Hormones: what the testis really sees
B. P. SetchellDepartment of Anatomical Sciences, University of Adelaide, Adelaide, SA 5005, Australia. email: brian.setchell@adelaide.edu.au
Reproduction, Fertility and Development 16(5) 535-545 https://doi.org/10.1071/RD03048
Submitted: 21 July 2003 Accepted: 19 November 2003 Published: 22 July 2004
Abstract
Various barriers in the testis may prevent hormones from readily reaching the cells they are supposed to stimulate, especially the hydrophilic hormones from the pituitary. For example, LH must pass through or between the endothelial cells lining the blood vessels to reach the surface of the Leydig cells, and FSH has the additional barrier of the peritubular myoid cells before it reaches the Sertoli cells. The specialised junctions between pairs of Sertoli cells would severely restrict the passage of peptides from blood to the luminal fluid and therefore to the cells inside this barrier, such as the later spermatocytes and spermatids. There is evidence in the literature that radioactively labelled LH does not pass readily into the testis from the blood, and the concentration of native LH in the interstitial extracellular fluid surrounding the Leydig cells in rats is only about one-fifth of that in blood plasma. Furthermore, after injection with LHRH, there are large rises in LH in the blood within 15 min, at which time the Leydig cells have already responded by increasing their content of testosterone, but with no significant change in the concentration of LH in the interstitial extracellular fluid. Either the Leydig cells respond to very small changes in LH, or the testicular endothelial cells in some way mediate the response of the Leydig cells to LH, for which there is now some evidence from co-cultures of endothelial and Leydig cells. The lipophilic steroid hormones, such as testosterone, which are produced by the Leydig cells, have actions within the seminiferous tubules in the testis but also in other parts of the body. They should pass more readily through cells than the hydrophilic peptides; however, the concentration of testosterone in the fluid inside the seminiferous tubules is less than in the interstitial extracellular fluid in the testis, especially after stimulation by LH released after injection of LHRH and despite the presence inside the tubules of high concentrations of an androgen-binding protein. The concentration of testosterone in testicular venous blood does not rise to the same extent as that in the interstitial extracellular fluid, suggesting that there may also be some restriction to movement of the steroid across the endothelium. There is a very poor correlation between the concentrations of testosterone in fluids from the various compartments of the testis and in peripheral blood plasma. Determination of the testosterone concentration in the whole testis is also probably of little predictive value, because the high concentrations of lipid in the Leydig cells would tend to concentrate testosterone there, and hormones inside these cells are unlikely to have any direct effect on other cells in the testis. The best predictor of testosterone concentrations around cells in the testis is the level of testosterone in testicular venous blood, the collection of which for testosterone analysis is a reasonably simple procedure in experimental animals and should be substituted for tissue sampling. There seems to be no simple way of determining the concentrations of peptide hormones in the vicinity of the testicular cells.
Extra keywords: interstitial fluid, luteinising hormone, seminiferous tubule fluid, testosterone.
Anderson, R. A. , and Sharpe, R. M. (2000). Regulation of inhibin production in the human male and its clinical applications. Int. J. Androl. 23, 136–144.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Awoniyi, C. A. , Santulli, R. , Chandrashekar, V. , Schanbacher, B. D. , and Zirkin, B. R. (1989). Quantitative restoration of advanced spermatogenic cells in adult male rats made azoospermic by active immunization against luteinizing hormone or gonadotropin-releasing hormone. Endocrinology 125, 1303–1309.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Awoniyi, C. A. , Sprando, R. L. , Santulli, R. , Chandrashekhar, V. , Ewing, L. L. , and Zirkin, B. R. (1990). Restoration of spermatogenesis by exogenously administered testosterone in rats made azoospermic by hypophysectomy or withdrawal of luteinizing hormone alone. Endocrinology 127, 177–184.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Awoniyi, C. A. , Zirkin, B. R. , Chandrashekhar, V. , and Schlaff, W. D. (1992). Exogenously adminitered testosterone maintains spermatogenesis quantitatively in adult rats actively immunized against gonadotropin-releasing hormone. Endocrinology 130, 3283–3288.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Au, C. L. , Robertson, D. M. , and de Kretser, D. M. (1984). An in-vivo method for estimating inhibin production by adult rat testes. J. Reprod. Fertil. 71, 259–265.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Bartlett, J. M. S. , Weinbauer, G. F. , and Nieschlag, E. (1990). Stability of spermatogenic synchronization achieved by depletion and restoration of vitamin A in rats. Biol. Reprod. 42, 603–612.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Boitani, C. , Stefanini, M. , Fragale, A. , and Morena, A. R. (1995). Activin stimulates Sertoli cell proliferation in a defined period of rat testis development. Endocrinology 136, 5438–5444.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Bollman, J. L. , Cain, J. L. , and Grindley, J. H. (1948). Techniques for the collection of lymph from the liver, small intestine and thoracic duct of the rat. J. Lab. Clin. Med. 33, 1349–1352.
![](../../media/share/OpenURL_Image.gif)
Buhl, A. E. , Cornette, J. C. , Kirton, K. T. , and Yuan, Y.-D. (1982). Hypophysectomized male rats treated with polydimethylsiloxane capsules containing testosterone: effects on spermatogenesis, fertility, and reproductive tract concentrations of androgens. Biol. Reprod. 27, 183–188.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Christensen, A. K. (1975). Leydig cells. In
Cooke, B. A. , de Jong, F. H. , van der Molen, H. J. , and Rommerts, F. F. G. (1972). Endogenous testosterone concentrations in rat testis interstitial tissue and seminiferous tubules during in vitro incubation. Nature 237, 255–256.
![](../../media/share/OpenURL_Image.gif)
de Jong, F. H. (1988). Inhibin. Physiol. Rev. 68, 555–607.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
de Jong, F. H. , Hey, A. H. , and van der Molen, H. J. (1974). Oestradiol-17β and testosterone in rat testis tissue: effect of gonadotropins, localization and production in vitro. J. Endocrinol. 60, 409–419.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
de Kretser, D. M. , Hedger, M. P. , and Phillips, D. J. (1999). Activin A and follistatin: their role in the acute phase reaction and inflammation. J. Endocrinol. 161, 195–198.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Eddie, L. W. , Baker, H. W. G. , Higginson, R. E. , and Hudson, B. (1979). A bioassay for inhibin using pituitary cell cultures. J. Endocrinol. 81, 49–60.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Fawcett, D. W. (1975). Ultrastructure and function of the Sertoli cell. In
Fawcett, D. W. , Leak, L. V. , and Heidger, P. M. (1970). Electron microscopic observations on the structural components of the bloodâtestis barrier. J. Reprod. Fertil. , 105–121.Suppl. .
![](../../media/share/OpenURL_Image.gif)
French, F. S. , and Ritzen, E. M. (1973). Androgen binding protein in efferent duct fluid of rat testis. J. Reprod. Fertil. 32, 479–483.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Ghabriel, M. N. , Lu, J. J. , Hermanis, G. , Zhu, C. , and Setchell, B. P. (2002). Expression of a blood-brain barrier-specific antigen in the reproductive tract of the male rat. Reproduction 123, 389–397.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Ghinea, N. , and Milgrom, E. (1995). Transport of protein hormones through the vascular endothelium. J. Endocrinol. 145, 1–9.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Ghinea, N. , Hai, M. T. V. , Groyer-Picard, M. T. , and Milgrom, E. (1994). How protein hormones reach their target cells. Receptor-mediated transcytosis of hCG through endothelial cells. J. Cell Biol. 125, 87–97.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Gustafsson, K. , Sultana, T. , Zetterstrom, C. K. , Setchell, B. P. , Siddiqui, A. , Weber, G. , and Soder, O. (2002). Production and secretion of interleukin-1α proteins by rat testis. Biochem. Biophys. Res. Commun. 297, 492–497.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Heap, R. B. , Symons, A. M. , and Watkins, J. C. (1970). Steroids and their interactions with phospholipids: solubility, distribution coefficient and effect on potassium permeability of liposomes. Biochim. Biophys. Acta 218, 482–495.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Holash, J. A. , Harik, S. I. , Perry, G. , and Stewart, P. A. (1993). Barrier properties of testis microvessels. Proc. Natl Acad. Sci. USA 90, 11069–11073.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Huang, H. F. S. , and Nieschlag, E. (1986). Suppression of the intratesticular testosterone is associated with quantitative changes in spermatogonial populations in intact adult rats. Endocrinology 118, 619–627.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Huang, H. F. S. , Pogach, L. M. , Nathan, E. , Giglio, W. , and Seebode, J. J. (1991). Synergistic effects of follicle-stimulating hormone and testosterone on the maintenance of spermiogenesis in hypophysectomized rats: relationship with the androgen-binding protein status. Endocrinology 128, 3152–3161.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Jegou, B. , Dacheux, J. L. , Garnier, D. H. , Terqui, M. , Colas, G. , and Courot, M. (1979). Biochemical and physiological studies of androgen-binding protein in the reproductive tract of the ram. J. Reprod. Fertil. 57, 311–318.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Jin, W. , Arai, K. Y. , Herath, C. B. , Kondon, M. , Ishi, H. , Tanioka, Y. , Watanabe, G. , Groome, N. P. , and Taya, K. (2001a). Inhibins in the male Gottingen miniature pig: Leydig cells are the predominant source of inhibin B. J. Androl. 22, 953–960.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Jin, W. , Wada, S. , Arai, K. Y. , Kishi, H. , Herath, C. B. , Watanabe, G. , Suzuki, A. K. , Groome, N. P. , and Taya, K. (2001b). Testicular secretion of inhibin in the male golden hamster (Mesocricetus auratus). J. Androl. 22, 207–211.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Johnson, A. D. (1970). Testicular lipids. In
Kaneko, H. , Noguchi, J. , Kikuchi, K. , and Hasegawa, Y. (2003). Molecular weight forms of inhibin A and inhibin B in the bovine testis change with age. Biol. Reprod. 68, 1918–1925.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Kerr, J. B. , and de Kretser, D. M. (1975). Cyclic variations in Sertoli cell lipid content throughout the spermatogenic cycle in the rat. J. Reprod. Fertil. 43, 1–8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Khan, S. , Soder, O. , Syed, V. , Gustafsson, K. , Lindh, M. , and Ritzen, E. M. (1987). The rat testis produces large amounts of an interleukin-1-like factor. Int. J. Androl. 10, 495–503.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Klinefelter, G. R. , Hall, P. F. , and Ewing, L. L. (1987). Effect of luteinizing hormone deprivation in situ on steroidogenesis of rat Leydig cells purified by a multistep procedure. Biol. Reprod. 36, 769–783.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Klinefelter, G. R. , Kelce, W. R. , and Hardy, M. P. (1993). Isolation and culture of Leydig cells from adult rats. Meth. Toxicology 3A, 166–181.
![](../../media/share/OpenURL_Image.gif)
Kormano, M. (1967). Dye permeability and alkaline phosphatase activity of testicular capillaries in the postnatal rat. Histochemie 9, 327–338.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Lui, W.-Y. , Lee, W. M. , and Cheng, C. Y. (2003). TGF-βs: their role in testicular function and Sertoli cell tight junction dynamics. Int. J. Androl. 26, 147–160.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Maddocks, S. , and Setchell, B. P. (1989a). Testosterone concentrations in testicular interstitial fluid collected with a push-pull cannula or by drip-collection from adult rats given testosterone or aminoglutethamide. J. Endocrinol. 121, 303–309.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Maddocks, S. , and Setchell, B. P. (1989b). Effects of a single injection of human chorionic gonadotrophin on testosterone levels in testicular interstitial fluid and in testicular and peripheral venous blood plasma in adult rats. J. Endocrinol. 121, 311–316.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Maddocks, S. , and Sharpe, R. M. (1989). The route of secretion of inhibin from the rat testis. J. Endocrinol. 120, R5–R8.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Marchetti, C. , Hamdane, M. , Mitchell, V. , Mayo, K. , Devisme, L. , Rigot, J. M. , Beauvillain, J. C. , Hermand, E. , and Defossez, A. (2003). Immunolocalaization of inhibin and activin α and βB subunits and expression of corresponding messenger RNAs in the human adult testis. Biol. Reprod. 68, 230–235.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Mendel, C. M. (1992). The free hormone hypothesis. Distinction from the free hormone transport hypothesis. J. Androl. 13, 107–116.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Moore, A. , Krummen, L. A. , and Mather, J. P. (1994). Inhibins, activins, their binding proteins and receptors: interactions underlying paracrine activity in the testis. Mol. Cell. Endocrinol. 100, 81–86.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Mori, H. , and Christensen, A. K. (1980). Morphometric analysis of Leydig cells in the normal rat testis. J. Cell Biol. 84, 340–354.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Nagata, S.-I. , Tsunoda, N. , Nagamine, N. , Tanaka, Y. , Taniyama, H. , Nambo, Y. , Watanabe, G. , and Taya, K. (1998). Testicular inhibin in the stallion: cellular source and seasonal changes in its secretion. Biol. Reprod. 59, 62–68.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Niemi, M. , and Setchell, B. P. (1986). Gamma glutamyl transpeptidase in the vasculature of the rat testis. Biol. Reprod. 35, 385–391.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Nieschlag, E., Behre, H. M. and Weinbauer, G. F. (1992). Hormonal male contraception: a real chance? In
O’Donnell, L. , Stanton, P. G. , Wreford, N. G. , Robertson, D. M. , and McLachlan, R. I. (1996). Inhibition of 5α-reductase activity impairs the testosterone-dependent restoration of spermiogenesis in adult rats. Endocrinology 137, 2703–2710.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
O’Donnell, L. , Pratis, K. , Stanton, P. G. , Robertson, D. M. , and McLachlan, R. I. (1999). Testosterone-dependent restoration of spermatogenesis in adult rats is impaired by a 5α-reductase inhibitor. J. Androl. 20, 109–117.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Parvinen, M. , and Huhtaniemi, I. (1990). Testosterone micromilieu in stage rat seminiferous tubules. J. Steroid Biochem. 36, 377–381.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Pierroz, D. P. , Aebi, A. C. , Huhtaniemi, I. , and Aubert, M. L. (1999). Many LH peaks are needed to physiologically stimulated testosterone secretion: modulation by fasting and NPY. Am. J. Physiol. 276, E603–E610.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Risbridger, G. P. , and Cancilla, B. (2000). Role of activins in the male reproductive tract. Rev. Reprod. 5, 99–104.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Ritzen, E. M. , Boitani, C. , Parvinen, M. , French, F. C. , and Feldman, M. (1982). Stage-dependent secretion of ABP by rat seminiferous tubules. Mol. Cell. Endocrinol. 25, 25–33.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Robertson, D. M., McLachlan, R. I., Burger, H. G. and de Kretser, D. M. (1989). Inhibin and inhibin-related proteins in the male. In
