Skip to main content
Log in

A cytochemical study of the nucleolus and nucleolus-related structures during human spermatogenesis

  • Original Articles
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Besides the components of typical nucleoli, three other nuclear structures were identified in spermatogonia by positive silver staining: dense centers, fibrillar regions, and dense granules. There was a close relationship between the dense centers and fibrillar regions in spermatogonia and spermatocytes, whereas the dense granules, which appeared dispersed throughout the nucleoplasm of spermatogonia, became localized at the periphery of chromosomes in spermatocytes. From the beginning of spermiogenesis, these three structures then appeared in direct relationship with the dense fibrillar component of the nucleolus. At the Golgi phase, a new nuclear structure also appeared in close relationship with the dense fibrillar component. As it was morphologically similar to the fibrillar region, but not silver stained, it was designated fibrillar structure. With further spermatid development, as the dense fibrillar component gradually disappeared, a sharp increase in the number of the associated dense granules was observed; these granules then disappeared as well. In spermatids at cap phase, each fibrillar region appeared intimately associated with several fibrillar structures. In maturing spermatids, silver staining became confined to the fibrils that appeared located inside the nuclear vacuole. The nuclear vacuole also contained a dense fibrillar structure in intimate relationship with these fibrils and the peripheral condensed chromatin. Ethidium bromide-PTA, Na-tungstate and EDTA regressive staining suggest the presence of RNP in the fibrillar regions, dense granules and intravacuolar fibrils, and the presence of DNP in the fibrillar structures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arroua M-L, Hartung M, DeVictor M, Berge-Lefranc J-L, Stahl A (1982) Localization of ribosomal genes by in situ hybridization in the fibrillar centre of the nucleolus in the human spermatocyte. Biol Cell 44:337–340

    Google Scholar 

  • Bernhard W (1969) A new staining procedure for electron microscopical cytology. J Ultrastruct Res 27:250–265

    CAS  PubMed  Google Scholar 

  • Biggiogera M, Biggiogera FF (1989) Ethidium bromide- and propidium iodide-PTA staining of nucleic acids at the electron microscopic level. J Histochem Cytochem 37:1161–1166

    Google Scholar 

  • Biggiogera M, Kaufmann SH, Shaper JH, Gas N, Amalric F, Fakan S (1991) Distribution of nucleolar proteins B23 and nucleolin during mouse spermatogenesis. Chromosoma 100:162–172

    Google Scholar 

  • Borer RA, Lehner CF, Eppenberger HM, Nigg EA (1989) Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell 56:379–390

    Google Scholar 

  • Courtens JL, Biggiogera M, Fakan S (1991) A cytochemical and immunocytochemical study of DNA distribution in spermatid nuclei of mouse, rabbit, and bull. Cell Tissue Res 265:517–525

    Google Scholar 

  • Czaker R (1985a) Ultrastructural observations on nucleolar changes during mouse spermiogenesis. Andrologia 17:42–53

    Google Scholar 

  • Czaker R (1985b) Distinct argyrophilic cytoplasmic organelles revealed during mouse spermiogenesis. A fine structural and cytochemical study. Anat Embryol 172:247–254

    Google Scholar 

  • Dadoune JP, Alfonsi MF (1986) Ultrastructural and cytochemical changes of the head components of human spermatids and spermatozoa. Gamete Res 14:33–46

    Google Scholar 

  • Dadoune J-P, Alfonsi M-F, Fain-Maurel M-A (1991) Cytochemical variations in the nucleolus during spermiogenesis in man and monkey. Cell Tissue Res 264:167–173

    Google Scholar 

  • Erard MS, Belenguer P, Caizergues-Ferrer M, Pantaloni A, Amalric F (1988) A major nucleolar protein, nucleolin, induces chromatin decondensation by binding to histone H1. Eur J Biochem 175:525–530

    Google Scholar 

  • Goodpasture C, Bloom SE (1975) Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining. Chromosoma 53:37–50

    Google Scholar 

  • Hartung M, Wachtier F, De 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 22:25–37

    Google Scholar 

  • Hernandez-Verdun D (1991) The nucleolus today. J Cell Sci 99:465–471

    Google Scholar 

  • Hernandez-Verdun D, Derenzini M, Bouteille M (1982) The morphological relationship in electron microscopy between NOR-silver proteins and intranucleolar chromatin. Chromosoma 85:461–473

    Google Scholar 

  • Holstein AF, Roosen-Runge EC (1981) Atlas of human spermatogenesis. Grosse, Berlin

    Google Scholar 

  • Hozak P, Roussel P, Hernandez-Verdun D (1992) Procedures for specific detection of silver-stained nucleolar proteins on western blots. J Histochem Cytochem 40:1089–1096

    CAS  Google Scholar 

  • Jordan EG (1984) Nucleolar nomenclature. J Cell Sci 67:217–220

    Google Scholar 

  • Paniagua R, Nistal M, Amat P, Rodriguez MC (1986) Ultrastructural observations on nucleoli and related structures during human spermatogenesis. Anat Embryol 174:301–306

    Google Scholar 

  • Pessot CA, Brito M, Figueroa J, Concha II, Yanez A, Burzio LO (1989) Presence of RNA in the sperm nucleus. Biochem Biophys Res Commun 158:272–278

    Google Scholar 

  • Roussel P, Belenguer P, Amalric F, Hernandez-Verdun D (1992) Nucleolin is an Ag-NOR protein; this property is determined by its amino-terminal domain independently of its phosphorylation state. Exp Cell Res 203:259–269

    Google Scholar 

  • Rowley MJ, Berlin JD, Heller CG (1971) The ultrastructure of four types of human spermatogonia. Z Zellforsch Mikrosk Anat 112:139–157

    Google Scholar 

  • Schulze C (1979) Morphological characteristics of the spermatogonial stem cells in man. Cell Tissue Res 198:191–199

    Google Scholar 

  • Sousa M, Azevedo C (1988) Ultrastructure and silver-staining analysis of spermatogenesis in the sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). J Morphol 195:177–188

    Google Scholar 

  • Sousa M, Azevedo C (1990) Ultrastructure and AG staining of Echinoderm spermatogenesis. In: Dale B (ed) Mechanism of fertilization: plants of humans. NATO ASI Series, vol H45. Springer, New York Berlin Heidelberg, pp 115–129

    Google Scholar 

  • Sousa M, Azevedo C (1992) Silver staining of the postacrosomal sheath during human spermiogenesis. Anat Embryol 185:271–274

    Google Scholar 

  • Stahl A, Wachtler F, Hartung M, DeVictor M, Schofer C, Mosgoller W, De Lanversin A, Fouet C, Schwarzacher HG (1991) Nucleoli, nucleolar chromosomes and ribosomal genes in the human spermatocyte. Chromosoma 101:231–244

    Google Scholar 

  • Stockert JC (1977) Sodium tungstate as a stain in electron microscopy. Biol Cell 29:211–214

    Google Scholar 

  • Tesarik J, Kopecny V (1989) Nucleic acid synthesis and development of human male pronucleus. J Reprod Fertil 86:549–558

    Google Scholar 

  • Tesarik J, Kopecny V (1990) Assembly of the nucleolar precursor bodies in human male pronuclei is correlated with an early RNA synthetic activity. Exp Cell Res 191:153–156

    Google Scholar 

  • Tesarik J, Kopency V, Plachot M, Mandelbaum J, Da Lage C, Fléchon J-E (1986) Nucleologenesis in the human embryo developing in vitro: ultrastructural and autoradiographic analysis. Dev Biol 115:193–203

    Google Scholar 

  • 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 101:777–791

    Google Scholar 

  • Tres LL (1975) Nucleolar RNA synthesis of meiotic prophase spermatocytes in the human testis. Chromosoma 53:141–151

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sousa, M., Carvalheiro, J. A cytochemical study of the nucleolus and nucleolus-related structures during human spermatogenesis. Anat Embryol 190, 479–487 (1994). https://doi.org/10.1007/BF00235495

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00235495

Key words

Navigation