Herpesviruses 2 pp 135–214 Edited by Roizman B. New York: Plenum Press;
    [Google Scholar]
  34. McCullough K. C. 1986; Monoclonal antibodies: implications for virology. Archives of Virology 87:1–36
    [Google Scholar]
  35. Marshall R. L., Letchworth G. J. III 1988; Passively administered neutralizing monoclonal antibodies do not protect calves against bovine herpesvirus 1 infection. Vaccine 6:343–348
    [Google Scholar]
  36. Marshall R. L., Rodriguez L. L., Letchworth G. J. III 1986; Characterization of envelope proteins of infectious bovine rhinotra-cheitis virus (bovine herpesvirus 1) by biochemical and immunological methods. Journal of Virology 57:745–753
    [Google Scholar]
  37. Marshall R. L., Israel B. A., Letchworth G. J. III 1988; Monoclonal antibody analysis of bovine herpesvirus 1 glycoprotein antigenic areas relevant to natural infection. Virology 165:338–347
    [Google Scholar]
  38. Miller G. W., Nussenzweig V. 1975; A new complement function: solubilization of antigen-antibody aggregates. Proceedings of the National Academy of Sciences, U.S.A. 72:418–422
    [Google Scholar]
  39. Minson A. C., Hodgman T. C., Digard P., Hancock D. C., Bell S. E., Buckmaster E. A. 1986; An analysis of the biological properties of monoclonal antibodies against glycoprotein D of herpes simplex virus and identification of amino acid substitutions that confer resistance to neutralization. Journal of General Virology 67:1001–1013
    [Google Scholar]
  40. Misra V., Blumenthal R. M., Babiuk L. A. 1981; Proteins specified by bovine herpesvirus 1 (infectious bovine rhinotracheitis virus). Journal of Virology 40:367–378
    [Google Scholar]
  41. Misra V., Nelson R., Smith M. 1988; Sequence of a bovine herpesvirus type-1 glycoprotein gene that is homologous to the herpes simplex gene for the glycoprotein gB. Virology 166:542–549
    [Google Scholar]
  42. Noble A. G., Lee G. T. -Y., Sprague R., Parish M. L., Spear P. G. 1983; Anti-gD monoclonal antibodies inhibit cell fusion induced by herpes simplex virus type 1. Virology 129:218–224
    [Google Scholar]
  43. Okazaki K., Honda E., Minetoma T., Kumagai T. 1986; Mechanisms of neutralization by monoclonal antibodies to different antigenic sites on the bovine herpesvirus type 1 glycoproteins. Virology 150:260–264
    [Google Scholar]
  44. Okazaki K., Honda E., Minetoma T., Kumagai T. 1987; Bovine herpesvirus type 1 gp87 mediates both attachment of virions to susceptible cells and hemagglutination. Archives of Virology 97:297–307
    [Google Scholar]
  45. Okazaki K., Matsuzaki T., Sugahara Y., Okada J., Hasebe M., Iwamura Y., Ohnishi M., Kanno T., Shimizu M., Honda E., Kono Y. 1991; BHV-1 adsorption is mediated by the interaction of glycoprotein gIII with heparinlike moiety on the cell surface. Virology 181:666–670
    [Google Scholar]
  46. Örvell C., Kristensson K. 1985; The effects of monoclonal antibodies against the hemagglutinin-neuraminidase and fusion protein on the release of Sendai virus from infected cells. Archives of Virology 86:1–15
    [Google Scholar]
  47. Para M. F., Parish M. L., Noble A. G., Spear P. G. 1985; Potent neutralizing activity associated with anti-glycoprotein D specificity among monoclonal antibodies selected for binding to herpes simplex virions. Journal of Virology 55:483–488
    [Google Scholar]
  48. Possee R. D., Schild G. C., Dimmock N. J. 1982; Studies on the mechanism of neutralization of influenza virus by antibody: evidence that neutralizing antibody (anti-haemagglutinin) inactivates influenza virus in vivo by inhibiting virion transcriptase activity. Journal of General Virology 58:373–386
    [Google Scholar]
  49. Reed L. J., Muench H. 1938; A simple method of estimating fifty percent endpoints. American Journal of Hygiene 27:493–497
    [Google Scholar]
  50. Sarmiento M., Haffey M., Spear P. G. 1979; Membrane proteins specified by herpes simplex viruses. III. Role of glycoprotein VP7 (B2) in virion infectivity. Journal of Virology 29:1149–1158
    [Google Scholar]
  51. Thomas A. A. M., Vrijsen R., Boeyé A. 1986; Relationship between poliovirus neutralization and aggregation. Journal of Virology 59:479–485
    [Google Scholar]
  52. Tikoo S. K., Fitzpatrick D. R., Babiuk L. A., Zamb T. J. 1990; Molecular cloning, sequencing, and expression of functional bovine herpesvirus 1 glycoprotein gIV in transfected bovine cells. Journal of Virology 64:5132–5142
    [Google Scholar]
  53. van Drunen Littel-van den Hurk S., Babiuk L. A. 1985a; Antigenic and immunogenic characteristics of bovine herpesvirus type-1 glycoproteins GVP 3/9 and GVP 6/11a/16, purified by immunoadsorbent chromatography. Virology 144:204–215
    [Google Scholar]
  54. van Drunen Littel-van den Hurk S., Babiuk L. A. 1985b; Effect of tunicamycin and monensin on biosynthesis, transport, and maturation of bovine herpesvirus type-1 glycoproteins. Virology 143:104–118
    [Google Scholar]
  55. van Drunen Littel-van den Hurk S., Babiuk L. A. 1986; Synthesis and processing of bovine herpesvirus 1 glycoproteins. Journal of Virology 59:401–410
    [Google Scholar]
  56. van Drunen Littel-van den Hurk S., van den Hurk J. V., Gilchrist J. E., Misra V., Babiuk L. A. 1984; Interactions of monoclonal antibodies and bovine herpesvirus type 1 (BHV1) glycoproteins: characterization of their biochemical and immunological properties. Virology 135:466–479
    [Google Scholar]
  57. van Drunen Littel-van den Hurk S., van den Hurk J. V., Babiuk L. A. 1985; Topographical analysis of bovine herpesvirus type 1 glycoproteins: use of monoclonal antibodies to identify and characterize functional epitopes. Virology 144:217–227
    [Google Scholar]
  58. Wallis C., Melnick J. L. 1971; Herpesvirus neutralization: the role of complement. Journal of Immunology 107:1235–1242
    [Google Scholar]
  59. Weiss W., Brown J. H., Cusack S., Pauson J. C., Skehel J. J., Wiley D. C. 1988; Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature, London 333:426–431
    [Google Scholar]
  60. Whitbeck J. C., Bello L. J., Lawrence W. C. 1988; Comparison of the herpesvirus 1 gI gene and the herpes simplex virus type 1 gB gene. Journal of Virology 62:3319–3327
    [Google Scholar]
  61. Wyler R., Engels M., Schwyzer M. 1989; Infectious bovine rhinotracheitis/vulvovaginitis. In Herpesvirus Diseases of Cattle, Horses and Pigs. Developments in Veterinary Virology pp. 1–72 Edited by Wittmann G. Boston: Kluwer Academic;
    [Google Scholar]
  62. Yates W. D. G. 1982; A review of infectious bovine rhinotracheitis, shipping fever pneumonia and viral-bacterial synergism in respiratory disease of cattle. Canadian Journal of Comparative Medicine 46:225–263
    [Google Scholar]
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