RNA polymerase (RNA pol) subunit composition.
Abstract
RNA polymerases are heteromultimeric complexes responsible of RNA synthesis. In yeast, as in the other eukaryotes, these complexes contain five common subunits (Rpb5, Rpb6, Rpb8, Rpb10 and Rpb12) that must have similar functions in the three RNA polymerases. However, some of these proteins have been shown to also have specific roles. In the last few decades, substantial progress has been made to understand the role of these common subunits in transcription, but their participation in the activity of each enzyme remains unclear. This review gives a comprehensive overview of current knowledge on the five common subunits of eukaryotic RNA pol, placing attention not only on their common roles in the activity of the RNA pols but also on describing specific roles for some of the complexes.
Keywords
- RNA polymerases
- transcription
- protein complexes
- common subunits
- RNA
1. Introduction
Transcription is carried out by the RNA polymerases (RNA pol). While archaea and bacteria contain only one RNA pol, most eukarya contain three different enzymes responsible for the specific synthesis of different types of RNAs [1]. RNA pol I synthesises the precursor of the three largest rRNAs, whereas RNA pol III sy\nthesises mostly tRNAs and 5S rRNA, together with several short non-translated RNAs. Meanwhile, RNA pol II produces all mRNAs and many non-coding RNAs [1, 2]. Moreover, in plants, two additional polymerases, IV and V (or nuclear RNA polymerases D and E), reportedly synthesise small interfering RNAs (siRNAs), regulating methylation and participating in gene silencing, as well as long non-coding RNAs involved in development and response to environmental changes [3, 4, 5].
While bacteriophage T7 and some related enzymes that transcribe the mitochondrial genome or contribute to chloroplast transcription are single-subunit RNA polymerase [6], bacterial, archaeal and eukaryotic enzymes are heteromultimeric complexes (Table 1). As in other eukaryotes, yeast RNA pol I, II and III are composed of 14, 12 and 17 subunits, respectively. These contain a catalytic core formed by the two largest subunits, which are highly conserved through evolution (Rpb1 and Rpb2). Moreover, among all eukaryotic RNA pol subunits, five have bacterial homologues (Rpb1, Rpb2, Rpb3, Rpb6 and Rpb11) and others are common to archaea, but without bacterial homologues (Rpb4, Rpb5, Rpb7, Rpb8, Rpb9, Rpb10, and Rpb12) [1, 2, 6, 7, 8, 9]. Finally, eukaryotic RNA pols contain five common subunits to the three enzymes (Rpb5, rpb6, Rpb8, Rpb10 and Rpb12), which have archaeal homologues (Figure 1) [10, 11, 12].
Eukaryotes | ||||||
---|---|---|---|---|---|---|
Bacteria | Archaea | RNA pol I | RNA pol II | RNA pol III | RNA pol IV (plants) | RNA pol V (plants) |
β | Rpo1 (RpoA) | RPA190 | RPB1 | RPC160 | NRPD1 | NRPE1 |
β | Rpo2 (RpoB) | RPBA135 | RPB2 | RPC128 | NRPD/E2 | NRPD/E2 |
α | Rpo3 (RpoD) | RPAC40 | RPB3 | RPAC40 | RPB3 [1] | RPB3 [1] |
α | Rpo11 (RpoL) | RPAC19 | RPB11 | RPAC19 | RPB11 | RPB11 |
ω | Rpo6 (RpoK) | RPB6 | RPB6 | RPB6 | RPB6 [1] | RPB6 |
Rpo5 (RpoH) | RPB5 | RPB5 | RPB5 | RPB5 [3] | NRPES5 | |
Rpb8 (RpoG)* | RPB8 | RPB8 | RPB8 | RPB8 [1] | RPB8 [1] | |
Rpo10 (RpoN) | RPB10 | RPB10 | RPB10 | RPB10 | RPB10 | |
Rpo12 (RpoP) | RPB12 | RPB12 | RPB12 | RPB12 | RPB12 | |
Rpo4 (RpoF) | RPA14 | RPB4 | RPC17 | NRPD/E4 | NRPD/E4 | |
Rpo7(RpoE) | RPA43 | RPB7 | RPC25 | NRPD7 [1] | NRPE7 | |
RPA12 | RPB9 | RPC11 | NRPD9b | RPB9 | ||
Rpo13* | ||||||
RPA49 | RPC53 | |||||
RPA34.5 | RPC37 | |||||
RPC82 | ||||||
RPC34 | ||||||
RPC31 |
In the last few decades, substantial progress has been made to understand the role of the RNA pol common subunits in transcription, but their participation in the activity of each enzyme remains unclear. This review gives a comprehensive overview of current knowledge on the five common subunits of eukaryotic RNA pol, placing attention not only on their common roles in the activity of the RNA pols but also on describing specific roles for some of the complexes.
