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. 1986 Aug;59(2):401–410. doi: 10.1128/jvi.59.2.401-410.1986

Synthesis and processing of bovine herpesvirus 1 glycoproteins.

S van Drunen Littel-van den Hurk, L A Babiuk
PMCID: PMC253090  PMID: 2426466

Abstract

Four unique glycoproteins or glycoprotein complexes were recognized by a panel of monoclonal antibodies to bovine herpesvirus 1 (BHV-1), i.e., GVP 6/11a/16 (130,000-molecular-weight glycoprotein [130K glycoprotein]/74K/55K), GVP 7 (108K), GVP 3/9 (180K/91K), and GVP 11b (71K). The absence of any antigenic or structural relationship between GVP 11a and GVP 11b, which were previously identified as one glycoprotein, GVP 11, demonstrated that these two GVP 11 species are unique glycoproteins. GVP 3 and GVP 9 showed complete sequence homology, as shown by the identity of their antigenic determinants and by partial peptide mapping. This observation, as well as the ratio of their apparent molecular weights, indicated that GVP 3 (180K) is a dimeric form of GVP 9 (91K). GVP 6 and GVP 11a, as well as GVP 6 and GVP 16, showed at least partial sequence homology, since they shared several antigenic determinants and peptides. In addition, GVP 6, GVP 11a, and GVP 16 were derived from one primary precursor. These results, as well as the ratio of their apparent molecular weights, indicated that the GVP 6/11a/16 complex consists of two forms: one in which GVP 6 (130K) is uncleaved and the other one in which GVP 6 is cleaved and composed of GVP 11a (74K) and GVP 16 (55K), linked by disulfide bridges. An antigenically distinct precursor to each of the four BHV-1 glycoproteins or glycoprotein complexes was identified by monoclonal antibodies. These precursors, pGVP 6 (117K), pGVP 11a (62K), pGVP 7 (100K), pGVP 9 (69K), and pGVP 11b (63K) were sensitive to endo-beta-N-acetylglucosaminidase H treatment, indicating that they represent the partially glycosylated high-mannose-type intermediate forms generated by cotranslational glycosylation of the primary, unglycosylated precursors to GVP 6/11a/16, GVP 7, GVP 3/9, and GVP 11b, which were identified as having apparent molecular weights of 105,000, 90,000, 61,000, and 58,000, respectively. A new nomenclature for the BHV-1 glycoproteins, based on roman numerals, is proposed.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Babiuk L. A., Wardley R. C., Rouse B. T. Defense mechanisms against bovine herpesvirus: relationship of virus-host cell events to susceptibility to antibody-complement cell lysis. Infect Immun. 1975 Nov;12(5):958–963. doi: 10.1128/iai.12.5.958-963.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Balachandran N., Harnish D., Rawls W. E., Bacchetti S. Glycoproteins of herpes simplex virus type 2 as defined by monoclonal antibodies. J Virol. 1982 Oct;44(1):344–355. doi: 10.1128/jvi.44.1.344-355.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Balachandran N., Hutt-Fletcher L. M. Synthesis and processing of glycoprotein gG of herpes simplex virus type 2. J Virol. 1985 Jun;54(3):825–832. doi: 10.1128/jvi.54.3.825-832.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bolton D. C., Zee Y. C., Ardans A. A. Identification of envelope and nucleocapsid proteins of infectious bovine rhinotracheitis virus by SDS-polyacrylamide gel electrophoresis. Vet Microbiol. 1983 Feb;8(1):57–68. doi: 10.1016/0378-1135(83)90019-6. [DOI] [PubMed] [Google Scholar]
  5. Burnette W. N. "Western blotting": electrophoretic transfer of proteins from sodium dodecyl sulfate--polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. 1981 Apr;112(2):195–203. doi: 10.1016/0003-2697(81)90281-5. [DOI] [PubMed] [Google Scholar]
  6. Chan W. L. Protective immunization of mice with specific HSV-1 glycoproteins. Immunology. 1983 Jun;49(2):343–352. [PMC free article] [PubMed] [Google Scholar]
  7. Chantler J. K., Hudson J. B. Proteins of murine cytomegalovirus: identification of structural and nonstructural antigens in infected cells. Virology. 1978 May 1;86(1):22–36. doi: 10.1016/0042-6822(78)90004-1. [DOI] [PubMed] [Google Scholar]
  8. Dolyniuk M., Pritchett R., Kieff E. Proteins of Epstein-Barr virus. I. Analysis of the polypeptides of purified enveloped Epstein-Barr virus. J Virol. 1976 Mar;17(3):935–949. doi: 10.1128/jvi.17.3.935-949.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eberle R., Courtney R. J. Multimeric forms of herpes simplex virus type 2 glycoproteins. J Virol. 1982 Jan;41(1):348–351. doi: 10.1128/jvi.41.1.348-351.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Glorioso J. C., Smith J. W. Immune interactions with cells infected with herpes simplex virus: antibodies to radioiodinated surface antigens. J Immunol. 1977 Jan;118(1):114–121. [PubMed] [Google Scholar]
  11. Grefrath S. P., Reynolds J. A. The molecular weight of the major glycoprotein from the human erythrocyte membrane. Proc Natl Acad Sci U S A. 1974 Oct;71(10):3913–3916. doi: 10.1073/pnas.71.10.3913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grewal A. S., Carpio M., Babiuk L. A. Polymorphonuclear neutrophil-mediated antibody-dependent cell cytotoxicity of herpesvirus-infected cells: ultrastructural studies. Can J Microbiol. 1980 Apr;26(4):427–435. doi: 10.1139/m80-071. [DOI] [PubMed] [Google Scholar]
  13. Grewal A. S., Rouse B. T., Babiuk L. A. Mechanisms of resistant of herpesviruses: comparison of the effectiveness of different cell types in mediating antibody-dependent cell-mediated cytotoxicity. Infect Immun. 1977 Mar;15(3):698–703. doi: 10.1128/iai.15.3.698-703.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grose C., Edwards D. P., Friedrichs W. E., Weigle K. A., McGuire W. L. Monoclonal antibodies against three major glycoproteins of varicella-zoster virus. Infect Immun. 1983 Apr;40(1):381–388. doi: 10.1128/iai.40.1.381-388.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Grose C., Edwards D. P., Weigle K. A., Friedrichs W. E., McGuire W. L. Varicella-zoster virus-specific gp140: a highly immunogenic and disulfide-linked structural glycoprotein. Virology. 1984 Jan 15;132(1):138–146. doi: 10.1016/0042-6822(84)90098-9. [DOI] [PubMed] [Google Scholar]
  16. Grose C. The synthesis of glycoproteins in human melanoma cells infected with varicella-zoster virus. Virology. 1980 Feb;101(1):1–9. doi: 10.1016/0042-6822(80)90478-x. [DOI] [PubMed] [Google Scholar]
  17. Hampl H., Ben-Porat T., Ehrlicher L., Habermehl K. O., Kaplan A. S. Characterization of the envelope proteins of pseudorabies virus. J Virol. 1984 Nov;52(2):583–590. doi: 10.1128/jvi.52.2.583-590.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hardwick J. M., Bussell R. H. Glycoproteins of measles virus under reducing and nonreducing conditions. J Virol. 1978 Feb;25(2):687–692. doi: 10.1128/jvi.25.2.687-692.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hubbard S. C., Ivatt R. J. Synthesis and processing of asparagine-linked oligosaccharides. Annu Rev Biochem. 1981;50:555–583. doi: 10.1146/annurev.bi.50.070181.003011. [DOI] [PubMed] [Google Scholar]
  20. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  21. Laver W. G. Separation of two polypeptide chains from the hemagglutinin subunit of influenza virus. Virology. 1971 Jul;45(1):275–288. doi: 10.1016/0042-6822(71)90134-6. [DOI] [PubMed] [Google Scholar]
  22. Lischwe M. A., Ochs D. A new method for partial peptide mapping using N-chlorosuccinimide/urea and peptide silver staining in sodium dodecyl sulfate-polyacrylamide gels. Anal Biochem. 1982 Dec;127(2):453–457. doi: 10.1016/0003-2697(82)90203-2. [DOI] [PubMed] [Google Scholar]
