Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Science 2 September 1988:
Vol. 241. no. 4870, pp. 1192 - 1197
DOI: 10.1126/science.3413483

Articles

Science, Vol 241, Issue 4870, 1192-1197
Copyright © 1988 by American Association for the Advancement of Science


articles

Functional cooperativity between transcription factors UBF1 and SL1 mediates human ribosomal RNA synthesis

SP Bell, RM Learned, HM Jantzen, and R Tjian

Howard Hughes Medical Institute, Department of Biochemistry, University of California, Berkeley 94720.

The human ribosomal RNA promoter contains two distinct control elements (UCE and core) both of which are recognized by the sequence-specific DNA binding protein UBF1, which has now been purified to apparent homogeneity. The purified factor activates RNA polymerase I (RNA pol I) transcription through direct interactions with either control element. A second RNA pol I transcription factor, designated SL1, participates in the promoter recognition process and is required to reconstitute transcription in vitro. Although SL1 alone has no sequence-specific DNA binding activity, deoxyribonuclease I footprinting experiments reveal that a cooperative interaction between UBF1 and SL1 leads to the formation of a new protein-DNA complex at the UCE and core elements. In vitro transcription experiments indicate that formation of the UBF1-SL1 complex is vital for transcriptional activation by UBF1. Thus, protein-protein interactions between UBF1 and SL1 are required for targeting of SL1 to cis-control sequences of the promoter.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules.
K. Merz, M. Hondele, H. Goetze, K. Gmelch, U. Stoeckl, and J. Griesenbeck (2008)
Genes & Dev. 22, 1190-1204
   Abstract »    Full Text »    PDF »
Two RNA Polymerase I Subunits Control the Binding and Release of Rrn3 during Transcription.
F. Beckouet, S. Labarre-Mariotte, B. Albert, Y. Imazawa, M. Werner, O. Gadal, Y. Nogi, and P. Thuriaux (2008)
Mol. Cell. Biol. 28, 1596-1605
   Abstract »    Full Text »    PDF »
Mass spectrometric identification of phosphorylation sites of rRNA transcription factor upstream binding factor.
C. H. Lin, M. D. Platt, S. B. Ficarro, M. H. Hoofnagle, J. Shabanowitz, L. Comai, D. F. Hunt, and G. K. Owens (2007)
Am J Physiol Cell Physiol 292, C1617-C1624
   Abstract »    Full Text »    PDF »
Pol I Transcription and Pre-rRNA Processing Are Coordinated in a Transcription-dependent Manner in Mammalian Cells.
K. Kopp, J. Z. Gasiorowski, D. Chen, R. Gilmore, J. T. Norton, C. Wang, D. J. Leary, E.K.L. Chan, D. A. Dean, and S. Huang (2007)
Mol. Biol. Cell 18, 394-403
   Abstract »    Full Text »    PDF »
CK2-mediated stimulation of Pol I transcription by stabilization of UBF-SL1 interaction.
C.-Y. Lin, S. Navarro, S. Reddy, and L. Comai (2006)
Nucleic Acids Res. 34, 4752-4766
   Abstract »    Full Text »    PDF »
Casein kinase 2 associates with initiation-competent RNA polymerase I and has multiple roles in ribosomal DNA transcription..
T. B. Panova, K. I. Panov, J. Russell, and J. C. B. M. Zomerdijk (2006)
Mol. Cell. Biol. 26, 5957-5968
   Abstract »    Full Text »    PDF »
Nucleolar protein upstream binding factor is sequestered into adenovirus DNA replication centres during infection without affecting RNA polymerase I location or ablating rRNA synthesis.
F. J. Lawrence, B. McStay, and D. A. Matthews (2006)
J. Cell Sci. 119, 2621-2631
   Abstract »    Full Text »    PDF »
Acetylation of UBF changes during the cell cycle and regulates the interaction of UBF with RNA polymerase I..
J. Meraner, M. Lechner, A. Loidl, M. Goralik-Schramel, R. Voit, I. Grummt, and P. Loidl (2006)
Nucleic Acids Res. 34, 1798-1806
   Abstract »    Full Text »    PDF »
TBP-TAF Complex SL1 Directs RNA Polymerase I Pre-initiation Complex Formation and Stabilizes Upstream Binding Factor at the rDNA Promoter.
J. K. Friedrich, K. I. Panov, P. Cabart, J. Russell, and J. C. B. M. Zomerdijk (2005)
J. Biol. Chem. 280, 29551-29558
   Abstract »    Full Text »    PDF »
Modifications of both selectivity factor and upstream binding factor contribute to poliovirus-mediated inhibition of RNA polymerase I transcription.
R. Banerjee, M. K. Weidman, S. Navarro, L. Comai, and A. Dasgupta (2005)
J. Gen. Virol. 86, 2315-2322
   Abstract »    Full Text »    PDF »
Condensed mitotic chromatin is accessible to transcription factors and chromatin structural proteins.
D. Chen, M. Dundr, C. Wang, A. Leung, A. Lamond, T. Misteli, and S. Huang (2005)
J. Cell Biol. 168, 41-54
   Abstract »    Full Text »    PDF »
UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery.
C. Mais, J. E. Wright, J.-L. Prieto, S. L. Raggett, and B. McStay (2005)
Genes & Dev. 19, 50-64
   Abstract »    Full Text »    PDF »
Upstream binding factor association induces large-scale chromatin decondensation.
D. Chen, A. S. Belmont, and S. Huang (2004)
PNAS 101, 15106-15111
   Abstract »    Full Text »    PDF »
Cloning and Characterization of Granulosa Cell High-Mobility Group (HMG)-Box Protein-1, a Novel HMG-Box Transcriptional Regulator Strongly Expressed in Rat Ovarian Granulosa Cells.
T. Kajitani, T. Mizutani, K. Yamada, T. Yazawa, T. Sekiguchi, M. Yoshino, H. Kawata, and K. Miyamoto (2004)
Endocrinology 145, 2307-2318
   Abstract »    Full Text »    PDF »
Regulation of Ribosomal RNA Synthesis During the Final Phases of Porcine Oocyte Growth.
B. Bjerregaard, C. Wrenzycki, V. V. Philimonenko, P. Hozak, J. Laurincik, H. Niemann, J. Motlik, and P. Maddox-Hyttel (2004)
Biol Reprod 70, 925-935
   Abstract »    Full Text »    PDF »
Phosphatidylinositol 3-Kinase and mTOR Signaling Pathways Regulate RNA Polymerase I Transcription in Response to IGF-1 and Nutrients.
M. J. James and J. C. B. M. Zomerdijk (2004)
J. Biol. Chem. 279, 8911-8918
   Abstract »    Full Text »    PDF »
A Functional Screen in Human Cells Identifies UBF2 as an RNA Polymerase II Transcription Factor That Enhances the {beta}-Catenin Signaling Pathway.
D. A. Grueneberg, L. Pablo, K.-Q. Hu, P. August, Z. Weng, and J. Papkoff (2003)
Mol. Cell. Biol. 23, 3936-3950
   Abstract »    Full Text »    PDF »
Rrn3 Becomes Inactivated in the Process of Ribosomal DNA Transcription.
I. Hirschler-Laszkiewicz, A. H. Cavanaugh, A. Mirza, M. Lun, Q. Hu, T. Smink, and L. I. Rothblum (2003)
J. Biol. Chem. 278, 18953-18959
   Abstract »    Full Text »    PDF »
Upstream binding factor up-regulated in hepatocellular carcinoma is related to the survival and cisplatin-sensitivity of cancer cells.
R. HUANG, T. WU, L. XU, A. LIU, Y. JI, and G. HU (2002)
FASEB J 16, 293-301
   Abstract »    Full Text »    PDF »
A Novel RNA Polymerase I Transcription Initiation Factor, TIF-IE, Commits rRNA Genes by Interaction with TIF-IB, Not by DNA Binding.
A. M. Al-Khouri and M. R. Paule (2002)
Mol. Cell. Biol. 22, 750-761
   Abstract »    Full Text »    PDF »
UBF Binding In Vivo Is Not Restricted to Regulatory Sequences within the Vertebrate Ribosomal DNA Repeat.
A. C. O'Sullivan, G. J. Sullivan, and B. McStay (2002)
Mol. Cell. Biol. 22, 657-658
   Abstract »    Full Text »    PDF »
Interactions between HMG boxes.
S. Taudte, H. Xin, A. J. Bell Jr, and N. R. Kallenbach (2001)
Protein Eng. Des. Sel. 14, 1015-1023
   Abstract »    Full Text »    PDF »
The role of acetylation in rDNA transcription.
I. Hirschler-Laszkiewicz, A. Cavanaugh, Q. Hu, J. Catania, M. L. Avantaggiati, and L. I. Rothblum (2001)
Nucleic Acids Res. 29, 4114-4124
   Abstract »    Full Text »    PDF »
A Step Subsequent to Preinitiation Complex Assembly at the Ribosomal RNA Gene Promoter Is Rate Limiting for Human RNA Polymerase I-Dependent Transcription.
K. I. Panov, J. K. Friedrich, and J. C. B. M. Zomerdijk (2001)
Mol. Cell. Biol. 21, 2641-2649
   Abstract »    Full Text »    PDF »
Repression of RNA Polymerase I Transcription by the Tumor Suppressor p53.
W. Zhai and L. Comai (2000)
Mol. Cell. Biol. 20, 5930-5938
   Abstract »    Full Text »    PDF »
TATA Binding Protein Can Stimulate Core-Directed Transcription by Yeast RNA Polymerase I.
P. Aprikian, B. Moorefield, and R. H. Reeder (2000)
Mol. Cell. Biol. 20, 5269-5275
   Abstract »    Full Text »    PDF »
SURVEY AND SUMMARY Transcription by RNA polymerases I and III.
M. R. Paule and R. J. White (2000)
Nucleic Acids Res. 28, 1283-1298
   Abstract »    Full Text »    PDF »
Identification of a novel 70 kDa protein that binds to the core promoter element and is essential for ribosomal DNA transcription.
K. Yamamoto, A. Koga, M. Yamamoto, Y.-i. Nishi, T.-a. Tamura, Y. Nogi, and M. Muramatsu (2000)
Nucleic Acids Res. 28, 1199-1205
   Abstract »    Full Text »    PDF »
Inhibition of RNA Polymerase I Transcription in Differentiated Myeloid Leukemia Cells by Inactivation of Selectivity Factor 1.
L. Comai, Y. Song, C. Tan, and T. Bui (2000)
Cell Growth Differ. 11, 63-70
   Abstract »    Full Text »
Basonuclin, a zinc finger protein of keratinocytes and reproductive germ cells, binds to the rRNA gene promoter.
S. Iuchi and H. Green (1999)
PNAS 96, 9628-9632
   Abstract »    Full Text »    PDF »
A Kinase Activity Associated with Simian Virus 40 Large T Antigen Phosphorylates Upstream Binding Factor (UBF) and Promotes Formation of a Stable Initiation Complex between UBF and SL1.
W. Zhai and L. Comai (1999)
Mol. Cell. Biol. 19, 2791-2802
   Abstract »    Full Text »    PDF »
Recruitment of TATA-Binding Protein-TAFI Complex SL1 to the Human Ribosomal DNA Promoter Is Mediated by the Carboxy-Terminal Activation Domain of Upstream Binding Factor (UBF) and Is Regulated by UBF Phosphorylation.
J. C. Tuan, W. Zhai, and L. Comai (1999)
Mol. Cell. Biol. 19, 2872-2879
   Abstract »    Full Text »    PDF »
The mitotically phosphorylated form of the transcription termination factor TTF-1 is associated with the repressed rDNA transcription machinery.
V Sirri, P Roussel, and D Hernandez-Verdun (1999)
J. Cell Sci. 112, 3259-3268
   Abstract »    PDF »
Basonuclin is associated with the ribosomal RNA genes on human keratinocyte mitotic chromosomes.
H Tseng, J. Biegel, and R. Brown (1999)
J. Cell Sci. 112, 3039-3047
   Abstract »    PDF »
Transactivation of a Ribosomal Gene by Simian Virus 40 Large-T Antigen Requires at Least Three Activities of the Protein.
J. F. Cavender, C. Mummert, and M. J. Tevethia (1999)
J. Virol. 73, 214-224
   Abstract »    Full Text »    PDF »
Histone Acetyltransferase and Protein Kinase Activities Copurify with a Putative Xenopus RNA Polymerase I Holoenzyme Self-Sufficient for Promoter-Dependent Transcription.
A.-C. Albert, M. Denton, M. Kermekchiev, and C. S. Pikaard (1999)
Mol. Cell. Biol. 19, 796-806
   Abstract »    Full Text »    PDF »
Reconstitution of Yeast RNA Polymerase I Transcription in Vitro from Purified Components. TATA-BINDING PROTEIN IS NOT REQUIRED FOR BASAL TRANSCRIPTION.
J. Keener, C. A. Josaitis, J. A. Dodd, and M. Nomura (1998)
J. Biol. Chem. 273, 33795-33802
   Abstract »    Full Text »    PDF »
Phosphorylation of the rRNA transcription factor upstream binding factor promotes its association with TATA binding protein.
A. J. Kihm, J. C. Hershey, T. A. J. Haystead, C. S. Madsen, and G. K. Owens (1998)
PNAS 95, 14816-14820
   Abstract »    Full Text »    PDF »
Chromatin Structure and Transcriptional Control Elements of the Erythroid Kruppel-like Factor (EKLF) Gene.
X. Chen, M. Reitman, and J. J. Bieker (1998)
J. Biol. Chem. 273, 25031-25040
   Abstract »    Full Text »    PDF »
Presence of Pre-rRNAs before Activation of Polymerase I Transcription in the Building Process of Nucleoli during Early Development of Xenopus laevis.
C. Verheggen, S. Le Panse, G. Almouzni, and D. Hernandez-Verdun (1998)
J. Cell Biol. 142, 1167-1180
   Abstract »    Full Text »    PDF »
Regulation of gene expression by TBP-associated proteins.
T. I. Lee and R. A. Young (1998)
Genes & Dev. 12, 1398-1408
   Full Text »
Extensive purification of a putative RNA polymerase I holoenzyme from plants that accurately initiates rRNA gene transcription vitro.
J. Saez-Vasquez and C. S. Pikaard (1997)
PNAS 94, 11869-11874
   Abstract »    Full Text »    PDF »
SV40 large T antigen binds to the TBP-TAF(I) complex SL1 and coactivates ribosomal RNA transcription..
W Zhai, J A Tuan, and L Comai (1997)
Genes & Dev. 11, 1605-1617
   Abstract »    PDF »
Cloning of murine RNA polymerase I-specific TAF factors: Conserved interactions between the subunits of the species-specific transcription initiation factor TIF-IB/SL1.
J. Heix, J. C. B. M. Zomerdijk, A. Ravanpay, R. Tjian, and I. Grummt (1997)
PNAS 94, 1733-1738
   Abstract »    Full Text »    PDF »
When rDNA transcription is arrested during mitosis, UBF is still associated with non-condensed rDNA.
J Gebrane-Younes, N Fomproix, and D Hernandez-Verdun (1997)
J. Cell Sci. 110, 2429-2440
   Abstract »    PDF »
Association of the nucleolar transcription factor UBF with the transcriptionally inactive rRNA genes of pronuclei and early Xenopus embryos.
P Bell, C Mais, B McStay, and U Scheer (1997)
J. Cell Sci. 110, 2053-2063
   Abstract »    PDF »
Virtually the Entire Xenopus laevis rDNA Multikilobase Intergenic Spacer Serves to Stimulate Polymerase I Transcription.
E. B. Mougey, L. K. Pape, and B. Sollner-Webb (1996)
J. Biol. Chem. 271, 27138-27145
   Abstract »    Full Text »    PDF »
The role of TBP in rDNA transcription by RNA polymerase I in Saccharomyces cerevisiae: TBP is required for upstream activation factor-dependent recruitment of core factor..
J S Steffan, D A Keys, J A Dodd, and M Nomura (1996)
Genes & Dev. 10, 2551-2563
   Abstract »    PDF »
RRN11 Encodes the Third Subunit of the Complex Containing Rrn6p and Rrn7p That Is Essential for the Initiation of rDNA Transcription by Yeast RNA Polymerase I.
D. Lalo, J. S. Steffan, J. A. Dodd, and M. Nomura (1996)
J. Biol. Chem. 271, 21062-21067
   Abstract »    Full Text »    PDF »
Specific Interaction between Human Kinetochore Protein CENP-C and a Nucleolar Transcriptional Regulator.
A. F. Pluta and W. C. Earnshaw (1996)
J. Biol. Chem. 271, 18767-18774
   Abstract »    Full Text »    PDF »
Multiprotein transcription factor UAF interacts with the upstream element of the yeast RNA polymerase I promoter and forms a stable preinitiation complex..
D A Keys, B S Lee, J A Dodd, T T Nguyen, L Vu, E Fantino, L M Burson, Y Nogi, and M Nomura (1996)
Genes & Dev. 10, 887-903
   Abstract »    PDF »
Coactivator and Promoter-Selective Properties of RNA Polymerase I TAFs.
H. Beckmann, J.-L. Chen, T. O'Brien, and R. Tjian (1995)
Science 270, 1506-1509
   Abstract »    PDF »
Angiotensin II-induced Hypertrophy of Rat Vascular Smooth Muscle Is Associated with Increased 18 S rRNA Synthesis and Phosphorylation of the rRNA Transcription Factor, Upstream Binding Factor.
J. C. Hershey, M. Hautmann, M. M. Thompson, L. I. Rothblum, T. A. J. Haystead, and G. K. Owens (1995)
J. Biol. Chem. 270, 25096-25101
   Abstract »    Full Text »    PDF »
Characterization of the Components of Reconstituted Saccharomyces cerevisiae RNA Polymerase I Transcription Complexes.
D. L. Riggs, C. L. Peterson, J. Q. Wickham, L. M. Miller, E. M. Clarke, J. A. Crowell, and J.-C. Sergere (1995)
J. Biol. Chem. 270, 6205-6210
   Abstract »    Full Text »    PDF »
Reconstitution of transcription factor SL1: exclusive binding of TBP by SL1 or TFIID subunits.
L Comai, J. Zomerdijk, H Beckmann, S Zhou, A Admon, and R Tjian (1994)
Science 266, 1966-1972
   Abstract »    PDF »
RRN6 and RRN7 encode subunits of a multiprotein complex essential for the initiation of rDNA transcription by RNA polymerase I in Saccharomyces cerevisiae..
D A Keys, L Vu, J S Steffan, J A Dodd, R T Yamamoto, Y Nogi, and M Nomura (1994)
Genes & Dev. 8, 2349-2362
   Abstract »    PDF »
Architectural transcription factors.
A. Wolffe (1994)
Science 264, 1100-1101
   PDF »
Short-range DNA looping by the Xenopus HMG-box transcription factor, xUBF.
D. Bazett-Jones, B Leblanc, M Herfort, and T Moss (1994)
Science 264, 1134-1137
   Abstract »    PDF »
TBP, a universal eukaryotic transcription factor?.
N Hernandez (1993)
Genes & Dev. 7, 1291-1308
   PDF »
Localization of the RNA polymerase I transcription factor hUBF during the cell cycle.
P Roussel, C Andre, C Masson, G Geraud, and D Hernandez-Verdun (1993)
J. Cell Sci. 104, 327-337
   Abstract »    PDF »
Coactivators and TAFs: A New Class of Eukaryotic Transcription Factors That Connect Activators to the Basal Machinery.
N. Tanese and R. Tjian (1993)
Cold Spring Harb Symp Quant Biol 58, 179-185
   Abstract »    PDF »
Characterization and immunolocalization of RNA polymerase I transcription factor UBF with anti-NOR serum in protozoa, higher plant and vertebrate cells.
R. M. Rodrigo, M. C. Rendon, J. Torreblanca, G. Garcia-Herdugo, and F. J. Moreno (1992)
J. Cell Sci. 103, 1053-1063
   Abstract »    PDF »
A yeast TFIIB-related factor involved in RNA polymerase III transcription..
T Colbert and S Hahn (1992)
Genes & Dev. 6, 1940-1949
   Abstract »    PDF »
Multiple domains of the RNA polymerase I activator hUBF interact with the TATA-binding protein complex hSL1 to mediate transcription..
H M Jantzen, A M Chow, D S King, and R Tjian (1992)
Genes & Dev. 6, 1950-1963
   Abstract »    PDF »
xUBF contains a novel dimerization domain essential for RNA polymerase I transcription..
B McStay, M W Frazier, and R H Reeder (1991)
Genes & Dev. 5, 1957-1968
   Abstract »    PDF »
Similarity of human mitochondrial transcription factor 1 to high mobility group proteins.
M. Parisi and D. Clayton (1991)
Science 252, 965-969
   Abstract »    PDF »
Assembly of alternative multiprotein complexes directs rRNA promoter selectivity..
S P Bell, H M Jantzen, and R Tjian (1990)
Genes & Dev. 4, 943-954
   Abstract »    PDF »
A transcription factor, TFIS, interacts with both the promoter and enhancer of the Xenopus rRNA genes..
M Dunaway (1989)
Genes & Dev. 3, 1768-1778
   Abstract »    PDF »
The Xenopus ribosomal gene enhancers bind an essential polymerase I transcription factor, xUBF..
C S Pikaard, B McStay, M C Schultz, S P Bell, and R H Reeder (1989)
Genes & Dev. 3, 1779-1788
   Abstract »    PDF »
Cloning and expression of AP-2, a cell-type-specific transcription factor that activates inducible enhancer elements..
T Williams, A Admon, B Luscher, and R Tjian (1988)
Genes & Dev. 2, 1557-1569
   Abstract »    PDF »
RNA polymerase I transcription factor Rrn3 is functionally conserved between yeast and human.
B. Moorefield, E. A. Greene, and R. H. Reeder (2000)
PNAS 97, 4724-4729
   Abstract »    Full Text »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)