Regulation of RNA polymerase III transcription by Maf1 protein

• Autorzy: Ciesla M. , Boguta M.
• Języki publikacji: EN

Abstrakty

EN

Maf1 was the first protein discovered to regulate polymerase III RNA in yeast and because it is evolutionarily conserved, a Maf1 ortholog also serves to restrain transcription in mouse and human cells. Understanding the mechanism of the regulation has been made possible by recent studies showing that Maf1 is a nuclear/cytoplasmic protein whose subcellular distribution and hence negative regulation of Pol III transcription is mediated by the nutrient-sensing signaling pathways, TOR and RAS. Under stress conditions and during growth in a nonfermentable carbon source Maf1 is dephosphorylated and imported to the nucleus. In its non-phosphorylated form, Maf1 interacts with the polymerase III transcription machinery. Phosphorylation serves to locate Maf1 to the cytoplasm under favorable growth conditions, thereby preventing it from non-negatively regulating polymerase III when high levels of tRNA transcription are required. Relocation of Maf1 to the cytoplasm is dependent on Msn5, a carrier responsible for export of several other phosphoproteins out of the nucleus. The absence of Maf1-mediated control of tRNA synthesis impairs yeast viability in nonfermentable carbon sources. Moreover, in cells grown in a nonfer mentable carbon source, Maf1 regulates the levels of different tRNAs to various extents. This differential regulation may contribute to the physiological role of Maf1.

Słowa kluczowe

PL

RNA polymerase III; transcription regulation; tRNA synthesis; Maf1 protein; yeast; phosphorylation; physiological role

• Wydawca: -
• Czasopismo: Acta Biochimica Polonica
• Rocznik: 2008
• Tom: 55
• Numer: 2
• Opis fizyczny: p.215-225,fig.,ref.

Twórcy

autor

Ciesla M.

• Polish Academy of Sciences, A.Pawinskiego 5a, 02-106 Warsaw, Poland

autor

Boguta M.

Bibliografia

• Bartholomew B, Kassavetis GA, Geiduschek EP (1991) Two components of Saccharomyces cerevisiae transcription factor IIIB (TFIIIB) are stereospecifically located upstream of a tRNA gene and interact with the second-largest subunit of TFIIIC. Mol Cell Biol 11: 5181–5189.
• Boguta M, Czerska K, Zoladek T (1997) Mutation in a new gene MAF1 affects tRNA suppressor efficiency in Saccharomyces cerevisiae. Gene 185: 291–296.
• Borchert GM, Lanier W, Davidson BL (2006) RNA polymerase III transcribes human microRNAs. Nat Struct Mol Biol 13: 1097–1101.
• Broach JR (1991) RAS genes in Saccharomyces cerevisiae: signal transduction in search of a pathway. Trends Genet 7: 28–33.
• Brun I, Sentenac A, Werner M (1997) Dual role of the C34 subunit of RNA polymerase III in transcription initiation. EMBO J 16: 5730–5741.
• Budovskaya YV, Stephan JS, Deminoff SJ, Herman PK (2005) An evolutionary proteomics approach identifies substrates of the cAMP-dependent protein kinase. Proc Natl Acad Sci USA 102: 13933–13938.
• Chedin S, Ferri ML, Peyroche G, Andrau JC, Jourdain S, Lefebvre O, Werner M, Carles C, Sentenac A (1998) The yeast RNA polymerase III transcription machinery: a paradigm for eukaryotic gene activation. Cold Spring Harb Symp Quant Biol 63: 381–389.
• 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.
• Collins SR, Kemmeren P, Zhao XC, Greenblatt JF, Spencer F, Holstege FC, Weissman JS, Krogan NJ (2007) Toward a comprehensive atlas of the physical interactome of Saccharomyces cerevisiae. Mol Cell Proteomics 6:439–450.
• Cozzarelli NR, Gerrard SP, Schlissel M, Brown DD, Bogenhagen DF (1983) Purified RNA polymerase III accurately and efficiently terminates transcription of 5S RNA genes. Cell 34: 829–835.
• Deng W, Zhu X, Skogerbo G, Zhao Y, Fu Z, Wang Y, He H, Cai L, Sun H, Liu C, Li B, Bai B, Wang J, Jia D, Sun S, He H, Cui Y, Wang Y, Bu D, Chen R (2006) Organization of the Caenorhabditis elegans small non-coding transcriptome: genomic features, biogenesis, and expression. Genome Res 16: 20–29.
• Desai N, Lee J, Upadhya R, Chu Y, Moir RD, Willis IM (2005) Two steps in Maf1-dependent repression of transcription by RNA polymerase III. J Biol Chem 280: 6455–6462.
• Dieci G, Fiorino G, Castelnuovo M, Teichmann M, Pagano A (2007) The expanding RNA polymerase III transcriptome. Trends Genet 23: 614–22.
• Dieci G, Sentenac A (1996) Facilitated recycling pathway for RNA polymerase III. Cell 84: 245–252.
• Duvel K, Broach JR (2004) The role of phosphatases in TOR signaling in yeast. Curr Top Microbiol Immunol 279: 19–38.
• Felton-Edkins ZA, Kondrashov A, Karali D, Fairley JA, Dawson CW, Arrand JR, Young LS, White RJ (2006) Epstein-Barr virus induces cellular transcription factors to allow active expression of EBER genes by RNA polymerase III. J Biol Chem 281: 33871–33880.
• Fernandez-Tornero C, Bottcher B, Riva M, Carles C, Steuerwald U, Ruigrok RW, Sentenac A, Muller CW, Schoehn G (2007) Insights into transcription initiation and termination from the electron microscopy structure of yeast RNA polymerase III. Mol Cell 25: 813–823.
• Ferrari R, Rivetti C, Acker J, Dieci G (2004) Distinct roles of transcription factors TFIIIB and TFIIIC in RNA polymerase III transcription reinitiation. Proc Natl Acad Sci USA 101: 13442–13447.
• Ferri ML, Peyroche G, Siaut M, Lefebvre O, Carles C, Conesa C, Sentenac A (2000) A novel subunit of yeast RNA polymerase III interacts with the TFIIB-related domain of TFIIIB70. Mol Cell Biol 20: 488–495.
• Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, Remor M, Hofert C, Schelder M, Brajenovic M, Ruffner H, Merino A, Klein K, Hudak M, Dickson D, Rudi T, Gnau V, Bauch A, Bastuck S, Huhse B, Leutwein C, Heurtier MA, Copley RR, Edelmann A, Querfurth E, Rybin V, Drewes G, Raida M, Bouwmeester T, Bork P, Seraphin B, Kuster B, Neubauer G, Superti-Furga G (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141–147.
• Gavin AC, Aloy P, Grandi P, Krause R, Boesche M, Marzioch M, Rau C, Jensen LJ, Bastuck S, Dumpelfeld B, Edelmann A, Heurtier MA, Hoffman V, Hoefert C, Klein K, Hudak M, Michon AM, Schelder M, Schirle M, Remor M, Rudi T, Hooper S, Bauer A, Bouwmeester T, Casari G, Drewes G, Neubauer G, Rickn JM, Kuster B, Bork P, Russell RB, Superti-Furga G (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature 440: 631–636.
• Geiduschek EP, Kassavetis GA (2001) The RNA polymerase III transcription apparatus. J Mol Biol 310: 1–26.
• Goodfellow SJ, Graham EL, Kantidakis T, Marshall L, Coppins BA, Oficjalska-Pham D, Gerard M, Lefebvre O, White RJ (2008) Regulation of RNA polymerase III transcription by Maf1 in mammalian cells. J Mol Biol (in press).
• Harismendy O, Gendrel CG, Soularue P, Gidrol X, Sentenac A, Werner M, Lefebvre O (2003) Genome-wide location of yeast RNA polymerase III transcription machinery. EMBO J 22: 4738–4747.
• Hernandez N (1993) TBP, a universal eukaryotic transcription factor? Genes Dev 7: 1291–1308.
• Hsieh YJ, Kundu TK, Wang Z, Kovelman R, Roeder RG (1999) The TFIIIC90 subunit of TFIIIC interacts with multiple components of the RNA polymerase III machinery and contains a histone-specific acetyltransferase activity. Mol Cell Biol 19: 7697–7704.
• Jasiak AJ, Armache KJ, Martens B, Jansen RP, 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.
• Johnson SS, Zhang C, Fromm J, Willis IM, Johnson DL (2007) Mammalian Maf1 is a negative regulator of transcription by all three nuclear RNA polymerases. Mol Cell 26: 367–379.
• Juo ZS, Kassavetis GA, Wang J, Geiduschek EP, Sigler PB (2003) Crystal structure of a transcription factor IIIB core interface ternary complex. Nature 422: 534–539.
• Kassavetis GA, Bardeleben C, Kumar A, Ramirez E, Geiduschek EP (1997) Domains of the Brf component of RNA polymerase III transcription factor IIIB (TFIIIB): functions in assembly of TFIIIB-DNA complexes and recruitment of RNA polymerase to the promoter. Mol Cell Biol 17: 5299–5306.
• Kolesnikova OA, Entelis NS, Mireau H, Fox TD, Martin RP, Tarassov IA (2000) Suppression of mutations in mitochondrial DNA by tRNAs imported from the cytoplasm. Science 289: 1931–1933.
• Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, Ignatchenko A, Li J, Pu S, Datta N, Tikuisis AP, Punna T, Peregrin-Alvarez JM, Shales M, Zhang X, Davey M, Robinson MD, Paccanaro A, Bray JE, Sheung A, Beattie B, Richards DP, Canadien V, Lalev A, Mena F, Wong P, Starostine A, Canete MM, Vlasblom J, Wu S, Orsi C, Collins SR, Chandran S, Haw R, Rilstone JJ, Gandi K, Thompson NJ, Musso G, St Onge P, Ghanny S, Lam MH, Butland G, Altaf-Ul AM, Kanaya S, Shilatifard A, O’Shea E, Weissman JS, Ingles CJ, Hughes TR, Parkinson J, Gerstein M, Wodak SJ, Emili A, Greenblatt JF (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440:637–643.
• Kwapisz M, Smagowicz WJ, Oficjalska D, Hatin I, Rousset JP, Zoladek T, Boguta M (2002) Up-regulation of tRNA biosynthesis affects translational readthrough in maf1- delta mutant of Saccharomyces cerevisiae. Curr Genet 42: 147–152.
• Landrieux E, Alic N, Ducrot C, Acker J, Riva M, Carles C (2006) A subcomplex of RNA polymerase III subunits involved in transcription termination and reinitiation. EMBO J 25: 118–128.
• Moir RD, Lee J, Haeusler RA, Desai N, Engelke DR, Willis IM (2006) Protein kinase A regulates RNA polymerase III transcription through the nuclear localization of Maf1. Proc Natl Acad Sci USA103: 15044–15049.
• Moqtaderi Z, Struhl K (2004) Genome-wide occupancy profile of the RNA polymerase III machinery in Saccharomyces cerevisiae reveals loci with incomplete transcription complexes. Mol Cell Biol 24: 4118–4127.
• Mrazek J, Kreutmayer SB, Grasser FA, Polacek N, Huttenhofer A (2007) Subtractive hybridization identifies novel differentially expressed ncRNA species in EBV-infected human B cells. Nucleic Acids Res 35: e73.
• Murawski M, Szczesniak B, Zoladek T, Hopper AK, Martin NC, Boguta M (1994) maf1 mutation alters the subellular localization of the Mod5 protein in yeast. Acta Biochim Polon 41: 441–448.
• Ng HH, Robert F, Young RA, Struhl K (2002) Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex. Genes Dev 16: 806–819.
• Oficjalska-Pham D, Harismendy O, Smagowicz WJ, Gonzalez de Peredo A, Boguta M, Sentenac A, Lefebvre O (2006) General repression of RNA polymerase III transcription is triggered by protein phosphatase type 2A-mediated dephosphorylation of Maf1. Mol Cell 22: 623–632.
• Olivas WM, Muhlrad D, Parker R (1997) Analysis of the yeast genome: identification of new non-coding and small ORF-containing RNAs. Nucleic Acids Res 25: 4619–4625.
• 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.
• Proshkina GM, Shematorova EK, Proshkin SA, Zaros C, Thuriaux P, Shpakovski GV (2006) Ancient origin, functional conservation and fast evolution of DNA-dependent RNA polymerase III. Nucleic Acids Res 34: 3615–3624.
• Reina JH, Azzouz TN, Hernandez N (2006) Maf1, a new player in the regulation of human RNA polymerase III transcription. PLoS ONE 1: e134.
• Rinehart J, Krett B, Rubio MA, Alfonzo JD, Soll D (2005) Saccharomyces cerevisiae imports the cytosolic pathway for Gln-tRNA synthesis into the mitochondrion. Genes Dev 19: 583–592.
• Roberts DN, Stewart AJ, Huff JT, Cairns BR (2003) The RNA polymerase III transcriptome revealed by genome-wide localization and activity-occupancy relationships. Proc Natl Acad Sci USA 100: 14695–14700.
• Roberts DN, Wilson B, Huff JT, Stewart AJ, Cairns BR (2006) Dephosphorylation and genome-wide association of Maf1 with Pol III-transcribed genes during repression. Mol Cell 22: 633–644.
• Rollins J, Veras I, Cabarcas S, Willis I, Schramm L (2007) Human Maf1 negatively regulates RNA polymerase III transcription via the TFIIB family members Brf1 and Brf2. Int J Biol Sci 3: 292–302.
• Schramm L, Hernandez N (2002) Recruitment of RNA polymerase III to its target promoters. Genes Dev 16: 2593–2620.
• Thevelein JM, de Winde JH (1999) Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol Microbiol 33: 904–918.
• 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.
• Towpik J, Graczyk D, Gajda A, Lefebvre O, Boguta M (2008) Derepression of RNA polymerase III transcription by phosphorylation and nuclear export of its negative regulator, Maf1. J Biol Chem 283: 17168–17174.
• Tsang CK, Zheng XF (2007) TOR-in(g) the nucleus. Cell Cycle 6: 25–29.
• Upadhya R, Lee J, Willis IM (2002) Maf1 is an essential mediator of diverse signals that repress RNA polymerase III transcription. Mol Cell 10: 1489–1494.
• van Zyl W, Huang W, Sneddon AA, Stark M, Camier S,
• Werner M, Marck C, Sentenac A, Broach JR (1992) In activation of the protein phosphatase 2A regulatory subunit A results in morphological and transcriptional defects in Saccharomyces cerevisiae. Mol Cell Biol 12: 4946–4959.
• Wang Z, Roeder RG (1997) Three human RNA polymerase III-specific subunits form a subcomplex with a selective function in specific transcription initiation. Genes Dev 11: 1315–1326.
• Werner M, Hermann-Le Denmat S, Treich I, Sentenac A, Thuriaux P (1992) Effect of mutations in a zinc-binding domain of yeast RNA polymerase C (III) on enzyme function and subunit association. Mol Cell Biol 12: 1087–1095.
• Werner M, Chaussivert N, Willis IM, Sentenac A (1993) Interaction between a complex of RNA polymerase III subunits and the 70-kDa component of transcription factor IIIB. J Biol Chem 268: 20721–20724.
• White RJ (2005) RNA polymerases I and III, growth control and cancer. Nat Rev Mol Cell Biol 6: 69–78.
• Willis IM, Desai N, Upadhya R (2004) Signaling repression of transcription by RNA polymerase III in yeast. Prog Nucleic Acid Res Mol Biol 77: 323–353. Vol. 55
• Willis IM, Moir RD (2007) Integration of nutritional and stress signaling pathways by Maf1. Trends Biochem Sci 32: 51–53.
• Yoshihisa T, Yunoki-Esaki K, Ohshima C, Tanaka N, Endo T (2003) Possibility of cytoplasmic pre-tRNA splicing: the yeast tRNA splicing endonuclease mainly localizes on the mitochondria. Mol Biol Cell 14: 3266–3279.
• Yoshihisa T, Ohshima C, Yunoki-Esaki K, Endo T (2007) Cytoplasmic splicing of tRNA in Saccharomyces cerevisiae. Genes Cells 12: 285–297.
• Zaragoza D, Ghavidel A, Heitman J, Schultz MC (1998) Rapamycin induces the G0 program of transcriptional repression in yeast by interfering with the TOR signaling pathway. Mol Cell Biol 18: 4463–4470.
• Zaros C, Thuriaux P (2005) Rpc25, a conserved RNA polymerase III subunit, is critical for transcription initiation. Mol Microbiol 55: 104–114.