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Postnatal development of the tubular lamina propria and the intertubular tissue in the bovine testis

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Summary

The postnatal development of intertubular cells and vessels and of the tubular lamina propria was studied in three locations of perfusion-fixed bovine testes from 31 animals ranging from 4 to 78 weeks. The postnatal morphological differentiation of the testis is not uniform, regional differences have to be considered. The intertubular cell population is composed of mesenchyme-like cells, fibrocytes, Leydig cells, peritubular cells and mononuclear cells. In 4 and 8-week-old testes mesenchyme-like cells are the dominating element. These pluripotent cells proliferate by frequent mitoses and are the precursors of Leydig cells, contractile peritubular cells and fibrocytes. Morphologically differentiated Leydig cells are encountered throughout the entire period of postnatal development. In 4-week-old testes degenerating fetal and newly formed postnatal Leydig cells are seen in juxtaposition to each other. From the 8th week on, only postnatal Leydig cells are present. Between 16 and 30 weeks large-scale degeneration of prepuberal Leydig cells is observed. The Leydig cells that survive this degenerative phase constitute the long-lasting adult population. 20–30% (numerically) of all intertubular cells at all ages are free mononuclear cells. These are found as lymphocytes, plasma cells, monocytes, macrophages and light intercalated cells (LIC). The latter are monocyte-derived, Leydig cell-associated typical cells of the bovine testis. The differentiation of the two main components of the tubular lamina propria, (i) basal lamina and (ii) peritubular cell sheath, seems to be effected rather independent from each other and also from hormonal signals important for the development of the germinal cells. The laminated basal lamina reaches nearly 3 μm at 16 weeks and is later on continuously reduced. At 25 weeks the peritubular cells have transformed into contractile myofibroblasts. At this period the germinal epithelium is still in a prepuberal state.

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References

  • Abdel-Raouf M (1960) The postnatal development of the reproductive organs in bulls with special reference to puberty. Acta Endocrinol (Kbh) [Suppl] 49

  • Amann RP (1962) Reproductive capacity of dairy bulls. III. The effect of ejaculation frequency, unilateral vasectomy, and age on spermatogenesis. Am J Anat 110:49–67

    Google Scholar 

  • Aoki A, Fawcett DW (1975) Impermeability of Sertoli cell junctions to prolonged exposure to peroxidase. Andrologia 7:63–76

    Google Scholar 

  • Attal J, Courot M (1963) Développement testiculaire et établissement de la spermatogenèse chez le Taureau. Ann Biol Anim Biochim Biophys 3:219–241

    Google Scholar 

  • Bascom KF (1923) The interstitial cells of the gonads of cattle with special reference to their embryonic development and significance. Am J Anat 31:223–259

    Google Scholar 

  • Berliner DL, Nabors CJ, Dougherty TF (1964) The role of hepatic and adrenal reticuloendothelial cells in steroid biotransformation. J Reticuloendothel Soc 1:1–17

    Google Scholar 

  • Bressler RS, Ross MH (1969) Pituitary involvement in testicular peritubular cell maturation. Anat Rec 163:158–159

    Google Scholar 

  • Bustos-Obregón E, Courot M (1974) Ultrastructure of the lamina propria in the ovine seminiferous tubule. Development and some endocrine considerations. Cell Tissue Res 150:481–492

    Google Scholar 

  • Curtis SK, Amann RP (1981) Testicular development and establishment of spermatogenesis in Holstein bulls. J Anim Sci 53:1645–1657

    Google Scholar 

  • Dierichs R, Wrobel KH (1973) Licht- und elektronenmikroskopische Untersuchungen an den peritubulären Zellen des Schweinehodens während der postnatalen Entwicklung. Z Anat Entwickl Gesch 143:49–64

    Google Scholar 

  • Fawcett DW, Neaves WB, Flores MN (1973) Comparative observations on intertubular lymphatics and the organization of the interstitial tissue of the mammalian testis. Biol Reprod 9:500–532

    Google Scholar 

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

    Google Scholar 

  • Fossland RC, Schultze AB (1961) A histological study of the postnatal development of the bovine testis. Res Bull Univ Nebraska Agric Exper Stat 199:3–16

    Google Scholar 

  • Hooker CW (1944) The postnatal history and functions of the interstitial cells of the testis of the bull. Am J Anat 74:1–38

    Google Scholar 

  • Hovatta O (1972) Effect of androgens and antiandrogens on the development of the myoid cells of the rat seminiferous tubules (organ culture). Z Zellforsch 131:299–308

    Google Scholar 

  • Hullinger RL, Wensing CJG (1985) Testicular organogenesis in the fetal calf: interstitial endocrine (Leydig) cell development. Acta Anat 121:99–109

    Google Scholar 

  • Humphrey JD, Ladds PW (1975) A quantitative histological study of changes in the bovine testis and epididymis associated with age. Res Vet Sci 19:135–141

    Google Scholar 

  • Kormano M, Hovatta O (1972) Contractility and histochemistry of the myoid cell layer of the rat seminiferous tubules during postnatal development. Z Anat Entwickl Gesch 137:239–248

    Google Scholar 

  • Leeson CR, Forman DE (1981) Postnatal development and differentiation of contractile cells within the rabbit testis. J Anat 132:491–511

    Google Scholar 

  • Milewich L, Chen GT, Lyons C, Tucker TF, Uhr JW, MacDonald PC (1982) Metabolism of androstenedione by guinea-pig peritoneal macrophages: synthesis of testosterone and 5α-reduced metabolites. J Steroid Biochem 17:61–65

    Google Scholar 

  • Miller SC (1982) Localization of plutonium-241 in the testis. An interspecies comparison using light and electron microscope autoradiography. Int J Radiat Biol 41:633–643

    Google Scholar 

  • Nistal M, Paniagua R, Regadera J, Santamaria L, Amat P (1986) A quantitative morphological study of human Leydig cells from birth to adulthood. Cell Tissue Res 246:229–236

    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

    Article  CAS  PubMed  Google Scholar 

  • Ross MH (1967) The fine structure and development of the peritubular contractile cell component in the seminiferous tubules of the mouse. Am J Anat 121:523–558

    Google Scholar 

  • Russell JJ, Lindenbaum A (1979) One-year study of nonuniformly distributed plutonium in mouse testis as related to spermatogonial irradiation. Health Phys 36:153–157

    Google Scholar 

  • Scheubeck M, Wrobel KH (1984) Eine einfache transportable Apparatur zur Durchführung von Perfusionsfixierungen. Mikroskopie 41:108–111

    Google Scholar 

  • Schrag D (1983) Licht- und elektronenmikroskopische Untersuchungen zur fetalen Differenzierung der männlichen Keimdrüse des Rindes. Inaug Diss LMU München

    Google Scholar 

  • Schwark HJ, Lühmann P, Carl WD (1972) Untersuchungen an Hoden von Jungbullen. 1. Mitt.: Die Entwicklung der Hoden und deren Beziehung zur Altersund Körpermasseentwicklung und zu einigen Spermamerkmalen. Monatsh Veterinärmed 27:172–176

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ströbel H (1967) Histometrische Untersuchungen am Hodeninterstitium von Stieren mit Störungen der Spermatogenèse und der Libido. Inaug Diss LMU München

    Google Scholar 

  • Strübing Ch (1986) Morphologische Veränderungen in nicht hormonsubstituierten Organkulturen von Hodenparenchym adulter männlicher Rinder. Dipl Arb (Biol) Regensburg

    Google Scholar 

  • Swierstra EE (1966) Structural composition of shorthorn bull testes and daily spermatozoa production as determined by quantitative testicular histology. Can J Anim Sci 46:107–119

    Google Scholar 

  • Vernon-Roberts B (1972) The Macrophage. University Press, Cambridge

    Google Scholar 

  • Wrobel KH, El Etreby MF (1971) Enzymhistotopochemie an der männlichen Keimdrüse des Rindes während ihrer fetalen und postnatalen Entwicklung. Histochemie 26:160–179

    Google Scholar 

  • Wrobel KH, Schilling E, Dierichs R (1973) Enzymhistochemische Untersuchungen an den Leydigzellen des Schweines während der postnatalen Ontogenese. Histochemie 36:321–333

    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. Zentralbl Veterinärmed (C) Anat Histol Embryol 7:320–335

    Google Scholar 

  • Wrobel KH, Mademann R, Sinowatz F (1979) The lamina propria of the bovine seminiferous tubule. Cell Tissue Res 202:357–377

    Google Scholar 

  • Wrobel KH, Sinowatz F, Mademann R (1981) Intertubular topography in the bovine testis. Cell Tissue Res 217:289–310

    Google Scholar 

  • Wrobel KH, Schilling E, Zwack M (1986) Postnatal development of the connexion between tubulus seminiferus and tubulus rectus in the bovine testis. Cell Tissue Res 246:387–400

    Google Scholar 

  • Yee JB, Hutson JC (1983) Testicular macrophages: isolation, characterization and hormonal responsiveness. Biol Reprod 29:1319–1326

    Google Scholar 

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To Dr. E. Schilling, Mariensee, on the occasion of his 65th birthday

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Wrobel, KH., Dostal, S. & Schimmel, M. Postnatal development of the tubular lamina propria and the intertubular tissue in the bovine testis. Cell Tissue Res. 252, 639–653 (1988). https://doi.org/10.1007/BF00216652

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