Cited by 83Nuclear Structure and FunctionGenomics and Chromatin DynamicsChromosomal and Genetic Variations

Nucleolus and chromatin

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Schöfer, Christian, Weipoltshammer, Klara·2018·Histochemistry and Cell Biology

Abstract

The nucleolus as site of ribosome biogenesis holds a pivotal role in cell metabolism. It is composed of ribosomal DNA (rDNA), which is present as tandem arrays located in nucleolus organizer regions (NORs). In interphase cells, rDNA can be found inside and adjacent to nucleoli and the location is indicative for transcriptional activity of ribosomal genes-inactive rDNA (outside) versus active one (inside). Moreover, the nucleolus itself acts as a spatial organizer of non-nucleolar chromatin. Microscopy-based approaches offer the possibility to explore the spatially distinct localization of the different DNA populations in relation to the nucleolar structure. Recent technical developments in microscopy and preparatory methods may further our understanding of the functional architecture of nucleoli. This review will attempt to summarize the current understanding of mammalian nucleolar chromatin organization as seen from a microscopist's perspective.

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  1. Ahmad K Henikoff S The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly Mol Cell 2002 9 1191 1200 12086617
  2. Albert B Perez-Fernandez J Leger-Silvestre I Gadal O Regulation of ribosomal RNA production by RNA polymerase I: does elongation come first? Genet Res Int 2012 2012 276948 22567380 PMC3335655
  3. Barr ML Bertram EG A morphological distinction between neurones of the male and female, and the behaviour of the nucleolar satellite during accelerated nucleoprotein synthesis Nature 1949 163 676 677 18120749
  4. Bartova E Stixova L Galiova G Harnicarova Horakova A Legartova S Kozubek S Mutant genetic background affects the functional rearrangement and kinetic properties of JMJD2b histone demethylase J Mol Biol 2011 405 679 695 21073875
  5. Baschong W Lucocq JM Roth J “Thiocyanate gold”: small (2–3 nm) colloidal gold for affinity cytochemical labeling in electron microscopy Histochemistry 1985 83 404 411 3878348
  6. Berger C Horlebein A Gogel E Grummt F Temporal order of replication of mouse ribosomal RNA genes during the cell cycle Chromosoma 1997 106 479 484 9426279
  7. Bernhard W A new staining procedure for electron microscopical cytology J Ultrastruct Res 1969 27 250 265 4181256
  8. Bernhard W Haguenau F Oberling C L’ultrastructure du nucleole de quelques cellules animales, revelee par le microscope electronique Experientia 1952 8 58 59 14945402
  9. Berry J Weber SC Vaidya N Haataja M Brangwynne CP RNA transcription modulates phase transition-driven nuclear body assembly Proc Natl Acad Sci USA 2015 112 E5237 E5245 26351690 PMC4586886
  10. Bierhoff H Dammert MA Brocks D Dambacher S Schotta G Grummt I Quiescence-induced LncRNAs trigger H4K20 trimethylation and transcriptional silencing Mol Cell 2014 54 675 682 24768537
  11. Bierhoff H Postepska-Igielska A Grummt I Noisy silence non-coding RNA and heterochromatin formation at repetitive elements Epigenetics 2014 9 53 61 24121539 PMC3928186
  12. Biggiogera M Fakan S Fine structural specific visualization of RNA on ultrathin sections J Histochem Cytochem 1998 46 389 395 9487121
  13. Biggiogera M Malatesta M Abolhassani-Dadras S Amalric F Rothblum LI Fakan S Revealing the unseen: the organizer region of the nucleolus J Cell Sci 2001 114 3199 3205 11590246
  14. Booth DG Ki-67 is a PP1-interacting protein that organises the mitotic chromosome periphery Elife 2014 3 e01641 24867636 PMC4032110
  15. Boyarchuk E Montes de Oca R Almouzni G Cell cycle dynamics of histone variants at the centromere, a model for chromosomal landmarks Curr Opin Cell Biol 2011 23 266 276 21470840
  16. Briggs SD Bryk M Strahl BD Cheung WL Davie JK Winston F Allis CD Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae Genes Dev 2001 15 3286 3295 11751634 PMC312847
  17. Brown DD Gurdon JB Absence of ribosomal RNA synthesis in the anucleolate mutant of Xenopus laevis Proc Natl Acad Sci USA 1964 51 139 146 14106673 PMC300879
  18. Caburet S Conti C Schurra C Lebofsky R Edelstein SJ Bensimon A Human ribosomal RNA gene arrays display a broad range of palindromic structures Genome Res 2005 15 1079 1085 16024823 PMC1182220
  19. Caudron-Herger M Pankert T Seiler J Nemeth A Voit R Grummt I Rippe K Alu element-containing RNAs maintain nucleolar structure and function EMBO J 2015 34 2758 2774 26464461 PMC4682651
  20. Chen H Fan M Pfeffer LM Laribee RN The histone H3 lysine 56 acetylation pathway is regulated by target of rapamycin (TOR) signaling and functions directly in ribosomal RNA biogenesis Nucleic Acids Res 2012 40 6534 6546 22553361 PMC3413144
  21. Chen F Tillberg PW Boyden ES Optical imaging. Expansion microscopy Science 2015 347 543 548 25592419 PMC4312537
  22. Cheutin T O´Donohue MF Beorchia A Vandelaer M Kaplan H Deféver B Ploton D Thiry M Three-dimensional organization of active rRNA genes within the nucleolus J Cell Sci 2002 115 3297 3307 12140261
  23. Cogliati R Gautier A Mise en évidence de l’ADN et des polysaccharides á l’aide d’un nouveau réactif “de type Schiff” C R Acad Sci 1973 276 3041 3044 4198810
  24. Conconi A Widmer RM Koller T Sogo JM Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle Cell 1989 57 753 761 2720786
  25. Cong R Das S Douet J Wong J Buschbeck M Mongelard F Bouvet P macroH2A1 histone variant represses rDNA transcription Nucleic Acids Res 2014 42 181 192 24071584 PMC3874179
  26. Dammann R Lucchini R Koller T Sogo JM Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae Nucleic Acids Res 1993 21 2331 2338 8506130 PMC309528
  27. Dass RA Wnt5a signals through DVL1 to repress ribosomal DNA transcription by RNA polymerase I PLoS Genet 2016 12 e1006217 27500936 PMC4976976
  28. Denissov S A model for the topology of active ribosomal RNA genes EMBO Rep 2011 12 231 237 21331097 PMC3059908
  29. Derenzini M Viron A Puvion-Dutilleul F The Feulgen-like osmium–ammine reaction as a tool to investigate chromatin structure in thin sections J Ultrastruct Res 1982 80 133 147 6181267
  30. Derenzini M Pession A Licastro F Novello F Electron microscopic evidence that ribosomal chromatin of human circulating lymphocytes is devoid of histones Exp Cell Res 1985 157 50 62 3918877
  31. Dillinger S Straub T Nemeth A Nucleolus association of chromosomal domains is largely maintained in cellular senescence despite massive nuclear reorganisation PloS One 2017 12 e0178821 28575119 PMC5456395
  32. Douet J MacroH2A histone variants maintain nuclear organization and heterochromatin architecture J Cell Sci 2017 130 1570 1582 28283545
  33. Dousset T Wang C Verheggen C Chen D Hernandez-Verdun D Huang S Initiation of nucleolar assembly is independent of RNA polymerase I transcription Mol Biol Cell 2000 11 2705 2717 10930464 PMC14950
  34. Drygin D Targeting RNA polymerase I with an oral small molecule CX-5461 inhibits ribosomal RNA synthesis and solid tumor growth Cancer Res 2011 71 1418 1430 21159662
  35. Dundr M Olson MO Partially processed pre-rRNA is preserved in association with processing components in nucleolus-derived foci during mitosis Mol Biol Cell 1998 9 2407 2422 9725903 PMC25507
  36. Dundr M Hoffmann-Rohrer U Hu Q Grummt I Rothblum LI Phair RD Misteli T A kinetic framework for a mammalian RNA polymerase in vivo Science 2002 298 1623 1626 12446911
  37. Durut N Saez-Vasquez J Nucleolin: dual roles in rDNA chromatin transcription Gene 2015 556 7 12 25225127
  38. Espada J Epigenetic disruption of ribosomal RNA genes and nucleolar architecture in DNA methyltransferase 1 (Dnmt1) deficient cells Nucleic Acids Res 2007 35 2191 2198 17355984 PMC1874631
  39. Fakan S Bernhard W Localisation of rapidly and slowly labelled nuclear RNA as visualized by high resolution autoradiography Exp Cell Res 1971 67 129 141 4105558
  40. Fedoriw AM Starmer J Yee D Magnuson T Nucleolar association and transcriptional inhibition through 5S rDNA in mammals PloS Genet 2012 8 e1002468 22275877 PMC3261910
  41. Felle M Exler JH Merkl R Dachauer K Brehm A Grummt I Langst G DNA sequence encoded repression of rRNA gene transcription in chromatin Nucleic Acids Res 2010 38 5304 5314 20421213 PMC2938192
  42. Feng W Yonezawa M Ye J Jenuwein T Grummt I PHF8 activates transcription of rRNA genes through H3K4me3 binding and H3K9me1/2 demethylation Nat Struct Mol Biol 2010 17 445 450 20208542
  43. Fiserova J Efenberkova M Sieger T Maninova M Uhlirova J Hozak P Chromatin organization at the nuclear periphery as revealed by image analysis of structured illumination microscopy data J Cell Sci 2017 130 2066 2077 28476938
  44. Floutsakou I Agrawal S Nguyen TT Seoighe C Ganley ARD McStay B The shared genomic architecture of human nucleolar organizer regions Genome Res 2013 23 2003 2012 23990606 PMC3847771
  45. Foltankova V Legartova S Kozubek S Hofer M Bartova E DNA-damage response in chromatin of ribosomal genes and the surrounding genome Gene 2013 522 156 167 23566839
  46. Foltz DR Jansen LE Black BE Bailey AO Yates JR III Cleveland DW The human CENP-A centromeric nucleosome-associated complex Nat Cell Biol 2006 8 458 469 16622419
  47. Ford E Voit R Liszt G Magin C Grummt I Guarente L Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription Genes Dev 2006 20 1075 1080 16618798 PMC1472467
  48. French SL Osheim YN Cioci F Nomura M Beyer AL 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 2003 23 1558 1568 12588976 PMC151703
  49. Fu Y MacroH2A1 associates with nuclear lamina and maintains chromatin architecture in mouse liver cells Sci Rep 2015 5 17186 26603343 PMC4658601
  50. Gagnon-Kugler T Langlois F Stefanovsky V Lessard F Moss T Loss of human ribosomal gene CpG methylation enhances cryptic RNA polymerase II transcription and disrupts ribosomal RNA processing Mol Cell 2009 35 414 425 19716787
  51. Galbiati A Epigenetic up-regulation of ribosome biogenesis and more aggressive phenotype triggered by the lack of the histone demethylase JHDM1B in mammary epithelial cells Oncotarget 2017 8 37091 37103 28415746 PMC5514893
  52. Gibbons JG Branco AT Yu S Lemos B Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans Nat Commun 2014 5 4850 25209200
  53. Gibbons JG Branco AT Godinho SA Yu S Lemos B Concerted copy number variation balances ribosomal DNA dosage in human and mouse genomes Proc Natl Acad Sci USA 2015 112 2485 2490 25583482 PMC4345604
  54. Goldberg AD Distinct factors control histone variant H3.3 localization at specific genomic regions Cell 2010 140 678 691 20211137 PMC2885838
  55. Granboulan N Granboulan P Cytochimie ultrastructurale du nucleole. I. Mise en evidence de chromatine a l’interieur du nucleole Exp Cell Res 1964 34 71 87 14134538
  56. Granboulan N Granboulan P Cytochimie ultractructurale du nucleole. II. Etude des sites de synthese du RNA dans le nucleole et le noyau Exp Cell Res 1965 38 604 619 14330679
  57. Grob A Roussel P Wright JE McStay B Hernandez-Verdun D Sirri V Involvement of SIRT7 in resumption of rDNA transcription at the exit from mitosis J Cell Sci 2009 122 489 498 19174463 PMC2714433
  58. Grob A Colleran C McStay B Construction of synthetic nucleoli in human cells reveals how a major functional nuclear domain is formed and propagated through cell division Genes Dev 2014 28 220 230 24449107 PMC3923965
  59. Grummt I Langst G Epigenetic control of RNA polymerase I transcription in mammalian cells Biochim Biophys Acta 2013 1829 393 404 23063748
  60. Guelen L Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions Nature 2008 453 948 951 18463634
  61. Haaf T Hayman DL Schmid M Quantitative determination of rDNA transcription units in vertebrate cells Exp Cell Res 1991 193 78 86 1995304
  62. Haeusler RA Engelke DR Spatial organization of transcription by RNA polymerase III Nucleic Acids Res 2006 34 4826 4836 16971453 PMC1635290
  63. Hamdane N Conditional inactivation of upstream binding factor reveals its epigenetic functions and the existence of a somatic nucleolar precursor body PLoS Genet 2014 10 e1004505 25121932 PMC4133168
  64. Hancock R The crowded nucleus Int Rev Cel Mol Bio 2014 307 15 26 24380591
  65. Harris B Cohesion promotes nucleolar structure and function Mol Biol Cell 2014 25 337 346 24307683 PMC3907274
  66. Henderson AS Warburton D Atwood KC Locatoin of ribosomal DNA in the human chromosome complement Proc Natl Acad Sci USA 1972 69 3394 3398 4508329 PMC389778
  67. Herdman C A unique enhancer boundary complex on the mouse ribosomal RNA genes persists after loss of Rrn3 or UBF and the inactivation of RNA polymerase I transcription PLoS Genet 2017 13 e1006899 28715449 PMC5536353
  68. Hernandez-Hernandez A Soto-Reyes E Ortiz R Arriaga-Canon C Echeverria-Martinez OM Vazquez-Nin GH Recillas-Targa F Changes of the nucleolus architecture in absence of the nuclear factor CTCF Cytogenet Genome Res 2012 136 89 96 22286186
  69. Hirschler-Laszkiewicz I Cavanaugh A Hu Q Catania J Avantaggiati ML Rothblum LI The role of acetylation in rDNA transcription Nucleic Acids Res 2001 29 4114 4124 11600700 PMC60214
  70. Holmberg Olausson K Nister M Lindstrom MS Loss of nucleolar histone chaperone NPM1 triggers rearrangement of heterochromatin and synergizes with a deficiency in DNA methyltransferase DNMT3A to drive ribosomal DNA transcription J Biol Chem 2014 289 34601 34619 25349213 PMC4263867
  71. Hornacek M Kovacik L Mazel T Cmarko D Bartova E Raska I Smirnov E Fluctuations of pol I and fibrillarin contents of the nucleoli Nucleus 2017 8 421 432 28622108 PMC5597295
  72. Huang K Ribosomal RNA gene transcription mediated by the master genome regulator protein CCCTC-binding factor (CTCF) is negatively regulated by the condensin complex J Biol Chem 2013 288 26067 26077 23884423 PMC3764810
  73. Ianni A Hoelper S Krueger M Braun T Bober E Sirt7 stabilizes rDNA heterochromatin through recruitment of DNMT1 and Sirt1 Biochem Biophys Res Commun 2017 492 434 440 28842251
  74. Jackson DA Iborra FJ Manders EM Cook PR Numbers and organization of RNA polymerases, nascent transcripts, and transcription units in HeLa nuclei Mol Biol Cell 1998 9 1523 1536 9614191 PMC25378
  75. Jacob MD Audas TE Uniacke J Trinkle-Mulcahy L Lee S Environmental cues induce a long noncoding RNA-dependent remodeling of the nucleolus Mol Biol Cell 2013 24 2943 2953 23904269 PMC3771955
  76. Jakociunas T Jordo MD Mebarek MA Bunner CM Verhein-Hansen J Oddershede LB Thon G Subnuclear relocalization and silencing of a chromosomal region by an ectopic ribosomal DNA repeat Proc Natl Acad Sci USA 2013 110 E4465 E4473 24191010 PMC3839722
  77. Jin C Zang C Wei G Cui K Peng W Zhao K Felsenfeld G H3.3/H2A.Z double variant-containing nucleosomes mark ‘nucleosome-free regions’ of active promoters and other regulatory regions in the human genome Nat Genet 2009 41 941 945 19633671 PMC3125718
  78. Johnson JM French SL Osheim YN Li M Hall L Beyer AL Smith JS Rpd3- and spt16-mediated nucleosome assembly and transcriptional regulation on yeast ribosomal DNA genes Mol Cell Biol 2013 33 2748 2759 23689130 PMC3700123
  79. Jones HS Kawauchi J Braglia P Alen CM Kent NA Proudfoot NJ RNA polymerase I in yeast transcribes dynamic nucleosomal rDNA Nat Struct Mol Biol 2007 14 123 130 17259992 PMC6941936
  80. Judelson HS Vogt VM Accessibility of ribosomal genes to trimethyl psoralen in nuclei of Physarum polycephalum Mol Cell Biol 1982 2 211 220 6287230 PMC369779
  81. Kalmarova M Smirnov E Masata M Koberna K Ligasova A Popov A Raska I Positioning of NORs and NOR-bearing chromosomes in relation to nucleoli J Struct Biol 2007 160 49 56 17698369 PMC2446407
  82. Kind J Single-cell dynamics of genome-nuclear lamina interactions Cell 2013 153 178 192 23523135
  83. Kiran S Chatterjee N Singh S Kaul SC Wadhwa R Ramakrishna G Intracellular distribution of human SIRT7 and mapping of the nuclear/nucleolar localization signal Febs J 2013 280 3451 3466 23680022
  84. Kitamura H The actin family protein ARP6 contributes to the structure and the function of the nucleolus Biochem Biophys Res Commun 2015 464 554 560 26164235 PMC5920680
  85. Kobayashi T A new role of the rDNA and nucleolus in the nucleus–rDNA instability maintains genome integrity BioEssays 2008 30 267 272 18293366
  86. Koiwai K TdIF2 is a nucleolar protein that promotes rRNA gene promoter activity Genes Cells 2011 16 748 764 21668587
  87. Lavelle C Prunell A Chromatin polymorphism and the nucleosome superfamily: a genealogy Cell Cycle 2007 6 2113 2119 17786045
  88. Lee D An J Park YU Liaw H Woodgate R Park JH Myung K SHPRH regulates rRNA transcription by recognizing the histone code in an mTOR-dependent manner Proc Natl Acad Sci USA 2017 114 E3424 E3433 28400511 PMC5410823
  89. Lee D Park JH Kim S Lee SG Myung K SHPRH as a new player in ribosomal RNA transcription and its potential role in homeostasis of ribosomal DNA repeats Transcription 2018 9 190 195 29139335 PMC5927684
  90. Li J Santoro R Koberna K Grummt I The chromatin remodeling complex NoRC controls replication timing of rRNA genes EMBO J 2005 24 120 127 15577942 PMC544905
  91. Li J Langst G Grummt I NoRC-dependent nucleosome positioning silences rRNA genes EMBO J 2006 25 5735 5741 17139253 PMC1698900
  92. Lyko F The DNA methyltransferase family: a versatile toolkit for epigenetic regulation Nat Rev Genet 2018 19 81 92 29033456
  93. Manuelidis L Different central nervous system cell types display distinct and nonrandom arrangements of satellite DNA sequences Proc Natl Acad Sci USA 1984 81 3123 3127 6587343 PMC345233
  94. Manuelidis L Borden J Reproducible compartmentalization of individual chromosome domains in human CNS cells revealed by in situ hybridization and 3-D reconstruction Chromosoma 1988 96 397 410 3219911
  95. Masiello I Biggiogera M Ultrastructural localization of 5-methylcytosine on DNA and RNA Cell Mol Life Sci 2017 74 3057 3064 28391361 PMC11107537
  96. Matera AG Frey MR Margelot K Wolin SL A perinucleolar compartment contains several RNA polymerase III transcripts as well as the polypyrimidine tract-binding protein hnRNP I J Cell Biol 1995 129 1181 1193 7539809 PMC2120477
  97. Mayer C Schmitz KM Li J Grummt I Santoro R Intergenic transcripts regulate the epigenetic state of rRNA genes Mol Cell 2006 22 351 361 16678107
  98. Mayer C Neubert M Grummt I The structure of NoRC-associated RNA is crucial for targeting the chromatin remodelling complex NoRC to the nucleolus EMBO Rep 2008 9 774 780 18600236 PMC2515205
  99. McStay B Grummt I The epigenetics of rRNA genes: from molecular to chromosome biology Annu Rev Cell Dev Biol 2008 24 131 157 18616426
  100. Meneghini MD Wu M Madhani HD Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin Cell 2003 112 725 736 12628191
  101. Merz K Hondele M Goetze H Gmelch K Stoeckl U Griesenbeck J 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 2008 22 1190 1204 18451108 PMC2335315
  102. Miller OL Beatty BR Visualization of nucleolar genes Science 1969 164 955 957 5813982
  103. Mills EW Green R Ribosomopathies: there’s strength in numbers Science 2017 29097519
  104. Mosgoeller W Schöfer C Wesierska-Gadek J Steiner M Müller M Wachtler F Ribosomal gene transcription is organized in foci within nucleolar components Histochem Cell Biol 1998 109 111 118 9504771
  105. Murayama A Epigenetic control of rDNA loci in response to intracellular energy status Cell 2008 133 627 639 18485871
  106. Naetar N Ferraioli S Foisner R Lamins in the nuclear interior—life outside the lamina J Cell Sci 2017 130 2087 2096 28668931
  107. Nemeth A Initial genomics of the human nucleolus PLoS Genet 2010 6 e1000889 20361057 PMC2845662
  108. Ochs RL Press RI Centromere autoantigens are associated with the nucleolus Exp Cell Res 1992 200 339 350 1572401
  109. Osheim YN French SL Sikes ML Beyer AL Electron microscope visualization of RNA transcription and processing in Saccharomyces cerevisiae by Miller chromatin spreading Methods Mol Biol 2009 464 55 69 18951179
  110. Padeken J Heun P Nucleolus and nuclear periphery: velcro for heterochromatin Curr Opin Cell Biol 2014 28 54 60 24690547
  111. Paredes S Angulo-Ibanez M Tasselli L Carlson SM Zheng W Li TM Chua KF The epigenetic regulator SIRT7 guards against mammalian cellular senescence induced by ribosomal DNA instability J Biol Chem 2018 29728458 PMC6052228
  112. Peters AHFM Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability Cell 2001 107 323 337 11701123
  113. Picart C Pontvianne F Plant nucleolar DNA: green light shed on the role of nucleolin in genome organization Nucleus 2017 8 11 16 27644794 PMC5287095
  114. Prior CP Cantor CR Johnson EM Allfrey VG Incorporation of exogenous pyrene-labeled histone into Physarum chromatin: a system for studying changes in nucleosomes assembled in vivo Cell 1980 20 597 608 7417999
  115. Protacio RU Widom J Nucleosome transcription studied in a real-time synchronous system: test of the lexosome model and direct measurement of effects due to histone octamer J Mol Biol 1996 256 458 472 8604131
  116. Ragoczy T Telling A Scalzo D Kooperberg C Groudine M Functional redundancy in the nuclear compartmentalization of the late-replicating genome Nucleus 2014 5 626 635 25493640 PMC4615584
  117. Rattner JB Saunders C Davie JR Hamkalo BA Ultrastructural organization of yeast chromatin J Cell Biol 1982 93 217 222 7040415 PMC2112099
  118. Rickards B Flint SJ Cole MD LeRoy G Nucleolin is required for RNA polymerase I transcription in vivo Mol Cell Biol 2007 27 937 948 17130237 PMC1800701
  119. Saka K Ide S Ganley AR Kobayashi T Cellular senescence in yeast is regulated by rDNA noncoding transcription Curr Biol 2013 23 1794 1798 23993840
  120. Sanij E Hannan RD The role of UBF in regulating the structure and dynamics of transcriptionally active rDNA chromatin Epigenetics 2009 4 374 382 19717978
  121. Santoro R Li J Grummt I The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription Nat Genet 2002 32 393 396 12368916
  122. Scheer U Changes of nucleosome frequency in nucleolar and non-nucleolar chromatin as a function of transcription: an electron microscopic study Cell 1978 13 535 549 566162
  123. Scheer U Rose KM Localization of RNA polymerase I in interphase cells and mitotic chromosomes by light-and elctron microscopic immunocytochemistry Proc Natl Acad Sci USA 1984 81 1431 1435 6369327 PMC344849
  124. Schlesinger S Selig S Bergman Y Cedar H Allelic inactivation of rDNA loci Genes Dev 2009 23 2437 2447 19833769 PMC2764490
  125. Schmickel RD Quantitation of human ribosomal DNA: hybridization of human DNA with ribosomal RNA for quantitation and fractionation Pediatr Res 1973 7 5 12 4687000
  126. Schöfer C Weipoltshammer K Almeder M Wachtler F Arrangement of individual human ribosomal DNA fragments on stretched DNA fibers Histochem Cell Biol 1998 110 201 205 9720993
  127. Schwann T Mikroskopische Untersuchungen über die Übereinstimmung in der Struktur und dem Wachstum der Tiere und Pflanzen 1839 Berlin Sander 21516882
  128. Sen Gupta A Sengupta K Lamin B2 modulates nucleolar morphology, dynamics, and function Mol Cell Biol 2017 37 e000274 e000217 PMC5705821 28993479
  129. Shen M The chromatin remodeling factor CSB recruits histone acetyltransferase PCAF to rRNA gene promoters in active state for transcription initiation PloS One 2013 8 e62668 23667505 PMC3646882
  130. Shi L Wang J Hong F Spector DL Fang Y Four amino acids guide the assembly or disassembly of Arabidopsis histone H3.3-containing nucleosomes Proc Natl Acad Sci USA 2011 108 10574 10578 21670303 PMC3127877
  131. Shiue CN Berkson RG Wright AP c-Myc induces changes in higher order rDNA structure on stimulation of quiescent cells Oncogene 2009 28 1833 1842 19270725
  132. Shiue CN Nematollahi-Mahani A Wright AP Myc-induced anchorage of the rDNA IGS region to nucleolar matrix modulates growth-stimulated changes in higher-order rDNA architecture Nucleic Acids Res 2014 42 5505 5517 24609384 PMC4027186
  133. Smetana KB Busch H Studies on the ultrastructure of the nucleoli of the Walker tumor and rat liver Cancer Res 1964 24 537 557 14188456
  134. Smirnov E Reproduction of the FC/DFC units in nucleoli Nucleus 2016 7 203 215 26934002 PMC4916892
  135. Smith CL A separable domain of the p150 subunit of human chromatin assembly factor-1 promotes protein and chromosome associations with nucleoli Mol Biol Cell 2014 25 2866 2881 25057015 PMC4161520
  136. Snyers L Zupkovitz G Almeder M Fliesser M Stoisser A Weipoltshammer K Schofer C Distinct chromatin signature of histone H3 variant H3.3 in human cells Nucleus 2014 5 449 461 25482197 PMC4164487
  137. Strohner R Nemeth A Jansa P Hofmann-Rohrer U Santoro R Langst G Grummt I NoRC—a novel member of mammalian ISWI-containing chromatin remodeling machines EMBO J 2001 20 4892 4900 11532953 PMC125270
  138. Stults DM Killen MW Pierce HH Pierce AJ Genomic architecture and inheritance of human ribosomal RNA gene clusters Genome Res 2008 18 13 18 18025267 PMC2134781
  139. Sullivan GJ Bridger JM Cuthbert AP Newbold RF Bickmore WA McStay B Human acrocentric chromosomes with transcriptionally silent nucleolar organizer regions associate with nucleoli EMBO J 2001 20 2867 2874 11387219 PMC125486
  140. Sylvester JE Whiteman DA Podolsky R Pozsgay J Respess J Schmickel RD The human ribosomal RNA genes: structure and organization of the complete repeating unit Hum Genet 1986 73 193 198 3015766
  141. Tanaka Y JmjC enzyme KDM2A is a regulator of rRNA transcription in response to starvation EMBO J 2010 29 1510 1522 20379134 PMC2876952
  142. Tessarz P Santos-Rosa H Robson SC Sylvestersen KB Nelson CJ Nielsen ML Kouzarides T Glutamine methylation in histone H2A is an RNA-polymerase-I-dedicated modification Nature 2014 505 564 568 24352239 PMC3901671
  143. Thiry M Thiry-Blaise L In situ hybridization at the electron microscopic level: an improved method for the precise localization of ribosomal DNA and RNA Eur J Cell Biol 1989 50 235 243 2612500
  144. Tongaonkar P French SL Oakes ML Vu L Schneider DA Beyer AL Nomura M Histones are required for transcription of yeast rRNA genes by RNA polymerase I Proc Natl Acad Sci USA 2005 102 10129 10134 16002464 PMC1177414
  145. Torrano V Targeting of CTCF to the nucleolus inhibits nucleolar transcription through a poly(ADP-ribosyl)ation-dependent mechanism J Cell Sci 2006 119 1746 1759 16595548
  146. Tsai YC Greco TM Boonmee A Miteva Y Cristea IM Functional proteomics establishes the interaction of SIRT7 with chromatin remodeling complexes and expands its role in regulation of RNA polymerase I transcription Moll Cell Proteom 2012 11 60 76 PMC3418843 22586326
  147. Udugama M Ribosomal DNA copy loss and repeat instability in ATRX-mutated cancers Proc Natl Acad Sci USA 2018 115 4737 4742 29669917 PMC5939086
  148. van Sluis M McStay B Ribosome biogenesis: Achilles heel of cancer? Genes Cancer 2014 5 152 153 25061498 PMC4104764
  149. van Koningsbruggen S High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli Mol Biol Cell 2010 21 3735 3748 20826608 PMC2965689
  150. van de Nobelen S CTCF regulates the local epigenetic state of ribosomal DNA repeats Epigenet Chromatin 2010 3 19 PMC2993708 21059229
  151. Vizuet-de-Rueda JC Florencio-Martinez LE Padilla-Mejia NE Manning-Cela R Hernandez-Rivas R Martinez-Calvillo S Ribosomal RNA genes in the protozoan parasite Leishmania major possess a nucleosomal structure Protist 2016 167 121 135 26963795
  152. Wachtler F Human ribosomal RNA gene repeats are localized in the dense fibrillar component of nucleoli: light and electron microscopic in situ hybridization in human Sertoli cells Exp Cell Res 1992 198 135 143 1727047
  153. Wallace HB Birnstiel ML Ribosomal cistrons and the nucleolar organizer Biochim Biophys Acta Nucleic Acids Protein Synth 1966 114 296 310 5943882
  154. Wang M Lemos B Ribosomal DNA copy number amplification and loss in human cancers is linked to tumor genetic context, nucleolus activity, and proliferation PLoS Genet 2017 13 e1006994 28880866 PMC5605086
  155. Weipoltshammer K Schofer C Morphology of nuclear transcription Histochem Cell Biol 2016 145 343 358 26847177 PMC4796325
  156. Weipoltshammer K Schöfer C Almeder M Sylvester J Wachtler F Spatial distribution of sex chromosomes and ribosomal genes: a study on human lymphocytes and testicular cells Cytogenet Cell Genet 1996 73 108 113 8646876
  157. Weipoltshammer K Schöfer C Wachtler F Hozak P The transcription unit of ribosomal genes is attached to the nuclear skeleton Exp Cell Res 1996 227 374 379 8831576
  158. Weipoltshammer K Schöfer C Almeder M Philimonenko VV Frei K Wachtler F Hozák P Intranuclear anchoring of repetitive DNA sequences: centromeres, telomeres, and ribosomal DNA J Cell Biol 1999 147 1409 1418 10613900 PMC2174248
  159. Wen Y Wang C Huang S The perinucleolar compartment associates with malignancy Front Biol (Beijing) 2013 8 369 376 PMC3862354 24348523
  160. Wittner M Hamperl S Stockl U Seufert W Tschochner H Milkereit P Griesenbeck J Establishment and maintenance of alternative chromatin states at a multicopy gene locus Cell 2011 145 543 554 21565613
  161. Wong LH ATRX interacts with H3.3 in maintaining telomere structural integrity in pluripotent embryonic stem cells Genome Res 2010 20 351 360 20110566 PMC2840985
  162. Xie W The chromatin remodeling complex NuRD establishes the poised state of rRNA genes characterized by bivalent histone modifications and altered nucleosome positions Proc Natl Acad Sci USA 2012 109 8161 8166 22570494 PMC3361413
  163. Xu B Lu S Gerton JL Roberts syndrome: a deficit in acetylated cohesin leads to nucleolar dysfunction Rare Dis 2014 2 e27743 25054091 PMC4091327
  164. Xu HH Su T Xue Y Histone H3 N-terminal acetylation sites especially K14 are important for rDNA silencing and aging Sci Rep 2016 6 21900 26906758 PMC4764821
  165. Xu B Ribosomal DNA copy number loss and sequence variation in cancer PLoS Genet 2017 13 e1006771 28640831 PMC5480814
  166. Yang L Regulation of SirT1-nucleomethylin binding by rRNA coordinates ribosome biogenesis with nutrient availability Mol Cell Biol 2013 33 3835 3848 23897426 PMC3811878
  167. Yang F The lncRNA Firre anchors the inactive X chromosome to the nucleolus by binding CTCF and maintains H3K27me3 methylation Genome Biol 2015 16 52 25887447 PMC4391730
  168. Yasuzumi GS Sugihara T Kiriyama R Sugioka M Electron microscope researches on the ultrastructure of nucleoli in animal tissues Z Zellforsch Mikrosk Anat 1958 48 10 23 13604846
  169. Yu S Lemos B A portrait of ribosomal DNA contacts with Hi-C reveals 5S and 45S rDNA anchoring points in the folded human genome Genome Biol Evol 2016 8 3545 3558 27797956 PMC5203791
  170. Yu S Lemos B The long-range interaction map of ribosomal DNA arrays PLoS Genet 2018 14 e1007258 29570716 PMC5865718
  171. Yusufzai TM Tagami H Nakatani Y Felsenfeld G CTCF tethers an insulator to subnuclear sites, suggesting shared insulator mechanisms across species Mol Cell 2004 13 291 298 14759373
  172. Zhang Y Ng HH Erdjument-Bromage H Tempst P Bird A Reinberg D Analysis of the NuRD subunits reveals a histone deacetylase core complex and a connection with DNA methylation Genes Dev 1999 13 1924 1935 10444591 PMC316920
  173. Zhang LF Huynh KD Lee JT Perinucleolar targeting of the inactive X during S phase: evidence for a role in the maintenance of silencing Cell 2007 129 693 706 17512404
  174. Zheng Y Histone H1 phosphorylation is associated with transcription by RNA polymerases I and II J Cell Biol 2010 189 407 415 20439994 PMC2867294
  175. Zhou Y Schmitz KM Mayer C Yuan X Akhtar A Grummt I Reversible acetylation of the chromatin remodelling complex NoRC is required for non-coding RNA-dependent silencing Nat Cell Biol 2009 11 1010 1016 19578370
  176. Zhou J Eickbush MT Eickbush TH A population genetic model for the maintenance of R2 retrotransposons in rRNA gene loci PLoS Genet 2013 9 e1003179 23326244 PMC3542110
  177. Zhu Z PHF8 is a histone H3K9me2 demethylase regulating rRNA synthesis Cell Res 2010 20 794 801 20531378
  178. Zillner K Filarsky M Rachow K Weinberger M Langst G Nemeth A Large-scale organization of ribosomal DNA chromatin is regulated by Tip5 Nucleic Acids Res 2013 41 5251 5262 23580549 PMC3664807
  179. Zillner K Komatsu J Filarsky K Kalepu R Bensimon A Nemeth A Active human nucleolar organizer regions are interspersed with inactive rDNA repeats in normal and tumor cells Epigenomics 2015 7 363 378 26077426

Cited by

Sorted by citations

Authors
Schöfer, C., & Weipoltshammer, K.
Affiliations
Medical University of Vienna (AT)
Corresponding author
Schöfer, Christian
Venue
Histochemistry and Cell Biology
Published
2018-07-25
Volume
150
Issue
3
Pages
209-225
ISSN
  • 0948-6143 (ISSN-L)
  • 1432-119X
OpenAlex
W2884385526
Cited by
83
References
5
Citations by year
2026: 5 · 2025: 5 · 2024: 13 · 2023: 9 · 2022: 13 · 2021: 12 · 2020: 12 · 2019: 12 · 2018: 1 · 2017: 1
FWCI
0.91
Type
journal article
Language
en
Open access
Locations
  • Histochemistry and Cell Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
Austrian Science Fund FWF and Herzfelder´sche Familienstiftung (P30642-b28)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
Keywords
nucleolus, nucleolar chromatin, ribosome biogenesis, ribosomal DNA, nucleolar organizer regions, rDNA transcription, mammalian cells
MeSH terms
Animals, Cell Nucleus, Chromatin, Humans, Microscopy

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