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Basic Mechanisms in RNA Polymerase I Transcription of the Ribosomal RNA Genes

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Part of the book series: Subcellular Biochemistry ((SCBI,volume 61))

Abstract

RNA Polymerase (Pol) I produces ribosomal (r)RNA, an essential component of the cellular protein synthetic machinery that drives cell growth, underlying many fundamental cellular processes. Extensive research into the mechanisms governing transcription by Pol I has revealed an intricate set of control mechanisms impinging upon rRNA production. Pol I-specific transcription factors guide Pol I to the rDNA promoter and contribute to multiple rounds of transcription initiation, promoter escape, elongation and termination. In addition, many accessory factors are now known to assist at each stage of this transcription cycle, some of which allow the integration of transcriptional activity with metabolic demands. The organisation and accessibility of rDNA chromatin also impinge upon Pol I output, and complex mechanisms ensure the appropriate maintenance of the epigenetic state of the nucleolar genome and its effective transcription by Pol I. The following review presents our current understanding of the components of the Pol I transcription machinery, their functions and regulation by associated factors, and the mechanisms operating to ensure the proper transcription of rDNA chromatin. The importance of such stringent control is demonstrated by the fact that deregulated Pol I transcription is a feature of cancer and other disorders characterised by abnormal translational capacity.

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References

  • Albert B, Leger-Silvestre I, Normand C, Ostermaier MK, Perez-Fernandez J, Panov KI, Zomerdijk JC, Schultz P, Gadal O (2011) RNA polymerase I-specific subunits promote polymerase clustering to enhance the rRNA gene transcription cycle. J Cell Biol 192:277–293

    Article  PubMed  CAS  Google Scholar 

  • Aprikian P, Moorefield B, Reeder RH (2001) New model for the yeast RNA polymerase I transcription cycle. Mol Cell Biol 21:4847–4855

    Article  PubMed  CAS  Google Scholar 

  • Arabi A, Wu S, Ridderstrale K, Bierhoff H, Shiue C, Fatyol K, Fahlen S, Hydbring P, Soderberg O, Grummt I, Larsson LG, Wright AP (2005) c-Myc associates with ribosomal DNA and activates RNA polymerase I transcription. Nat Cell Biol 7:303–310

    Article  PubMed  CAS  Google Scholar 

  • Ayrault O, Andrique L, Fauvin D, Eymin B, Gazzeri S, Seite P (2006) Human tumor suppressor p14ARF negatively regulates rRNA transcription and inhibits UBF1 transcription factor phosphorylation. Oncogene 25:7577–7586

    Article  PubMed  CAS  Google Scholar 

  • Bazett-Jones DP, Leblanc B, Herfort M, Moss T (1994) Short-range DNA looping by the Xenopus HMG-box transcription factor, xUBF. Science 264:1134–1137

    Article  PubMed  CAS  Google Scholar 

  • Beckmann H, Chen JL, O’Brien T, Tjian R (1995) Coactivator and promoter-selective properties of RNA polymerase I TAFs. Science 270:1506–1509

    Article  PubMed  CAS  Google Scholar 

  • Beckouet F, Labarre-Mariotte S, Albert B, Imazawa Y, Werner M, Gadal O, Nogi Y, Thuriaux P (2008) Two RNA polymerase I subunits control the binding and release of Rrn3 during transcription. Mol Cell Biol 28:1596–1605

    Article  PubMed  CAS  Google Scholar 

  • Bell SP, Learned RM, Jantzen HM, Tjian R (1988) Functional cooperativity between transcription factors UBF1 and SL1 mediates human ribosomal RNA synthesis. Science 241:1192–1197

    Article  PubMed  CAS  Google Scholar 

  • Bierhoff H, Dundr M, Michels AA, Grummt I (2008) Phosphorylation by casein kinase 2 facilitates rRNA gene transcription by promoting dissociation of TIF-IA from elongating RNA polymerase I. Mol Cell Biol 28:4988–4998

    Article  PubMed  CAS  Google Scholar 

  • Birch JL, Zomerdijk JC (2008) Structure and function of ribosomal RNA gene chromatin. Biochem Soc Trans 36:619–624

    Article  PubMed  CAS  Google Scholar 

  • Birch JL, Tan BC, Panov KI, Panova TB, Andersen JS, Owen-Hughes TA, Russell J, Lee SC, Zomerdijk JC (2009) FACT facilitates chromatin transcription by RNA polymerases I and III. EMBO J 28:854–865

    Article  PubMed  CAS  Google Scholar 

  • Bodem J, Dobreva G, Hoffmann-Rohrer U, Iben S, Zentgraf H, Delius H, Vingron M, Grummt I (2000) TIF-IA, the factor mediating growth-dependent control of ribosomal RNA synthesis, is the mammalian homolog of yeast Rrn3p. EMBO Rep 1:171–175

    Article  PubMed  CAS  Google Scholar 

  • Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI (2007) The multifunctional nucleolus. Nat Rev Mol Cell Biol 8:574–585

    Article  PubMed  CAS  Google Scholar 

  • Boukhgalter B, Liu M, Guo A, Tripp M, Tran K, Huynh C, Pape L (2002) Characterization of a fission yeast subunit of an RNA polymerase I essential transcription initiation factor, SpRrn7h/TAF(I)68, that bridges yeast and mammals: association with SpRrn11h and the core ribosomal RNA gene promoter. Gene 291:187–201

    Article  PubMed  CAS  Google Scholar 

  • Bradsher J, Auriol J, Proietti de Santis L, Iben S, Vonesch JL, Grummt I, Egly JM (2002) CSB is a component of RNA pol I transcription. Mol Cell 10:819–829

    Article  PubMed  CAS  Google Scholar 

  • Braglia P, Heindl K, Schleiffer A, Martinez J, Proudfoot NJ (2010) Role of the RNA/DNA kinase Grc3 in transcription termination by RNA polymerase I. EMBO Rep 11:758–764

    Article  PubMed  CAS  Google Scholar 

  • Braglia P, Kawauchi J, Proudfoot NJ (2011) Co-transcriptional RNA cleavage provides a failsafe termination mechanism for yeast RNA polymerase I. Nucleic Acids Res 39:1439–1448

    Article  PubMed  CAS  Google Scholar 

  • Brandenburger Y, Jenkins A, Autelitano DJ, Hannan RD (2001) Increased expression of UBF is a critical determinant for rRNA synthesis and hypertrophic growth of cardiac myocytes. FASEB J 15:2051–2053

    PubMed  CAS  Google Scholar 

  • Brill SJ, DiNardo S, Voelkel-Meiman K, Sternglanz R (1987) Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. Nature 326:414–416

    Article  PubMed  CAS  Google Scholar 

  • Brown SE, Szyf M (2007) Epigenetic programming of the rRNA promoter by MBD3. Mol Cell Biol 27:4938–4952

    Article  PubMed  CAS  Google Scholar 

  • Caburet S, Conti C, Schurra C, Lebofsky R, Edelstein SJ, Bensimon A (2005) Human ribosomal RNA gene arrays display a broad range of palindromic structures. Genome Res 15:1079–1085

    Article  PubMed  CAS  Google Scholar 

  • Camacho JA, Peterson CJ, White GJ, Morgan HE (1990) Accelerated ribosome formation and growth in neonatal pig hearts. Am J Physiol 258:C86–91

    PubMed  CAS  Google Scholar 

  • Cavanaugh AH, Hempel WM, Taylor LJ, Rogalsky V, Todorov G, Rothblum LI (1995) Activity of RNA polymerase I transcription factor UBF blocked by Rb gene product. Nature 374:177–180

    Article  PubMed  CAS  Google Scholar 

  • Cavanaugh AH, Hirschler-Laszkiewicz I, Hu Q, Dundr M, Smink T, Misteli T, Rothblum LI (2002) Rrn3 phosphorylation is a regulatory checkpoint for ribosome biogenesis. J Biol Chem 277:27423–27432

    Article  PubMed  CAS  Google Scholar 

  • Chen D, Belmont AS, Huang S (2004) Upstream binding factor association induces large-scale chromatin decondensation. Proc Natl Acad Sci USA 101:15106–15111

    Article  PubMed  CAS  Google Scholar 

  • Claypool JA, French SL, Johzuka K, Eliason K, Vu L, Dodd JA, Beyer AL, Nomura M (2004) Tor pathway regulates Rrn3p-dependent recruitment of yeast RNA polymerase I to the promoter but does not participate in alteration of the number of active genes. Mol Biol Cell 15:946–956

    Article  PubMed  CAS  Google Scholar 

  • Comai L, Tanese N, Tjian R (1992) The TATA-binding protein and associated factors are integral components of the RNA polymerase I transcription factor, SL1. Cell 68:965–976

    Article  PubMed  CAS  Google Scholar 

  • Comai L, Zomerdijk JC, Beckmann H, Zhou S, Admon A, Tjian R (1994) Reconstitution of transcription factor SL1: exclusive binding of TBP by SL1 or TFIID subunits. Science 266:1966–1972

    Article  PubMed  CAS  Google Scholar 

  • Conconi A, Bespalov VA, Smerdon MJ (2002) Transcription-coupled repair in RNA polymerase I-transcribed genes of yeast. Proc Natl Acad Sci USA 99:649–654

    Article  PubMed  CAS  Google Scholar 

  • Dauwerse JG, Dixon J, Seland S, Ruivenkamp CA, van Haeringen A, Hoefsloot LH, Peters DJ, Boers AC, Daumer-Haas C, Maiwald R, Zweier C, Kerr B, Cobo AM, Toral JF, Hoogeboom AJ, Lohmann DR, Hehr U, Dixon MJ, Breuning MH, Wieczorek D (2011) Mutations in genes encoding subunits of RNA polymerases I and III cause Treacher Collins syndrome. Nat Genet 43:20–22

    Article  PubMed  CAS  Google Scholar 

  • De Winter RF, Moss T (1986) Spacer promoters are essential for efficient enhancement of X. laevis ribosomal transcription. Cell 44:313–318

    Article  PubMed  Google Scholar 

  • Denissov S, van Driel M, Voit R, Hekkelman M, Hulsen T, Hernandez N, Grummt I, Wehrens R, Stunnenberg H (2007) Identification of novel functional TBP-binding sites and general factor repertoires. EMBO J 26:944–954

    Article  PubMed  CAS  Google Scholar 

  • Denissov S, Lessard F, Mayer C, Stefanovsky V, van Driel M, Grummt I, Moss T, Stunnenberg HG (2011) A model for the topology of active ribosomal RNA genes. EMBO Rep 12:231–237

    Article  PubMed  CAS  Google Scholar 

  • Drygin D, Rice WG, Grummt I (2010) The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu Rev Pharmacol Toxicol 50:131–156

    Article  PubMed  CAS  Google Scholar 

  • Dundr M, Hoffmann-Rohrer U, Hu Q, Grummt I, Rothblum LI, Phair RD, Misteli T (2002) A kinetic framework for a mammalian RNA polymerase in vivo. Science 298:1623–1626

    Article  PubMed  CAS  Google Scholar 

  • Eberhard D, Tora L, Egly JM, Grummt I (1993) A TBP-containing multiprotein complex (TIF-IB) mediates transcription specificity of murine RNA polymerase I. Nucleic Acids Res 21:4180–4186

    Article  PubMed  CAS  Google Scholar 

  • El Hage A, Koper M, Kufel J, Tollervey D (2008) Efficient termination of transcription by RNA polymerase I requires the 5′ exonuclease Rat1 in yeast. Genes Dev 22:1069–1081

    Article  PubMed  CAS  Google Scholar 

  • El Hage A, French SL, Beyer AL, Tollervey D (2010) Loss of Topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis. Genes Dev 24:1546–1558

    Article  PubMed  CAS  Google Scholar 

  • Espada J, Ballestar E, Santoro R, Fraga MF, Villar-Garea A, Nemeth A, Lopez-Serra L, Ropero S, Aranda A, Orozco H, Moreno V, Juarranz A, Stockert JC, Langst G, Grummt I, Bickmore W, Esteller M (2007) Epigenetic disruption of ribosomal RNA genes and nucleolar architecture in DNA methyltransferase 1 (Dnmt1) deficient cells. Nucleic Acids Res 35:2191–2198

    Article  PubMed  CAS  Google Scholar 

  • Fath S, Milkereit P, Peyroche G, Riva M, Carles C, Tschochner H (2001) Differential roles of phosphorylation in the formation of transcriptional active RNA polymerase I. Proc Natl Acad Sci USA 98:14334–14339

    Article  PubMed  CAS  Google Scholar 

  • Fath S, Kobor MS, Philippi A, Greenblatt J, Tschochner H (2004) Dephosphorylation of RNA polymerase I by Fcp1p is required for efficient rRNA synthesis. J Biol Chem 279:25251–25259

    Article  PubMed  CAS  Google Scholar 

  • Feng W, Yonezawa M, Ye J, Jenuwein T, Grummt I (2010) PHF8 activates transcription of rRNA genes through H3K4me3 binding and H3K9me1/2 demethylation. Nat Struct Mol Biol 17(4):445–450

    Article  PubMed  CAS  Google Scholar 

  • French SL, Osheim YN, Cioci F, Nomura M, Beyer AL (2003) In exponentially growing Saccharomyces cerevisiae cells, rRNA synthesis is determined by the summed RNA polymerase I loading rate rather than by the number of active genes. Mol Cell Biol 23:1558–1568

    Article  PubMed  CAS  Google Scholar 

  • French SL, Sikes ML, Hontz RD, Osheim YN, Lambert TE, El Hage A, Smith MM, Tollervey D, Smith JS, Beyer AL (2011) Distinguishing the roles of Topoisomerases I and II in relief of transcription-induced torsional stress in yeast rRNA genes. Mol Cell Biol 31:482–494

    Article  PubMed  CAS  Google Scholar 

  • Frescas D, Guardavaccaro D, Bassermann F, Koyama-Nasu R, Pagano M (2007) JHDM1B/FBXL10 is a nucleolar protein that represses transcription of ribosomal RNA genes. Nature 450:309–313

    Article  PubMed  CAS  Google Scholar 

  • Friedrich JK, Panov KI, Cabart P, Russell J, Zomerdijk JC (2005) TBP-TAF complex SL1 directs RNA polymerase I pre-initiation complex formation and stabilizes upstream binding factor at the rDNA promoter. J Biol Chem 280:29551–29558

    Article  PubMed  CAS  Google Scholar 

  • Gadal O, Labarre S, Boschiero C, Thuriaux P (2002) Hmo1, an HMG-box protein, belongs to the yeast ribosomal DNA transcription system. EMBO J 21:5498–5507

    Article  PubMed  CAS  Google Scholar 

  • Geiger SR, Lorenzen K, Schreieck A, Hanecker P, Kostrewa D, Heck AJ, Cramer P (2010) RNA polymerase I contains a TFIIF-related DNA-binding subcomplex. Mol Cell 39:583–594

    Article  PubMed  CAS  Google Scholar 

  • Gorski JJ, Pathak S, Panov K, Kasciukovic T, Panova T, Russell J, Zomerdijk JC (2007) A novel TBP-associated factor of SL1 functions in RNA polymerase I transcription. EMBO J 26:1560–1568

    Article  PubMed  CAS  Google Scholar 

  • Gorski SA, Snyder SK, John S, Grummt I, Misteli T (2008) Modulation of RNA polymerase assembly dynamics in transcriptional regulation. Mol Cell 30:486–497

    Article  PubMed  CAS  Google Scholar 

  • Grandori C, Gomez-Roman N, Felton-Edkins ZA, Ngouenet C, Galloway DA, Eisenman RN, White RJ (2005) c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat Cell Biol 7:311–318

    Article  PubMed  CAS  Google Scholar 

  • Granneman S, Baserga SJ (2005) Crosstalk in gene expression: coupling and co-regulation of rDNA transcription, pre-ribosome assembly and pre-rRNA processing. Curr Opin Cell Biol 17:281–286

    Article  PubMed  CAS  Google Scholar 

  • Grimaldi G, Di Nocera PP (1988) Multiple repeated units in Drosophila melanogaster ribosomal DNA spacer stimulate rRNA precursor transcription. Proc Natl Acad Sci USA 85:5502–5506

    Article  PubMed  CAS  Google Scholar 

  • Grummt I (2003) Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17:1691–1702

    Article  PubMed  CAS  Google Scholar 

  • Grummt I, Pikaard CS (2003) Epigenetic silencing of RNA polymerase I transcription. Nat Rev Mol Cell Biol 4:641–649

    Article  PubMed  CAS  Google Scholar 

  • Grummt I, Voit R (2010) Linking rDNA transcription to the cellular energy supply. Cell Cycle 9:225–226

    Article  PubMed  CAS  Google Scholar 

  • Guerrero PA, Maggert KA (2011) The CCCTC-binding factor (CTCF) of Drosophila contributes to the regulation of the ribosomal DNA and nucleolar stability. PLoS One 6:e16401

    Article  PubMed  CAS  Google Scholar 

  • Guetg C, Lienemann P, Sirri V, Grummt I, Hernandez-Verdun D, Hottiger MO, Fussenegger M, Santoro R (2010) The NoRC complex mediates the heterochromatin formation and stability of silent rRNA genes and centromeric repeats. EMBO J 29:2135–2146

    Article  PubMed  CAS  Google Scholar 

  • Haaf T, Hayman DL, Schmid M (1991) Quantitative determination of rDNA transcription units in vertebrate cells. Exp Cell Res 193:78–86

    Article  PubMed  CAS  Google Scholar 

  • Haag JR, Pikaard CS (2007) RNA polymerase I: a multifunctional molecular machine. Cell 131:1224–1225

    Article  PubMed  CAS  Google Scholar 

  • Halkidou K, Logan IR, Cook S, Neal DE, Robson CN (2004) Putative involvement of the histone acetyltransferase Tip60 in ribosomal gene transcription. Nucleic Acids Res 32:1654–1665

    Article  PubMed  CAS  Google Scholar 

  • Hall DB, Wade JT, Struhl K (2006) An HMG protein, Hmo1, associates with promoters of many ribosomal protein genes and throughout the rRNA gene locus in Saccharomyces cerevisiae. Mol Cell Biol 26:3672–3679

    Article  PubMed  CAS  Google Scholar 

  • Hanada K, Song CZ, Yamamoto K, Yano K, Maeda Y, Yamaguchi K, Muramatsu M (1996) RNA polymerase I associated factor 53 binds to the nucleolar transcription factor UBF and functions in specific rDNA transcription. EMBO J 15:2217–2226

    PubMed  CAS  Google Scholar 

  • Hannan RD, Cavanaugh A, Hempel WM, Moss T, Rothblum L (1999) Identification of a mammalian RNA polymerase I holoenzyme containing components of the DNA repair/replication system. Nucleic Acids Res 27:3720–3727

    Article  PubMed  CAS  Google Scholar 

  • Hannan KM, Hannan RD, Smith SD, Jefferson LS, Lun M, Rothblum LI (2000) Rb and p130 regulate RNA polymerase I transcription: Rb disrupts the interaction between UBF and SL-1. Oncogene 19:4988–4999

    Article  PubMed  CAS  Google Scholar 

  • Hannan KM, Brandenburger Y, Jenkins A, Sharkey K, Cavanaugh A, Rothblum L, Moss T, Poortinga G, McArthur GA, Pearson RB, Hannan RD (2003) mTOR-dependent regulation of ribosomal gene transcription requires S6K1 and is mediated by phosphorylation of the carboxy-terminal activation domain of the nucleolar transcription factor UBF. Mol Cell Biol 23:8862–8877

    Article  PubMed  CAS  Google Scholar 

  • Heix J, Grummt I (1995) Species specificity of transcription by RNA polymerase I. Curr Opin Genet Dev 5:652–656

    Article  PubMed  CAS  Google Scholar 

  • Heix J, Zomerdijk JC, Ravanpay A, Tjian R, Grummt I (1997) Cloning of murine RNA polymerase I-specific TAF factors: conserved interactions between the subunits of the species-specific transcription initiation factor TIF-IB/SL1. Proc Natl Acad Sci USA 94:1733–1738

    Article  PubMed  CAS  Google Scholar 

  • Hempel WM, Cavanaugh AH, Hannan RD, Taylor L, Rothblum LI (1996) The species-specific RNA polymerase I transcription factor SL-1 binds to upstream binding factor. Mol Cell Biol 16:557–563

    PubMed  CAS  Google Scholar 

  • Hirschler-Laszkiewicz I, Cavanaugh AH, Mirza A, Lun M, Hu Q, Smink T, Rothblum LI (2003) Rrn3 becomes inactivated in the process of ribosomal DNA transcription. J Biol Chem 278:18953–18959

    Article  PubMed  CAS  Google Scholar 

  • Hoppe S, Bierhoff H, Cado I, Weber A, Tiebe M, Grummt I, Voit R (2009) AMP-activated protein kinase adapts rRNA synthesis to cellular energy supply. Proc Natl Acad Sci USA 106:17781–17786

    Article  PubMed  CAS  Google Scholar 

  • Huet J, Buhler JM, Sentenac A, Fromageot P (1975) Dissociation of two polypeptide chains from yeast RNA polymerase A. Proc Natl Acad Sci USA 72:3034–3038

    Article  PubMed  CAS  Google Scholar 

  • Iben S, Tschochner H, Bier M, Hoogstraten D, Hozak P, Egly JM, Grummt I (2002) TFIIH plays an essential role in RNA polymerase I transcription. Cell 109:297–306

    Article  PubMed  CAS  Google Scholar 

  • Ide S, Miyazaki T, Maki H, Kobayashi T (2010) Abundance of ribosomal RNA gene copies maintains genome integrity. Science 327:693–696

    Article  PubMed  CAS  Google Scholar 

  • Jansa P, Grummt I (1999) Mechanism of transcription termination: PTRF interacts with the largest subunit of RNA polymerase I and dissociates paused transcription complexes from yeast and mouse. Mol Gen Genet 262:508–514

    Article  PubMed  CAS  Google Scholar 

  • Jantzen HM, Admon A, Bell SP, Tjian R (1990) Nucleolar transcription factor hUBF contains a DNA-binding motif with homology to HMG proteins. Nature 344:830–836

    Article  PubMed  CAS  Google Scholar 

  • Jantzen HM, Chow AM, King DS, Tjian R (1992) Multiple domains of the RNA polymerase I activator hUBF interact with the TATA-binding protein complex hSL1 to mediate transcription. Genes Dev 6:1950–1963

    Article  PubMed  CAS  Google Scholar 

  • Jones HS, Kawauchi J, Braglia P, Alen CM, Kent NA, Proudfoot NJ (2007) RNA polymerase I in yeast transcribes dynamic nucleosomal rDNA. Nat Struct Mol Biol 14:123–130

    Article  PubMed  CAS  Google Scholar 

  • Kasahara K, Ohtsuki K, Ki S, Aoyama K, Takahashi H, Kobayashi T, Shirahige K, Kokubo T (2007) Assembly of regulatory factors on rRNA and ribosomal protein genes in Saccharomyces cerevisiae. Mol Cell Biol 27:6686–6705

    Article  PubMed  CAS  Google Scholar 

  • Kawauchi J, Mischo H, Braglia P, Rondon A, Proudfoot NJ (2008) Budding yeast RNA polymerases I and II employ parallel mechanisms of transcriptional termination. Genes Dev 22:1082–1092

    Article  PubMed  CAS  Google Scholar 

  • Kermekchiev M, Workman JL, Pikaard CS (1997) Nucleosome binding by the polymerase I transactivator upstream binding factor displaces linker histone H1. Mol Cell Biol 17:5833–5842

    PubMed  CAS  Google Scholar 

  • Kihm AJ, Hershey JC, Haystead TA, Madsen CS, Owens GK (1998) Phosphorylation of the rRNA transcription factor upstream binding factor promotes its association with TATA binding protein. Proc Natl Acad Sci USA 95:14816–14820

    Article  PubMed  CAS  Google Scholar 

  • Knutson BA, Hahn S (2011) Yeast Rrn7 and human TAF1B are TFIIB-related RNA polymerase I general transcription factors. Science 333:1637–1640

    Article  PubMed  CAS  Google Scholar 

  • Kruhlak M, Crouch EE, Orlov M, Montano C, Gorski SA, Nussenzweig A, Misteli T, Phair RD, Casellas R (2007) The ATM repair pathway inhibits RNA polymerase I transcription in response to chromosome breaks. Nature 447:730–734

    Article  PubMed  CAS  Google Scholar 

  • Kuhn A, Grummt I (1987) A novel promoter in the mouse rDNA spacer is active in vivo and in vitro. EMBO J 6:3487–3492

    PubMed  CAS  Google Scholar 

  • Kuhn CD, Geiger SR, Baumli S, Gartmann M, Gerber J, Jennebach S, Mielke T, Tschochner H, Beckmann R, Cramer P (2007) Functional architecture of RNA polymerase I. Cell 131:1260–1272

    Article  PubMed  CAS  Google Scholar 

  • Labhart P, Reeder RH (1984) Enhancer-like properties of the 60/81 bp elements in the ribosomal gene spacer of Xenopus laevis. Cell 37:285–289

    Article  PubMed  CAS  Google Scholar 

  • Laferte A, Favry E, Sentenac A, Riva M, Carles C, Chedin S (2006) The transcriptional activity of RNA polymerase I is a key determinant for the level of all ribosome components. Genes Dev 20:2030–2040

    Article  PubMed  CAS  Google Scholar 

  • Langst G, Blank TA, Becker PB, Grummt I (1997) RNA polymerase I transcription on nucleosomal templates: the transcription termination factor TTF-I induces chromatin remodeling and relieves transcriptional repression. EMBO J 16:760–768

    Article  PubMed  CAS  Google Scholar 

  • Lawrence RJ, Earley K, Pontes O, Silva M, Chen ZJ, Neves N, Viegas W, Pikaard CS (2004) A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol Cell 13:599–609

    Article  PubMed  CAS  Google Scholar 

  • Leporé N, Lafontaine DLJ (2011) A functional interface at the rDNA connects rRNA synthesis, pre-rRNA processing and nucleolar surveillance in budding yeast. PLoS One 6:e24962

    Article  PubMed  CAS  Google Scholar 

  • Lessard F, Morin F, Ivanchuk S, Langlois F, Stefanovsky V, Rutka J, Moss T (2010) The ARF tumor suppressor controls ribosome biogenesis by regulating the RNA polymerase I transcription factor TTF-I. Mol Cell 38:539–550

    Article  PubMed  CAS  Google Scholar 

  • Lewis JD, Tollervey D (2000) Like attracts like: getting RNA processing together in the nucleus. Science 288:1385–1389

    Article  PubMed  CAS  Google Scholar 

  • Liebhaber SA, Wolf S, Schlessinger D (1978) Differences in rRNA metabolism of primary and SV40-transformed human fibroblasts. Cell 13:121–127

    Article  PubMed  CAS  Google Scholar 

  • Lin CY, Navarro S, Reddy S, Comai L (2006) CK2-mediated stimulation of Pol I transcription by stabilization of UBF-SL1 interaction. Nucleic Acids Res 34:4752–4766

    Article  PubMed  CAS  Google Scholar 

  • Mais C, Wright JE, Prieto JL, Raggett SL, McStay B (2005) UBF-binding site arrays form pseudo-NORs and sequester the RNA polymerase I transcription machinery. Genes Dev 19:50–64

    Article  PubMed  CAS  Google Scholar 

  • Mayer C, Grummt I (2005) Cellular stress and nucleolar function. Cell Cycle 4:1036–1038

    Article  PubMed  CAS  Google Scholar 

  • Mayer C, Zhao J, Yuan X, Grummt I (2004) mTOR-dependent activation of the transcription factor TIF-IA links rRNA synthesis to nutrient availability. Genes Dev 18:423–434

    Article  PubMed  CAS  Google Scholar 

  • Mayer C, Bierhoff H, Grummt I (2005) The nucleolus as a stress sensor: JNK2 inactivates the transcription factor TIF-IA and down-regulates rRNA synthesis. Genes Dev 19:933–941

    Article  PubMed  CAS  Google Scholar 

  • Mayer C, Schmitz KM, Li J, Grummt I, Santoro R (2006) Intergenic transcripts regulate the epigenetic state of rRNA genes. Mol Cell 22:351–361

    Article  PubMed  CAS  Google Scholar 

  • Mayer C, Neubert M, Grummt I (2008) The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus. EMBO Rep 9:774–780

    Article  PubMed  CAS  Google Scholar 

  • McStay B, Grummt I (2008) The epigenetics of rRNA genes: from molecular to chromosome biology. Annu Rev Cell Dev Biol 24:131–157

    Article  PubMed  CAS  Google Scholar 

  • Merz K, Hondele M, Goetze H, Gmelch K, Stoeckl U, Griesenbeck J (2008) Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules. Genes Dev 22:1190–1204

    Article  PubMed  CAS  Google Scholar 

  • Milkereit P, Tschochner H (1998) A specialized form of RNA polymerase I, essential for initiation and growth-dependent regulation of rRNA synthesis, is disrupted during transcription. EMBO J 17:3692–3703

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Panov KI, Friedrich JK, Trinkle-Mulcahy L, Lamond AI, Zomerdijk JC (2001) hRRN3 is essential in the SL1-mediated recruitment of RNA polymerase I to rRNA gene promoters. EMBO J 20:1373–1382

    Article  PubMed  CAS  Google Scholar 

  • Moore PB, Steitz TA (2002) The involvement of RNA in ribosome function. Nature 418:229–235

    Article  PubMed  CAS  Google Scholar 

  • Moss T (2004) At the crossroads of growth control; making ribosomal RNA. Curr Opin Genet Dev 14:210–217

    Article  PubMed  CAS  Google Scholar 

  • Moss T, Stefanovsky VY (2002) At the center of eukaryotic life. Cell 109:545–548

    Article  PubMed  CAS  Google Scholar 

  • Murano K, Okuwaki M, Hisaoka M, Nagata K (2008) Transcription regulation of the rRNA gene by a multifunctional nucleolar protein, B23/nucleophosmin, through its histone chaperone activity. Mol Cell Biol 28:3114–3126

    Article  PubMed  CAS  Google Scholar 

  • Murayama A, Ohmori K, Fujimura A, Minami H, Yasuzawa-Tanaka K, Kuroda T, Oie S, Daitoku H, Okuwaki M, Nagata K, Fukamizu A, Kimura K, Shimizu T, Yanagisawa J (2008) Epigenetic control of rDNA loci in response to intracellular energy status. Cell 133:627–639

    Article  PubMed  CAS  Google Scholar 

  • Muth V, Nadaud S, Grummt I, Voit R (2001) Acetylation of TAF(I)68, a subunit of TIF-IB/SL1, activates RNA polymerase I transcription. EMBO J 20:1353–1362

    Article  PubMed  CAS  Google Scholar 

  • Naidu S, Friedrich JK, Russell J, Zomerdijk JC (2011) TAF1B is a TFIIB-like component of the basal transcription machinery for RNA polymerase I. Science 333:1640–1642

    Article  PubMed  CAS  Google Scholar 

  • Narla A, Ebert BL (2010) Ribosomopathies: human disorders of ribosome dysfunction. Blood 115:3196–3205

    Article  PubMed  CAS  Google Scholar 

  • Nemeth A, Langst G (2011) Genome organization in and around the nucleolus. Trends Genet 27:149–156

    Article  PubMed  CAS  Google Scholar 

  • Nemeth A, Guibert S, Tiwari VK, Ohlsson R, Langst G (2008) Epigenetic regulation of TTF-I-mediated promoter-terminator interactions of rRNA genes. EMBO J 27:1255–1265

    Article  PubMed  CAS  Google Scholar 

  • Nemeth A, Conesa A, Santoyo-Lopez J, Medina I, Montaner D, Peterfia B, Solovei I, Cremer T, Dopazo J, Langst G (2010) Initial genomics of the human nucleolus. PLoS Genet 6:e1000889

    Article  PubMed  CAS  Google Scholar 

  • O’Sullivan AC, Sullivan GJ, McStay B (2002) UBF binding in vivo is not restricted to regulatory sequences within the vertebrate ribosomal DNA repeat. Mol Cell Biol 22:657–668

    Article  PubMed  CAS  Google Scholar 

  • Panov KI, Friedrich JK, Zomerdijk JC (2001) A step subsequent to preinitiation complex assembly at the ribosomal RNA gene promoter is rate limiting for human RNA polymerase I-dependent transcription. Mol Cell Biol 21:2641–2649

    Article  PubMed  CAS  Google Scholar 

  • Panov KI, Friedrich JK, Russell J, Zomerdijk JC (2006a) UBF activates RNA polymerase I transcription by stimulating promoter escape. EMBO J 25:3310–3322

    Article  PubMed  CAS  Google Scholar 

  • Panov KI, Panova TB, Gadal O, Nishiyama K, Saito T, Russell J, Zomerdijk JC (2006b) RNA polymerase I-specific subunit CAST/hPAF49 has a role in the activation of transcription by upstream binding factor. Mol Cell Biol 26:5436–5448

    Article  PubMed  CAS  Google Scholar 

  • Panova TB, Panov KI, Russell J, Zomerdijk JC (2006) Casein kinase 2 associates with initiation-competent RNA polymerase I and has multiple roles in ribosomal DNA transcription. Mol Cell Biol 26:5957–5968

    Article  PubMed  CAS  Google Scholar 

  • Paredes S, Maggert KA (2009) Ribosomal DNA contributes to global chromatin regulation. Proc Natl Acad Sci USA 106:17829–17834

    Article  PubMed  CAS  Google Scholar 

  • Paule MR, White RJ (2000) Survey and summary: transcription by RNA polymerases I and III. Nucleic Acids Res 28:1283–1298

    Article  PubMed  CAS  Google Scholar 

  • Pelletier G, Stefanovsky VY, Faubladier M, Hirschler-Laszkiewicz I, Savard J, Rothblum LI, Cote J, Moss T (2000) Competitive recruitment of CBP and Rb-HDAC regulates UBF acetylation and ribosomal transcription. Mol Cell 6:1059–1066

    Article  PubMed  CAS  Google Scholar 

  • Percipalle P, Fomproix N, Cavellan E, Voit R, Reimer G, Kruger T, Thyberg J, Scheer U, Grummt I, Farrants AK (2006) The chromatin remodelling complex WSTF-SNF2h interacts with nuclear myosin 1 and has a role in RNA polymerase I transcription. EMBO Rep 7:525–530

    PubMed  CAS  Google Scholar 

  • Peyroche G, Milkereit P, Bischler N, Tschochner H, Schultz P, Sentenac A, Carles C, Riva M (2000) The recruitment of RNA polymerase I on rDNA is mediated by the interaction of the A43 subunit with Rrn3. EMBO J 19:5473–5482

    Article  PubMed  CAS  Google Scholar 

  • Pietrzak M, Rempala G, Nelson PT, Zheng JJ, Hetman M (2011) Epigenetic silencing of nucleolar rRNA genes in Alzheimer’s disease. PLoS One 6:e22585

    Article  PubMed  CAS  Google Scholar 

  • Pistoni M, Verrecchia A, Doni M, Guccione E, Amati B (2010) Chromatin association and regulation of rDNA transcription by the Ras-family protein RasL11a. EMBO J 29:1215–1224

    Article  PubMed  CAS  Google Scholar 

  • Pontes O, Li CF, Costa Nunes P, Haag J, Ream T, Vitins A, Jacobsen SE, Pikaard CS (2006) The Arabidopsis chromatin-modifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126:79–92

    Article  PubMed  CAS  Google Scholar 

  • Prescott EM, Osheim YN, Jones HS, Alen CM, Roan JG, Reeder RH, Beyer AL, Proudfoot NJ (2004) Transcriptional termination by RNA polymerase I requires the small subunit Rpa12p. Proc Natl Acad Sci USA 101:6068–6073

    Article  PubMed  CAS  Google Scholar 

  • Preuss SB, Costa-Nunes P, Tucker S, Pontes O, Lawrence RJ, Mosher R, Kasschau KD, Carrington JC, Baulcombe DC, Viegas W, Pikaard CS (2008) Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol Cell 32:673–684

    Article  PubMed  CAS  Google Scholar 

  • Reeder RH (1999) Regulation of RNA polymerase I transcription in yeast and vertebrates. Prog Nucleic Acid Res Mol Biol 62:293–327

    Article  PubMed  CAS  Google Scholar 

  • Rickards B, Flint SJ, Cole MD, LeRoy G (2007) Nucleolin is required for RNA polymerase I transcription in vivo. Mol Cell Biol 27:937–948

    Article  PubMed  CAS  Google Scholar 

  • Rose KM, Szopa J, Han FS, Cheng YC, Richter A, Scheer U (1988) Association of DNA topoisomerase I and RNA polymerase I: a possible role for topoisomerase I in ribosomal gene transcription. Chromosoma 96:411–416

    Article  PubMed  CAS  Google Scholar 

  • Rudloff U, Eberhard D, Tora L, Stunnenberg H, Grummt I (1994) TBP-associated factors interact with DNA and govern species specificity of RNA polymerase I transcription. EMBO J 13:2611–2616

    PubMed  CAS  Google Scholar 

  • Ruggero D, Pandolfi PP (2003) Does the ribosome translate cancer? Nat Rev Cancer 3:179–192

    Article  PubMed  CAS  Google Scholar 

  • Russell J, Zomerdijk JC (2005) RNA-polymerase-I-directed rDNA transcription, life and works. Trends Biochem Sci 30:87–96

    Article  PubMed  CAS  Google Scholar 

  • Sanij E, Hannan RD (2008) Chromatin organization and expression. Genome Biol 9:305

    Article  PubMed  Google Scholar 

  • Sanij E, Poortinga G, Sharkey K, Hung S, Holloway TP, Quin J, Robb E, Wong LH, Thomas WG, Stefanovsky V, Moss T, Rothblum L, Hannan KM, McArthur GA, Pearson RB, Hannan RD (2008) UBF levels determine the number of active ribosomal RNA genes in mammals. J Cell Biol 183:1259–1274

    Article  PubMed  CAS  Google Scholar 

  • Santoro R, Grummt I (2001) Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. Mol Cell 8:719–725

    Article  PubMed  CAS  Google Scholar 

  • Santoro R, Grummt I (2005) Epigenetic mechanism of rRNA gene silencing: temporal order of NoRC-mediated histone modification, chromatin remodeling, and DNA methylation. Mol Cell Biol 25:2539–2546

    Article  PubMed  CAS  Google Scholar 

  • Santoro R, Li J, Grummt I (2002) The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nat Genet 32:393–396

    Article  PubMed  CAS  Google Scholar 

  • Santoro R, Schmitz KM, Sandoval J, Grummt I (2010) Intergenic transcripts originating from a subclass of ribosomal DNA repeats silence ribosomal RNA genes in trans. EMBO Rep 11:52–58

    Article  PubMed  CAS  Google Scholar 

  • Saunders A, Core LJ, Lis JT (2006) Breaking barriers to transcription elongation. Nat Rev Mol Cell Biol 7:557–567

    Article  PubMed  CAS  Google Scholar 

  • Schlesinger S, Selig S, Bergman Y, Cedar H (2009) Allelic inactivation of rDNA loci. Genes Dev 23:2437–2447

    Article  PubMed  CAS  Google Scholar 

  • Schmitz KM, Schmitt N, Hoffmann-Rohrer U, Schafer A, Grummt I, Mayer C (2009) TAF12 recruits Gadd45a and the nucleotide excision repair complex to the promoter of rRNA genes leading to active DNA demethylation. Mol Cell 33:344–353

    Article  PubMed  CAS  Google Scholar 

  • Schmitz KM, Mayer C, Postepska A, Grummt I (2010) Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev 24:2264–2269

    Article  PubMed  CAS  Google Scholar 

  • Schnapp G, Santori F, Carles C, Riva M, Grummt I (1994) The HMG box-containing nucleolar transcription factor UBF interacts with a specific subunit of RNA polymerase I. EMBO J 13:190–199

    PubMed  CAS  Google Scholar 

  • Schneider DA, French SL, Osheim YN, Bailey AO, Vu L, Dodd J, Yates JR, Beyer AL, Nomura M (2006) RNA polymerase II elongation factors Spt4p and Spt5p play roles in transcription elongation by RNA polymerase I and rRNA processing. Proc Natl Acad Sci USA 103:12707–12712

    Article  PubMed  CAS  Google Scholar 

  • Schneider DA, Michel A, Sikes ML, Vu L, Dodd JA, Salgia S, Osheim YN, Beyer AL, Nomura M (2007) Transcription elongation by RNA polymerase I is linked to efficient rRNA processing and ribosome assembly. Mol Cell 26:217–229

    Article  PubMed  CAS  Google Scholar 

  • Schultz MC, Brill SJ, Ju Q, Sternglanz R, Reeder RH (1992) Topoisomerases and yeast rRNA transcription: negative supercoiling stimulates initiation and topoisomerase activity is required for elongation. Genes Dev 6:1332–1341

    Article  PubMed  CAS  Google Scholar 

  • Seither P, Zatsepina O, Hoffmann M, Grummt I (1997) Constitutive and strong association of PAF53 with RNA polymerase I. Chromosoma 106:216–225

    Article  PubMed  CAS  Google Scholar 

  • Shiratori M, Suzuki T, Itoh C, Goto M, Furuichi Y, Matsumoto T (2002) WRN helicase accelerates the transcription of ribosomal RNA as a component of an RNA polymerase I-associated complex. Oncogene 21:2447–2454

    Article  PubMed  CAS  Google Scholar 

  • Shiue CN, Berkson RG, Wright AP (2009) c-Myc induces changes in higher order rDNA structure on stimulation of quiescent cells. Oncogene 28:1833–1842

    Article  PubMed  CAS  Google Scholar 

  • Siehl D, Chua BH, Lautensack-Belser N, Morgan HE (1985) Faster protein and ribosome synthesis in thyroxine-induced hypertrophy of rat heart. Am J Physiol 248:C309–319

    PubMed  CAS  Google Scholar 

  • Stefanovsky VY, Pelletier G, Hannan R, Gagnon-Kugler T, Rothblum LI, Moss T (2001) An immediate response of ribosomal transcription to growth factor stimulation in mammals is mediated by ERK phosphorylation of UBF. Mol Cell 8:1063–1073

    Article  PubMed  CAS  Google Scholar 

  • Stefanovsky V, Langlois F, Gagnon-Kugler T, Rothblum LI, Moss T (2006) Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling. Mol Cell 21:629–639

    Article  PubMed  CAS  Google Scholar 

  • Tanaka Y, Okamoto K, Teye K, Umata T, Yamagiwa N, Suto Y, Zhang Y, Tsuneoka M (2010) JmjC enzyme KDM2A is a regulator of rRNA transcription in response to starvation. EMBO J 29:1510–1522

    Article  PubMed  CAS  Google Scholar 

  • Tschochner H, Hurt E (2003) Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol 13:255–263

    Article  PubMed  CAS  Google Scholar 

  • Tseng H, Chou W, Wang J, Zhang X, Zhang S, Schultz RM (2008) Mouse ribosomal RNA genes contain multiple differentially regulated variants. PLoS One 3:e1843

    Article  PubMed  CAS  Google Scholar 

  • Tuan JC, Zhai W, Comai L (1999) Recruitment of TATA-binding protein-TAFI complex SL1 to the human ribosomal DNA promoter is mediated by the carboxy-terminal activation domain of upstream binding factor (UBF) and is regulated by UBF phosphorylation. Mol Cell Biol 19:2872–2879

    PubMed  CAS  Google Scholar 

  • Tucker S, Vitins A, Pikaard CS (2010) Nucleolar dominance and ribosomal RNA gene silencing. Curr Opin Cell Biol 22:351–356

    Article  PubMed  CAS  Google Scholar 

  • Valdez BC, Henning D, So RB, Dixon J, Dixon MJ (2004) The Treacher Collins syndrome (TCOF1) gene product is involved in ribosomal DNA gene transcription by interacting with upstream binding factor. Proc Natl Acad Sci USA 101:10709–10714

    Article  PubMed  CAS  Google Scholar 

  • van de Nobelen S, Rosa-Garrido M, Leers J, Heath H, Soochit W, Joosen L, Jonkers I, Demmers J, van der Reijden M, Torrano V, Grosveld F, Delgado MD, Renkawitz R, Galjart N, Sleutels F (2010) CTCF regulates the local epigenetic state of ribosomal DNA repeats. Epigenetics Chromatin 3:19

    Article  PubMed  CAS  Google Scholar 

  • van Koningsbruggen S, Gierlinski M, Schofield P, Martin D, Barton GJ, Ariyurek Y, den Dunnen JT, Lamond AI (2010) High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol Biol Cell 21:3735–3748

    Article  PubMed  CAS  Google Scholar 

  • Vincent T, Kukalev A, Andang M, Pettersson R, Percipalle P (2008) The glycogen synthase kinase (GSK) 3beta represses RNA polymerase I transcription. Oncogene 27:5254–5259

    Article  PubMed  CAS  Google Scholar 

  • Voit R, Grummt I (2001) Phosphorylation of UBF at serine 388 is required for interaction with RNA polymerase I and activation of rDNA transcription. Proc Natl Acad Sci USA 98:13631–13636

    Article  PubMed  CAS  Google Scholar 

  • Voit R, Schnapp A, Kuhn A, Rosenbauer H, Hirschmann P, Stunnenberg HG, Grummt I (1992) The nucleolar transcription factor mUBF is phosphorylated by casein kinase II in the C-terminal hyperacidic tail which is essential for transactivation. EMBO J 11:2211–2218

    PubMed  CAS  Google Scholar 

  • Voit R, Schafer K, Grummt I (1997) Mechanism of repression of RNA polymerase I transcription by the retinoblastoma protein. Mol Cell Biol 17:4230–4237

    PubMed  CAS  Google Scholar 

  • Voit R, Hoffmann M, Grummt I (1999) Phosphorylation by G1-specific cdk-cyclin complexes activates the nucleolar transcription factor UBF. EMBO J 18:1891–1899

    Article  PubMed  CAS  Google Scholar 

  • Werner M, Thuriaux P, Soutourina J (2009) Structure-function analysis of RNA polymerases I and III. Curr Opin Struct Biol 19:740–745

    Article  PubMed  CAS  Google Scholar 

  • White RJ (2008) RNA polymerases I and III, non-coding RNAs and cancer. Trends Genet 24:622–629

    Article  PubMed  CAS  Google Scholar 

  • Whitehead CM, Winkfein RJ, Fritzler MJ, Rattner JB (1997) ASE-1: a novel protein of the fibrillar centres of the nucleolus and nucleolus organizer region of mitotic chromosomes. Chromosoma 106:493–502

    Article  PubMed  CAS  Google Scholar 

  • Wittner M, Hamperl S, Stockl U, Seufert W, Tschochner H, Milkereit P, Griesenbeck J (2011) Establishment and maintenance of alternative chromatin states at a multicopy gene locus. Cell 145:543–554

    Article  PubMed  CAS  Google Scholar 

  • Yamamoto K, Yamamoto M, Hanada K, Nogi Y, Matsuyama T, Muramatsu M (2004) Multiple protein-protein interactions by RNA polymerase I-associated factor PAF49 and role of PAF49 in rRNA transcription. Mol Cell Biol 24:6338–6349

    Article  PubMed  CAS  Google Scholar 

  • Ye J, Zhao J, Hoffmann-Rohrer U, Grummt I (2008) Nuclear myosin I acts in concert with polymeric actin to drive RNA polymerase I transcription. Genes Dev 22:322–330

    Article  PubMed  CAS  Google Scholar 

  • Yuan X, Feng W, Imhof A, Grummt I, Zhou Y (2007) Activation of RNA polymerase I transcription by cockayne syndrome group B protein and histone methyltransferase G9a. Mol Cell 27:585–595

    Article  PubMed  CAS  Google Scholar 

  • Zentner GE, Hurd EA, Schnetz MP, Handoko L, Wang C, Wang Z, Wei C, Tesar PJ, Hatzoglou M, Martin DM, Scacheri PC (2010) CHD7 functions in the nucleolus as a positive regulator of ribosomal RNA biogenesis. Hum Mol Genet 19:3491–3501

    Article  PubMed  CAS  Google Scholar 

  • Zetterberg A, Killander D (1965) Quantitative cytophotometric and autoradiographic studies on the rate of protein synthesis during interphase in mouse fibroblasts in vitro. Exp Cell Res 40:1–11

    Article  PubMed  CAS  Google Scholar 

  • Zhai W, Comai L (2000) Repression of RNA polymerase I transcription by the tumor suppressor p53. Mol Cell Biol 20:5930–5938

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Wang JC, Liu LF (1988) Involvement of DNA topoisomerase I in transcription of human ribosomal RNA genes. Proc Natl Acad Sci USA 85:1060–1064

    Article  PubMed  CAS  Google Scholar 

  • Zhang C, Comai L, Johnson DL (2005) PTEN represses RNA Polymerase I transcription by disrupting the SL1 complex. Mol Cell Biol 25:6899–6911

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Sikes ML, Beyer AL, Schneider DA (2009) The Paf1 complex is required for efficient transcription elongation by RNA polymerase I. Proc Natl Acad Sci USA 106:2153–2158

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Smith AD, Renfrow MB, Schneider DA (2010) The RNA polymerase-associated factor 1 complex (Paf1C) directly increases the elongation rate of RNA polymerase I and is required for efficient regulation of rRNA synthesis. J Biol Chem 285:14152–14159

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Yuan X, Frodin M, Grummt I (2003) ERK-dependent phosphorylation of the transcription initiation factor TIF-IA is required for RNA polymerase I transcription and cell growth. Mol Cell 11:405–413

    Article  PubMed  CAS  Google Scholar 

  • Zhou Y, Santoro R, Grummt I (2002) The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription. EMBO J 21:4632–4640

    Article  PubMed  CAS  Google Scholar 

  • Zomerdijk JC, Beckmann H, Comai L, Tjian R (1994) Assembly of transcriptionally active RNA polymerase I initiation factor SL1 from recombinant subunits. Science 266:2015–2018

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Dr Jackie Russell for critical reading and helpful comments. We thank the Wellcome Trust for supporting our research through a Wellcome Trust Programme Grant (085441/Z/08/Z) awarded to JCBMZ.

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Goodfellow, S.J., Zomerdijk, J.C.B.M. (2013). Basic Mechanisms in RNA Polymerase I Transcription of the Ribosomal RNA Genes. In: Kundu, T. (eds) Epigenetics: Development and Disease. Subcellular Biochemistry, vol 61. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4525-4_10

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