Functional interaction of the v-Rel and c-Rel oncoproteins with the TATA-binding protein and association with transcription factor IIB. (original) (raw)

Mol Cell Biol. 1993 Nov; 13(11): 6733–6741.

Center for Advanced Biotechnology and Medicine, Robert Wood Johnson Medical School, University of Medicine and Dentistry of New Jersey, Piscataway 08854-5638.

Abstract

Rel family proteins regulate the expression of genes linked to kappa B-binding motifs. Little is known, however, of the mechanism by which they enhance transcription. We have investigated the ability of the v-Rel and c-Rel oncoproteins to interact with components of the basal transcription machinery. Here we report that both the acidic transcription activation domain mapping to the unique C terminus of chicken c-Rel and the F9 cell-specific activation region common to both v-Rel and c-Rel interact with the TATA-binding protein (TBP) and transcription factor IIB (TFIIB) in vitro and in vivo. We also demonstrate that TPB interaction with Rel activation regions leads to synergistic activation of transcription of a kappa B-linked reporter gene. Combined with the observation that the mouse c-Rel and human RelA proteins also interact with TBP and TFIIB in vitro, these results suggest that association with basal transcription factors is important for the transcriptional activities of Rel family proteins.

Full text

Full text is available as a scanned copy of the original print version. Get a printable copy (PDF file) of the complete article (2.0M), or click on a page image below to browse page by page. Links to PubMed are also available for Selected References.

Images in this article

Click on the image to see a larger version.

Selected References

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

Ballard DW, Walker WH, Doerre S, Sista P, Molitor JA, Dixon EP, Peffer NJ, Hannink M, Greene WC. The v-rel oncogene encodes a kappa B enhancer binding protein that inhibits NF-kappa B function. Cell. 1990 Nov 16;63(4):803–814. [PubMed] [Google Scholar]
Blank V, Kourilsky P, Israël A. NF-kappa B and related proteins: Rel/dorsal homologies meet ankyrin-like repeats. Trends Biochem Sci. 1992 Apr;17(4):135–140. [PubMed] [Google Scholar]
Bose HR., Jr The Rel family: models for transcriptional regulation and oncogenic transformation. Biochim Biophys Acta. 1992 Sep 14;1114(1):1–17. [PubMed] [Google Scholar]
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. [PubMed] [Google Scholar]
Bull P, Morley KL, Hoekstra MF, Hunter T, Verma IM. The mouse c-rel protein has an N-terminal regulatory domain and a C-terminal transcriptional transactivation domain. Mol Cell Biol. 1990 Oct;10(10):5473–5485. [PMC free article] [PubMed] [Google Scholar]
Capobianco AJ, Simmons DL, Gilmore TD. Cloning and expression of a chicken c-rel cDNA: unlike p59v-rel, p68c-rel is a cytoplasmic protein in chicken embryo fibroblasts. Oncogene. 1990 Mar;5(3):257–265. [PubMed] [Google Scholar]
Chen C, Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. [PMC free article] [PubMed] [Google Scholar]
Chou PY, Fasman GD. Empirical predictions of protein conformation. Annu Rev Biochem. 1978;47:251–276. [PubMed] [Google Scholar]
Colgan J, Wampler S, Manley JL. Interaction between a transcriptional activator and transcription factor IIB in vivo. Nature. 1993 Apr 8;362(6420):549–553. [PubMed] [Google Scholar]
Dougherty JP, Wisniewski R, Yang SL, Rhode BW, Temin HM. New retrovirus helper cells with almost no nucleotide sequence homology to retrovirus vectors. J Virol. 1989 Jul;63(7):3209–3212. [PMC free article] [PubMed] [Google Scholar]
Garson K, Percival H, Kang CY. The N-terminal env-derived amino acids of v-rel are required for full transforming activity. Virology. 1990 Jul;177(1):106–115. [PubMed] [Google Scholar]
Ghosh S, Gifford AM, Riviere LR, Tempst P, Nolan GP, Baltimore D. Cloning of the p50 DNA binding subunit of NF-kappa B: homology to rel and dorsal. Cell. 1990 Sep 7;62(5):1019–1029. [PubMed] [Google Scholar]
Gilmore TD, Temin HM. v-rel oncoproteins in the nucleus and in the cytoplasm transform chicken spleen cells. J Virol. 1988 Mar;62(3):703–714. [PMC free article] [PubMed] [Google Scholar]
Gorman CM, Moffat LF, Howard BH. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. [PMC free article] [PubMed] [Google Scholar]
Greenblatt J. Transcription. Riding high on the TATA box. Nature. 1992 Nov 5;360(6399):16–17. [PubMed] [Google Scholar]
Ha I, Roberts S, Maldonado E, Sun X, Kim LU, Green M, Reinberg D. Multiple functional domains of human transcription factor IIB: distinct interactions with two general transcription factors and RNA polymerase II. Genes Dev. 1993 Jun;7(6):1021–1032. [PubMed] [Google Scholar]
Hagemeier C, Bannister AJ, Cook A, Kouzarides T. The activation domain of transcription factor PU.1 binds the retinoblastoma (RB) protein and the transcription factor TFIID in vitro: RB shows sequence similarity to TFIID and TFIIB. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1580–1584. [PMC free article] [PubMed] [Google Scholar]
Hagemeier C, Walker S, Caswell R, Kouzarides T, Sinclair J. The human cytomegalovirus 80-kilodalton but not the 72-kilodalton immediate-early protein transactivates heterologous promoters in a TATA box-dependent mechanism and interacts directly with TFIID. J Virol. 1992 Jul;66(7):4452–4456. [PMC free article] [PubMed] [Google Scholar]
Hahn S. Structure(?) and function of acidic transcription activators. Cell. 1993 Feb 26;72(4):481–483. [PubMed] [Google Scholar]
Han K, Levine MS, Manley JL. Synergistic activation and repression of transcription by Drosophila homeobox proteins. Cell. 1989 Feb 24;56(4):573–583. [PubMed] [Google Scholar]
Horikoshi N, Maguire K, Kralli A, Maldonado E, Reinberg D, Weinmann R. Direct interaction between adenovirus E1A protein and the TATA box binding transcription factor IID. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5124–5128. [PMC free article] [PubMed] [Google Scholar]
Inoue J, Kerr LD, Ransone LJ, Bengal E, Hunter T, Verma IM. c-rel activates but v-rel suppresses transcription from kappa B sites. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3715–3719. [PMC free article] [PubMed] [Google Scholar]
Kamens J, Richardson P, Mosialos G, Brent R, Gilmore T. Oncogenic transformation by vrel requires an amino-terminal activation domain. Mol Cell Biol. 1990 Jun;10(6):2840–2847. [PMC free article] [PubMed] [Google Scholar]
Kumar S, Rabson AB, Gélinas C. The RxxRxRxxC motif conserved in all Rel/kappa B proteins is essential for the DNA-binding activity and redox regulation of the v-Rel oncoprotein. Mol Cell Biol. 1992 Jul;12(7):3094–3106. [PMC free article] [PubMed] [Google Scholar]
Lee WS, Kao CC, Bryant GO, Liu X, Berk AJ. Adenovirus E1A activation domain binds the basic repeat in the TATA box transcription factor. Cell. 1991 Oct 18;67(2):365–376. [PubMed] [Google Scholar]
Leuther KK, Salmeron JM, Johnston SA. Genetic evidence that an activation domain of GAL4 does not require acidity and may form a beta sheet. Cell. 1993 Feb 26;72(4):575–585. [PubMed] [Google Scholar]
Lieberman PM, Berk AJ. The Zta trans-activator protein stabilizes TFIID association with promoter DNA by direct protein-protein interaction. Genes Dev. 1991 Dec;5(12B):2441–2454. [PubMed] [Google Scholar]
Lillie JW, Green MR. Transcription activation by the adenovirus E1a protein. Nature. 1989 Mar 2;338(6210):39–44. [PubMed] [Google Scholar]
Lin YS, Green MR. Mechanism of action of an acidic transcriptional activator in vitro. Cell. 1991 Mar 8;64(5):971–981. [PubMed] [Google Scholar]
Lin YS, Ha I, Maldonado E, Reinberg D, Green MR. Binding of general transcription factor TFIIB to an acidic activating region. Nature. 1991 Oct 10;353(6344):569–571. [PubMed] [Google Scholar]
McDonnell PC, Kumar S, Rabson AB, Gélinas C. Transcriptional activity of rel family proteins. Oncogene. 1992 Jan;7(1):163–170. [PubMed] [Google Scholar]
Mosialos G, Hamer P, Capobianco AJ, Laursen RA, Gilmore TD. A protein kinase-A recognition sequence is structurally linked to transformation by p59v-rel and cytoplasmic retention of p68c-rel. Mol Cell Biol. 1991 Dec;11(12):5867–5877. [PMC free article] [PubMed] [Google Scholar]
Nakayama K, Shimizu H, Mitomo K, Watanabe T, Okamoto S, Yamamoto K. A lymphoid cell-specific nuclear factor containing c-Rel-like proteins preferentially interacts with interleukin-6 kappa B-related motifs whose activities are repressed in lymphoid cells. Mol Cell Biol. 1992 Apr;12(4):1736–1746. [PMC free article] [PubMed] [Google Scholar]
Pugh BF, Tjian R. Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell. 1990 Jun 29;61(7):1187–1197. [PubMed] [Google Scholar]
Richardson PM, Gilmore TD. vRel is an inactive member of the Rel family of transcriptional activating proteins. J Virol. 1991 Jun;65(6):3122–3130. [PMC free article] [PubMed] [Google Scholar]
Ruben SM, Dillon PJ, Schreck R, Henkel T, Chen CH, Maher M, Baeuerle PA, Rosen CA. Isolation of a rel-related human cDNA that potentially encodes the 65-kD subunit of NF-kappa B. Science. 1991 Mar 22;251(5000):1490–1493. [PubMed] [Google Scholar]
Sadowski I, Ma J, Triezenberg S, Ptashne M. GAL4-VP16 is an unusually potent transcriptional activator. Nature. 1988 Oct 6;335(6190):563–564. [PubMed] [Google Scholar]
Sarkar S, Gilmore TD. Transformation by the vRel oncoprotein requires sequences carboxy-terminal to the Rel homology domain. Oncogene. 1993 Aug;8(8):2245–2252. [PubMed] [Google Scholar]
Seto E, Usheva A, Zambetti GP, Momand J, Horikoshi N, Weinmann R, Levine AJ, Shenk T. Wild-type p53 binds to the TATA-binding protein and represses transcription. Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):12028–12032. [PMC free article] [PubMed] [Google Scholar]
Simek S, Rice NR. p59v-rel, the transforming protein of reticuloendotheliosis virus, is complexed with at least four other proteins in transformed chicken lymphoid cells. J Virol. 1988 Dec;62(12):4730–4736. [PMC free article] [PubMed] [Google Scholar]
Stringer KF, Ingles CJ, Greenblatt J. Direct and selective binding of an acidic transcriptional activation domain to the TATA-box factor TFIID. Nature. 1990 Jun 28;345(6278):783–786. [PubMed] [Google Scholar]
Tanaka M, Herr W. Differential transcriptional activation by Oct-1 and Oct-2: interdependent activation domains induce Oct-2 phosphorylation. Cell. 1990 Feb 9;60(3):375–386. [PubMed] [Google Scholar]
Truant R, Xiao H, Ingles CJ, Greenblatt J. Direct interaction between the transcriptional activation domain of human p53 and the TATA box-binding protein. J Biol Chem. 1993 Feb 5;268(4):2284–2287. [PubMed] [Google Scholar]
Van Hoy M, Leuther KK, Kodadek T, Johnston SA. The acidic activation domains of the GCN4 and GAL4 proteins are not alpha helical but form beta sheets. Cell. 1993 Feb 26;72(4):587–594. [PubMed] [Google Scholar]
Walker WH, Stein B, Ganchi PA, Hoffman JA, Kaufman PA, Ballard DW, Hannink M, Greene WC. The v-rel oncogene: insights into the mechanism of transcriptional activation, repression, and transformation. J Virol. 1992 Aug;66(8):5018–5029. [PMC free article] [PubMed] [Google Scholar]
Zawel L, Reinberg D. Advances in RNA polymerase II transcription. Curr Opin Cell Biol. 1992 Jun;4(3):488–495. [PubMed] [Google Scholar]
Zawel L, Reinberg D. Initiation of transcription by RNA polymerase II: a multi-step process. Prog Nucleic Acid Res Mol Biol. 1993;44:67–108. [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis