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

Verónica Martínez-Fernández; Francisco Navarro; Verónica Martínez-Fernández; Francisco Navarro

doi:10.3934/genet.2018.1.63

AIMS Genetics

2018, Volume 5, Issue 1: 63-74. doi: 10.3934/genet.2018.1.63

Previous Article Next Article

Mini review

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

Department of Experimental Biology, Faculty of Experimental Sciences, University of Jaén, Paraje de las Lagunillas, s/n, 23071, Jaén, Spain

Received: 08 October 2017 Accepted: 05 February 2018 Published: 27 February 2018

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.
- Rpb5,
- prefoldin-like,
- Bud27/URI,
- RNA polymerases,
- transcription
Citation: Verónica Martínez-Fernández, Francisco Navarro. Rpb5, a subunit shared by eukaryotic RNA polymerases, cooperates with prefoldin-like Bud27/URI[J]. AIMS Genetics, 2018, 5(1): 63-74. doi: 10.3934/genet.2018.1.63

Related Papers:

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.

References

[1]	Jun SH, Hirata A, Kanai T, et al. (2014) The X-ray crystal structure of the euryarchaeal RNA polymerase in an open-clamp configuration. Nat Commun 5: 5132. doi: 10.1038/ncomms6132
[2]	Leśniewska E, Boguta M (2017) Novel layers of RNA polymerase III control affecting tRNA gene transcription in eukaryotes. Open Biol 7: 170001. doi: 10.1098/rsob.170001
[3]	Torreira E, Louro JA, Pazos I, et al. (2017) The dynamic assembly of distinct RNA polymerase I complexes modulates rDNA transcription. Elife, 6.
[4]	Werner F, Grohmann D (2011) Evolution of multisubunit RNA polymerases in the three domains of life. Nat Rev Microbiol 9: 85–98. doi: 10.1038/nrmicro2507
[5]	Werner M, Thuriaux P, Soutourina J (2009) Structure-function analysis of RNA polymerases I and III. Curr Opin Struct Biol 19: 740–745. doi: 10.1016/j.sbi.2009.10.005
[6]	Khatter H, Vorländer MK, Müller CW (2017) RNA polymerase I and III: Similar yet unique. Curr Opin Struct Biol 47: 88–94. doi: 10.1016/j.sbi.2017.05.008
[7]	Fong N, Saldi T, Sheridan RM, et al. (2017) RNA Pol II Dynamics Modulate Co-transcriptional Chromatin Modification, CTD Phosphorylation, and Transcriptional Direction. Mol Cell 66: 546. doi: 10.1016/j.molcel.2017.04.016
[8]	Haag JR, Pikaard CS (2011) Multisubunit RNA polymerases IV and V: Purveyors of non-coding RNA for plant gene silencing. Nat Rev Mol Cell Biol1 12: 483–492. doi: 10.1038/nrm3152
[9]	Böhmdorfer G, Rowley MJ, Kuciński J, et al. (2014) RNA‐directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA. Plant J Cell Mol Biol 79: 181–191. doi: 10.1111/tpj.12563
[10]	Haag JR, Brower-Toland B, Krieger EK, et al. (2014) Functional diversification of maize RNA polymerase IV and V subtypes via alternative catalytic subunits. Cell Rep 9: 378–390. doi: 10.1016/j.celrep.2014.08.067
[11]	Bernecky C, Herzog F, Baumeister W, et al. (2016) Structure of transcribing mammalian RNA polymerase II. Nature 529: 551–554. doi: 10.1038/nature16482
[12]	Kwapisz M, Beckouët F, Thuriaux P (2008) Early evolution of eukaryotic DNA-dependent RNA polymerases. Trends Genet 24: 211–215. doi: 10.1016/j.tig.2008.02.002
[13]	Zaros C, Briand JF, Boulard Y, et al. (2007) Functional organization of the Rpb5 subunit shared by the three yeast RNA polymerases. Nucleic Acids Res 35: 634–647. doi: 10.1093/nar/gkl686
[14]	Woychik NA, Liao SM, Kolodziej PA, et al. (1990) Subunits shared by eukaryotic nuclear RNA polymerases. Genes Dev 4: 313–323. doi: 10.1101/gad.4.3.313
[15]	Shpakovski GV, Acker J, Wintzerith M, et al. (1995) Four subunits that are shared by the three classes of RNA polymerase are functionally interchangeable between Homo sapiens and Saccharomyces cerevisiae. Mol Cell Biol 15: 4702–4710. doi: 10.1128/MCB.15.9.4702
