Yeast Rrn7 and Human TAF1B Are TFIIB-related RNA Polymerase I General Transcription Factors

Overview

Journal Science

Specialty Science

Date 2011 Sep 17

PMID 21921198

Citations 41

Authors

Bruce A Knutson

Steven Hahn

Affiliations

Soon will be listed here.

Abstract

Eukaryotic and archaeal multisubunit RNA polymerases (Pols) are structurally related and require several similar components for transcription initiation. However, none of the Pol I factors were known to share homology with transcription factor IIB (TFIIB) or TFIIB-related proteins, key factors in the initiation mechanisms of the other Pols. Here we show that Rrn7, a subunit of the yeast Pol I core factor, and its human ortholog TAF1B are TFIIB-like factors. Although distantly related, Rrn7 shares many activities associated with TFIIB-like factors. Domain swaps between TFIIB-related factors show that Rrn7 is most closely related to the Pol III general factor Brf1. Our results point to the conservation of initiation mechanisms among multisubunit Pols and reveal a key function of yeast core factor/human SL1 in Pol I transcription.

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References

Gorski J, Pathak S, Panov K, Kasciukovic T, Panova T, Russell J . A novel TBP-associated factor of SL1 functions in RNA polymerase I transcription. EMBO J. 2007; 26(6):1560-8. PMC: 1829371. DOI: 10.1038/sj.emboj.7601601. View

Lin C, Moorefield B, Payne J, Aprikian P, Mitomo K, Reeder R . A novel 66-kilodalton protein complexes with Rrn6, Rrn7, and TATA-binding protein to promote polymerase I transcription initiation in Saccharomyces cerevisiae. Mol Cell Biol. 1996; 16(11):6436-43. PMC: 231645. DOI: 10.1128/MCB.16.11.6436. View

Boukhgalter B, Liu M, Guo A, Tripp M, Tran K, Huynh C . Characterization of a fission yeast subunit of an RNA polymerase I essential transcription initiation factor, SpRrn7h/TAF(I)68, that bridges yeast and mammals: association with SpRrn11h and the core ribosomal RNA gene promoter. Gene. 2002; 291(1-2):187-201. DOI: 10.1016/s0378-1119(02)00597-8. View

Kassavetis G, Driscoll R, Geiduschek E . Mapping the principal interaction site of the Brf1 and Bdp1 subunits of Saccharomyces cerevisiae TFIIIB. J Biol Chem. 2006; 281(20):14321-9. DOI: 10.1074/jbc.M601702200. View

Carter R, Drouin G . The evolutionary rates of eukaryotic RNA polymerases and of their transcription factors are affected by the level of concerted evolution of the genes they transcribe. Mol Biol Evol. 2009; 26(11):2515-20. DOI: 10.1093/molbev/msp164. View

Hahn S . Structure and mechanism of the RNA polymerase II transcription machinery. Nat Struct Mol Biol. 2004; 11(5):394-403. PMC: 1189732. DOI: 10.1038/nsmb763. View

Aprikian P, Moorefield B, Reeder R . New model for the yeast RNA polymerase I transcription cycle. Mol Cell Biol. 2001; 21(15):4847-55. PMC: 87188. DOI: 10.1128/MCB.21.15.4847-4855.2001. View

Friedrich J, Panov K, cabart P, Russell J, Zomerdijk J . TBP-TAF complex SL1 directs RNA polymerase I pre-initiation complex formation and stabilizes upstream binding factor at the rDNA promoter. J Biol Chem. 2005; 280(33):29551-8. PMC: 3858828. DOI: 10.1074/jbc.M501595200. View

Hahn S . Structural biology: New beginnings for transcription. Nature. 2009; 462(7271):292-3. DOI: 10.1038/462292a. View

10.

Chen H, Hahn S . Binding of TFIIB to RNA polymerase II: Mapping the binding site for the TFIIB zinc ribbon domain within the preinitiation complex. Mol Cell. 2003; 12(2):437-47. DOI: 10.1016/s1097-2765(03)00306-x. View

11.

Lalo D, Steffan J, Dodd J, Nomura M . 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. J Biol Chem. 1996; 271(35):21062-7. DOI: 10.1074/jbc.271.35.21062. View

12.

Zomerdijk J, Beckmann H, Comai L, Tjian R . Assembly of transcriptionally active RNA polymerase I initiation factor SL1 from recombinant subunits. Science. 1994; 266(5193):2015-8. DOI: 10.1126/science.7801130. View

13.

Liao Y, Willis I, Moir R . The Brf1 and Bdp1 subunits of transcription factor TFIIIB bind to overlapping sites in the tetratricopeptide repeats of Tfc4. J Biol Chem. 2003; 278(45):44467-74. DOI: 10.1074/jbc.M308354200. View

14.

Steffan J, Keys D, Dodd J, Nomura M . 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. Genes Dev. 1996; 10(20):2551-63. DOI: 10.1101/gad.10.20.2551. View

15.

Imamura S, Hanaoka M, Tanaka K . The plant-specific TFIIB-related protein, pBrp, is a general transcription factor for RNA polymerase I. EMBO J. 2008; 27(17):2317-27. PMC: 2529366. DOI: 10.1038/emboj.2008.151. View

16.

Soding J, Biegert A, Lupas A . The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 2005; 33(Web Server issue):W244-8. PMC: 1160169. DOI: 10.1093/nar/gki408. View

17.

Khoo B, Brophy B, Jackson S . Conserved functional domains of the RNA polymerase III general transcription factor BRF. Genes Dev. 1994; 8(23):2879-90. DOI: 10.1101/gad.8.23.2879. View

18.

Bushnell D, Westover K, Davis R, Kornberg R . Structural basis of transcription: an RNA polymerase II-TFIIB cocrystal at 4.5 Angstroms. Science. 2004; 303(5660):983-8. DOI: 10.1126/science.1090838. View

19.

Cavel E, Pillot M, Pontier D, Lahmy S, Bies-Etheve N, Vega D . A plant-specific transcription factor IIB-related protein, pBRP2, is involved in endosperm growth control. PLoS One. 2011; 6(2):e17216. PMC: 3044737. DOI: 10.1371/journal.pone.0017216. View

20.

Nogi Y, Yano R, Nomura M . Synthesis of large rRNAs by RNA polymerase II in mutants of Saccharomyces cerevisiae defective in RNA polymerase I. Proc Natl Acad Sci U S A. 1991; 88(9):3962-6. PMC: 51573. DOI: 10.1073/pnas.88.9.3962. View