2. Rpb5
In budding yeast, the essential Rpb5 subunit, also known as ABC27, consists of 215 amino acid residues and has a molecular mass of 27 kDa [11, 13, 14, 15]. Contrary to other RNA polymerase common subunits, human Rpb5 homologue (RPB5), with 44% identity and 80% similarity to the yeast polypeptide, fails to complement the
Structurally, Rpb5 has a bipartite organisation combining two globular modules separated by a short hinge: an N-terminal domain (“
The periphery localization of Rpb5 on all three enzymes [7, 30, 31] would allow possible interactions with general transcription factors or specific gene regulators. It should be the basis of the interaction between Rpb5 and Rsc4, a subunit of RSC (chromatin remodeler complex) in
The HBx transactivation seems to be modulated by the protein URI/RMP (Unconventional Prefoldin Rpb5 Interactor) that specifically binds to RPB5 both
Furthermore, it has been proposed that Bud27 modulates the association between Sth1 (subunit of RSC complex) and the RNA pol II probably through Rpb5 interaction in
3. Rpb6
Rpb6 (also known as ABC23 or Rpo26) is an acidic 155-amino acid subunit with apparent and predicted molecular masses of 23 and 18 kDa, respectively [11, 47]. It is phosphorylated in all three RNA pols, mainly on serine and threonine residues [48, 49, 50, 51]. Moreover, the
A role for Rpb6 in transcription elongation has been proposed. In fact, some temperature-sensitive mutants in
According to a global role of Rpb6 in transcription, the
Rpb6 was found to make contact with three small RNA pol subunits, Rpb5, Rpb7 and Rpb8, as well as with the foot of the RNA pol II, with its largest subunits Rpb1 and Rpb2 [7, 61]. Similarly, Rpb6 interacts on the crystal structure with the largest subunit of the RNA pol I, Rpa190 [30] and probably with its homologue in the RNA pol III, Rpc160. Notably, the contact between Rpb6 and Rpb7 involves the residue Gln100 of Rpb6 and Gly66 of Rpb7 on the RNA pol II core and the
While the C-terminal segment of Rpb6, from amino acids 72 to 155, is well organised on the crystal structure of yeast RNA pol II [7], the N-terminal domain 71-amino acid segment on the RNA pol II structure, as well as the N-terminal 54-amino acid segment on the RNA pol I structure is disordered [24, 28, 30]. Moreover, the segment from amino acids 55 to 71 of Rpb6 on the RNA pol I structure comprises an α-helix that provides additional contacts with Rpa43 and Rpa14 [28, 30]. The N-terminal region of Rpb6 seems to be dispensable for the functions of this subunit, explaining the lack of conservation of this region with its archaeal homologues and the low degree of similarity of the Rpb6 sequence among various eukaryotes [63]. However, a region of 13 amino acids in the C-terminal domain of Rpb6 is highly conserved in eukaryotes and archaea, suggesting an essential function [63]. Rpb6 is connected to the base of a flexible module containing portions of Rpb1 and Rpb2, called the clamp, through a set of five “switches” that control clamp movement [7]. In addition, the association of Rpb6 with Rpb4/Rpb7 dimmer suggest that these two subunits could modulate the clamp movement and may regulate the position of the clamp by signalling through Rpb6 [62].
Rpb6 and its bacterial homologue have been proposed to promote RNA pol II assembly and/or increase RNA pol stability, through specific interactions with the RNA pol II largest subunit, Rpb1, in the case of
In
4. Rpb8
Rpb8 (also known as ABC14.5) is an essential subunit of 16.5 kDa conserved among eukaryotes and thought to be restricted to them [11, 12, 67]. However, recently, the Rpb8 archaeal orthologues, called G or Rpo8, has been identified in
Rpb8 crystal structure in RNA pol II contains nine closely packed β-strands forming a double OB-fold [7]. Rpb8 interacts with the largest subunit of the RNA pol II, Rpb1, and shows a subunit interface between Rpb3 and Rpb11. Two-hybrid analyses identified similar binding of Rpb8 to the Rpb1-like subunits of RNA pol I (Rpa190) and RNA pol III (Rpc160) [61]. In addition, mutational analysis of
As opposed to the Rpb8 human orthologue,
5. Rpb10
Rpb10, also called AB10β in yeast, is one of the smallest polypeptides (70-aminoacid polypeptide in
All the eukaryotic forms of Rpb10 share an invariant HVDLIEK motif (located between positions His-53 and Pro-65 in
Rpb10 is localised in the periphery of all three RNA polymerases [7, 30, 31]. In budding yeast, Rpb10 was described to interact not only with two essential subunits of the RNA pols I and III, Rpac40 and Rpac19 (homologous to Rpb3 and Rpb11, respectively, in the RNA pol II) but also with the two largest subunits of RNA pol I (Rpa190 and Rpa135) and their homologues in RNA pol III (Rpc160 and Rpc128) [23, 72].
Rpb10 has been found to be involved in the assembly of RNA polymerases in eukaryotes as part of the assembly platform. In fact, it has been proposed that Rpb10 and Rpb12 form a stable complex with Rpb3-Rpb11 (homologous to the bacterial α-subunit homodimer) [77]. Rpb10 and Rpb12 fill concave depressions of Rpb2 and thereby act as structural adaptors between Rpb2 and Rpb3 (reviewed in [1]). Notably, mutations of the invariant HVDLIEK motif lead to a complete depletion of the largest RNA pol I subunit (Rpa190) and decrease the accumulation of mature rRNA species transcribed by RNA pol I [73]. However, Rpb10 could have additional functions beyond RNA polymerases assembly. In accordance, Rpb10 is localised in proximity to TBP in the structural model of the DNA-TBP-TFIIB-RNA pol II transcription initiation complex [79].
6. Rpb12
The eukaryotic subunit Rpb12, also designated as ABC10α [71, 80], together with Rpb10 are the smallest common subunits to the RNA pols. The corresponding gene is essential for growth in
The importance of Rpb12 in transcription is extrapolated from studies on the archaeal P subunit. The P subunit is involved in promoter opening. The ΔP enzyme is unable to form stable open complexes and its activity can be rescued by the addition of Rpb12 or subunit P to transcription reactions. Notably, mutation of cysteine residues in the zinc ribbon impairs the activity of the enzyme in transcription reactions. The conserved zinc ribbon in the N-terminus seems to be important for proper interaction of the complete subunit with other RNA polymerase subunits, and a 17-amino acid C-terminal peptide is sufficient to support all basic RNA polymerase functions
The contact between
Acknowledgments
This work has been supported by grants from the Spanish Ministry of Economy and Competitiveness, MINECO, and FEDER funds (BFU2013-48643-C3-2-P and BFU2016-77728-C3-2-P to F.N.) and Junta de Andalucía (BIO258).
A.C.B. was a recipient of a FPI predoctoral contract from MINECO. V.M.F. was recipient of a fellowship from Junta de Andalucía and a postdoctoral fellowship from the Junta de Andalucía-University of Jaén. A.I.G-G was a recipient of MEC and a postdoctoral fellowship from the University of Jaén.
References
- 1.
Werner F, Grohmann D. Evolution of multisubunit RNA polymerases in the three domains of life. Nature Reviews. Microbiology. 2011; 9 :85-98 - 2.
Werner M, Thuriaux P, Soutourina J. Structure-function analysis of RNA polymerases I and III. Current Opinion in Structural Biology. 2009; 19 :740-745 - 3.
Haag JR, Pikaard CS. Multisubunit RNA polymerases IV and V: Purveyors of non-coding RNA for plant gene silencing. Nature Reviews. Molecular Cell Biology. 2011; 12 :483-492 - 4.
Bohmdorfer G, Rowley MJ, Kucinski J, Zhu Y, Amies I, Wierzbicki AT. RNA-directed DNA methylation requires stepwise binding of silencing factors to long non-coding RNA. The Plant Journal. 2014; 79 :181-191 - 5.
Haag JR, Brower-Toland B, Krieger EK, Sidorenko L, Nicora CD, Norbeck AD, Irsigler A, LaRue H, Brzeski J, McGinnis K, Ivashuta S, Pasa-Tolic L, Chandler VL, Pikaard CS. Functional diversification of maize RNA polymerase IV and V subtypes via alternative catalytic subunits. Cell Rep. 2014; 9 :1-13 - 6.
Kwapisz M, Beckouet F, Thuriaux P. Early evolution of eukaryotic DNA-dependent RNA polymerases. Trends Genet. 2008 - 7.
Cramer P, Bushnell DA, Kornberg RD. Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science. 2001; 292 :1863-1876 - 8.
Ruprich-Robert G, Thuriaux P. Non-canonical DNA transcription enzymes and the conservation of two-barrel RNA polymerases. Nucleic Acids Research. 2010; 38 :4559-4569 - 9.
Cramer P, Armache KJ, Baumli S, Benkert S, Brueckner F, Buchen C, Damsma GE, Dengl S, Geiger SR, Jasiak AJ, Jawhari A, Jennebach S, Kamenski T, Kettenberger H, Kuhn CD, Lehmann E, Leike K, Sydow JF, Vannini A. Structure of eukaryotic RNA polymerases. Annual Review of Biophysics. 2008; 37 :337-352 - 10.
Zaros C, Briand JF, Boulard Y, Labarre-Mariotte S, Garcia-Lopez MC, Thuriaux P, Navarro F. Functional organization of the Rpb5 subunit shared by the three yeast RNA polymerases. Nucleic Acids Research. 2007; 35 :634-647 - 11.
Woychik NA, Liao SM, Kolodziej PA, Young RA. Subunits shared by eukaryotic nuclear RNA polymerases. Genes & Development. 1990; 4 :313-323 - 12.
Shpakovski GV, Acker J, Wintzerith M, Lacroix JF, Thuriaux P, Vigneron M. Four subunits that are shared by the three classes of RNA polymerase are functionally interchangeable between Homo sapiens andSaccharomyces cerevisiae . Molecular and Cellular Biology. 1995;15 :4702-4710 - 13.
Navarro F, Thuriaux P. In vivo misreading by tRNA overdose. RNA. 2000; 6 :103-110 - 14.
Odawara J, Harada A, Yoshimi T, Maehara K, Tachibana T, Okada S, Akashi K, Ohkawa Y. The classification of mRNA expression levels by the phosphorylation state of RNAPII CTD based on a combined genome-wide approach. BMC Genomics. 2011; 12 :516 - 15.
Nonet M, Scafe C, Sexton J, Young R, Eukaryotic RNA. polymerase conditional mutant that rapidly ceases mRNA synthesis. Molecular and Cellular Biology. 1987; 7 :1602-1611 - 16.
Langer D, Hain J, Thuriaux P, Zillig W. Transcription in archaea: Similarity to that in eukarya. Proceedings of the National Academy of Sciences of the United States of America. 1995; 92 :5768-5772 - 17.
Devaux S, Kelly S, Lecordier L, Wickstead B, Perez-Morga D, Pays E, Vanhamme L, Gull K. Diversification of function by different isoforms of conventionally shared RNA polymerase subunits. Molecular Biology of the Cell. 2007; 18 :1293-1301 - 18.
Cramer P, Bushnell DA, Fu J, Gnatt AL, Maier-Davis B, Thompson NE, Burgess RR, Edwards AM, David PR, Kornberg RD. Architecture of RNA polymerase II and implications for the transcription mechanism. Science. 2000; 288 :640-649 - 19.
Todone F, Weinzierl RO, Brick P, Onesti S. Crystal structure of RPB5, a universal eukaryotic RNA polymerase subunit and transcription factor interaction target. Proceedings of the National Academy of Sciences of the United States of America. 2000; 97 :6306-6310 - 20.
