Advertisement

Structure and evolution of the nucleolus during oogenesis

  • Antonio Coimbra
  • Carlos Azevedo
Part of the Electron Microscopy in Biology and Medicine book series (EMBM, volume 2)

Abstract

To a large extent, the morphological organization of nucleoli reflects the degree of ribosomal RNA (rRNA) synthesis taking place in cells. Oocytes are cells in which ribosome formation is extremely active, but only at specific stages of oogenesis. Nucleoli of developing oocytes offer a wealth of morphological information related to the physiological state of the cell. Correlations of nucleolar structure and function during oogenesis can be made on the basis of new formation, in large numbers, intense growth and numerous morphological transformations.

Keywords

Xenopus Laevis Human Oocyte Vitellogenic Oocyte Pachytene Stage Lampbrush Chromosome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Van Gansen P, Schram A: Evolution of the nucleoli during oogenesis in Xenopus laevis studied by electron microscopy. J Cell Sci 10: 339–367, 1972.PubMedGoogle Scholar
  2. 2.
    Miller OL, Beatty BR, Hamkalo BA: Nuclear structure and function during amphibian oogenesis. In: Oogenesis. Biggers JD, Schuetz AW (eds) Univ Park Press-Baltimore, London, 1972, pp 119–128.Google Scholar
  3. 3.
    Lane NJ: Spheroidal and ring nucleoli in amphibian oocytes. J Cell Biol 35: 421–434, 1967.PubMedCrossRefGoogle Scholar
  4. 4.
    Mirre C, Stahl A: Ultrastructural study of nucleolar organizers in the quail oocyte during meiotic prophase I. J Ultrastruct Res 56: 186–201, 1976.PubMedCrossRefGoogle Scholar
  5. 5.
    Goessens G, Lepoint A: The nucleolus-organizing regions (NOR’s): recent data and hypotheses. Biol Cell 35: 211–220, 1979.Google Scholar
  6. 6.
    Knibiehler B, Navarro A, Mirre C, Stahl A: Localization of ribosomal cistrons in the quail oocyte during meiotic prophase I. Exptl Cell Res 110: 153–157, 1977.PubMedCrossRefGoogle Scholar
  7. 7.
    Altmann GG, Leblond CP: Changes in size and structure of the nucleolus of columnar cells during their migration from crypt base to villus top in rat jejunum. J Cell Sci 56: 83–100, 1982.PubMedGoogle Scholar
  8. 8.
    Chouinard LA: A light and electron microscope study of the nucleolus during growth of the oocyte in the prepubertal mouse. J Cell Sci 9: 637–663, 1971.PubMedGoogle Scholar
  9. 9.
    Crozet N, Motlik J, Szollosi D: Nucleolar fine structure and RNA synthesis in porcine oocytes during the early stages of antrum formation. Biol Cell 41: 35–42, 1981.Google Scholar
  10. 10.
    Fakan S, Puvion E: The ultrastructural visualization of nucleolar and extranucleolar RNA synthesis and distribution. Int Rev Cytol 65: 255–299, 1980.PubMedCrossRefGoogle Scholar
  11. 11.
    Kalt MR: Ultrastructural observations on the germ line of Xenopus laevis. Z Zellforsch 138: 41–62, 1973.PubMedCrossRefGoogle Scholar
  12. 12.
    Al-Mukhtar KK, Webb AC: An ultrastructural study of primordial germ cells, oogonia and early oocytes in Xenopus laevis. J Embryol exp Morph 26: 195–217, 1971.PubMedGoogle Scholar
  13. 13.
    Gall JG: Lampbrush chromosomes from oocyte nuclei of the newt. J Morph 94: 283–351, 1954.CrossRefGoogle Scholar
  14. 14.
    Coggins LW, Gall JG: The timing of meiosis and DNA synthesis during ovogenesis in the toad, Xenopus laevis. J Cell Biol 52: 569–576, 1972.PubMedCrossRefGoogle Scholar
  15. 15.
    Pardue ML: Nucleic and hibridization in cytochemical preparations. J Cell Biol 43: 101a, 1969.Google Scholar
  16. 16.
    Gall JG: The genes for ribosomal RNA during oogenesis. Genetics Suppl 61: 121–132, 1969.Google Scholar
  17. 17.
    Cave MD, Allen ER: Synthesis of nucleic acids associated with a DNA- containing body in oocytes of Acheta. Exptl Cell Res 58: 201–212, 1969.PubMedCrossRefGoogle Scholar
  18. 18.
    Lima-de-Faria A, Jaworska H, Gustafsson T, Daskaloff S: Amplification of ribosomal DNA in Acheta. Ill - The release of DNA copies from chromomeres. Hereditas 73: 163–184, 1973.PubMedCrossRefGoogle Scholar
  19. 19.
    Gall JG, Macgregor HC, Kidston ME: Gene amplification in the oocytes of dytiscid water beetles. Chromosoma 26: 169–187, 1969.PubMedCrossRefGoogle Scholar
  20. 20.
    Lima-de-Faria A, Moses MJ: Ultrastructure and cytochemistry of metabolic DNA in Tipula. J Cell Biol 30: 177–192, 1966.PubMedCrossRefGoogle Scholar
  21. 21.
    Kloc M: Extrachromosomal DNA and its activity in RNA synthesis in oogonia and oocytes in the pupal ovary of Creophilus maxillosus (Staphylinidae, Coleoptera-Polyphaga). Eur J Cell Biol 21: 328–334, 1980.PubMedGoogle Scholar
  22. 22.
    Mirre C, Stahl A: Ultrastructure and activity of the nucleolar organizer in the mouse oocyte during meiotic prophase. J Cell Sci 31: 79–100, 1978.PubMedGoogle Scholar
  23. 23.
    Palombi F, Viron A: Nuclear cytochemistry of mouse oogenesis. I - Changes in extranucleolar ribonucleoprotein components through meiotic prophase. J Ultrastruct Res 61: 10–20, 1977.PubMedCrossRefGoogle Scholar
  24. 24.
    Palombi F, Stefanini M: Ultrastructural analysis of nucleolar evolution in the rat primary oocyte. J Ultrastruct Res 47: 61–73, 1974.PubMedCrossRefGoogle Scholar
  25. 25.
    Härtung M, Stahl A: Autoradiographic study of RNA synthesis during meiotic prophase in the human oocyte. Cytogenet Cell Genet 20: 51–58, 1978.PubMedCrossRefGoogle Scholar
  26. 26.
    Härtung M, Mirre C, Stahl A: Nucleolar organizers in human oocytes at meiotic prophase I, studied by the silver-NOR method and electron microscopy. Hum Genet 52: 295–308, 1979.PubMedCrossRefGoogle Scholar
  27. 27.
    Mirre C, Härtung M, Stahl A: Association of ribosomal genes in the fibrillar center of the nucleolus: A factor influencing translocation and nondisjunction in the human meiotic oocyte. Proc Nat Acad Sci, USA 77: 6017–6021, 1980.CrossRefGoogle Scholar
  28. 28.
    Stahl A, Mirre C, Härtung M, Knibiehler B: Localisation, structure et activité des gènes ribosomiques dans le nucléole de Tovocyte en prophase de méiose. Reprod Nutr Develop 20: 469–483, 1980.CrossRefGoogle Scholar
  29. 29.
    Wolgemuth DJ, Jagiello GM, Henderson AS: Quantitation of ribosomal RNA genes in fetal human oocyte nuclei using rRNA: DNA hybridization in situ. Exptl Cell Res 118: 181–190, 1979.PubMedCrossRefGoogle Scholar
  30. 30.
    Gall JG: Differential synthesis of the genes for ribosomal RNA during amphibian oogenesis. Proc Nat Acad Sci, USA 60: 553–560, 1968.CrossRefGoogle Scholar
  31. 31.
    Ficq A: RNA synthesis in early oogenesis of Xenopus laevis. Exptl Cell Res 63: 453–457, 1970.PubMedCrossRefGoogle Scholar
  32. 32.
    Ficq A: Meiosis in early amphibian oogenesis: synthesis and location of proteins. Exptl Cell Res 73: 242–248, 1972.PubMedCrossRefGoogle Scholar
  33. 33.
    Wallace H, Birnstiel ML: Ribosomal cistrons and the nucleolar organizer. Biochim Biophys Acta 114: 296–310, 1966.PubMedGoogle Scholar
  34. 34.
    Brown DD, Dawid IB: Specific gene amplification in oocytes. Science 160: 272–280, 1968.PubMedCrossRefGoogle Scholar
  35. 35.
    Birnstiel ML, Wallace H, Sirlin JL, Fischberg M: Localization of the ribosomal DNA complements in the nucleolar organizer region of Xenopus laevis. Natl Cancer Inst Monograph 23: 431–448, 1966.Google Scholar
  36. 36.
    Kahn J: The nucleolar organizer in the mitotic chromosome complement of Xenopus laevis. Quart J Microscop Sci 103: 407, 1962.Google Scholar
