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The nucleolus: a model for the organization of nuclear functions

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Abstract

Nucleoli are the prominent contrasted structures of the cell nucleus. In the nucleolus, ribosomal RNAs (rRNAs) are synthesized, processed and assembled with ribosomal proteins. The size and organization of the nucleolus are directly related to ribosome production. The organization of the nucleolus reveals the functional compartmentation of the nucleolar machineries that depends on nucleolar activity. When this activity is blocked, disrupted or impossible, the nucleolar proteins have the capacity to interact independently of the processing activity. In addition, nucleoli are dynamic structures in which nucleolar proteins rapidly associate and dissociate with nucleolar components in continuous exchanges with the nucleoplasm. At the time of nucleolar assembly, the processing machineries are recruited in a regulated manner in time and space, controlled by different kinases and form intermediate structures, the prenucleolar bodies. The participation of stable pre-rRNAs in nucleolar assembly was demonstrated after mitosis and during development but this is an intriguing observation since the role of these pre-rRNAs is presently unknown. A brief report on the nucleolus and diseases is proposed as well as of nucleolar functions different from ribosome biogenesis.

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References

  • Adachi Y, Copeland TD, Hatanaka M, Oroszlan S (1993) Nucleolar targeting signal of Rex protein of human T-cell leukemia virus type I specifically binds to nucleolar shuttle protein B-23. J Biol Chem 268:13930–13934

    PubMed  CAS  Google Scholar 

  • Andersen JS, Lam YW, Leung AK, Ong SE, Lyon CE, Lamond AI, Mann M (2005) Nucleolar proteome dynamics. Nature 433:77–83

    PubMed  CAS  Google Scholar 

  • Angelier N, Tramier M, Louvet E, Coppey-Moisan M, Savino TM, De Mey JR, Hernandez-Verdun DD (2005) Tracking the interactions of rRNA processing proteins during nucleolar assembly in living cells. Mol Biol Cell 16:2862–2871

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Azum-Gélade MC, Noaillac-Depeyre J, Caizergues-Ferrer M, Gas N (1994) Cell cycle redistribution of U3 snRNA and fibrillarin. Presence in the cytoplasmic nucleolus remnant and in the prenucleolar bodies at telophase. J Cell Sci 107:463–475

    PubMed  Google Scholar 

  • Bertrand E, Houser-Scott F, Kendall A, Singer RH, Engelke DR (1998) Nucleolar localization of early tRNA processing. Genes Dev 12:2463–2468

    PubMed  CAS  Google Scholar 

  • Biggiogera M, Fakan S, Kaufmann SH, Black A, Shaper JH, Busch H (1989) Simultaneous immunoelectron microscopic visualization of protein B23 and C23 distribution in the HeLa cell nucleolus. J Histochem Cytochem 37:1371–1374

    PubMed  CAS  Google Scholar 

  • Bourgeois CA, Hubert J (1988) Spatial relationship between the nucleolus and the nuclear envelope: structural aspects and functional significance. Int Rev Cytol 111:1–52

    Article  PubMed  CAS  Google Scholar 

  • Brosh RM Jr, Karmakar P, Sommers JA, Yang Q, Wang XW, Spillare EA, Harris CC, Bohr VA (2001) p53 modulates the exonuclease activity of Werner syndrome protein. J Biol Chem 276:35093–35102

    PubMed  CAS  Google Scholar 

  • Carmo-Fonseca M, Mendes-Soares L, Campos I (2000) To be or not to be in the nucleolus. Nat Cell Biol 2:107–112

    Google Scholar 

  • Caspersson TO (1950) Cell growth and cell function. W.W. Norton and Co, New York, pp 85

    Google Scholar 

  • Chan PK, Qi Y, Amley J, Koller CA (1996) Quantitation of the nucleophosmin/B23-translocation using imaging analysis. Cancer Lett 100:191–197

    PubMed  CAS  Google Scholar 

  • Chen D, Huang S (2001) Nucleolar components involved in ribosome biogenesis cycle between the nucleolus and nucleoplasm in interphase cells. J Cell Biol 153:169–176

    PubMed  CAS  Google Scholar 

  • Chubb JR, Boyle S, Perry P, Bickmore WA (2002) Chromatin motion is constrained by association with nuclear compartments in human cells. Curr Biol 12:439–445

    PubMed  CAS  Google Scholar 

  • Clute P, Pines J (1999) Temporal and spatial control of cyclin B1 destruction in metaphase. Nat Cell Biol 1:82–87

    PubMed  CAS  Google Scholar 

  • Cmarko D, Verschure PJ, Rothblum LI, Hernandez-Verdun D, Amalric F, van Driel R, Fakan S (2000) Ultrastructural analysis of nucleolar transcription in cells microinjected with 5-bromo-UTP. Histochem Cell Biol 113:181–187

    PubMed  CAS  Google Scholar 

  • Cockell MM, Gasser SM (1999) The nucleolus: nucleolar space for rent. Curr Biol 9:R575–R576

    PubMed  CAS  Google Scholar 

  • Colau G, Thiry M, Leduc V, Bordonne R, Lafontaine DL (2004) The small nucle(ol)ar RNA cap trimethyltransferase is required for ribosome synthesis and intact nucleolar morphology. Mol Cell Biol 24:7976–7986

    PubMed  CAS  Google Scholar 

  • de la Cruz J, Kressler D, Linder P (2004) Ribosome subunit assembly. In: Olson MOJ (ed) The nucleolus. Landes, Biosciences/eurekah.com, Austin, pp 258–285

  • David-Pfeuty T, Nouvian-Dooghe Y, Sirri V, Roussel P, Hernandez-Verdun D (2001) Common and reversible regulation of wild-type p53 function and of ribosomal biogenesis by protein kinases in human cells. Oncogene 20:5951–5963

    PubMed  CAS  Google Scholar 

  • Desterro JM, Keegan LP, Lafarga M, Berciano MT, O’Connell M, Carmo-Fonseca M (2003) Dynamic association of RNA-editing enzymes with the nucleolus. J Cell Sci 116:1805–1818

    PubMed  CAS  Google Scholar 

  • Dousset T, Wang C, Verheggen C, Chen D, Hernandez-Verdun D, Huang S (2000) Initiation of nucleolar assembly is independent of RNA polmerase I transcription. Mol Biol Cell 11:2705–2717

    PubMed  CAS  Google Scholar 

  • Dragon F, Gallagher JE, Compagnone-Post PA, Mitchell BM, Porwancher KA, Wehner KA, Wormsley S, Settlage RE, Shabanowitz J, Osheim Y, Beyer AL, Hunt DF, Baserga SJ (2002) A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417:967–970

    PubMed  CAS  Google Scholar 

  • Dundr M, Olson MOJ (1998) Partially processed pre-rRNA is preserved in association with processing components in nucleolus derived foci during mitosis. Mol Biol Cell 9:2407–2422

    PubMed  CAS  Google Scholar 

  • Dundr M, Misteli T, Olson MOJ (2000) The dynamics of postmitotic reassembly of the nucleolus. J Cell Biol 150:433–446

    PubMed  CAS  Google Scholar 

  • Dundr M, Hebert MD, Karpova TS, Stanek D, Xu H, Shpargel KB, Meier UT, Neugebauer KM, Matera AG, Misteli T (2004) In vivo kinetics of Cajal body components. J Cell Biol 164:831–842

    PubMed  CAS  Google Scholar 

  • Emmett SR, Dove B, Mahoney L, Wurm T, Hiscox JA (2005) The cell cycle and virus infection. Methods Mol Biol 296:197–218

    PubMed  CAS  Google Scholar 

  • Fankhauser C, Izaurralde E, Adachi Y, Wingfield P, Laemmli UK (1991) Specific complex of human immunodeficiency virus type 1 rev and nucleolar B23 proteins: dissociation by the Rev response element. Mol Cell Biol 11:2567–2575

    PubMed  CAS  Google Scholar 

  • Fatica A, Tollervey D (2002) Making ribosomes. Curr Opin Cell Biol 14:313–318

    PubMed  CAS  Google Scholar 

  • Fomproix N, Gébrane-Younès J, Hernandez-Verdun D (1998) Effects of anti-fibrillarin antibodies on building of functional nucleoli at the end of mitosis. J Cell Sci 111:359–372

    PubMed  CAS  Google Scholar 

  • Fromont-Racine M, Senger B, Saveanu C, Fasiolo F (2003) Ribosome assembly in eukaryotes. Gene 313:17–42

    PubMed  CAS  Google Scholar 

  • Ganot P, Jady BE, Bortolin M-L, Darzacq X, Kiss T (1999) Nucleolar factors direct the 2’-O-ribose methylation and pseudouridylation of U6 spliceosomal RNA. Mol Cell Biol 19:6906–6917

    PubMed  CAS  Google Scholar 

  • Gautier T, Dauphin-Villemant C, André C, Masson C, Arnoult J, Hernandez-Verdun D (1992) Identification and characterization of a new set of nucleolar ribonucleoproteins which line the chromosomes during mitosis. Exp Cell Res 200:5–15

    PubMed  CAS  Google Scholar 

  • Gautier T, Fomproix N, Masson C, Azum-Gélade MC, Gas N, Hernandez-Verdun D (1994) Fate of specific nucleolar perichromosomal proteins during mitosis: cellular distribution and association with U3 snoRNA. Biol Cell 82:81–93

    PubMed  CAS  Google Scholar 

  • Gébrane-Younès J, Sirri V, Junéra HR, Roussel P, Hernandez-Verdun D (2005) Nucleolus: an essential nuclear domain. In: Hemmerich P, Diekmann S (eds) Visions of the cell nucleus. ASP, California, pp 120–135

    Google Scholar 

  • Géraud G, Laquerriere F, Masson C, Arnoult J, Hernandez-Verdun D (1989) Three-dimensional organization of micronuclei induced by colchicine in PtK1 cells. Exp Cell Res 181:27–39

    PubMed  Google Scholar 

  • Gerbi SA, Borovjagin AV (2004) Pre-ribosomal RNA processing in multicellular organisms. In: Olson MOJ (ed) The nucleolus. Landes, Biosciences/eurekah.com, Austin, pp. 170–198

  • Ginisty H, Amalric F, Bouvet P (1998) Nucleolin functions in the first step of ribosomal RNA processing. EMBO J 17:1476–1486

    PubMed  CAS  Google Scholar 

  • Goessens G, Thiry M, Lepoint A (1987) Relations between nucleoli and nucleolus-organizing regions during the cell cycle. Chromosomes Today 9:261–271

    Google Scholar 

  • Grandi P, Rybin V, Bassler J, Petfalski E, Strauss D, Marzioch M, Schafer T, Kuster B, Tschochner H, Tollervey D, Gavin AC, Hurt E (2002) 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol Cell 10:105–115

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Granick D (1975) Nucleolar necklaces in chick embryo fibroblast cells. II. Microscope observations of the effect of adenosine analogues on nucleolar necklace formation. J Cell Biol 65:418–427

    PubMed  CAS  Google Scholar 

  • Grisendi S, Bernardi R, Rossi M, Cheng K, Khandker L, Manova K, Pandolfi PP (2005) Role of nucleophosmin in embryonic development and tumorigenesis. Nature 437:147–153

    PubMed  CAS  Google Scholar 

  • Guarente L (2000) Sir2 links chromatin silencing, metabolism, and aging. Genes Dev 14:1021–1026

    PubMed  CAS  Google Scholar 

  • Guillot PV, Martin S, Pombo A (2005) The organization of transcription in the nucleus of mammalian cells. In: Hemmerich P, Diekmann S (eds) Visions of the cell nucleus. ASP, California, pp 95–105

    Google Scholar 

  • Haaf T, Ward DC (1996) Inhibition of RNA polymerase II transcription causes chromatin decondensation, loss of nucleolar structure, and dispersion of chromosomal domains. Exp Cell Res 224:163–173

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hadjiolov AA (1985) The nucleolus and ribosome biogenesis. Springer, Berlin Heidelberg New York, pp 1–268

    Google Scholar 

  • Hadjiolova KV, Hadjiolov A, Bachelerie J-P (1995) Actinomycin D stimulates the transcription of rRNA minigenes transfected into mouse cells. Applications for the in vivo hypersensitivity of rRNA gene transcription. Eur J Biochem 228:605–615

    CAS  Google Scholar 

  • Hatanaka M (1990) Discovery of the nucleolar targeting signal. Bioessays 12:143–148

    PubMed  CAS  Google Scholar 

  • Heiss NS, Girod A, Salowsky R, Wiemann S, Pepperkok R, Poustka A (1999) Dyskerin localizes to the nucleolus and its mislocalization is unlikely to play a role in the pathogenesis of dyskeratosis congenita. Hum Mol Genet 8:2515–2524

    PubMed  CAS  Google Scholar 

  • Heix J, Vente A, Voit R, Budde A, Michaelidis TM, Grummt I (1998) Mitotic silencing of human rRNA synthesis: inactivation of the promoter selectivity factor SL1 by cdc2/cyclin B-mediated phosphorylation. EMBO J 17:7373–7381

    PubMed  CAS  Google Scholar 

  • Herbert MD, Matera AG (2000) Self-association of coilin reveals a common theme in nuclear body localization. Mol Biol Cell 11:4159–4171

    Google Scholar 

  • Hernandez-Verdun D (2004) Behavior of the nucleolus during mitosis. In: Olson MOJ (ed) The nucleolus. Landes, Biosciences/eurekah.com, Austin, pp 41–57

    Google Scholar 

  • Hernandez-Verdun D, Junéra HR (1995) The nucleolus. In: Principles of medical biology, cellular organelles, vol. 2. Jai Press Inc., USA, pp 73–92

  • Hernandez-Verdun D, Bouteille M, Ege T, Ringertz NR (1979) Fine structure of nucleoli in micronucleated cells. Exp Cell Res 124:223–235

    PubMed  CAS  Google Scholar 

  • Hernandez-Verdun D, Robert-Nicoud M, Géraud G, Masson C (1991) Behaviour of nucleolar proteins in nuclei lacking ribosomal genes. A study by confocal laser scanning microscopy. J Cell Sci 98(Pt 1):99–105

    CAS  Google Scholar 

  • Herrera JE, Correia JJ, Jones AE, Olson MO (1996) Sedimentation analyses of the salt- and divalent metal ion-induced oligomerization of nucleolar protein B23. Biochemistry 35:2668–2673

    PubMed  CAS  Google Scholar 

  • Hiscox JA (2002) The nucleolus—a gateway to viral infection? Arch Virol 147:1077–1089

    PubMed  CAS  Google Scholar 

  • Hozàk P, Novak JT, Smetana K (1989) Three-dimensional reconstructions of nucleolus-organizing regions in PHA-stimulated human lymphocytes. Biol Cell 66:225–233

    PubMed  Google Scholar 

  • Hozàk P, Cook PR, Schöfer C, Mosgöller W, Wachtler F (1994) Site of transcription of ribosomal RNA and intranucleolar structure in HeLa cells. J Cell Sci 107:639–648

    PubMed  Google Scholar 

  • Isaac C, Marsh KL, Paznekas WA, Dixon J, Dixon MJ, Jabs EW, Meier UT (2000) Characterization of the nucleolar gene product, treacle, in Treacher Collins syndrome. Mol Biol Cell 11:3061–3071

    PubMed  CAS  Google Scholar 

  • Jarrous N, Wolenski D, Wesolowski D, Lee C, Altman S (1999) Localization in the nucleolus and coiled bodies of protein subunits of the ribonucleoprotein ribonuclease P. J Cell Biol 146:559–571

    PubMed  CAS  Google Scholar 

  • Jiménez-Garcia LF, Segura-Valdez MdL, Ochs RL, Rothblum LI, Hannan R, Spector DL (1994) Nucleologenesis: U3 snRNA-containing prenucleolar bodies move to sites of active pre-rRNA transcription after mitosis. Mol Biol Cell 5:955–966

    PubMed  Google Scholar 

  • Junéra HR, Masson C, Géraud G, Hernandez-Verdun D (1995) The three-dimensional organization of ribosomal genes and the architecture of the nucleoli vary with G1, S and G2 phases. J Cell Sci 108:3427–3441

    PubMed  Google Scholar 

  • Junéra HR, Masson C, Géraud G, Suja J, Hernandez-Verdun D (1997) Involvement of in situ conformation of ribosomal genes and selective distribution of UBF in rRNA transcription. Mol Biol Cell 8:145–156

    PubMed  Google Scholar 

  • Knibiehler B, Mirre C, Rosset R (1982) Nucleolar organizer structure and activity in a nucleolus without fibrillar centres: the nucleolus in an established Drosophila cell line. J Cell Sci 57:351–364

    PubMed  CAS  Google Scholar 

  • Knibiehler B, Mirre C, Navarro A, Rosset R (1984) Studies on chromatin organization in a nucleolus without fibrillar centres. Presence of sub-nucleolar structure in KCo cells of Drosophila. Cell Tissue Res 236:279–288

    PubMed  CAS  Google Scholar 

  • Kubota S, Siomi H, Satoh T, Endo S, Maki M, Hatanaka M (1989) Functional similarity of HIV-I rev and HTLV-I rex proteins: identification of a new nucleolar-targeting signal in rev protein. Biochem Biophys Res Commun 162:963–970

    PubMed  CAS  Google Scholar 

  • Labidi B, Broders F, Meyer JL, Hernandez-Verdun D (1990) Distribution of rDNA and 28S, 18S, and 5S rRNA in micronuclei containing a single chromosome. Biochem Cell Biol 68:957–964

    Article  PubMed  CAS  Google Scholar 

  • Le Panse S, Masson C, Héliot L, Chassery J-M, Junéra HR, Hernandez-Verdun D (1999) 3-D organization of single ribosomal transcription units after DRB inhibition of RNA polymerase II transcription. J Cell Sci 112:2145–2154

    CAS  Google Scholar 

  • Lippincott-Schwartz J, Snapp E, Kenworthy A (2001) Studying protein dynamics in living cells. Nat Rev Mol Cell Biol 2:444–456

    PubMed  CAS  Google Scholar 

  • Louvet E, Junéra HR, Le Panse S, Hernandez-Verdun D (2005) Dynamics and compartmentation of the nucleolar processing machinery. Exp Cell Res 304:457–470

    PubMed  CAS  Google Scholar 

  • Louvet E, Junéra HR, Berthuy I, Hernandez-Verdun D (2006) Compartmentation of the nucleolar processing proteins in the granular component is a CK2-driven process. Mol Biol Cell 17:2537–2546

    PubMed  CAS  Google Scholar 

  • Marciniak RA, Lombard DB, Johnson FB, Guarente L (1998) Nucleolar localization of the Werner syndrome protein in human cells. Proc Natl Acad Sci USA 95:6887–6892

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Meggio F, Pinna LA (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J 17:349–368

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Mosgoller W (2004) Nucleolar ultrastructure in vertebrates. In: Olson MOJ (ed) The nucleolus. Landes, Biosciences/eurekah.com, Austin, pp 10–20

    Google Scholar 

  • Ochs RL, Lischwe MA, Shen E, Caroll RE, Busch H (1985a) Nucleologenesis: composition and fate of prenucleolar bodies. Chromosoma 92:330–336

    CAS  Google Scholar 

  • Ochs RL, Lischwe MA, Spohn WH, Busch H (1985b) Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol Cell 54:123–134

    CAS  Google Scholar 

  • Okuwaki M, Tsujimoto M, Nagata K (2002) The RNA binding activity of a ribosome biogenesis factor, nucleophosmin/B23, is modulated by phosphorylation with a cell cycle-dependent kinase and by association with its subtype. Mol Biol Cell 13:2016–2030

    PubMed  CAS  Google Scholar 

  • Olson MOJ (2004) Nontraditional roles of the nucleolus. In: Olson MOJ (ed) The nucleolus. Landes, Biosciences/eurekah.com, Austin, pp 329–342

    Google Scholar 

  • Patterson GH, Lippincott-Schwartz J (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297:1873–1877

    PubMed  CAS  Google Scholar 

  • Pébusque MJ, Seïte (1981) Electron microscopic studies of silver-stained proteins in nucleolar organizer regions: location in nucleoli of rat sympathetic neurons during light and dark periods. J Cell Sci 51:85–94

    PubMed  Google Scholar 

  • Pederson T (1998) The plurifunctional nucleolus. Nucleic Acids Res 26:3871–3876

    PubMed  CAS  Google Scholar 

  • Perry RP (1962) The cellular sites of ribosomal and 4S RNA. Proc Natl Acad Sci USA 48:2179–2186

    PubMed  CAS  Google Scholar 

  • Pestov DG, Strezoska Z, Lau LF (2001) Evidence of p53-dependent cross-talk between ribosome biogenesis and the cell cycle: effects of nucleolar protein Bop1 on G(1)/S transition. Mol Cell Biol 21:4246–4255

    PubMed  CAS  Google Scholar 

  • Phair RD, Misteli T (2000) High mobility of proteins in the mammalian cell nucleus. Nature 404:604–609

    PubMed  CAS  Google Scholar 

  • Pinol-Roma S (1999) Association of nonribosomal nucleolar proteins in ribonucleoprotein complexes during interphase and mitosis. Mol Biol Cell 10:77–90

    PubMed  CAS  Google Scholar 

  • Politz JC, Yarovoi S, Kilroy SM, Gowda K, Zwieb C, Pederson T (2000) Signal recognition particle components in the nucleolus. Proc Natl Acad Sci USA 97:55–60

    PubMed  CAS  Google Scholar 

  • Politz JC, Lewandowski LB, Pederson T (2002) Signal recognition particle RNA localization within the nucleolus differs from the classical sites of ribosome synthesis. J Cell Biol 159:411–418

    PubMed  CAS  Google Scholar 

  • Puvion-Dutilleul F, Bachellerie J-P, Puvion E (1991) Nucleolar organization of HeLa cells as studied by in situ hybridization. Chromosoma 100:395–409

    PubMed  CAS  Google Scholar 

  • Puvion-Dutilleul F, Puvion E, Bachellerie J-P (1997) Early stages of pre-rRNA formation within the nucleolar ultrastructure of mouse cells studied by in situ hybridization with 5’ETS leader probe. Chromosoma 105:496–505

    PubMed  CAS  Google Scholar 

  • Raué HA (2004) Pre-ribosomal RNA processing and assembly in Saccharomyces cerevisiae: the machine that makes the machine. In: Olson MOJ (eds) The nucleolus. Landes, Biosciences/eurekah.com, Austin, pp 199–222

    Google Scholar 

  • Rego E, Ruggero D, Tribioli C, Gattoretti G, Kogan S, Redner R, Pandolfi PP (2006) Leukemia with distinct phenotypes in transgenic mice expressing PML/RARa, PLZF/RARa or NPM/RARa. Oncogene 25:1974–1979

    PubMed  CAS  Google Scholar 

  • Ritossa F, Spiegelman S (1965) Localization of DNA complementary to rRNA in the nucleolus organizer region of Drosophila melanogaster. Proc Natl Acad Sci USA 53:737–745

    PubMed  CAS  Google Scholar 

  • Roussel P, André 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 133:235–246

    PubMed  CAS  Google Scholar 

  • Rubbi CP, Milner J (2003) Disruption of the nucleolus mediates stabilization of p53 in response to DNA damage and other stresses. EMBO J 22:6068–6077

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Savino TM, Bastos R, Jansen E, Hernandez-Verdun D (1999) The nucleolar antigen Nop52, the human homologue of the yeast ribosomal RNA processing RRP1, is recruited at late stages of nucleologenesis. J Cell Sci 112:1889–1900

    PubMed  CAS  Google Scholar 

  • Savino TM, Gébrane-Younès J, De Mey J, Sibarita J-B, Hernandez-Verdun D (2001) Nucleolar assembly of the rRNA processing machinery in living cells. J Cell Biol 153:1097–1110

    PubMed  CAS  Google Scholar 

  • Scheer U, Benavente R (1990) Functional and dynamic aspects of the mammalian nucleolus. BioEssays 12:14–21

    PubMed  CAS  Google Scholar 

  • Scheer U, Hock R (1999) Structure and function of the nucleolus. Curr Opin Cell Biol 11:385–390

    PubMed  CAS  Google Scholar 

  • Scheer U, Rose KM (1984) Localisation of RNA polymerase I in interphase cells and mitotic chromosomes by light and electron microscopic immunocytochemistry. Proc Natl Acad Sci USA 81:1431–1435

    PubMed  CAS  Google Scholar 

  • Scheer U, Thiry M, Goessens G (1993) Structure, function and assembly of the nucleolus. Trends Cell Biol 3:236–241

    PubMed  CAS  Google Scholar 

  • Shav-Tal Y, Blechman J, Darzacq X, Montagna C, Dye BT, Patton JG, Singer RH, Zipori D (2005) Dynamic sorting of nuclear components into distinct nucleolar caps during transcriptional inhibition. Mol Biol Cell 16:2395–2413

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sirri V, Roussel P, Hernandez-Verdun D (2000) In vivo release of mitotic silencing of ribosomal gene transcription does not give rise to precursor ribosomal RNA processing. J Cell Biol 148:259–270

    PubMed  CAS  Google Scholar 

  • Sirri V, Hernandez-Verdun D, Roussel P (2002) Cyclin-dependent kinases govern formation and maintenance of the nucleolus. J Cell Biol 156:969–981

    PubMed  CAS  Google Scholar 

  • Snaar S, Wiesmeijer K, Jochemsen AG, Tanke HJ, Dirks RW (2000) Mutational analysis of fibrillarin and its mobility in living human cells. J Cell Biol 151:653–662

    PubMed  CAS  Google Scholar 

  • Sollner-Webb B, Tycowski KT, Steitz JA (1996) Ribosomal RNA processing in eukaryotes. In: Ribosomal RNA: structure, evolution, processing, and function in protein biosynthesis. CRC, New York, pp 469–490

  • Stevens B (1965) The fine structure of the nucleolus during mitosis in the grasshopper neuroblast cell. J Cell Biol 24:349–368

    PubMed  CAS  Google Scholar 

  • Strouboulis J, Wolffe AP (1996) Functional compartmentalization of the nucleus. J Cell Sci 109:1991–2000

    PubMed  CAS  Google Scholar 

  • Thiry M, Goessens G (1996) The nucleolus during the cell cycle. Springer, Berlin Heidelberg New York, pp 146

    Google Scholar 

  • Thiry M, Lafontaine DL (2005) Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol 15:194–199

    PubMed  CAS  Google Scholar 

  • Tollervey D (1996) Trans-acting factors in ribosome synthesis. Exp Cell Res 229:226–232

    PubMed  CAS  Google Scholar 

  • Tsai RY, McKay RD (2002) A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. Genes Dev 16:2991–3003

    PubMed  CAS  Google Scholar 

  • Tsai RY, McKay RD (2005) A multistep, GTP-driven mechanism controlling the dynamic cycling of nucleostemin. J Cell Biol 168:179–184

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Verheggen C, Le Panse S, Almouzni G, Hernandez-Verdun D (1998) Presence of pre-rRNAs before activation of polymerase I transcription in the building process of nucleoli during early development of Xenopus laevis. J Cell Biol 142:1167–1180

    PubMed  CAS  Google Scholar 

  • Verheggen C, Almouzni G, Hernandez-Verdun D (2000) The ribosomal RNA processing machinery is recruited to the nucleolar domain before RNA polymerase I during Xenopus laevis development. J Cell Biol 149:293–305

    PubMed  CAS  Google Scholar 

  • Visitin R, Amon A (2000) The nucleolus: the magician’s hat for cell cycle tricks. Curr Opin Cell Biol 12:372–377

    Google Scholar 

  • Weisenberger D, Scheer U (1995) A possible mechanism for the inhibition of ribosomal RNA gene transcription during mitosis. J Cell Biol 129:561–575

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank Myriam Barre for help in photographic work and A.L. Haenni for critical reading of the manuscript. This work was supported in part by grants from the Centre National de la Recherche Scientifique and the Association pour la Recherche sur le Cancer (Contracts 3303).

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  1. Nuclei and Cell Cycle, Institut Jacques Monod, CNRS, Université Paris VI, Université Paris VII, 2 place Jussieu, 75251, Paris Cedex 05, France

    Danièle Hernandez-Verdun

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  1. Danièle Hernandez-Verdun
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Correspondence to Danièle Hernandez-Verdun.

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Robert Feulgen Lecture presented at the 48th Symposium of the Society for Histochemistry in Stresa, Lake Maggiore, Italy, 7–10 September 2006.

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Hernandez-Verdun, D. The nucleolus: a model for the organization of nuclear functions. Histochem Cell Biol 126, 135–148 (2006). https://doi.org/10.1007/s00418-006-0212-3

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  • DOI: https://doi.org/10.1007/s00418-006-0212-3

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