[16]	Kelly S, Wickstead B, Gull K (2005) An in silico analysis of trypanosomatid RNA polymerases: Insights into their unusual transcription. Biochem Soc Trans 33: 1435–1437.
[17]	Armache KJ, Mitterweger S, Meinhart A, et al. (2005) Structures of complete RNA polymerase II and its subcomplex, Rpb4/7. J Biol Chem 280: 7131–7134. doi: 10.1074/jbc.M413038200
[18]	Bushnell DA, Kornberg RD (2003) Complete, 12-subunit RNA polymerase II at 4.1-A resolution: Implications for the initiation of transcription. Proc Natl Acad Sci U S A 100: 6969–6973.
[19]	Cramer P, Bushnell DA, Kornberg RD (2001) Structural basis of transcription: RNA polymerase II at 2.8 Ångstrom resolution. Science 292: 1863–1876.
[20]	Fernándeztornero C, Morenomorcillo M, Rashid UJ, et al. (2013) Crystal structure of the 14-subunit RNA polymerase I. Nature 502: 644–649. doi: 10.1038/nature12636
[21]	Hoffmann NA, Jakobi AJ, Maria MM, et al. (2015) Molecular structures of unbound and transcribing RNA polymerase III. Nature 528: 231–236. doi: 10.1038/nature16143
[22]	Nonet M, Scafe C, Sexton J, et al. (1987) Eucaryotic RNA polymerase conditional mutant that rapidly ceases mRNA synthesis. Mol Cell Biol 7: 1602–1611. doi: 10.1128/MCB.7.5.1602
[23]	Mitsuzawa H, Ishihama A (2004) RNA polymerase II transcription apparatus in Schizosaccharomyces pombe. Curr Genet 44: 287–294. doi: 10.1007/s00294-003-0446-8
[24]	Langer D, Hain J, Thuriaux P, et al. (1995) Transcription in archaea: Similarity to that in eucarya. Proc Natl Acad Sci U S A 92: 5768–5772. doi: 10.1073/pnas.92.13.5768
[25]	Korkhin Y, Unligil UM, Littlefield O, et al. (2009) Evolution of complex RNA polymerases: The complete archaeal RNA polymerase structure. PLoS Biol 7: e1000102. doi: 10.1371/journal.pbio.1000102
[26]	Sommer B, Waege I, Pöllmann D, et al. (2014) Activation of a chimeric Rpb5/RpoH subunit using library selection. PLoS One 9: e87485. doi: 10.1371/journal.pone.0087485
[27]	Iyer LM, Balaji S, Koonin EV, et al. (2006) Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Res 117: 156–184. doi: 10.1016/j.virusres.2006.01.009
[28]	Raoult D, Audic S, Robert C, et al. (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306: 1344–1350.
[29]	Cramer P, Bushnell DA, Fu J, et al. (2000) Architecture of RNA polymerase II and implications for the transcription mechanism. Science 288: 640–649. doi: 10.1126/science.288.5466.640
[30]	Todone F, Brick P, Onesti S (2000) Crystal structure of RPB5, a universal eukaryotic RNA polymerase subunit and transcription factor interaction target. Proc Natl Acad Sci U S A 97: 6306–6310. doi: 10.1073/pnas.97.12.6306
[31]	Navarro F, Thuriaux P (2000) In vivo misreading by tRNA overdose. RNA 6: 103–110. doi: 10.1017/S1355838200991714
[32]	Flores A, Briand JF, Gadal O, et al. (1999) A protein-protein interaction map of yeast RNA polymerase III. Proc Natl Acad Sci U S A 96: 7815–7820. doi: 10.1073/pnas.96.14.7815
[33]	Grünberg S, Reich C, Zeller ME, et al. (2010) Rearrangement of the RNA polymerase subunit H and the lower jaw in archaeal elongation complexes. Nucleic Acids Res 38: 1950–1963. doi: 10.1093/nar/gkp1190
[34]	Barnes CO, Calero M, Malik I, et al. (2015) Crystal structure of a transcribing RNA polymerase II complex reveals a complete transcription bubble. Mol Cell 59: 258–269. doi: 10.1016/j.molcel.2015.06.034
[35]	Kimura M, Ishiguro A, Ishihama A (1997) RNA polymerase II subunits 2, 3, and 11 form a core subassembly with DNA binding activity. J Biol Chem 272: 25851–25855. doi: 10.1074/jbc.272.41.25851
[36]	Bartholomew B, Durkovich D, Kassavetis G, et al. (1993) Orientation and topography of RNA polymerase III in transcription complexes. Mol Cell Biol 13: 942–952. doi: 10.1128/MCB.13.2.942
[37]	He Y, Fang J, Taatjes DJ, et al. (2013) Structural visualization of key steps in human transcription initiation. Nature 495: 481. doi: 10.1038/nature11991
[38]	Fishburn J, Tomko E, Galburt E, et al. (2015) 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 112: 3961–3966. doi: 10.1073/pnas.1417709112
[39]	Soutourina J, Bordas-Le FV, Gendrel G, et al. (2006) Rsc4 connects the chromatin remodeler RSC to RNA polymerases. Mol Cell Biol 26: 4920–4933. doi: 10.1128/MCB.00415-06
[40]	Peeters E, Driessen RP, Werner F, et al. (2015) The interplay between nucleoid organization and transcription in archaeal genomes. Nat Rev Microbiol 13: 333. doi: 10.1038/nrmicro3467
[41]	Miyao T, Woychik NA (1998) RNA polymerase subunit RPB5 plays a role in transcriptional activation. Proc Natl Acad Sci U S A 95: 15281–15286. doi: 10.1073/pnas.95.26.15281
[42]	Cheong JH, Yi M, Lin Y, et al. (1995) 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 14: 143–150.
[43]	Haviv I, Shamay MG, Shaul Y (1998) Hepatitis B virus pX targets TFIIB in transcription coactivation. Mol Cell Biol 18: 1562–1569. doi: 10.1128/MCB.18.3.1562
[44]	Dorjsuren D, Lin Y, Wei W, et al. (1998) RMP, a novel RNA polymerase II subunit 5-interacting protein, counteracts transactivation by hepatitis B virus X protein. Mol Cell Biol 18: 7546–7555. doi: 10.1128/MCB.18.12.7546
[45]	Le TT, Zhang S, Hayashi N, et al. (2005) 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 138: 215–224. doi: 10.1093/jb/mvi119
[46]	Wei W, Dorjsuren D, Lin Y, et al. (2001) 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 276: 12266–12273. doi: 10.1074/jbc.M009634200
[47]	Wei W, Gu JX, Zhu CQ, et al. (2003) Interaction with general transcription factor IIF (TFIIF) is required for the suppression of activated transcription by RPB5-mediating protein (RMP). Cell Res 13: 111. doi: 10.1038/sj.cr.7290155
[48]	Morohoshi F, Arai K, Takahashi EI, et al. (1996) Cloning and Mapping of a Human RBP56 Gene Encoding a Putative RNA Binding Protein Similar to FUS/TLS and EWS Proteins. Genomics 38: 51–57. doi: 10.1006/geno.1996.0591
[49]	Bertolotti A, Lutz Y, Heard DJ, et al. (1996) 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 15: 5022.
[50]	Bertolotti A, Melot T, Acker J, et al. (1998) 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 18: 1489–1497. doi: 10.1128/MCB.18.3.1489
[51]	Makino Y, Yogosawa S, Kayukawa K, et al. (1999) TATA-binding protein-interacting protein 120, TIP120, stimulates three classes of eukaryotic transcription via a unique mechanism. Mol Cell Biol 19: 7951–7960. doi: 10.1128/MCB.19.12.7951
[52]	Grünberg S, Hahn S (2013) Structural insights into transcription initiation by RNA polymerase II. Trends Biochem Sci 38: 603–611. doi: 10.1016/j.tibs.2013.09.002
[53]	Martínezfernández V, Garridogodino AI, Miróngarcía MC, et al. (2017) Rpb5 modulates the RNA polymerase II transition from initiation to elongation by influencing Spt5 association and backtracking. Biochim Biophys Acta 1861: 1–13. doi: 10.1016/j.bbagen.2016.11.023
[54]	Martínezfernández V, Garridogodino AI, Cuevas-Bermudez A, et al. (2015) Cytoplasmic and Nuclear Functions for the Prefoldin-like URI/Bud27. Nova Science Publishers.
[55]	Miróngarcía MC, Garridogodino AI, Garcíamolinero V, et al. (2013) The prefoldin Bud27 mediates the assembly of the eukaryotic RNA polymerases in an Rpb5-dependent manner. PLoS Genet 9: e1003297. doi: 10.1371/journal.pgen.1003297
[56]	Gstaiger M, Luke B, Hess D, et al. (2003) Control of nutrient-sensitive transcription programs by the unconventional prefoldin URI. Science 302: 1208–1212. doi: 10.1126/science.1088401
[57]	Riveracalzada A, Pal M, Muñozhernández H, et al. (2017) The structure of the R2TP complex defines a platform for recruiting diverse client proteins to the HSP90 molecular chaperone system. Structure 25: 1145–1152. doi: 10.1016/j.str.2017.05.016
[58]	Boulon S, Bertrand E, Pradet-Balade B (2012) HSP90 and the R2TP co-chaperone complex: Building multi-protein machineries essential for cell growth and gene expression. RNA Biolo 9: 148–154. doi: 10.4161/rna.18494
[59]	Boulon S, Pradet-Balade B, Verheggen C, et al. (2010) HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II. Mol Cell 39: 912–924. doi: 10.1016/j.molcel.2010.08.023
[60]	Mita P, Savas JN, Ha S, et al. (2013) Analysis of URI nuclear interaction with RPB5 and components of the R2TP/Prefoldin-like complex. PLoS One 8: e63879. doi: 10.1371/journal.pone.0063879
[61]	Cloutier P, Poitras C, Durand M, et al. (2017) R2TP/Prefoldin-like component RUVBL1/RUVBL2 directly interacts with ZNHIT2 to regulate assembly of U5 small nuclear ribonucleoprotein. Nat Commun 8: 15615. doi: 10.1038/ncomms15615
[62]	Yart A, Gstaiger M, Wirbelauer C, et al. (2005) The HRPT2 tumor suppressor gene product parafibromin associates with human PAF1 and RNA polymerase II. Mol Cell Biol 25: 5052–5060. doi: 10.1128/MCB.25.12.5052-5060.2005
[63]	Parusel CT, Kritikou EA, Hengartner MO, et al. (2006) URI-1 is required for DNA stability in C. elegans. Development 133: 621–629.
[64]	Kirchner J, Vissi E, Gross S, et al. (2008) Drosophila Uri, a PP1alpha binding protein, is essential for viability, maintenance of DNA integrity and normal transcriptional activity. BMC Mol Biol 9: 1–17. doi: 10.1186/1471-2199-9-1
[65]	Tummala KS, Gomes AL, Yilmaz M, et al. (2014) Inhibition of De Novo NAD Synthesis by Oncogenic URI Causes Liver Tumorigenesis through DNA Damage. Cancer Cell 26: 826–839. doi: 10.1016/j.ccell.2014.10.002
[66]	Burén S, Gomes AL, Teijeiro A, et al. (2016) Regulation of OGT by URI in Response to Glucose Confers c-MYC-Dependent Survival Mechanisms. Cancer Cell 30: 290–307. doi: 10.1016/j.ccell.2016.06.023
[67]	Deplazes A, Mockli N, Luke B, et al. (2009) Yeast Uri1p promotes translation initiation and may provide a link to cotranslational quality control. EMBO J 28: 1429–1441. doi: 10.1038/emboj.2009.98
[68]	Lin Y, Nomura T, Cheong J, et al. (1997) 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 272: 7132–7139. doi: 10.1074/jbc.272.11.7132
[69]	Mita P, Savas JN, Djouder N, et al. (2011) Regulation of androgen receptor-mediated transcription by RPB5 binding protein URI/RMP. Mol Cell Biol 31: 3639–3652. doi: 10.1128/MCB.05429-11
[70]	Vernekar DV, Bhargava P (2015) Yeast Bud27 modulates the biogenesis of Rpc128 and Rpc160 subunits and the assembly of RNA polymerase III. Biochim Biophys Acta 1849: 1340–1353. doi: 10.1016/j.bbagrm.2015.09.010
[71]	Ciesla M, Makala E, Plonka M, et al. (2015) Rbs1, a new protein implicated in RNA polymerase III biogenesis in yeast Saccharomyces cerevisiae. Mol Cell Biol 35: 1169–1181. doi: 10.1128/MCB.01230-14
[72]	Miróngarcía MC, Garridogodino AI, Martínezfernández V, et al. (2014) The yeast prefoldin-like URI-orthologue Bud27 associates with the RSC nucleosome remodeler and modulates transcription. Nucleic Acids Res 42: 9666–9676. doi: 10.1093/nar/gku685

Reader Comments

Your name:*

Email:*
© 2018 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)