This Article Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kassavetis, G A Articles by Geiduschek, E P Search for Related Content PubMed PubMed Citation Articles by Kassavetis, G A Articles by Geiduschek, E P

Transcription factor IIIB generates extended DNA interactions in RNA polymerase III transcription complexes on tRNA genes.

Department of Biology, University of California, San Diego, La Jolla 92093.

ABSTRACT

Transcription complexes that assemble on tRNA genes in a crude Saccharomyces cerevisiae cell extract extend over the entire transcription unit and approximately 40 base pairs of contiguous 5'-flanking DNA. We show here that the interaction with 5'-flanking DNA is due to a protein that copurifies with transcription factor TFIIIB through several steps of purification and shares characteristic properties that are normally ascribed to TFIIIB: dependence on prior binding of TFIIIC and great stability once the TFIIIC-TFIIIB-DNA complex is formed. SUP4 gene (tRNATyr) DNA that was cut within the 5'-flanking sequence (either 31 or 28 base pairs upstream of the transcriptional start site) was no longer able to stably incorporate TFIIIB into a transcription complex. The TFIIIB-dependent 5'-flanking DNA protein interaction was predominantly not sequence specific. The extension of the transcription complex into this DNA segment does suggest two possible explanations for highly diverse effects of flanking-sequence substitutions on tRNA gene transcription: either (i) proteins that are capable of binding to these upstream DNA segments are also potentially capable of stimulating or interfering with the incorporation of TFIIIB into transcription complexes or (ii) 5'-flanking sequence influences the rate of assembly of TFIIIB into stable transcription complexes.

This article has been cited by other articles:

• Chung, T., Siol, O., Dingermann, T., Winckler, T. (2007). Protein Interactions Involved in tRNA Gene-Specific Integration of Dictyostelium discoideum Non-Long Terminal Repeat Retrotransposon TRE5-A. Mol. Cell. Biol. 27: 8492-8501 [Abstract] [Full Text]  
• Rothfels, K., Rowland, O., Segall, J. (2007). Zinc fingers 1 and 7 of yeast TFIIIA are essential for assembly of a functional transcription complex on the 5 S RNA gene. Nucleic Acids Res 0: gkm517v1-13 [Abstract] [Full Text]  
• Siol, O., Boutliliss, M., Chung, T., Glockner, G., Dingermann, T., Winckler, T. (2006). Role of RNA Polymerase III Transcription Factors in the Selection of Integration Sites by the Dictyostelium Non-Long Terminal Repeat Retrotransposon TRE5-A. Mol. Cell. Biol. 26: 8242-8251 [Abstract] [Full Text]  
• Summerer, D., Chen, S., Wu, N., Deiters, A., Chin, J. W., Schultz, P. G. (2006). A genetically encoded fluorescent amino acid. Proc. Natl. Acad. Sci. USA 103: 9785-9789 [Abstract] [Full Text]  
• Kassavetis, G. A., Driscoll, R., Geiduschek, E. P. (2006). Mapping the Principal Interaction Site of the Brf1 and Bdp1 Subunits of Saccharomyces cerevisiae TFIIIB. J. Biol. Chem. 281: 14321-14329 [Abstract] [Full Text]  
• Ducrot, C., Lefebvre, O., Landrieux, E., Guirouilh-Barbat, J., Sentenac, A., Acker, J. (2006). Reconstitution of the Yeast RNA Polymerase III Transcription System with All Recombinant Factors. J. Biol. Chem. 281: 11685-11692 [Abstract] [Full Text]  
• Shivaswamy, S., Bhargava, P. (2006). Positioned Nucleosomes Due to Sequential Remodeling of the Yeast U6 Small Nuclear RNA Chromatin Are Essential for Its Transcriptional Activation. J. Biol. Chem. 281: 10461-10472 [Abstract] [Full Text]  
• Kassavetis, G. A., Steiner, D. F. (2006). Nhp6 Is a Transcriptional Initiation Fidelity Factor for RNA Polymerase III Transcription in Vitro and in Vivo. J. Biol. Chem. 281: 7445-7451 [Abstract] [Full Text]  
