Epigenetics: Development and Disease pp 261-287 | Cite as
RNA Polymerase III Transcription – Regulated by Chromatin Structure and Regulator of Nuclear Chromatin Organization
Abstract
RNA polymerase III (Pol III) transcription is regulated by modifications of the chromatin. DNA methylation and post-translational modifications of histones, such as acetylation, phosphorylation and methylation have been linked to Pol III transcriptional activity. In addition to being regulated by modifications of DNA and histones, Pol III genes and its transcription factors have been implicated in the organization of nuclear chromatin in several organisms. In yeast, the ability of the Pol III transcription system to contribute to nuclear organization seems to be dependent on direct interactions of Pol III genes and/or its transcription factors TFIIIC and TFIIIB with the structural maintenance of chromatin (SMC) protein-containing complexes cohesin and condensin. In human cells, Pol III genes and transcription factors have also been shown to colocalize with cohesin and the transcription regulator and genome organizer CCCTC-binding factor (CTCF). Furthermore, chromosomal sites have been identified in yeast and humans that are bound by partial Pol III machineries (extra TFIIIC sites – ETC; chromosome organizing clamps – COC). These ETCs/COC as well as Pol III genes possess the ability to act as boundary elements that restrict spreading of heterochromatin.
Keywords
tRNA Gene Condensin Complex International Human Genome Sequencing Consortium Roberts Syndrome Cohesin LoadingNotes
Acknowledgements
The authors’ laboratory is funded by the national league against cancer (Equipe labellisée par la Ligue National Contre le Cancer). In addition it has received grants from the French national institutes of health (INSERM), the national research agency (ANR), the national institute of cancer (INCa), the regional government of Aquitaine and the French-Italian University.
References
- Albert I, Mavrich TN, Tomsho LP, Qi J, Zanton SJ, Schuster SC, Pugh BF (2007) Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446(7135):572–576PubMedCrossRefGoogle Scholar
- Alemán C, Roy-Engel AM, Shaikh TH, Deininger PL (2000) Cis-acting influences on Alu RNA levels. Nucleic Acids Res 28(23):4755–4761PubMedCrossRefGoogle Scholar
- Altaf M, Auger A, Monnet-Saksouk J, Brodeur J, Piquet S, Cramet M, Bouchard N, Lacoste N, Utley RT, Gaudreau L, Côté J (2010) NuA4-dependent acetylation of nucleosomal histones H4 and H2A directly stimulates incorporation of H2A.Z by the SWR1 complex. J Biol Chem 285(21):15966–15977PubMedCrossRefGoogle Scholar
- Anamika K, Krebs AR, Thompson J, Poch O, Devys D, Tora L (2010) Lessons from genome-wide studies: an integrated definition of the coactivator function of histone acetyl transferases. Epigenetics Chromatin 3(1):18PubMedCrossRefGoogle Scholar
- Bachman N, Gelbart ME, Tsukiyama T, Boeke JD (2005) TFIIIB subunit Bdp1p is required for periodic integration of the Ty1 retrotransposon and targeting of Isw2p to S. cerevisiae tDNAs. Genes Dev 19(8):955–964PubMedCrossRefGoogle Scholar
- Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21(3):381–395PubMedCrossRefGoogle Scholar
- Barski A, Chepelev I, Liko D, Cuddapah S, Fleming AB, Birch J, Cui K, White RJ, Zhao K (2010) Pol II and its associated epigenetic marks are present at Pol III-transcribed noncoding RNA genes. Nat Struct Mol Biol 17(5):629–634PubMedCrossRefGoogle Scholar
- Berger A, Strub K (2011) Multiple roles of Alu-related noncoding RNAs. Prog Mol Subcell Biol 51:119–146PubMedCrossRefGoogle Scholar
- Black JC, Whetstine JR (2011) Chromatin landscape: methylation beyond transcription. Epigenetics 6(1):9–15PubMedCrossRefGoogle Scholar
- Bose T, Gerton JL (2010) Cohesinopathies, gene expression, and chromatin organization. J Cell Biol 189(2):201–210PubMedCrossRefGoogle Scholar
- Boyd DC, Greger IH, Murphy S (2000) In vivo footprinting studies suggest a role for chromatin in transcription of the human 7SK gene. Gene 247(1–2):33–44PubMedCrossRefGoogle Scholar
- Braglia P, Dugas SL, Donze D, Dieci G (2007) Requirement of Nhp6 proteins for transcription of a subset of tRNA genes and heterochromatin barrier function in Saccharomyces cerevisiae. Mol Cell Biol 27(5):1545–1557PubMedCrossRefGoogle Scholar
