Chromosoma

, 118:11 | Cite as

Chromatin: linking structure and function in the nucleolus

Review

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.

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.

Notes

Acknowledgement

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

References

  1. Allis CD, Ziegler YS, Gorovsky MA, Olmsted JB (1982) A conserved histone variant enriched in nucleoli of mammalian cells. Cell 31:131–136PubMedGoogle Scholar
  2. 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 98:457–463PubMedCrossRefGoogle Scholar
  3. 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 12:1–11PubMedGoogle Scholar
  4. 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 25:1669–1679PubMedGoogle Scholar
  5. 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 21:6832–6841PubMedGoogle Scholar
  6. Avramova ZV (2002) Update on heterochromatin. Plant Physiol 129:40–49PubMedGoogle Scholar
  7. Benecke A (2006) Chromatin code, local non-equilibrium dynamics, and the emergence of transcription regulatory programs. Eur Phys J E 19:353–366PubMedGoogle Scholar
  8. 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 26:381–390PubMedGoogle Scholar
  9. 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 105:303–309PubMedGoogle Scholar
  10. Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI (2007) The multifunctional nucleolus. Nature Rev Mol Cell Biol 8:574–585Google Scholar
  11. Brown SE, Szyf M (2007) Epigenetic programming of the rRNA promoter by MBD3. Mol Cell Biol 27:4938–4952PubMedGoogle Scholar
  12. 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 115:2839–2846PubMedGoogle Scholar
  13. Carmo-Fonseca M, Mendes-Soares L, Campos I (2000) To be or not to be in the nucleolus. Nature Cell Biol 2:E107–E112PubMedGoogle Scholar
  14. 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 17:485–497PubMedGoogle Scholar
  15. 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 11:2124–2136PubMedGoogle Scholar
  16. 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 95:14891–14896PubMedGoogle Scholar
  17. Chen DY, Belmont AS, Huang S (2004) Upstream binding factor association induces large scale chromatin decondensation. Proc Natl Acad Sci USA 101:15106–15111PubMedGoogle Scholar
  18. Clarke AS, Samal E, Pillus L (2006) Distinct roles for the essential MYST family HAT Esa1p in transcriptional silencing. Mol Biol Cell 17:1744–1757PubMedGoogle Scholar
  19. Conconi A, Widmer RM, Koller T, Sogo JM (1989) Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell 57:753–761PubMedGoogle Scholar
  20. 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 127:2283–2289PubMedGoogle Scholar
  21. Csink AK, Henikoff S (1996) Genetic modification of heterochromatic association and nuclear organization in Drosophila. Nature 381:529–531PubMedGoogle Scholar
  22. 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 100:667–674Google Scholar
  23. 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 20:1283–1293PubMedGoogle Scholar
  24. Eden S, Hashimshony T, Keshet I, Cedar H, Thorne AW (1998) DNA methylation models histone acetylation. Nature 394:842PubMedGoogle Scholar
  25. 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 175:525–530PubMedGoogle Scholar
  26. Espada J, Esteller M (2007) Epigenetic control of nuclear architecture. Cell Mol Life Sci 64:449–457PubMedGoogle Scholar
  27. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A (2004a) H2AX: the histone guardian of the genome. DNA Repair 3:959–967PubMedGoogle Scholar
  28. Fernandez-Capetillo O, Allis CD, Nussenzweig A (2004b) Phosphorylation of histone H2B at DNA double-strand breaks. J Exp Med 199:1671–1677PubMedGoogle Scholar
  29. Flavell RB, O’Dell M, Thompson WF (1988) Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat. J Mol Biol 204:523–534PubMedGoogle Scholar
  30. 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 20:1075–1080PubMedGoogle Scholar
  31. Frehlick LJ, Eirin-Lopez JM, Ausio J (2007) New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones. Bioessays 29:49–59PubMedGoogle Scholar
  32. Fritze CE, Verschueren K, Strich R, Esposito RE (1997) Direct evidence for SIR2 modulation of chromatin structure in yeast rDNA. EMBO J 16:6495–6509PubMedGoogle Scholar
  33. Fuchs J, Demidov D, Houben A, Schubert I (2006) Chromosomal histone modification patterns—from conservation to diversity. Trends Plant Sci 11:199–208PubMedGoogle Scholar
  34. 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 403:108–112PubMedGoogle Scholar
  35. 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 5:205–210PubMedGoogle Scholar
  36. 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 281:8153–8160PubMedGoogle Scholar
  37. 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 198:199–207PubMedGoogle Scholar
  38. 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 16:3243–3255PubMedGoogle Scholar
  39. Gottlieb S, Esposito RE (1989) A new role for a yeast transcriptional silencer gene, Sir2, in regulation of recombination in ribosomal DNA. Cell 56:771–776PubMedGoogle Scholar
  40. Grummt I (2003) Life on a planet of its own: regulation of RNA polymerase I in the nucleolus. Genes Dev 17:1691–1702PubMedGoogle Scholar
  41. Grummt I (2007) Different epigenetic layers engage in complex crosstalk to define the epigenetic state of mammalian rRNA genes. Hum Mol Gen 16:R21–R27PubMedGoogle Scholar
  42. Grummt I, Pikaard CS (2003) Epigenetic silencing of RNA polymerase I transcription. Nature Rev Mol Cell Biol 4:641–649Google Scholar
  43. 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 32:1654–1665PubMedGoogle Scholar
  44. Hallows WC, Lee S, Denu JM (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc Natl Acad Sci USA 103:10230–10235PubMedGoogle Scholar
  45. Hancock R (2004) Internal organisation of the nucleus: assembly of compartments by macromolecular crowding and the nuclear matrix model. Biol Cell 96:595–601PubMedGoogle Scholar
  46. Hasterok R, Maluszynska J (2000) Different rRNA gene expression in primary and adventitious roots of Allium cepa. Folia Hist Cytobiol 38:181–184Google Scholar
  47. 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 8:2199–2216PubMedGoogle Scholar
  48. Henikoff S, Ahmad K (2005) Assembly of variant histones into chromatin. Ann Rev Cell Dev Biol 21:133–153Google Scholar
  49. Hernandez-Verdun D (2005) Tracking the interactions of rRNA processing proteins during nucleolar assembly in living cells. Medec Sci 21:1025–1027Google Scholar
  50. Hernandez-Verdun D, Roussel P, Gebrane-Younes J (2002) Emerging concepts of nucleolar assembly. J Cell Sci 115:2265–2270PubMedGoogle Scholar
  51. 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 104:843–852Google Scholar
  52. Hiscox JA (2007) RNA viruses: hijacking the dynamic nucleolus. Nature Rev Microbiol 5:119–127Google Scholar
  53. Houben A, Belyaev ND, Turner BM, Schubert I (1996) Differential immunostaining of plant chromosomes by antibodies recognizing acetylated histone H4 variants. Chromosome Res 4:191–194PubMedGoogle Scholar
  54. 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 17:2162–2176PubMedGoogle Scholar
  55. Huang S, Rothblum LI, Chen DY (2006) Ribosomal chromatin organization. Biochem Cell Biol 84:444–449PubMedGoogle Scholar
  56. 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 144:1508–1519PubMedGoogle Scholar
  57. Idei S, Kondo K, Turner BM, Fukui K (1996) Tomographic distribution of acetylated histone H4 in plant chromosomes, nuclei and nucleoli. Chromosoma 105:293–302PubMedGoogle Scholar
  58. Imai S-I, Armstrong CM, Keaberlein M, Guarente L (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403:795–800PubMedGoogle Scholar
  59. 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 12:2087–2100PubMedGoogle Scholar
  60. 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 19:187–191Google Scholar
  61. 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 14:123–130Google Scholar
  62. 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 160:49–56PubMedGoogle Scholar
  63. 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 94:13458–13462PubMedGoogle Scholar
  64. Kermekchiev M, Workman JL, Pikaard CS (1997) Nucleosome binding by the polymerase I transactivator upstream binding factor displaces linker histone H1. Mol Cell Biol 17:5833–5842PubMedGoogle Scholar
  65. Kimura A, Matsubara K, Horikoshi M (2005) A decade of histone acetylation: marking eukaryotic chromosomes with specific codes. J Biochem 138:647–662PubMedGoogle Scholar
  66. 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 117:441–453PubMedGoogle Scholar
  67. 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 2:991–1003Google Scholar
  68. 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 18:394–403PubMedGoogle Scholar
  69. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705PubMedGoogle Scholar
  70. 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 8:527–541PubMedGoogle Scholar
  71. Kurakin A (2005) Self-organization versus Watchmaker: stochastic dynamics of cellular organization. Biol Chem 386:247–254PubMedGoogle Scholar
  72. Kuzuhara T, Horikoshi M (2004) A nuclear FK506-binding protein is a histone chaperone regulating rDNA silencing. Nature Struct Mol Biol 11:275–283Google Scholar
  73. 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 11:5361–5380PubMedGoogle Scholar
  74. Lam YW, Lamond AI, Mann M, Andersen JS (2007) Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr Biol 17:749–760PubMedGoogle Scholar
  75. Lamond AI, Sleeman JE (2003) Nuclear substructure and dynamics. Curr Biol 13:R825–R828PubMedGoogle Scholar
  76. Lawrence RJ, Pikaard CS (2004) Chromatin turn ons and turn offs of ribosomal RNA genes. Cell Cycle 3:880–883PubMedGoogle Scholar
  77. 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 113:599–609Google Scholar
  78. 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 167:931–939PubMedGoogle Scholar
  79. 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 126:93–106PubMedGoogle Scholar
  80. Li CH, Mueller JE, Bryk M (2006b) Sir2 represses endogenous polymerase II transcription units in the ribosomal DNA nontranscribed spacer. Mol Biol Cell 17:3848–3859PubMedGoogle Scholar
  81. Li JW, Santoro R, Koberna K, Grummt I (2005) The chromatin remodelling complex NoRC controls replication timing of rRNA genes. EMBO J 24:120–127PubMedGoogle Scholar
  82. 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 109:161–172PubMedGoogle Scholar
  83. Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619PubMedGoogle Scholar
  84. Lyon CE, Lamond AI (2000) The nucleolus. Curr Biol 10:R323–R323PubMedGoogle Scholar
  85. Maggi LB, Weber JD (2005) Nucleolar adaptation in human cancer. Cancer Invest 23:599–608PubMedGoogle Scholar
  86. Mais C, Scheer U (2001) Molecular architecture of the amplified nucleoli of Xenopus oocytes. J Cell Sci 114:709–718PubMedGoogle Scholar
  87. 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 19:50–64PubMedGoogle Scholar
  88. 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 281:22062–22072PubMedGoogle Scholar
  89. Malik HS, Henikoff S (2003) Phylogenomics of the nucleosome. Nature Struct Biol 10:882–891PubMedGoogle Scholar
  90. 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 133:1336–1350PubMedGoogle Scholar
  91. Martin C, Zhang Y (2005) The diverse functions of histone lysine methylation. Nature Rev Mol Cell Biol 6:838–849Google Scholar
  92. May BP, Lippman ZB, Fang YD, Spector DL, Martienssen RA (2005) Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Gen 1:705–714Google Scholar
  93. McClintock B (1934) The relation of a particular chromosomal element to the development of the nucleoli in Zea mays. Z Zellforsch Mikrol Anat 21:294–328Google Scholar
  94. McStay B (2006) Nucleolar dominance: a model for rRNA gene silencing. Genes Dev 20:1207–1214PubMedGoogle Scholar
  95. 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 15:3169–3182PubMedGoogle Scholar
  96. Melese T, Xue Z (1995) The nucleolus—an organelle formed by the act of building a ribosome. Curr Op Cell Biol 7:319–324PubMedGoogle Scholar
  97. 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 34:1798–1806PubMedGoogle Scholar
  98. 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 12:247–251PubMedGoogle Scholar
  99. Misteli T (2001) The concept of self-organization in cellular architecture. J Cell Biol 155:181–185PubMedGoogle Scholar
  100. Mongelard F, Bouvet P (2007) Nucleolin: a multiFACeTed protein. Trends Cell Biol 17:80–86PubMedGoogle Scholar
  101. 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 8:341–351PubMedGoogle Scholar
  102. 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 64:29–49PubMedGoogle Scholar
  103. 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 133:627–639PubMedGoogle Scholar
  104. 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 12:2149–2160PubMedGoogle Scholar
  105. 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 100:1820–1825PubMedGoogle Scholar
  106. Nierras CR, Liebman SW, Warner JR (1997) Does S. cerevisiae need an organized nucleolus? Chromosoma 105:444–451PubMedGoogle Scholar
  107. North BJ, Marshall BL, Borra MT, Denu JM, Verdin E (2003) The human Sir2 ortholog, SIRT2, is an NAD(+)-dependent tubulin deacetylase. Mol Cell 11:437–444PubMedGoogle Scholar
  108. 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 19:8559–8569PubMedGoogle Scholar
  109. 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 26:3889–3901PubMedGoogle Scholar
  110. Okuwaki M, Matsumoto K, Tsujimoto M, Nagata K (2001) Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone. FEBS Lett 506:272–276PubMedGoogle Scholar
  111. Omer AD, Lowe TM, Russell AG, Ebhardt H, Eddy SR, Dennis PP (2000) Homologs of small nucleolar RNAs in archaea. Science 288:517–522PubMedGoogle Scholar
  112. 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 22:657–668PubMedGoogle Scholar
  113. Ouzounis CA, Kyrpides NC (1996) Parallel origins of the nucleosome core and eukaryotic transcription from archeae. J Mol Evol 42:234–239PubMedGoogle Scholar
  114. Palaniswamy V, Moraes KCM, Wilusz CJ, Wilusz J (2006) Nucleophosmin is selectively deposited on mRNA during polyadenylation. Nature Struct Mol Biol 13:429–435Google Scholar
  115. Panov KI, Friedrich JK, Russell J, Zomerdijk J (2006) UBF activates RNA polymerase I transcription by stimulating promoter escape. EMBO J 25:3310–3322PubMedGoogle Scholar
  116. Parsons XH, Garcia SN, Pillus L, Kadonaga JT (2003) Histone deacetylation by Sir2 generates a transcriptionally repressed nucleoprotein complex. Proc Natl Acad Sci USA 100:1609–1614PubMedGoogle Scholar
  117. Payne C, Braun RE (2006) Histone lysine trimethylation exhibits a distinct perinuclear distribution in Plzf-expressing spermatogonia. Dev Biol 293:461–472PubMedGoogle Scholar
  118. 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 16:260–269PubMedGoogle Scholar
  119. Peng JC, Karpen GH (2007) H3K9 methylation and RNA interference regulate nucleolar organization and repeated DNA stability. Nature Cell Biol 9:25–35PubMedGoogle Scholar
  120. 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 12:2225–2232PubMedGoogle Scholar
  121. 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 7:525–530PubMedGoogle Scholar
  122. Pikaard CS (1999) Nucleolar dominance and silencing of transcription. Trends Plant Sci 4:478–483PubMedGoogle Scholar
  123. Pluta AF, Mackay AM, Ainsztein AM, Goldberg IG, Earnshaw WC (1995) Centromere—hub of chromosomal activities. Science 270:1591–1594PubMedGoogle Scholar
  124. 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 103:18957–18962PubMedGoogle Scholar
  125. 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 100:11418–11423PubMedGoogle Scholar
  126. 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 126:79–92PubMedGoogle Scholar
  127. 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 18:369–379PubMedGoogle Scholar
  128. Preuss S, Pikaard CS (2007) rRNA gene silencing and nucleolar dominance: insights into a chromosome-scale epigenetic on/off switch. Biochim Biophys Acta 1769:383–392PubMedGoogle Scholar
  129. 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 21:2041–2054PubMedGoogle Scholar
  130. 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 16:1021–1034PubMedGoogle Scholar
  131. Rando O (2007) Global patterns of histone modifications. Curr Op Genet Devel 17:94–99Google Scholar
  132. Raska I (2003) Oldies but goldies: searching for Christmas trees within the nucleolar architecture. Trends Cell Biol 13:517–525PubMedGoogle Scholar
  133. Raska I, Shaw PJ, Cmarko D (2006) Structure and function of the nucleolus in the spotlight. Curr Op Cell Biol 18:325–334PubMedGoogle Scholar
  134. Richards B, Flint SJ, Cole MD, LeRoy G (2007) Nucleolin is required for RNA polymerase I transcription in vivo. Mol Cell Biol 27:937–948Google Scholar
  135. Riddle NC, Richards EJ (2002) The control of natural variation in cytosine methylation in Arabidopsis. Genetics 162:355–363PubMedGoogle Scholar
  136. Riddle NC, Richards EJ (2005) Genetic variation in epigenetic inheritance of ribosomal RNA gene methylation in Arabidopsis. Plant J 41:524–532PubMedGoogle Scholar
  137. Roussel P, Sirri V, Hernandez-Verdun D (1994) Quantification of Ag-NOR proteins using Ag-NOR staining on Western blots. J Histochem Cytochem 42:1513–1517PubMedGoogle Scholar
  138. 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 133:235–346PubMedGoogle Scholar
  139. Santoro R (2005) The silence of the ribosomal RNA genes. Cell Mol Life Sci 62:2067–2079PubMedGoogle Scholar
  140. Santoro R, Grummt I (2001) Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. Mol Cell 8:719–725PubMedGoogle Scholar
  141. 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 25:2539–2546PubMedGoogle Scholar
  142. 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 13:4100–4109PubMedGoogle Scholar
  143. Schwartz BE, Ahmad K (2005) Transcriptional activation triggers deposition and removal of the histone variant H3.3. Genes Dev 19:804–814PubMedGoogle Scholar
  144. Sharma M (2004) NO29, a histone chaperone in the nucleolus. Prot Sci 13:115–116Google Scholar
  145. Shaw PJ, Jordan EG (1995) The nucleolus. Ann Rev Cell Dev Biol 11:93–121Google Scholar
  146. Shaw PJ, Highett MI, Beven AF, Jordan EG (1995) The nucleolar architecture of polymerase I transcription and processing. EMBO J 14:2896–2906PubMedGoogle Scholar
  147. Shaw PJ, Beven AF, Leader DJ, Brown JWS (1998) Localization and processing from a polycistronic precursor of novel snoRNAs in maize. J Cell Science 111:2121–2128PubMedGoogle Scholar
  148. 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 311:844–847PubMedGoogle Scholar
  149. 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 8:45–55PubMedGoogle Scholar
  150. 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 71:25–35Google Scholar
  151. 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 178:897–919PubMedGoogle Scholar
  152. 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 104:5437–5442PubMedGoogle Scholar
  153. Spector DL (2003) The dynamics of chromosome organization and gene regulation. Ann Rev Biochem 72:573–608PubMedGoogle Scholar
  154. 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 7:2641–2651PubMedGoogle Scholar
  155. 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 5:735–739PubMedGoogle Scholar
  156. 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 97:245–256PubMedGoogle Scholar
  157. 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 23:1301–1312PubMedGoogle Scholar
  158. Tanaka I, Akahori Y, Gomi K, Suzuki T, Ueda K (1999) A novel histone variant localized in nucleoli of higher plant cells. Chromosoma 108:190–199PubMedGoogle Scholar
  159. Thompson WF, Flavell RB (1988) DNase I sensitivity of ribosomal RNA genes in chromatin and nucleolar dominance in wheat. J Mol Biol 204:535–548PubMedGoogle Scholar
  160. 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 34:5461–5470PubMedGoogle Scholar
  161. 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 102:10129–10134PubMedGoogle Scholar
  162. 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 22:6045–6056PubMedGoogle Scholar
  163. 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 19:445–457PubMedGoogle Scholar
  164. 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 107:149–159PubMedGoogle Scholar
  165. 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 51:533–541PubMedGoogle Scholar
  166. Wierzbicki AT, Jerzmanowski A (2005) Suppression of histone H1 genes in Arabidopsis results in heritable developmental defects and stochastic changes in DNA methylation. Genetics 169:997–1008PubMedGoogle Scholar
  167. Wu K, Tian L, Zhao C, Brown D, Miki B (2003) Repression of gene expression by Arabidopsis HD2 histone deacetylases. Plant J 34:241–247PubMedGoogle Scholar
  168. Ye JQ, Eickbush TH (2006) Chromatin structure and transcription of the R1- and R2-inserted rRNA genes of Drosophila melanogaster. Mol Cell Biol 26:8781–8790PubMedGoogle Scholar
  169. 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 445:442–446PubMedGoogle Scholar
  170. 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 26:3798–3809PubMedGoogle Scholar
  171. 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 21:4632–4640PubMedGoogle Scholar
  172. 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 38:715–724PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  1. 1.Department of Cell and Developmental BiologyJohn Innes Centre, Norwich Research ParkNorwichUK

Personalised recommendations