Rbs1, a New Protein Implicated in RNA Polymerase III Biogenesis in Yeast Saccharomyces cerevisiae

REFERENCES

• Lalo D, Carles C, Sentenac A, Thuriaux P. 1993. Interactions between three common subunits of yeast RNA polymerases I and III. Proc Natl Acad Sci U S A 90:5524–5528. http://dx.doi.org/10.1073/pnas.90.12.5524.
   PubMed Web of Science ®Google Scholar
• Carter R, Drouin G. 2010. The increase in the number of subunits in eukaryotic RNA polymerase III relative to RNA polymerase II is due to the permanent recruitment of general transcription factors. Mol Biol Evol 27:1035–1043. http://dx.doi.org/10.1093/molbev/msp316.
   PubMed Web of Science ®Google Scholar
• Ishihama A. 1981. Subunit of assembly of Escherichia coli RNA polymerase. Adv Biophys 14:1–35.
   PubMedGoogle Scholar
• 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. http://dx.doi.org/10.1074/jbc.272.41.25851.
   PubMed Web of Science ®Google Scholar
• Lane LA, Fernández-Tornero C, Zhou M, Morgner N, Ptchelkine D, Steuerwald U, Politis A, Lindner D, Gvozdenovic J, Gavin A-C, Müller CW, Robinson CV. 2011. Mass spectrometry reveals stable modules in holo and apo RNA polymerases I and III. Structure 19:90–100. http://dx.doi.org/10.1016/j.str.2010.11.009.
   PubMed Web of Science ®Google Scholar
• Wild T, Cramer P. 2012. Biogenesis of multisubunit RNA polymerases. Trends Biochem Sci 37:99–105. http://dx.doi.org/10.1016/j.tibs.2011.12.001.
   PubMed Web of Science ®Google Scholar
• Schoenfelder S, Clay I, Fraser P. 2010. The transcriptional interactome: gene expression in 3D. Curr Opin Genet Dev 20:127–133. http://dx.doi.org/10.1016/j.gde.2010.02.002.
   PubMed Web of Science ®Google Scholar
• Bertrand E, Houser-Scott F, Kendall A, Singer RH, Engelke DR. 1998. Nucleolar localization of early tRNA processing. Genes Dev 12:2463–2468. http://dx.doi.org/10.1101/gad.12.16.2463.
   PubMed Web of Science ®Google Scholar
• Chen M, Gartenberg MR. 2014. Coordination of tRNA transcription with export at nuclear pore complexes in budding yeast. Genes Dev 28:959–970. http://dx.doi.org/10.1101/gad.236729.113.
   PubMed Web of Science ®Google Scholar
• Boulon S, Pradet-Balade B, Verheggen C, Molle D, Boireau S, Georgieva M, Azzag K, Robert M-C, Ahmad Y, Neel H, Lamond AI, Bertrand E. 2010. HSP90 and its R2TP/prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II. Mol Cell 39:912–924. http://dx.doi.org/10.1016/j.molcel.2010.08.023.
   PubMed Web of Science ®Google Scholar
• Forget D, Lacombe A-A, Cloutier P, Lavallée-Adam M, Blanchette M, Coulombe B. 2013. Nuclear import of RNA polymerase II is coupled with nucleocytoplasmic shuttling of the RNA polymerase II-associated protein 2. Nucleic Acids Res 41:6881–6891. http://dx.doi.org/10.1093/nar/gkt455.
   PubMedGoogle Scholar
• Forget D, Lacombe A-A, Cloutier P, Al-Khoury R, Bouchard A, Lavallée-Adam M, Faubert D, Jeronimo C, Blanchette M, Coulombe B. 2010. The protein interaction network of the human transcription machinery reveals a role for the conserved GTPase RPAP4/GPN1 and microtubule assembly in nuclear import and biogenesis of RNA polymerase II. Mol Cell Proteomics 9:2827–2839. http://dx.doi.org/10.1074/mcp.M110.003616.
   PubMed Web of Science ®Google Scholar
• Staresincic L, Walker J, Dirac-Svejstrup AB, Mitter R, Svejstrup JQ. 2011. GTP-dependent binding and nuclear transport of RNA polymerase II by Npa3 protein. J Biol Chem 286:35553–35561. http://dx.doi.org/10.1074/jbc.M111.286161.
   PubMed Web of Science ®Google Scholar
• Di Croce L. 2011. Regulating the shuttling of eukaryotic RNA polymerase II. Mol Cell Biol 31:3918–3920. http://dx.doi.org/10.1128/MCB.06093-11.
   PubMedGoogle Scholar
• Peiró-Chova L, Estruch F. 2007. Specific defects in different transcription complexes compensate for the requirement of the negative cofactor 2 repressor in Saccharomyces cerevisiae. Genetics 176:125–138. http://dx.doi.org/10.1534/genetics.106.066829.
   PubMedGoogle Scholar
• Gómez-Navarro N, Peiró-Chova L, Rodriguez-Navarro S, Polaina J, Estruch F. 2013. Rtp1p is a karyopherin-like protein required for RNA polymerase II biogenesis. Mol Cell Biol 33:1756–1767. http://dx.doi.org/10.1128/MCB.01449-12.
   PubMed Web of Science ®Google Scholar
• Czeko E, Seizl M, Augsberger C, Mielke T, Cramer P. 2011. Iwr1 directs RNA polymerase II nuclear import. Mol Cell 42:261–266. http://dx.doi.org/10.1016/j.molcel.2011.02.033.
   PubMed Web of Science ®Google Scholar
• Mirón-García MC, Garrido-Godino AI, García-Molinero V, Hernández-Torres F, Rodríguez-Navarro S, Navarro F. 2013. The prefoldin bud27 mediates the assembly of the eukaryotic RNA polymerases in an rpb5-dependent manner. PLoS Genet 9:e1003297. http://dx.doi.org/10.1371/journal.pgen.1003297.
   PubMed Web of Science ®Google Scholar
• Minaker SW, Filiatrault MC, Ben-Aroya S, Hieter P, Stirling PC. 2013. Biogenesis of RNA polymerases II and III requires the conserved GPN small GTPases in Saccharomyces cerevisiae. Genetics 193:853–864. http://dx.doi.org/10.1534/genetics.112.148726.
   PubMed Web of Science ®Google Scholar
• Cieśla M, Towpik J, Graczyk D, Oficjalska-Pham D, Harismendy O, Suleau A, Balicki K, Conesa C, Lefebvre O, Boguta M. 2007. Maf1 is involved in coupling carbon metabolism to RNA polymerase III transcription. Mol Cell Biol 27:7693–7702. http://dx.doi.org/10.1128/MCB.01051-07.
   PubMed Web of Science ®Google Scholar
• Kwapisz M, Smagowicz WJ, Oficjalska D, Hatin I, Rousset J-P, Zoładek T, Boguta M. 2002. Up-regulation of tRNA biosynthesis affects translational readthrough in maf1-delta mutant of Saccharomyces cerevisiae. Curr Genet 42:147–152. http://dx.doi.org/10.1007/s00294-002-0342-7.
   PubMedGoogle Scholar
• 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. 2006. Rsc4 connects the chromatin remodeler RSC to RNA polymerases. Mol Cell Biol 26:4920–4933. http://dx.doi.org/10.1128/MCB.00415-06.
   PubMed Web of Science ®Google Scholar
• Sikorski RS, Hieter P. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar
• Neville M, Rosbash M. 1999. The NES-Crm1p export pathway is not a major mRNA export route in Saccharomyces cerevisiae. EMBO J 18:3746–3756. http://dx.doi.org/10.1093/emboj/18.13.3746.
   PubMed Web of Science ®Google Scholar
• Thuillier V, Stettler S, Sentenac A, Thuriaux P, Werner M. 1995. A mutation in the C31 subunit of Saccharomyces cerevisiae RNA polymerase III affects transcription initiation. EMBO J 14:351–359.
   PubMed Web of Science ®Google Scholar
• Dieci G, Hermann-Le Denmat S, Lukhtanov E, Thuriaux P, Werner M, Sentenac A. 1995. A universally conserved region of the largest subunit participates in the active site of RNA polymerase III. EMBO J 14:3766–3776.
   PubMedGoogle Scholar
• Thuillier V, Brun I, Sentenac A, Werner M. 1996. Mutations in the alpha-amanitin conserved domain of the largest subunit of yeast RNA polymerase III affect pausing, RNA cleavage and transcriptional transitions. EMBO J 15:618–629.
   PubMed Web of Science ®Google Scholar
• Rozenfeld S, Thuriaux P. 2001. A genetic look at the active site of RNA polymerase III. EMBO Rep 2:598–603. http://dx.doi.org/10.1093/embo-reports/kve136.