Siaut M, Zaros C, Levivier E, Ferri ML, Court M, Werner M, Callebaut I, Thuriaux P, Sentenac A, Conesa C. An Rpb4/Rpb7-like complex in yeast RNA polymerase III contains the orthologue of mammalian CGRP-RCP. Molecular and Cellular Biology. 2003; 23 :195-205 - 21.
Armache KJ, Mitterweger S, Meinhart A, Cramer P. Structures of complete RNA polymerase II and its subcomplex, Rpb4/7. The Journal of Biological Chemistry. 2005; 280 :7131-7134 - 22.
Bushnell DA, Kornberg RD. Complete, 12-subunit RNA polymerase II at 4.1-A resolution: Implications for the initiation of transcription. Proceedings of the National Academy of Sciences of the United States of America. 2003; 100 :6969-6973 - 23.
Flores A, Briand JF, Gadal O, Andrau JC, Rubbi L, Van Mullem V, Boschiero C, Goussot M, Marck C, Carles C, Thuriaux P, Sentenac A, Werner M. A protein-protein interaction map of yeast RNA polymerase III. Proceedings of the National Academy of Sciences of the United States of America. 1999; 96 :7815-7820 - 24.
Gnatt AL, Cramer P, Fu J, Bushnell DA, Kornberg RD. Structural basis of transcription: An RNA polymerase II elongation complex at 3.3 A resolution. Science. 2001; 292 :1876-1882 - 25.
Bartholomew B, Durkovich D, Kassavetis GA, Geiduschek EP. Orientation and topography of RNA polymerase III in transcription complexes. Molecular and Cellular Biology. 1993; 13 :942-952 - 26.
Kim TK, Lagrange T, Wang YH, Griffith JD, Reinberg D, Ebright RH. Trajectory of DNA in the RNA polymerase II transcription preinitiation complex. Proceedings of the National Academy of Sciences of the United States of America. 1997; 94 :12268-12273 - 27.
Bushnell DA, Cramer P, Kornberg RD. Structural basis of transcription: Alpha-amanitin-RNA polymerase II cocrystal at 2.8 A resolution. Proceedings of the National Academy of Sciences of the United States of America. 2002; 99 :1218-1222 - 28.
Engel C, Sainsbury S, Cheung AC, Kostrewa D, Cramer P. RNA polymerase I structure and transcription regulation. Nature. 2013; 502 :650-655 - 29.
Fernandez-Tornero C, Bottcher B, Rashid UJ, Muller CW. Analyzing RNA polymerase III by electron cryomicroscopy. RNA Biology. 2011; 8 :760-765 - 30.
Fernandez-Tornero C, Moreno-Morcillo M, Rashid UJ, Taylor NM, Ruiz FM, Gruene T, Legrand P, Steuerwald U, Muller CW. Crystal structure of the 14-subunit RNA polymerase I. Nature. 2013; 502 :644-649 - 31.
Hoffmann NA, Jakobi AJ, Moreno-Morcillo M, Glatt S, Kosinski J, Hagen WJ, Sachse C, Müller CW. Molecular structures of unbound and transcribing RNA polymerase III. Nature. 2015; 528 :231-236 - 32.
Soutourina J, Bordas-Le Floch V, Gendrel G, Flores A, Ducrot C, Dumay-Odelot H, Soularue P, Navarro F, Cairns BR, Lefebvre O, Werner M. Rsc4 connects the chromatin remodeler RSC to RNA polymerases. Molecular and Cellular Biology. 2006; 26 :4920-4933 - 33.
Hayashi K, Watanabe T, Tanaka A, Furumoto T, Sato-Tsuchiya C, Kimura M, Yokoi M, Ishihama A, Hanaoka F, Ohkuma Y. Studies of Schizosaccharomyces pombe TFIIE indicate conformational and functional changes in RNA polymerase II at transcription initiation. Genes to Cells. 2005;10 :207-224 - 34.
Lin Y, Nomura T, Cheong J, Dorjsuren D, Iida K, Murakami S. Hepatitis B virus X protein is a transcriptional modulator that communicates with transcription factor IIB and the RNA polymerase II subunit 5. The Journal of Biological Chemistry. 1997; 272 :7132-7139 - 35.
Bertolotti A, Lutz Y, Heard DJ, Chambon P, Tora L. 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. The EMBO Journal. 1996; 15 :5022 - 36.
Bertolotti A, Melot T, Acker J, Vigneron M, Delattre O, Tora L. 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. Molecular and Cellular Biology. 1998; 18 :1489-1497 - 37.
Morohoshi F, Arai K, Takahashi E-i, Tanigami A, Ohki M. 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 - 38.
Makino Y, Yogosawa S, Kayukawa K, Coin F, Egly JM, Wang Z, Roeder RG, Yamamoto K, Muramatsu M, Tamura T. TATA-binding protein-interacting protein 120, TIP120, stimulates three classes of eukaryotic transcription via a unique mechanism. Molecular and Cellular Biology. 1999; 19 :7951-7960 - 39.
Le TT, Zhang S, Hayashi N, Yasukawa M, Delgermaa L, Murakami S. 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. Journal of Biochemistry (Tokyo). 2005; 138 :215-224 - 40.
Dorjsuren D, Lin Y, Wei W, Yamashita T, Nomura T, Hayashi N, Murakami S. RMP, a novel RNA polymerase II subunit 5-interacting protein, counteracts transactivation by hepatitis B virus X protein. Molecular and Cellular Biology. 1998; 18 :7546-7555 - 41.
P. Mita, J.N. Savas, N. Djouder, J.R. Yates 3rd, S. Ha, R. Ruoff, E.D. Schafler, J.C. Nwachukwu, N. Tanese, N.J. Cowan, J. Zavadil, M.J. Garabedian, S.K. Logan, Regulation of androgen receptor mediated transcription by Rpb5 binding protein URI/RMP, Molecular and Cellular Biology. 2011; 31 :3639-3652 - 42.
Miron-Garcia MC, Garrido-Godino AI, Garcia-Molinero V, Hernandez-Torres F, Rodriguez-Navarro S, Navarro F. The prefoldin bud27 mediates the assembly of the eukaryotic RNA polymerases in an rpb5-dependent manner. PLoS Genetics. 2013; 9 :e1003297 - 43.
Gstaiger M, Luke B, Hess D, Oakeley EJ, Wirbelauer C, Blondel M, Vigneron M, Peter M, Krek W. Control of nutrient-sensitive transcription programs by the unconventional prefoldin URI. Science. 2003; 302 :1208-1212 - 44.
Boulon S, Pradet-Balade B, Verheggen C, Molle D, Boireau S, Georgieva M, Azzag K, Robert MC, Ahmad Y, Neel H, Lamond AI, Bertrand E. HSP90 and its R2TP/prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II. Molecular Cell. 2010; 39 :912-924 - 45.
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 Biology. 2012; 9 :1-8 - 46.
Miron-Garcia MC, Garrido-Godino AI, Martinez-Fernandez V, Fernandez-Pevida A, Cuevas-Bermudez A, Martin-Exposito M, Chavez S, de la Cruz J, Navarro F. The yeast prefoldin-like URI-orthologue Bud27 associates with the RSC nucleosome remodeler and modulates transcription. Nucleic Acids Research. 2014; 42 :9666-9676 - 47.
Archambault J, Schappert KT, Friesen JD. A suppressor of an RNA polymerase II mutation of Saccharomyces cerevisiae encodes a subunit common to RNA polymerases I, II, and III. Molecular and Cellular Biology. 1990;10 :6123-6131 - 48.
Bell GI, Valenzuela P, Rutter WJ. Phosphorylation of yeast RNA polymerases. Nature. 1976; 261 :429-431 - 49.
Bell GI, Valenzuela P, Rutter WJ. Phosphorylation of yeast DNA-dependent RNA polymerases in vivo and in vitro. Isolation of enzymes and identification of phosphorylated subunits. The Journal of Biological Chemistry. 1977; 252 :3082-3091 - 50.
Buhler JM, Iborra F, Sentenac A, Fromageot P. The presence of phosphorylated subunits in yeast RNA polymerases A and B. FEBS Letters. 1976; 72 :37-41 - 51.
Kolodziej PA, Woychik N, Liao SM, Young RA. RNA polymerase II subunit composition, stoichiometry, and phosphorylation. Molecular and Cellular Biology. 1990; 10 :1915-1920 - 52.
Kayukawa K, Makino Y, Yogosawa S, Tamura T. A serine residue in the N-terminal acidic region of rat RPB6, one of the common subunits of RNA polymerases, is exclusively phosphorylated by casein kinase II in vitro. Gene. 1999; 234 :139-147 - 53.
Minakhin L, Bhagat S, Brunning A, Campbell EA, Darst SA, Ebright RH, Severinov K. Bacterial RNA polymerase subunit omega and eukaryotic RNA polymerase subunit RPB6 are sequence, structural, and functional homologs and promote RNA polymerase assembly. Proceedings of the National Academy of Sciences of the United States of America. 2001; 98 :892-897 - 54.
McKune K, Moore PA, Hull MW, Woychik NA. Six human RNA polymerase subunits functionally substitute for their yeast counterparts. Molecular and Cellular Biology. 1995; 15 :6895-6900 - 55.
McKune K, Woychik NA. Functional substitution of an essential yeast RNA polymerase subunit by a highly conserved mammalian counterpart. Molecular and Cellular Biology. 1994; 14 :4155-4159 - 56.
Lanzendorfer M, Smid A, Klinger C, Schultz P, Sentenac A, Carles C, Riva M. A shared subunit belongs to the eukaryotic core RNA polymerase. Genes & Development. 1997; 11 :1037-1047 - 57.
Ishiguro A, Nogi Y, Hisatake K, Muramatsu M, Ishihama A. The Rpb6 subunit of fission yeast RNA polymerase II is a contact target of the transcription elongation factor TFIIS. Molecular and Cellular Biology. 2000; 20 :1263-1270 - 58.
Wani S, Hirose Y, Ohkuma Y. Human RNA polymerase II-associated protein 2 (RPAP2) interacts directly with the RNA polymerase II subunit Rpb6 and participates in pre-mRNA 3′-end formation. Drug Discoveries & Therapeutics. 2014; 8 :255-261 - 59.
Magill CP, Jackson SP, Bell SD. Identification of a conserved archaeal RNA polymerase subunit contacted by the basal transcription factor TFB. The Journal of Biological Chemistry. 2001; 276 :46693-46696 - 60.
Qiu ZR, Schwer B, Shuman S. Two routes to genetic suppression of RNA trimethylguanosine cap deficiency via C-terminal truncation of U1 snRNP subunit Snp1 or overexpression of RNA polymerase subunit Rpo26. G3 (Bethesda). 2015; 5 :1361-1370 - 61.
Briand JF, Navarro F, Rematier P, Boschiero C, Labarre S, Werner M, Shpakovski GV, Thuriaux P. Partners of Rpb8p, a small subunit shared by yeast RNA polymerases I, II and III. Molecular and Cellular Biology. 2001; 21 :6056-6065 - 62.
Tan Q, Prysak MH, Woychik NA. Loss of the Rpb4/Rpb7 subcomplex in a mutant form of the Rpb6 subunit shared by RNA polymerases I, II, and III. Molecular and Cellular Biology. 2003; 23 :3329-3338 - 63.
Nouraini S, Archambault J, Friesen JD. Rpo26p, a subunit common to yeast RNA polymerases, is essential for the assembly of RNA polymerases I and II and for the stability of the largest subunits of these enzymes. Molecular and Cellular Biology. 1996; 16 :5985-5996 - 64.
Garrido-Godino AI, Garcia-Lopez MC, Navarro F. Correct assembly of RNA polymerase II depends on the foot domain and is required for multiple steps of transcription in Saccharomyces cerevisiae . Molecular and Cellular Biology. 2013;33 :3611-3626 - 65.
Garrido-Godino AI, Garcia-Lopez MC, Garcia-Martinez J, Pelechano V, Medina DA, Perez-Ortin JE, Navarro F. Rpb1 foot mutations demonstrate a major role of Rpb4 in mRNA stability during stress situations in yeast. Biochimica et Biophysica Acta. 2016; 1859 :731-743 - 66.
Shalem O, Groisman B, Choder M, Dahan O, Pilpel Y. Transcriptome kinetics is governed by a genome-wide coupling of mRNA production and degradation: A role for RNA Pol II. PLoS Genetics. 2011; 7 :e1002273 - 67.
Briand JF, Navarro F, Gadal O, Thuriaux P. Cross talk between tRNA and rRNA synthesis in Saccharomyces cerevisiae . Molecular and Cellular Biology. 2001;21 :189-195 - 68.
Koonin EV, Makarova KS, Elkins JG. Orthologs of the small RPB8 subunit of the eukaryotic RNA polymerases are conserved in hyperthermophilic Crenarchaeota and “Korarchaeota”. Biology Direct. 2007; 2 :38 - 69.
Korkhin Y, Unligil UM, Littlefield O, Nelson PJ, Stuart DI, Sigler PB, Bell SD, Abrescia NG. Evolution of complex RNA polymerases: The complete archaeal RNA polymerase structure. PLoS Biology. 2009; 7 :e1000102 - 70.
Voutsina A, Riva M, Carles C, Alexandraki D. Sequence divergence of the RNA polymerase shared subunit ABC14.5 (Rpb8) selectively affects RNA polymerase III assembly in Saccharomyces cerevisiae . Nucleic Acids Research. 1999;27 :1047-1055 - 71.
Carles C, Treich I, Bouet F, Riva M, Sentenac A. Two additional common subunits, ABC10 alpha and ABC10 beta, are shared by yeast RNA polymerases. Journal of Biological Chemistry. 1991; 266 :24092-24096 - 72.
Lalo D, Carles C, Sentenac A, Thuriaux P. Interactions between three common subunits of yeast RNA polymerases I and III. Proceedings of the National Academy of Sciences of the United States of America. 1993; 90 :5524-5528 - 73.
Gadal O, Shpakovski GV, Thuriaux P. Mutants in ABC10beta, a conserved subunit shared by all three yeast RNA polymerases, specifically affect RNA polymerase I assembly. The Journal of Biological Chemistry. 1999; 274 :8421-8427 - 74.
Lanzendörfer M, Langer D, Hain J, Klenk H-P, Holz I, Arnold-Ammer I, Zillig W. Structure and function of the DNA-dependent RNA polymerase of Sulfolobus . Systematic and Applied Microbiology. 1993;16 :656-664 - 75.
Amegadzie BY, Ahn B-Y, Moss B. Characterization of a 7-kilodalton subunit of vaccinia virus DNA-dependent RNA polymerase with structural similarities to the smallest subunit of eukaryotic RNA polymerase II. Journal of Virology. 1992; 66 :3003-3010 - 76.
Iyer LM, Balaji S, Koonin EV, Aravind L. Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. Virus Research. 2006; 117 :156-184 - 77.
Wild T, Cramer P. Biogenesis of multisubunit RNA polymerases. Trends in Biochemical Sciences. 2012; 37 :99-105 - 78.
Iyer V, Struhl K. Absolute mRNA levels and transcriptional initiation rates in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America. 1996; 93 :5208-5212 - 79.
Kostrewa D, Zeller ME, Armache KJ, Seizl M, Leike K, Thomm M, Cramer P. RNA polymerase II-TFIIB structure and mechanism of transcription initiation. Nature. 2009; 462 :323-330 - 80.
Rubbi L, Labarre-Mariotte S, Chedin S, Thuriaux P. Functional characterization of ABC10alpha, an essential polypeptide shared by all three forms of eukaryotic DNA-dependent RNA polymerases. The Journal of Biological Chemistry. 1999; 274 :31485-31492 - 81.
Treich I, Carles C, Riva M, Sentenac A. RPC10 encodes a new mini subunit shared by yeast nuclear RNA polymerases. Gene Expression. 1992; 2 :31-37 - 82.
Reich C, Zeller M, Milkereit P, Hausner W, Cramer P, Tschochner H, Thomm M. The archaeal RNA polymerase subunit P and the eukaryotic polymerase subunit Rpb12 are interchangeable in vivo and in vitro. Molecular Microbiology. 2009; 71 :989-1002 - 83.
Dumay H, Rubbi L, Sentenac A, Marck C. Interaction between yeast RNA polymerase III and transcription factor TFIIIC via ABC10α and τ131 subunits. Journal of Biological Chemistry. 1999; 274 :33462-33468