Abstract
Eukaryotic ribosomal gene promoters are preceded by a terminator element which is recognized by the transcription termination factor TTF-I. We have studied the function of this promoter-proximal terminator and show that binding of TTF-I is the key event which leads to ATP-dependent nucleosome remodeling and transcriptional activation of mouse rDNA pre-assembled into chromatin. We have analyzed TTF-I mutants for their ability to bind to free or nucleosomal DNA, and show that the DNA binding domain of TTF-I on its own is not sufficient for interaction with chromatin, indicating that specific protein features exist that endow a transcription factor with chromatin binding and remodeling properties. This first analysis of RNA polymerase I transcription in chromatin provides a clue for the function of the upstream terminator and establishes a dual role for TTF-I both as a termination factor and a chromatin-specific transcription activator.
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Selected References
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- Becker P. B. The establishment of active promoters in chromatin. Bioessays. 1994 Aug;16(8):541–547. doi: 10.1002/bies.950160807. [DOI] [PubMed] [Google Scholar]
- Elgin S. C. The formation and function of DNase I hypersensitive sites in the process of gene activation. J Biol Chem. 1988 Dec 25;263(36):19259–19262. [PubMed] [Google Scholar]
- Evers R., Smid A., Rudloff U., Lottspeich F., Grummt I. Different domains of the murine RNA polymerase I-specific termination factor mTTF-I serve distinct functions in transcription termination. EMBO J. 1995 Mar 15;14(6):1248–1256. doi: 10.1002/j.1460-2075.1995.tb07108.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grummt I., Maier U., Ohrlein A., Hassouna N., Bachellerie J. P. Transcription of mouse rDNA terminates downstream of the 3' end of 28S RNA and involves interaction of factors with repeated sequences in the 3' spacer. Cell. 1985 Dec;43(3 Pt 2):801–810. doi: 10.1016/0092-8674(85)90253-3. [DOI] [PubMed] [Google Scholar]
- Grummt I., Rosenbauer H., Niedermeyer I., Maier U., Ohrlein A. A repeated 18 bp sequence motif in the mouse rDNA spacer mediates binding of a nuclear factor and transcription termination. Cell. 1986 Jun 20;45(6):837–846. doi: 10.1016/0092-8674(86)90558-1. [DOI] [PubMed] [Google Scholar]
- Henderson S., Sollner-Webb B. A transcriptional terminator is a novel element of the promoter of the mouse ribosomal RNA gene. Cell. 1986 Dec 26;47(6):891–900. doi: 10.1016/0092-8674(86)90804-4. [DOI] [PubMed] [Google Scholar]
- Kuhn A., Bartsch I., Grummt I. Specific interaction of the murine transcription termination factor TTF I with class-I RNA polymerases. Nature. 1990 Apr 5;344(6266):559–562. doi: 10.1038/344559a0. [DOI] [PubMed] [Google Scholar]
- Kulkens T., van der Sande C. A., Dekker A. F., van Heerikhuizen H., Planta R. J. A system to study transcription by yeast RNA polymerase I within the chromosomal context: functional analysis of the ribosomal DNA enhancer and the RBP1/REB1 binding sites. EMBO J. 1992 Dec;11(12):4665–4674. doi: 10.1002/j.1460-2075.1992.tb05568.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lucchini R., Sogo J. M. Replication of transcriptionally active chromatin. Nature. 1995 Mar 16;374(6519):276–280. doi: 10.1038/374276a0. [DOI] [PubMed] [Google Scholar]
- McStay B., Reeder R. H. A termination site for Xenopus RNA polymerase I also acts as an element of an adjacent promoter. Cell. 1986 Dec 26;47(6):913–920. doi: 10.1016/0092-8674(86)90806-8. [DOI] [PubMed] [Google Scholar]
- Morrow B. E., Johnson S. P., Warner J. R. Proteins that bind to the yeast rDNA enhancer. J Biol Chem. 1989 May 25;264(15):9061–9068. [PubMed] [Google Scholar]
- Morse R. H. Nucleosome disruption by transcription factor binding in yeast. Science. 1993 Dec 3;262(5139):1563–1566. doi: 10.1126/science.8248805. [DOI] [PubMed] [Google Scholar]
- Pazin M. J., Sheridan P. L., Cannon K., Cao Z., Keck J. G., Kadonaga J. T., Jones K. A. NF-kappa B-mediated chromatin reconfiguration and transcriptional activation of the HIV-1 enhancer in vitro. Genes Dev. 1996 Jan 1;10(1):37–49. doi: 10.1101/gad.10.1.37. [DOI] [PubMed] [Google Scholar]
- Sandaltzopoulos R., Blank T., Becker P. B. Transcriptional repression by nucleosomes but not H1 in reconstituted preblastoderm Drosophila chromatin. EMBO J. 1994 Jan 15;13(2):373–379. doi: 10.1002/j.1460-2075.1994.tb06271.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnapp A., Grummt I. Transcription complex formation at the mouse rDNA promoter involves the stepwise association of four transcription factors and RNA polymerase I. J Biol Chem. 1991 Dec 25;266(36):24588–24595. [PubMed] [Google Scholar]
- Svaren J., Schmitz J., Hörz W. The transactivation domain of Pho4 is required for nucleosome disruption at the PHO5 promoter. EMBO J. 1994 Oct 17;13(20):4856–4862. doi: 10.1002/j.1460-2075.1994.tb06812.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taylor I. C., Workman J. L., Schuetz T. J., Kingston R. E. Facilitated binding of GAL4 and heat shock factor to nucleosomal templates: differential function of DNA-binding domains. Genes Dev. 1991 Jul;5(7):1285–1298. doi: 10.1101/gad.5.7.1285. [DOI] [PubMed] [Google Scholar]
- Tsukiyama T., Wu C. Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell. 1995 Dec 15;83(6):1011–1020. doi: 10.1016/0092-8674(95)90216-3. [DOI] [PubMed] [Google Scholar]
- Varga-Weisz P. D., Blank T. A., Becker P. B. Energy-dependent chromatin accessibility and nucleosome mobility in a cell-free system. EMBO J. 1995 May 15;14(10):2209–2216. doi: 10.1002/j.1460-2075.1995.tb07215.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wallrath L. L., Lu Q., Granok H., Elgin S. C. Architectural variations of inducible eukaryotic promoters: preset and remodeling chromatin structures. Bioessays. 1994 Mar;16(3):165–170. doi: 10.1002/bies.950160306. [DOI] [PubMed] [Google Scholar]
- Wilson C. J., Chao D. M., Imbalzano A. N., Schnitzler G. R., Kingston R. E., Young R. A. RNA polymerase II holoenzyme contains SWI/SNF regulators involved in chromatin remodeling. Cell. 1996 Jan 26;84(2):235–244. doi: 10.1016/s0092-8674(00)80978-2. [DOI] [PubMed] [Google Scholar]
- Wu C. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature. 1980 Aug 28;286(5776):854–860. doi: 10.1038/286854a0. [DOI] [PubMed] [Google Scholar]