Summary
The present light and electron microscopic study deals with the morphology and cytochemical properties of the nucleolus in mature granule cells of the rat cerebellum. Nucleolar organization has been examined by several different methodological approaches: (a) determination of the number of nucleoli per cell from smear preparations, (b) morphometric estimation of nucleolar size, and (c) ultrastructural and cytochemical characterization of nucleolar components. The mean number of nucleoli per cell was found to be 1.46 ± 0.02 (mean ± SEM). The morphometric measurement of the nucleolar area showed an average value of 0.359 ± 0.07 μm2 (mean ± SDM). At the electron microscope level, most granule cell nucleoli displayed a fine texture which does not differ substantially from the ‘ring-shaped’ configuration usually found in cells with low levels of protein synthesis activity; i.e., a large round fibrillar centre surrounded by the dense fibrillar component, and small masses of granular component segregated from the preceding constituents. The meaning of this nucleolar configuration is discussed in the light of recent ultrastructural and biochemical data on nucleolar function. A relationship between this pattern of nucleolar organization and metabolic characteristics of the granule cells is suggested.
Similar content being viewed by others
References
Altman, J. (1963) Regional utilization of leucine (3H) by normal rat brain: microdensitometric evaluations of autoradiograms.Journal of Histochemistry and Cytochemistry 11, 74–85.
Bernhard, W. (1969) A new staining procedure for electron microscopical cytology.Jaurnal of Ultrastructure Research 27, 250–65.
Busch, H., Daskal, Y., Giorkey, F. &Smetana, K. (1979) Silver staining of nucleolar granules in tumor cells.Cancer Research 39, 857–63.
Buschmann, MB. T. &Lavelle, A. (1981) Morphological changes of the pyramidal cell nucleolus and nucleus in hamster frontal cortex during development and aging.Mechanisms of Ageing and Development 15, 385–97.
Cajal, S. R. (1911)Histologie du systeme nerveux de l'homme et des vertebrés, Vol. 2, pp. 32–42. Paris: Maloine.
Derenzini, M., Farabegoli, F., Pession, A. &Novello, F. (1987) Spatial redistribution of ribosomal chromatin in the fibrillar centres of human circulating lymphocytes after stimulation of transcription.Experimental Cell Research 170, 31–41.
Goessens, G. (1984) Nucleolar structure.International Review of Cytology 87, 107–57.
Hadjiolov, A. A. (1985)The Nucleolus and Ribosome Biogenesis, New York: Springer.
Hernandez-Verdun, D. (1986) Structural organization of the nucleolus in mammalian cells. InMethods and Achievements in Experimental Pathology (edited byJasmin, G. &Simard, R.), pp. 26–62. Basel: S. Karger.
Hervas, J. P., Santa-Cruz, M. C., Crespo, D., Villegas, J. &Laf.Arga, M. (1981) Silver staining of the neuronal nucleus in electron microscopy: nucleolar organization in supraoptic nuclei of the rat hypothalamus.Anatomy and Embryology 163, 265–73.
Howell, W. M., &Black, D. A. (1980) Controlled silver staining of nucleolus organizer regions with a protectivecolloidal developer: 1 step method.Experientia 36, 1014–5.
Ito, M. (1984)The Cerebellum and Neural Control, pp. 74–85. New York: Raven Press.
Jordan, E. G. (1984) Nucleolar nomenclature.Journal of Cell Science 67, 217–20.
Jordan, E. G. &Mcgovern, J. H. (1981) The quantitative relationship of the fibrillar centres and other nucleolar components to changes in growth conditions, serum deprivation and low doses of actynomycin D in cultured diploid human fibroblast (strain MRC-5).Journal of Cell Science 52, 373–89.
Jordan, E. G., Martini, G., Bennet, M. D. &Flavell, R. B. (1982) Nucleolar fusion in wheat.Journal of Cell Science 56, 485–95.
Kano, Y., Maeda, S. &Sugiyama, T. (1976) The location of ribosomal cistrons (r-DNA) in chromosomes of the rat.Chromosoma 55, 37–42.
Lafarga, M., Villegas, J. &Cresfo, D. (1985) Changes in nucleolar morphology and volume of the supraoptic nucleus neurons during postnatal development of the rat.Developmental Brain Research 22, 310–13.
