Abstract
Silver-staining in the nuclei and chromosomes of spermatogenesis of four species of mammals (Man, Mus musculus, Rattus norvegicus, and Cavia cobaya) was investigated qualitatively and quantitatively. These species show a very similar pattern of activity of the nucleolus organizer regions (NORs) during the various stages of spermatogenesis. Silver precipitates are detectable in growing spermatogonia and up until the pachytene stage of meiotic prophase. During the meiotic metaphases I and II and during interkinesis silver-stainability disappears completely. A resumption of silverstainability occurs in round spermatids indicating a postmeiotic reactivation of NORs. This process does not persist beyond the early elongation phase. The quantitative determination of the silver-covered areas in relation to the total nuclear areas reveals minor differences between the species investigated with regard to the times and extents of maximum activation. The known localizations of the NORs in the karyotypes of the species investigated was confirmed using metaphase-preparations derived from somatic tissues.
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Barlow, P., Vosa, C.G.: The Y chromosome in human spermatozoa. Nature (Lond.) 226, 961–962 (1970)
Beatty, R.A.: The genetics of the mammalian gamete. Biol. Rev. 45, 73–119 (1970)
Betlach, C.J., Erickson, R.P.: 28S and 18S ribonucleic acid from mammalian spermatozoa. J. Exp. Zool. 198, 49–56 (1976)
Clermont, Y., Leblond, C.P.: Spermiogenesis of man, monkey, ram and other mammals as shown by the Periodic Acid-Schiff technique. Amer. J. Anat. 96, 229–254 (1955)
Committee for a standardized karyotype of Rattus norvegicus. Standard karyotype of the Norway rat, Rattus norvegicus. Cytogenet. Cell Genet. 12, 199–205 (1973)
Elsdale, T.R., Fischberg, M., Smith, S.: A mutation that reduces nucleolar number in Xenopus laevis. Exp. Cell Res. 14, 642–643 (1958)
Dym, M., Fawcett, D.W.: Further observations on the number of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol. Reprod. Fert. 4, 195–215 (1971)
Engel, W., Zenzes, M.T., Schmid, M.: Activation of mouse ribosomal RNA genes at the 2 cell stage. Hum. Genet. 38, 57–63 (1977)
Evans, E.P., Breckon, G., Ford, C.E.: An air-drying method for meiotic preparations from mammalian testes. Cytogenetics 3, 289–294 (1964)
Geraedts, J., Pearson, P.L.: Spatial distribution of chromosomes 1 and Y in human spermatozoa. J. Reprod. Fert. 45, 515–517 (1975)
Geremia, R., D'Agostino, A., Monesi, V.: Biochemical evidence of haploid gene activity in spermatogenesis of the mouse. Exp. Cell Res. 111, 23–30 (1978)
Goodpasture, C., Bloom, S.E.: Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma (Berl.) 53, 37–50 (1975)
Hansmann, I., Gebauer, J., Bihl, L., Grimm, T.: Onset of nucleolus organizer activity in early mouse embryogenesis and evidence for its regulation. Exp. Cell Res. 114, 263–268 (1978)
Henderson, A.S., Eicher, E.M., Yu, M.T., Atwood, K.C.: The chromosomal location of ribosomal DNA sites in the mouse. Chromosoma (Berl.) 49, 155–160 (1974)
Hsu, T.C., Cooper, J.E.K., Mace, Jr., M.L., Brinkley, B.R.: Arrangement of centromeres in mouse cells. Chromosoma (Berl.) 34, 73–87 (1971)
Hsu, T.C., Patton, J.L.: Bone marrow preparations for chromosome studies. In: Comparative mammalian cytogenetics (K. Benirschke, ed.), pp. 454–460. Berlin-Heidelberg-New York: Springer 1969
Kano, Y., Maeda, S., Sugiyama, T.: The location of ribosomal cistrons (rDNA) in chromosomes of the rat. Chromosoma (Berl.) 55, 37–42 (1976)
Kierszenbaum, A.L., Tres, L.L.: Nucleolar and perichromosomal RNA synthesis during meiotic prophase in the mouse testis. J. Cell Biol. 60, 39–53 (1974a)
Kierszenbaum, A.L., Tres, L.L.: Transcription sites in spread meiotic prophase chromosomes from mouse spermatocytes. J. Cell Biol. 63, 923–935 (1974b)
Kierszenbaum, A.L., Tres, L.L.: Structural and transcriptional features of the mouse spermatid genome. J. Cell Biol. 65, 258–270 (1975)
Leblond, C.P., Clermont, Y.: Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann. N. Y. Acad. Sci. 55, 548–573 (1952)
Mayfield, J.E., Ellison, J.R.: The fluorescence localization of mouse satellite DNA in interphase nuclei. Chromosoma (Berl.) 54, 27–31 (1976)
Meredith, R.: A simple method for preparing meiotic chromosomes from mammalian testis. Chromosoma (Berl.) 26, 254–258 (1969)
Mikelsaar, A.-V., Schmid, M., Krone, W., Schwarzacher, H.G., Schnedl, W.: Frequency of Agstained nucleolus organizer regions in the acrocentric chromosomes of man. Hum. Genet. 37, 73–77 (1977)
Miller, D.A., Dev, V.G., Tantravahi, R., Miller, O.J.: Suppression of human nucleolus organizer activity in mouse-human somatic hybrid cells. Exp. Cell Res. 101, 235–243 (1976a)
Miller, O.J., Miller, D.A., Dev, V.G., Tantravahi, R., Croce, C.M.: Expression of human and suppression of mouse nucleolus organizer activity in mouse-human somatic cell hybrids. Proc. nat. Acad. Sci. (Wash.) 73, 4531–4535 (1976b)
Monesi, V.: Synthetic activities during spermatogenesis in the mouse. RNA and protein. Exp. Cell Res. 39, 197–224 (1965)
Monesi, V., Geremia, R., D'Agostino, A., Boitani, C.: Biochemistry of male germ cell differentiation in mammals: RNA synthesis in meiotic and postmeiotic cells. In: Current topics in developmental biology (A.A. Moscona and A. Monroy, eds.), pp. 11–36. New York-San Francisco-London: Academic Press 1978
Moses, M.J.: Synaptonemal complex karyotyping in spermatocytes of the Chinese hamster (Cricetulus griseus). II. Morphology of the XY pair in spread preparations. Chromosoma (Berl.) 60, 127–137 (1977)
Nesbitt, F., Francke, U.: A system of nomenclature for band patterns of mouse chromosomes. Chromosoma (Berl.) 41, 145–158 (1973)
Oakberg, E.F.: A description of spermiogenesis in the mouse and its use in analysis of the cycle of the seminiferous epithelium and germ cell renewal. Amer. J. Anat. 99, 391–413 (1956)
Ohno, S., Kaplan, W.D., Kinosita, R.: Heterochromatic regions and nucleolus organizers in chromosomes of the mouse, Mus musculus. Exp. Cell Res. 13, 358–364 (1957)
Pawlowitzki, I.H., Bosse, H.G.: Y chromosomes associated with vacuoles in human spermatozoa. Hum. Genet. 13, 338–340 (1971)
Pearson, P.L., Bobrow, M., Vosa, C.G.: Technique for identifying Y chromosomes in human interphase nuclei. Nature (Lond.) 226, 78–80 (1970)
Pfeiffer, R.A.: Cell cultures from blood and bone marrow. In: Methods in human cytogenetics (H.G. Schwarzacher and U. Wolf, eds.), pp. 1–37. Berlin-Heidelberg-New York: Springer 1974
Phillips, D.M.: Spermiogenesis. New York-London: Academic Press 1974
Quack, B., Noel, B.: The XY chromosome pair in mouse and human spermatocytes, visualized by silver staining. Nature (Lond.) 267, 431–433 (1977)
Schmid, M., Vogel, W., Krone, W.: Attraction between centric heterochromatin in human chromosomes. Cytogenet. Cell Genet. 15, 66–80 (1975)
Schmid, M., Hofgärtner, F.J., Zenzes, M.T., Engel, W.: Evidence for postmeiotic expression of ribosomal RNA genes during male gametogenesis. Hum. Genet. 38, 279–284 (1977)
Schwarzacher, H.G.: Preparations of metaphase chromosomes. In: Methods in human cytogenetics (H.G. Schwarzacher and U. Wolf, eds.), pp. 71–81. Berlin-Heidelberg-New York: Springer 1974
Schwarzacher, H.G., Mikelsaar, A.-V., Schnedl, W.: The nature of the Ag-staining of nucleolus organizer regions. Electron- and light-microscopic studies on human cells in interphase, mitosis, and meiosis. Cytogenet. Cell Genet. 20, 24–39 (1978)
Stahl, A., Luciani, J.M., Devictor, M., Capodano, A.M., Gagné, R.: Constitutive heterochromatin and micronucleoli in the human oocyte at the diplotene stage. Hum. Genet. 26, 315–327 (1975)
Szabo, P., Lee, M.R., Elder, F.B., Prensky, W.: Localization of 5S RNA and rRNA genes in the Norway rat. Chromosoma (Berl.) 65, 161–172 (1978)
Utakoji, T.: Chronology of nucleic acid synthesis in meiosis of the male Chinese hamster. Exp. Cell Res. 42, 585–596 (1966)
Wolf, U.: Cell cultures from tissue explants. In: Methods in human cytogenetics (H.G. Schwarzacher and U. Wolf, eds.), pp. 39–57. Berlin-Heidelberg-New York: Springer 1974
Wolgemuth-Jarashow, D.J., Jagiello, G.M., Henderson, A.S.: The localization of rDNA in small, nucleolus-like structures in human diplotene oocyte nuclei. Hum. Genet. 36, 63–68 (1977)
Zenzes, M.T., Schmid, M., Engel, W.: Silver-stained nucleolus organizers in the guinea pig, Cavia cobaya. Cytogenet. Cell Genet. 19, 368–372 (1977)
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Hofgärtner, F.J., Schmid, M., Krone, W. et al. Pattern of activity of nucleolus organizers during spermatogenesis in mammals as analyzed by silver-staining. Chromosoma 71, 197–216 (1979). https://doi.org/10.1007/BF00292823
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DOI: https://doi.org/10.1007/BF00292823