Summary
The nucleoli of dictyate-stage growing oocytes in rat ovaries were examined both with routine electron microscopy and electron microscopy after silver nitrate and ammoniacal silver nitrate (Ag-AS) staining. The nucleoli of the unilaminar follicular oocytes consist of twisted strands of dense fibrillar components, aggregates of granular components, and small fibrillar centers. After Ag-AS staining, silver grains are numerous on the dense fibrillar strands, fewer on the fibrillar centers, and very sporadic on the granular aggregates. The same stainability of three nucleolar components with the Ag-AS method was also confirmed in the nucleoli segregated by actinomycin D. During the transition of growing oocytes from bilaminar to plurilaminar follicle stage, the nucleolar dense fibrillar strands gradually conglomerate and are transformed into large and compact spherules. The stainability of dense fibrillar components with the Ag-AS method was lost along with this nucleolar transformation. These results may provide some new clues on the functional significance of AgAS-positive proteins in the nucleoli.
Similar content being viewed by others
References
Adams EC, Hertig AT (1964) Studies on guinea pig oocytes. I. Electron microscopic observations on the development of cytoplasmic organelles in oocytes of primordial and primary follicles. J Cell Biol 21:397–427
Angelier N, Hernandez-Verdun D, Bouteille M (1982) Visualization of Ag-NOR proteins on nucleolar transcriptional units in molecular spreads. Chromosoma 86:661–672
Bernhard W (1971) Drug-induced changes in the interphase nucleus. In: Clementi F, Ceccarelli B (eds) Advances in cytopharmacology. Vol. 1. Raven Press Publ. New York, pp 49–67
Bourgeois CA, Hernandez-Verdun D, Hubert J, Bouteille M (1979) Silver staining of NORs in electron microscopy. Exp Cell Res 123:449–452
Busch H, Lischwe MA, Michalik J, Chan P-K, 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 Univ Press, Cambridge, pp 43–71
Buys CHCM, Osinga J (1980) Abundance of protein-bound sulfhydryl and disulfide groups of chromosomal nucleolus organizing regions. A cytochemical study on the selective silver staining of NORs. Chromosoma 77:1–11
Chouinard LA (1971) A lightand electron-microscope study of the nucleolus during growth of the oocyte in the prepubertal mouse. J Cell Sci 9:637–663
Chouinard LA (1975) A lightand electron-microscope study of the oocyte nucleus during development of the antral follicle in the prepubertal mouse. J Cell Sci 17:589–615
Crozet N, Motlik J, Szollosi D (1981) Nucleolar fine structure and RNA synthesis in porcine oocytes during the early stages of antrum formation. Biol Cell 41:35–42
Daskal Y, Smetana K, Busch H (1980) Evidence from studies on segregated nucleoli that nucleolar silver staining proteins C23 and B23 are in the fibrillar component. Exp Cell Res 127:285–291
Dimova RN, Markov DV, Gajdardjieva KC, Dabeva MD, Hadjiolov AA (1982) Electron microscopic localization of silver staining NOR-proteins in rat liver nucleoli upon D-galactosamine block of transcription. Eur J Cell Biol 28:272–277
Fourcroy JL (1982) RNA synthesis in immature mouse oocyte development. J Exp Zool 219:257–266
Goessens G (1976) The nucleolar fibrillar centres in various cell types in vivo or in vitro. Cell Tissue Res 173:315–324
Goessens G, Lepoint A (1982) Localization of Ag NOR-proteins in Ehrlich tumour cell nucleoli. Biol Cell 43:139–142
Goodpasture C, Bloom SE (1975) Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma 53:37–50
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
Hartung M, Keeling JW, Patel C, Bobrow M, Stahl A (1983) Nucleoli, micronucleoli, and nucleolus-like structures in human oocytes at meiotic prophase I studied by the silver-NOR technique. Cytogenet Cell Genet 35:2–8
Hernandez-Verdun D, Derenzini M, Bouteille M (1980) The morphological relationship in electron microscopy between NORsilver proteins and intranucleolar chromatin. Chromosoma 85:461–473
Hernandez-Verdun D, Hubert J, Bourgeois CA, Bouteille M (1980) Ultrastructural localization of Ag-NOR stained proteins in the nucleolus during the cell cycle and in other nucleolar structures. Chromosoma 79:349–362
Hervás JP, Santa-Cruz MC, Crespo D, Villegas J, Lafarga M (1981) Silver staining of the neuronal nucleus in electron microscopy: nucleolar organization in supraoptic nuclei of the rat hypothalamus. Anat Embryol 163:265–273
Howell WM (1977) Visualization of ribosomal gene activity: silver stains proteins associated with rRNA transcribed from oocyte chromosomes. Chromosoma 62:361–367
Kling H, Lepore L, Krone W, Olert J, Sawatzki G (1980) Chemical studies on the silver staining of nucleoli. Experientia 36:249–250
Lischwe MA, Smetana K, Olson MOJ, Busch H (1979) Proteins C23 and B23 are the major nucleolar silver staining proteins. Life Sci 25:701–708
Mirre C, Knibiehler B (1982) A re-evaluation of the relationships between the fibrillar centres and the nucleolus-organizing regions in reticulated nucleoli: ultrastructural organization, number and distribution of the fibrillar centres in the nucleolus of the mouse Sertoli cell. J Cell Sci 55:247–259
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
Mirre C, Stahl A (1981) Ultrastructural organization, sites of transcription and distribution of fibrillar centres in the nucleolus of the mouse oocyte. J Cell Sci 48:105–126
Mirre C, Hartung M, Stahl A (1980) Association of ribosomal genes in the fibrillar center of the nucleolus: a factor influencing translocation and nondisjunction in the human meiotic oocyte. Proc Natl Acad Sci USA 77:6017–6021
Moore GPM, Lintern-Moore S, Peters H, Faber M (1974) RNA synthesis in the mouse oocyte. J Cell Biol 60:416–422
Oakberg EF (1968) Relationship between stage of follicular development and RNA synthesis in the mouse oocyte. Mutat Res 6:155–165
Odor DL, Blandau RJ (1969) Ultrastructural studies on fetal and early postnatal mouse ovaries. II. Cytodifferentiation. Am J Anat 125:177–216
Olert J, Sawatzki G, Kling H, Gebauer J (1979) Cytological and histochemical studies on the mechanism of the selective silver staining of nucleolus organizer regions (NORs). Histochemistry 60:91–99
Palombi F, Viron A (1977) Nuclear cytochemistry of mouse oogenesis. 1. Changes in extranucleolar ribonucleoprotein compnents through meiotic prophase. J Ultrastruct Res 61:10–20
Pébusque M-J, Seite R (1981) Electron microscopic studies of silver-stained proteins in nucleolar organizer regions: location in nucleoli of rat sympathetic neurons during light and dark periods. J Cell Sci 51:85–94
Pébusque M-J, Vio M, Seïte R (1981) Ultrastructural location of Ag-NOR stained proteins in nucleoli of rat sympathetic neurons during the dark period. Biol Cell 40:151–154
Recher L, Sykes JA, Chan H (1976) Further studies on the mammalian cell nucleolus. J Ultrastruct Res 56:152–163
Schoefl GI (1964) The effect of actinomycin D on the fine structure of the nucleolus. J Ultrastruct Res 10:224–243
Schwarzacher HG, Mikelsaar A-V, Schnedl W (1978) The nature of the Ag-staining of nucleolus organizer regions. Electronand light-microscopic studies on human cells in interphase, mitosis, and meiosis. Cytogenet Cell Genet 20:24–39
Stahl A (1982) The nucleolus and nucleolar chromosomes. In: Jordan EG, Cullis CA (eds) The nucleolus. Cambridge Univ Press, Cambridge, pp 1–24
Takeuchi IK, Sonta S (1983) Silver staining of the nucleolus-like bodies in postimplantation rat embryos and the nuage in Chinese hamster oocytes. J Electron Microsc 32:176–179
Wasserman PM, Josefowicz WJ (1978) Oocyte development in the mouse: an ultrastructural comparison of oocytes isolated at various stages of growth and meiotic competence. J Morphol 156:209–236
Weakley BS (1966) Electron microscopy of the oocyte and granulosa cells in the developing ovarian follicles of the golden hamster (Mesocricetus auratus). J Anat 100:503–534
Williams MA, Kleinschmidt JA, Krohne G, Franke WW (1982) Argyrophilic nuclear and nucleolar proteins of Xenopus laevis oocytes identified by gel electrophoresis. Exp Cell Res 137:341–351
Zamboni L (1972) Comparative studies on the ultrastructure of mammalian oocytes. In: Biggers JD, Schuetz AW (eds) Oogenesis. Univ Park Press, Baltimore, pp 5–45
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Takeuchi, I.K. Electron-microscopic study of silver staining of nucleoli in growing oocytes of rat ovaries. Cell Tissue Res. 236, 249–255 (1984). https://doi.org/10.1007/BF00214225
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00214225