- Briand JF, Navarro F, Gadal O, Thuriaux P (2001) Cross talk between tRNA and rRNA synthesis in Saccharomyces cerevisiae. Mol Cell Biol 21(1):189–195PubMedCrossRefGoogle Scholar
- Burnol AF, Margottin F, Huet J, Almouzni G, Prioleau MN, Méchali M, Sentenac A (1993a) TFIIIC relieves repression of U6 snRNA transcription by chromatin. Nature 362(6419):475–477PubMedCrossRefGoogle Scholar
- Burnol AF, Margottin F, Schultz P, Marsolier MC, Oudet P, Sentenac A (1993b) Basal promoter and enhancer element of yeast U6 snRNA gene. J Mol Biol 233(4):644–658PubMedCrossRefGoogle Scholar
- Callinan PA, Batzer MA (2006) Retrotransposable elements and human disease. Genome Dyn 1:104–115PubMedCrossRefGoogle Scholar
- Canella D, Praz V, Reina JH, Cousin P, Hernandez N (2010) Defining the RNA polymerase III transcriptome: genome-wide localization of the RNA polymerase III transcription machinery in human cells. Genome Res 20(6):710–721PubMedCrossRefGoogle Scholar
- Chang CR, Wu CS, Hom Y, Gartenberg MR (2005) Targeting of cohesin by transcriptionally silent chromatin. Genes Dev 19(24):3031–3042PubMedCrossRefGoogle Scholar
- Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Shevchenko A, Nasmyth K (2000) Cohesin’s binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5(2):243–254PubMedCrossRefGoogle Scholar
- Clark RM, Dalgliesh GL, Endres D, Gomez M, Taylor J, Bidichandani SI (2004) Expansion of GAA triplet repeats in the human genome: unique origin of the FRDA mutation at the center of an Alu. Genomics 83(3):373–383PubMedCrossRefGoogle Scholar
- Cordaux R, Batzer MA (2009) The impact of retrotransposons on human genome evolution. Nat Rev Genet 10(10):691–703PubMedCrossRefGoogle Scholar
- D’Ambrosio C, Schmidt CK, Katou Y, Kelly G, Itoh T, Shirahige K, Uhlmann F (2008) Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 22(16):2215–2227PubMedCrossRefGoogle Scholar
- Dai MS, Sun XX, Lu H (2010) Ribosomal protein L11 associates with c-Myc at 5 S rRNA and tRNA genes and regulates their expression. J Biol Chem 285(17):12587–12594PubMedCrossRefGoogle Scholar
- Deininger PL, Batzer MA (1999) Alu repeats and human disease. Mol Genet Metab 67(3):183–193PubMedCrossRefGoogle Scholar
- Demmerle J, Koch AJ, Holaska JM (2012) The nuclear envelope protein emerin binds directly to histone deacetylase 3 (HDAC3) and activates HDAC3 activity. J Biol Chem [Epub ahead of print]Google Scholar
- Dhillon N, Raab J, Guzzo J, Szyjka SJ, Gangadharan S, Aparicio OM, Andrews B, Kamakaka RT (2009) DNA polymerase epsilon, acetylases and remodellers cooperate to form a specialized chromatin structure at a tRNA insulator. EMBO J 28(17):2583–2600PubMedCrossRefGoogle Scholar
- Dieci G, Fiorino G, Castelnuovo M, Teichmann M, Pagano A (2007) The expanding RNA polymerase III transcriptome. Trends Genet 23(12):614–622PubMedCrossRefGoogle Scholar
- Donze D, Kamakaka RT (2001) RNA polymerase III and RNA polymerase II promoter complexes are heterochromatin barriers in Saccharomyces cerevisiae. EMBO J 20(3):520–531PubMedCrossRefGoogle Scholar
- Donze D, Adams CR, Rine J, Kamakaka RT (1999) The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev 13(6):698–708PubMedCrossRefGoogle Scholar
- Dubey RN, Gartenberg MR (2007) A tDNA establishes cohesion of a neighboring silent chromatin domain. Genes Dev 21(17):2150–2160PubMedCrossRefGoogle Scholar
- Ducrot C, Lefebvre O, Landrieux E, Guirouilh-Barbat J, Sentenac A, Acker J (2006) Reconstitution of the yeast RNA polymerase III transcription system with all recombinant factors. J Biol Chem 281(17):11685–11692PubMedCrossRefGoogle Scholar
- Dumay-Odelot H, Marck C, Durrieu-Gaillard S, Lefebvre O, Jourdain S, Prochazkova M, Pflieger A, Teichmann M (2007) Identification, molecular cloning, and characterization of the sixth subunit of human transcription factor TFIIIC. J Biol Chem 282(23):17179–17189PubMedCrossRefGoogle Scholar
- Dumay-Odelot H, Durrieu-Gaillard S, Da Silva D, Roeder RG, Teichmann M (2010) Cell growth- and differentiation-dependent regulation of RNA polymerase III transcription. Cell Cycle 9(18):3687–3699PubMedCrossRefGoogle Scholar
- Eilers M, Eisenman RN (2008) Myc’s broad reach. Genes Dev 22(20):2755–2766PubMedCrossRefGoogle Scholar
- Englander EW, Howard BH (1995) Nucleosome positioning by human Alu elements in chromatin. J Biol Chem 270(17):10091–10096PubMedCrossRefGoogle Scholar
- Englander EW, Wolffe AP, Howard BH (1993) Nucleosome interactions with a human Alu element. Transcriptional repression and effects of template methylation. J Biol Chem 268(26):19565–19573PubMedGoogle Scholar
- Eot-Houllier G, Fulcrand G, Watanabe Y, Magnaghi-Jaulin L, Jaulin C (2008) Histonedeacetylase 3 is required for centromeric H3K4 deacetylation and sister chromatid cohesion. Genes Dev 22(19):2639–2644PubMedCrossRefGoogle Scholar
- Eschenlauer JB, Kaiser MW, Gerlach VL, Brow DA (1993) Architecture of a yeast U6 RNA gene promoter. Mol Cell Biol 13(5):3015–3026PubMedGoogle Scholar
- Felts SJ, Weil PA, Chalkley R (1990) Transcription factor requirements for in vitro formation of transcriptionally competent 5S rRNA gene chromatin. Mol Cell Biol 10(5):2390–2401PubMedGoogle Scholar
- Flinn EM, Wallberg AE, Hermann S, Grant PA, Workman JL, Wright AP (2002) Recruitment of Gcn5-containing complexes during c-Myc-dependent gene activation. Structure and function aspects. J Biol Chem 277(26):23399–23406PubMedCrossRefGoogle Scholar
- Gard S, Light W, Xiong B, Bose T, McNairn AJ, Harris B, Fleharty B, Seidel C, Brickner JH, Gerton JL (2009) Cohesinopathy mutations disrupt the subnuclear organization of chromatin. J Cell Biol 187(4):455–462PubMedCrossRefGoogle Scholar
- Gatta R, Mantovani R (2010) Single nucleosome ChIPs identify an extensive switch of acetyl marks on cell cycle promoters. Cell Cycle 9(11):2149–2159PubMedCrossRefGoogle Scholar
- Geiduschek EP, Kassavetis GA (2001) The RNA polymerase III transcription apparatus. J Mol Biol 310(1):1–26PubMedCrossRefGoogle Scholar
- Gelbart ME, Bachman N, Delrow J, Boeke JD, Tsukiyama T (2005) Genome-wide identification of Isw2 chromatin-remodeling targets by localization of a catalytically inactive mutant. Genes Dev 19(8):942–954PubMedCrossRefGoogle Scholar
- Giuliodori S, Percudani R, Braglia P, Ferrari R, Guffanti E, Ottonello S, Dieci G (2003) A composite upstream sequence motif potentiates tRNA gene transcription in yeast. J Mol Biol 333(1):1–20PubMedCrossRefGoogle Scholar
- Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, Louis EJ, Mewes HW, Murakami Y, Philippsen P, Tettelin H, Oliver SG (1996) Life with 6000 genes. Science 274(5287):546, 563–567PubMedCrossRefGoogle Scholar
- Gomez-Roman N, Grandori C, Eisenman RN, White RJ (2003) Direct activation of RNA polymerase III transcription by c-Myc. Nature 421(6920):290–294PubMedCrossRefGoogle Scholar
- Gottesfeld J, Bloomer LS (1982) Assembly of transcriptionally active 5S RNA gene chromatin in vitro. Cell 28(4):781–791PubMedCrossRefGoogle Scholar
- Guffanti E, Percudani R, Harismendy O, Soutourina J, Werner M, Iacovella MG, Negri R, Dieci G (2006) Nucleosome depletion activates poised RNA polymerase III at unconventional transcription sites in Saccharomyces cerevisiae. J Biol Chem 281(39):29155–29164PubMedCrossRefGoogle Scholar
- Haeusler RA, Pratt-Hyatt M, Good PD, Gipson TA, Engelke DR (2008) Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. Genes Dev 22(16):2204–2214PubMedCrossRefGoogle Scholar
- Hakimi MA, Bochar DA, Schmiesing JA, Dong Y, Barak OG, Speicher DW, Yokomori K, Shiekhattar R (2002) A chromatin remodelling complex that loads cohesin ontohuman chromosomes. Nature 418(6901):994–998PubMedCrossRefGoogle Scholar
- 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(18):4738–4747PubMedCrossRefGoogle Scholar
- Hartman HB, Yu J, Alenghat T, Ishizuka T, Lazar MA (2005) The histone-binding code of nuclear receptor co-repressors matches the substrate specificity of histone deacetylase 3. EMBO Rep 6(5):445–451Google Scholar
- Häsler J, Samuelsson T, Strub K (2007) Useful ‘junk’: Alu RNAs in the human transcriptome. Cell Mol Life Sci 64(14):1793–1800PubMedCrossRefGoogle Scholar
- Haurie V, Durrieu-Gaillard S, Dumay-Odelot H, Da Silva D, Rey C, Prochazkova M, Roeder RG, Besser D, Teichmann M (2010) Two isoforms of human RNA polymerase III with specific functions in cell growth and transformation. Proc Natl Acad Sci USA 107(9):4176–4181PubMedCrossRefGoogle Scholar
- Hirano T (2005) Condensins: organizing and segregating the genome. Curr Biol 15(7):R265–R275PubMedCrossRefGoogle Scholar
- 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(11):7697–7704PubMedGoogle Scholar
- Huang Y, Maraia RJ (2001) Comparison of the RNA polymerase III transcription machinery in Schizosaccharomyces pombe, Saccharomyces cerevisiae and human. Nucleic Acids Res 29(13):2675–2690PubMedCrossRefGoogle Scholar
- Hudson DF, Marshall KM, Earnshaw WC (2009) Condensin: architect of mitotic chromosomes. Chromosome Res 17(2):131–144PubMedCrossRefGoogle Scholar
- Hull MW, Erickson J, Johnston M, Engelke DR (1994) tRNA genes as transcriptional repressor elements. Mol Cell Biol 14(2):1266–1277PubMedGoogle Scholar
- International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409(6822):860–921CrossRefGoogle Scholar
- International Human Genome Sequencing Consortium (2004) Finishing the euchromatic sequence of the human genome. Nature 431(7011):931–945CrossRefGoogle Scholar
- Iwasaki O, Tanaka A, Tanizawa H, Grewal SI, Noma K (2010) Centromeric localization of dispersed Pol III genes in fission yeast. Mol Biol Cell 21(2):254–265PubMedCrossRefGoogle Scholar
- Jin C, Zang C, Wei G, Cui K, Peng W, Zhao K, Felsenfeld G (2009) H3.3/H2A.Z double variant-containing nucleosomes mark ‘nucleosome-free regions’ of active promoters and other regulatory regions. Nat Genet 41(8):941–945PubMedCrossRefGoogle Scholar
- Johnson SA, Dubeau L, Johnson DL (2008) Enhanced RNA polymerase III-dependent transcription is required for oncogenic transformation. J Biol Chem 283(28):19184–19191PubMedCrossRefGoogle Scholar
- Johnson A, Li G, Sikorski TW, Buratowski S, Woodcock CL, Moazed D (2009) Reconstitution of heterochromatin-dependent transcriptional gene silencing. Mol Cell 35(6):769–781PubMedCrossRefGoogle Scholar
- Justice CM, Den Z, Nguyen SV, Stoneking M, Deininger PL, Batzer MA, Keats BJ (2001) Phylogenetic analysis of the Friedreich ataxia GAA trinucleotide repeat. J Mol Evol 52(3):232–238PubMedGoogle Scholar
- Kamath RV, Thor AD, Wang C, Edgerton SM, Slusarczyk A, Leary DJ, Wang J, Wiley EL, Jovanovic B, Wu Q, Nayar R, Kovarik P, Shi F, Huang S (2005) Perinucleolar compartment prevalence has an independent prognostic value for breast cancer. Cancer Res 65(1):246–253PubMedGoogle Scholar
- Kendall A, Hull MW, Bertrand E, Good PD, Singer RH, Engelke DR (2000) A CBF5 mutation that disrupts nucleolar localization of early tRNA biosynthesis in yeast also suppresses tRNA gene-mediated transcriptional silencing. Proc Natl Acad Sci USA 97(24):13108–13113PubMedCrossRefGoogle Scholar
- Kenneth NS, Ramsbottom BA, Gomez-Roman N, Marshall L, Cole PA, White RJ (2007) TRRAP and GCN5 are used by c-Myc to activate RNA polymerase III transcription. Proc Natl Acad Sci USA 104(38):14917–14922PubMedCrossRefGoogle Scholar
- Kim C, Rubin CM, Schmid CW (2001) Genome-wide chromatin remodeling modulates the Alu heat shock response. Gene 276(1–2):127–133PubMedCrossRefGoogle Scholar
- Kinsey PT, Sandmeyer SB (1991) Adjacent pol II and pol III promoters: transcription of the yeast retrotransposon Ty3 and a target tRNA gene. Nucleic Acids Res 19(6):1317–1324PubMedCrossRefGoogle Scholar
- Kundu TK, Wang Z, Roeder RG (1999) Human TFIIIC relieves chromatin-mediated repression of RNA polymerase III transcription and contains an intrinsic histone acetyltransferase activity. Mol Cell Biol 19(2):1605–1615PubMedGoogle Scholar
- Kurosaki T, Ninokata A, Wang L, Ueda S (2006) Evolutionary scenario for acquisition of CAG repeats in human SCA1 gene. Gene 373:23–27PubMedCrossRefGoogle Scholar
- Kurosaki T, Matsuura T, Ohno K, Ueda S (2009) Alu-mediated acquisition of unstable ATTCT pentanucleotide repeats in the human ATXN10 gene. Mol Biol Evol 26(11):2573–2579PubMedCrossRefGoogle Scholar
- Kurukuti S, Tiwari VK, Tavoosidana G, Pugacheva E, Murrell A, Zhao Z, Lobanenkov V, Reik W, Ohlsson R (2006) CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc Natl Acad Sci USA 103(28):10684–10689PubMedCrossRefGoogle Scholar
- Lassar AB, Hamer DH, Roeder RG (1985) Stable transcription complex on a class III gene in a minichromosome. Mol Cell Biol 5(1):40–45PubMedGoogle Scholar
- Lavoie BD, Hogan E, Koshland D (2004) In vivo requirements for rDNA chromosome condensation reveal two cell-cycle-regulated pathways for mitotic chromosome folding. Genes Dev 18(1):76–87PubMedCrossRefGoogle Scholar
- Lee W, Tillo D, Bray N, Morse RH, Davis RW, Hughes TR, Nislow C (2007) A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39(10):1235–1244PubMedCrossRefGoogle Scholar
- Lengronne A, Katou Y, Mori S, Yokobayashi S, Kelly GP, Itoh T, Watanabe Y, Shirahige K, Uhlmann F (2004) Cohesin relocation from sites of chromosomal loading to places of convergent transcription. Nature 430(6999):573–578PubMedCrossRefGoogle Scholar
- Li TH, Kim C, Rubin CM, Schmid CW (2000) K562 cells implicate increased chromatin accessibility in Alu transcriptional activation. Nucleic Acids Res 28(16):3031–3039PubMedCrossRefGoogle Scholar
- Libby RT, Hagerman KA, Pineda VV, Lau R, Cho DH, Baccam SL, Axford MM, Cleary JD, Moore JM, Sopher BL, Tapscott SJ, Filippova GN, Pearson CE, La Spada AR (2008) CTCF cis-regulates trinucleotide repeat instability in an epigenetic manner: a novel basis for mutational hot spot determination. PLoS Genet 4(11):e1000257PubMedCrossRefGoogle Scholar
- Ling JQ, Li T, Hu JF, Vu TH, Chen HL, Qiu XW, Cherry AM, Hoffman AR (2006) CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science 312(5771):269–272PubMedCrossRefGoogle Scholar
- Listerman I, Bledau AS, Grishina I, Neugebauer KM (2007) Extragenic accumulation of RNA polymerase II enhances transcription by RNA polymerase III. PLoS Genet 3(11):e212PubMedCrossRefGoogle Scholar
- Liu J, Krantz ID (2008) Cohesin and human disease. Annu Rev Genomics Hum Genet 9:303–320PubMedCrossRefGoogle Scholar
- Liu WM, Schmid CW (1993) Proposed roles for DNA methylation in Alu transcriptional and mutational inactivation. Nucleic Acids Res 21(6):1351–1359PubMedCrossRefGoogle Scholar
- Liu WM, Maraia RJ, Rubin CM, Schmid CW (1994) Alu transcripts: cytoplasmic localisation and regulation by DNA methylation. Nucleic Acids Res 22(6):1087–1095PubMedCrossRefGoogle Scholar
- Lunyak VV, Prefontaine GG, Núñez E, Cramer T, Ju BG, Ohgi KA, Hutt K, Roy R, García-Díaz A, Zhu X, Yung Y, Montoliu L, Glass CK, Rosenfeld MG (2007) Developmentally regulated activation of a SINE B2 repeat as a domain boundary in organogenesis. Science 317(5835):248–251PubMedCrossRefGoogle Scholar
- Mahapatra S, Dewari PS, Bhardwaj A, Bhargava P (2011) Yeast H2A.Z, FACT complex and RSC regulate transcription of tRNA gene through differential dynamics of flanking nucleosomes. Nucleic Acids Res 39(10):4023–4034PubMedCrossRefGoogle Scholar
- Marques M, Laflamme L, Gervais AL, Gaudreau L (2010) Reconciling the positive and negative roles of histone H2A.Z in gene transcription. Epigenetics 5(4):267–272PubMedCrossRefGoogle Scholar
- Marshall L, White RJ (2008) Non-coding RNA production by RNA polymerase III is implicated in cancer. Nat Rev Cancer 8(12):911–914PubMedCrossRefGoogle Scholar
- Martinato F, Cesaroni M, Amati B, Guccione E (2008) Analysis of Myc-induced histone modifications on target chromatin. PLoS One 3(11):e3650PubMedCrossRefGoogle Scholar
- Marzluff WF Jr, Huang RC (1975) Chromatin directed transcription of 5S and tRNA genes. Proc Natl Acad Sci USA 72(3):1082–1086PubMedCrossRefGoogle Scholar
- Matera AG, Frey MR, Margelot K, Wolin SL (1995) A perinucleolar compartment contains several RNA polymerase III transcripts as well as the polypyrimidine tract-binding protein, hnRNP I. J Cell Biol 129(5):1181–1193PubMedCrossRefGoogle Scholar
- Matsuura T, Yamagata T, Burgess DL, Rasmussen A, Grewal RP, Watase K, Khajavi M, McCall AE, Davis CF, Zu L, Achari M, Pulst SM, Alonso E, Noebels JL, Nelson DL, Zoghbi HY, Ashizawa T (2000) Large expansion of the ATTCT pentanucleotide repeat in spinocerebellar ataxia type 10. Nat Genet 26(2):191–194PubMedCrossRefGoogle Scholar
- Mavrich TN, Ioshikhes IP, Venters BJ, Jiang C, Tomsho LP, Qi J, Schuster SC, Albert I, Pugh BF (2008) A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 18(7):1073–1083PubMedCrossRefGoogle Scholar
- Mellor J, Morillon A (2004) ISWI complexes in Saccharomyces cerevisiae. Biochim Biophys Acta 1677(1–3):100–112PubMedGoogle Scholar
- Mertens C, Roeder RG (2008) Different functional modes of p300 in activation of RNA polymerase III transcription from chromatin templates. Mol Cell Biol 28(18):5764–5776PubMedCrossRefGoogle Scholar
- Michishita E, McCord RA, Berber E, Kioi M, Padilla-Nash H, Damian M, Cheung P, Kusumoto R, Kawahara TL, Barrett JC, Chang HY, Bohr VA, Ried T, Gozani O, Chua KF (2008) SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin. Nature 452(7186):492–496PubMedCrossRefGoogle Scholar
- 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(10):4118–4127PubMedCrossRefGoogle Scholar
- Moqtaderi Z, Wang J, Raha D, White RJ, Snyder M, Weng Z, Struhl K (2010) Genomic binding profiles of functionally distinct RNA polymerase III transcription complexes in human cells. Nat Struct Mol Biol 17(5):635–640PubMedCrossRefGoogle Scholar
- Morris SA, Rao B, Garcia BA, Hake SB, Diaz RL, Shabanowitz J, Hunt DF, Allis CD, Lieb JD, Strahl BD (2007) Identification of histone H3 lysine 36 acetylation as a highly conserved histone modification. J Biol Chem 282(10):7632–7640PubMedCrossRefGoogle Scholar
- Morse RH, Roth SY, Simpson RT (1992) A transcriptionally active tRNA gene interferes with nucleosome positioning in vivo. Mol Cell Biol 12(9):4015–4025PubMedGoogle Scholar
- Nagy Z, Tora L (2007) Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 26(37):5341–5357PubMedCrossRefGoogle Scholar
- Nagy Z, Riss A, Fujiyama S, Krebs A, Orpinell M, Jansen P, Cohen A, Stunnenberg HG, Kato S, Tora L (2010) The metazoan ATAC and SAGA coactivator HAT complexes regulate different sets of inducible target genes. Cell Mol Life Sci 67(4):611–628PubMedCrossRefGoogle Scholar
- Nasmyth K, Haering CH (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43:525–558PubMedCrossRefGoogle Scholar
- Neznanov NS, Oshima RG (1993) Cis regulation of the keratin 18 gene in transgenic mice. Mol Cell Biol 13(3):1815–1823PubMedGoogle Scholar
- Ng HH, Robert F, Young RA, Struhl K (2002) Genome-wide location and regulated recruitment of the RSC nucleosome-remodeling complex. Genes Dev 16(7):806–819PubMedCrossRefGoogle Scholar
- Nimura K, Ura K, Kaneda Y (2010) Histone methyltransferases: regulation of transcription and contribution to human disease. J Mol Med 88(12):1213–1220PubMedCrossRefGoogle Scholar
- Noma K, Cam HP, Maraia RJ, Grewal SI (2006) A role for TFIIIC transcription factor complex in genome organization. Cell 125(5):859–872PubMedCrossRefGoogle Scholar
- Norton JT, Pollock CB, Wang C, Schink JC, Kim JJ, Huang S (2008) Perinucleolar compartment prevalence is a phenotypic pancancer marker of malignancy. Cancer 113(4):861–869PubMedCrossRefGoogle Scholar
- Norton JT, Wang C, Gjidoda A, Henry RW, Huang S (2009) The perinucleolar compartment is directly associated with DNA. J Biol Chem 284(7):4090–4101PubMedCrossRefGoogle Scholar
- Oki M, Kamakaka RT (2005) Barrier function at HMR. Mol Cell 19(5):707–716PubMedCrossRefGoogle Scholar
- Oler AJ, Alla RK, Roberts DN, Wong A, Hollenhorst PC, Chandler KJ, Cassiday PA, Nelson CA, Hagedorn CH, Graves BJ, Cairns BR (2010) Human RNA polymerase III transcriptomes and relationships to Pol II promoter chromatin and enhancer-binding factors. Nat Struct Mol Biol 17(5):620–628PubMedCrossRefGoogle Scholar
- Orioli A, Pascali C, Pagano A, Teichmann M, Dieci G (2012) RNA polymerase III transcription control elements: themes and variations. Gene 493(2):185–194PubMedCrossRefGoogle Scholar
- Ostertag EM, Goodier JL, Zhang Y, Kazazian HH Jr (2003) SVA elements are nonautonomous retrotransposons that cause disease in humans. Am J Hum Genet 73(6):1444–1451PubMedCrossRefGoogle Scholar
- Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, Cobb BS, Yokomori K, Dillon N, Aragon L, Fisher AG, Merkenschlager M (2008) Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132(3):422–433PubMedCrossRefGoogle Scholar
- Parker CS, Roeder RG (1977) Selective and accurate transcription of the Xenopus laevis 5S RNA genes in isolated chromatin by purified RNA polymerase III. Proc Natl Acad Sci USA 74(1):44–48PubMedCrossRefGoogle Scholar
- Phillips JE, Corces VG (2009) CTCF: master weaver of the genome. Cell 137(7):1194–1211PubMedCrossRefGoogle Scholar
- Pollock C, Huang S (2010) The perinucleolar compartment. Cold Spring Harb Perspect Biol 2(2):a000679PubMedCrossRefGoogle Scholar
- Pombo A, Jackson DA, Hollinshead M, Wang Z, Roeder RG, Cook PR (1999) Regional specialization in human nuclei: visualization of discrete sites of transcription by RNA polymerase III. EMBO J 18(8):2241–2253PubMedCrossRefGoogle Scholar
- Ponicsan SL, Kugel JF, Goodrich JA (2010) Genomic gems: SINE RNAs regulate mRNA production. Curr Opin Genet Dev 20(2):149–155PubMedCrossRefGoogle Scholar
