Skip to main content

Advertisement

SpringerLink
Log in

Chromatin: linking structure and function in the nucleolus

  • Review
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

The nucleolus is an informative model structure for studying how chromatin-regulated transcription relates to nuclear organisation. In this review, we describe how chromatin controls nucleolar structure through both the modulation of rDNA activity by convergently-evolved remodelling complexes and by direct effects upon rDNA packaging. This packaging not only regulates transcription but may also be important for suppressing internal recombination between tandem rDNA repeats. The identification of nucleolar histone chaperones and novel chromatin proteins by mass spectrometry suggests that structure-specific chromatin components remain to be characterised and may regulate the nucleolus in novel ways. However, it also suggests that there is considerable overlap between nucleolar and non-nucleolar-chromatin components. We conclude that a fuller understanding of nucleolar chromatin will be essential for understanding how gene organisation is linked with nuclear architecture.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

DNMT:

DNA methyltransferase

HAT:

histone acetyltransferase

HDAC:

histone deacetylase

HMT:

histone methyltransferase

MS:

mass spectrometry

NOR:

nucleolar organiser region

rDNA:

ribosomal DNA

rRNA:

ribosomal RNA

UBF:

upstream binding factor.

References

  • Allis CD, Ziegler YS, Gorovsky MA, Olmsted JB (1982) A conserved histone variant enriched in nucleoli of mammalian cells. Cell 31:131–136

    PubMed  CAS  Google Scholar 

  • Alvarez M, Quezada C, Molina A, Krauskopf M, Vera MI, Thiry M (2006) Ultrastructural changes of the carp (Cyprinus carpio) hepatocyte nucleolus during seasonal acclimatization. Biol Cell 98:457–463

    Article  PubMed  CAS  Google Scholar 

  • Andersen JS, Lyon CE, Fox AH, Leung AKL, Lam YW, Steen H, Mann M, Lamond AI (2002) Directed proteomic analysis of the human nucleolus. Curr Biol 12:1–11

    PubMed  Google Scholar 

  • Angelov D, Bondarenko VA, Almagro S, Menoni H, Mongelard F, Hans F, Mietton F, Studitsky VM, Hamiche A, Dimitrov S, Bouvet P (2006) Nucleolin is a histone chaperone with FACT-like activity and assists remodelling of nucleosomes. EMBO J 25:1669–1679

    PubMed  CAS  Google Scholar 

  • Aufsatz W, Mette MF, van der Winden J, Matzke M, Matzke AJM (2002) HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J 21:6832–6841

    PubMed  CAS  Google Scholar 

  • Avramova ZV (2002) Update on heterochromatin. Plant Physiol 129:40–49

    PubMed  CAS  Google Scholar 

  • Benecke A (2006) Chromatin code, local non-equilibrium dynamics, and the emergence of transcription regulatory programs. Eur Phys J E 19:353–366

    PubMed  CAS  Google Scholar 

  • Bird A, Taggart M, Macleod D (1981) Loss of rDNA methylation accompanies the onset of ribosomal gene activity in early development of X. laevis. Cell 26:381–390

    PubMed  CAS  Google Scholar 

  • Boggs BA, Connors B, Sobel RE, Chinault AC, Allis CD (1996) Reduced levels of histone H3 acetylation on the inactive X chromosome in human females. Chromosoma 105:303–309

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Caperta AD, Neves N, Morais-Cecilio L, Malho R, Viegas W (2002) Genome restructuring in rye affects the expression, organization and disposition of homologous rDNA loci. J Cell Sci 115:2839–2846

    PubMed  CAS  Google Scholar 

  • Carmo-Fonseca M, Mendes-Soares L, Campos I (2000) To be or not to be in the nucleolus. Nature Cell Biol 2:E107–E112

    PubMed  CAS  Google Scholar 

  • Cervantes MD, Xi XH, Vermaak D, Yao MC, Malik HS (2006) The CNA1 histone of the ciliate Tetrahymena thermophila is essential for chromosome segregation in the germline micronucleus. Mol Biol Cell 17:485–497

    PubMed  CAS  Google Scholar 

  • Chen ZJ, Pikaard CS (1997) Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. Genes Dev 11:2124–2136

    PubMed  CAS  Google Scholar 

  • Chen ZJ, Comai L, Pikaard CS (1998) Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids. Proc Natl Acad Sci USA 95:14891–14896

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Clarke AS, Samal E, Pillus L (2006) Distinct roles for the essential MYST family HAT Esa1p in transcriptional silencing. Mol Biol Cell 17:1744–1757

    PubMed  CAS  Google Scholar 

  • Conconi A, Widmer RM, Koller T, Sogo JM (1989) Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell 57:753–761

    PubMed  CAS  Google Scholar 

  • Costanzi C, Stein P, Worrad DM, Schultz RM, Pehrson JR (2000) Histone macroH2A1 is concentrated in the inactive X chromosome of female preimplantation mouse embryos. Development 127:2283–2289

    PubMed  CAS  Google Scholar 

  • Csink AK, Henikoff S (1996) Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381:529–531

    PubMed  CAS  Google Scholar 

  • de la Torre C, Giminez-Abian JF, Gonzalez-Fernandez A (1991) Dominance of a NOR (nucleolar organizer region) over its allele and over its sister NOR after asymmetric 5-azacytidine substitution in plant chromosomes. J Cell Sci 100:667–674

    Google Scholar 

  • Earley K, Lawrence RJ, Pontes O, Reuther R, Encisco AJ, Silva M, Neves N, Gross M, Viegas W, Pikaard CS (2006) Erasure of histone acetylation by Arabidopsis HDA6 mediates large-scale gene silencing in nucleolar dominance. Genes Dev 20:1283–1293

    PubMed  CAS  Google Scholar 

  • Eden S, Hashimshony T, Keshet I, Cedar H, Thorne AW (1998) DNA methylation models histone acetylation. Nature 394:842

    PubMed  CAS  Google Scholar 

  • Erard MS, Belenguer P, Caizerguesferrer M, Pantaloni A, Amalric F (1988) A major nucleolar protein, nucleolin, induces chromatin decondensation by binding to histone H1. Eur J Biochem 175:525–530

    PubMed  CAS  Google Scholar 

  • Espada J, Esteller M (2007) Epigenetic control of nuclear architecture. Cell Mol Life Sci 64:449–457

    PubMed  CAS  Google Scholar 

  • Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A (2004a) H2AX: the histone guardian of the genome. DNA Repair 3:959–967

    PubMed  CAS  Google Scholar 

  • Fernandez-Capetillo O, Allis CD, Nussenzweig A (2004b) Phosphorylation of histone H2B at DNA double-strand breaks. J Exp Med 199:1671–1677

    PubMed  CAS  Google Scholar 

  • Flavell RB, O’Dell M, Thompson WF (1988) Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat. J Mol Biol 204:523–534

    PubMed  CAS  Google Scholar 

  • Ford E, Voit R, Liszt G, Magin C, Grummt I, Guarente L (2006) Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription. Genes Dev 20:1075–1080

    PubMed  CAS  Google Scholar 

  • Frehlick LJ, Eirin-Lopez JM, Ausio J (2007) New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. Bioessays 29:49–59

    PubMed  CAS  Google Scholar 

  • Fritze CE, Verschueren K, Strich R, Esposito RE (1997) Direct evidence for SIR2 modulation of chromatin structure in yeast rDNA. EMBO J 16:6495–6509

    PubMed  CAS  Google Scholar 

  • Fuchs J, Demidov D, Houben A, Schubert I (2006) Chromosomal histone modification patterns—from conservation to diversity. Trends Plant Sci 11:199–208

    PubMed  CAS  Google Scholar 

  • Galy V, Olivo-Marin JC, Scherthan H, Dove V, Rasalou N, Nehrbass U (2000) Nuclear pore complexes in the organisation of silent telomeric chromatin. Nature 403:108–112

    PubMed  CAS  Google Scholar 

  • Gonda K, Fowler J, Katoku-Kikyo N, Haroldsen J, Wudel J, Kikyo N (2003) Reversible disassembly of somatic nucleoli by the germ cell proteins FRGY2a and FRGY2b. Nature Cell Biol 5:205–210

    PubMed  CAS  Google Scholar 

  • Gonda K, Wudel J, Nelson D, Katoku-Kikyo N, Reed P, Tamada H, Kikyo N (2006) Requirement of the protein B23 for nucleolar disassembly induced by the FRGY2a family proteins. J Biol Chem 281:8153–8160

    PubMed  CAS  Google Scholar 

  • Gonzalez-Melendi P, Beven A, Boudonck K, Abranches R, Wells B, Dolan L, Shaw P (2000) The nucleus: a highly organized but dynamic structure. J Microsc 198:199–207

    PubMed  CAS  Google Scholar 

  • Gotta M, Strahl-Bolsinger S, Renauld H, Laroche T, Kennedy BK, Grunstein M, Gasser SM (1997) Localization of Sir2p: the nucleolus as a compartment for silent information regulators. EMBO J 16:3243–3255

    PubMed  CAS  Google Scholar 

  • Gottlieb S, Esposito RE (1989) A new role for a yeast transcriptional silencer gene, Sir2, in regulation of recombination in ribosomal DNA. Cell 56:771–776

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Grummt I (2007) Different epigenetic layers engage in complex crosstalk to define the epigenetic state of mammalian rRNA genes. Hum Mol Gen 16:R21–R27

    PubMed  CAS  Google Scholar 

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

    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. Nucl Acids Res 32:1654–1665

    PubMed  CAS  Google Scholar 

  • Hallows WC, Lee S, Denu JM (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci USA 103:10230–10235

    PubMed  CAS  Google Scholar 

  • Hancock R (2004) Internal organisation of the nucleus: assembly of compartments by macromolecular crowding and the nuclear matrix model. Biol Cell 96:595–601

    PubMed  CAS  Google Scholar 

  • Hasterok R, Maluszynska J (2000) Different rRNA gene expression in primary and adventitious roots of Allium cepa. Folia Hist Cytobiol 38:181–184

    CAS  Google Scholar 

  • Heliot L, Kaplan H, Lucas L, Klein C, Beorchia A, Doco-Fenzy M, Menager M, Thiry M, O’Donohue M-F, Ploton D (1997) Electron tomography of metaphase nucleolar organizer regions: evidence for a twisted-loop organization. Mol Biol Cell 8:2199–2216

    PubMed  CAS  Google Scholar 

  • Henikoff S, Ahmad K (2005) Assembly of variant histones into chromatin. Ann Rev Cell Dev Biol 21:133–153

    CAS  Google Scholar 

  • Hernandez-Verdun D (2005) Tracking the interactions of rRNA processing proteins during nucleolar assembly in living cells. Medec Sci 21:1025–1027

    Google Scholar 

  • Hernandez-Verdun D, Roussel P, Gebrane-Younes J (2002) Emerging concepts of nucleolar assembly. J Cell Sci 115:2265–2270

    PubMed  CAS  Google Scholar 

  • Highett MI, Rawlins DJ, Shaw PJ (1993) Different patterns of rDNA distribution in Pisum sativum nucleoli correlate with different levels of nucleolar activity. J Cell Sc 104:843–852

    CAS  Google Scholar 

  • Hiscox JA (2007) RNA viruses: hijacking the dynamic nucleolus. Nature Rev Microbiol 5:119–127

    CAS  Google Scholar 

  • Houben A, Belyaev ND, Turner BM, Schubert I (1996) Differential immunostaining of plant chromosomes by antibodies recognizing acetylated histone H4 variants. Chromosome Res 4:191–194

    PubMed  CAS  Google Scholar 

  • Huang J, Moazed D (2003) Association of the RENT complex with nontranscribed and coding regions of rDNA and a regional requirement for the replication fork block protein Fob1 in rDNA silencing. Genes Dev 17:2162–2176

    PubMed  CAS  Google Scholar 

  • Huang S, Rothblum LI, Chen DY (2006) Ribosomal chromatin organization. Biochem Cell Biol 84:444–449

    PubMed  CAS  Google Scholar 

  • Huang LM, Sun QW, Qin FJ, Li C, Zhao Y, Zhou DX (2007) Down-regulation of a SILENT INFORMATION REGULATOR2-related histone deacetylase gene, OsSRT1, induces DNA fragmentation and cell death in rice. Plant Physiol 144:1508–1519

    PubMed  CAS  Google Scholar 

  • Idei S, Kondo K, Turner BM, Fukui K (1996) Tomographic distribution of acetylated histone H4 in plant chromosomes, nuclei and nucleoli. Chromosoma 105:293–302

    PubMed  CAS  Google Scholar 

  • Imai S-I, Armstrong CM, Keaberlein M, Guarente L (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403:795–800

    PubMed  CAS  Google Scholar 

  • Jasencakova Z, Meister A, Walter J, Turner BM, Schubert I (2000) Histone H4 acetylation of euchromatin and heterochromatin is cell cycle dependent and correlated with replication rather than with transcription. Plant Cell 12:2087–2100

    PubMed  CAS  Google Scholar 

  • Jones PL, Veenstra GJC, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP (1998) Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nature Gen 19:187–191

    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. Nature Struct Mol Biol 14:123–130

    CAS  Google Scholar 

  • Kalmarova M, Smirnov E, Masata M, Koberna K, Ligasova A, Popov A, Raska I (2007) Positioning of NORs and NOR-bearing chromosomes in relation to nucleoli. J Struct Biol 160:49–56

    PubMed  CAS  Google Scholar 

  • Keener J, Dodd JA, Lalo D, Nomura M (1997) Histones H3 and H4 are components of upstream activation factor required for the high-level transcription of yeast rDNA by RNA polymerase I. Proc Natl Acad Sci USA 94:13458–13462

    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 

  • Kimura A, Matsubara K, Horikoshi M (2005) A decade of histone acetylation: marking eukaryotic chromosomes with specific codes. J Biochem 138:647–662

    PubMed  CAS  Google Scholar 

  • Kobayashi T, Horiuchi T, Tongaonkat P, Vu L, Nomura M (2004) SIR2 regulates recombination between different rDNA repeats, but not recombination within individual rRNA genes. Cell 117:441–453

    PubMed  CAS  Google Scholar 

  • Kohlmaier A, Savarese F, Lachner M, Martens J, Jenuwein T, Wutz A (2004) A chromosomal memory triggered by Xist regulates histone methylation in X inactivation. PLoS Biol 2:991–1003

    CAS  Google Scholar 

  • Kopp K, Gasiorowski JZ, Chen D, Gilmore R, Norton JT, Wang C, Leary DJ, Chan EKL, Dean DA, Huang S (2007) Pol I transcription and pre-rRNA processing are coordinated in a transcription-dependent manner in mammalian cells. Mol Biol Cell 18:394–403

    PubMed  CAS  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705

    PubMed  CAS  Google Scholar 

  • Kovarik A, Koukalova B, Lim KY, Matyasek R, Lichtenstein CP, Leitch AR, Bezdek M (2000) Comparative analysis of DNA methylation in tobacco heterochromatic sequences. Chrom Res 8:527–541

    PubMed  CAS  Google Scholar 

  • Kurakin A (2005) Self-organization versus Watchmaker: stochastic dynamics of cellular organization. Biol Chem 386:247–254

    PubMed  CAS  Google Scholar 

  • Kuzuhara T, Horikoshi M (2004) A nuclear FK506-binding protein is a histone chaperone regulating rDNA silencing. Nature Struct Mol Biol 11:275–283

    CAS  Google Scholar 

  • La Volpe A, Taggart M, McStay B, Bird A (1983) DNaseI-hypersensitive sites at promoter-like sequences in the space of Xenopus laevis and Xenopus borealis ribosomal DNA. Nucl Acids Res 11:5361–5380

    PubMed  Google Scholar 

  • Lam YW, Lamond AI, Mann M, Andersen JS (2007) Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr Biol 17:749–760

    PubMed  CAS  Google Scholar 

  • Lamond AI, Sleeman JE (2003) Nuclear substructure and dynamics. Curr Biol 13:R825–R828

    PubMed  CAS  Google Scholar 

  • Lawrence RJ, Pikaard CS (2004) Chromatin turn ons and turn offs of ribosomal RNA genes. Cell Cycle 3:880–883

    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 113:599–609

    Google Scholar 

  • Lewis MS, Cheverud JM, Pikaard CS (2004) Evidence for nucleolus organizer regions as the units of regulation in nucleolar dominance in Arabidopsis thaliana interecotype hybrids. Genetics 167:931–939

    PubMed  CAS  Google Scholar 

  • Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV, Chan SWL, Lagrange T, Pikaard CS, Jacobsen SE (2006a) An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126:93–106

    PubMed  CAS  Google Scholar 

  • Li CH, Mueller JE, Bryk M (2006b) Sir2 represses endogenous polymerase II transcription units in the ribosomal DNA nontranscribed spacer. Mol Biol Cell 17:3848–3859

    PubMed  CAS  Google Scholar 

  • Li JW, Santoro R, Koberna K, Grummt I (2005) The chromatin remodelling complex NoRC controls replication timing of rRNA genes. EMBO J 24:120–127

    PubMed  Google Scholar 

  • Lim KY, Kovarik A, Matyasek R, Bezdek M, Lichtenstein CP, Leitch AR (2000) Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units. Chromosoma 109:161–172

    PubMed  CAS  Google Scholar 

  • Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619

    PubMed  CAS  Google Scholar 

  • Lyon CE, Lamond AI (2000) The nucleolus. Curr Biol 10:R323–R323

    PubMed  CAS  Google Scholar 

  • Maggi LB, Weber JD (2005) Nucleolar adaptation in human cancer. Cancer Invest 23:599–608

    PubMed  CAS  Google Scholar 

  • Mais C, Scheer U (2001) Molecular architecture of the amplified nucleoli of Xenopus oocytes. J Cell Sci 114:709–718

    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

    PubMed  CAS  Google Scholar 

  • Majumder S, Ghoshal K, Datta J, Smith DS, Bai SM, Jacob ST (2006) Role of DNA methyltransferases in regulation of human ribosomal RNA gene transcription. J Biol Chem 281:22062–22072

    PubMed  CAS  Google Scholar 

  • Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nature Struct Biol 10:882–891

    PubMed  CAS  Google Scholar 

  • Marian CO, Bordoli SJ, Goltz M, Santarella RA, Jackson LP, Danilevskaya O, Beckstette M, Meeley R, Bass HW (2003) The maize Single myb histone 1 gene, Smh1, belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro. Plant Physiol 133:1336–1350

    PubMed  CAS  Google Scholar 

  • Martin C, Zhang Y (2005) The diverse functions of histone lysine methylation. Nature Rev Mol Cell Biol 6:838–849

    CAS  Google Scholar 

  • May BP, Lippman ZB, Fang YD, Spector DL, Martienssen RA (2005) Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Gen 1:705–714

    CAS  Google Scholar 

  • McClintock B (1934) The relation of a particular chromosomal element to the development of the nucleoli in Zea mays. Z Zellforsch Mikrol Anat 21:294–328

    Google Scholar 

  • McStay B (2006) Nucleolar dominance: a model for rRNA gene silencing. Genes Dev 20:1207–1214

    PubMed  CAS  Google Scholar 

  • Meijsing SH, Ehrenhofer-Murray AE (2001) The silencing complex SAS-I links histone acetylation to the assembly of repressed chromatin by CAF-I and Asf1 in S. cerevisiae. Genes Dev 15:3169–3182

    PubMed  CAS  Google Scholar 

  • Melese T, Xue Z (1995) The nucleolus—an organelle formed by the act of building a ribosome. Curr Op Cell Biol 7:319–324

    PubMed  CAS  Google Scholar 

  • Meraner J, Lechner M, Loidl A, Goralik-Schramel M, Voit R, Grummt I, Loidl P (2006) Acetylation of UBF changes during the cell cycle and regulates the interaction of UBF with RNA polymerase I. Nucl Acids Res 34:1798–1806

    PubMed  CAS  Google Scholar 

  • Mermoud JE, Popova B, Peters AHFM, Jenuwein T, Brockdorff N (2002) Histone H3 lysine 9 methylation occurs rapidly at the onset of random X chromosome inactivation. Curr Biol 12:247–251

    PubMed  CAS  Google Scholar 

  • Misteli T (2001) The concept of self-organization in cellular architecture. J Cell Biol 155:181–185

    PubMed  CAS  Google Scholar 

  • Mongelard F, Bouvet P (2007) Nucleolin: a multiFACeTed protein. Trends Cell Biol 17:80–86

    PubMed  CAS  Google Scholar 

  • Morais-Cecilio L, Delgado M, Jones RN, Viegas W (2000) Modification of wheat rDNA loci by rye B chromosomes: a chromatin organization model. Chrom Res 8:341–351

    PubMed  CAS  Google Scholar 

  • Moss T, Langlois F, Gagnon-Kugler T, Stefanovsky V (2007) A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell Mol Life Sci 64:29–49

    PubMed  CAS  Google Scholar 

  • Murayama A, Ohmori K, Fujimara 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 or rDNA loci in response to intracellular energy status. Cell 133:627–639

    PubMed  CAS  Google Scholar 

  • Namboodiri VMH, Akey IV, Schmidt-Zachmann MS, Head JF, Akey CW (2004) The structure and function of Xenopus NO38-core, a histone chaperone in the nucleolus. Structure 12:2149–2160

    PubMed  CAS  Google Scholar 

  • Ng HH, Ciccone DN, Morshead KB, Oettinger MA, Struhl K (2003) Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: a potential mechanism for position-effect variegation. Proc Natl Acad Sci USA 100:1820–1825

    PubMed  CAS  Google Scholar 

  • Nierras CR, Liebman SW, Warner JR (1997) Does S. cerevisiae need an organized nucleolus? Chromosoma 105:444–451

    PubMed  CAS  Google Scholar 

  • North BJ, Marshall BL, Borra MT, Denu JM, Verdin E (2003) The human Sir2 ortholog, SIRT2, is an NAD(+)-dependent tubulin deacetylase. Mol Cell 11:437–444

    PubMed  CAS  Google Scholar 

  • Oakes ML, Siddiqi I, Vu L, Aris J, Nomura M (1999) Transcription factor UAF, expansion and contraction of ribosomal DNA (rDNA) repeats, and RNA polymerase switch in transcription of yeast rDNA. Mol Cell Biol 19:8559–8569

    PubMed  CAS  Google Scholar 

  • Oakes ML, Siddiqi I, French SL, Vu L, Sato M, Aris JP, Beyer AL, Nomura M (2006) Role of histone deacetylase Rpd3 in regulating rRNA gene transcription and nucleolar structure in yeast. Mol Cell Biol 26:3889–3901

    PubMed  CAS  Google Scholar 

  • Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K (2001) Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett 506:272–276

    PubMed  CAS  Google Scholar 

  • Omer AD, Lowe TM, Russell AG, Ebhardt H, Eddy SR, Dennis PP (2000) Homologs of small nucleolar RNAs in archaea. Science 288:517–522

    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

    PubMed  CAS  Google Scholar 

  • Ouzounis CA, Kyrpides NC (1996) Parallel origins of the nucleosome core and eukaryotic transcription from archeae. J Mol Evol 42:234–239

    PubMed  CAS  Google Scholar 

  • Palaniswamy V, Moraes KCM, Wilusz CJ, Wilusz J (2006) Nucleophosmin is selectively deposited on mRNA during polyadenylation. Nature Struct Mol Biol 13:429–435

    CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Parsons XH, Garcia SN, Pillus L, Kadonaga JT (2003) Histone deacetylation by Sir2 generates a transcriptionally repressed nucleoprotein complex. Proc Natl Acad Sci USA 100:1609–1614

    PubMed  CAS  Google Scholar 

  • Payne C, Braun RE (2006) Histone lysine trimethylation exhibits a distinct perinuclear distribution in Plzf-expressing spermatogonia. Dev Biol 293:461–472

    PubMed  CAS  Google Scholar 

  • Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, Andersen J, Mann M, Lamond AI, Brown JW, Shaw PJ (2005) Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol Biol Cell 16:260–269

    PubMed  CAS  Google Scholar 

  • Peng JC, Karpen GH (2007) H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nature Cell Biol 9:25–35

    PubMed  CAS  Google Scholar 

  • Pennock DG, Reeder RH (1984) In vitro methylation of HpaII sites in Xenopus laevis rDNA does not affect its transcription in oocytes. Nucl Acids Res 12:2225–2232

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pikaard CS (1999) Nucleolar dominance and silencing of transcription. Trends Plant Sci 4:478–483

    PubMed  Google Scholar 

  • Pluta AF, Mackay AM, Ainsztein AM, Goldberg IG, Earnshaw WC (1995) Centromere—hub of chromosomal activities. Science 270:1591–1594

    PubMed  CAS  Google Scholar 

  • Politz JCR, Zhang F, Pederson T (2006) MicroRNA-206 colocalizes with ribosome-rich regions in both the nucleolus and cytoplasm of rat myogenic cells. Proc Natl Acad Sci USA 103:18957–18962

    PubMed  CAS  Google Scholar 

  • Pontes O, Lawrence RJ, Neves N, Silva M, Lee JH, Chen ZJ, Viegas W, Pikaard CS (2003) Natural variation in nucleolar dominance reveals the relationship between nucleolus organizer chromatin topology and rRNA gene transcription in Arabidopsis. Proc Natl Acad Sci USA 100:11418–11423

    PubMed  CAS  Google Scholar 

  • Pontes O, Li CF, Nunes PC, 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

    PubMed  CAS  Google Scholar 

  • Pontvianne F, Matia I, Douet J, Tourmente S, Medina FJ, Echeverria M, Saez-Vasquez J (2007) Characterization of AtNUC-L1 reveals a central role of nucleolin in nucleolus organization and silencing of AtNUC-L2 gene in Arabidopsis. Mol Biol Cell 18:369–379

    PubMed  CAS  Google Scholar 

  • Preuss S, Pikaard CS (2007) rRNA gene silencing and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch. Biochim Biophys Acta 1769:383–392

    PubMed  CAS  Google Scholar 

  • Prieto JL, McStay B (2007) Recruitment of factors linking transcription and processing of pre-rRNA to NOR chromatin is UBF-dependent and occurs independent of transcription in human cells. Genes Dev 21:2041–2054

    PubMed  CAS  Google Scholar 

  • Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, Earley K, Lawrence RJ, Pikaard CS, Murfett J, Furner I, Vaucheret H, Sheid OM (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16:1021–1034

    PubMed  CAS  Google Scholar 

  • Rando O (2007) Global patterns of histone modifications. Curr Op Genet Devel 17:94–99

    CAS  Google Scholar 

  • Raska I (2003) Oldies but goldies: searching for Christmas trees within the nucleolar architecture. Trends Cell Biol 13:517–525

    PubMed  CAS  Google Scholar 

  • Raska I, Shaw PJ, Cmarko D (2006) Structure and function of the nucleolus in the spotlight. Curr Op Cell Biol 18:325–334

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Riddle NC, Richards EJ (2002) The control of natural variation in cytosine methylation in Arabidopsis. Genetics 162:355–363

    PubMed  CAS  Google Scholar 

  • Riddle NC, Richards EJ (2005) Genetic variation in epigenetic inheritance of ribosomal RNA gene methylation in Arabidopsis. Plant J 41:524–532

    PubMed  CAS  Google Scholar 

  • Roussel P, Sirri V, Hernandez-Verdun D (1994) Quantification of Ag-NOR proteins using Ag-NOR staining on Western blots. J Histochem Cytochem 42:1513–1517

    PubMed  CAS  Google Scholar 

  • Roussel P, Andre C, Comai L, Hernandez-Verdun D (1996) The rDNA transcription machinery is assembled during mitosis in active NORs and absent in inactive NORs. J Cell Biol 133:235–346

    PubMed  CAS  Google Scholar 

  • Santoro R (2005) The silence of the ribosomal RNA genes. Cell Mol Life Sci 62:2067–2079

    PubMed  CAS  Google Scholar 

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

    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

    PubMed  CAS  Google Scholar 

  • Scherl A, Coute Y, Deon C, Calle A, Kindbeiter K, Sanchez JC, Greco A, Hochstrasser D, Diaz JJ (2002) Functional proteomic analysis of human nucleolus. Mol Biol Cell 13:4100–4109

    PubMed  CAS  Google Scholar 

  • Schwartz BE, Ahmad K (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19:804–814

    PubMed  CAS  Google Scholar 

  • Sharma M (2004) NO29, a histone chaperone in the nucleolus. Prot Sci 13:115–116

    Google Scholar 

  • Shaw PJ, Jordan EG (1995) The nucleolus. Ann Rev Cell Dev Biol 11:93–121

    CAS  Google Scholar 

  • Shaw PJ, Highett MI, Beven AF, Jordan EG (1995) The nucleolar architecture of polymerase I transcription and processing. EMBO J 14:2896–2906

    PubMed  CAS  Google Scholar 

  • Shaw PJ, Beven AF, Leader DJ, Brown JWS (1998) Localization and processing from a polycistronic precursor of novel snoRNAs in maize. J Cell Science 111:2121–2128

    PubMed  Google Scholar 

  • Shogren-Knaak M, Ishii H, Sun J-M, Pazin MJ, Davie JR, Peterson CL (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844–847

    PubMed  CAS  Google Scholar 

  • Shou WY, Sakamoto KM, Keener J, Morimoto KW, Traverso EE, Azzam R, Hoppe GJ, Feldman RMR, DeModena J, Moazed D, Charbonneau H, Nomura M, Deshaies RJ (2001) Net1 stimulates RNA polymerase I transcription and regulates nucleolar structure independently of controlling mitotic exit. Mol Cell 8:45–55

    PubMed  CAS  Google Scholar 

  • Slusarczyk J, Wierzbicki A, Przewloka M, Tykarska T, Jerzmanowski A, Kuras M (2003) Influence of change in the proportion of H1 histone variants on microsporogenesis and development of male gametophyte in transgenic plants of tobacco (Nicotiana tabacum L.). Acta Soc Botan Pol 71:25–35

    Google Scholar 

  • Sogo JM, Ness PJ, Widmer RM, Parish RW, Koller T (1984) Psoralen-crosslinking of DNA as a probe for the structure of active nucleolar chromatin. J Mol Biol 178:897–919

    PubMed  CAS  Google Scholar 

  • Song L, Han MH, Lesicka J, Federoff N (2007) Arabidopsis primary microRNA processing proteins HYL1 and DCL1 define a nuclear body distinct from the Cajal body. Proc Natl Acad Sci USA 104:5437–5442

    PubMed  CAS  Google Scholar 

  • Spector DL (2003) The dynamics of chromosome organization and gene regulation. Ann Rev Biochem 72:573–608

    PubMed  CAS  Google Scholar 

  • Stargell LA, Bowen J, Dadd CA, Dedon PC, Davis M, Cook RG, Allis CD, Gorovsky MA (1993) Temporal and spatial association of histone H2A variant hv1 with transcriptionally competent chromatin during nuclear development in Tetrahymena thermophila. Genes Dev 7:2641–2651

    PubMed  CAS  Google Scholar 

  • Stefanovsky V, Moss T (2006) Regulation of rRNA synthesis in human and mouse cells is not determined by changes in active gene count. Cell Cycle 5:735–739

    PubMed  CAS  Google Scholar 

  • Straight AF, Shou WY, Dowd GJ, Turck CW, Deshaies RJ, Johnson AD, Moazed D (1999) Net1, a Sir2-associated nucleolar protein required for rDNA silencing and nucleolar integrity. Cell 97:245–256

    PubMed  CAS  Google Scholar 

  • Taddei A, Hediger F, Neumann FR, Bauer C, Gasser SM (2004) Separation of silencing from perinuclear acnhoring functions in yeast Ku80, Sir4 and Esc1 proteins. EMBO J 23:1301–1312

    PubMed  CAS  Google Scholar 

  • Tanaka I, Akahori Y, Gomi K, Suzuki T, Ueda K (1999) A novel histone variant localized in nucleoli of higher plant cells. Chromosoma 108:190–199

    PubMed  CAS  Google Scholar 

  • Thompson WF, Flavell RB (1988) DNase I sensitivity of ribosomal RNA genes in chromatin and nucleolar dominance in wheat. J Mol Biol 204:535–548

    PubMed  CAS  Google Scholar 

  • Thorstensen T, Fischer A, Sandvik SV, Johnsen SS, Grini PE, Reuter G, Aalen RB (2006) The Arabidopsis SUVR4 protein is a nucleolar histone methyltransferase with preference for monomethylated H3K9. Nucl Acids Res 34:5461–5470

    PubMed  CAS  Google Scholar 

  • Tongaonkar P, French SL, Oakes ML, Vu L, Schneider DA, Beyer AL, Nomura M (2005) Histones are required for transcription of yeast rRNA genes by RNA polyrnerase I. Proc Natl Acad Sci USA 102:10129–10134

    PubMed  CAS  Google Scholar 

  • Tsang CK, Bertram PG, Ai WD, Drenan R, Zheng XFS (2003) Chromatin-mediated regulation of nucleolar structure and RNA Pol I localization by TOR. EMBO J 22:6045–6056

    PubMed  CAS  Google Scholar 

  • Ueno Y, Ishikawa T, Watanabe K, Terakura S, Iwakawa H, Okada K, Machida C, Machida Y (2007) Histone deacetylases and ASYMMETRIC LEAVES2 are involved in the establishment of polarity in leaves of Arabidopsis. Plant Cell 19:445–457

    PubMed  CAS  Google Scholar 

  • Vaziri H, Dessain SK, Eaton EN, Imai S-I, Frye RA, Pandita TK, Guarente L, Weinberg RA (2001) hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107:149–159

    PubMed  CAS  Google Scholar 

  • Wako T, Houben A, Furushima-Shimogawarana R, Belyaev ND, Fukui K (2003) Centromere-specific acetylation of histone H4 in barley detected through three-dimensional microscopy. Plant Mol Biol 51:533–541

    PubMed  CAS  Google Scholar 

  • Wierzbicki AT, Jerzmanowski A (2005) Suppression of histone H1 genes in Arabidopsis results in heritable developmental defects and stochastic changes in DNA methylation. Genetics 169:997–1008

    PubMed  CAS  Google Scholar 

  • Wu K, Tian L, Zhao C, Brown D, Miki B (2003) Repression of gene expression by Arabidopsis HD2 histone deacetylases. Plant J 34:241–247

    PubMed  CAS  Google Scholar 

  • Ye JQ, Eickbush TH (2006) Chromatin structure and transcription of the R1- and R2-inserted rRNA genes of Drosophila melanogaster. Mol Cell Biol 26:8781–8790

    PubMed  CAS  Google Scholar 

  • Young DW, Hassan MQ, Pratap J, Galindo M, Zaidi SK, Lee SH, Yang XQ, Xie R, Javed A, Underwood JM, Furcinitti P, Imbalzano AN, Penman S, Nickerson JA, Montecino MA, Lian JB, Stein JL, van Wijnen AJ, Stein GS (2007) Mitotic occupancy and lineage-specific transcriptional control of rRNA genes by Runx2. Nature 445:442–446

    PubMed  CAS  Google Scholar 

  • Yu Y, Maggi LB, Brady SN, Apicelli AJ, Dai MS, Lu H, Weber JD (2006) Nucleophosmin is essential for ribosomal protein L5 nuclear export. Mol Cell Biol 26:3798–3809

    PubMed  CAS  Google Scholar 

  • Zhou YG, 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

    PubMed  CAS  Google Scholar 

  • Zhou C, Labbe H, Sridha S, Wang L, Tian L, Latoszek-Green M, Yang Z, Brown D, Miki B, Wu K (2004) Repression and function of HD2-type histone deacetylases in Arabidopsis development. Plant J 38:715–724

    PubMed  CAS  Google Scholar 

Download references

Acknowledgement

This work was funded by the Biotechnology and Biological Sciences Research Council of the UK (BBSRC).

Author information

Author notes

  1. Peter C. McKeown

    Present address: Genetics and Biotechnology Laboratory, Biochemistry Department, Lee Maltings, University of College Cork, Cork, Ireland

Authors and Affiliations

  1. Department of Cell and Developmental Biology, John Innes Centre, Norwich Research Park, Colney Lane, Norwich, Norfolk, UK, NR4 7UH

    Peter C. McKeown & Peter J. Shaw

Authors
  1. Peter C. McKeown
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter J. Shaw
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter C. McKeown.

Additional information

Communicated by E. Nigg

Rights and permissions

Reprints and permissions

About this article

Cite this article

McKeown, P.C., Shaw, P.J. Chromatin: linking structure and function in the nucleolus. Chromosoma 118, 11–23 (2009). https://doi.org/10.1007/s00412-008-0184-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-008-0184-2

Keywords

Search

Navigation