Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1994 Sep;68(9):5623–5628. doi: 10.1128/jvi.68.9.5623-5628.1994

The receptor for the subgroup A avian leukosis-sarcoma viruses binds to subgroup A but not to subgroup C envelope glycoprotein.

J M Gilbert 1, P Bates 1, H E Varmus 1, J M White 1
PMCID: PMC236963  PMID: 8057442

Abstract

The putative subgroup A avian leukosis-sarcoma virus (ALSV) receptor (Tva) was recently cloned by gene transfer (P. Bates, J. A. Young, and H. E. Varmus, Cell 74:1043-1051, 1993; J. A. T. Young, P. Bates, and H. E. Varmus, J. Virol. 67:1811-1816, 1993). Susceptibility to infection by subgroup A ALSV is conferred on cells upon transfection with cDNAs encoding tva. The hypothesis that tva encodes a specific receptor for subgroup A ALSV predicts that the Tva protein should bind to subgroup A, but not to subgroup C, envelope glycoprotein. In this study, we examined this prediction by using several biochemical assays. We established stable NIH 3T3 cell lines expressing either Tva, the subgroup A envelope glycoprotein (Env-A), or the subgroup C envelop glycoprotein (Env-C) and used them in conjunction with soluble forms of these molecules to demonstrate specific binding. When cell lysates containing Tva were mixed with lysates of either Env-A or Env-C, an immunoprecipitable complex formed between Tva and Env-A but not between Tva and Env-C. A soluble, oligomeric form, of Env-A, not Env-C, binds to cells expressing Tva. Reciprocally, a secreted form of Tva can bind to cells expressing Env-A but not to cells expressing Env-C. A specific and stable complex formed between soluble Env-A and secreted Tva as demonstrated by sucrose density gradient centrifugation. Thus, by three kinds of assays, Tva appears to bind specifically to Env-A, which is consistent with genetic evidence that it serves as the cell surface receptor of subgroup A ALSV and the main determinant of subgroup specificity.

Full text

PDF
5626

Images in this article

5625Image
on p.5625
5625Image
on p.5625
5626Image
on p.5626
5626Image
on p.5626
5627Image
on p.5627

Selected References

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

  1. Bates P., Young J. A., Varmus H. E. A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor. Cell. 1993 Sep 24;74(6):1043–1051. doi: 10.1016/0092-8674(93)90726-7. [DOI] [PubMed] [Google Scholar]
  2. Bova C. A., Manfredi J. P., Swanstrom R. env genes of avian retroviruses: nucleotide sequence and molecular recombinants define host range determinants. Virology. 1986 Jul 30;152(2):343–354. doi: 10.1016/0042-6822(86)90137-6. [DOI] [PubMed] [Google Scholar]
  3. Bova C. A., Olsen J. C., Swanstrom R. The avian retrovirus env gene family: molecular analysis of host range and antigenic variants. J Virol. 1988 Jan;62(1):75–83. doi: 10.1128/jvi.62.1.75-83.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chang L. J., Stoltzfus C. M. Cloning and nucleotide sequences of cDNAs spanning the splice junctions of Rous sarcoma virus mRNAs. J Virol. 1985 Mar;53(3):969–972. doi: 10.1128/jvi.53.3.969-972.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chubb R. C., Biggs P. M. The neutralization of Rous sarcoma virus. J Gen Virol. 1968 Jul;3(1):87–96. doi: 10.1099/0022-1317-3-1-87. [DOI] [PubMed] [Google Scholar]
  6. Crittenden L. B. Observations on the nature of a genetic cellular resistance to avian tumor viruses. J Natl Cancer Inst. 1968 Jul;41(1):145–153. [PubMed] [Google Scholar]
  7. Crittenden L. B., Stone H. A., Reamer R. H., Okazaki W. Two loci controlling genetic cellular resistance to avian leukosis-sarcoma viruses. J Virol. 1967 Oct;1(5):898–904. doi: 10.1128/jvi.1.5.898-904.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dorner A. J., Coffin J. M. Determinants for receptor interaction and cell killing on the avian retrovirus glycoprotein gp85. Cell. 1986 May 9;45(3):365–374. doi: 10.1016/0092-8674(86)90322-3. [DOI] [PubMed] [Google Scholar]
  9. Einfeld D., Hunter E. Oligomeric structure of a prototype retrovirus glycoprotein. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8688–8692. doi: 10.1073/pnas.85.22.8688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gilbert J. M., Hernandez L. D., Chernov-Rogan T., White J. M. Generation of a water-soluble oligomeric ectodomain of the Rous sarcoma virus envelope glycoprotein. J Virol. 1993 Nov;67(11):6889–6892. doi: 10.1128/jvi.67.11.6889-6892.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gilbert J. M., Mason D., White J. M. Fusion of Rous sarcoma virus with host cells does not require exposure to low pH. J Virol. 1990 Oct;64(10):5106–5113. doi: 10.1128/jvi.64.10.5106-5113.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. HANAFUSA H. ANALYSIS OF THE DEFECTIVENESS OF ROUS SARCOMA VIRUS. 3. DETERMINING INFLUENCE OF A NEW HELPER VIRUS ON THE HOST RANGE AND SUSCEPTIBILITY TO INTERFERENCE OF RSV. Virology. 1965 Feb;25:248–255. doi: 10.1016/0042-6822(65)90203-5. [DOI] [PubMed] [Google Scholar]
  13. Ishizaki R., Vogt P. K. Immunological relationships among envelope antigens of avian tumor viruses. Virology. 1966 Nov;30(3):375–387. doi: 10.1016/0042-6822(66)90116-4. [DOI] [PubMed] [Google Scholar]
  14. Koke J. A., Yang M., Henner D. J., Volwerk J. J., Griffith O. H. High-level expression in Escherichia coli and rapid purification of phosphatidylinositol-specific phospholipase C from Bacillus cereus and Bacillus thuringiensis. Protein Expr Purif. 1991 Feb;2(1):51–58. doi: 10.1016/1046-5928(91)90009-8. [DOI] [PubMed] [Google Scholar]
  15. Kozak M. Comparison of initiation of protein synthesis in procaryotes, eucaryotes, and organelles. Microbiol Rev. 1983 Mar;47(1):1–45. doi: 10.1128/mr.47.1.1-45.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Maddon P. J., Dalgleish A. G., McDougal J. S., Clapham P. R., Weiss R. A., Axel R. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell. 1986 Nov 7;47(3):333–348. doi: 10.1016/0092-8674(86)90590-8. [DOI] [PubMed] [Google Scholar]
  17. Marsh M., Helenius A. Virus entry into animal cells. Adv Virus Res. 1989;36:107–151. doi: 10.1016/S0065-3527(08)60583-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Notter M. F., Leary J. F., Balduzzi P. C. Adsorption of Rous sarcoma virus to genetically susceptible and resistant chicken cells studied by laser flow cytometry. J Virol. 1982 Mar;41(3):958–964. doi: 10.1128/jvi.41.3.958-964.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Payne L. N., Biggs P. M. Genetic basis of cellular susceptibility to the Schmidt-Ruppin and Harris strains of Rous sarcoma virus. Virology. 1966 Jun;29(2):190–198. doi: 10.1016/0042-6822(66)90025-0. [DOI] [PubMed] [Google Scholar]
  20. RUBIN H. GENETIC CONTROL OF CELLULAR SUSCEPTIBILITY TO PSEUDOTYPES OF ROUS SARCOMA VIRUS. Virology. 1965 Jun;26:270–276. doi: 10.1016/0042-6822(65)90274-6. [DOI] [PubMed] [Google Scholar]
  21. Stegmann T., Doms R. W., Helenius A. Protein-mediated membrane fusion. Annu Rev Biophys Biophys Chem. 1989;18:187–211. doi: 10.1146/annurev.bb.18.060189.001155. [DOI] [PubMed] [Google Scholar]
  22. Vogt P. K., Ishizaki R. Patterns of viral interference in the avian leukosis and sarcoma complex. Virology. 1966 Nov;30(3):368–374. doi: 10.1016/0042-6822(66)90115-2. [DOI] [PubMed] [Google Scholar]
  23. White J. M. Integrins as virus receptors. Curr Biol. 1993 Sep 1;3(9):596–599. doi: 10.1016/0960-9822(93)90007-B. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. White J. M. Membrane fusion. Science. 1992 Nov 6;258(5084):917–924. doi: 10.1126/science.1439803. [DOI] [PubMed] [Google Scholar]
  25. White J. M., Wilson I. A. Anti-peptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza virus hemagglutinin. J Cell Biol. 1987 Dec;105(6 Pt 2):2887–2896. doi: 10.1083/jcb.105.6.2887. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Wigler M., Silverstein S., Lee L. S., Pellicer A., Cheng Y. c., Axel R. Transfer of purified herpes virus thymidine kinase gene to cultured mouse cells. Cell. 1977 May;11(1):223–232. doi: 10.1016/0092-8674(77)90333-6. [DOI] [PubMed] [Google Scholar]
  27. Wiley D. C., Skehel J. J. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu Rev Biochem. 1987;56:365–394. doi: 10.1146/annurev.bi.56.070187.002053. [DOI] [PubMed] [Google Scholar]
  28. Young J. A., Bates P., Varmus H. E. Isolation of a chicken gene that confers susceptibility to infection by subgroup A avian leukosis and sarcoma viruses. J Virol. 1993 Apr;67(4):1811–1816. doi: 10.1128/jvi.67.4.1811-1816.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES