Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1980 Jan;77(1):67–71. doi: 10.1073/pnas.77.1.67

Differences in glycosylation patterns of closely related murine leukemia viruses

Marsha Rich Rosner 1, Lynn S Grinna 1, Phillips W Robbins 1
PMCID: PMC348209  PMID: 6244574

Abstract

The nature of the carbohydrate chains in the major envelope glycoprotein of murine leukemia virus, gp70, and its cellular precursor has been investigated. A difference in the oligosaccharide composition of gp70 from an ecotropic murine leukemia virus (Akv) and three recombinant dual-tropic viruses [mink cell focus-inducing viruses (MCFs)] derived from Akv was demonstrated. Glycosidase digestion and gel filtration were utilized to identify the two classes of N-asparagine-linked oligosaccharides, high-mannose and complex. The gp70 of the ecotropic virus contained only N-linked oligosaccharides of the complex type. In contrast, the gp70s of the dual-tropic viruses contained both high-mannose and complex oligosaccharides. Analysis of gp70 glycopeptides from an MCF-related xenotropic virus showed an elution profile similar, but not identical, to profiles of the MCFs. The gp70 precursors isolated from cells infected with Akv or MCF virus contained N-linked oligosaccharides that were exclusively of the high-mannose type. Comparison of the high-mannose oligosaccharides of the MCF gp70 precursors with those of the corresponding gp70s indicated that very little further processing of the high-mannose residues in the gp70s had occurred. The presence of the high-mannose oligosaccharides in the envelope glycoprotein of the dual-tropic viruses results from altered carbohydrate processing. The conservation of this altered carbohydrate pattern in a number of hosts and under various conditions of growth suggests that the viral protein structure is the primary factor in determining the different mode of glycosylation of the MCF gp70s. Thus, these viral glycoproteins provide an important model system for studying the relationship between protein structure and patterns of glycosylation.

Keywords: glycoprotein gp70, mink cell focus-inducing viruses, high-mannose and complex oligosaccharides

Full text

PDF
67

Selected References

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

  1. Besmer P., Baltimore D. Mechanism of restriction of ecotropic and xenotropic murine leukemia viruses and formation of pseudotypes between the two viruses. J Virol. 1977 Mar;21(3):965–973. doi: 10.1128/jvi.21.3.965-973.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bolognesi D. P., Montelaro R. C., Frank H., Schäfer W. Assembly of type C oncornaviruses: a model. Science. 1978 Jan 13;199(4325):183–186. doi: 10.1126/science.202022. [DOI] [PubMed] [Google Scholar]
  3. Chien Y. H., Verma I. M., Shih T. Y., Scolnick E. M., Davidson N. Heteroduplex analysis of the sequence relations between the RNAs of mink cell focus-inducing and murine leukemia viruses. J Virol. 1978 Oct;28(1):352–360. doi: 10.1128/jvi.28.1.352-360.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DeLarco J., Todaro G. J. Membrane receptors for murine leukemia viruses: characterization using the purified viral envelope glycoprotein, gp71. Cell. 1976 Jul;8(3):365–371. doi: 10.1016/0092-8674(76)90148-3. [DOI] [PubMed] [Google Scholar]
  5. Del Vellano B. C., Nave B., Croker B. P., Lerner R. A., Dixon F. J. The oncornavirus glycoprotein gp69/71: a constituent of the surface of normal and malignant thymocytes. J Exp Med. 1975 Jan 1;141(1):172–187. doi: 10.1084/jem.141.1.172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Donoghue D. J., Rothenberg E., Hopkins N., Baltimore D., Sharp P. A. Heteroduplex analysis of the nonhomology region between Moloney MuLV and the dual host range derivative HIX virus. Cell. 1978 Aug;14(4):959–970. doi: 10.1016/0092-8674(78)90350-1. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Fischinger P. J., Frankel A. E., Elder J. H., Lerner R. A., Ihle J. N., Bolognesi D. P. Biological, immunological, and biochemical evidence that HIX virus is a recombinant between Moloney leukemia virus and a murine xenotropic C type virus. Virology. 1978 Oct 15;90(2):241–254. doi: 10.1016/0042-6822(78)90308-2. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Hubbard S. C., Robbins P. W. Synthesis and processing of protein-linked oligosaccharides in vivo. J Biol Chem. 1979 Jun 10;254(11):4568–4576. [PubMed] [Google Scholar]
  11. Ikeda H., Pincus T., Yoshiki T., Strand M., August J. T., Boyse E. A., Mellors R. C. Biological expression of antigenic determinants of murine leukemia virus proteins gp69-71 and p30. J Virol. 1974 Nov;14(5):1274–1280. doi: 10.1128/jvi.14.5.1274-1280.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kawashima K., Ikeda H., Hartley J. W., Stockert E., Rowe W. P., Old L. J. Changes in expression of murine leukemia virus antigens and production of xenotropic virus in the late preleukemic period in AKR mice. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4680–4684. doi: 10.1073/pnas.73.12.4680. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kennel S. J., Del Villano B. C., Levy R. L., Lerner R. A. Properties of an oncornavirus glycoprotein: evidence for its presence on the surface of virions and infected cells. Virology. 1973 Oct;55(2):464–475. doi: 10.1016/0042-6822(73)90188-8. [DOI] [PubMed] [Google Scholar]
  14. Kennel S. J., Feldman J. D. Distribution of viral glycoprotein gp 69/71 on cell surfaces of producer and nonproducer cells. Cancer Res. 1976 Jan;36(1):200–208. [PubMed] [Google Scholar]
  15. Kessler S. W. Rapid isolation of antigens from cells with a staphylococcal protein A-antibody adsorbent: parameters of the interaction of antibody-antigen complexes with protein A. J Immunol. 1975 Dec;115(6):1617–1624. [PubMed] [Google Scholar]
  16. Kornfeld R., Kornfeld S. Comparative aspects of glycoprotein structure. Annu Rev Biochem. 1976;45:217–237. doi: 10.1146/annurev.bi.45.070176.001245. [DOI] [PubMed] [Google Scholar]
  17. Ledbetter J., Nowinski R. C., Emery S. Viral proteins expressed on the surface of murine leukemia cells. J Virol. 1977 Apr;22(1):65–73. doi: 10.1128/jvi.22.1.65-73.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Li E., Tabas I., Kornfeld S. The synthesis of complex-type oligosaccharides. I. Structure of the lipid-linked oligosaccharide precursor of the complex-type oligosaccharides of the vesicular stomatitis virus G protein. J Biol Chem. 1978 Nov 10;253(21):7762–7770. [PubMed] [Google Scholar]
  19. Liu T., Stetson B., Turco S. J., Hubbard S. C., Robbins P. W. Arrangement of glucose residues in the lipid-linked oligosaccharide precursor of asparaginyl oligosaccharides. J Biol Chem. 1979 Jun 10;254(11):4554–4559. [PubMed] [Google Scholar]
  20. McLellan W. L., August J. T. Analysis of the envelope of Rauscher murine oncornavirus: in vitro labeling of glycopeptides. J Virol. 1976 Dec;20(3):627–636. doi: 10.1128/jvi.20.3.627-636.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Muramatsu T., Koide N., Ceccarini C., Atkinson P. H. Characterization of mannose-labeled glycopeptides from human diploid cells and their growth-dependent alterations. J Biol Chem. 1976 Aug 10;251(15):4673–4679. [PubMed] [Google Scholar]
  22. 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]
  23. 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]
  24. 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]
  25. Shih T. Y., Weeks M. O., Troxler D. H., Coffin J. M., Scolnick E. M. Mapping host range-specific oligonucleotides within genomes of the ecotropic and mink cell focus-inducing strains of Moloney murine leukemia virus. J Virol. 1978 Apr;26(1):71–83. doi: 10.1128/jvi.26.1.71-83.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tarentino A. L., Maley F. Purification and properties of an endo-beta-N-acetylglucosaminidase from Streptomyces griseus. J Biol Chem. 1974 Feb 10;249(3):811–817. [PubMed] [Google Scholar]
  27. Troxler D. H., Lowy D., Howk R., Young H., Scolnick E. M. Friend strain of spleen focus-forming virus is a recombinant between ecotropic murine type C virus and the env gene region of xenotropic type C virus. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4671–4675. doi: 10.1073/pnas.74.10.4671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Vogt M. Properties of "mink cell focus-inducing" (MCF) virus isolated from spontaneous lymphoma lines of BALB/c mice carrying Moloney leukemia virus as an endogenous virus. Virology. 1979 Feb;93(1):226–236. doi: 10.1016/0042-6822(79)90290-3. [DOI] [PubMed] [Google Scholar]
  29. Waechter C. J., Lucas J. J., Lennarz W. J. Membrane glycoproteins. I. Enzymatic synthesis of mannosyl phosphoryl polyisoprenol and its role as a mannosyl donor in glycoprotein synthesis. J Biol Chem. 1973 Nov 10;248(21):7570–7579. [PubMed] [Google Scholar]
  30. Witte O. N., Baltimore D. Mechanism of formation of pseudotypes between vesicular stomatitis virus and murine leukemia virus. Cell. 1977 Jul;11(3):505–511. doi: 10.1016/0092-8674(77)90068-x. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Witte O. N., Weissman I. L., Kaplan H. S. Structural characteristics of some murine RNA tumor viruses studied by lactoperoxidase iodination. Proc Natl Acad Sci U S A. 1973 Jan;70(1):36–40. doi: 10.1073/pnas.70.1.36. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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 Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES