Skip to main content
SpringerLink
Log in

The nucleolus

  • Review article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Nucleoli are the sites of biosynthesis of the ribosomal precursors. They contain may copies of the genes for the main rRNAs (18 S- and 28 S-rRNA) in the form of tandemly arranged repeats at the chromosomal nucleolar organizer regions (NORs). They also contain the small rRNA (5 S-rRNA) that is synthesized outside the nucleolus, specific nucleolar proteins, among them the factors and enzymes necessary for transcription and transcript processing, and the precursor units of the ribosomes. In man as in may vertebrate species, three main components of nucleoli, besides chromatin, can be detected: fibrillar centres (FC), dense fibrillar component (DCF), and granular component (GC). Within a nucleolus the FCs are in many cases situated in its central region. The DFc forms a network of strands surrounding the FCs, but may sometimes reach for out towards the periphery of the nucleolus. The GC is usually situated in the peripheral regions of the nucleolus. In cells with a low level of ribosomal biosynthesis the nucleoli are small, usually with a single FC and little surrounding DFC and GC (“ring-shaped nucleolus”). In active cells the DFC forms a large network enclosing several, sometimes up to hundreds of FCs, and the GC covers a large area in the periphery (“compact nucleoli”). In cells at the onset of a new stimulation, the DFC is very prominent whereas the FCs are few and small, and the GC is also not very extensive (“reticulate nucleoli”). In some special cell types that are very active other arrangements of the structural components are found. In Sertoli cells, for instance, only one nucleolus is found, or occasionally two, each with a single large FC and a distinct area of GC, both areas being engulfed by DFC intermingled with some peripheral GC. Immunocytological and in situ hybridization studies to localize the rRNA genes within the nucleolus have so far led to divergent results. Both fibrillar components, the FCs and the DFC, have been claimed as the most probable candiates. Transcription of rDNA and the subsequent early steps of ribosome biosynthesis are localized in the DFC, whereas later steps (mature rRNA, preribosomes) are localized in the GC. The FCs may also serve as sites for the preparation of the rDNA for transcription, and as a store for certain nucleolar proteins. During mitosis, parts of the nucleolar proteins remain at the NORs. A direct contact between the nucleolus and the nuclear envelope is frequently observed but is not dependent on nucleolar activity. The number of nucleoli per cell nucleus depends on the activity of the NORs and on the duration of the cell cycle. Intense activity combined with a long interphase leads to an association of the NORs and hence to a decrease in the number of nucleoli. In malignant cells, increased nucleoli are a sign of an increased ribosomal biogenesis, but need not be directly related to the degree of malignancy.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Benavente R, Krohne G, Schmidt-Zachmann MS, Hügle B, Franke WW (1984) Karyoskeletal proteins and the organization of the amphibian oocyte nucleus. J Cell Sci 1[Suppl]:161–186

    Google Scholar 

  • Benavente R, Rose KM, Reimer G, Hügle-Dörr B, Scheer U (1987) Inhibition of nucleolar reformation after microinjection of antibodies to RNA polymerase I into mitotic cells. J Cell Biol 105:1483–1491

    Google Scholar 

  • Benavente R, Reimer G, Rose KM, Huegle-Doerr B, Scheer U (1988) Nucleolar changes after microinjection of antibodies to RNA polymerase I into the nucleus of mammalian cells. Chromosoma 97:115–123

    Google Scholar 

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

    Google Scholar 

  • Biggiogera M, Buerki K, Kaufmann SH, Shaper JH, Gas N, Amalric F, Fakan S (1990) Nucleolar distribution of proteins B23 and nucleolin in mouse preimplantation embryos as visualized by immunoelectron microscopy. Development 110:1263–1270

    Google Scholar 

  • Biggiogera M, Kaufmann SH, Shaper JH, Gas N, Amalric F, Fakan S (1991) Distribution of nucleolar proteins B23 and nucleolin during mouse spermatogenesis. Chromosoma 100:162–172

    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

    Google Scholar 

  • Bourgeois CA, Hernandez-Verdun D, Hubert J, Bouteille M (1979) Silver staining of NORs in electron microscopy. Exp Cell Res 123:449–452

    Google Scholar 

  • Bourgeois CA, Hemon D, Bouteille M (1982) Changes in the nucleolus envelope region during interphase in synchronized TG cells. J Ultrastruct Res 68:328–340

    Google Scholar 

  • Brechard MP (1992) Analyse par autoradiographie quantitative ultrastructurale de la transcription des ARN ribosomique dans les cellules de Sertoli humaines. Diplome d'Etudes Aprofondies Reproduction-Développement, Univesity of Montpellier

  • Busch H, Smetana K (1970) The nucleolus. Academic Press, New York London

    Google Scholar 

  • Busch H, Lischwe MA, Michalik J, Puikwong CH, Busch RK (1982) Nucleolar proteins of special interest: silver-staining proteins B23 and C23, and antigens of human tumor nucleoli. In: Jordan EG, Cullis CA (eds) The nucleolus, Cambridge University Press, Cambridge, London, pp 43–71

    Google Scholar 

  • Buys CHCM, Osinga J (1980) Abundance of protein-bound sulfhydryl and disulfide groups at chromosomal nucleolus organizing regions. Chromosoma 77:1–11

    Google Scholar 

  • Cajal SR (1910) El nucleo de los celulas piramidales del cerebro humano y de algunos mamiferos. Trab Lab Invest Biol Madrid 8:27–62

    Google Scholar 

  • Cataldo C, Souchier C, Vasserot M, Calisti A, Vagner-Capodano AM, Stahl A (1985) Three-dimensional analysis of human oocytes in primordial follicles. Biol Cell 54:191–194

    Google Scholar 

  • Cataldo C, Souchier C, Stahl A (1988) Three dimensional ultrastucture and quantitative analysis of the human Sertoli cell nucleolus. Biol Cell 63:277–285

    Google Scholar 

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

    Google Scholar 

  • Conconi A, Sogo JM, Ryan CA (1992) Ribosomal gene clusters are uniquely proportioned between open and closed chromatin structures in both tomato leaf cells and exponentially growing suspension cultures. Proc Natl Acad Sci USA 89:5256–5260

    Google Scholar 

  • Cook PR (1991) The nucleoskeleton and the topology of replication. Cell 66:627–635

    Google Scholar 

  • Deltour R, Motte P (1990) The nucleolonema of plant and animal cells. Biol Cell 68:5–11

    Google Scholar 

  • Derenzini M, Ploton D (1991) Interphase nucleolar organizer regions in cancer cells. Int Rev Exp Pathol 32:149–192

    Google Scholar 

  • Derenzini M, Trere D (1991) Importance of interphase nucleolar organizer regions in tumor pathology. Virchows Arch [B] 61:1–8

    Google Scholar 

  • Derenzini M, Hernandez-Verdun D, Bouteille M (1982) Visualization in situ of extended DNA filaments in nucleolar chromatin of rat hepatocytes. Exp Cell Res 141:463–469

    Google Scholar 

  • Derenzini M, Farabegolli F, Pession A, Novello F (1987) Spatial redistribution of ribosomal chromatin in the fibrillar centres of human circulating lymphocytes after stimulation of transcription. Exp Cell Res 170:31–41

    Google Scholar 

  • Derenzini M, Thiry M, Goessens G (1990) Ultrasructural cytochemistry of the mammalian cell nucleus. J Histochem Cytochem 38:1237–1256

    Google Scholar 

  • Derenzini M, Pession A, Trere D (1991) Siver stained nucleolar organizer regions in cancer cells — reply. Lab Invest 64:718–719

    Google Scholar 

  • Derenzini M, Farabegoli F, Trere D (1993) Localization of DNA in the fibrillar components of the nucleolus: a cytochemical and morphometric study. J Histochem Cytochem 41:829–836

    Google Scholar 

  • Earnshaw WC, Bernat RL (1991) Chromosomal passengers: toward an integrated view of mitosis. Chromosoma 100:139–146

    Google Scholar 

  • Egan MJ, Crocker J (1992) Nucleolar organiser regions in pathology. Br J Cancer 65:1–7

    Google Scholar 

  • Ellinger A, Wachtler F (1980) Über eine Methode zur Darstellung des Nucleolus im Licht- und Elektronenmikroskop. Mikroskopie 36:330–335

    Google Scholar 

  • Escande-Geraud ML, Azum MC, Tichadou JL, Gas N (1985) Correlation between rDNA transcription and distribution of a 100 kD nucleolar protein in CHO-cells. Exp Cell Res 161:353–363

    Google Scholar 

  • Estable C, Sotelo JR (1950) Una nueva estructura celular: el nucleolonema. Publ Inst Invest Cien Biol Montevideo 1:105–126

    Google Scholar 

  • Fakan S, Puvion S (1980) Ultrastructural visualization of nucleolar and extranucleolar RNA synthesis and distribution. Int Rev Cytol 65:255–299

    Google Scholar 

  • Ferguson-Smith MA, Handmaker SD (1961) Observations on the satellited human chromosomes. Lancet I: 638

    Google Scholar 

  • Fischer D, Weisenberger D, Scheer U (1991) Review: assigning functions to nucleolar structures. Chromosoma 101:133–140

    Google Scholar 

  • Flavell RB (1986) The structure and control of expression of ribosomal RNA genes. Oxford Surv Plant Mol Cell Biol 3:251–274

    Google Scholar 

  • Franke WW, Kleinschmidt JA, Spring H, Krohne G, Grund C, Trendelenburg MF, Stoehr M, Scheer U (1981) A nucleolar skeleton of protein filaments demonstrated in amplified nucleoli of Xenopus laevis. J Cell Biol 90:289–299

    Google Scholar 

  • Gas N, Escande ML, Stevens BJ (1985) Immunolocalization of the 100-kDa nucleolar protein during the mitotic cycle in CHO cells. Biol Cell 53:209–218

    Google Scholar 

  • Gautier T, Masson C, Quintana C, Arnoult J, Hernandez-Verdun D (1992a) The ultrastructure of the chromosome periphery in human cell lines. An in situ study using cryomethods in electron microscopy. Chromosoma 101:502–510

    Google Scholar 

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

    Google Scholar 

  • Gautier T, Robert-Nicoud M, Guilly MN, Hernandez-Verdun D (1992c) Relocation of nucleolar proteins around chromosomes at mitosis. A study by confocal laser scanning microscopy. J Cell Sci 102:729–737

    Google Scholar 

  • Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H (1984) Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 133:1710–1715

    Google Scholar 

  • Ghosh S, Paweletz N (1990) Localization of ribosomal cistrons at the ultrastructural level by in situ hybridization technique. Cell Biol Int Rep 14:521–525

    Google Scholar 

  • Goessens G (1984) Nucleolar structure. Int Rev Cytol 87:107–158

    Google Scholar 

  • Goessens G, Lepoint A (1974) The fine structure of the nucleolus during interphase and mitosis in Ehrlich tumour cells cultivated in vitro. Exp Cell Res 87:63–72

    Google Scholar 

  • Goessens G, Lepoint A (1982) Localization of Ag-NOR-proteins in Ehrlich tumor cell nucleoli. Biol Cell 43:139–142

    Google Scholar 

  • Gonzales MF, Wichmann I, Yelamos J, Melero J, Magarino R, Sanchez-Roman J, Nunez-Roldan A, Sanchez B (1992) A human monoclonal autoantibody to a nucleolar structure. Clin Exp Immunol 88:324–328

    Google Scholar 

  • Gonzales SP, Nardone RM (1968) Cyclic nucleolar changes during the cell cycle I. Variations in number, size, morphology and position. Exp Cell Res 50:599–615

    Google Scholar 

  • Goodpasture C, Bloom SE (1975) Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma 53:37–50

    Google Scholar 

  • Granboulan N, Granboulan P (1965) Cytochimie ultrastructurale du nucléole. II. Etude des sites de synthese du RNA dans le nucléole et le noyau. Exp Cell Res 38:604–619

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Hartung M, Mirre C, Stahl A (1979) Nucleolar organizers in human oocytes at meiotic prophase I studied by the silver NOR-method and electron microscopy. Hum Genet 52:295–308

    Google Scholar 

  • Hartung M, Wachtler F, Lanversin A, Fouet C, Schwarzacher HG, Stahl A (1990) Sequential changes in the nucleoli of human spermatogonia with special reference to rDNA location and transcription. Tissue Cell 22:25–27

    Google Scholar 

  • Heitz E (1931) Die Ursache der gesetzmäßigen Zahl, Lage, Form und Größe pflanzlicher Nucleolen. Planta 12:775–844

    Google Scholar 

  • Hernandez Verdun D (1991) The nucleolus today. J Cell Sci 99:465–471

    Google Scholar 

  • Hernandez-Verdun D, Hubert J, Bourgeois CA, Bouteille M (1980) Ultrastructural localization of Ag-NOR stained proteins in the nucleolus during cell cycle and in other nucleolar structures. Chromosoma 79:349–362

    Google Scholar 

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

    Google Scholar 

  • Heslop-Harrison JS, Mosgoeller W, Schwarzacher T, Leitch AR (1991) Volumes and positions of chromosomes in reconstructions of fibroblasts. Am J Hum Genet [Suppl] 49:380

    Google Scholar 

  • Howell WM, Denton TE, Diamond JR (1975) Differential staining of satellite regions of human acrocentric chromosomes. Experientia 31:260–262

    Google Scholar 

  • Hozak P, Zatsepina O, Vasilyeva I, Chentsov Y (1986) An electron microscopic study of nucleolus organizing regions at some stages of the cell cycle (G0 period, G2 period, mitosis). Biol Cell 57:197–206

    Google Scholar 

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

    Google Scholar 

  • Hozak P, Geraud G, Hernandez-Verdun D (1992) Revealing nucleolar architecture by low ionic strength treatment. Exp Cell Res 203:128–133

    Google Scholar 

  • Hozak P, Schoefer C, Sylvester J, Wachtler F (1993) A study on nucleolar DNA: isolation of DNA from fibrillar components and ultrastructural localization of different DNA probes. J Cell Sci 104:1199–1205

    Google Scholar 

  • Hsu TC, Brinkley BR, Arrighi FD (1967) The structure and behavior of the nucleolar organizers in mammalian cells. Chromosoma 23:137–153

    Google Scholar 

  • Hubbell HR, Lau YF, Brown RL, Hsu TC (1979) Cell cycle analysis and drug inhibition studies of silver staining in synchronous Hela-cells. Exp Cell Res 129:139–147

    Google Scholar 

  • Huegle B, Hazan R, Scheer U, Franke WW (1985) Localization of ribosomal protein S1 in the granular component of the interphase nucleolus and its distribution during mitosis. J Cell Biol 100:873–886

    Google Scholar 

  • Ingle J, Sinclair J (1972) Ribosomal RNA genes and plant development. Nature 235:30–32

    Google Scholar 

  • Jackson DA, Cook PR (1988) Visualization of a nucleoskeleton with a 23-nm axial repeat. EMBO J 7:3667–3677

    Google Scholar 

  • Johnson RT, Rao PN (1970) Mammalian cell fusion: induction of premature chromosome condensation in interphase nuclei. Nature 226:712–722

    Google Scholar 

  • Jordan EG (1979) The nucleolus at Weimar. Nature 281:529–530

    Google Scholar 

  • Jordan EG (1987) Nucleolar organizers in plants. In: Stahl A, Luciani JM, Vagner-Capodano AM (eds) Chromosomes today, vol 9. Allen & Unwin, London, pp 272–283

    Google Scholar 

  • Jordan EG (1991) Interpreting nucleolar structure: where are the transcribing genes? J Cell Sci 98:437–442

    Google Scholar 

  • Jordan EG, McGovern JH (1981) The quantitative relationship of the fibrillar centers and other nucleolar components to changes in growth conditions, serum deprivation and low doses of actinomycin D in cultured diploid human fibroblasts (strain MRCS) J Cell Sci 52:373–389

    Google Scholar 

  • Jordan EG, Rawlins DJ (1990) Three-dimensional localisation of DNA in the nucleolus of Spirogyra by correlated optical tomography and serial ultra-thin sectioning. J Cell Sci 95:343–352

    Google Scholar 

  • Jordan EG, Zatsepina O, Shaw PJ (1992) Widely dispersed DNA within plant and animal nucleoli visualised by 3-D fluorescence microscopy. Chromosoma 101:478–482

    Google Scholar 

  • Kaneko S, Ishida T, Sugio K, Yokoyama H, Sugimachi K (1991) Nucleolar organizer regions as a prognostic indicator for stage-I non-small-cell lung cancer. Cancer Res 51:4008–40

    Google Scholar 

  • Kaplan FS, Murray J, Sylvester JE, Gonzalez IL, O'Connor P, Doering JL, Muenke M, Zasloff MA (1992) A repetitive element map of the nucleolus. Genomics 15:123–132

    Google Scholar 

  • Kass S, Tyc K, Steitz JA, Sollner-Webb B (1990) The U3 small nucleolar ribonucleoprotein functions in the 1st step of preribosomal RNA processing. Cell 60:897–908

    Google Scholar 

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

    Google Scholar 

  • Lapeyre B, Bourbon H, Amalric F (1987) Nucleolin, the major nucleolar protein of growing eukaryotic cells: an unusual protein structure revealed by the nucleotide sequence. Proc Natl Acad Sci USA 84:1472–1476

    Google Scholar 

  • Lavelle A, Lavelle FW (1970) Cytodifferentiation in the neuron. In: Himwich WA (ed) Developmental neurobiology. Thomas, Springfield, Ill

    Google Scholar 

  • Leitch AR, Mosgoeller W, Shi M, Heslop-Harrison JS (1992) Different patterns of rDNA organization at interphase in nuclei of wheat and rye. J Cell Sci 101:751–757

    Google Scholar 

  • Leydig F (1852) Anatomische Notizen ueber Synapta digitata. Arch Anat Physiol Wiss Med: 507–519

  • Manuelidis L, Chen TL (1990) A unified model of eukaryotic chromosomes. Cytometry 11:8–25

    Google Scholar 

  • Marinesco G (1905) Recherches sur le noyau et le nucléole de la cellule nerveuse à l'état normal et pathologique. J Psychol Neurol 5:151–172

    Google Scholar 

  • Martin M, Moreno Diaz dela Espina S, Medina FJ (1989) Immunolocalization of DNA at nucleolar structural components in onion cells. Chromosoma 98:368–377

    Google Scholar 

  • Martin M, Garcia-Fernandez LF, Moreno Diaz dela Espina S, Noaillac-Depeyre J, Gas N, Medina FJ (1992) Identification and localization of a nucleolin homologue in onion nucleoli. Exp Cell Res 199:74–84

    Google Scholar 

  • Matsui S, Sasaki M (1973) Differential staining of nucleolus organizers in mammalian chromosomes. Nature 246:148–150

    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 

  • Medina FJ (1989) The nucleolus in the spotlight. Meeting on the nucleolus, Toledo (Spain), December 15–18, 1988. Eur J Cell Biol 50:244–246

    Google Scholar 

  • Medina FJ, Solanilla EL, Sanchez-Pina MA, Fernandez-Gomez ME, Risueno MC (1986) Cytological approach to the nucleolar functions detected by silver staining. Chromosoma 94:259–266

    Google Scholar 

  • Mirre C, Stahl A (1978) Ultrastructure and activity of the nucleolar organizer in the mouse oocyte during meiotic prophase. J Cell Sci 31:79–100

    Google Scholar 

  • Mirre C, Stahl A (1981) Ultrastructural organization, sites of transcription and distribution of fibrillar centers in the nucleolus of the mouse oocyte. J Cell Sci 48:105–126

    Google Scholar 

  • Montgomery TH (1899) Comparative cytological studies with especial regard to the morphology of the nucleolus. J Morphol 15:265–283

    Google Scholar 

  • Moreno FJ, Rodrigo RM, Garcia-Herdugo G (1990) Ag-NOR proteins and rDNA transcriptional activity in plant cells. J Histochem Cytochem 38:1879–1887

    Google Scholar 

  • Morita M, Kuwano H, Matsuda H, Moriguchi S, Sugimachi K (1991) Prognostic significance of argyrophilic nucleolar organizer regions in esophageal carcinoma. Cancer Res 51:5339–5341

    Google Scholar 

  • Mosgoeller W, Monschein H, Wachtler F, Schwarzacher HG (1991a) Über den Uridineinbau in Nukleolen von Lymphozyten des menschlichen peripheren Blutes. Anat Anz [Suppl] 168:277–278

    Google Scholar 

  • Mosgoeller W, Leitch AR, Brown JKM, Heslop-Harrison JS (1991b) Chromosome arrangements in human fibroblasts at mitosis. Hum Genet 88:27–33

    Google Scholar 

  • Mosgoeller W, Schoefer C, Wachtler F, Fliesser M, Mueller M, Schwarzacher HG (1992) Localization of polymerase I and its activity in human nucleoli. Eur J Cell Biol [Suppl 36] 57:56

    Google Scholar 

  • Mosgoeller W, Schoefer C, Derenzini M, Steiner M, Maier U, Wachtler F (1993) Distribution of DNA in human Sertoli cells nucleoli. J Histochem Cytochem 41:1487–1493

    Google Scholar 

  • Motte P, Deltour R, Mosen H, Bronchart R (1988) Three-dimensional electron microscopy of the nucleolus and nucleolus-associated chromatin (NAC) during early germination of Zea mays L. Biol Cell 62:65–81

    Google Scholar 

  • Negri C, Chiese R, Cerino A, Bestagno M, Sala C, Zini N, Maraldi NM, Astaldi-Ricotti GCB (1992) Monoclonal antibodies to human DNA topoisomerase I and the two isoforms of topoisomerase II: 170- and 180-kDA isozymes. Exp Cell Res 200:452–459

    Google Scholar 

  • Noel JS, Dewey WC, Abel JH, Thompson RP (1971) Ultrastructure of the nucleolus during Chinese hamster cell cycle. J Cell Biol 49:830–847

    Google Scholar 

  • Ochs RL, Smetana K (1991) Detection of fibrillarin in nucleolar remnants and the nucleolar matrix. Exp Cell Res 197:183–190

    Google Scholar 

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

    Google Scholar 

  • Olert J, Sawatzki G, Kling H, Gebauer J (1979) Cytological and histochemical studies on the mechanism of selective silver staining of nucleolus organizer regions (NORs). Histochemistry 60:91–99

    Google Scholar 

  • Paweletz N, Risueno MC (1982) Transmission-electron-microscopic studies on the mitotic cycle of nucleolar proteins impregnated with silver. Chromosoma 85:261–273

    Google Scholar 

  • Pebusque MJ, Robaglia A, Seite R (1981) Diurnal rhythm of nucleolar volume in sympathetic neurons of the rat superior cervical ganglion. Eur J Cell Biol 24:128–130

    Google Scholar 

  • Petrzilka GE, Schroeder HE (1979) Activation of human Tlymphocytes. A kinetic and stereological study. Cell Tissue Res 201:101–127

    Google Scholar 

  • Pischinger A (1926) Die Lage des isoelektrischen Punktes histologischer Elemente als Ursache ihrer verschiedenen Färbbarkeit. Z Zellforsch Mikrosk Anat 3:167–197

    Google Scholar 

  • Ploton D, Bendayan M, Adnet JJ (1983) Ultrastructural localization of Ag-NOR proteins and nucleic acids in reticulated nucleoli. Biol Cell 49:29–34

    Google Scholar 

  • Popp W, Wachtler F (1983) Changes in nucleolar structure, number and size in cellular activation and inactivation. Cell Tissue Res 234:377–388

    Google Scholar 

  • Popp W, Braun O, Wachtler F, Mosgöller W, Holzner JJ (1993) Nucleolar silver staining patterns and HLA-DR antigen expression in bronchial epithelial cells in chronic bronchitis. Pathol Res Pract 188:852–855

    Google Scholar 

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

    Google Scholar 

  • Raska I, Dundr M (1992) Compartmentalization of the cell nucleus: case of the nucleolus. Chromosomes Today 11:101–119

    Google Scholar 

  • Raska I, Reimer G, Jarnik M, Kostrouch Z, Raska K (1989) Does the synthesis of ribosomal RNA take place within nucleolar fibrillar centers or dense fibrillar components? Biol Cell 65:79–82

    Google Scholar 

  • Rawlins DJ, Shaw PJ (1990) Three-dimensional organization of ribosomal DNA in interphase nuclei of Pisum sativum by in situ hybridization and optical tomography. Chromosoma 99:143–151

    Google Scholar 

  • Reeder RH (1990) rRNA synthesis in the nucleolus. Trends Genet 6:390–395

    Google Scholar 

  • Reimer G, Raska I, Tan EM, Scheer U (1987) Human autoantibodies: probes for nucleolus structure and function. Virchows Arch [B] 54:131–143

    Google Scholar 

  • Rendon MC, Rodrigo RM, Goenechea LG, García-Herdugo G, Valdivia MM, Moreno FJ (1992) Characterization and immunolocalization of a nucleolar antigen with anti-NOR serum in Hela cells. Exp Cell Res 200:393–403

    Google Scholar 

  • Risueno MC, Medina FJ, Moreno Diaz de la Espina S (1982) Nucleolar fibrillar centres in plant meristematic cells: ultrastructure, cytochemistry and autoradiography. J Cell Sci 58:313–329

    Google Scholar 

  • Robaglia A, Seite R (1985) Changes in nucleoli and nucleolar fibrillar centers of chromaffin cells in rat adrenal medulla over 24-h period: an ultrastructural and stereological analysis. J Cell Sci 77:255–262

    Google Scholar 

  • Robert-Fortel I, Junéra HR, Géraud G, Hernandez-Verdun D (1993) Three-dimensional organization of ribosomal genes and Ag-NOR proteins during interphase and mitosis in PtK1 cells studied by confocal microscopy. Chromosoma 102:146–157

    Google Scholar 

  • Rodrigo RM, Rendón MC, Torreblanca J, Garcia-Herdugo G, Moreno FJ (1992) Characterization and immunolocalization of RNA polymerase I transcription factor UBF with anti-NOR serum in protozoa, higher plants and vertebrate cells. J Cell Sci 103:1053–1063

    Google Scholar 

  • Royal A, Simard R (1975) RNA-synthesis in the ultrastructural and biochemical components of the nucleolus of Chinese hamster ovary cells. J Cell Biol 66:577–585

    Google Scholar 

  • Ruzicka V (1899) Zur Geschichte und Kenntnis der feineren Structur der Nucleolen centraler Nervenzellen. Anat Anz 16:557–563

    Google Scholar 

  • Schedle A, Willheim M, Zeitelberger A, Gessl A, Frauendorfer K, Schoefer C, Wachtler F, Schwarzacher HG, Boltz-Nitulescu G (1992) Nucleolar morphology and rDNA in situ hybridization in monocytes. Cell Tissue Res 269:473–480

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Scheer U, Huegle B, Hazan R, Rose KM (1984) Drug induced dispersal of transcribed rRNA genes and transcriptional products: immunolocalization and silver staining of different nucleolar components in rat cells treated with 5,6-dichloro-β-ribofuranosylbenzimidazole. J Cell Biol 99:672–679

    Google Scholar 

  • Schmidt-Zachmann MS, Huegle-Doerr B, Franke WW (1987) A constitutive nucleolar protein identified as a member of the nucleoplasm family. EMBO J 6:1881–1890

    Google Scholar 

  • Schnedl W, Schnedl M (1972) Nucleoluszahl und -größe während des Zellzyklus. Z Zellforsch Mikrosk Anat 126:374–382

    Google Scholar 

  • Schoefer C, Wachtler F, Mosgoeller W, Hozak P, Stahl A, Derenzini M, Sylvester J, Schwarzacher HG (1992) Localization of DNA in the nucleolus of human Sertoli cells. Eur J Cell Biol [Suppl 36] 57:70

    Google Scholar 

  • Schoefer C, Mueller M, Leitner MD, Wachtler F (1993) The uptake of uridine in the nucleolus occurs in the dense fibrillar component. Immuno-gold localization of incorporated digoxigenin-UTP at the electron microscopic level. Cytogenet Cell Genet 64:27–30

    Google Scholar 

  • Schwarzacher HG, Wachtler F (1983) Nucleolus organizer regions and nucleoli. Hum Genet 63:89–99

    Google Scholar 

  • Schwarzacher HG, Wachtler F (1991) The functional significance of nucleolar structures. Ann Genet 34:151–160

    Google Scholar 

  • Schwarzacher HG, Mikelsaar AV, Schnedl W (1978) The nature of Ag-staining of nucleolus organizer regions. Cytogenet Cell Genet 20:24–39

    Google Scholar 

  • Shi L, Zumei N, Shi Z, Ge W, Yang Y (1987) Involvement of a nucleolar component, perichromonucleolin, in the condensation and decondensation of chromosomes. Proc Natl Acad Sci USA 84:7953–7956

    Google Scholar 

  • Sigmund J, Schwarzacher HG, Mikelsaar AV (1979) Satellite association frequency and number of nucleoli depend on cell cycle duration and NOR activity. Hum Genet 50:81–91

    Google Scholar 

  • Smetana K (1980) Nucleoli in maturing blood cells. In: Roath S (ed) Topical reviews in hematology. Academic Press, New York, pp 73–147

    Google Scholar 

  • Smetana K, Busch H (1974) The nucleolus and nucleolar DNA. In: Busch H (ed) The cell nucleus. Academic Press, New York, pp 75–147

    Google Scholar 

  • Sollner-Webb B, Mougey EB (1991) News from the nucleolus: rRNA gene expression. Trends Biochem Sci 16:58–62

    Google Scholar 

  • Srivastava AK, Schlessinger D (1991) Structure and organization of ribosomal DNA. Biochimie 73:631–638

    Google Scholar 

  • Stahl A (1982) The nucleolus and nucleolar chromosomes. In: Jordan EG, Cullis CA (eds) The nucleolus. Cambridge University Press, Cambridge, pp 1–24

    Google Scholar 

  • Stahl A, Wachtler F, Hartung M, Devictor M, Schoefer C, Mosgoeller W, Delanversin A, Fouet C (1991) Nucleoli, nucleolar chromosomes and ribosomal genes in the human spermatocyte. Chromosoma 101:231–244

    Google Scholar 

  • Sylvester JE, Whiteman DA, Podolsky R, Pozsgay J, Respess J, Schmickel RD (1986) The human ribosomal RNA genes: structure and organization of the complete repeating unit. Hum Genet 73:193–198

    Google Scholar 

  • Tesarik J, Kopecny V, Plachot M, Mandelbaum J (1987) High resolution autoradiographic localization of DNA-containing sites and RNA synthesis in developing nucleoli of human preimplantation embryos: a new concept of embryonic nucleologenesis. Development 101:777–791

    Google Scholar 

  • Testillano PS, Sánchez-Pina MA, López-Iglesias C, Olmedilla A, Christensen ME, Risueno MC (1992) Distribution of B-36 nucleolar protein in relation to transcriptional activity in plant cells. Chromosoma 102:41–49

    Google Scholar 

  • Thiry M (1988) Study of RNA distribution in the nucleolar components of Ehrlich cell using RNAse-gold method. Histochemistry 89:231–236

    Google Scholar 

  • Thiry M (1991a) DNase I-sensitive sites within the nuclear architecture visualized by immunoelectron microscopy. DNA Cell Biol 10:169–180

    Google Scholar 

  • Thiry M (1991b) In situ nick translation at the electron microscopic level: a tool for studying the location of DNaseI-sensitive regions within the cell. J Histochem Cytochem 39:871–874

    Google Scholar 

  • Thiry M (1992a) Ultrastructural detection of DNA within the nucleolus by sensitive molecular immunocytochemistry. Exp Cell Res 200:135–144

    Google Scholar 

  • Thiry M (1992b) New data concerning the functional organization of the mammalian cell nucleolus: detection of RNA and rRNA by in situ molecular immunocytochemistry. Nucleic Acids Res 20:6195–6200

    Google Scholar 

  • Thiry M (1993) Ultrastructural distribution of DNA and RNA within the nucleolus of human Sertoli cells as seen by molecular immunocytochemistry. J Cell Sci 105:33–39

    Google Scholar 

  • Thiry M, Goessens G (1991) Distinguishing the sites of pre-rRNA synthesis and accumulation in Ehrlich tumor cell nucleoli. J Cell Sci 99:759–767

    Google Scholar 

  • Thiry M, Goessens G (1992) Where, within the nucleolus, are the rRNA genes located? Exp Cell Res 200:1–4

    Google Scholar 

  • Thiry M, Thiry-Blaise L (1989) In situ hybridization at the electron microscopic level: an improved method for the precise localization of ribosomal DNA and RNA. Eur J Cell Biol 50:235–243

    Google Scholar 

  • Thiry M, Thiry-Blaise L (1991) Locating transcribed and non-transcribed DNA spacer sequences within the nucleolus by in situ hybridization and immunoelectron microscopy. Nucleic Acids Res 19:11–15

    Google Scholar 

  • Thiry M, Lepoint A, Goessens G (1985) Re-evaluation of the site of transcription in Ehrlich tumor cell nucleoli. Biol Cell 54:57–64

    Google Scholar 

  • Thiry M, Scheer U, Goessens G (1988) Localization of DNA within Ehrlich tumour cell nucleoli by immunoelectron microscopy. Biol Cell 63:27–34

    Google Scholar 

  • Thiry M, Scheer U, Goessens G (1991) Localization of nucleolar chromatin by immunocytochemistry and in situ hybrization at the electron microscopic level. Electron Microsc Rev 4:85–110

    Google Scholar 

  • Thiry M, Ploton D, Menager M, Goessens G (1993) Ultrastructural distribution of DNA within the nucleolus of various animal cell lines or tissues revealed by terminal deoxynucleotide transferase. Cell Tissue Res 271:33–45

    Google Scholar 

  • Tollervey D, Lethonen H, Carmo-Fonseca M, Hurt EC (1991) The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J 10:573–583

    Google Scholar 

  • Tres LL (1975) Nucleolar RNA synthesis of meiotic prophase spermatocytes in the human testis. Chromosoma 53:141–151

    Google Scholar 

  • Vandelaer M, Thiry M (1993) Ultrastructural distribution of DNA within the ring-shaped nucleolus of human resting T lymphocytes. Exp Cell Res 205:430–432

    Google Scholar 

  • Verheijen R, Kuijpers HJH, Driel R van, Beck JLM, Dierendonk JH van, Brakenhoff GJ, Ramaekers FCS (1989) Ki-67 detects a nuclear matrix associated proliferation-related antigen II. Localization in mitotic cells and association with chromosomes. J Cell Sci 92:531–540

    Google Scholar 

  • Voit R, Schnapp A, Kuhn A, Rosenbauer H, Hirschmann P, Stunnenberg HG, Grummt I (1992) The nucleolar transcription factor mUBF is phosphorylated by casein kinase-II in the C-terminal hyperacidic tail which is essential for transactivation. EMBO J 11:2211–2218

    Google Scholar 

  • Wachtler F, Stahl A (1993) The nucleolus: a functional interpretation. Micron (in press)

  • Wachtler F, Ellinger A, Schwarzacher HG (1980) Nucleolar changes in human phytohaemagglutinin-stimulated lymphocytes. Cell Tissue Res 213:351–360

    Google Scholar 

  • Wachtler F, Schwarzacher HG, Ellinger A (1982) The influence of the cell cycle on structure and number of nucleoli in cultured human lymphocytes. Cell Tissue Res 225:155–163

    Google Scholar 

  • Wachtler F, Hopman AHN, Wiegant J, Schwarzacher HG (1986) On the position of nucleolus organizer regions (NORs) in interphase nuclei. Studies with a new, non-autoradiographic in situ hybridization method. Exp Cell Res 167:227–240

    Google Scholar 

  • Wachtler F, Popp W, Schwarzacher HG (1987) Structural changes in nucleoli during inhibition of protein and RNA-biosynthesis. Cell Tissue Res 247:583–589

    Google Scholar 

  • Wachtler F, Hartung M, Devictor M, Wiegant J, Stahl A, Schwarzacher HG (1989) Ribosomal DNA is located and transcribed in the dense fibrillar component of human Sertoli cell nucleoli Exp Cell Res 184:61–71

    Google Scholar 

  • Wachtler F, Mosgoeller W, Schwarzacher HG (1990a) Electron microscopic in situ hybridization and autoradiography: localization and transcription of rDNA in human lymphocyte nucleoli. Exp Cell Res 187:346–348

    Google Scholar 

  • Wachtler F, Roubicek C, Schedle A, Mosgoeller W, Bretis G, Schwarzacher HG (1990b) Nucleolus organizer regions in human lymphocytes as studied with premature chromosome condensation. Hum Genet 84:244–248

    Google Scholar 

  • Wachtler F, Stahl A, Sylvester J, Gonzalez I, Schoefer C, Schedle A, Mosgoeller W, Schwarzacher HG (1991a) Localization of rDNA in nucleoli of human cells as revealed by in situ hybridization. The nucleus 34:59–73

    Google Scholar 

  • Wachtler F, Schoefer C, Schwarzacher HG, Hartung M, Stahl A, Gonzales I, Sylvester J (1991b) Transcribed and non-transcribed parts of the human ribosomal repeat show a similar pattern of distribution in nucleoli. Cytogenet Cell Genet 57:175–178

    Google Scholar 

  • Wachtler F, Schoefer C, Mosgoeller W, Weipoltshammer K, Schwarzacher HG, Guichaoua M, Hartung M, Stahl A, Bergé-Lefranc JL, Gonzales I, Sylvester J (1992) 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 198:135–143

    Google Scholar 

  • Wachtler F, Mosgoeller W, Schoefer C, Sylvester J, Hozak P, Derenzini M, Stahl A (1993) Ribosomal genes and nucleolar morphology. Chromosomes Today 11:63–77

    Google Scholar 

  • Warburton D, Henderson AS (1979) Sequential silver staining and hybridization in situ on nucleolus-organizing regions in human cells. Cytogenet Cell Genet 24:168–175

    Google Scholar 

  • Yasuda Y, Maul GG (1990) A nucleolar auto-antigen is part of a major chromosomal surface component. Chromosoma 99:152–160

    Google Scholar 

  • Zatsepina O, Chelidze PV, Chentsov YS (1988a) Changes in the number and volume of fibrillar centres with the inactivation of nucleoli at erythropoesis. J Cell Sci 91:439–448

    Google Scholar 

  • Zatsepina O, Hozak P, Babadjanyan D, Chentsov Y (1988b) Quantitative ultrastructural study of nucleolus-organizing regions at some stages of the cell cycle (G0 period, G2 period, mitosis). Biol Cell 62:211–218

    Google Scholar 

  • Zini N, Martelli AM, Sabatelli P, Santi S, Negri C, Astaldi-Ricotti GCB, Maraldi NM (1992) The 180-kDa isoform of topoisomerase II is localized in the nucleolus and belongs to the structural elements of the nucleolar remnant. Exp Cell Res 200:460–466

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Histologisch-Embryologisches Institut der Universität Wien, Schwarzspanierstrasse 17, A-1090, Wien, Austria

    Hans Georg Schwarzacher & Franz Wachtler

Authors
  1. Hans Georg Schwarzacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Franz Wachtler
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schwarzacher, H.G., Wachtler, F. The nucleolus. Anat Embryol 188, 515–536 (1993). https://doi.org/10.1007/BF00187008

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00187008

Key words

Search

Navigation