- Raha D, Wang Z, Moqtaderi Z, Wu L, Zhong G, Gerstein M, Struhl K, Snyder M (2010) Close association of RNA polymerase II and many transcription factors with Pol III genes. Proc Natl Acad Sci USA 107(8):3639–3644PubMedCrossRefGoogle Scholar
- Reynolds N, Salmon-Divon M, Dvinge H, Hynes-Allen A, Balasooriya G, Leaford D, Behrens A, Bertone P, Hendrich B (2011) NuRD-mediated deacetylation of H3K27 facilitates recruitment of Polycomb Repressive Complex 2 to direct gene repression. EMBO J 31(3):593–605Google Scholar
- 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(25):4695–4700CrossRefGoogle Scholar
- Roeder RG (2003) Lasker Basic Medical Research Award. The eukaryotic transcriptional machinery: complexities and mechanisms unforeseen. Nat Med 9:1239–1244PubMedCrossRefGoogle Scholar
- Roeder RG, Rutter WJ (1969) Multiple forms of DNA-dependent RNA polymerase in eukaryotic organisms. Nature 224(5216):234–237PubMedCrossRefGoogle Scholar
- Román AC, González-Rico FJ, Moltó E, Hernando H, Neto A, Vicente-Garcia C, Ballestar E, Gómez-Skarmeta JL, Vavrova-Anderson J, White RJ, Montoliu L, Fernández-Salguero PM (2011) Dioxin receptor and SLUG transcription factors regulate the insulator activity of B1 SINE retrotransposons via an RNA polymerase switch. Genome Res 21(3):422–432PubMedCrossRefGoogle Scholar
- Russanova VR, Driscoll CT, Howard BH (1995) Adenovirus type 2 preferentially stimulates polymerase III transcription of Alu elements by relieving repression: a potential role for chromatin. Mol Cell Biol 15(8):4282–4290PubMedGoogle Scholar
- Scharf AN, Imhof A (2011) Every methyl counts – epigenetic calculus. FEBS Lett 585(13):2001–2007PubMedCrossRefGoogle Scholar
- Schmid CW (1998) Does SINE evolution preclude Alu function? Nucleic Acids Res 26(20):4541–4550PubMedCrossRefGoogle Scholar
- Schramm L, Hernandez N (2002) Recruitment of RNA polymerase III to its target promoters. Genes Dev 16(20):2593–2620Google Scholar
- Scott KC, Merrett SL, Willard HF (2006) A heterochromatin barrier partitions the fission yeast centromere into discrete chromatin domains. Curr Biol 16(2):119–129PubMedCrossRefGoogle Scholar
- Shaikh TH, Roy AM, Kim J, Batzer MA, Deininger PL (1997) cDNAs derived from primary and small cytoplasmic Alu (scAlu) transcripts. J Mol Biol 271(2):222–234PubMedCrossRefGoogle Scholar
- Simms TA, Miller EC, Buisson NP, Jambunathan N, Donze D (2004) The Saccharomyces cerevisiae TRT2 tRNAThr gene upstream of STE6 is a barrier to repression in MATalpha cells and exerts a potential tRNA position effect in MATa cells. Nucleic Acids Res 32(17):5206–5213PubMedCrossRefGoogle Scholar
- Simms TA, Dugas SL, Gremillion JC, Ibos ME, Dandurand MN, Toliver TT, Edwards DJ, Donze D (2008) TFIIIC binding sites function as both heterochromatin barriers and chromatin insulators in Saccharomyces cerevisiae. Eukaryot Cell 7(12):2078–2086PubMedCrossRefGoogle 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(13):4920–4933PubMedCrossRefGoogle Scholar
- Sterner DE, Berger SL (2000) Acetylation of histones and transcription-related factors. Microbiol Mol Biol Rev 64(2):435–459PubMedCrossRefGoogle Scholar
- Stünkel W, Kober I, Seifart KH (1997) A nucleosome positioned in the distal promoter region activates transcription of the human U6 gene. Mol Cell Biol 17(8):4397–4405PubMedGoogle Scholar
- Tackett AJ, Dilworth DJ, Davey MJ, O’Donnell M, Aitchison JD, Rout MP, Chait BT (2005) Proteomic and genomic characterization of chromatin complexes at a boundary. J Cell Biol 169(1):35–47PubMedCrossRefGoogle Scholar
- Takahashi K, Murakami S, Chikashige Y, Niwa O, Yanagida M (1991) A large number of tRNA genes are symmetrically located in fission yeast centromeres. J Mol Biol 218(1):13–17PubMedCrossRefGoogle Scholar
- Tanaka Y, Yamashita R, Suzuki Y, Nakai K (2010) Effects of Alu elements on global nucleosome positioning in the human genome. BMC Genomics 11:309PubMedCrossRefGoogle Scholar
- Tang Y, Holbert MA, Wurtele H, Meeth K, Rocha W, Gharib M, Jiang E, Thibault P, Verreault A, Cole PA, Marmorstein R (2008) Fungal Rtt109 histone acetyltransferase is an unexpected structural homolog of metazoan p300/CBP. Nat Struct Mol Biol 15(9):998PubMedCrossRefGoogle Scholar
- Tavenet A, Suleau A, Dubreuil G, Ferrari R, Ducrot C, Michaut M, Aude JC, Dieci G, Lefebvre O, Conesa C, Acker J (2009) Genome-wide location analysis reveals a role for Sub1 in RNA polymerase III transcription. Proc Natl Acad Sci USA 106(34):14265–14270PubMedCrossRefGoogle Scholar