• Saxena, A., Ma, B., Schramm, L., Hernandez, N. (2005). Structure-Function Analysis of the Human TFIIB-Related Factor II Protein Reveals an Essential Role for the C-Terminal Domain in RNA Polymerase III Transcription. Mol. Cell. Biol. 25: 9406-9418 [Abstract] [Full Text]  
• Kassavetis, G. A., Soragni, E., Driscoll, R., Geiduschek, E. P. (2005). Reconfiguring the connectivity of a multiprotein complex: Fusions of yeast TATA-binding protein with Brf1, and the function of transcription factor IIIB. Proc. Natl. Acad. Sci. USA 102: 15406-15411 [Abstract] [Full Text]  
• Desai, N., Lee, J., Upadhya, R., Chu, Y., Moir, R. D., Willis, I. M. (2005). Two Steps in Maf1-dependent Repression of Transcription by RNA Polymerase III. J. Biol. Chem. 280: 6455-6462 [Abstract] [Full Text]  
• Ferrari, R., Rivetti, C., Acker, J., Dieci, G. (2004). Distinct roles of transcription factors TFIIIB and TFIIIC in RNA polymerase III transcription reinitiation. Proc. Natl. Acad. Sci. USA 101: 13442-13447 [Abstract] [Full Text]  
• Shivaswamy, S., Kassavetis, G. A., Bhargava, P. (2004). High-Level Activation of Transcription of the Yeast U6 snRNA Gene in Chromatin by the Basal RNA Polymerase III Transcription Factor TFIIIC. Mol. Cell. Biol. 24: 3596-3606 [Abstract] [Full Text]  
• Kassavetis, G. A., Han, S., Naji, S., Geiduschek, E. P. (2003). The Role of Transcription Initiation Factor IIIB Subunits in Promoter Opening Probed by Photochemical Cross-linking. J. Biol. Chem. 278: 17912-17917 [Abstract] [Full Text]  
• Wu, L., Pan, J., Thoroddsen, V., Wysong, D. R., Blackman, R. K., Bulawa, C. E., Gould, A. E., Ocain, T. D., Dick, L. R., Errada, P., Dorr, P. K., Parkinson, T., Wood, T., Kornitzer, D., Weissman, Z., Willis, I. M., McGovern, K. (2003). Novel Small-Molecule Inhibitors of RNA Polymerase III. Eukaryot Cell 2: 256-264 [Abstract] [Full Text]  
• Jourdain, S., Acker, J., Ducrot, C., Sentenac, A., Lefebvre, O. (2003). The tau 95 Subunit of Yeast TFIIIC Influences Upstream and Downstream Functions of TFIIIC{middle dot}DNA Complexes. J. Biol. Chem. 278: 10450-10457 [Abstract] [Full Text]  
• Schroder, O., Geiduschek, E. P., Kassavetis, G. A. (2003). A single-stranded promoter for RNA polymerase III. Proc. Natl. Acad. Sci. USA 100: 934-939 [Abstract] [Full Text]  
• Schramm, L., Hernandez, N. (2002). Recruitment of RNA polymerase III to its target promoters. Genes Dev. 16: 2593-2620 [Full Text]  
• Moir, R. D., Puglia, K. V., Willis, I. M. (2002). A Gain-of-Function Mutation in the Second Tetratricopeptide Repeat of TFIIIC131 Relieves Autoinhibition of Brf1 Binding. Mol. Cell. Biol. 22: 6131-6141 [Abstract] [Full Text]  
• Ishiguro, A., Kassavetis, G. A., Geiduschek, E. P. (2002). Essential Roles of Bdp1, a Subunit of RNA Polymerase III Initiation Factor TFIIIB, in Transcription and tRNA Processing. Mol. Cell. Biol. 22: 3264-3275 [Abstract] [Full Text]  
• Dieci, G., Giuliodori, S., Catellani, M., Percudani, R., Ottonello, S. (2002). Intragenic Promoter Adaptation and Facilitated RNA Polymerase III Recycling in the Transcription of SCR1, the 7SL RNA Gene of Saccharomyces cerevisiae. J. Biol. Chem. 277: 6903-6914 [Abstract] [Full Text]  
• Lee, B.-i., Nguyen, L. H., Barsky, D., Fernandes, M., Wilson III, D. M. (2002). Molecular interactions of human Exo1 with DNA. Nucleic Acids Res 30: 942-949 [Abstract] [Full Text]  
• Dumay-Odelot, H., Acker, J., Arrebola, R., Sentenac, A., Marck, C. (2002). Multiple Roles of the {tau}131 Subunit of Yeast Transcription Factor IIIC (TFIIIC) in TFIIIB Assembly. Mol. Cell. Biol. 22: 298-308 [Abstract] [Full Text]  
• Aye, M., Dildine, S. L., Claypool, J. A., Jourdain, S., Sandmeyer, S. B. (2001). A Truncation Mutant of the 95-Kilodalton Subunit of Transcription Factor IIIC Reveals Asymmetry in Ty3 Integration. Mol. Cell. Biol. 21: 7839-7851 [Abstract] [Full Text]  
• Hamada, M., Huang, Y., Lowe, T. M., Maraia, R. J. (2001). Widespread Use of TATA Elements in the Core Promoters for RNA Polymerases III, II, and I in Fission Yeast. Mol. Cell. Biol. 21: 6870-6881 [Abstract] [Full Text]  
• Paule, M. R., White, R. J. (2000). SURVEY AND SUMMARY Transcription by RNA polymerases I and III. Nucleic Acids Res 28: 1283-1298 [Abstract] [Full Text]  
• Ouyang, C., Martinez, M. J., Young, L. S., Sprague, K. U. (2000). TATA-Binding Protein-TATA Interaction Is a Key Determinant of Differential Transcription of Silkworm Constitutive and Silk Gland-Specific tRNAAla Genes. Mol. Cell. Biol. 20: 1329-1343 [Abstract] [Full Text]  
• Shah, S. M. A., Kumar, A., Geiduschek, E. P., Kassavetis, G. A. (1999). Alignment of the B" Subunit of RNA Polymerase III Transcription Factor IIIB in Its Promoter Complex. J. Biol. Chem. 274: 28736-28744 [Abstract] [Full Text]  
• Bhargava, P., Kassavetis, G. A. (1999). Abortive Initiation by Saccharomyces cerevisiae RNA Polymerase III. J. Biol. Chem. 274: 26550-26556 [Abstract] [Full Text]  
• Persinger, J., Sengupta, S. M., Bartholomew, B. (1999). Spatial Organization of the Core Region of Yeast TFIIIB-DNA Complexes. Mol. Cell. Biol. 19: 5218-5234 [Abstract] [Full Text]  
• Kassavetis, G. A., Kumar, A., Ramirez, E., Geiduschek, E. P. (1998). Functional and Structural Organization of Brf, the TFIIB-Related Component of the RNA Polymerase III Transcription Initiation Complex. Mol. Cell. Biol. 18: 5587-5599 [Abstract] [Full Text]  
• Zaragoza, D., Ghavidel, A., Heitman, J., Schultz, M. C. (1998). Rapamycin Induces the G0 Program of Transcriptional Repression in Yeast by Interfering with the TOR Signaling Pathway. Mol. Cell. Biol. 18: 4463-4470 [Abstract] [Full Text]  
• Manaud, N., Arrebola, R., Buffin-Meyer, B., Lefebvre, O., Voss, H., Riva, M., Conesa, C., Sentenac, A. (1998). A Chimeric Subunit of Yeast Transcription Factor IIIC Forms a Subcomplex with tau 95. Mol. Cell. Biol. 18: 3191-3200 [Abstract] [Full Text]  
• Damania, B., Mital, R., Alwine, J. C. (1998). Simian Virus 40 Large T Antigen Interacts with Human TFIIB-Related Factor and Small Nuclear RNA-Activating Protein Complex for Transcriptional Activation of TATA-Containing Polymerase III Promoters. Mol. Cell. Biol. 18: 1331-1338 [Abstract] [Full Text]  
• Arrebola, R., Manaud, N., Rozenfeld, S., Marsolier, M.-C., Lefebvre, O., Carles, C., Thuriaux, P., Conesa, C., Sentenac, A. (1998). tau 91, an Essential Subunit of Yeast Transcription Factor IIIC, Cooperates with tau 138 in DNA Binding. Mol. Cell. Biol. 18: 1-9 [Abstract] [Full Text]  
• Rowland, O., Segall, J. (1998). A Hydrophobic Segment within the 81-Amino-Acid Domain of TFIIIA from Saccharomyces cerevisiae Is Essential for Its Transcription Factor Activity. Mol. Cell. Biol. 18: 420-432 [Abstract] [Full Text]  
• Studitsky, V. M., Kassavetis, G. A., Geiduschek, E. P., Felsenfeld, G. (1997). Mechanism of Transcription Through the Nucleosome by Eukaryotic RNA Polymerase. Science 278: 1960-1963 [Abstract] [Full Text]  
• Ghavidel, A., Schultz, M. C. (1997). Casein kinase II regulation of yeast TFIIIB is mediated by the TATA-binding protein. Genes Dev. 11: 2780-2789 [Abstract] [Full Text]  
• Huet, J., Conesa, C., Carles, C., Sentenac, A. (1997). A Cryptic DNA Binding Domain at the COOH Terminus of TFIIIB70 Affects Formation, Stability, and Function of Preinitiation Complexes. J. Biol. Chem. 272: 18341-18349 [Abstract] [Full Text]  
• Librizzi, M. D., Moir, R. D., Brenowitz, M., Willis, I. M. (1996). Expression and Purification of the RNA Polymerase III Transcription Specificity Factor IIIB70 from Saccharomyces cerevisiae and Its Cooperative Binding with TATA-binding Protein. J. Biol. Chem. 271: 32695-32701 [Abstract] [Full Text]  
• Clarke, E. M., Peterson, C. L., Brainard, A. V., Riggs, D. L. (1996). Regulation of the RNA Polymerase I and III Transcription Systems in Response to Growth Conditions. J. Biol. Chem. 271: 22189-22195 [Abstract] [Full Text]  
• Joazeiro, C A, Kassavetis, G A, Geiduschek, E P (1996). Alternative outcomes in assembly of promoter complexes: the roles of TBP and a flexible linker in placing TFIIIB on tRNA genes.. Genes Dev. 10: 725-739 [Abstract]  
• Devine, S E, Boeke, J D (1996). Integration of the yeast retrotransposon Ty1 is targeted to regions upstream of genes transcribed by RNA polymerase III.. Genes Dev. 10: 620-633 [Abstract]  
• Whitehall, S K, Kassavetis, G A, Geiduschek, E P (1995). The symmetry of the yeast U6 RNA gene's TATA box and the orientation of the TATA-binding protein in yeast TFIIIB.. Genes Dev. 9: 2974-2985 [Abstract]  
• Sethy, I., Moir, R. D., Librizzi, M., Willis, I. M. (1995). In Vitro Evidence for Growth Regulation of tRNA Gene Transcription in Yeast. J. Biol. Chem. 270: 28463-28470 [Abstract] [Full Text]  
• Dieci, G., Duimio, L., Peracchia, G., Ottonello, S. (1995). Selective Inactivation of Two Components of the Multiprotein Transcription Factor TFIIIB in Cycloheximide Growth-arrested Yeast Cells. J. Biol. Chem. 270: 13476-13482 [Abstract] [Full Text]  
• Roberts, S, Colbert, T, Hahn, S (1995). TFIIIC determines RNA polymerase III specificity at the TATA-containing yeast U6 promoter.. Genes Dev. 9: 832-842 [Abstract]  
• Kirchner, J, Connolly, C., Sandmeyer, S. (1995). Requirement of RNA polymerase III transcription factors for in vitro position-specific integration of a retroviruslike element. Science 267: 1488-1491 [Abstract]  
• Khoo, B, Brophy, B, Jackson, S P (1994). Conserved functional domains of the RNA polymerase III general transcription factor BRF.. Genes Dev. 8: 2879-2890 [Abstract]  
• Sancar, A, Hearst, J. (1993). Molecular matchmakers. Science 259: 1415-1420 [Abstract]  
• Colbert, T, Hahn, S (1992). A yeast TFIIB-related factor involved in RNA polymerase III transcription.. Genes Dev. 6: 1940-1949 [Abstract]  
• Chalker, D L, Sandmeyer, S B (1992). Ty3 integrates within the region of RNA polymerase III transcription initiation.. Genes Dev. 6: 117-128 [Abstract]  
• Lobo, S M, Lister, J, Sullivan, M L, Hernandez, N (1991). The cloned RNA polymerase II transcription factor IID selects RNA polymerase III to transcribe the human U6 gene in vitro.. Genes Dev. 5: 1477-1489 [Abstract]  
• Young, L., Dunstan, H., Witte, P., Smith, T., Ottonello, S, Sprague, K. (1991). A class III transcription factor composed of RNA. Science 252: 542-546 [Abstract]  
• Margottin, F, Dujardin, G, Gerard, M, Egly, J., Huet, J, Sentenac, A (1991). Participation of the TATA factor in transcription of the yeast U6 gene by RNA polymerase C. Science 251: 424-426 [Abstract]  
• Brow, D A, Guthrie, C (1990). Transcription of a yeast U6 snRNA gene requires a polymerase III promoter element in a novel position.. Genes Dev. 4: 1345-1356 [Abstract]  
• Kovelman, R, Roeder, R G (1990). Sarkosyl defines three intermediate steps in transcription initiation by RNA polymerase III: application to stimulation of transcription by E1A.. Genes Dev. 4: 646-658 [Abstract]  
• Herendeen, D., Kassavetis, G., Barry, J, Alberts, B., Geiduschek, E. (1989). Enhancement of bacteriophage T4 late transcription by components of the T4 DNA replication apparatus. Science 245: 952-958 [Abstract]  
• Yieh, L., Kassavetis, G., Geiduschek, E. P., Sandmeyer, S. B. (2000). The Brf and TATA-binding Protein Subunits of the RNA Polymerase III Transcription Factor IIIB Mediate Position-specific Integration of the Gypsy-like Element, Ty3. J. Biol. Chem. 275: 29800-29807 [Abstract] [Full Text]  
• Huang, Y., Hamada, M., Maraia, R. J. (2000). Isolation and Cloning of Four Subunits of a Fission Yeast TFIIIC Complex That Includes an Ortholog of the Human Regulatory Protein TFIIICbeta. J. Biol. Chem. 275: 31480-31487 [Abstract] [Full Text]