CC BY 4.0 · AIMS Genet 2018; 05(01): 063-074
DOI: 10.3934/genet.2018.1.63
Mini Review

Rpb5, a subunit shared by eukaryotic RNA polymerases, cooperates with prefoldin-like Bud27/URI

Veránica Martónez-Ferníndez
Department of Experimental Biology, Faculty of Experimental Sciences, University of JaÉn, Paraje de las Lagunillas, s/n, 23071, JaÉn, Spain
,
Francisco Navarro
Department of Experimental Biology, Faculty of Experimental Sciences, University of JaÉn, Paraje de las Lagunillas, s/n, 23071, JaÉn, Spain
› Author Affiliations

Abstract

Rpb5 is one of the five common subunits to all eukaryotic RNA polymerases, which is conserved in archaea, but not in bacteria. Among these common subunits, it is the only one that is not interchangeable between yeasts and humans, and accounts for the functional incompatibility of yeast and human subunits. Rpb5 has been proposed to contribute to the gene-specific activation of RNA pol II, notably during the infectious cycle of the hepatitis B virus, and also to participate in general transcription mediated by all eukaryotic RNA pol. The structural analysis of Rpb5 and its interaction with different transcription factors, regulators and DNA, accounts for Rpb5 being necessary to maintain the correct conformation of the shelf module of RNA pol II, which favors the proper organization of the transcription bubble and the clamp closure of the enzyme.

In this work we provide details about subunit Rpb5's structure, conservation and the role it plays in transcription regulation by analyzing the different interactions with several factors, as well as its participation in the assembly of the three RNA pols, in cooperation with prefoldin-like Bud27/URI.



Publication History

Received: 08 October 2017

Accepted: 05 February 2018

Article published online:
10 May 2021

© 2018. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Jun SH, Hirata A, Kanai T. et al. The X-ray crystal structure of the euryarchaeal RNA polymerase in an open-clamp configuration. Nat Commun 2014; 5: 5132
  • 2 LeŚniewska E, Boguta M. Novel layers of RNA polymerase III control affecting tRNA gene transcription in eukaryotes. Open Biol 2017; 7: 170001
  • 3 Torreira E, Louro JA, Pazos I. et al. The dynamic assembly of distinct RNA polymerase I complexes modulates rDNA transcription. Elife 2017;6
  • 4 Werner F, Grohmann D. Evolution of multisubunit RNA polymerases in the three domains of life. Nat Rev Microbiol 2011; 9: 85-98
  • 5 Werner M, Thuriaux P, Soutourina J. Structure-function analysis of RNA polymerases I and III. Curr Opin Struct Biol 2009; 19: 740-745
  • 6 Khatter H, VorlÄnder MK, MÜller CW. RNA polymerase I and III: Similar yet unique. Curr Opin Struct Biol 2017; 47: 88-94
  • 7 Fong N, Saldi T, Sheridan RM. et al. RNA Pol II Dynamics Modulate Co-transcriptional Chromatin Modification, CTD Phosphorylation, and Transcriptional Direction. Mol Cell 2017; 66: 546
  • 8 Haag JR, Pikaard CS. Multisubunit RNA polymerases IV and V: Purveyors of non-coding RNA for plant gene silencing. Nat Rev Mol Cell Biol1 2011; 12: 483-492
  • 9 BÖhmdorfer G, Rowley MJ, KuciŃski J. et al. RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA. Plant J Cell Mol Biol 2014; 79: 181-191
  • 10 Haag JR, Brower-Toland B, Krieger EK. et al. Functional diversification of maize RNA polymerase IV and V subtypes via alternative catalytic subunits. Cell Rep 2014; 9: 378-390
  • 11 Bernecky C, Herzog F, Baumeister W. et al. Structure of transcribing mammalian RNA polymerase II. Nature 2016; 529: 551-554
  • 12 Kwapisz M, BeckouËt F, Thuriaux P. et al. Early evolution of eukaryotic DNA-dependent RNA polymerases. Trends Genet 2008; 24: 211-215
  • 13 Zaros C, Briand JF, Boulard Y. et al. Functional organization of the Rpb5 subunit shared by the three yeast RNA polymerases. Nucleic Acids Res 2007; 35: 634-647
  • 14 Woychik NA, Liao SM, Kolodziej PA. et al. Subunits shared by eukaryotic nuclear RNA polymerases. Genes Dev 1990; 4: 313-323
  • 15 Shpakovski GV, Acker J, Wintzerith M. et al. Four subunits that are shared by the three classes of RNA polymerase are functionally interchangeable between Homo sapiens and Saccharomyces cerevisiae. Mol Cell Biol 1995; 15: 4702-4710
  • 16 Kelly S, Wickstead B, Gull K. An in silico analysis of trypanosomatid RNA polymerases: Insights into their unusual transcription. Biochem Soc Trans 2005; 33: 1435-1437
  • 17 Armache KJ, Mitterweger S, Meinhart A. et al. Structures of complete RNA polymerase II and its subcomplex, Rpb4/7. J Biol Chem 2005; 280: 7131-7134
  • 18 Bushnell DA, Kornberg RD. Complete, 12-subunit RNA polymerase II at 4.1-A resolution: Implications for the initiation of transcription. Proc Natl Acad Sci U S A 2003; 100: 6969-6973
  • 19 Cramer P, Bushnell DA, Kornberg RD. Structural basis of transcription: RNA polymerase II at 2.8 Ångstrom resolution. Science 2001; 292: 1863-1876
  • 20 FernÁndeztornero C, Morenomorcillo M, Rashid UJ. et al. Crystal structure of the 14-subunit RNA polymerase I. Nature 2013; 502: 644-649
  • 21 Hoffmann NA, Jakobi AJ, Maria MM. et al. Molecular structures of unbound and transcribing RNA polymerase III. Nature 2015; 528: 231-236
  • 22 Nonet M, Scafe C, Sexton J. et al. Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol Cell Biol 1987; 7: 1602-1611
  • 23 Mitsuzawa H, Ishihama A. RNA polymerase II transcription apparatus in Schizosaccharomyces pombe. Curr Genet 2004; 44: 287-294
  • 24 Langer D, Hain J, Thuriaux P. et al. Transcription in archaea: Similarity to that in eucarya. Proc Natl Acad Sci U S A 1995; 92: 5768-5772
  • 25 Korkhin Y, Unligil UM, Littlefield O. et al. Evolution of complex RNA polymerases: The complete archaeal RNA polymerase structure. PLoS Biol 2009; 7: e1000102
  • 26 Sommer B, Waege I, PÖllmann D. et al. Activation of a chimeric Rpb5/RpoH subunit using library selection. PLoS One 2014; 9: e87485
  • 27 Iyer LM, Balaji S, Koonin EV. et al. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 2006; 117: 156-184
  • 28 Raoult D, Audic S, Robert C. et al. The 1.2-megabase genome sequence of Mimivirus. Science 2004; 306: 1344-1350
  • 29 Cramer P, Bushnell DA, Fu J. et al. Architecture of RNA polymerase II and implications for the transcription mechanism. Science 2000; 288: 640-649
  • 30 Todone F, Brick P, Onesti S. Crystal structure of RPB5, a universal eukaryotic RNA polymerase subunit and transcription factor interaction target. Proc Natl Acad Sci U S A 2000; 97: 6306-6310
  • 31 Navarro F, Thuriaux P. In vivo misreading by tRNA overdose. RNA 2000; 6: 103-110
  • 32 Flores A, Briand JF, Gadal O. et al. A protein-protein interaction map of yeast RNA polymerase III. Proc Natl Acad Sci U S A 1999; 96: 7815-7820
  • 33 GrÜnberg S, Reich C, Zeller ME. et al. Rearrangement of the RNA polymerase subunit H and the lower jaw in archaeal elongation complexes. Nucleic Acids Res 2010; 38: 1950-1963
  • 34 Barnes CO, Calero M, Malik I. et al. Crystal structure of a transcribing RNA polymerase II complex reveals a complete transcription bubble. Mol Cell 2015; 59: 258-269
  • 35 Kimura M, Ishiguro A, Ishihama A. RNA polymerase II subunits 2, 3, and 11 form a core subassembly with DNA binding activity. J Biol Chem 1997; 272: 25851-25855
  • 36 Bartholomew B, Durkovich D, Kassavetis G. et al. Orientation and topography of RNA polymerase III in transcription complexes. Mol Cell Biol 1993; 13: 942-952
  • 37 He Y, Fang J, Taatjes DJ. et al. Structural visualization of key steps in human transcription initiation. Nature 2013; 495: 481
  • 38 Fishburn J, Tomko E, Galburt E. et al. Double-stranded DNA translocase activity of transcription factor TFIIH and the mechanism of RNA polymerase II open complex formation. Proc Natl Acad Sci U S A 2015; 112: 3961-3966
  • 39 Soutourina J, Bordas-Le FV, Gendrel G. et al. Rsc4 connects the chromatin remodeler RSC to RNA polymerases. Mol Cell Biol 2006; 26: 4920-4933
  • 40 Peeters E, Driessen RP, Werner F. et al. The interplay between nucleoid organization and transcription in archaeal genomes. Nat Rev Microbiol 2015; 13: 333
  • 41 Miyao T, Woychik NA. RNA polymerase subunit RPB5 plays a role in transcriptional activation. Proc Natl Acad Sci U S A 1998; 95: 15281-15286
  • 42 Cheong JH, Yi M, Lin Y. et al. Human RPB5, a subunit shared by eukaryotic nuclear RNA polymerases, binds human hepatitis B virus X protein and may play a role in X transactivation. EMBO J 1995; 14: 143-150
  • 43 Haviv I, Shamay MG, Shaul Y. Hepatitis B virus pX targets TFIIB in transcription coactivation. Mol Cell Biol 1998; 18: 1562-1569
  • 44 Dorjsuren D, Lin Y, Wei W. et al. RMP, a novel RNA polymerase II subunit 5-interacting protein, counteracts transactivation by hepatitis B virus X protein. Mol Cell Biol 1998; 18: 7546-7555
  • 45 Le TT, Zhang S, Hayashi N. et al. Mutational analysis of human RNA polymerase II subunit 5 (RPB5): The residues critical for interactions with TFIIF subunit RAP30 and hepatitis B virus X protein. J Biochem 2005; 138: 215-224
  • 46 Wei W, Dorjsuren D, Lin Y. et al. Direct interaction between the subunit RAP30 of transcription factor IIF (TFIIF) and RNA polymerase subunit 5, which contributes to the association between TFIIF and RNA polymerase II. J Biol Chem 2001; 276: 12266-12273
  • 47 Wei W, Gu JX, Zhu CQ. et al. Interaction with general transcription factor IIF (TFIIF) is required for the suppression of activated transcription by RPB5-mediating protein (RMP). Cell Res 2003; 13: 111
  • 48 Morohoshi F, Arai K, Takahashi EI. et al. Cloning and Mapping of a Human RBP56 Gene Encoding a Putative RNA Binding Protein Similar to FUS/TLS and EWS Proteins. Genomics 1996; 38: 51-57
  • 49 Bertolotti A, Lutz Y, Heard DJ. et al. HTAF(II)68, a novel RNA/ssDNA-binding protein with homology to the pro-oncoproteins TLS/FUS and EWS is associated with both TFIID and RNA polymerase II. EMBO J 1996; 15: 5022
  • 50 Bertolotti A, Melot T, Acker J. et al. EWS, but not EWS-FLI-1, is associated with both TFIID and RNA polymerase II: Interactions between two members of the TET family, EWS and hTAFII68, and subunits of TFIID and RNA polymerase II complexes. Mol Cell Biol 1998; 18: 1489-1497