  23. Manservigi R., Spear P. G., Buchan A. Cell fusion induced by herpes simplex virus is promoted and suppressed by different viral glycoproteins. Proc Natl Acad Sci U S A. 1977 Sep;74(9):3913–3917. doi: 10.1073/pnas.74.9.3913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Misra V., Blumenthal R. M., Babiuk L. A. Proteins Specified by bovine herpesvirus 1 (infectious bovine rhinotracheitis virus). J Virol. 1981 Nov;40(2):367–378. doi: 10.1128/jvi.40.2.367-378.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Misra V., Gilchrist J. E., Weinmaster G., Qualtiere L., Van den Hurk S., Babiuk L. A. Herpesvirus-induced "early" glycoprotein: characterization and possible role in immune cytolysis. J Virol. 1982 Sep;43(3):1046–1054. doi: 10.1128/jvi.43.3.1046-1054.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Montalvo E. A., Parmley R. T., Grose C. Structural analysis of the varicella-zoster virus gp98-gp62 complex: posttranslational addition of N-linked and O-linked oligosaccharide moieties. J Virol. 1985 Mar;53(3):761–770. doi: 10.1128/jvi.53.3.761-770.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Norrild B., Shore S. L., Cromeans T. L., Nahmias A. J. Participation of three major glycoprotein antigens of herpes simplex virus type 1 early in the infectious cycle as determined by antibody-dependent cell-mediated cytotoxicity. Infect Immun. 1980 Apr;28(1):38–44. doi: 10.1128/iai.28.1.38-44.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Norrild B., Shore S. L., Nahmias A. J. Herpes simplex virus glycoproteins: participation of individual herpes simplex virus type 1 glycoprotein antigens in immunocytolysis and their correlation with previously identified glycopolypeptides. J Virol. 1979 Dec;32(3):741–748. doi: 10.1128/jvi.32.3.741-748.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Olshevsky U., Becker Y. Surface glycopeptides in the envelope of herpes simplex virions. Virology. 1972 Oct;50(1):277–279. doi: 10.1016/0042-6822(72)90371-6. [DOI] [PubMed] [Google Scholar]
  30. Ozawa M., Asano A., Okada Y. Importance of interpeptide disulfide bond in a viral glycoprotein with hemagglutination and neuraminidase activities. FEBS Lett. 1976 Nov;70(1):145–149. doi: 10.1016/0014-5793(76)80745-4. [DOI] [PubMed] [Google Scholar]
  31. Pereira L., Dondero D., Roizman B. Herpes simplex virus glycoprotein gA/B: evidence that the infected Vero cell products comap and arise by proteolysis. J Virol. 1982 Oct;44(1):88–97. doi: 10.1128/jvi.44.1.88-97.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Pereira L., Hoffman M., Gallo D., Cremer N. Monoclonal antibodies to human cytomegalovirus: three surface membrane proteins with unique immunological and electrophoretic properties specify cross-reactive determinants. Infect Immun. 1982 Jun;36(3):924–932. doi: 10.1128/iai.36.3.924-932.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pereira L., Klassen T., Baringer J. R. Type-common and type-specific monoclonal antibody to herpes simplex virus type 1. Infect Immun. 1980 Aug;29(2):724–732. doi: 10.1128/iai.29.2.724-732.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Roizman B., Spear P. G. Herpesvirus antigens on cell membranes detected by centrifugation of membrane-antibody complexes. Science. 1971 Jan 22;171(3968):298–300. doi: 10.1126/science.171.3968.298. [DOI] [PubMed] [Google Scholar]
  35. Rouse B. T., Babiuk L. A. The direct antiviral cytotoxicity by bovine lymphocytes is not restricted by genetic incompatibility of lymphocytes and target cells. J Immunol. 1977 Feb;118(2):618–624. [PubMed] [Google Scholar]
