1887

Abstract

Tat strongly stimulates transcription of the human immunodeficiency type 1 (HIV-1) provirus by interacting with various cellular transcription factors, including TFIID. The results presented in this report indicate that the effect exerted by Tat also involves an interaction with TFIIB. A direct protein-protein interaction between Tat and TFIIB was observed . Detailed analysis of this interaction showed that the cysteine-rich and core domains of Tat bind to the N-terminal moiety of the general transcription factor. The role of the interaction between Tat and TFIIB in the activation of the entire HIV-1 promoter was analysed. Transfection experiments performed using a reporter construct containing the HIV-1 long terminal repeat fused to a reporter gene showed that overexpression of TFIIB progressively suppressed Tat-induced transcription. This effect was weakened by an increase in the intracellular con centration of Tat. A similar consequence of TFIIB overexpression was observed in a HeLa cell line stably transformed with a construct corresponding to the gene under the control of the HIV-1 promoter. Mutants of TFIIB which differed in their ability to interact with Tat and to function in basal transcription were analysed. The ability of TFIIB mutants defective for basal transcription to inhibit Tat-induced activity of the HIV-1 promoter depended on their capacity to interact with Tat. Mutants of TFIIB functional for basal transcription, but defective for the interaction with Tat, exhibited a dominant negative effect. From these data we propose a model in which interaction between Tat and both general transcription factors TBP and TFIIB maintains the transcriptional initiation complex in an active configuration.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-78-9-2235
1997-09-01
2024-12-12
Loading full text...

Full text loading...

/deliver/fulltext/jgv/78/9/9292011.html?itemId=/content/journal/jgv/10.1099/0022-1317-78-9-2235&mimeType=html&fmt=ahah

References

  1. Bagasra O., Khalili K., Seshamma T., Taylor J. P., Pomerantz R. J. 1992; TAR-independent replication of human immunodeficiency virus type 1 in glial cells. Journal of Virology 66:7522–7528
    [Google Scholar]
  2. Bagby S., Kim S., Maldonado E., Tong K. I., Reinberg D., Ikura M. 1995; Solution structure of the C-terminal core domain of human TFIIB: similarity to cyclin A and interaction with TATA-binding protein. Cell 82:857–867
    [Google Scholar]
  3. Baniahmad A., Ha I., Reinberg D., Tsai S., Tsai M. J., O’Malley B. W. 1993; Interaction of human thyroid hormone receptor beta with transcription factor TFIIB may mediate target gene derepression and activation by thyroid hormone. Proceedings of the National Academy of Sciences, USA 90:8832–8836
    [Google Scholar]
  4. Barberis A., Muller C. W., Harrison S. C., Ptashne M. 1993; Delineation of two functional regions of transcription factor TFIIB. Proceedings of the National Academy of Sciences, USA 90:5628–5632
    [Google Scholar]
  5. Berkhout B., Gatignol A., Rabson A. B., Jeang K.-T. 1990; TAR- independent activation of the HIV-1 LTR: evidence that Tat requires specific region of the promoter. Cell 62:757–767
    [Google Scholar]
  6. Bogerd H. P., Fridell R. A., Blair W. S., Cullen B. R. 1993; Genetic evidence that the Tat proteins of human immunodeficiency virus types 1 and 2 can multimerize in the eukaryotic cell nucleus. Journal of Virology 67:5030–5034
    [Google Scholar]
  7. Chiang C.-M., Roeder R. G. 1995; Cloning of an intrinsic human TFIID subunit that interacts with multiple transcriptional activators. Science 267:531–536
    [Google Scholar]
  8. Clavel F., Charneau P. 1994; Fusion from without directed by human immunodeficiency virus particles. Journal of Virology 68:1179–1185
    [Google Scholar]
  9. Colgan J., Wampler S., Manley J. L. 1993; Interaction between a transcriptional activator and transcription factor IIB in vivo . Nature 362:549–553
    [Google Scholar]
  10. Colgan J., Ashali H., Manley J. L. 1995; A direct interaction between a glutamine-rich activator and the N terminus of TFIIB can mediate transcriptional activation in vivo . Molecular and Cellular Biology 15:2311–2320
    [Google Scholar]
  11. Dingwall C., Ernberg I., Gait M. J., Green S. M., Heaphy S., Karn J., Lowe A. D., Singh M., Skinner M. A., Vallerio R. 1989; Human immunodeficiency virus Tat protein binds transactivation responsive region (TAR) RNA in vitro . Proceedings of the National Academy of Sciences, USA 86:6925–6929
    [Google Scholar]
  12. Emerman M., Guyader M., Montagnier L., Baltimore D., Muesing M. A. 1987; The specificity of the human immunodeficiency virus type 2 transactivator is different from that of human immunodeficiency virus type 1. EMBO Journal 6:3755–3760
    [Google Scholar]
  13. Farr A., Roman A. 1992; A pitfall of using a second plasmid to determine transfection efficiency. Nucleic Acids Research 20:920
    [Google Scholar]
  14. Gorman C., Moffat L., Howard B. 1982; Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Molecular and Cellular Biology 2:1044–1051
    [Google Scholar]
  15. Green M., Ishino M., Loewenstein P. M. 1989; Mutational analysis of HIV-1 Tat minimal domain peptides: identification of trans-dominant mutants that suppress HIV-LTR-driven gene expression. Cell 58:215–223
    [Google Scholar]
  16. Ha I., Lane W. S., Reinberg D. 1991; Cloning of a human gene encoding the general transcription initiation factor IIB. Nature 352:689–695
    [Google Scholar]
  17. Ha I., Roberts S., Maldonado E., Sun X., Kim L. U., Green M., Reinberg D. 1993; Multiple functional domains of human transcription factor IIB: distinct interactions with two general transcription factors and RNA polymerase II. Genes & Development 7:1021–1032
    [Google Scholar]
  18. Hauber J., Perkins A., Heimer E. P., Cullen B. R. 1987; Transactivation of human immunodeficiency virus gene expression is mediated by nuclear events. Proceedings of the National Academy of Sciences, USA 84:6364–6368
    [Google Scholar]
  19. Hisatake K., Roeder R. G., Horikoshi M. 1993; Functional dissection of TFIIB domains required for TFIIB-TFIID-promoter complex formation and basal transcription activity. Nature 363:744–747
    [Google Scholar]
  20. Ho D. D., Neumann A. U., Perelson A. S., Chen W., Leonard J. M., Markowitz M. 1995; Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373:123–126
    [Google Scholar]
  21. Jeang K.-T., Chun R., Lin N. H., Gatignol A., Glabe C. G., Fan H. 1993; In vitro and in vivo binding of human immunodeficiency virus type 1 Tat protein and Sp1 transcription factor. Journal of Virology 67:6224–6233
    [Google Scholar]
  22. Jones K. A. 1993; Tat and the HIV-1 promoter. Current Opinion in Cell Biology 5:461–468
    [Google Scholar]
  23. Kamine J., Chinnadurai G. 1992; Synergistic activation of the human immunodeficiency virus type 1 promoter by the viral Tat protein and cellular transcription factor Sp1. Journal of Virology 66:3932–3936
    [Google Scholar]
  24. Kamine J., Subramanian T., Chinnadurai G. 1993; Activation of a heterologous promoter by human immunodeficiency virus type 1 Tat requires Sp1 and is distinct from the mode of activation by acidic transcriptional activators. Journal of Virology 67:6828–6834
    [Google Scholar]
  25. Kashanchi F., Piras G., Radonovich M. F., Duvall J. F., Fattaey A., Chiang C.-M., Roeder R. G., Brady J. N. 1994; Direct interaction of human TFIID with the HIV-1 transactivator Tat. Nature 367:295–299
    [Google Scholar]
  26. Kato H., Sumimoto H., Pognonec P., Chen C.-H., Rosen C. A., Roeder R. G. 1992; HIV-1 Tat acts as a processivity factor in vitro in conjunction with cellular elongation factors. Genes & Development 6:655–666
    [Google Scholar]
  27. Kim T. K., Roeder R. G. 1994; Proline-rich activator CTF1 targets the TFIIB assembly step during transcriptional activation. Proceedings of the National Academy of Sciences, USA 91:4170–4174
    [Google Scholar]
  28. Kuppuswamy M., Subramanian T., Srinivasan A., Chinnadurai G. 1989; Multiple functional domains of Tat, the trans-activator of HIV-1 defined by mutational analysis. Nucleci Acids Research 17:3551–3561
    [Google Scholar]
  29. Laspia M. F., Rice A. P., Mathews M. B. 1989; HIV-1 Tat protein increases transcriptional initiation and stabilizes elongation. Cell 59:283–292
    [Google Scholar]
  30. Lin Y.-S., Green M. R. 1991; Mechanism of action of an acidic transcriptional activator in vitro . Cell 64:971–981
    [Google Scholar]
  31. Malik S., Hisatake K., Sumimoto H., Horikoshi M., Roeder R. G. 1991; Sequence of general transcription factor TFIIB and relationships to other initiation factors. Proceedings of the National Academy of Sciences, USA 88:9553–9557
    [Google Scholar]
  32. Malik S., Lee D. K., Roeder R. G. 1993; Potential RNA polymerase II-induced interactions of transcription factor TFIIB. Molecular and Cellular Biology 13:6253–6259
    [Google Scholar]
  33. Marciniak R. A., Calnan B. J., Frankel A. D., Sharp P. A. 1990; HIV-1 Tat protein trans-activates transcription in vitro . Cell 63:791–802
    [Google Scholar]
  34. Moncollin V., Schaeffer L., Chalut C., Egly J. M. 1992; Expression in Escherichia coli: purification and properties of the recombinant human general transcription factor rTFIIB. Protein Expression and Purification 3:374–379
    [Google Scholar]
  35. Nikolov D. B., Chen H., Halay E. D., Usheva A. A., Hisatake K., Lee D. K., Roeder R. G., Burley S. K. 1995; Crystal structure of a TFIIB-TBP-TATA-element ternary complex. Nature 377:119–128
    [Google Scholar]
  36. Roberts S. G., Choy B., Walker S. S., Lin Y.-S., Green M. R. 1995; A role for activator-mediated TFIIB recruitment in diverse aspects of transcriptional regulation. Current Biology 5:508–516
    [Google Scholar]
  37. Roberts S. G., Green M. R. 1994; Activator-induced conformational change in general transcription factor TFIIB. Nature 371:717–720
    [Google Scholar]
  38. Roberts S. G., Ha I., Maldonado E., Reinberg D., Green M. R. 1993; Interaction between an acidic activator and transcription factor TFIIB is required for transcriptional activation. Nature 363:741–744
    [Google Scholar]
  39. Selby M. J., Bain E. S., Luciw P. A., Peterlin B. M. 1990; Trans-activation by HIV-1 Tat via a heterologous RNA binding protein. Cell 62:769–776
    [Google Scholar]
  40. Southgate C., Zapp M. L., Green M. R. 1990; Activation of transcription by HIV-1 Tat protein tethered to nascent RNA through another protein. Nature 345:640–642
    [Google Scholar]
  41. Southgate C. D., Green M. R. 1991; The HIV-1 Tat protein activates transcription from an upstream DNA-binding site : implications for Tat function. Genes & Development 5:2496–2507
    [Google Scholar]
  42. Taylor J. P., Pomerantz R., Bagasra O., Chowdhury M., Rappaport J., Khalili K., Amini S. 1992; TAR-independent transactivation by Tat in cells derived from the CNS: a novel mechanism of HIV-1 gene regulation. EMBO Journal 11:3395–3403
    [Google Scholar]
  43. Taylor J. P., Pomerantz R. J., Oakes J. W., Khalili K., Amini S. 1995; A CNS-enriched factor that binds to NF-kB and is required for interaction with HIV-1 Tat. Oncogene 10:395–400
    [Google Scholar]
  44. Veschambre P., Simard P., Jalinot P. 1995; Evidence for functional interaction between the HIV-1 Tat transactivator and the TATA box binding protein in vivo . Journal of Molecular Biology 250:169–180
    [Google Scholar]
  45. Wei X., Ghosh S. K., Taylor M. E., Johnson V. A., Emini E. A., Deutsch P., Lifson J. D., Bonhoeffer S., Nowak M. A., Hahn B. H., Saag M. S., Shaw G. M. 1995; Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373:117–122
    [Google Scholar]
  46. Yamashita S., Wada K., Horikoshi M., Gong D. W., Kokubo T., Hisatake K., Yokotani N., Malik S., Roeder R. G., Nakatani Y. 1992; Isolation and characterization of a cDNA encoding Drosophila transcription factor TFIIB. Proceedings of the National Academy of Sciences, USA 89:2839–2843
    [Google Scholar]
  47. Yu L., Loewenstein P. M., Zhang Z., Green M. 1995a; In vitro interaction of the human immunodeficiency virus type 1 Tat trans-activator and the general transcription factor TFIIB with the cellular protein TAP. Journal of Virology 69:3017–3023
    [Google Scholar]
  48. Yu L., Zhang Z., Loewenstein P. M., Desai K., Tang Q., Mao D., Symington J. S., Green M. 1995b; Molecular cloning and characterization of a cellular protein that interacts with the human immunodeficiency virus type 1 Tat transactivator and encodes a strong transcriptional activation domain. Journal of Virology 69:3007–3016
    [Google Scholar]
  49. Zawel L., Prasanna Kumar K., Reinberg D. 1995; Recycling ofthe general transcription factors during RNA polymerase II transcription. Genes & Development 9:1479–1490
    [Google Scholar]
  50. Zhou Q., Sharp P. A. 1995; Novel mechanism and factor for regulation by HIV-1 Tat. EMBO Journal 14:321–328
    [Google Scholar]
/content/journal/jgv/10.1099/0022-1317-78-9-2235
Loading
/content/journal/jgv/10.1099/0022-1317-78-9-2235
Loading

Data & Media loading...

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