Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1979 Jul;31(1):1–7. doi: 10.1128/jvi.31.1.1-7.1979

Glycopeptides of Murine Leukemia Viruses I. Comparison of Two Ecotropic Viruses

Maurice C Kemp 1, Sukla Basak 1, Richard W Compans 1
PMCID: PMC353415  PMID: 228050

Abstract

The glycopeptides obtained by pronase digestion of two ecotropic strains of murine leukemia virus (MuLV) were compared by gel filtration. Four different glycopeptide size classes, designated G1, G2, G3, and G4, with molecular weights of approximately 5,100, 2,900, 2,200, and 1,500, respectively, were shown to be associated with Rauscher MuLV virions grown in JLS-V9 cells. Various sugar precursors, including glucosamine, galactose, fucose, and mannose were incorporated into G1 and G2, suggesting that these are complex (type I) glycopeptides. The two smaller glycopeptide size classes, G3 and G4, were shown to be mannoserich (type II) glycopeptides. G4 was more sensitive to digestion with endo-β-N-acetylglucosaminidase H than G3, suggesting that the core of G3 may contain fewer mannose residues. Glycopeptides of the same size class as G1 and G2 were associated with both Rauscher MuLV and AKR-MuLV grown in III6A (mouse embryo) cells. Previous studies have shown that gp52, a proteolytic cleavage product of gp70, possessed primarily G1 glycopeptides and that gp52 was more highly sulfated than gp70. We observed that G1 is approximately twofold more highly sulfated than G2, explaining the observed difference in sulfation of gp52. The unusually large size of G1 suggested that infection with MuLV may alter the host cell glycosylation pattern. To test this possibility, glycopeptides from Sindbis virions grown in uninfected and Rauscher MuLV-infected JLS-V9 cells were compared, and no differences were observed. G1 was not detected in Sindbis virions, indicating that acquisition of G1 depends on properties of the virus-coded polypeptide backbone of the gp70 molecule.

Full text

PDF
1

Selected References

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

  1. Burge B. W., Huang A. S. Comparison of membrane protein glycopeptides of Sindbis virus and vesicular stomatitis virus. J Virol. 1970 Aug;6(2):176–182. doi: 10.1128/jvi.6.2.176-182.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burge B. W., Strauss J. H., Jr Glycopeptides of the membrane glycoprotein of Sindbis virus. J Mol Biol. 1970 Feb 14;47(3):449–466. doi: 10.1016/0022-2836(70)90314-1. [DOI] [PubMed] [Google Scholar]
  3. Choppin P. W. Replication of influenza virus in a continuous cell line: high yield of infective virus from cells inoculated at high multiplicity. Virology. 1969 Sep;39(1):130–134. doi: 10.1016/0042-6822(69)90354-7. [DOI] [PubMed] [Google Scholar]
  4. Devare S. G., Rapp U. R., Todaro G. J., Stephenson J. R. Acquisition of oncogenicity by endogenous mouse type C viruses: effects of variations in env and gag genes. J Virol. 1978 Nov;28(2):457–465. doi: 10.1128/jvi.28.2.457-465.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Elder J. H., Gautsch J. W., Jensen F. C., Lerner R. A., Hartley J. W., Rowe W. P. Biochemical evidence that MCF murine leukemia viruses are envelope (env) gene recombinants. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4676–4680. doi: 10.1073/pnas.74.10.4676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Etchison J. R., Holland J. J. Carbohydrate composition of the membrane glycoprotein of vesicular stomatitis virus grown in four mammalian cell lines. Proc Natl Acad Sci U S A. 1974 Oct;71(10):4011–4014. doi: 10.1073/pnas.71.10.4011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Etchison J. R., Robertson J. S., Summers D. F. Partial structural analysis of the oligosaccharide moieties of the vesicular stomatitis virus glycoprotein by sequential chemical and enzymatic degradation. Virology. 1977 May 15;78(2):375–392. doi: 10.1016/0042-6822(77)90115-5. [DOI] [PubMed] [Google Scholar]
  8. Famulari N. G., Jelalian K. Cell surface expression of the env gene polyprotein of dual-tropic mink cell focus-forming murine leukemia virus. J Virol. 1979 Jun;30(3):720–728. doi: 10.1128/jvi.30.3.720-728.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Forchhammer J., Turnock G. Glycoproteins from murine C-type virus are more acidic in virus derived from transformed cells than from nontransformed cells. Virology. 1978 Jul 1;88(1):177–182. doi: 10.1016/0042-6822(78)90121-6. [DOI] [PubMed] [Google Scholar]
  10. Galehouse D. M., Duesberg P. H. Glycoproteins of avian tumor virus recombinants: evidence for intragenic crossing-over. J Virol. 1978 Jan;25(1):86–96. doi: 10.1128/jvi.25.1.86-96.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hartley J. W., Rowe W. P. Clonal cells lines from a feral mouse embryo which lack host-range restrictions for murine leukemia viruses. Virology. 1975 May;65(1):128–134. doi: 10.1016/0042-6822(75)90013-6. [DOI] [PubMed] [Google Scholar]
  12. Hartley J. W., Wolford N. K., Old L. J., Rowe W. P. A new class of murine leukemia virus associated with development of spontaneous lymphomas. Proc Natl Acad Sci U S A. 1977 Feb;74(2):789–792. doi: 10.1073/pnas.74.2.789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hunt L. A., Etchison J. R., Summers D. F. Oligosaccharide chains are trimmed during synthesis of the envelope glycoprotein of vesicular stomatitis virus. Proc Natl Acad Sci U S A. 1978 Feb;75(2):754–758. doi: 10.1073/pnas.75.2.754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Keegstra K., Sefton B., Burke D. Sindbis virus glycoproteins: effect of the host cell on the oligosaccharides. J Virol. 1975 Sep;16(3):613–620. doi: 10.1128/jvi.16.3.613-620.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kemp M. C., Perdue M. L., Rogers H. W., O'Callaghan D. J., Randall C. C. Structural polypeptides of the hamster strain of equine herpes virus type 1: products associated with purification. Virology. 1974 Oct;61(2):361–375. doi: 10.1016/0042-6822(74)90274-8. [DOI] [PubMed] [Google Scholar]
  16. Kemp M. C., Wise K. S., Edlund L. E., Acton R. T., Compans R. W. Origin of the minor glycoproteins of murine leukemia viruses. J Virol. 1978 Oct;28(1):84–94. doi: 10.1128/jvi.28.1.84-94.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Krantz M. J., Strand M., August J. T. Biochemical and immunological characterization of the major envelope glycoprotein gp69/71 and degradation fragments from Rauscher leukemia virus. J Virol. 1977 Jun;22(3):804–815. doi: 10.1128/jvi.22.3.804-815.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. Lai M. M., Duesberg P. H. Differences between the envelope glycoproteins and glycopeptides of avian tumor viruses released from transformed and from nontransformed cells. Virology. 1972 Nov;50(2):359–372. doi: 10.1016/0042-6822(72)90387-x. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Mattila K., Luukkonen A., Renkonen O. Protein-bound oligosaccharides of Semliki Forest virus. Biochim Biophys Acta. 1976 Feb 6;419(3):435–444. doi: 10.1016/0005-2736(76)90257-1. [DOI] [PubMed] [Google Scholar]
  22. Moyer S. A., Tsang J. M., Atkinson P. H., Summers D. F. Oligosaccharide moieties of the glycoprotein of vesicular stomatitis virus. J Virol. 1976 Apr;18(1):167–175. doi: 10.1128/jvi.18.1.167-175.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nakamura K., Compans R. W. Glycopeptide components of influenza viral glycoproteins. Virology. 1978 May 15;86(2):432–442. doi: 10.1016/0042-6822(78)90083-1. [DOI] [PubMed] [Google Scholar]
  24. Nakamura K., Herrler G., Petri T., Meier-Ewert H., Compans R. W. Carbohydrate components of influenza C virions. J Virol. 1979 Mar;29(3):997–1005. doi: 10.1128/jvi.29.3.997-1005.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nakamura N., Compans R. W. Biosynthesis of the oligosaccharides of influenza viral glycoproteins. Virology. 1979 Feb;93(1):31–47. doi: 10.1016/0042-6822(79)90273-3. [DOI] [PubMed] [Google Scholar]
  26. O'Donnell P. V., Stockert E. Induction of GIX antigen and gross cell surface antigen after infection by ecotropic and xenotropic murine leukemia viruses in vitro. J Virol. 1976 Dec;20(3):545–554. doi: 10.1128/jvi.20.3.545-554.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. 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]
  28. Robbins P. W., Hubbard S. C., Turco S. J., Wirth D. F. Proposal for a common oligosaccharide intermediate in the synthesis of membrane glycoproteins. Cell. 1977 Dec;12(4):893–900. doi: 10.1016/0092-8674(77)90153-2. [DOI] [PubMed] [Google Scholar]
  29. Robertson M. A., Etchison J. R., Robertson J. S., Summers D. F., Stanley P. Specific changes in the oligosaccharide moieties of VSV grown in different lectin-resistnat CHO cells. Cell. 1978 Mar;13(3):515–526. doi: 10.1016/0092-8674(78)90325-2. [DOI] [PubMed] [Google Scholar]
  30. Rommelaere J., Faller D. V., Hopkins N. Characterization and mapping of RNase T1-resistant oligonucleotides derived from the genomes of Akv and MCF murine leukemia viruses. Proc Natl Acad Sci U S A. 1978 Jan;75(1):495–499. doi: 10.1073/pnas.75.1.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schwarz R. T., Schmidt M. F., Anwer U., Klenk H. D. Carbohydrates of influenza virus. I. Glycopeptides derived from viral glycoproteins after labeling with radioactive sugars. J Virol. 1977 Aug;23(2):217–226. doi: 10.1128/jvi.23.2.217-226.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sefton B. M. Immediate glycosylation of Sindbis virus membrane proteins. Cell. 1977 Apr;10(4):659–668. doi: 10.1016/0092-8674(77)90099-x. [DOI] [PubMed] [Google Scholar]
  33. Sefton B. M., Keegstra K. Glycoproteins of Sindbis virus: priliminary characterization of the oligosaccharides. J Virol. 1974 Sep;14(3):522–530. doi: 10.1128/jvi.14.3.522-530.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Tabas I., Schlesinger S., Kornfeld S. Processing of high mannose oligosaccharides to form complex type oligosaccharides on the newly synthesized polypeptides of the vesicular stomatitis virus G protein and the IgG heavy chain. J Biol Chem. 1978 Feb 10;253(3):716–722. [PubMed] [Google Scholar]
  35. Tarentino A. L., Maley F. A comparison of the substrate specificities of endo-beta-N-acetylglucosaminidases from Streptomyces griseus and Diplococcus Pneumoniae. Biochem Biophys Res Commun. 1975 Nov 3;67(1):455–462. doi: 10.1016/0006-291x(75)90337-x. [DOI] [PubMed] [Google Scholar]
  36. Tobita K., Sugiura A., Enomote C., Furuyama M. Plaque assay and primary isolation of influenza A viruses in an established line of canine kidney cells (MDCK) in the presence of trypsin. Med Microbiol Immunol. 1975 Dec 30;162(1):9–14. doi: 10.1007/BF02123572. [DOI] [PubMed] [Google Scholar]
  37. Wu A. M., Reitz M. S., Paran M., Gallo R. C. Mechanism of stimulation of murine type-C RNA tumor virus production by glucocorticoids: post-transcriptional effects. J Virol. 1974 Oct;14(4):802–812. doi: 10.1128/jvi.14.4.802-812.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES