1887

Journal of General Virology header logo

Volume 74, Issue 4

The role of gp55 -glycosylation in pathogenesis of Friend spleen focus-forming virus Free

Abstract

The product of the envelope gene (gp55) of Friend spleen focus-forming virus is responsible for the acute form of erythroleukaemia caused by this virus. In order to investigate the role that the four known -linked carbohydrate side-chains of gp55 play in pathogenesis, we have inactivated the four -glycosylation signals by mutating the asparagine residues of these four sites into serine. When glycosylation sites 1 and/or 2 were altered, the viruses remained fully pathogenic. However, mutation at either of glycosylation sites 3 or 4 rendered the virus apathogenic, independent of mutations at other sites. Furthermore, when site 3 was changed, a new product appeared which seemed to have acquired a carbohydrate chain at a position normally not glycosylated, presumably at position Asn.

  • Received:
  • Accepted:
  • Published Online:
© Society for General Microbiology 1993
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-74-4-699
1993-04-01
2022-01-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/74/4/JV0740040699.html?itemId=/content/journal/jgv/10.1099/0022-1317-74-4-699&mimeType=html&fmt=ahah

References

  1. Amanuma H., Katori H., Obata A., Sagata N., Ikawa Y. 1983; Complete nucleotide sequence of the gene for the specific glycoprotein (gp55) of Friend spleen focus-forming virus. Proceedings of the National Academy of Sciences, U.S.A. 80:3913–3917
     [Google Scholar]
  2. Casadevall N., Lacombe C., Muller O., Gisselbrecht S., Mayeux P. 1991; Multimeric structure of the membrane erythropoietin receptor of murine erythroleukemia cells (Friend cells): cross-linking of erythropoietin with the spleen focus-forming virus envelope protein. Journal of Biological Chemistry 266:16015–16020
     [Google Scholar]
  3. Chung S. W., Wolff L., Ruscetti S. K. 1989; Transmembrane domain of the envelope gene of a polycythemia-inducing retrovirus determines erythropoietin-independent growth. Proceedings of the National Academy of Sciences,U.S.A. 86:7657–7960
     [Google Scholar]
  4. Clark S. P., Mak T. W. 1983; Complete nucleotide sequence of an infectious clone of Friend spleen focus-forming provirus: gp55 is an envelope fusion glycoprotein. Proceedings of the National Academy of Sciences, U.S.A. 80:5037–5041
     [Google Scholar]
  5. Feigner P., Gadek T. R., Holm M., Roman R., Chan H. W., Wenz M., Northrop J. P., Ringold G. M., Danielsen M. 1987; Lipofection: a highly efficient, lipid-mediated DNA-trans-fection procedure. Proceedings of the National Academy of Sciences, U.S.A. 84:7413–7417
     [Google Scholar]
  6. Friedrich R., Friedrich U., Maennle G. 1991; Construction and properties of an ‘artificial’ spleen focus-forming virus. Virology 183:343–350
     [Google Scholar]
  7. Gliniak B. C., Kabat D. 1989; Leukemogenic membrane glycoprotein encoded by Friend spleen focus-forming virus: transport to cell surfaces and shedding are controlled by disulfide-bonded dimerization and by cleavage of a hydrophobic membrane anchor. Journal of Virology 63:3561–3568
     [Google Scholar]
  8. Gliniak B. C., Kozak S. L., Jones R. T., Kabat D. 1991; Disulfide bonding controls the processing of retroviral envelope glycoproteins. Journal of Biological Chemistry 266:22991–22997
     [Google Scholar]
  9. Hoatlin M. E., Kozak S. L., Lilly F., Chakraborti A., Kozak C. A., Kabat D. 1990; Activation of erythropoietin receptors by Friend viral gp55 and by erythropoietin and down-modulation by the murine Fv-2r resistance gene. Proceedings of the National Academy of Sciences, U.S.A. 87:9985–9989
     [Google Scholar]
  10. Kabat D. 1989; Molecular biology of Friend viral erythroleukemia. Current Topics in Microbiology and Immunology 148:1–12
     [Google Scholar]
  11. Kayman S. C., Kopelman R., Projan S., Kinney D. M., Pinter A. 1991; Mutational analysis of A-linked glycosylation sites of Friend murine leukemia virus envelope protein. Journal of Virology 65:5323–5332
     [Google Scholar]
  12. Kilpatrick D. R., Srinivas R. V., Compans R. W. 1989; The spleen focus-forming virus envelope glycoprotein is defective in oligomerization. Journal of Biological Chemistry 264:10732–10737
     [Google Scholar]
  13. Kotwal G. J., Buller R. ML., Wunner W. H., Pringle C. R., Ghosh H. P. 1986; Role of glycosylation in transport of vesicular stomatitis virus envelope glycoprotein: a new class of mutant defective in glycosylation and transport of G protein. Journal of Biological Chemistry 261:8936–8943
     [Google Scholar]
  14. Li J. P., Bestwick R. K., Machida C., Kabat D. 1986; Role of a membrane glycoprotein in Friend virus erythroleukemia: nucleotide sequences of nonleukemogenic mutant and spontaneous revertant viruses. Journal of Virology 57:534–538
     [Google Scholar]
  15. Li J. P., Bestwick R. K., Spiro C., Kabat D. 1987; The membrane glycoprotein of Friend spleen focus-forming virus: evidence that the cell surface component is required for pathogenesis and that it binds to a receptor. Journal of Virology 61:2782–2792
     [Google Scholar]
  16. Li J. P., D’Andrea A. D., Lodish H. F., Baltimore D. 1990; Activation of cell growth by binding of Friend spleen focus-forming virus gp55 glycoprotein to the erythropoietin receptor. Nature, London 343:762–764
     [Google Scholar]
  17. Linemeyer D. L., Ruscetti S. K., Scolnick E. M., Evans L. H., Duesberg P. H. 1981; Biological activity of the spleen focusforming virus is encoded by a molecularly cloned subgenomic fragment of spleen focus-forming virus DNA. Proceedings of the National Academy of Sciences 78:1401–1405
     [Google Scholar]
  18. Linemeyer D. L., Menke J. G., Ruscetti S. K., Evans L. H., Scolnick E. M. 1982; Envelope gene sequences which encode the gp52 protein of spleen focus-forming virus are required for the induction of erythroid cell proliferation. Journal of Virology 43:223–233
     [Google Scholar]
  19. Machamer C. E., Rose J. K. 1988a; Influence of new glycosylation sites on expression of the vesicular stomatitis virus G protein at the plasma membrane. Journal of Biological Chemistry 263:5948–5954
     [Google Scholar]
  20. Machamer C. E., Rose J. K. 1988b; Vesicular stomatitis virus G proteins with altered glycosylation sites display temperature-sensitive intracellular transport and are subject to aberrant intermolecular disulfide bonding. Journal of Biological Chemistry 263:5955–5960
     [Google Scholar]
  21. Machamer C. E., Florkiewicz R. Z., Rose J. K. 1985; A single A-linked oligosaccharide at either of the two normal sites is sufficient for transport of vesicular stomatitis virus G protein to the cell surface. Molecular and Cellular Biology 5:3074–3083
     [Google Scholar]
  22. Machida C. A., Bestwick R. K., Boswell B. A., Kabat D. 1985; Role of a membrane glycoprotein in Friend virus-induced erythroleukemia: studies of mutant and revertant viruses. Virology 144:158–172
     [Google Scholar]
  23. Moreau-Gachelin F., Tavitian A., Tambourin P. 1988; Spi-1 is a putative oncogene in virally induced murine erythroleukaemias. Nature, London 331:277–280
     [Google Scholar]
  24. Ostertag W., Vehmeyer K., Fagg B., Pragnell I. B., Paetz W., Le Bousse C., Smadja-Joffe F., Klein B., Jasmin C., Eisen H. 1980; Myeloproliferative virus, a cloned murine sarcoma virus with spleen focus-forming properties in adult mice. Journal of Virology 33:573–582
     [Google Scholar]
  25. Ostertag W., Stocking C., Johnson G. R., Kluge N., Kollek R., Franz T., Hess N. 1987; Transforming genes and target cells of murine spleen focus-forming viruses. Advances in Cancer Research 48:193–355
     [Google Scholar]
  26. Paeratakul U., De Stasio P. R., Taylor M. W. 1988; A fast and sensitive method for detecting specific viral RNA in mammalian cells. Journal of Virology 62:1132–1135
     [Google Scholar]
  27. Paul R., Schuetze S., Kozak S. L., Kozak C. A., Kabat D. 1991; The Sfpi-l proviral integration site of Friend erythroleukemia encodes the cts-related transcription factor Pu. 1. Journal of Virology 65:464–467
     [Google Scholar]
  28. Pinter A., Honnen W. J. 1985; The mature form of the Friend spleen focus-forming virus envelope protein, gp65, is efficiently secreted from cells. Virology 143:646–650
     [Google Scholar]
  29. Pinter A., Honnen W. J. 1989; Biochemical characterization of cell-associated and extracellular products of the Friend spleen focusforming virus env gene. Virology 173:136–143
     [Google Scholar]
  30. Pinter A., Honnen W. J., Li J. S. 1984; Studies with inhibitors of oligosaccharide processing indicate a functional role for complex sugars in the transport and proteolysis of Friend mink cell focus-inducing murine leukemia virus envelope proteins. Virology 136:196–210
     [Google Scholar]
  31. Polonoff E., Machida C. A., Kabat D. 1982; Glycosylation and intracellular transport of membrane glycoproteins encoded by murine leukemia viruses: inhibition by amino acid analogues and by tunicamycin. Journal of Biological Chemistry 257:14023–14028
     [Google Scholar]
  32. Ruscetti S., Wolff L. 1984; Spleen focus-forming virus: Relationship of an altered envelope gene to the development of a rapid erythroleukemia. Current Topics in Microbiology and Immunology 112:21–44
     [Google Scholar]
  33. Ruscetti S. K., Feild J. A., Scolnick E. M. 1981; Poly-cythaemia- and anaemia-inducing strains of spleen focus-forming virus differ in post-translational processing of envelope-related glycoproteins. Nature, London 294:663–665
     [Google Scholar]
  34. Ruscetti S. K., Janesch N. J., Chakraborti A., Sawyer S. T., Hankins W. D. 1990; Friend spleen focus-forming virus induces factor independence in an erythropoietin-dependent erythroleukemia cell line. Journal of Virology 63:1057–1062
     [Google Scholar]
  35. Ruta M., Clarke S., Boswell B., Kabat D. 1982; Heterogeneous metabolism and subcellular localization of a potentially leukemogenic membrane glycoprotein encoded by Friend erythroleukemia virus: isolation of viral and cellular processing mutants. Journal of Biological Chemistry 257:126–134
     [Google Scholar]
  36. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences 74:5463–5467
     [Google Scholar]
  37. Spiro C., Gliniak B., Kabat D. 1988; A tagged helper-free Friend virus causes clonal erythroblast immortality by specific proviral integration in the cellular genome. Journal of Virology 62:4129–1135
     [Google Scholar]
  38. Srinivas R. V., Compans R. W. 1983; Glycosylation and intracellular transport of spleen focus-forming virus glycoproteins. Virology 125:274–286
     [Google Scholar]
  39. Srinivas R. V., Tucker S. P., Kilpatrick D. R., Compans R. W. 1992; A 585-bp deletion found in the spleen focus-forming virus (SFFV) env gene is responsible for the defective intracellular transport of SFFV gp52. Virology 188:181–192
     [Google Scholar]
  40. Strube K. H., Geyer R. 1989; Carbohydrate structure of glycoprotein 65 encoded by the polycythemia-inducing strain of Friend spleen focus-forming virus. European Journal of Biochemistry 179:441–450
     [Google Scholar]
  41. Strube K. H., Schott H. H., Geyer R. 1988; Carbohydrate structure of glycoprotein 52 encoded by the polycythemia-inducing strain of Friend spleen focus-forming virus. Journal of Biological Chemistry 263:3762–3771
     [Google Scholar]
  42. Taylor J. W., Ott J., Eckstein F. 1985; The rapid generation of oligonucleotide-directed mutations at high frequency using phosphorothioate-modified DNA. Nucleic Acids Research 13:8765–8785
     [Google Scholar]
  43. Vogelstein B., Gillespie D. 1979; Preparative and analytical purification of DNA from agarose. Proceedings of the National Academy of Sciences, U.S.A. 76:615–619
     [Google Scholar]
  44. Watanabe N., Nishi M., Ikawa Y., Amanuma H. 1991; Conversion of Friend mink cell focus-forming virus to Friend spleen focus-forming virus by modification of the 3ʹ half of the env gene. Journal of Virology 65:132–137
     [Google Scholar]
  45. Wolff L., Ruscetti S. 1985; Malignant transformation of erythroid cells in vivo by introduction of a nonreplicating retrovirus vector. Science 228:1549–1552
     [Google Scholar]
  46. Wolff L., Ruscetti S. 1988; The spleen focus-forming virus (SFFV) envelope gene, when introduced into mice in the absence of other SFFV genes, induces acute erythroleukemia. Journal of Virology 62:2158–2163
     [Google Scholar]
  47. Wolff L., Scolnick E., Ruscetti S. 1983; Envelope gene of the Friend spleen focus-forming virus: deletion and insertions in 3ʹ gp70/pl5E-encoding region have resulted in unique features in the primary structure of its protein product. Proceedings of the National Academy of Sciences, U.S.A. 80:4718–4722
     [Google Scholar]
  48. Wright K. E., .Spiro R. C., Burns J. W., Buchmeier M. J. 1990; Post-translational processing of the glycoproteins of lymphocytic choriomeningitis virus. Virology 177:175–183
     [Google Scholar]
  49. Yang Y., Tojo A., Watanabe N., Amanuma H. 1990; Oligomerization of Friend spleen focus-forming virus (SFFV) env glycoproteins. Virology 177:312–316
     [Google Scholar]
  50. Yoshimura A., D’Andrea A. D., Lodish H. F. 1990; Friend spleen focus-forming virus glycoprotein gp55 interacts with the erythropoietin receptor in the endoplasmic reticulum and affects receptor metabolism. Proceedings of the National Academy of Sciences, U.S.A. 87:4139–4143
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-74-4-699
Loading
The role of gp55 N-glycosylation in pathogenesis of Friend spleen focus-forming virus
J. Gen. Virol. 74, 699 (1993); https://doi.org/10.1099/0022-1317-74-4-699
/content/journal/jgv/10.1099/0022-1317-74-4-699
/content/journal/jgv/10.1099/0022-1317-74-4-699
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error