Avian sarcoma virus RNA synthesis, RNA splicing and virus production in human foreskin fibroblasts: effect of co-infection with human cytomegalovirus Free

Abstract

The level of RNA transcripts in human foreskin fibroblast (HFF) cells initiated from the avian sarcoma virus (ASV) long terminal repeat (LTR) promoter was stimulated more than 10-fold when the cells were also infected with human cytomegalovirus (HCMV). HCMV was able to stimulate transcription from the ASV LTR promoter even when all the LTR sequence upstream of the TATA box was deleted, suggesting that only the basal LTR promoter is required for the effect. There were no significant changes in the ASV RNA splicing pattern in stimulated and unstimulated HFF cells. The mRNAs showing an increase during HCMV stimulation included aberrantly spliced ASV RNA species as well as unspliced , single-spliced and single-spliced mRNAs. This pattern was quite different from ASV splicing in chicken embryo fibroblasts (CEF) but typical of that seen in other mammalian cells. A dramatic increase in infectious ASV production from the normally non-permissive HFF was correlated with the increase in amount of ASV RNA in response to HCMV. Thus, there is not an absolute block to ASV production in human cells. However, infectious ASV production was inefficent in HCMV-stimulated HFF compared to that in CEF cells.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-74-12-2629
1993-12-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/74/12/JV0740122629.html?itemId=/content/journal/jgv/10.1099/0022-1317-74-12-2629&mimeType=html&fmt=ahah

References

  1. Barry P. A., Pratt-Lowe E., Peterlin B. M., Luciw P. A. 1990; Cytomegalovirus activates transcription directed by the long terminal repeat of human immunodeficiency virus type 1. Journal of Virology 64:2932–2940
    [Google Scholar]
  2. Berberich S. L., Stoltzfus C. M. 1991; Analysis of spliced and unspliced Rous sarcoma virus RNAs early and late after infection of chicken embryo fibroblasts: effect of cell culture conditions. Virology 182:135–144
    [Google Scholar]
  3. Berberich S. L., Macias M., Zhang L., Turek L. P., Stoltzfus C. M. 1990; Comparison of Rous sarcoma virus RNA processing in chicken and mouse fibroblasts: evidence for double-spliced RNA in nonpermissive mouse cells. Journal of Virology 64:4313–4320
    [Google Scholar]
  4. Biegalke B. J., Geballe A. P. 1991; Sequence requirements for activation of the HIV-1 LTR by human cytomegalovirus. Virology 183:381–385
    [Google Scholar]
  5. Bishop I. M., Deng C. T., Mahy B. W. J., Quintrell N., Stavnezer E., Varmus H. E. 1976; Synthesis of viral RNA in cells infected by avian sarcoma viruses. In Animal Virology pp 1–20 Edited by Baltimore D., Huang A., Fox C. F. New York: Academic Press;
    [Google Scholar]
  6. Boulden A., Sealy L. 1990; Identification of a third protein factor which binds to the Rous sarcoma virus LTR enhancer: possible homology with the serum response factor. Virology 174:204–216
    [Google Scholar]
  7. Bova C. A., Olsen J. C., Swanstrom R. 1988; The avian retrovirus env gene family: molecular analysis of host range and antigenic variants. Journal of Virology 62:75–83
    [Google Scholar]
  8. Chang L. J., Stoltzfus C. M. 1985; Cloning and nucleotide sequences of cDNAs spanning the splice junctions of Rous sarcoma virus mRNAs. Journal of Virology 53:969–972
    [Google Scholar]
  9. Cullen B. R., Raymond K., Ju G. 1985; Functional analysis of the transcription control region located within the avian retroviral long terminal repeat. Molecular and Cellular Biology 5:438–447
    [Google Scholar]
  10. Davis M. G., Kenny S. C., Kamine J., Pagano J. S., Huang E.-S. 1987; Immediate-early gene region of human cytomegalovirus transactivates the promoter of human immunodeficiency virus. Proceedings of the National Academy of Sciences, U,. S,. A 84:8642–8646
    [Google Scholar]
  11. Eisenman R., Vogt V. M., Diggelmann H. 1975; Synthesis of avian RNA tumor virus structural proteins. Cold Spring Harbor Symposia on Quantitative Biology 39:1067–1075
    [Google Scholar]
  12. Geryk J., Sainerova V., Sovova V., Svoboda J. 1984; Characterization of cryptovirogenic, virus-productive and helper-dependent virogenic hamster tumor cell lines. Folia Biologica 30:152–164
    [Google Scholar]
  13. Gilmarten G. M., Parsons J. T. 1983; Identification of transcriptional elements within the long terminal repeat of Rous sarcoma virus. Molecular and Cellular Biology 3:1834–1845
    [Google Scholar]
  14. Goodwin G. H. 1988; Identification of three sequence-specific DNA-binding proteins which interact with the Rous sarcoma virus enhancer and upstream promoter elements. Journal of Virology 62:2186–2190
    [Google Scholar]
  15. Gowda S., Rao A. S., Kim Y. W., Guntaka R. V. 1988; Identification of sequences in the long terminal repeat of avian sarcoma virus required for efficient transcription. Virology 162:243–247
    [Google Scholar]
  16. Hagemeier C., Walker S. M., Sissons P. J. G., Sinclair J. H. 1992; The 72K IE1 and 80K IE2 proteins of human cytomegalovirus independently trans-activate the c-fos, c-myc and hsp 70 promoters via basal promoter elements. Journal of General Virology 73:2385–2393
    [Google Scholar]
  17. Laimins L. A., Tsichlis P., Khoury G. 1984; Multiple enhancer domains in the 3′ terminus of the Prague strain of Rous sarcoma virus. Nucleic Acids Research 12:6427–6441
    [Google Scholar]
  18. Levy J. A. 1977; Murine xenotropic type C viruses. III. Phenotypic mixing with avian leukosis and sarcoma viruses. Virology 77:811–825
    [Google Scholar]
  19. Lopata M. A., Cleveland D. W., Sollner-Webb B. 1984; High level transient expression of a chloramphenicol acetyltransferase gene by DEAE-dextran mediated DNA transfection coupled with a dimethylsulfoxide or glycerol shock treatment. Nucleic Acids Research 12:5707–5717
    [Google Scholar]
  20. Luciw P. A., Bishop J. M., Varmus H. E., Capecchi M. R. 1983; Location and function of retroviral and SV40 sequences that enhance biochemical transformation after microinjection of DNA. Cell 33:705–716
    [Google Scholar]
  21. Markovitz D. M., Kenny S., Kamine J., Smith M. S., Davis M. H., Rosen C., Pagano J. S. 1989; Disparate effects of two herpesvirus immediate-early gene transactivators on the HIV-1 LTR. Virology 173:750–754
    [Google Scholar]
  22. Miller J. T., Stoltzfus C. M. 1992; Two distant upstream regions containing cis-acting signals regulating splicing facilitate 3′-end processing of avian sarcoma virus RNA. Journal of Virology 66:4242–4251
    [Google Scholar]
  23. Norton P. A., Coffin J. M. 1987; Characterization of Rous sarcoma virus sequences essential for viral gene expression. Journal of Virology 61:1171–1179
    [Google Scholar]
  24. Pulaski J. T., Tieber V. L., Coussens P. M. 1992; Marek’s disease virus-mediated enhancement of avian leukosis virus gene expression and virus production. Virology 186:113–121
    [Google Scholar]
  25. Quintrell N., Hughes S. H., Varmus H. E., Bishop J. M. 1980; The structure of viral RNAs in mammalian cells infected with avian sarcoma virus. Journal of Molecular Biology 143:363–393
    [Google Scholar]
  26. Rando R. F., Srinivasen A., Feingold J., Gonczol E., Plotkin S. 1990; Characterization of multiple molecular interactions between human cytomegalovirus (HCMV) and human immunodeficiency virus type 1 (HIV-1). Virology 176:87–97
    [Google Scholar]
  27. Ryden T. A., Beemon K. 1989; Avian retroviral long terminal repeats bind CCAAT/enhancer-binding protein. Molecular and Cellular Biology 9:1155–1164
    [Google Scholar]
  28. Sanger F., Nicklen S., Coulson A. R. 1977; DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences, U,. S,. A 74:5463–5467
    [Google Scholar]
  29. Schwartz D. E., Tizard R., Gilbert W. 1983; Nucleotide sequence of Rous sarcoma virus. Cell 32:853–869
    [Google Scholar]
  30. Sealy L., Chalkley R. 1987; At least two nuclear proteins bind specifically to the Rous sarcoma virus long terminal repeat enhancer. Molecular and Cellular Biology 7:787–798
    [Google Scholar]
  31. Sealy L. M., Privalsky M. L., Moscovici G., Moscovici C., Bishop J. M. 1983; Site-specific mutagenesis of avian erythroblastosis virus: erb-B is required for oncogenicity. Virology 130:155–178
    [Google Scholar]
  32. Stinski M. F. 1978; Sequence of protein synthesis in cells infected by human cytomegalovirus: early and late virus-induced polypeptides. Journal of Virology 26:686–701
    [Google Scholar]
  33. Stoltzfus C. M., Fogarty S. J. 1989; Multiple regions in the Rous sarcoma virus src gene intron act in cis to affect accumulation of unspliced RNA. Journal of Virology 63:1669–1676
    [Google Scholar]
  34. Stoltzfus C. M., Dimock K., Horikami S., Ficht T. A. 1983; Stabilities of avian sarcoma virus RNAs: comparison of subgenomic and genomic species with cellular mRNAs. Journal of General Virology 64:2191–2202
    [Google Scholar]
  35. Strohman R., Moss P., Micou-Eastwood J., Spector D., Przybyla A., Peterson B. 1977; Messenger RNA for myosin polypeptides: isolation from single myogenic cell cultures. Cell 10:265–273
    [Google Scholar]
  36. Svoboda J., Lhotak V., Geryk J., Saule S., Raes M. B., Stehelin D. 1983; Characterization of exogenous proviral sequences in hamster tumor cell lines transformed by Rous sarcoma virus rescued from XC cells. Virology 128:195–209
    [Google Scholar]
  37. Temin H. M. 1974; The cellular and molecular biology of RNA tumor viruses, especially avian leukosis-sarcoma viruses, and their relatives. Advances in Cancer Research 19:47–104
    [Google Scholar]
  38. Tieber V. L., Zalinskis L. L., Silva R. F., Finkelstein A., Coussens P. M. 1990; Transactivation of the Rous sarcoma virus long terminal repeat promoter by Marek’s disease virus. Virology 179:719–727
    [Google Scholar]
  39. Varmus H., Swanstrom R. 1982; Replication of retroviruses. In RNA Tumor Viruses pp 369–512 Edited by Weiss R., Teich N., Varmus H., Coffin J. New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  40. Vogt P. K. 1969; Focus assay of Rous sarcoma virus. In Fundamental Techniques of Virology pp 199–211 Edited by Habel K., Salzman N. P. New York: Academic Press;
    [Google Scholar]
  41. Vogt V. M., Eisenman R., Diggelmann H. 1975; Generation of avian myeloblastosis virus structural proteins by proteolytic cleavage of a precursor polypeptide. Journal of Molecular Biology 96:471–493
    [Google Scholar]
  42. Weiss R. A., Wong A. L. 1977; Phenotypic mixing between avian and mammalian RNA tumor viruses. I. Envelope pseudotypes of Rous sarcoma virus. Virology 76:826–834
    [Google Scholar]
  43. Wigler M., Pellicer A., Silverstein S., Axel R. 1978; Biochemical transfer of single-copy eukaryotic genes using total cellular DNA as donor. Cell 14:725–734
    [Google Scholar]
  44. Wills J. W., Craven R. C., Achacoso J. A. 1989; Creation and expression of myristylated forms of Rous sarcoma virus gag protein in mammalian cells. Journal of Virology 63:4331–4343
    [Google Scholar]
  45. Zachow K. R., Conklin K. F. 1992; CArG, CCAAT, and CCAAT-like protein binding sites in avian retrovirus long terminal repeat enhancers. Journal of Virology 66:1959–1970
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-74-12-2629
Loading
/content/journal/jgv/10.1099/0022-1317-74-12-2629
Loading

Data & Media loading...

Most cited Most Cited RSS feed