Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1988 Sep;62(9):3167–3174. doi: 10.1128/jvi.62.9.3167-3174.1988

Novel glycosylation pathways of retroviral envelope proteins identified with avian reticuloendotheliosis virus.

W P Tsai 1, S Oroszlan 1
PMCID: PMC253434  PMID: 2841469

Abstract

Previously, we identified two mature glycoproteins, gp90, the surface glycoprotein, and gp20, the transmembrane protein, from avian reticuloendotheliosis virus and an avian reticuloendotheliosis virus env gene-encoded intracellular polyprotein gPr77env, but the precise relationship of gPr77env to the mature envelope proteins was not determined (W.-P. Tsai, T.D. Copeland, and S. Oroszlan, Virology 155:567-583, 1986). In the present study, using metabolic labeling of viral proteins with [35S]cysteine, radioimmunoprecipitation, and carbohydrate structure analysis, we have identified a higher-molecular-weight endo-H-resistant env gene-encoded polyprotein designated gPr115env in addition to the endo-H-sensitive gPr77env. It appears that gPr77env is the primary polyprotein precursor, modified with mannosyloligosaccharides that are processed into sialic-acid-rich extraordinarily large complex-type carbohydrates (up to 17 kilodaltons for each N-linked site) on the gp90 domain but not on the gPr22 domain. In this process, gPr77env is converted into the apparently endo-H-resistant secondary polyprotein, gPr115env, which is rapidly processed into gp90 and gPr22. The proteolytic processing which occurs only after the appearance of an endo-H resistant precursor is now clearly demonstrated for a retrovirus. Some important aspects of carbohydrate structure, including the site-specific glycosylation, as well as the intracellular location and nature of the potential enzyme involved in the proteolytic cleavage of gPr115env are discussed.

Full text

PDF
3167

Images in this article

3168Image
on p.3168
3169Image
on p.3169
3170Image
on p.3170

Selected References

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

  1. Barbacid M., Hunter E., Aaronson S. A. Avian reticuloendotheliosis viruses: evolutionary linkage with mammalian type C retroviruses. J Virol. 1979 May;30(2):508–514. doi: 10.1128/jvi.30.2.508-514.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bathurst I. C., Brennan S. O., Carrell R. W., Cousens L. S., Brake A. J., Barr P. J. Yeast KEX2 protease has the properties of a human proalbumin converting enzyme. Science. 1987 Jan 16;235(4786):348–350. doi: 10.1126/science.3541206. [DOI] [PubMed] [Google Scholar]
  3. Bauer G., Temin H. M. Specific antigenic relationships between the RNA-dependent DNA polymerases of avian reticuloendotheliosis viruses and mammalian type C retroviruses. J Virol. 1980 Apr;34(1):168–177. doi: 10.1128/jvi.34.1.168-177.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beckers C. J., Keller D. S., Balch W. E. Semi-intact cells permeable to macromolecules: use in reconstitution of protein transport from the endoplasmic reticulum to the Golgi complex. Cell. 1987 Aug 14;50(4):523–534. doi: 10.1016/0092-8674(87)90025-0. [DOI] [PubMed] [Google Scholar]
  5. Beyer T. A., Rearick J. I., Paulson J. C., Prieels J. P., Sadler J. E., Hill R. L. Biosynthesis of mammalian glycoproteins. Glycosylation pathways in the synthesis of the nonreducing terminal sequences. J Biol Chem. 1979 Dec 25;254(24):12531–12534. [PubMed] [Google Scholar]
  6. Bhavanandan V. P., Davidson E. A. Characteristics of a mucin-type sialoglycopeptide produced by B16 mouse melanoma cells. Biochem Biophys Res Commun. 1976 May 3;70(1):139–145. doi: 10.1016/0006-291x(76)91119-0. [DOI] [PubMed] [Google Scholar]
  7. Bolognesi D. P., Bauer H., Gelderblom H., Hüper G. Polypeptides of avian RNA tumor viruses. IV. Components of the viral envelope. Virology. 1972 Mar;47(3):551–566. doi: 10.1016/0042-6822(72)90545-4. [DOI] [PubMed] [Google Scholar]
  8. Bosch J. V., Schwarz R. T., Ziemiecki A., Friis R. R. Oligosaccharide modifications and the site of processing of gPr92env, the precursor for the viral glycoproteins of Rous sarcoma virus. Virology. 1982 May;119(1):122–132. doi: 10.1016/0042-6822(82)90070-8. [DOI] [PubMed] [Google Scholar]
  9. Bradac J., Hunter E. Polypeptides of Mason-Pfizer monkey virus. II. Synthesis and processing of the env gene products. Virology. 1986 Apr 30;150(2):491–502. doi: 10.1016/0042-6822(86)90313-2. [DOI] [PubMed] [Google Scholar]
  10. Charman H. P., Gilden R. V., Oroszlan S. Reticuloendotheliosis virus: detection of immunological relationship to mammalian type C retroviruses. J Virol. 1979 Mar;29(3):1221–1225. doi: 10.1128/jvi.29.3.1221-1225.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Davis G. L., Hunter E. A charged amino acid substitution within the transmembrane anchor of the Rous sarcoma virus envelope glycoprotein affects surface expression but not intracellular transport. J Cell Biol. 1987 Sep;105(3):1191–1203. doi: 10.1083/jcb.105.3.1191. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Duesberg P. H., Martin G. S., Vogt P. K. Glycoprotein components of avian and murine RNA tumor viruses. Virology. 1970 Aug;41(4):631–646. doi: 10.1016/0042-6822(70)90428-9. [DOI] [PubMed] [Google Scholar]
  13. Elbein A. D. Inhibitors of the biosynthesis and processing of N-linked oligosaccharide chains. Annu Rev Biochem. 1987;56:497–534. doi: 10.1146/annurev.bi.56.070187.002433. [DOI] [PubMed] [Google Scholar]
  14. England J. M., Bolognesi D. P., Dietzschold B., Halpern M. S. Evidence that a precursor glycoprotein is cleaved to yield the major glycoprotein of avian tumor virus. J Virol. 1977 Feb;21(2):810–814. doi: 10.1128/jvi.21.2.810-814.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Finne J., Mäkelä P. H. Cleavage of the polysialosyl units of brain glycoproteins by a bacteriophage endosialidase. Involvement of a long oligosaccharide segment in molecular interactions of polysialic acid. J Biol Chem. 1985 Jan 25;260(2):1265–1270. [PubMed] [Google Scholar]
  16. Fleissner E. Chromatographic separation and antigenic analysis of proteins of the oncornaviruses. I. Avian leukemia-sarcoma viruses. J Virol. 1971 Nov;8(5):778–785. doi: 10.1128/jvi.8.5.778-785.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Garoff H., Frischauf A. M., Simons K., Lehrach H., Delius H. Nucleotide sequence of cdna coding for Semliki Forest virus membrane glycoproteins. Nature. 1980 Nov 20;288(5788):236–241. doi: 10.1038/288236a0. [DOI] [PubMed] [Google Scholar]
  18. Geyer R., Geyer H., Hunsmann G., Schneider J., Stirm S. Separation procedure and sugar composition of oligosaccharides in the surface glycoprotein of Friend murine leukemia virus. Biochim Biophys Acta. 1982 Aug 27;717(3):491–501. doi: 10.1016/0304-4165(82)90293-8. [DOI] [PubMed] [Google Scholar]
  19. Geyer R., Geyer H., Stirm S., Hunsmann G., Schneider J., Dabrowski U., Dabrowski J. Major oligosaccharides in the glycoprotein of Friend murine leukemia virus: structure elucidation by one- and two-dimensional proton nuclear magnetic resonance and methylation analysis. Biochemistry. 1984 Nov 6;23(23):5628–5637. doi: 10.1021/bi00318a038. [DOI] [PubMed] [Google Scholar]
  20. Griffiths G., Simons K. The trans Golgi network: sorting at the exit site of the Golgi complex. Science. 1986 Oct 24;234(4775):438–443. doi: 10.1126/science.2945253. [DOI] [PubMed] [Google Scholar]
  21. Gruters R. A., Neefjes J. J., Tersmette M., de Goede R. E., Tulp A., Huisman H. G., Miedema F., Ploegh H. L. Interference with HIV-induced syncytium formation and viral infectivity by inhibitors of trimming glucosidase. Nature. 1987 Nov 5;330(6143):74–77. doi: 10.1038/330074a0. [DOI] [PubMed] [Google Scholar]
  22. Hoelzer J. D., Franklin R. B., Bose H. R., Jr Transformation by reticuloendotheliosis virus: development of a focus assay and isolation of a nontransforming virus. Virology. 1979 Feb;93(1):20–30. doi: 10.1016/0042-6822(79)90272-1. [DOI] [PubMed] [Google Scholar]
  23. Hunt L. A., Wright S. E. Rous sarcoma virus glycoproteins contain hybrid-type oligosaccharides. J Virol. 1981 Aug;39(2):646–650. doi: 10.1128/jvi.39.2.646-650.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hunter E., Bhown A. S., Bennett J. C. Amino-terminal amino acid sequence of the major structural polypeptides of avian retroviruses: sequence homology between reticuloendotheliosis virus p30 and p30s of mammalian retroviruses. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2708–2712. doi: 10.1073/pnas.75.6.2708. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hunter E., Hill E., Hardwick M., Bhown A., Schwartz D. E., Tizard R. Complete sequence of the Rous sarcoma virus env gene: identification of structural and functional regions of its product. J Virol. 1983 Jun;46(3):920–936. doi: 10.1128/jvi.46.3.920-936.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ikeda H., Hardy W., Jr, Tress E., Fleissner E. Chromatographic separation and antigenic analysis of proteins of the oncornaviruses. V. Identification of a new murine viral protein, p15(E). J Virol. 1975 Jul;16(1):53–61. doi: 10.1128/jvi.16.1.53-61.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. 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]
  29. Lamblin G., Lhermitte M., Klein A., Roussel P., Van Halbeek H., Vliegenthart J. F. Carbohydrate chains from human bronchial mucus glycoproteins: a wide spectrum of oligosaccharide structures. Biochem Soc Trans. 1984 Aug;12(4):599–600. doi: 10.1042/bst0120599. [DOI] [PubMed] [Google Scholar]
  30. Laskey R. A., Mills A. D. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography. Eur J Biochem. 1975 Aug 15;56(2):335–341. doi: 10.1111/j.1432-1033.1975.tb02238.x. [DOI] [PubMed] [Google Scholar]
  31. Leamnson R. N., Halpern M. S. Subunit structure of the glycoprotein complex of avian tumor virus. J Virol. 1976 Jun;18(3):956–968. doi: 10.1128/jvi.18.3.956-968.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Maldonado R. L., Bose H. R., Jr Group-specific antigen shared by the members of the reticuloendotheliosis virus complex. J Virol. 1976 Mar;17(3):983–990. doi: 10.1128/jvi.17.3.983-990.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Marquardt H., Gilden R. V., Oroszlan S. Envelope glycoproteins of Rauscher murine leukemia virus: isolation and chemical characterization. Biochemistry. 1977 Feb 22;16(4):710–717. doi: 10.1021/bi00623a024. [DOI] [PubMed] [Google Scholar]
  34. Mizuochi T., Amano J., Kobata A. New evidence of the substrate specificity of endo-beta-N-acetylglucosaminidase D. J Biochem. 1984 Apr;95(4):1209–1213. doi: 10.1093/oxfordjournals.jbchem.a134711. [DOI] [PubMed] [Google Scholar]
  35. Murray M. J., Kabat D. Genetic and sialylation sources of heterogeneity of the murine leukemia virus membrane envelope glycoproteins gp69/71. J Biol Chem. 1979 Feb 25;254(4):1340–1348. [PubMed] [Google Scholar]
  36. Naso R. B., Arcement L. J., Karshin W. L., Jamjoom G. A., Arlinghaus R. B. A fucose-deficient glycoprotein precursor to Rauscher leukemia virus gp69/71. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2326–2330. doi: 10.1073/pnas.73.7.2326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ng V. L., Wood T. G., Arlinghaus R. B. Processing of the env gene products of Moloney murine leukaemia virus. J Gen Virol. 1982 Apr;59(Pt 2):329–343. doi: 10.1099/0022-1317-59-2-329. [DOI] [PubMed] [Google Scholar]
  38. Oroszlan S., Barbacid M., Copeland T. D., Aaronson S. A., Gilden R. V. Chemical and Immunological characterization of the major structural protein (p28) of MMC-1, a rhesus monkey endogenous type C virus: homology with the major structural protein of avian reticuloendotheliosis virus. J Virol. 1981 Sep;39(3):845–854. doi: 10.1128/jvi.39.3.845-854.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Oroszlan S., Copeland T. D., Gilden R. V., Todaro G. J. Structural homology of the major internal proteins of endogeneous type C viruses of two distantly related species of Old World monkeys: Macaca arctoides and Colobus polykomos. Virology. 1981 Dec;115(2):262–271. doi: 10.1016/0042-6822(81)90109-4. [DOI] [PubMed] [Google Scholar]
  40. Pauli G., Rohde W., Harms E. The structure of the Rous sarcoma virus glycoprotein complex. Arch Virol. 1978;58(1):61–64. doi: 10.1007/BF01315536. [DOI] [PubMed] [Google Scholar]
  41. Pinter A., Honnen W. J. O-linked glycosylation of retroviral envelope gene products. J Virol. 1988 Mar;62(3):1016–1021. doi: 10.1128/jvi.62.3.1016-1021.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Pollack L., Atkinson P. H. Correlation of glycosylation forms with position in amino acid sequence. J Cell Biol. 1983 Aug;97(2):293–300. doi: 10.1083/jcb.97.2.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Polonoff E., Machida C. A., Kabat D. Glycosylation and intracellular transport of membrane glycoproteins encoded by murine leukemia viruses. Inhibition by amino acid analogues and by tunicamycin. J Biol Chem. 1982 Dec 10;257(23):14023–14028. [PubMed] [Google Scholar]
  44. Porter A. G., Barber C., Carey N. H., Hallewell R. A., Threlfall G., Emtage J. S. Complete nucleotide sequence of an influenza virus haemagglutinin gene from cloned DNA. Nature. 1979 Nov 29;282(5738):471–477. doi: 10.1038/282471a0. [DOI] [PubMed] [Google Scholar]
  45. Power M. D., Marx P. A., Bryant M. L., Gardner M. B., Barr P. J., Luciw P. A. Nucleotide sequence of SRV-1, a type D simian acquired immune deficiency syndrome retrovirus. Science. 1986 Mar 28;231(4745):1567–1572. doi: 10.1126/science.3006247. [DOI] [PubMed] [Google Scholar]
  46. Purchase H. G., Ludford C., Nazerian K., Cox H. W. A new group of oncogenic viruses: reticuloendotheliosis, chick syncytial, duck infectious anemia, and spleen necrosis viruses. J Natl Cancer Inst. 1973 Aug;51(2):489–499. [PubMed] [Google Scholar]
  47. Rice C. M., Lenches E. M., Eddy S. R., Shin S. J., Sheets R. L., Strauss J. H. Nucleotide sequence of yellow fever virus: implications for flavivirus gene expression and evolution. Science. 1985 Aug 23;229(4715):726–733. doi: 10.1126/science.4023707. [DOI] [PubMed] [Google Scholar]
  48. Rosner M. R., Tung J. S., Hopkins N., Robbins P. W. Relationship of GIX antigen expression to the glycosylation of murine leukemia virus glycoprotein. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6420–6424. doi: 10.1073/pnas.77.11.6420. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Shinnick T. M., Lerner R. A., Sutcliffe J. G. Nucleotide sequence of Moloney murine leukaemia virus. Nature. 1981 Oct 15;293(5833):543–548. doi: 10.1038/293543a0. [DOI] [PubMed] [Google Scholar]
  50. Snider M. D., Rogers O. C. Membrane traffic in animal cells: cellular glycoproteins return to the site of Golgi mannosidase I. J Cell Biol. 1986 Jul;103(1):265–275. doi: 10.1083/jcb.103.1.265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Sonigo P., Barker C., Hunter E., Wain-Hobson S. Nucleotide sequence of Mason-Pfizer monkey virus: an immunosuppressive D-type retrovirus. Cell. 1986 May 9;45(3):375–385. doi: 10.1016/0092-8674(86)90323-5. [DOI] [PubMed] [Google Scholar]
  52. Steiner D. F., Docherty K., Carroll R. Golgi/granule processing of peptide hormone and neuropeptide precursors: a minireview. J Cell Biochem. 1984;24(2):121–130. doi: 10.1002/jcb.240240204. [DOI] [PubMed] [Google Scholar]
  53. Tai T., Yamashita K., Ogata-Arakawa M., Koide N., Muramatsu T., Iwashita S., Inoue Y., Kobata A. Structural studies of two ovalbumin glycopeptides in relation to the endo-beta-N-acetylglucosaminidase specificity. J Biol Chem. 1975 Nov 10;250(21):8569–8575. [PubMed] [Google Scholar]
  54. Tarentino A. L., Gómez C. M., Plummer T. H., Jr Deglycosylation of asparagine-linked glycans by peptide:N-glycosidase F. Biochemistry. 1985 Aug 13;24(17):4665–4671. doi: 10.1021/bi00338a028. [DOI] [PubMed] [Google Scholar]
  55. Trimble R. B., Maley F. Optimizing hydrolysis of N-linked high-mannose oligosaccharides by endo-beta-N-acetylglucosaminidase H. Anal Biochem. 1984 Sep;141(2):515–522. doi: 10.1016/0003-2697(84)90080-0. [DOI] [PubMed] [Google Scholar]
  56. Troy F. A., Hallenbeck P. C., McCoy R. D., Vimr E. R. Detection of polysialosyl-containing glycoproteins in brain using prokaryotic-derived probes. Methods Enzymol. 1987;138:169–185. doi: 10.1016/0076-6879(87)38014-0. [DOI] [PubMed] [Google Scholar]
  57. Tsai W. P., Copeland T. D., Oroszlan S. Biosynthesis and chemical and immunological characterization of avian reticuloendotheliosis virus env gene-encoded proteins. Virology. 1986 Dec;155(2):567–583. doi: 10.1016/0042-6822(86)90217-5. [DOI] [PubMed] [Google Scholar]
  58. Tsai W. P., Copeland T. D., Oroszlan S. Purification and chemical and immunological characterization of avian reticuloendotheliosis virus gag-gene-encoded structural proteins. Virology. 1985 Jan 30;140(2):289–312. doi: 10.1016/0042-6822(85)90367-8. [DOI] [PubMed] [Google Scholar]
  59. Walker B. D., Kowalski M., Goh W. C., Kozarsky K., Krieger M., Rosen C., Rohrschneider L., Haseltine W. A., Sodroski J. Inhibition of human immunodeficiency virus syncytium formation and virus replication by castanospermine. Proc Natl Acad Sci U S A. 1987 Nov;84(22):8120–8124. doi: 10.1073/pnas.84.22.8120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Wilhelmsen K. C., Eggleton K., Temin H. M. Nucleic acid sequences of the oncogene v-rel in reticuloendotheliosis virus strain T and its cellular homolog, the proto-oncogene c-rel. J Virol. 1984 Oct;52(1):172–182. doi: 10.1128/jvi.52.1.172-182.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Wills J. W., Srinivas R. V., Hunter E. Mutations of the Rous sarcoma virus env gene that affect the transport and subcellular location of the glycoprotein products. J Cell Biol. 1984 Dec;99(6):2011–2023. doi: 10.1083/jcb.99.6.2011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Witte O. N., Tsukamoto-Adey A., Weissman I. L. Cellular maturation of oncornavirus glycoproteins: topological arrangement of precursor and product forms in cellular membranes. Virology. 1977 Feb;76(2):539–553. doi: 10.1016/0042-6822(77)90236-7. [DOI] [PubMed] [Google Scholar]
  63. Witte O. N., Wirth D. F. Structure of the murine leukemia virus envelope glycoprotein precursor. J Virol. 1979 Feb;29(2):735–743. doi: 10.1128/jvi.29.2.735-743.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES