Anatomy and Embryology

, Volume 188, Issue 6, pp 515–536 | Cite as

The nucleolus

  • Hans Georg Schwarzacher
  • Franz Wachtler
Review article

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.

Key words

Nucleolus rDNA-transcription rRNA Nucleolar proteins Nucleolar components 

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References

  1. 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]:161–186Google Scholar
  2. 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 105:1483–1491Google Scholar
  3. 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 97:115–123Google Scholar
  4. 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 37:1371–1374Google Scholar
  5. 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 110:1263–1270Google Scholar
  6. Biggiogera M, Kaufmann SH, Shaper JH, Gas N, Amalric F, Fakan S (1991) Distribution of nucleolar proteins B23 and nucleolin during mouse spermatogenesis. Chromosoma 100:162–172Google Scholar
  7. Bourgeois CA, Hubert J (1988) Spatial relationship between the nucleolus and the nuclear envelope: structural aspects and functional significance. Int Rev Cytol 111:1–52Google Scholar
  8. Bourgeois CA, Hernandez-Verdun D, Hubert J, Bouteille M (1979) Silver staining of NORs in electron microscopy. Exp Cell Res 123:449–452Google Scholar
  9. Bourgeois CA, Hemon D, Bouteille M (1982) Changes in the nucleolus envelope region during interphase in synchronized TG cells. J Ultrastruct Res 68:328–340Google Scholar
  10. 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 MontpellierGoogle Scholar
  11. Busch H, Smetana K (1970) The nucleolus. Academic Press, New York LondonGoogle Scholar
  12. 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 43–71Google Scholar
  13. Buys CHCM, Osinga J (1980) Abundance of protein-bound sulfhydryl and disulfide groups at chromosomal nucleolus organizing regions. Chromosoma 77:1–11Google Scholar
  14. Cajal SR (1910) El nucleo de los celulas piramidales del cerebro humano y de algunos mamiferos. Trab Lab Invest Biol Madrid 8:27–62Google Scholar
  15. 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 54:191–194Google Scholar
  16. Cataldo C, Souchier C, Stahl A (1988) Three dimensional ultrastucture and quantitative analysis of the human Sertoli cell nucleolus. Biol Cell 63:277–285Google Scholar
  17. Conconi A, Widmer RM, Koller T, Sogo JM (1989) Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell 57:753–761Google Scholar
  18. 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 89:5256–5260Google Scholar
  19. Cook PR (1991) The nucleoskeleton and the topology of replication. Cell 66:627–635Google Scholar
  20. Deltour R, Motte P (1990) The nucleolonema of plant and animal cells. Biol Cell 68:5–11Google Scholar
  21. Derenzini M, Ploton D (1991) Interphase nucleolar organizer regions in cancer cells. Int Rev Exp Pathol 32:149–192Google Scholar
  22. Derenzini M, Trere D (1991) Importance of interphase nucleolar organizer regions in tumor pathology. Virchows Arch [B] 61:1–8Google Scholar
  23. Derenzini M, Hernandez-Verdun D, Bouteille M (1982) Visualization in situ of extended DNA filaments in nucleolar chromatin of rat hepatocytes. Exp Cell Res 141:463–469Google Scholar
  24. 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 170:31–41Google Scholar
  25. Derenzini M, Thiry M, Goessens G (1990) Ultrasructural cytochemistry of the mammalian cell nucleus. J Histochem Cytochem 38:1237–1256Google Scholar
  26. Derenzini M, Pession A, Trere D (1991) Siver stained nucleolar organizer regions in cancer cells — reply. Lab Invest 64:718–719Google Scholar
  27. 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 41:829–836Google Scholar
  28. Earnshaw WC, Bernat RL (1991) Chromosomal passengers: toward an integrated view of mitosis. Chromosoma 100:139–146Google Scholar
  29. Egan MJ, Crocker J (1992) Nucleolar organiser regions in pathology. Br J Cancer 65:1–7Google Scholar
  30. Ellinger A, Wachtler F (1980) Über eine Methode zur Darstellung des Nucleolus im Licht- und Elektronenmikroskop. Mikroskopie 36:330–335Google Scholar
  31. 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 161:353–363Google Scholar
  32. Estable C, Sotelo JR (1950) Una nueva estructura celular: el nucleolonema. Publ Inst Invest Cien Biol Montevideo 1:105–126Google Scholar
  33. Fakan S, Puvion S (1980) Ultrastructural visualization of nucleolar and extranucleolar RNA synthesis and distribution. Int Rev Cytol 65:255–299Google Scholar
  34. Ferguson-Smith MA, Handmaker SD (1961) Observations on the satellited human chromosomes. Lancet I: 638Google Scholar
  35. Fischer D, Weisenberger D, Scheer U (1991) Review: assigning functions to nucleolar structures. Chromosoma 101:133–140Google Scholar
  36. Flavell RB (1986) The structure and control of expression of ribosomal RNA genes. Oxford Surv Plant Mol Cell Biol 3:251–274Google Scholar
  37. 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 90:289–299Google Scholar
  38. Gas N, Escande ML, Stevens BJ (1985) Immunolocalization of the 100-kDa nucleolar protein during the mitotic cycle in CHO cells. Biol Cell 53:209–218Google Scholar
  39. 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 101:502–510Google Scholar
  40. 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 200:5–15Google Scholar
  41. 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 102:729–737Google Scholar
  42. 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 133:1710–1715Google Scholar
  43. Ghosh S, Paweletz N (1990) Localization of ribosomal cistrons at the ultrastructural level by in situ hybridization technique. Cell Biol Int Rep 14:521–525Google Scholar
  44. Goessens G (1984) Nucleolar structure. Int Rev Cytol 87:107–158Google Scholar
  45. 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 87:63–72Google Scholar
  46. Goessens G, Lepoint A (1982) Localization of Ag-NOR-proteins in Ehrlich tumor cell nucleoli. Biol Cell 43:139–142Google Scholar
  47. 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 88:324–328Google Scholar
  48. Gonzales SP, Nardone RM (1968) Cyclic nucleolar changes during the cell cycle I. Variations in number, size, morphology and position. Exp Cell Res 50:599–615Google Scholar
  49. Goodpasture C, Bloom SE (1975) Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma 53:37–50Google Scholar
  50. 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 38:604–619Google Scholar
  51. Haaf T, Hayman DL, Schmid M (1991) Quantitative determination of rDNA transcription units in vertebrate cells. Exp Cell Res 193:78–86Google Scholar
  52. Hadjiolov AA (1985) The nucleolus and ribosome biogenesis. Springer, Berlin Heidelberg New YorkGoogle Scholar
  53. 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 52:295–308Google Scholar
  54. 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 22:25–27Google Scholar
  55. Heitz E (1931) Die Ursache der gesetzmäßigen Zahl, Lage, Form und Größe pflanzlicher Nucleolen. Planta 12:775–844Google Scholar
  56. Hernandez Verdun D (1991) The nucleolus today. J Cell Sci 99:465–471Google Scholar
  57. 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 79:349–362Google Scholar
  58. 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 98:99–105Google Scholar
  59. Heslop-Harrison JS, Mosgoeller W, Schwarzacher T, Leitch AR (1991) Volumes and positions of chromosomes in reconstructions of fibroblasts. Am J Hum Genet [Suppl] 49:380Google Scholar
  60. Howell WM, Denton TE, Diamond JR (1975) Differential staining of satellite regions of human acrocentric chromosomes. Experientia 31:260–262Google Scholar
  61. 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 57:197–206Google Scholar
  62. Hozak P, Novak JT, Smetana K (1989) Three-dimensional reconstructions of nucleolus organizing regions in PHA-stimulated lymphocytes. Biol Cell 66:225–233Google Scholar
  63. Hozak P, Geraud G, Hernandez-Verdun D (1992) Revealing nucleolar architecture by low ionic strength treatment. Exp Cell Res 203:128–133Google Scholar
  64. 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 104:1199–1205Google Scholar
  65. Hsu TC, Brinkley BR, Arrighi FD (1967) The structure and behavior of the nucleolar organizers in mammalian cells. Chromosoma 23:137–153Google Scholar
  66. 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 129:139–147Google Scholar
  67. 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 100:873–886Google Scholar
  68. Ingle J, Sinclair J (1972) Ribosomal RNA genes and plant development. Nature 235:30–32Google Scholar
  69. Jackson DA, Cook PR (1988) Visualization of a nucleoskeleton with a 23-nm axial repeat. EMBO J 7:3667–3677Google Scholar
  70. Johnson RT, Rao PN (1970) Mammalian cell fusion: induction of premature chromosome condensation in interphase nuclei. Nature 226:712–722Google Scholar
  71. Jordan EG (1979) The nucleolus at Weimar. Nature 281:529–530Google Scholar
  72. Jordan EG (1987) Nucleolar organizers in plants. In: Stahl A, Luciani JM, Vagner-Capodano AM (eds) Chromosomes today, vol 9. Allen & Unwin, London, pp 272–283Google Scholar
  73. Jordan EG (1991) Interpreting nucleolar structure: where are the transcribing genes? J Cell Sci 98:437–442Google Scholar
  74. 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 52:373–389Google Scholar
  75. 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 95:343–352Google Scholar
  76. Jordan EG, Zatsepina O, Shaw PJ (1992) Widely dispersed DNA within plant and animal nucleoli visualised by 3-D fluorescence microscopy. Chromosoma 101:478–482Google Scholar
  77. 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 51:4008–40Google Scholar
  78. 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 15:123–132Google Scholar
  79. 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 60:897–908Google Scholar
  80. 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 57:351–364Google Scholar
  81. 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 84:1472–1476Google Scholar
  82. Lavelle A, Lavelle FW (1970) Cytodifferentiation in the neuron. In: Himwich WA (ed) Developmental neurobiology. Thomas, Springfield, IllGoogle Scholar
  83. 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 101:751–757Google Scholar
  84. Leydig F (1852) Anatomische Notizen ueber Synapta digitata. Arch Anat Physiol Wiss Med: 507–519Google Scholar
  85. Manuelidis L, Chen TL (1990) A unified model of eukaryotic chromosomes. Cytometry 11:8–25Google Scholar
  86. Marinesco G (1905) Recherches sur le noyau et le nucléole de la cellule nerveuse à l'état normal et pathologique. J Psychol Neurol 5:151–172Google Scholar
  87. Martin M, Moreno Diaz dela Espina S, Medina FJ (1989) Immunolocalization of DNA at nucleolar structural components in onion cells. Chromosoma 98:368–377Google Scholar
  88. 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 199:74–84Google Scholar
  89. Matsui S, Sasaki M (1973) Differential staining of nucleolus organizers in mammalian chromosomes. Nature 246:148–150Google Scholar
  90. McClintock B (1934) The relation of a particular chromosomal element to the development of the nucleoli in Zea mays. Z Zellforsch Mikrosk Anat 21:294–328Google Scholar
  91. Medina FJ (1989) The nucleolus in the spotlight. Meeting on the nucleolus, Toledo (Spain), December 15–18, 1988. Eur J Cell Biol 50:244–246Google Scholar
  92. Medina FJ, Solanilla EL, Sanchez-Pina MA, Fernandez-Gomez ME, Risueno MC (1986) Cytological approach to the nucleolar functions detected by silver staining. Chromosoma 94:259–266Google Scholar
  93. Mirre C, Stahl A (1978) Ultrastructure and activity of the nucleolar organizer in the mouse oocyte during meiotic prophase. J Cell Sci 31:79–100Google Scholar
  94. 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 48:105–126Google Scholar
  95. Montgomery TH (1899) Comparative cytological studies with especial regard to the morphology of the nucleolus. J Morphol 15:265–283Google Scholar
  96. Moreno FJ, Rodrigo RM, Garcia-Herdugo G (1990) Ag-NOR proteins and rDNA transcriptional activity in plant cells. J Histochem Cytochem 38:1879–1887Google Scholar
  97. Morita M, Kuwano H, Matsuda H, Moriguchi S, Sugimachi K (1991) Prognostic significance of argyrophilic nucleolar organizer regions in esophageal carcinoma. Cancer Res 51:5339–5341Google Scholar
  98. Mosgoeller W, Monschein H, Wachtler F, Schwarzacher HG (1991a) Über den Uridineinbau in Nukleolen von Lymphozyten des menschlichen peripheren Blutes. Anat Anz [Suppl] 168:277–278Google Scholar
  99. Mosgoeller W, Leitch AR, Brown JKM, Heslop-Harrison JS (1991b) Chromosome arrangements in human fibroblasts at mitosis. Hum Genet 88:27–33Google Scholar
  100. 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] 57:56Google Scholar
  101. Mosgoeller W, Schoefer C, Derenzini M, Steiner M, Maier U, Wachtler F (1993) Distribution of DNA in human Sertoli cells nucleoli. J Histochem Cytochem 41:1487–1493Google Scholar
  102. 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 62:65–81Google Scholar
  103. 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 200:452–459Google Scholar
  104. Noel JS, Dewey WC, Abel JH, Thompson RP (1971) Ultrastructure of the nucleolus during Chinese hamster cell cycle. J Cell Biol 49:830–847Google Scholar
  105. Ochs RL, Smetana K (1991) Detection of fibrillarin in nucleolar remnants and the nucleolar matrix. Exp Cell Res 197:183–190Google Scholar
  106. Ochs RL, Lischwe MA, Spohn WH, Busch H (1985) Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol Cell 54:123–134Google Scholar
  107. 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 60:91–99Google Scholar
  108. Paweletz N, Risueno MC (1982) Transmission-electron-microscopic studies on the mitotic cycle of nucleolar proteins impregnated with silver. Chromosoma 85:261–273Google Scholar
  109. 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 24:128–130Google Scholar
  110. Petrzilka GE, Schroeder HE (1979) Activation of human Tlymphocytes. A kinetic and stereological study. Cell Tissue Res 201:101–127Google Scholar
  111. Pischinger A (1926) Die Lage des isoelektrischen Punktes histologischer Elemente als Ursache ihrer verschiedenen Färbbarkeit. Z Zellforsch Mikrosk Anat 3:167–197Google Scholar
  112. Ploton D, Bendayan M, Adnet JJ (1983) Ultrastructural localization of Ag-NOR proteins and nucleic acids in reticulated nucleoli. Biol Cell 49:29–34Google Scholar
  113. Popp W, Wachtler F (1983) Changes in nucleolar structure, number and size in cellular activation and inactivation. Cell Tissue Res 234:377–388Google Scholar
  114. 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 188:852–855Google Scholar
  115. Puvion-Dutilleul F, Bachellerie JP, Puvion E (1991) Nucleolar organization of Hela cells as studied by in situ hybridization. Chromosoma 100:395–409Google Scholar
  116. Raska I, Dundr M (1992) Compartmentalization of the cell nucleus: case of the nucleolus. Chromosomes Today 11:101–119Google Scholar
  117. 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 65:79–82Google Scholar
  118. 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 99:143–151Google Scholar
  119. Reeder RH (1990) rRNA synthesis in the nucleolus. Trends Genet 6:390–395Google Scholar
  120. Reimer G, Raska I, Tan EM, Scheer U (1987) Human autoantibodies: probes for nucleolus structure and function. Virchows Arch [B] 54:131–143Google Scholar
  121. 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 200:393–403Google Scholar
  122. 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 58:313–329Google Scholar
  123. 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 77:255–262Google Scholar
  124. 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 102:146–157Google Scholar
  125. 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 103:1053–1063Google Scholar
  126. Royal A, Simard R (1975) RNA-synthesis in the ultrastructural and biochemical components of the nucleolus of Chinese hamster ovary cells. J Cell Biol 66:577–585Google Scholar
  127. Ruzicka V (1899) Zur Geschichte und Kenntnis der feineren Structur der Nucleolen centraler Nervenzellen. Anat Anz 16:557–563Google Scholar
  128. 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 269:473–480Google Scholar
  129. Scheer U, Benavente R (1990) Functional and dynamic aspects of the mammalian nucleolus. Bioessays 12:14–21Google Scholar
  130. 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 81:1431–1435Google Scholar
  131. 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 99:672–679Google Scholar
  132. Schmidt-Zachmann MS, Huegle-Doerr B, Franke WW (1987) A constitutive nucleolar protein identified as a member of the nucleoplasm family. EMBO J 6:1881–1890Google Scholar
  133. Schnedl W, Schnedl M (1972) Nucleoluszahl und -größe während des Zellzyklus. Z Zellforsch Mikrosk Anat 126:374–382Google Scholar
  134. 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] 57:70Google Scholar
  135. 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 64:27–30Google Scholar
  136. Schwarzacher HG, Wachtler F (1983) Nucleolus organizer regions and nucleoli. Hum Genet 63:89–99Google Scholar
  137. Schwarzacher HG, Wachtler F (1991) The functional significance of nucleolar structures. Ann Genet 34:151–160Google Scholar
  138. Schwarzacher HG, Mikelsaar AV, Schnedl W (1978) The nature of Ag-staining of nucleolus organizer regions. Cytogenet Cell Genet 20:24–39Google Scholar
  139. 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 84:7953–7956Google Scholar
  140. Sigmund J, Schwarzacher HG, Mikelsaar AV (1979) Satellite association frequency and number of nucleoli depend on cell cycle duration and NOR activity. Hum Genet 50:81–91Google Scholar
  141. Smetana K (1980) Nucleoli in maturing blood cells. In: Roath S (ed) Topical reviews in hematology. Academic Press, New York, pp 73–147Google Scholar
  142. Smetana K, Busch H (1974) The nucleolus and nucleolar DNA. In: Busch H (ed) The cell nucleus. Academic Press, New York, pp 75–147Google Scholar
  143. Sollner-Webb B, Mougey EB (1991) News from the nucleolus: rRNA gene expression. Trends Biochem Sci 16:58–62Google Scholar
  144. Srivastava AK, Schlessinger D (1991) Structure and organization of ribosomal DNA. Biochimie 73:631–638Google Scholar
  145. Stahl A (1982) The nucleolus and nucleolar chromosomes. In: Jordan EG, Cullis CA (eds) The nucleolus. Cambridge University Press, Cambridge, pp 1–24Google Scholar
  146. 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 101:231–244Google Scholar
  147. 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 73:193–198Google Scholar
  148. 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 101:777–791Google Scholar
  149. 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 102:41–49Google Scholar
  150. Thiry M (1988) Study of RNA distribution in the nucleolar components of Ehrlich cell using RNAse-gold method. Histochemistry 89:231–236Google Scholar
  151. Thiry M (1991a) DNase I-sensitive sites within the nuclear architecture visualized by immunoelectron microscopy. DNA Cell Biol 10:169–180Google Scholar
  152. 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 39:871–874Google Scholar
  153. Thiry M (1992a) Ultrastructural detection of DNA within the nucleolus by sensitive molecular immunocytochemistry. Exp Cell Res 200:135–144Google Scholar
  154. 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 20:6195–6200Google Scholar
  155. Thiry M (1993) Ultrastructural distribution of DNA and RNA within the nucleolus of human Sertoli cells as seen by molecular immunocytochemistry. J Cell Sci 105:33–39Google Scholar
  156. Thiry M, Goessens G (1991) Distinguishing the sites of pre-rRNA synthesis and accumulation in Ehrlich tumor cell nucleoli. J Cell Sci 99:759–767Google Scholar
  157. Thiry M, Goessens G (1992) Where, within the nucleolus, are the rRNA genes located? Exp Cell Res 200:1–4Google Scholar
  158. 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 50:235–243Google Scholar
  159. 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 19:11–15Google Scholar
  160. Thiry M, Lepoint A, Goessens G (1985) Re-evaluation of the site of transcription in Ehrlich tumor cell nucleoli. Biol Cell 54:57–64Google Scholar
  161. Thiry M, Scheer U, Goessens G (1988) Localization of DNA within Ehrlich tumour cell nucleoli by immunoelectron microscopy. Biol Cell 63:27–34Google Scholar
  162. 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 4:85–110Google Scholar
  163. 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 271:33–45Google Scholar
  164. 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 10:573–583Google Scholar
  165. Tres LL (1975) Nucleolar RNA synthesis of meiotic prophase spermatocytes in the human testis. Chromosoma 53:141–151Google Scholar
  166. Vandelaer M, Thiry M (1993) Ultrastructural distribution of DNA within the ring-shaped nucleolus of human resting T lymphocytes. Exp Cell Res 205:430–432Google Scholar
  167. 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 92:531–540Google Scholar
  168. 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 11:2211–2218Google Scholar
  169. Wachtler F, Stahl A (1993) The nucleolus: a functional interpretation. Micron (in press)Google Scholar
  170. Wachtler F, Ellinger A, Schwarzacher HG (1980) Nucleolar changes in human phytohaemagglutinin-stimulated lymphocytes. Cell Tissue Res 213:351–360Google Scholar
  171. 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 225:155–163Google Scholar
  172. 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 167:227–240Google Scholar
  173. Wachtler F, Popp W, Schwarzacher HG (1987) Structural changes in nucleoli during inhibition of protein and RNA-biosynthesis. Cell Tissue Res 247:583–589Google Scholar
  174. 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 184:61–71Google Scholar
  175. 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 187:346–348Google Scholar
  176. 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 84:244–248Google Scholar
  177. 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 34:59–73Google Scholar
  178. 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 57:175–178Google Scholar
  179. 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 198:135–143Google Scholar
  180. Wachtler F, Mosgoeller W, Schoefer C, Sylvester J, Hozak P, Derenzini M, Stahl A (1993) Ribosomal genes and nucleolar morphology. Chromosomes Today 11:63–77Google Scholar
  181. Warburton D, Henderson AS (1979) Sequential silver staining and hybridization in situ on nucleolus-organizing regions in human cells. Cytogenet Cell Genet 24:168–175Google Scholar
  182. Yasuda Y, Maul GG (1990) A nucleolar auto-antigen is part of a major chromosomal surface component. Chromosoma 99:152–160Google Scholar
  183. 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 91:439–448Google Scholar
  184. 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 62:211–218Google Scholar
  185. 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 200:460–466Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Hans Georg Schwarzacher
    • 1
  • Franz Wachtler
    • 1
  1. 1.Histologisch-Embryologisches Institut der Universität WienWienAustria

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