The nucleolus and transcription of ribosomal genes

Abstract Ribosome biogenesis is a highly dynamic, steady‐state nucleolar process that involves synthesis and maturation of rRNA, its transient interactions with non‐ribosomal proteins and RNPs and assembly with ribosomal proteins. In the few years of the 21st century, an exciting progress in the molecular understanding of rRNA and ribosome biogenesis has taken place. In this review, we discuss the recent results on the regulation of rRNA synthesis in relation to the functional organization of the nucleolus, and put an emphasis on the situation encountered in mammalian somatic cells.

[1]  T. Misteli.  The concept of self-organization in cellular architecture , 2001, The Journal of cell biology.

[2]  L. Comai,et al.  Repression of RNA Polymerase I Transcription by the Tumor Suppressor p53 , 2000, Molecular and Cellular Biology.

[3]  J. Politz,et al.  Signal recognition particle RNA localization within the nucleolus differs from the classical sites of ribosome synthesis , 2002, The Journal of cell biology.

[4]  T. Moss,et al.  At the Center of Eukaryotic Life , 2002, Cell.

[5]  M. Nomura,et al.  Transcription of chromosomal rRNA genes by both RNA polymerase I and II in yeast uaf30 mutants lacking the 30 kDa subunit of transcription factor UAF , 2001, The EMBO journal.

[6]  Christopher M. Gallo,et al.  RPD3 is required for the inactivation of yeast ribosomal DNA genes in stationary phase , 2002, The EMBO journal.

[7]  P. Cook,et al.  Site of transcription of ribosomal RNA and intranucleolar structure in HeLa cells. , 1994, Journal of cell science.

[8]  P. Gleizes,et al.  Assembly and functional organization of the nucleolus: ultrastructural analysis of Saccharomyces cerevisiae mutants. , 2000, Molecular biology of the cell.

[9]  O. Miller,et al.  Visualization of Nucleolar Genes , 1969, Science.

[10]  L. I. Rothblum,et al.  Ultrastructural analysis of nucleolar transcription in cells microinjected with 5-bromo-UTP , 2000, Histochemistry and Cell Biology.

[11]  M. O'Reilly,et al.  The terminal balls characteristic of eukaryotic rRNA transcription units in chromatin spreads are rRNA processing complexes. , 1993, Genes & development.

[12]  F. Harper,et al.  Non-nucleolar transcription complexes of rat liver as revealed by spreading isolated nuclei. , 1979, Journal of cell science.

[13]  U. Scheer,et al.  The nucleolus. , 1994, Current opinion in cell biology.

[14]  J. Shabanowitz,et al.  A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis , 2002, Nature.

[15]  B Sollner-Webb,et al.  Metazoan rDNA enhancer acts by making more genes transcriptionally active , 1996, The Journal of cell biology.

[16]  Michael. Delannoy,et al.  Analysis of nucleolar transcription and processing domains and pre-rRNA movements by in situ hybridization , 1997, Chromosoma.

[17]  D. Hernandez-Verdun,et al.  Initiation of nucleolar assembly is independent of RNA polymerase I transcription. , 2000, Molecular biology of the cell.

[18]  D. Treré,et al.  Nucleolar size indicates the rapidity of cell proliferation in cancer tissues , 2000, The Journal of pathology.

[19]  D. Hernandez-Verdun,et al.  Cyclin-dependent kinases govern formation and maintenance of the nucleolus , 2002, The Journal of cell biology.

[20]  R. Reeder,et al.  Transcription in cloned spacers of Xenopus laevis ribosomal DNA. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[21]  D. Hernandez-Verdun,et al.  The mitotically phosphorylated form of the transcription termination factor TTF-1 is associated with the repressed rDNA transcription machinery. , 1999, Journal of cell science.

[22]  R. Roeder,et al.  Ribosomal RNA synthesis in isolated nuclei. , 1972, Journal of molecular biology.

[23]  D. Jackson,et al.  Visualization of focal sites of transcription within human nuclei. , 1993, The EMBO journal.

[24]  Nicole Granboulan,et al.  Cytochimie ultrastructurale du nucléole: II. Étude des sites de synthèse du RNA dans le nucléole et le noyau , 1965 .

[25]  Dominique Ploton,et al.  Three-dimensional organization of active rRNA genes within the nucleolus. , 2002, Journal of cell science.

[26]  N. Mailand,et al.  Deregulated human Cdc14A phosphatase disrupts centrosome separation and chromosome segregation , 2002, Nature Cell Biology.

[27]  R. Benavente,et al.  Functional and dynamic aspects of the mammalian nucleolus , 1990, BioEssays : news and reviews in molecular, cellular and developmental biology.

[28]  B. Mayr,et al.  Species-specific non-expression of ribosomal RNA genes in a mammalian hybrid, the mule , 2004, Chromosoma.

[29]  Y. Nogi,et al.  Structural alterations of the nucleolus in mutants of Saccharomyces cerevisiae defective in RNA polymerase I , 1993, Molecular and cellular biology.

[30]  P. Shaw,et al.  The nucleolar architecture of polymerase I transcription and processing. , 1995, The EMBO journal.

[31]  T. Honjo,et al.  Preferential transcription of Xenopus laevis ribosomal RNA in interspecies hybrids between Xenopus laevis and Xenopus mulleri. , 1973, Journal of molecular biology.

[32]  R. McKay,et al.  A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. , 2002, Genes & development.

[33]  A. Schnapp,et al.  TIF‐IC, a factor involved in both transcription initiation and elongation of RNA polymerase I. , 1994, The EMBO journal.

[34]  D. Hernandez-Verdun,et al.  Emerging concepts of nucleolar assembly. , 2002, Journal of cell science.

[35]  R. Tjian,et al.  Assembly of alternative multiprotein complexes directs rRNA promoter selectivity. , 1990, Genes & development.

[36]  J. Windle,et al.  Upstream domains of the Xenopus laevis rDNA promoter are revealed in microinjected oocytes , 1986, Molecular and cellular biology.

[37]  R. Reeder,et al.  Regulation of RNA polymerase I transcription in yeast and vertebrates. , 1999, Progress in nucleic acid research and molecular biology.

[38]  D Ploton,et al.  Dynamics and three-dimensional localization of ribosomal RNA within the nucleolus. , 2000, RNA.

[39]  Prof. Dr. Asen A. Hadjiolov.  The Nucleolus and Ribosome Biogenesis , 1985, Cell Biology Monographs.

[40]  M Anastassova-Kristeva,et al.  The nucleolar cycle in man. , 1977, Journal of cell science.

[41]  Tom Misteli,et al.  The Dynamics of Postmitotic Reassembly of the Nucleolus , 2000, The Journal of cell biology.

[42]  I. Grummt.  Regulation of mammalian ribosomal gene transcription by RNA polymerase I. , 1999, Progress in nucleic acid research and molecular biology.

[43]  A. Blackler,et al.  Repression of nucleolar organizer activity in an interspecific hybrid of the genus Xenopus. , 1974, Developmental biology.

[44]  M. Dorée,et al.  Mitotic phosphorylation of the TBP-containing factor SL1 represses ribosomal gene transcription. , 1998, Journal of molecular biology.

[45]  L. Taylor,et al.  Activity of RNA polymerase I transcription factor UBF blocked by Rb gene product , 1995, Nature.

[46]  J. Sogo,et al.  Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle , 1989, Cell.

[47]  H. Spring,et al.  Structural organization of an active, chromosomal nucleolar organizer region (NOR) identified by light microscopy, and subsequent TEM and STEM electron microscopy , 2004, Chromosoma.

[48]  B. van Steensel,et al.  Fluorescent labeling of nascent RNA reveals transcription by RNA polymerase II in domains scattered throughout the nucleus , 1993, The Journal of cell biology.

[49]  J. Sogo,et al.  Replication of transcriptionally active chromatin , 1995, Nature.

[50]  M. Trendelenburg.  Morphology of ribosomal RNA cistrons in oocytes of the water beetle, Dytiscus marginalis L. , 2004, Chromosoma.

[51]  W. Bickmore,et al.  Human acrocentric chromosomes with transcriptionally silent nucleolar organizer regions associate with nucleoli , 2001, The EMBO journal.

[52]  David Tollervey,et al.  Making ribosomes. , 2002, Current opinion in cell biology.

[53]  D. Hernandez-Verdun,et al.  The rDNA transcription machinery is assembled during mitosis in active NORs and absent in inactive NORs , 1996, The Journal of cell biology.

[54]  I. Gonzalez,et al.  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. , 1992, Experimental cell research.

[55]  R. Tjian,et al.  Cloning of murine RNA polymerase I-specific TAF factors: conserved interactions between the subunits of the species-specific transcription initiation factor TIF-IB/SL1. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[56]  A. Gautier,et al.  Fixations et colorations , 1962 .

[57]  M. Nomura,et al.  Mutational Analysis of the Structure and Localization of the Nucleolus in the Yeast Saccharomyces cerevisiae , 1998, The Journal of cell biology.

[58]  D Hernandez-Verdun,et al.  The three-dimensional organization of ribosomal genes and the architecture of the nucleoli vary with G1, S and G2 phases. , 1995, Journal of cell science.

[59]  T. Cheutin,et al.  Three-dimensional organization of rDNA and transcription , 2004 .

[60]  I. Raška,et al.  Nonisotopic ultrastructural mapping of transcription sites within the nucleolus. , 1993, Experimental cell research.

[61]  H. Spring,et al.  Morphology of nucleolar cistrons in a plant cell, Acetabularia mediterranea. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[62]  K. Leiby,et al.  An electron microscopic method for localization of ribosomal proteins during transcription of ribosomal DNA: a method for studying protein assembly. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[63]  G. Längst,et al.  NoRC—a novel member of mammalian ISWI‐containing chromatin remodeling machines , 2001, The EMBO journal.

[64]  L. Rothblum,et al.  Domains of the rat rDNA promoter must be aligned stereospecifically , 1992, Molecular and cellular biology.

[65]  K. Smetana,et al.  A note to the demonstration of DNA in nuclei of blood cells in smear preparations. , 1967, Folia haematologica.

[66]  I. Raška,et al.  Fibrillar centres and condensed nucleolar chromatin in resting and stimulated human lymphocytes. , 1983, Zeitschrift fur mikroskopisch-anatomische Forschung.

[67]  U. Scheer,et al.  Localization of RNA polymerase I in interphase cells and mitotic chromosomes by light and electron microscopic immunocytochemistry. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[68]  A. Budde,et al.  Mitotic silencing of human rRNA synthesis: inactivation of the promoter selectivity factor SL1 by cdc2/cyclin B‐mediated phosphorylation , 1998, The EMBO journal.

[69]  S. Penman,et al.  Products of RNA polymerases in HeLa cell nuclei. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[70]  I. Raška,et al.  Immunocytochemistry of the cell nucleus. , 1990, Electron microscopy reviews.

[71]  M. Thiry,et al.  Localization of nucleolar chromatin by immunocytochemistry and in situ hybridization at the electron microscopic level. , 1991, Electron microscopy reviews.

[72]  U. Scheer,et al.  A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis , 1995, The Journal of cell biology.

[73]  I. Grummt,et al.  The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription , 2002, Nature Genetics.

[74]  R. Weinberg,et al.  The retinoblastoma protein and cell cycle control , 1995, Cell.

[75]  Ed Hurt,et al.  Pre-ribosomes on the road from the nucleolus to the cytoplasm. , 2003, Trends in cell biology.

[76]  Ivan Raska,et al.  Oldies but goldies: searching for Christmas trees within the nucleolar architecture. , 2003, Trends in cell biology.

[77]  Denis Hochstrasser,et al.  Functional proteomic analysis of human nucleolus. , 2002, Molecular biology of the cell.

[78]  I. Raška,et al.  Ultrastructural nonisotopic mapping of nucleolar transcription sites in onion protoplasts. , 1996, Journal of structural biology.

[79]  I. Raška,et al.  Immunocytochemical localization of RNA polymerase I in the fibrillar centers of nucleoli , 1987 .

[80]  W. Langridge,et al.  Alternative model for gene amplification. , 1971, Nature: New biology.

[81]  I. Raška,et al.  Analysis of ring-shaped nucleoli in serially sectioned human lymphocytes , 2004, Cell and Tissue Research.

[82]  I B Dawid,et al.  Repeated genes in eukaryotes. , 1980, Annual review of biochemistry.

[83]  M. Thiry,et al.  In situ hybridization at the electron microscope level: an improved method for precise localization of ribosomal DNA and RNA. , 1989, European journal of cell biology.

[84]  I. Grummt,et al.  Mechanism of repression of RNA polymerase I transcription by the retinoblastoma protein , 1997, Molecular and cellular biology.

[85]  I. Grummt,et al.  Cell cycle-dependent regulation of RNA polymerase I transcription: the nucleolar transcription factor UBF is inactive in mitosis and early G1. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[86]  Z. Chen,et al.  Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. , 1997, Genes & development.

[87]  P. Borst,et al.  Subnuclear localization of the active variant surface glycoprotein gene expression site in Trypanosoma brucei. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[88]  C. Pikaard,et al.  Uniting the paths to gene silencing , 2002, Nature Genetics.

[89]  U. Scheer.  Contributions of electron microscopic spreading preparations ("Miller spreads") to the analysis of chromosome structure. , 1987, Results and problems in cell differentiation.

[90]  G. Reimer,et al.  Does the synthesis of ribosomal RNA take place‐within nucleolar fibrillar centers or dense fibrillar components? , 1989, Biology of the cell.

[91]  M. Olson,et al.  Conventional and nonconventional roles of the nucleolus , 2002, International Review of Cytology.

[92]  R. Perry,et al.  RIBOSOME PRECURSOR PARTICLES IN NUCLEOLI , 1969, The Journal of cell biology.

[93]  Artem Pliss,et al.  Non-isotopic mapping of ribosomal RNA synthesis and processing in the nucleolus , 2001, Chromosoma.

[94]  I. Grummt,et al.  Phosphorylation of UBF at serine 388 is required for interaction with RNA polymerase I and activation of rDNA transcription , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[95]  I. Grummt.  Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. , 2003, Genes & development.

[96]  J. Sylvester,et al.  Human rDNA: evolutionary patterns within the genes and tandem arrays derived from multiple chromosomes. , 2001, Genomics.

[97]  M. Thiry,et al.  Re‐evaluation of the site of transcription in Ehrlich tumour cell nucleoli , 1985, Biology of the cell.

[98]  J. Gall.  Differential synthesis of the genes for ribosomal RNA during amphibian oögenesis. , 1968, Proceedings of the National Academy of Sciences of the United States of America.

[99]  R. Tjian,et al.  Purification and characterization of a transcription factor that confers promoter specificity to human RNA polymerase I , 1985, Molecular and cellular biology.

[100]  R. Tjian,et al.  Two distinct promoter elements in the human rRNA gene identified by linker scanning mutagenesis , 1986, Molecular and cellular biology.

[101]  T. Misteli.  A nucleolar disappearing act in somatic cloning , 2003, Nature Cell Biology.

[102]  M. Nomura,et 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 , 2003, Molecular and Cellular Biology.

[103]  D. Hernandez-Verdun,et al.  Regulators of nucleolar functions. , 2003, Progress in cell cycle research.

[104]  G. Goessens.  Nucleolar structure. , 1984, International review of cytology.

[105]  Z. Xue,et al.  The nucleolus: an organelle formed by the act of building a ribosome. , 1995, Current opinion in cell biology.

[106]  C. Cantor,et al.  Reversible changes in nucleosome structure and histone H3 accessibility in transcriptionally active and inactive states of rDNA chromatin , 1983, Cell.

[107]  T. Pederson,et al.  The plurifunctional nucleolus. , 1998, Nucleic acids research.

[108]  Y. Xiong,et al.  Control of p53 ubiquitination and nuclear export by MDM2 and ARF. , 2001, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[109]  V. Vogt,et al.  The ribosomal RNA gene cluster in aneuploid chickens: evidence for increased gene dosage and regulation of gene expression , 1985, The Journal of cell biology.

[110]  J. Warner,et al.  The economics of ribosome biosynthesis in yeast. , 1999, Trends in biochemical sciences.

[111]  S. Bell,et al.  The Xenopus ribosomal gene enhancers bind an essential polymerase I transcription factor, xUBF. , 1989, Genes & development.

[112]  D. Hernandez-Verdun,et al.  In Vivo Release of Mitotic Silencing of Ribosomal Gene Transcription Does Not Give Rise to Precursor Ribosomal RNA Processing , 2000, The Journal of cell biology.

[113]  P. Pandolfi,et al.  The nucleolus: at the stem of immortality , 2003, Nature Medicine.

[114]  T. Toda,et al.  Essential roles of the RNA polymerase I largest subunit and DNA topoisomerases in the formation of fission yeast nucleolus , 1989, The Journal of cell biology.

[115]  T Misteli,et al.  Protein dynamics: implications for nuclear architecture and gene expression. , 2001, Science.

[116]  H. Zentgraf,et al.  Different chromatin structures in Physarum polycephalum , 1981, Chromosoma.

[117]  J. Sogo,et al.  Chromatin structure and transcriptional activity around the replication forks arrested at the 3' end of the yeast rRNA genes , 1994, Molecular and cellular biology.

[118]  S. Smith,et al.  Rb and p130 regulate RNA polymerase I transcription: Rb disrupts the interaction between UBF and SL-1 , 2000, Oncogene.

[119]  I. Grummt,et al.  Molecular mechanisms mediating methylation-dependent silencing of ribosomal gene transcription. , 2001, Molecular cell.

[120]  L. Recher,et al.  The fine structure of a nucleolar constituent. , 1969, Journal of ultrastructure research.

[121]  S. Jacob.  Regulation of ribosomal gene transcription. , 1995, The Biochemical journal.

[122]  D. Granick.  Nucleolar necklaces in chick embryo fibroblast cells. II. Microscope observations of the effect of adenosine analogues on nucleolar necklace formation , 1975, The Journal of cell biology.

[123]  H. Busch.  The Cell Nucleus , 1966, Nature.

[124]  S. Fakan,et al.  Revealing the unseen: the organizer region of the nucleolus. , 2001, Journal of cell science.

[125]  W. Franke,et al.  Transcription of ribosomal RNA cistrons. Correlation of morphological and biochemical data. , 1973, Experimental cell research.

[126]  S. Ghosh,et al.  The nucleolar structure. , 1976, International review of cytology.

[127]  S. Fakan,et al.  Fine structural ribonucleoprotein components of the cell nucleus visualized after spreading and high resolution autoradiography , 1989, Chromosoma.

[128]  Deutsches Krebsforschungszentrum,et al.  Nucleocytoplasmic Transport , 1986, Springer Berlin Heidelberg.

[129]  F. Wachtler,et al.  The nucleolus: A structural and functional interpretation , 1993 .

[130]  U. Scheer.  Changes of nucleosome frequency in nucleolar and non-nucleolar chromatin as a function of transcription: an electron microscopic study , 1978, Cell.

[131]  G. Karpen,et al.  A Drosophila rRNA gene located in euchromatin is active in transcription and nucleolus formation. , 1988, Genes & development.

[132]  T. Misteli,et al.  A Kinetic Framework for a Mammalian RNA Polymerase in Vivo , 2002, Science.

[133]  K. Smetana,et al.  Chromatin structures in ring-shaped nucleoli of human lymphocytes. , 1968, Experimental cell research.

[134]  C. Pikaard,et al.  Epigenetic silencing of RNA polymerase I transcription , 2003, Nature Reviews Molecular Cell Biology.

[135]  M. Okuwaki,et al.  [Structure and function of the nucleolus]. , 2006, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[136]  I. Grummt,et al.  TFIIH Plays an Essential Role in RNA Polymerase I Transcription , 2002, Cell.

[137]  A. Budde,et al.  p53 represses ribosomal gene transcription , 1999, Oncogene.

[138]  S. Fakan.  Structural support for RNA synthesis in the cell nucleus. , 1986, Methods and achievements in experimental pathology.

[139]  J. Sinclair,et al.  The Relationship between Satellite Deoxyribonucleic Acid, Ribosomal Ribonucleic Acid Gene Redundancy, and Genome Size in Plants. , 1975, Plant physiology.

[140]  J. Warner,et al.  Does Saccharomyces need an organized nucleolus? , 1997, Chromosoma.

[141]  A. Schnapp,et al.  A growth‐dependent transcription initiation factor (TIF‐IA) interacting with RNA polymerase I regulates mouse ribosomal RNA synthesis. , 1990, The EMBO journal.

[142]  P. Shaw,et al.  Single ribosomal transcription units are linear, compacted Christmas trees in plant nucleoli. , 2001, The Plant journal : for cell and molecular biology.

[143]  S. Rogers,et al.  Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer , 1987, Plant Molecular Biology.

[144]  A. Schnapp,et al.  The nucleolar transcription factor mUBF is phosphorylated by casein kinase II in the C‐terminal hyperacidic tail which is essential for transactivation. , 1992, The EMBO journal.

[145]  M. Carmo-Fonseca,et al.  Dynamic association of RNA-editing enzymes with the nucleolus , 2003, Journal of Cell Science.

[146]  Localization of transcription in nucleoli of rat sympathetic neurons. A quantitative ultrastructural autoradiography study. , 1986, Journal of submicroscopic cytology.

[147]  M. Nomura,et al.  Transcription Factor UAF, Expansion and Contraction of Ribosomal DNA (rDNA) Repeats, and RNA Polymerase Switch in Transcription of Yeast rDNA , 1999, Molecular and Cellular Biology.

[148]  F. Wachtler,et al.  The uptake of uridine in the nucleolus occurs in the dense fibrillar component. Immunogold localization of incorporated digoxigenin-UTP at the electron microscopic level. , 1993, Cytogenetics and cell genetics.

[149]  M. Thiry,et al.  Distinguishing the sites of pre-rRNA synthesis and accumulation in Ehrlich tumor cell nucleoli. , 1991, Journal of cell science.

[150]  U. Scheer,et al.  Looking at christmas trees in the nucleolus , 1997, Chromosoma.

[151]  P. Biberfeld.  Morphogenesis in blood lymphocytes stimulated with phytohaemagglutinin (PHA). A light and electron microscopic study. , 1971, Acta pathologica et microbiologica Scandinavica. Supplement.

[152]  M. Thiry,et al.  Electron tomography of metaphase nucleolar organizer regions: evidence for a twisted-loop organization. , 1997, Molecular biology of the cell.

[153]  Nobuko Katoku-Kikyo,et al.  Reversible disassembly of somatic nucleoli by the germ cell proteins FRGY2a and FRGY2b , 2003, Nature Cell Biology.

[154]  I. Raška,et al.  Pre-ribosomal RNA is processed in permeabilised cells at the site of transcription. , 2000, European journal of cell biology.

[155]  I. Raška,et al.  Does the synthesis of ribosomal RNA take place within nucleolar fibrillar centers or dense fibrillar components? A critical appraisal. , 1995, Journal of structural biology.

[156]  B. Hamkalo,et al.  Visualization of genetic transcription. , 1973, Basic life sciences.

[157]  N. Maizels,et al.  Dictyostelium ribosomal RNA is processed during transcription , 1980, Cell.

[158]  J. C. Vuletin,et al.  A Light and Electron Microscopic Study , 1976 .

[159]  V. Vogt,et al.  Characterization of ribosomal RNA synthesis in a gene dosage mutant: the relationship of topoisomerase I and chromatin structure to transcriptional activity , 1987, The Journal of cell biology.

[160]  D. Jackson,et al.  Coupled Transcription and Translation Within Nuclei of Mammalian Cells , 2001, Science.

[161]  A. Pliss,et al.  Nuclear organization studied with the help of a hypotonic shift: its use permits hydrophilic molecules to enter into living cells , 1999, Chromosoma.

[162]  I. Grummt,et al.  The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription , 2002, The EMBO journal.

[163]  D. Hernandez-Verdun,et al.  The three-dimensional organization of ribosomal genes and the architecture of the nucleoli vary with G 1 , S and G 2 phases , 1995 .

[164]  M. Mann,et al.  Directed Proteomic Analysis of the Human Nucleolus , 2002, Current Biology.

[165]  P. Scalia,et al.  The Cell Cycle Regulatory Factor TAF1 Stimulates Ribosomal DNA Transcription by Binding to the Activator UBF , 2002, Current Biology.

[166]  M. Pébusque,et al.  Circadian rhythm of nucleoli in rat superior cervical ganglion neurons: the two types of fibrillar centres and their quantitative relationship with the nucleolar organizing regions. , 1985, Journal of Cell Science.

[167]  E M Manders,et al.  Numbers and organization of RNA polymerases, nascent transcripts, and transcription units in HeLa nuclei. , 1998, Molecular biology of the cell.

[168]  K. Smetana,et al.  Fibrillar center distribution in nucleoli of PHA-stimulated human lymphocytes. , 1989, Experimental cell research.