  37. 37.
    Perkowska E, MacGregor HC, Birnstiel ML: Gene amplification in the oocyte nucleus of mutant and Wild-type Xenopus-laevis. Nature 217: 649–650, 1968.PubMedCrossRefGoogle Scholar
  38. 38.
    Hourcade D, Dressler D, Wolfson J: The nucleolus and the rolling circle. In: ‘Chromosome Structure and Function’. Cold Spring Harbor Symposia on Quantitative Biology 38: 537–550, 1973.Google Scholar
  39. 39.
    Raikova EV: Evolution of the nucleolar apparatus during oogenesis in Acipenseridae. J Embryol exp Morph 35: 667–687, 1976.PubMedGoogle Scholar
  40. 40.
    Vincent WS, Halvorson HO, Chen H-R, Shin D: A comparison of ribosomal gene amplification in uni-and multinucleolate oocytes. Exptl Cell Res 57: 240–250, 1969.PubMedCrossRefGoogle Scholar
  41. 41.
    Vlad M: Nucleolar DNA in oocytes of Salmo irideus (Gibbons). Cell Tissue Res 167: 407–424, 1976.PubMedCrossRefGoogle Scholar
  42. 42.
    Denis H, Wegnez M: Biochemical research on oogenesis. Oocytes and liver cells of the teleost fish Tinea tinea contain different kinds of 5S RNA. Dev Biol 59: 228–236, 1977.PubMedCrossRefGoogle Scholar
  43. 43.
    Ullman JS, Lima-de-Faria A, Jaworska H and Bryngelsson T: Amplifi-cation of ribosomal DNA in Acheta. V. Hybridization of RNA complementary to ribosomal DNA with pachytene chromosomes. Hereditas 74: 13–24, 1973.PubMedCrossRefGoogle Scholar
  44. 44.
    Jaworska H, Lima-de-Faria A: Amplification of ribosomal DNA in Acheta. VII-Transfer of DNA-RNA assemblies from the nucleus to the cytoplasm. Hereditas 74: 187–204, 1973.PubMedCrossRefGoogle Scholar
  45. 45.
    Pero R, Lima-de-Faria A, Stähle U, Granström H, Ghatnekar R: Amplification of ribosomal DNA in Acheta. IV - The number of cistrons for 28S and 18S ribosomal RNA. Hereditas 73: 195–210, 1973.PubMedCrossRefGoogle Scholar
  46. 46.
    Gall JG, Rochaix JD: The amplified ribosomal DNA of dytiscid beetles. Proc Nat Acad Sci, USA 71: 1819–1823, 1974.CrossRefGoogle Scholar
  47. 47.
    Scheer U, Zentgraf H: Nucleosomal and supranucleosomal organization of transcriptionally inactive rDNA circles in Dytiscus oocytes. Chromosoma 69: 243–254, 1978.PubMedCrossRefGoogle Scholar
  48. 48.
    Rindt KP, Nover L: Chromatin structure and function. Biol Zbl 99: 641–673, 1980.Google Scholar
  49. 49.
    Kidder GM: The ribosomal RNA cistrons in clam gametes. Dev Biol 48: 132–142, 1976.CrossRefGoogle Scholar
  50. 50.
    Comings EE, Mattoccia E: Studies of microchromosomes and a G-C rich DNA satellite in the quail. Chromosoma 30: 202–214, 1970.PubMedGoogle Scholar
  51. 51.
    Stahl A, Luciani LM, Devictor M, Capodano AM, Härtung M: Heterochromatin and nucleolar organizers during first meiotic prophase in quail oocytes. Exptl Cell Res 91: 365–371, 1974.CrossRefGoogle Scholar
  52. 52.
    Mirre C, Stahl A: Peripheral RNA synthesis of fibrillar center in nucleoli of Japanese quail oocytes and somatic cells. J Ultrastruct Res 64: 377–387, 1978.PubMedCrossRefGoogle Scholar
  53. 53.
    Dumont JN: Oogenesis in Xenopus laevis (Daudin). I - Stages of oocyte development in laboratory maintained animals. J Morph 136: 153–180, 1972.PubMedCrossRefGoogle Scholar
  54. 54.
    Thiébaud CH: Quantitative determination of amplified rRNA and its distribution during oogenesis in Xenopus laevis. Chromosoma 73: 37–44, 1979.PubMedCrossRefGoogle Scholar
  55. 55.
    Van Gänsen P, Schram A: Incorporation of (3H) uridine and (3H) thymidine during the phase of nucleolar multiplication in Xenopus laevis oogenesis: a high-resolution autoradiographic study. J Cell Sei 14: 85–103, 1974.Google Scholar
  56. 56.
    Van Gänsen P, Thomas C, Schram A: Nucleolar activity and RNA metabolism in previtellogenic and vitellogenic oocytes of Xenopus laevis. Exptl Cell Res 98: 111–119, 1976.PubMedCrossRefGoogle Scholar
  57. 57.
    Denis H: Accumulation du RNA dans les oocytes des vertébrés inférieurs. Biol Cell 28: 87–92, 1977.Google Scholar
  58. 58.
    Thomas C: Évolution des structures ribosomales au cours de l’oogenèse chez Xenopus laevis. Arch Biol (Liège) 78: 347–369, 1967.Google Scholar
  59. 59.
    Scheer U, Trendelenburg MF, Franke WW: Regulation of transcription of genes of ribosomal RNA during amphibian oogenesis. J Cell Biol 69: 465–489, 1976.PubMedCrossRefGoogle Scholar
  60. 60.
    MacGregor HC: The nucleolus and its genes in amphibian oogenesis. Biol Rev 47: 177–210, 1972.PubMedCrossRefGoogle Scholar
  61. 61.
    Denis H, Mairy M: Recherches biochimiques sur Toogenèse. I - Distribution intracellulaire du RNA dans les petits oocytes de Xenopus laevis. Eur J Biochem 25: 524–534, 1972.PubMedCrossRefGoogle Scholar
  62. 62.
    Callan HG, Lloyd L: Lampbrush chromosomes of crested newts Triturus Cristatus (Laurenti). Phil Trans B 243: 135–219, 1960.CrossRefGoogle Scholar
  63. 63.
    Callan HG: Chromosomes and nucleoli of the axolotl. Ambystoma mexicanum. J Cell Sei 1: 85–108, 1966.Google Scholar
  64. 64.
    Bruslé S, Bruslé J: Les apports de la microscopie électronique à la connaissance des cellules germinales précoces des poissons. Vie Millieu, 28–29: 267–285, 1979.Google Scholar
  65. 65.
    Cave MD: Localization of ribosomal DNA within oocytes of the house cricket, Acheta Domesticus (Orthoptera: Gryllidae). J Cell Biol 55: 310–321, 1972.PubMedCrossRefGoogle Scholar
  66. 66.
    Jaworska H, Lima-de-Faria A: Amplification of ribosomal DNA in Acheta. VI - Ultrastructure of two types of nucleolar components associated with ribosomal DNA. Hereditas 74: 169–186, 1973.CrossRefGoogle Scholar
  67. 67.
    Trendelenburg MF, Franke WW, Scheer U: Frequencies of circular units of nucleolar DNA in oocytes of two insects, Acheta domesticus and Dytiscus marginalis, and changes of nucleolar morphology during oogenesis. Differentiation 7: 133–158, 1977.PubMedCrossRefGoogle Scholar
  68. 68.
    Trendelenburg MF, Scheer U, Zentgraf H, Franke WW: Heterogeneity of spacer lengths in circles of amplified ribosomal DNA of two insect species, Dytiscus marginalis and Acheta domesticus. J Mol Biol 108: 453–470, 1976.PubMedCrossRefGoogle Scholar
  69. 69.
    Halkka L: Ultrastructural changes and kinetic relationships of the secondary nucleolus and nuclear bodies in previtellogenic oocytes of the dragonfly Cordulia aenea. Hereditas 95: 259–268, 1981.CrossRefGoogle Scholar
  70. 70.
    Chouinard LA: An electron-microscope study of the extranucleolar bodies during growth of the oocyte in the prepubertal mouse. J Cell Sei 12: 55–69, 1973.Google Scholar
  71. 71.
    Mirre C, Stahl A: Ultrastructural organization, sites of transcription and distribution of fibrillar centres in the nucleolus of the mouse oocyte. J Cell Sei 48: 105–126, 1981.Google Scholar
  72. 72.
    Chouinard LA: A light and electron-microscope study of the oocyte nucleus during development of the antral follicle in the prepubertal mouse. J Cell Sci 17: 589–600, 1975.PubMedGoogle Scholar
  73. 73.
    Goodpasture C, Bloom SE: Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma 53: 37–50, 1975.PubMedCrossRefGoogle Scholar
  74. 74.
    Wolgemuth-Jarashow DJ, Jagiello GM, Henderson AS: The localization of rDNA in small nucleolus-like structures in human diplotene oocyte nuclei. Hum Genet 36: 63–68, 1977.PubMedCrossRefGoogle Scholar
  75. 75.
    Brachet J, Hanocq F, Van Gansen P: A cytochemical and ultrastructural analysis of in vitro maturation in amphibian oocytes. Dev Biol 21: 157–195, 1970.PubMedCrossRefGoogle Scholar
  76. 76.
    Van Gansen P, Schram A: Ultrastructure et cytochimie ultrastructurale de la vésicule germinative et du cytoplasme périnucléaire de l’oocyte mûr de Xenopus laevis. J Embryol exp Morph 20: 375–389, 1968.PubMedGoogle Scholar
  77. 77.
    Steinert G, Thomas C, Brachet J: Localization by in situ hybridization of amplified ribosomal DNA during Xenopus laevis oocyte maturation (a light and electron microscopy study). Proc Nat Acad Sci, USA 73: 833–836, 1976.CrossRefGoogle Scholar
  78. 78.
    Azevedo C, Coimbra A: Evolution of nucleoli in the course of oogenesis in a viviparous Teleost (Xiphophorus helleri). Biol Cell 38: 43–48, 1980.Google Scholar
  79. 79.
    Clérot J-C: Les groupements mitochondriaux des cellules germinales des poissons téléostéens cyprinidés. II - Étude autoradiographique à haute résolution de l’incorporation de phénylalanine 3H et d’uridine 3H. Exptl Cell Res 120: 237–244, 1979.PubMedCrossRefGoogle Scholar
  80. 80.
    Schultz RM, Letourneau GE, Wassarman PM: Program of early development in the mammal: changes in patterns and absolute rates of tubulin and total protein synthesis during oogenesis and early embryo- genesis in the mouse. Dev Biol 68: 341–359, 1979.PubMedCrossRefGoogle Scholar
  81. 81.
    Zamboni L: Comparative studies on the ultrastructure of mammalian oocytes. In: Oogenesis. Biggers JD, Schuetz AW (eds) Univ Park Press- Baltimore, London, 1972, pp 5–45.Google Scholar
  82. 82.
    Moore GPM, Lintern-Moore S, Peters H, Faber M: RNA synthesis in the mouse oocyte. J Cell Biol 60: 416–422, 1974.PubMedCrossRefGoogle Scholar
  83. 83.
    Wassarman PM, Letourneau GE: RNA synthesis in fully-grown mouse oocytes. Nature 261: 73–74, 1976.PubMedCrossRefGoogle Scholar
  84. 84.
    Azevedo C, Coimbra A: Nucleolar fine structure in oocytes of Helcion pellucidus (Gastropoda, Prosobranchia). Ciênc Biol (Portugal) 7: 43a, 1982.Google Scholar
  85. 85.
    Wallace RA, Nickol JM, Ho T, Jared DW: Studies on amphibian yolk. X. The relative roles of autosynthetic and heterosynthetic processes during yolk protein assembly by isolated oocytes. Dev Biol 29: 255–272, 1972.PubMedCrossRefGoogle Scholar
  86. 86.
    Brown DD: The nucleolus and synthesis of ribosomal RNA during oogenesis and embryogenesis of Xenopus laevis. Natl Cancer Inst Monograph 23: 297–309, 1966.Google Scholar
  87. 87.
    Bouloukhère M, Thomas C, Heilporn-Pohl V, Hanocq F, Brachet J: Nucleolar localization of ‘template-bound’ RNA polymerase I in nuclei of Xenopus laevis blastulae. Exptl Cell Res 130: 291–295, 1980.CrossRefGoogle Scholar
  88. 88.
    Pikô L, Clegg KB: Quantitative changes in total RNA, total poly (A), and ribosomes in early mouse embryos. Dev Biol 89: 362–378, 1982.PubMedCrossRefGoogle Scholar
  89. 89.
    Bachvarova R, De Leon V: Polyadenylated RNA of mouse ova and loss of maternal RNA in early development. Dev Biol 74: 1–8, 1980.PubMedCrossRefGoogle Scholar
  90. 90.
    Van Blerkom J, Brockway GO: Qualitative patterns of protein in the synthesis in the preimplantation mouse embryo. I. Normal pregnancy. Dev Biol 44: 148–157, 1975.PubMedCrossRefGoogle Scholar
  91. 91.
    Fourcroy JL: RNA synthesis in immature mouse oocyte development. J Exp Zool 219: 257–266, 1982.PubMedCrossRefGoogle Scholar

Copyright information

© Martinus Nijhoff Publishers, Boston, The Hague, Dordrecht, Lancaster 1984

Authors and Affiliations

  • Antonio Coimbra
    • 1
  • Carlos Azevedo
    • 2
  1. 1.Institute of Histology and Embryology Faculty of MedicineUniversity of OportoOportoPortugal
  2. 2.Department of Cell Biology Institute of Biomedical SciencesUniversity of OportoOportoPortugal

Personalised recommendations