- Teichmann M, Dieci G, Pascali C, Boldina G (2010) General transcription factors and subunits of RNA polymerase III: paralogs for promoter- and cell type-specific transcription in multicellular eukaryotes. Transcription 1(3):130–135PubMedCrossRefGoogle Scholar
- Thompson M, Haeusler RA, Good PD, Engelke DR (2003) Nucleolar clustering of dispersed tRNA genes. Science 302(5649):1399–1401PubMedCrossRefGoogle Scholar
- Tie F, Banerjee R, Stratton CA, Prasad-Sinha J, Stepanik V, Zlobin A, Diaz MO, Scacheri PC, Harte PJ (2009) CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 136(18):3131–3141PubMedCrossRefGoogle Scholar
- Tremethick D, Zucker K, Worcel A (1990) The transcription complex of the 5S RNA gene, but not transcription factor IIIA alone, prevents nucleosomal repression of transcription. J Biol Chem 265(9):5014–5023PubMedGoogle Scholar
- Valenzuela L, Dhillon N, Kamakaka RT (2009) Transcription independent insulation at TFIIIC-dependent insulators. Genetics 183(1):131–148PubMedCrossRefGoogle Scholar
- Waldschmidt R, Wanandi I, Seifart KH (1991) Identification of transcription factors required for the expression of mammalian U6 genes in vitro. EMBO J 10(9):2595–2603PubMedGoogle Scholar
- Wang C, Politz JC, Pederson T, Huang S (2003) RNA polymerase III transcripts and the PTB protein are essential for the integrity of the perinucleolar compartment. Mol Biol Cell 14(6):2425–2435PubMedCrossRefGoogle Scholar
- Wang L, Haeusler RA, Good PD, Thompson M, Nagar S, Engelke DR (2005) Silencing near tRNA genes requires nucleolar localization. J Biol Chem 280(10):8637–8639PubMedCrossRefGoogle Scholar
- Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 40(7):897–903PubMedCrossRefGoogle Scholar
- Wasylyk B, Oudet P, Chambon P (1979) Preferential in vitro assembly of nucleosome cores on some AT-rich regions of SV40 DNA. Nucleic Acids Res 7(3):705–713PubMedCrossRefGoogle Scholar
- Weinmann R, Roeder RG (1974) Role of DNA-dependent RNA polymerase 3 in the transcription of the tRNA and 5S RNA genes. Proc Natl Acad Sci USA 71(5):1790–1794PubMedCrossRefGoogle Scholar
- Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, Aburatani H, Nakao M, Imamoto N, Maeshima K, Shirahige K, Peters JM (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451(7180):796–801PubMedCrossRefGoogle Scholar
- Westenberger SJ, Cui L, Dharia N, Winzeler E, Cui L (2009) Genome-wide nucleosome mapping of Plasmodium falciparum reveals histone-rich coding and histone-poor intergenic regions and chromatin remodeling of core and subtelomeric genes. BMC Genomics 10:610PubMedCrossRefGoogle Scholar
- White RJ (2008) RNA polymerases I and III, non-coding RNAs and cancer. Trends Genet 24(12):622–629PubMedCrossRefGoogle Scholar
- Willoughby DA, Vilalta A, Oshima RG (2000) An Alu element from the K18 gene confers position-independent expression in transgenic mice. J Biol Chem 275(2):759–768PubMedCrossRefGoogle Scholar
- Wood AJ, Severson AF, Meyer BJ (2010) Condensin and cohesin complexity: the expanding repertoire of functions. Nat Rev Genet 11(6):391–404Google Scholar
- Xhemalce B, Kouzarides T (2010) A chromodomain switch mediated by histone H3 Lys 4 acetylation regulates heterochromatin assembly. Genes Dev 24(7):647–652PubMedCrossRefGoogle Scholar
- Yang X, Yu W, Shi L, Sun L, Liang J, Yi X, Li Q, Zhang Y, Yang F, Han X, Zhang D, Yang J, Yao Z, Shang Y (2011) HAT4, a Golgi apparatus-anchored B-type histone acetyltransferase, acetylates free histone H4 and facilitates chromatin assembly. Mol Cell 44(1):39–50Google Scholar
- Zhang H, Roberts DN, Cairns BR (2005) Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123(2):219–231PubMedCrossRefGoogle Scholar
- Zhang Q, Zhong Q, Evans AG, Levy D, Zhong S (2011) Phosphorylation of histone H3 serine 28 modulates RNA polymerase III-dependent transcription. Oncogene 30(37):3943–3952PubMedCrossRefGoogle Scholar
- Zhao X, Pendergrast PS, Hernandez N (2001) A positioned nucleosome on the human U6 promoter allows recruitment of SNAPc by the Oct-1 POU domain. Mol Cell 7(3):539–549PubMedCrossRefGoogle Scholar
- Zhou VW, Goren A, Bernstein BE (2011) Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 12(1):7–18PubMedCrossRefGoogle Scholar