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. 1987 Sep;61(9):2877–2884. doi: 10.1128/jvi.61.9.2877-2884.1987

Assembly and processing of the disulfide-linked varicella-zoster virus glycoprotein gpII(140).

E A Montalvo, C Grose
PMCID: PMC255809  PMID: 3039175

Abstract

Varicella-zoster virus (VZV) specifies the synthesis of at least four families of glycoproteins, which have been designated gpI, gpII, gpIII, and gpIV. In this report we describe the assembly and processing of VZV gpII, a structural protein of an apparent Mr of 140,000, which is the homolog of gB of herpes simplex virus. For these studies, we used two anti-gpII monoclonal antibodies which exhibited both complement-independent neutralization activity and inhibition of virus-induced cell-to-cell fusion. Pulse-chase labeling experiments identified a 124,000-Mr intermediate which was chased to the mature 140,000-Mr product when analyzed in nonreducing gels; in the presence of a reducing agent, the native gp140 was cleaved into two closely migrating species (gp66 and gp68). The biosynthesis of VZV gpII was further analyzed in the presence of the following inhibitors of glycoprotein processing: tunicamycin, monensin, castanospermine, swainsonine, and deoxymannojirimycin. All intermediate and mature forms were digested with endoglycosidases H and F, neuraminidase, and O-glycanase to further define high-mannose, complex, and O-linked glycans. Finally, the addition of sulfate residues was investigated. This characterization of VZV gpII revealed the following results. (i) gp128 and gp124 were early high-mannose forms, (ii) gp126 was an intermediate form with complex N-linked oligosaccharides, (iii) gp130 was a later intermediate with both N-linked and O-linked glycans, and (iv) the mature product gp140 contained a mixture of N-linked and O-linked glycans which were both sialated and sulfated. Further investigations indicated that gpII sulfation was inhibited by tunicamycin and castanospermine but not by deoxymannojirimycin or swainsonine. We also concluded that VZV gpII displayed many biological and biochemical properties similar to those of its herpes simplex virus homolog gB.

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Selected References

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

  1. Bzik D. J., Debroy C., Fox B. A., Pederson N. E., Person S. The nucleotide sequence of the gB glycoprotein gene of HSV-2 and comparison with the corresponding gene of HSV-1. Virology. 1986 Dec;155(2):322–333. doi: 10.1016/0042-6822(86)90196-0. [DOI] [PubMed] [Google Scholar]
  2. Bzik D. J., Fox B. A., DeLuca N. A., Person S. Nucleotide sequence specifying the glycoprotein gene, gB, of herpes simplex virus type 1. Virology. 1984 Mar;133(2):301–314. doi: 10.1016/0042-6822(84)90397-0. [DOI] [PubMed] [Google Scholar]
  3. Davison A. J., Edson C. M., Ellis R. W., Forghani B., Gilden D., Grose C., Keller P. M., Vafai A., Wroblewska Z., Yamanishi K. New common nomenclature for glycoprotein genes of varicella-zoster virus and their glycosylated products. J Virol. 1986 Mar;57(3):1195–1197. doi: 10.1128/jvi.57.3.1195-1197.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Davison A. J., Scott J. E. The complete DNA sequence of varicella-zoster virus. J Gen Virol. 1986 Sep;67(Pt 9):1759–1816. doi: 10.1099/0022-1317-67-9-1759. [DOI] [PubMed] [Google Scholar]
  5. Eberle R., Courtney R. J. gA and gB glycoproteins of herpes simplex virus type 1: two forms of a single polypeptide. J Virol. 1980 Dec;36(3):665–675. doi: 10.1128/jvi.36.3.665-675.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Edson C. M., Hosler B. A., Poodry C. A., Schooley R. T., Waters D. J., Thorley-Lawson D. A. Varicella-zoster virus envelope glycoproteins: biochemical characterization and identification in clinical material. Virology. 1985 Aug;145(1):62–71. doi: 10.1016/0042-6822(85)90201-6. [DOI] [PubMed] [Google Scholar]
  7. Edson C. M., Hosler B. A., Respess R. A., Waters D. J., Thorley-Lawson D. A. Cross-reactivity between herpes simplex virus glycoprotein B and a 63,000-dalton varicella-zoster virus envelope glycoprotein. J Virol. 1985 Oct;56(1):333–336. doi: 10.1128/jvi.56.1.333-336.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Elbein A. D., Dorling P. R., Vosbeck K., Horisberger M. Swainsonine prevents the processing of the oligosaccharide chains of influenza virus hemagglutinin. J Biol Chem. 1982 Feb 25;257(4):1573–1576. [PubMed] [Google Scholar]
  9. Elbein A. D., Legler G., Tlusty A., McDowell W., Schwarz R. The effect of deoxymannojirimycin on the processing of the influenza viral glycoproteins. Arch Biochem Biophys. 1984 Dec;235(2):579–588. doi: 10.1016/0003-9861(84)90232-7. [DOI] [PubMed] [Google Scholar]
  10. Ellis R. W., Keller P. M., Lowe R. S., Zivin R. A. Use of a bacterial expression vector to map the varicella-zoster virus major glycoprotein gene, gC. J Virol. 1985 Jan;53(1):81–88. doi: 10.1128/jvi.53.1.81-88.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Forghani B., Dupuis K. W., Schmidt N. J. Varicella-zoster viral glycoproteins analyzed with monoclonal antibodies. J Virol. 1984 Oct;52(1):55–62. doi: 10.1128/jvi.52.1.55-62.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gong M., Ooka T., Matsuo T., Kieff E. Epstein-Barr virus glycoprotein homologous to herpes simplex virus gB. J Virol. 1987 Feb;61(2):499–508. doi: 10.1128/jvi.61.2.499-508.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Hope R. G., Palfreyman J., Suh M., Marsden H. S. Sulphated glycoproteins induced by herpes simplex virus. J Gen Virol. 1982 Feb;58(Pt 2):399–415. doi: 10.1099/0022-1317-58-2-399. [DOI] [PubMed] [Google Scholar]
  16. Hsu C. H., Kingsbury D. W. Contribution of oligosaccharide sulfation to the charge heterogeneity of a viral glycoprotein. J Biol Chem. 1982 Aug 10;257(15):9035–9038. [PubMed] [Google Scholar]
  17. Ito M., Ihara T., Grose C., Starr S. Human leukocytes kill varicella-zoster virus-infected fibroblasts in the presence of murine monoclonal antibodies to virus-specific glycoproteins. J Virol. 1985 Apr;54(1):98–103. doi: 10.1128/jvi.54.1.98-103.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Johnson D. C., Spear P. G. O-linked oligosaccharides are acquired by herpes simplex virus glycoproteins in the Golgi apparatus. Cell. 1983 Mar;32(3):987–997. doi: 10.1016/0092-8674(83)90083-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Keller P. M., Davison A. J., Lowe R. S., Bennett C. D., Ellis R. W. Identification and structure of the gene encoding gpII, a major glycoprotein of varicella-zoster virus. Virology. 1986 Jul 15;152(1):181–191. doi: 10.1016/0042-6822(86)90383-1. [DOI] [PubMed] [Google Scholar]
  20. Keller P. M., Neff B. J., Ellis R. W. Three major glycoprotein genes of varicella-zoster virus whose products have neutralization epitopes. J Virol. 1984 Oct;52(1):293–297. doi: 10.1128/jvi.52.1.293-297.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kitamura K., Namazue J., Campo-Vera H., Ogino T., Yamanishi K. Induction of neutralizing antibody against varicella-zoster virus (VZV) by VZV gp3 and cross-reactivity between VZV gp3 and herpes simplex viruses gB. Virology. 1986 Feb;149(1):74–82. doi: 10.1016/0042-6822(86)90088-7. [DOI] [PubMed] [Google Scholar]
  22. Kornfeld R., Kornfeld S. Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 1985;54:631–664. doi: 10.1146/annurev.bi.54.070185.003215. [DOI] [PubMed] [Google Scholar]
  23. Leavitt R., Schlesinger S., Kornfeld S. Tunicamycin inhibits glycosylation and multiplication of Sindbis and vesicular stomatitis viruses. J Virol. 1977 Jan;21(1):375–385. doi: 10.1128/jvi.21.1.375-385.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Montalvo E. A., Grose C. Neutralization epitope of varicella zoster virus on native viral glycoprotein gp118 (VZV glycoprotein gpIII). Virology. 1986 Mar;149(2):230–241. doi: 10.1016/0042-6822(86)90124-8. [DOI] [PubMed] [Google Scholar]
  25. Montalvo E. A., Grose C. Varicella zoster virus glycoprotein gpI is selectively phosphorylated by a virus-induced protein kinase. Proc Natl Acad Sci U S A. 1986 Dec;83(23):8967–8971. doi: 10.1073/pnas.83.23.8967. [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. Namazue J., Campo-Vera H., Kitamura K., Okuno T., Yamanishi K. Processing of virus-specific glycoproteins of varicella zoster virus. Virology. 1985 May;143(1):252–259. doi: 10.1016/0042-6822(85)90112-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pan Y. T., Hori H., Saul R., Sanford B. A., Molyneux R. J., Elbein A. D. Castanospermine inhibits the processing of the oligosaccharide portion of the influenza viral hemagglutinin. Biochemistry. 1983 Aug 2;22(16):3975–3984. doi: 10.1021/bi00285a038. [DOI] [PubMed] [Google Scholar]
  29. Pinter A., Compans R. W. Sulfated components of enveloped viruses. J Virol. 1975 Oct;16(4):859–866. doi: 10.1128/jvi.16.4.859-866.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Shiraki K., Okuno T., Yamanishi K., Takahashi M. Polypeptides of varicella-zoster virus (VZV) and immunological relationship of VZV and herpes simplex virus (HSV). J Gen Virol. 1982 Aug;61(Pt 2):255–269. doi: 10.1099/0022-1317-61-2-255. [DOI] [PubMed] [Google Scholar]
  31. Snowden B. W., Kinchington P. R., Powell K. L., Halliburton I. W. Antigenic and biochemical analysis of gB of herpes simplex virus type 1 and type 2 and of cross-reacting glycoproteins induced by bovine mammillitis virus and equine herpesvirus type 1. J Gen Virol. 1985 Feb;66(Pt 2):231–247. doi: 10.1099/0022-1317-66-2-231. [DOI] [PubMed] [Google Scholar]
  32. Weigle K. A., Grose C. Molecular dissection of the humoral immune response to individual varicella-zoster viral proteins during chickenpox, quiescence, reinfection, and reactivation. J Infect Dis. 1984 May;149(5):741–749. doi: 10.1093/infdis/149.5.741. [DOI] [PubMed] [Google Scholar]
  33. Wroblewska Z., Gilden D., Green M., Devlin M., Vafai A. Affinity-purified varicella-zoster virus glycoprotein gp1/gp3 stimulates the production of neutralizing antibody. J Gen Virol. 1985 Aug;66(Pt 8):1795–1799. doi: 10.1099/0022-1317-66-8-1795. [DOI] [PubMed] [Google Scholar]

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