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.
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
Clermont Y (1972) Kinetics of spermatogenesis in mammals seminferous epithelium cycle and spermatogonial renewal. Physiol Rev 52:198–236
De Rooij DG (1973) Spermatogonial stem cell renewal in the mouse. I. Normal situation. Cell Tissue Kinet 6:281–287
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
Ertl C, Wrobel KH (1992) Ultrastructure and morphometry of prepuberal postnatal germ cell development in the bovine testis. Reprod Dom Anim 27:73–84
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
Hilscher B (1981) Spermatogoniogenesis, an interacting proliferation process between stem cell spermatogonia and differentiating spermatogonia. Fortschr Androl 7:46–57
Hilscher B, Hilscher W, Maurer W (1969) Autoradiographische Untersuchungen zum Modus der Proliferation und Regeneration des Samenepithels der Wistarratte. Z Zellforsch 94:593–604
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
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
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
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
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
Huckins C (1971) The spermatogonial stem cell population in adult rats. I. Their morphology, proliferation and maturation. Anat Rec 169:533–558
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
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
Kramer MF (1960) Spermatogenesis bij de stier. Proefschrift Rijksuniversiteit Utrecht
Kramer MF, Lange A de, Visser MBH (1964) Spermatogonia in the bull. Z Zellforsch 63:735–758
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
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
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
Oakberg EF (1971) Spermatogonial stem-cell renewal in the mouse. Anat Rec 169:515–532
Ortavant R (1959) Dé oulement et durée du cycle spermatogénétique chez le bélier. Ann Zootech 8:183–321
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
Richardson KC, Jarett L, Finke HE (1960) Embedding in epoxy resin for ultrathin sectioning in electron microscopy. Stain Technol 35:313–323
Schwarzacher HG, Wachtler F (1993) The nucleolus. Anat Embryol 188:515–536
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
Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43
Van Haaster LH, De Rooij DG (1993) Cycle of the seminiferous epithelium in the Djungarian hamster (Phodopus sungorus sungorus). Biol Reprod 48:515–521
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
Wrobel KH, Bickel D, Kujat R, Schimmel M (1995) Configuration and distribution of bovine spermatogonia. Cell Tissue Res 279:277–289
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
Author information
Authors and Affiliations
Rights 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
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00583394