Lafarga, M., Gonzalez, C. &Berciano, M. T. (1986a) An improved cytological silver staining method for the demonstration of neuronal nuclear bodies.Journal of Neuroscience Methods 18, 317–24.
Lafarga, M., Hervas, J. P., Berciano, M. T. &Silos, I. (1986b) Nuclear organization in cerebellar granule cells: a morphometric and stereological approach.Neuroscience Letters [Supplement] 26, S481.
Lee, G. M., Rasch, E. M. &Thornthwaite, J. T. (1984) Cytophotometric comparisons of DNA levels in neuronal and glial cells of the cerebellum: a comparative study.Cell Biochemistry and Function 2, 225–36.
Lischwe, M. A., Smetana, K., Olson, M. O. J. &Busch, H. (1979) Proteins C23 and B23 are the major nucleolar silver staining proteins.Life Sciences 25, 701–8.
Lischwe, M. A., Richards, R. L., Busch, R. K. &Busch, H. (1981) Localization of phosphoprotein C23 to nucleolar structures and to the nucleolus organizer regions.Experimental Cell Research 136, 101–9.
Manuelidis, L. (1984a) Active nucleolar organizers are precisely positioned in adult central nervous system cells but not in neuroectodermal tumor cells.Journal of Neuropathology and Experimental Neurology 43, 225–41.
Manuelidis, L. (1984b) Different central nervous system cell types display distinct and nonrandom arrangements of satellite DNA sequences.Proceedings of the National Academy of Sciences USA 81, 3123–7.
Miller, L. &Gonzales, F. (1976) The relationship of ribosomal RNA synthesis to the formation of segregated nucleoli and nucleolus like bodies.Journal of Cell Biology 71, 939–45.
Moreno, F. J., Hernandez-Verdun, D., Masson, C. &Bouteille, M. (1985) Silver staining of the nucleolar organizer regions (NORs) on Lowicril and cryo-ultrathin sections.Journal of Histochemistry and Cytochemistry 33, 389–99.
Palay, S. &Chan-Palay, V. (1974)Cerebellar Cortex: cytology and organization, pp. 63–99. New York: Springer.
Patel, N. J., Cohen, J. &Balazs, R. (1984) Protein synthesis in cells isolated from the developing rat cerebellum.International Journal of Developmental Neuroscience 2, 287–99.
Peters, A., Palay, S. L. &Webster, H. Def. (1976)The Fine Structure of the Nervous System: The Neurons and Supporting Cells, pp. 47–58. Philadelphia: Saunders.
Popp, W. &Wachtler, F. (1983) Changes in nucleolar structure, number and size in cellular activation and inactivation. Observations in human phytohaemagglu-tinin-treated lymphocytes.Cell and Tissue Research 234, 377–88.
Raska, I., Armbruster, B. L., Frey, J. R. &Smetana, K. (1983) Analysis of ring-shaped nucleoli in serial sections human lymphocytes.Cell and Tissue Research 234, 707–11.
Scheer, U., Hugle, B., Kazan, R. &Rose, K. M. (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-dicloro-β-d-ribofuranosyl-benzimidazole.Journal of Cell Biology 99, 672–79.
Stoykova, A. S., Debeva, M. D., Dimova, R. N. &Hadjiolov, A. A. (1985) Ribosome biogenesis and nucleolar ultrastructure in neuronal and oligodendroglial rat brain cells.Journal of Neurochemistry 45, 1667–76.
Vazquez Nin, G., Echevarria, O. M., Zavala, G., Jimenez-Garcia, L. F., Gonzalez, M. A. &Parra, R. (1986) Relations between nucleolar morphometric parameters and pre-rRNA synthesis and animal and plant cells.Acta Anatomica 126, 141–6.
Wachtler, F. &Schwarzacher, H. G. (1984) On the fusion of nucleoli in interphase.European Journal of Cell Biology 34, 190–2.
Wachtler, F., Hopman, A. H. N., Wiegant, J. &Schwarzacher, H. G. (1986) On the position of nucleolus organizer regions (NORs) in interphase nuclei. Studies with a new, non-autoradiographicin situ hybridization method.Experimental Cell Research 167, 227–40.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lafarga, M., Berciano, M.T., Hervas, J.P. et al. Nucleolar organization in granule cell neurons of the rat cerebellum. J Neurocytol 18, 19–26 (1989). https://doi.org/10.1007/BF01188420
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01188420