  • 51 Makino Y, Yogosawa S, Kayukawa K. et al. TATA-binding protein-interacting protein 120, TIP120, stimulates three classes of eukaryotic transcription via a unique mechanism. Mol Cell Biol 1999; 19: 7951-7960
  • 52 GrÜnberg S, Hahn S. Structural insights into transcription initiation by RNA polymerase II. Trends Biochem Sci 2013; 38: 603-611
  • 53 MartÍnezfernÁndez V, Garridogodino AI, MirÓngarcÍa MC. et al. Rpb5 modulates the RNA polymerase II transition from initiation to elongation by influencing Spt5 association and backtracking. Biochim Biophys Acta 2017; 1861: 1-13
  • 54 MartÍnezfernÁndez V, Garridogodino AI, Cuevas-Bermudez A. et al. Cytoplasmic and Nuclear Functionsfor the Prefoldin-like URI/Bud27. Nova Science Publishers 2015
  • 55 MirÓngarcÍa MC, Garridogodino AI, GarcÍamolinero V. et al. The prefoldin Bud27 mediates the assembly of the eukaryotic RNA polymerases in an Rpb5-dependent manner. PLoS Genet 2013; 9: e1003297
  • 56 Gstaiger M, Luke B, Hess D. et al. Control of nutrient-sensitive transcription programs by the unconventional prefoldin URI. Science 2003; 302: 1208-1212
  • 57 Riveracalzada A, Pal M, MuÑozhernÁndez H. et al. The structure of the R2TP complex defines a platform for recruiting diverse client proteins to the HSP90 molecular chaperone system. Structure 2017; 25: 1145-1152
  • 58 Boulon S, Bertrand E, Pradet-Balade B. HSP90 and the R2TP co-chaperone complex: Building multi-protein machineries essential for cell growth and gene expression. RNA Biolo 2012; 9: 148-154
  • 59 Boulon S, Pradet-Balade B, Verheggen C. et al. HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II. Mol Cell 2010; 39: 912-924
  • 60 Mita P, Savas JN, Ha S. et al. Analysis of URI nuclear interaction with RPB5 and components of the R2TP/Prefoldin-like complex. PLoS One 2013; 8: e63879
  • 61 Cloutier P, Poitras C, Durand M. et al. R2TP/Prefoldin-like component RUVBL1/RUVBL2 directly interacts with ZNHIT2 to regulate assembly of U5 small nuclear ribonucleoprotein. Nat Commun 2017; 8: 15615
  • 62 Yart A, Gstaiger M, Wirbelauer C. et al. The HRPT2 tumor suppressor gene product parafibromin associates with human PAF1 and RNA polymerase II. Mol Cell Biol 2005; 25: 5052-5060
  • 63 Parusel CT, Kritikou EA, Hengartner MO. et al. URI-1 is required for DNA stability in C. elegans. Development 2006; 133: 621-629
  • 64 Kirchner J, Vissi E, Gross S. et al. Drosophila Uri, a PP1alpha binding protein, is essential for viability, maintenance of DNA integrity and normal transcriptional activity. BMC Mol Biol 2008; 9: 1-17
  • 65 Tummala KS, Gomes AL, Yilmaz M. et al. Inhibition of De Novo NAD Synthesis by Oncogenic URI Causes Liver Tumorigenesis through DNA Damage. Cancer Cell 2014; 26: 826-839
  • 66 BurÉn S, Gomes AL, Teijeiro A. et al. Regulation of OGT by URI in Response to Glucose Confers c-MYC-Dependent Survival Mechanisms. Cancer Cell 2016; 30: 290-307
  • 67 Deplazes A, Mockli N, Luke B. et al. Yeast Uri1p promotes translation initiation and may provide a link to cotranslational quality control. EMBO J 2009; 28: 1429-1441
  • 68 Lin Y, Nomura T, Cheong J. et al. Hepatitis B virus X protein is a transcriptional modulator that communicates with transcription factor IIB and the RNA polymerase II subunit 5. J Biol Chem 1997; 272: 7132-7139
  • 69 Mita P, Savas JN, Djouder N. et al. Regulation of androgen receptor-mediated transcription by RPB5 binding protein URI/RMP. Mol Cell Biol 2011; 31: 3639-3652
  • 70 Vernekar DV, Bhargava P. Yeast Bud27 modulates the biogenesis of Rpc128 and Rpc160 subunits and the assembly of RNA polymerase III. Biochim Biophys Acta 2015; 1849: 1340-1353
  • 71 Ciesla M, Makala E, Plonka M. et al. Rbs1, a new protein implicated in RNA polymerase III biogenesis in yeast Saccharomyces cerevisiae. Mol Cell Biol 2015; 35: 1169-1181
  • 72 MirÓngarcÍa MC, Garridogodino AI. , MartÍnezfern#x00EE;ndez V, et al. The yeast prefoldin-like URI-orthologue Bud27 associates with the RSC nucleosome remodeler and modulates transcription. Nucleic Acids Res 2014; 42: 9666-9676