   PubMedGoogle Scholar
• Chédin S, Riva M, Schultz P, Sentenac A, Carles C. 1998. The RNA cleavage activity of RNA polymerase III is mediated by an essential TFIIS-like subunit and is important for transcription termination. Genes Dev 12:3857–3871. http://dx.doi.org/10.1101/gad.12.24.3857.
   PubMed Web of Science ®Google Scholar
• Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953–961.
   PubMed Web of Science ®Google Scholar
• Stettler S, Chiannilkulchai N, Hermann-Le Denmat S, Lalo D, Lacroute F, Sentenac A, Thuriaux P. 1993. A general suppressor of RNA polymerase I, II and III mutations in Saccharomyces cerevisiae. Mol Gen Genet 239:169–176.
   PubMedGoogle Scholar
• Nasmyth KA, Reed SI. 1980. Isolation of genes by complementation in yeast: molecular cloning of a cell-cycle gene. Proc Natl Acad Sci U S A 77:2119–2123. http://dx.doi.org/10.1073/pnas.77.4.2119.
   PubMed Web of Science ®Google Scholar
• Chen DC, Yang BC, Kuo TT. 1992. One-step transformation of yeast in stationary phase. Curr Genet 21:83–84. http://dx.doi.org/10.1007/BF00318659.
   PubMed Web of Science ®Google Scholar
• Schmitt ME, Brown TA, Trumpower BL. 1990. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res 18:3091–3092. http://dx.doi.org/10.1093/nar/18.10.3091.
   PubMed Web of Science ®Google Scholar
• Cieśla M, Mierzejewska J, Adamczyk M, Farrants A-KÖ, Boguta M. 2014. Fructose bisphosphate aldolase is involved in the control of RNA polymerase III-directed transcription. Biochim Biophys Acta 1843:1103–1110. http://dx.doi.org/10.1016/j.bbamcr.2014.02.007.
   PubMedGoogle Scholar
• Płociński P, Laubitz D, Cysewski D, Stoduœ K, Kowalska K, Dziembowski A. 2014. Identification of protein partners in mycobacteria using a single-step affinity purification method. PLoS One 9:e91380. http://dx.doi.org/10.1371/journal.pone.0091380.
   PubMedGoogle Scholar
• Orlowska KP, Klosowska K, Szczesny RJ, Cysewski D, Krawczyk PS, Dziembowski A. 2013. A new strategy for gene targeting and functional proteomics using the DT40 cell line. Nucleic Acids Res 41:e167. http://dx.doi.org/10.1093/nar/gkt650.
   PubMedGoogle Scholar
• Cox J, Mann M. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 26:1367–1372. http://dx.doi.org/10.1038/nbt.1511.
   PubMed Web of Science ®Google Scholar
• Jasiak AJ, Armache K-J, Martens B, Jansen R-P, Cramer P. 2006. Structural biology of RNA polymerase III: subcomplex C17/25 X-ray structure and 11 subunit enzyme model. Mol Cell 23:71–81. http://dx.doi.org/10.1016/j.molcel.2006.05.013.
   PubMed Web of Science ®Google Scholar
• Engel C, Sainsbury S, Cheung AC, Kostrewa D, Cramer P. 2013. RNA polymerase I structure and transcription regulation. Nature 502:650–655. http://dx.doi.org/10.1038/nature12712.
   PubMed Web of Science ®Google Scholar
• Fernández-Tornero C, Böttcher B, Rashid UJ, Steuerwald U, Flörchinger B, Devos DP, Lindner D, Müller CW. 2010. Conformational flexibility of RNA polymerase III during transcriptional elongation. EMBO J 29:3762–3772. http://dx.doi.org/10.1038/emboj.2010.266.
   PubMed Web of Science ®Google Scholar
• Hampsey M. 1997. A review of phenotypes in Saccharomyces cerevisiae. Yeast 13:1099–1133.
   PubMed Web of Science ®Google Scholar
• Gadal O, Shpakovski GV, Thuriaux P. 1999. Mutants in ABC10beta, a conserved subunit shared by all three yeast RNA polymerases, specifically affect RNA polymerase I assembly. J Biol Chem 274:8421–8427. http://dx.doi.org/10.1074/jbc.274.13.8421.
   PubMed Web of Science ®Google Scholar
• Archambault J, Friesen JD. 1993. Genetics of eukaryotic RNA polymerases I, II, and III. Microbiol Rev 57:703–724.
