Skip to main content
Log in

Evolution and ultrastructure of the bovine spermatogonia precursor cell line

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The spermatogonial stem cell line in prepubertal and adult bovine testis was studied by electron microscopy and protein gene product 9.5 immunohistochemistry. Three successive spermatogonia precursor cell configurations were observed. Small basal stem cells were found to possess a spherical shape and nuclei with two to three nucleoli. They were observed in prepubertal testes (25 and 30 weeks) and in low numbers during all the stages of the seminiferous epithelial cycle in the adult. Aggregated spermatogonia precursor cells are the dominating germ cell type in the 25-week-old and 30-week-old calf. In the adult seminiferous epithelium, they cause expansion of the basal tubular compartment as they form dense groups containing up to 15 cells. These groups are observed concomitantly with cycling A-spermatogonia and preleptotenes at the beginning of spermatocytogenesis. At the end of A-spermatogonia propagation, the aggregated spermatogonia precursor cells separate and intermingle with cycling A-spermatogonia. The spermatogonia precursor cells can later be found together with I-spermatogonia as members of an interconnected cellular network of medium-sized cells. When the I-spermatogonia divide to form the smaller B-spermatogonia, the precursor cells, which stay connected with the cycling spermatogonial population, pass through a growth phase. They can now be considered as committed spermatogonia precursor cells and are continuously being transformed into A1-spermatogonia to start a new round of spermatocytogenesis. Ultrastructurally, all members of the precursor cell line are similar. However, a number of features have been found to show a quantitative increase (endoplasmic reticulum, mitochondria) or to exhibit a rising degree of complexity (nucleolus) during the progression from basal stem cells to committed spermatogonia precursor cells.

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

  • Amann RP (1962) Reproductive capacity of dairy bulls. IV. Spermatogenesis and testicular germ cell degeneration. Am J Anat 110:69–78

    Google Scholar 

  • Clermont Y (1972) Kinetics of spermatogenesis in mammals seminferous epithelium cycle and spermatogonial renewal. Physiol Rev 52:198–236

    Google Scholar 

  • De Rooij DG (1973) Spermatogonial stem cell renewal in the mouse. I. Normal situation. Cell Tissue Kinet 6:281–287

    Google Scholar 

  • Ekstedt E, Söderquist L, Plöen L (1986) Fine structure of spermatogenesis and Sertoli cells (Epitheliocytus sustentans) in the bull. Anat Histol Embryol 15:23–48

    Google Scholar 

  • Ertl C, Wrobel KH (1992) Ultrastructure and morphometry of prepuberal postnatal germ cell development in the bovine testis. Reprod Dom Anim 27:73–84

    Google Scholar 

  • Forssmann WG, Ito S, Weihe E, Aoki A, Dym M, Fawcett DW (1977) An improved perfusion fixation method of the testis. Anat Rec 188:307–314

    Google Scholar 

  • Hilscher B (1981) Spermatogoniogenesis, an interacting proliferation process between stem cell spermatogonia and differentiating spermatogonia. Fortschr Androl 7:46–57

    Google Scholar 

  • Hilscher B, Hilscher W, Maurer W (1969) Autoradiographische Untersuchungen zum Modus der Proliferation und Regeneration des Samenepithels der Wistarratte. Z Zellforsch 94:593–604

    Google Scholar 

  • Hochereau-de Reviers MT (1970) Etude des dividions spermatogoniales et du renouvellement de la spermatogonie souche chez le taureau. Thèse, Université Paris

  • Hochereau-de Reviers MT (1976) Variation in the stock of testicular stem cells and in the yield of spermatogonial division in ram and bull testes. Andrologia 8:137–146

    Google Scholar 

  • Hochereau-de Reviers MT (1981) Control of spermatogonial multiplication. In: McKerns KW (ed) Reproductive processes and contraception. Plenum Press, New York London, pp 307–331

    Google Scholar 

  • Hochereau-de Reviers MT, Monet-Kuntz C, Courot M (1987) Spermatogenesis and Sertoli cell numbers and function in rams and bulls. J Reprod Fertil [Suppl] 34:101–114

    Google Scholar 

  • Hochereau-de Reviers MT, Courtens JL, Courot M, Reviers M de (1990) Spermatogenesis in mammals and birds. In: Lamming GE (ed) Marshall's physiology of reproduction, vol 2. Reproduction in the male, 4th edn. Churchill Livingstone, Edinburgh London Melbourne, pp 106–182

    Google Scholar 

  • Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580

    Google Scholar 

  • Huckins C (1971) The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat Rec 169:533–558

    Google Scholar 

  • Huckins C, Oakberg EF (1978) Morphological and quantitative analysis in mouse testes using whole-mounted seminiferous tubules. I. The normal testes. Anat Rec 192:519–528

    Google Scholar 

  • Jasani B, Wynford-Thomas D, Thomas ND, Newman GR (1986) Broad-spectrum, non-deleterious inhibition of endogenous peroxidase: LM and EM application (abstract). Histochem J 18:56

    Google Scholar 

  • Kramer MF (1960) Spermatogenesis bij de stier. Proefschrift Rijksuniversiteit Utrecht

    Google Scholar 

  • Kramer MF, Lange A de, Visser MBH (1964) Spermatogonia in the bull. Z Zellforsch 63:735–758

    Google Scholar 

  • Kujat R, Rose C, Wrobel KH (1993) The innervation of the bovine ductus deferens: comparison of a modified acetylcholinesterase-reaction with immunoreactivities of cholinacetyltrans-ferase and panneuronal markers. Histochemistry 99:231–239

    Google Scholar 

  • Lengfelder KD (1978) Elektronenmikroskopische Untersuchungen zur Differenzierung männlicher Keimzellen des Rindes. Inaugural Dissertation, LMU München

  • Lok D, Weenk D, De Rooij DG (1982) Morphology, proliferation and differentiation of undifferentiated spermatogonia in the Chinese hamster and the ram. Anat Rec 203:83–99

    Google Scholar 

  • Meistrich ML, Beek EAB van (1993) Spermatogonial stem cells. In: Desjardins C, Ewing LL (eds) Cell and molecular biology of the testis. Oxford University Press, New York Oxford, pp 266–295

    Google Scholar 

  • Oakberg EF (1971) Spermatogonial stem-cell renewal in the mouse. Anat Rec 169:515–532

    Google Scholar 

  • Ortavant R (1959) Dé oulement et durée du cycle spermatogénétique chez le bélier. Ann Zootech 8:183–321

    Google Scholar 

  • Reynolds EG (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Google Scholar 

  • Richardson KC, Jarett L, Finke HE (1960) Embedding in epoxy resin for ultrathin sectioning in electron microscopy. Stain Technol 35:313–323

    Google Scholar 

  • Schwarzacher HG, Wachtler F (1993) The nucleolus. Anat Embryol 188:515–536

    Google Scholar 

  • Singh Pawar H, Wrobel KH (1991) The Sertoli cell of the water buffalo (Bubalus bubalis) during the spermatogenic cycle. Cell Tissue Res 265:43–50

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Google Scholar 

  • Van Haaster LH, De Rooij DG (1993) Cycle of the seminiferous epithelium in the Djungarian hamster (Phodopus sungorus sungorus). Biol Reprod 48:515–521

    Google Scholar 

  • Wrobel KH, Sinowatz F, Kugler P (1978) Zur funktionellen Morphologie des Rete testis, der Tubuli recti und der Terminalsegmente der Tubuli seminiferi des geschlechtsreifen Rindes. Anat Histol Embryol 7:320–335

    Google Scholar 

  • Wrobel KH, Bickel D, Kujat R, Schimmel M (1995) Configuration and distribution of bovine spermatogonia. Cell Tissue Res 279:277–289

    Google Scholar 

  • Wynford-Thomas D, Jasani B, Newman GR (1986) Immunohistochemical localisation of cell surface receptors using a novel method permitting simple, rapid and reliable LM/EM correlation. Histochem J 18:387–396

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wrobel, KH., Bickel, D., Kujat, R. et al. Evolution and ultrastructure of the bovine spermatogonia precursor cell line. Cell Tissue Res. 281, 249–259 (1995). https://doi.org/10.1007/BF00583394

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00583394

Key words

Navigation