1887

Journal of General Virology header logo

Volume 72, Issue 8

Proteins of the Nuclear Factor-1 Family Act As An Activator of the Late Promoter in Human Polyomavirus BK 1 Free

Abstract

The cis-acting elements for the early and late promoters, as well as the enhancer in the prototype strains of human polyomavirus BK (BKV) are located within a 500 bp intergenic region. We previously studied the specificity of protein binding in this region and showed that the interaction of proteins of the nuclear factor-1 (NF-1) family is crucial for early promoter activity. We have now extended our study to the BKV late promoter. We show that the late promoter activity in HeLa cell extracts is poor compared to the activity of the early promoter. Using a high template to protein ratio, multiple start sites were detected by primer extension analysis. DNase I protection experiments revealed the presence of three NF-1 binding sites in the late side, in addition to those identified previously in the 68 bp repeats and C element. Competition transcription assays using binding sites for NF-1, AP-1, Sp-1 and a complete 68 bp repeat indicated that only the 68 bp repeat and the NF-1 binding site competed significantly with the late promoter activity. A point mutation in the NF-1 binding site, which destroys the ability of the oligonucleotide to bind NF-1, also impaired its capacity to compete with the late promoter. The ability of NF-1 to activate both the early and late promoters suggests that the proteins of this family act as a bidirectional transcriptional activator in this virus.

  • Received:
  • Accepted:
  • Published Online:
© Journal of General Virology 1991
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-72-8-1935
1991-08-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/72/8/JV0720081935.html?itemId=/content/journal/jgv/10.1099/0022-1317-72-8-1935&mimeType=html&fmt=ahah

References

  1. Alwine J. C., Picardi J. 1986; Activity of simian virus 40 late promoter elements in the absence of large T-antigen: evidence for repression of late gene expression. Journal of Virology 60:400–404
     [Google Scholar]
  2. Alwine J. C., Reed S. I., Ferguson J., Stark G. R. 1975; Properties of T antigens induced by wild-type SV40 and tsA mutants in lytic infection. Cell 6:529–533
     [Google Scholar]
  3. Ayer D., Dynan W. S. 1988; Simian virus 40 major late promoter: a novel tripartite structure that includes intragenic sequences. Molecular and Cellular Biology 8:2021–2033
     [Google Scholar]
  4. Brady J., Khoury G. 1985; Trans activation of the simian virus 40 late transcription unit by T-antigen. Molecular and Cellular Biology 5:1391–1399
     [Google Scholar]
  5. Brady J., Radonovich M., Vodkin M., Natarajan V., Thoren M., Das G., Janik J., Salzman N. P. 1982; Site-specific base substitutions and deletions that enhance or suppress transcription of the SV40 major late RNA. Cell 31:625–633
     [Google Scholar]
  6. Brady J., Radonovich M., Thoren M., Das G., Salzman N. P. 1984; Simian virus 40 major late promoter: an upstream DNA sequence required for efficient in vitro transcription. Molecular and Cellular Biology A133–141
     [Google Scholar]
  7. Cahill K. B., Carmichael G. G. 1989; Deletion analysis of the polyomavirus late promoter: evidence for both positive and negative elements in the absence of early proteins. Journal of Virology 63:3634–3642
     [Google Scholar]
  8. Cassil J. A., Subramani S. 1988; The late promoter of the human papovavirus BK is contained within the early promoter enhancer region. Virology 166:175–185
     [Google Scholar]
  9. Chakraborty T., Das G. C. 1989; Identification of HeLa cell nuclear factors that bind to and activate the early promoter of human polyomavirus Bk in vitro . Molecular and Cellular Biology 9:3821–3828
     [Google Scholar]
  10. Chodosh L. A., Baldwin A. S., Carthew R. W., Sharp P. A. 1988; Human CCAAT binding proteins have heterologous sub-units. Cell 53:11–24
     [Google Scholar]
  11. Contreras R., Gheysen D., Knowland J., van der Voorder A., Fiers W. 1982; Evidence for the direct involvement of DNA replication origin in synthesis of late SV40 RNA. Nature, London 300:500–504
     [Google Scholar]
  12. Das G. C., Piatigorsky J. 1986; The chicken delta 1-crystalline gene promoter: binding of transcription factors to the upstream G + C-rich region is necessary for promoter function in vitro . Proceedings of the National Academy of Sciences, U.S.A 83:3131–3135
     [Google Scholar]
  13. Das G. C., Salzman N. P. 1985; Simian virus 40 early promoter mutations that affect promoter function and autoregulation by T-antigen. Journal of Molecular Biology 182:229–239
     [Google Scholar]
  14. De Vries E., van Driel W., van den Heuvel S. J. L., van der Vliet P. C. 1987; Contact point analysis of the HeLa nuclear factor 1 recognition site reveals symmetrical binding at one side of the DNA helix. EMBO Journal 6:161–168
     [Google Scholar]
  15. Deyerle K. L., Subramani S. 1988; Linker scan analysis of the early regulatory region of human papovavirus BK. Journal of Virology 62:3378–3387
     [Google Scholar]
  16. Deyerle K. L., Cassill J. A., Subramani S. 1987; Analysis of the early regulatory region of human papovavirus BK. Virology 158:181–193
     [Google Scholar]
  17. Dignam J. D., Lebovitz R. M., Roeder R. G. 1983; Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Research 11:1475–1489
     [Google Scholar]
  18. Dorn A., Bolkens J., Staub A., Benoist C., Mathis D. 1987; A multiplicity of CCAAT box-binding proteins. Cell 50:863–872
     [Google Scholar]
  19. Dynan W. S. 1989; Modularity in promoter and enhancers. Cell 58:1–4
     [Google Scholar]
  20. Dynan W. S., Tjian R. 1985; Control of eukaryotic mRNA synthesis by sequence specific DNA binding proteins. Nature, London 316:774–778
     [Google Scholar]
  21. Ernoult-Lange M., Omilli F., May E. 1987; Contribution of different GC motifs to the control of simian virus 40 late promoter activity. Nucleic Acids Research 15:8177–8193
     [Google Scholar]
  22. Gallo G. J., Gruda M. C., Manuppello J., Alwine J. C. 1990; Activity of DNA-binding factors is altered in the presence of simian virus 40 (SV40) early proteins: characterization of factors binding to elements involved in activation of the SV40 late promoter. Journal of Virology 64:173–184
     [Google Scholar]
  23. Gardner S. D., Field A. M., Coleman D. V., Hulme B. 1971; New human papovavirus (BK) isolated from urine after renal transplantation. Lancet i:1253–1257
     [Google Scholar]
  24. Gidoni D., Kadonaga J. T., Barrera-Saldana H., Takahashi K., Chambon P., Tjian R. 1985; Bidirectional SV40 transcription mediated by tandem Spl binding interactions. Science 230:511–517
     [Google Scholar]
  25. Gong S. S., Subramanian K. N. 1988; Functional anatomy of the simian virus 40 late promoter. Virology 163:481–493
     [Google Scholar]
  26. Gorski K., Carneir M., Schibler U. 1986; Tissue-specific in vitro transcription from the mouse albumin promoter. Cell 47:767–776
     [Google Scholar]
  27. Grinnel B. W., Berg D. T., Walls J. D. 1988; Negative regulation of the human polyomavirus BK enhancer involves cell specific interaction with a nuclear repressor. Molecular and Cellular Biology 8:3448–3457
     [Google Scholar]
  28. Gronostajski R., Knox J., Berry D., Miyamoto N. G. 1988; Stimulation of transcription in vitro by binding sites for nuclear factor 1. Nucleic Acids Research 16:2087–2098
     [Google Scholar]
  29. Hartzell S. W., Byrne B. J., Subramanian K. N. 1984; The simian virus 40 minimal origin and the 72-base-pair repeat are required simultaneously for efficient induction of late gene expression with large tumor antigen. Proceedings of the National Academy of Sciences, U.S.A 81:6335–6339
     [Google Scholar]
  30. Hertz G. Z., Mertz J. E. 1988; The enhancer elements and GGGCGG boxes of SV40 provide similar functions in bidirectionally promoting transcription. Virology 163:579–590
     [Google Scholar]
  31. Huang H. C., Sundseth R., Hansen U. 1990; Transcription factor LSF binds to variant bipartite sites within the SV40 late promoter. Genes and Development 4:287–298
     [Google Scholar]
  32. Jat P., Roberts J. W., Cowie A., Kamen R. 1982; Comparision of the polyomavirus early and late promoters by transcription in vitro . Nucleic Acids Research 10:871–887
     [Google Scholar]
  33. Jeang K. D., Rawlins D. R., Rosenfeld P. J., Shero J. H., Kelly T. J., Hayward G. S. 1987; Multiple tandemly repeated binding sites for cellular nuclear factor 1 that surround the major immediateearly promoters of simian and human cytomegalovirus. Journal of Virology 61:1559–1570
     [Google Scholar]
  34. Johnson P. F., McKnight S. L. 1989; Eukaryotic transcriptional regulatory proteins. Annual Review of Biochemistry 58:799–839
     [Google Scholar]
  35. Jones K. A., Yamamoto K. R., Tjian R. 1985; Two distinct transcription factors bind to the HSV thymidine kinase promoter in vitro . Cell 42:559–572
     [Google Scholar]
  36. Jones K. A., Kadonago J. T., Rosenfeld P. J., Kelly T. J., Tjian R. 1987; A cellular DNA binding protein that activates eukaryotic transcription and DNA replication. Cell 48:79–89
     [Google Scholar]
  37. Keller J. M., Alwine J. C. 1984; Activation of the SV40 late promoter: direct effect of T-antigen in the absence of viral replication. Cell 36:381–389
     [Google Scholar]
  38. Keller J. M., Alwine J. C. 1985; Analysis of an activatable promoter: sequences in the simian virus 40 late promoter required for T-antigen-mediated trans-activation. Molecular and Cellular Biology 5:1859–1869
     [Google Scholar]
  39. Kim C. H., Heath C., Bertuch A., Hansen U. 1987; Specific stimulation of simian virus 40 late transcription in vitro by a cellular factor binding the simian virus 40 21-base-pair repeat promoter element. Proceedings of the National Academy of Sciences, U.S.A 84:6025–6029
     [Google Scholar]
  40. Knight G. B., Guidas J. M., Pardee A. B. 1987; Cell-cycle-specific interaction of nuclear DNA-binding proteins with a CCAAT sequence from the human thymidine kinase gene. Proceedings of the National Academy of Sciences, U.S.A 84:8350–8354
     [Google Scholar]
  41. Maity S. N., Golumbek P. L., Karsenty G., De Crumbrugghe B. 1988; Selective activation of transcription by a novel CCAAT binding factors. Science 241:582–585
     [Google Scholar]
  42. Manley J. L., Fire A., Cano A., Sharp P. A., Gefter M. L. 1980; DNA-dependent transcription and adenovirus genes in a soluble whole cell extract. Proceedings of the National Academy of Sciences, U.S.A 77:3855–3859
     [Google Scholar]
  43. Markowitz R. B., Dynan W. S. 1988; Binding of cellular proteins to the regulatory region of BK virus DNA. Journal of Virology 62:3388–3398
     [Google Scholar]
  44. May E., Omilli F., Ernoult-Lange M., Zenke M., Chambon P. 1987; The sequence motifs that are involved in SV40 enhancer function also control SV40 late promoter activity. Nucleic Acids Research 15:2445–2461
     [Google Scholar]
  45. Mermod N., Williams T. J., Tjian R. 1988; Enhancer binding factors AP-4 and AP-1 act in concert to activate SV40 late transcription in vitro . Nature, London 332:557–561
     [Google Scholar]
  46. Mitchell P. J., Tjian R. 1989; Transcriptional regulation in mammalian cells by sequence-specific DNA-binding proteins. Science 245:371–378
     [Google Scholar]
  47. Mitchell P. J., Wang C., Tjian R. 1987; Positive and negative regulation of transcription in vitro: enhancer binding protein AP-2 is inhibited by SV40 T-antigen. Cell 50:847–861
     [Google Scholar]
  48. Moens U., Sundsfjord A., Flagstad T., Traavik T. 1990; BK virus early RNA transcripts in stably transformed cells: enhanced levels induced by dibutyryl cyclic AMP, forskolin and 12-O-tetradecanoylphorbol-13-acetate treatment. Journal of General Virology 71:1461–1471
     [Google Scholar]
  49. Nagata K., Guggenheimer R. A., Hurwitz J. 1983; Specific binding of a cellular DNA replication protein to the origin of replication of adenovirus DNA. Proceedings of the National Academy of Sciences, U.S.A 80:6177–6181
     [Google Scholar]
  50. Nandi A., Das G. C., Salzman N. P. 1985; Characterization of a surrogate TATA box promoter that regulates in vitro transcription of the simian virus 40 major late gene. Molecular and Cellular Biology 5:591–594
     [Google Scholar]
  51. Omilli F., Ernoult-Lange M., Borde J., May E. 1986; Sequences involved in initiation of simian virus 40 late transcription in the absence of T-antigen. Molecular and Cellular Biology 6:1875–1885
     [Google Scholar]
  52. Padgett B. 1980; Human Papovaviruses. In Molecular Biology of DNA Tumor Viruses: DNA Tumor Viruses pp 339–370 Edited by Tooze J. New York: Cold Spring Harbor Laboratory;
     [Google Scholar]
  53. Rio D. C., Tjian R. 1984; Multiple control elements involved in the initiation of SV40 late transcription. Journal of Molecular and Applied Genetics 2:423–435
     [Google Scholar]
  54. Rosenfeld P. J., Kelly T. J. 1986; Purification of nuclear factor 1 by DNA recognition site affinity chromatography. Journal of Biological Chemistry 261:1398–1408
     [Google Scholar]
  55. Rosenfeld P. J., O’Neill E. A., Wides R. J., Kelly T. J. 1987; Sequence specific interactions between cellular DNA-binding proteins and the adenovirus DNA replication. Molecular and Cellular Biology 7:875–886
     [Google Scholar]
  56. Saffer J. D., Jackson S. P., Thruston S. J. 1990; SV40 stimulates expression of the trans-acting factor Spl at the mRNA level. Genes and Development 4:659–666
     [Google Scholar]
  57. Santoro C., Mermod N., Andrews P. C., Tjian R. 1988; Cloning of cDNAs encoding human CCAAT-box binding proteins: a family of transcription and replication factors. Nature, 1-ondon 334:218–224
     [Google Scholar]
  58. Sawadogo M., Roeder R. G. 1985; Factors involved in specific transcription by human RNA polymerase II: analysis by a rapid and quantitative in vitro assay. Proceedings of the National Academy of Sciences, U.S.A 82:4394–4398
     [Google Scholar]
  59. Schorpp M., Kuglor W., Wagner U., Ryffel G. U. 1988; Hepatocyte-specific promoter element HP-1 of the Xenopus albumin gene interacts with transcriptional factors of mammalian hepato-cytes. Journal of Molecular Biology 202:307–320
     [Google Scholar]
  60. Seif I., Khoury G., Dhar R. 1979; The genome of human papovavirus BKV. Cell 18:963–977
     [Google Scholar]
  61. Somasekhar M. B., Mertz J. E. 1985; Sequences involved in determining the locations of 5′ ends of the late RNAs of simian virus 40. Journal of Virology 56:1002–1013
     [Google Scholar]
  62. Vecchio D. M. A., Steinman R. A., Ricciardi R. P. 1989; An element of the BK virus enhancer required for DNA replication. Journal of Virology 63:1519–1524
     [Google Scholar]
  63. Watanabe S., Yoshiike K. 1982; Change of DNA near the origin of replication enhances the transcriptional capacity of human papovavirus BK. Journal of Virology 42:978–985
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-72-8-1935
Loading
Proteins of the Nuclear Factor-1 Family Act As An Activator of the Late Promoter in Human Polyomavirus BK in vitro 1
J. Gen. Virol. 72, 1935 (1991); https://doi.org/10.1099/0022-1317-72-8-1935
/content/journal/jgv/10.1099/0022-1317-72-8-1935
/content/journal/jgv/10.1099/0022-1317-72-8-1935
Loading

Data & Media loading...

Most cited 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