  36. Sarmiento M., Haffey M., Spear P. G. Membrane proteins specified by herpes simplex viruses. III. Role of glycoprotein VP7(B2) in virion infectivity. J Virol. 1979 Mar;29(3):1149–1158. doi: 10.1128/jvi.29.3.1149-1158.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sarmiento M., Spear P. G. Membrane proteins specified by herpes simplex viruses. IV. Conformation of the virion glycoprotein designated VP7(B2). J Virol. 1979 Mar;29(3):1159–1167. doi: 10.1128/jvi.29.3.1159-1167.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Scheid A., Choppin P. W. Two disulfide-linked polypeptide chains constitute the active F protein of paramyxoviruses. Virology. 1977 Jul 1;80(1):54–66. doi: 10.1016/0042-6822(77)90380-4. [DOI] [PubMed] [Google Scholar]
  39. Spear P. G. Glycoproteins specified by herpes simplex virus type 1: their synthesis, processing and antigenic relatedness to HSV -2 glycoproteins. IARC Sci Publ. 1975;(11 Pt 1):49–61. [PubMed] [Google Scholar]
  40. Spear P. G. Membrane proteins specified by herpes simplex viruses. I. Identification of four glycoprotein precursors and their products in type 1-infected cells. J Virol. 1976 Mar;17(3):991–1008. doi: 10.1128/jvi.17.3.991-1008.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Spear P. G., Roizman B. Proteins specified by herpes simplex virus. V. Purification and structural proteins of the herpesvirion. J Virol. 1972 Jan;9(1):143–159. doi: 10.1128/jvi.9.1.143-159.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Stevely W. S. Virus-induced proteins in pseudorabies-infected cells. II. Proteins of the virion and nucleocapsid. J Virol. 1975 Oct;16(4):944–950. doi: 10.1128/jvi.16.4.944-950.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Stinski M. F. Human cytomegalovirus: glycoproteins associated with virions and dense bodies. J Virol. 1976 Aug;19(2):594–609. doi: 10.1128/jvi.19.2.594-609.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Stinski M. F. Synthesis of proteins and glycoproteins in cells infected with human cytomegalovirus. J Virol. 1977 Sep;23(3):751–767. doi: 10.1128/jvi.23.3.751-767.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Strnad B. C., Schuster T., Klein R., Hopkins R. F., 3rd, Witmer T., Neubauer R. H., Rabin H. Production and characterization of monoclonal antibodies against the Epstein-Barr virus membrane antigen. J Virol. 1982 Jan;41(1):258–264. doi: 10.1128/jvi.41.1.258-264.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Strnad B. C., Schuster T., Klein R., Neubauer R. H. Biochemical characterization of Epstein-Barr virus membrane antigen associated glycoproteins. Biochem Biophys Res Commun. 1981 Feb 27;98(4):1121–1127. doi: 10.1016/0006-291x(81)91227-4. [DOI] [PubMed] [Google Scholar]
  47. Waechter C. J., Lennarz W. J. The role of polyprenol-linked sugars in glycoprotein synthesis. Annu Rev Biochem. 1976;45:95–112. doi: 10.1146/annurev.bi.45.070176.000523. [DOI] [PubMed] [Google Scholar]
  48. Wagh P. V., Bahl O. P. Sugar residues on proteins. CRC Crit Rev Biochem. 1981;10(4):307–377. doi: 10.3109/10409238109113602. [DOI] [PubMed] [Google Scholar]
  49. Zweerink H. J., Neff B. J. Immune response after exposure to varicella zoster virus: characterization of virus-specific antibodies and their corresponding antigens. Infect Immun. 1981 Jan;31(1):436–444. doi: 10.1128/iai.31.1.436-444.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Zweig M., Heilman C. J., Jr, Rabin H., Hampar B. Shared antigenic determinants between two distinct classes of proteins in cells infected with herpes simplex virus. J Virol. 1980 Sep;35(3):644–652. doi: 10.1128/jvi.35.3.644-652.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. van Drunen Littel-van den Hurk S., Babiuk L. A. Effect of tunicamycin and monensin on biosynthesis, transport, and maturation of bovine herpesvirus type-1 glycoproteins. Virology. 1985 May;143(1):104–118. doi: 10.1016/0042-6822(85)90100-X. [DOI] [PMC free article] [PubMed] [Google Scholar]

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