   PubMedGoogle Scholar
• Jensen TH, Neville M, Rain JC, McCarthy T, Legrain P, Rosbash M. 2000. Identification of novel Saccharomyces cerevisiae proteins with nuclear export activity: cell cycle-regulated transcription factor ace2p shows cell cycle-independent nucleocytoplasmic shuttling. Mol Cell Biol 20:8047–8058. http://dx.doi.org/10.1128/MCB.20.21.8047-8058.2000.
   PubMedGoogle Scholar
• Pluta K, Lefebvre O, Martin NC, Smagowicz WJ, Stanford DR, Ellis SR, Hopper AK, Sentenac A, Boguta M. 2001. Maf1p, a negative effector of RNA polymerase III in Saccharomyces cerevisiae. Mol Cell Biol 21:5031–5040. http://dx.doi.org/10.1128/MCB.21.15.5031-5040.2001.
   PubMed Web of Science ®Google Scholar
• Garrido-Godino AI, García-López MC, Navarro F. 2013. Correct assembly of RNA polymerase II depends on the foot domain and is required for multiple steps of transcription in Saccharomyces cerevisiae. Mol Cell Biol 33:3611–3626. http://dx.doi.org/10.1128/MCB.00262-13.
   PubMed Web of Science ®Google Scholar
• Panse VG, Hardeland U, Werner T, Kuster B, Hurt E. 2004. A proteome-wide approach identifies sumoylated substrate proteins in yeast. J Biol Chem 279:41346–41351. http://dx.doi.org/10.1074/jbc.M407950200.
   PubMed Web of Science ®Google Scholar
• Wohlschlegel JA, Johnson ES, Reed SI, Yates JR. 2004. Global analysis of protein sumoylation in Saccharomyces cerevisiae. J Biol Chem 279:45662–45668. http://dx.doi.org/10.1074/jbc.M409203200.
   PubMed Web of Science ®Google Scholar
• Albuquerque CP, Wang G, Lee NS, Kolodner RD, Putnam CD, Zhou H. 2013. Distinct SUMO ligases cooperate with Esc2 and Slx5 to suppress duplication-mediated genome rearrangements. PLoS Genet 9:e1003670. http://dx.doi.org/10.1371/journal.pgen.1003670.
   PubMedGoogle Scholar
• Hardeland U, Hurt E. 2006. Coordinated nuclear import of RNA polymerase III subunits. Traffic 7:465–473. http://dx.doi.org/10.1111/j.1600-0854.2006.00399.x.
   PubMedGoogle Scholar
• Archambault J, Schappert KT, Friesen JD. 1990. A suppressor of an RNA polymerase II mutation of Saccharomyces cerevisiae encodes a subunit common to RNA polymerases I, II, and III. Mol Cell Biol 10:6123–6131.
   PubMedGoogle Scholar
• Thuriaux P, Mariotte S, Buhler JM, Sentenac A, Vu L, Lee BS, Nomura M. 1995. Gene RPA43 in Saccharomyces cerevisiae encodes an essential subunit of RNA polymerase I. J Biol Chem 270:24252–24257. http://dx.doi.org/10.1074/jbc.270.41.24252.
   PubMedGoogle Scholar
• 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. 1999. A protein-protein interaction map of yeast RNA polymerase III. Proc Natl Acad Sci U S A 96:7815–7820. http://dx.doi.org/10.1073/pnas.96.14.7815.
   PubMedGoogle Scholar
• Voutsina A, Riva M, Carles C, Alexandraki D. 1999. Sequence divergence of the RNA polymerase shared subunit ABC14.5 (Rpb8) selectively affects RNA polymerase III assembly in Saccharomyces cerevisiae. Nucleic Acids Res 27:1047–1055. http://dx.doi.org/10.1093/nar/27.4.1047.
   PubMedGoogle Scholar
• Kutay U, Güttinger S. 2005. Leucine-rich nuclear-export signals: born to be weak. Trends Cell Biol 15:121–124. http://dx.doi.org/10.1016/j.tcb.2005.01.005.
   PubMed Web of Science ®Google Scholar
• Grishin NV. 1998. The R3H motif: a domain that binds single-stranded nucleic acids. Trends Biochem Sci 23:329–330. http://dx.doi.org/10.1016/S0968-0004(98)01258-4.
   PubMedGoogle Scholar
• Alberti S, Halfmann R, King O, Kapila A, Lindquist S. 2009. A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137:146–158. http://dx.doi.org/10.1016/j.cell.2009.02.044.
   PubMed Web of Science ®Google Scholar