Rommerts, F. F. G. , van Doorn, L. G. , Galjaard, H. , Cooke, B. A. , and van der Molen, H. J. (1973). Dissection of wet tissue and of freeze-dried sections in the investigation of seminiferous tubules and interstitial tissue from rat testis. J. Histochem. Cytochem. 21, 572–579.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Rosner, W. , Hryb, D. J. , Khan, M. S. , Nakhla, A. M. , and Romas, N. A. (1992). Sex hormone-binding globulin. Binding to cell membranes and generation of a second messenger. J. Androl. 13, 101–106.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Rosolowsky, L. J. , and Campbell, W. B. (1994). Endothelial cells stimulate aldosterone release from bovine adrenal zona glomerulosa cells. Am. J. Physiol. 266, E107–E117.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Rosolowsky, L. J. , Hanke, C. J. , and Campbell, W. B. (1999). Adrenal capillary endothelial cells stimulate aldosterone release through a protein that is distinct from endothelin. Endocrinology 140, 4411.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Russell, L. D. (1993). Form, dimensions and cytology of mammalian Sertoli cells. In
Russell, L. D. (1996). Mammalian Leydig cell structure. In
Sakiyama, R. , Pardridge, W. M. , and Musto, N. A. (1988). Influx of testosterone-binding globulin (TeBG) and TeBG-bound sex steroid hormones into rat testis and prostate. J. Clin. Endocrinol. Metab. 67, 98–103.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P. (1974). Secretions of the testis and epididymis. J. Reprod. Fertil. 37, 165–177.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P. (1980). The functional significance of the blood–testis barrier. J. Androl. 1, 3–10.
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P. (1994). Possible physiological bases for contraceptive techniques in the male. Hum. Reprod. 9, 1081–1087.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P. , and Cox, J. E. (1982). Secretion of free and conjugated steroids by the horse testis into lymph and venous blood. J. Reprod. Fertil. , 123–127.Suppl.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P. , and Galil, K. A. A. (1983). Limitations imposed by testicular blood flow on the function of the Leydig cells in vivo. Aust. J. Biol. Sci. 36, 285–293.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P. and Waites, G. M. H. (1975). The blood–testis barrier. In
Setchell, B. P. , and Wallace, A. L. C. (1972). The penetration of iodine-labelled FSH and albumin into the seminiferous tubules of sheep and rats. J. Endocrinol. 54, 67–77.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P. and Zupp, J. L. (1987). The passage of testosterone and DHA sulphate into blood and lymph after intratesticular injection in rats. In
Setchell, B.P. , Hinton, B.T. , Jacks, F. , and Davies, R. V. (1976). The restricted penetrations of iodinated rat FSH and LH into the seminiferous tubules of the rats testis. Mol. Cell. Endocrinol 6, 59–69.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P., Davies, R. V. and Main, S. J. (1977).
Setchell, B. P. , Laurie, M. S. , Main, S. J. , and Goats, G. C. (1978). The mechanism of transport of testosterone though the walls of the seminiferous tubules of the rat testis. Int. J. Androl. , 506–512.Suppl.
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P. , Laurie, M. S. , Flint, A. P. F. , and Heap, R. B. (1983). Transport of free and conjugated steroids from the boar testis in lymph, venous blood and rete testis fluid. J. Endocrinol. 96, 127–136.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P. , Pollanen, P. P. , and Zupp, J. L. (1988). The development of the blood–testis barrier and changes in vasular permeability at puberty in rats. Int. J. Androl. 11, 225–233.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P., Maddocks, S. and Brooks, D. E. (1994). Anatomy, vasculature, innervation and fluids of the male reproductive tract. In
Setchell, B. P. , Ploen, L. , and Ritzen, E. M. (2001). Reduction of long-term effects of local heating of the testis by treatment of rats with a GnRH agonist and an anti-androgen. Reproduction 122, 255–263.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Setchell, B. P. , Pakarinen, P. , and Huhtaniemi, I. (2002). How much LH do the Leydig cells see? J. Endocrinol. 175, 375–382.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Sharpe, R. M. (1981). The importance of testicular interstitial fluid in the transport of injected hCG to the Leydig cells. Int. J. Androl. 4, 64–74.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Sharpe, R. M. , Turner, K. J. , McKinnell, C. , Groome, N. P. , Atanassova, N. , Millar, M. R. , Buchanan, D. L. , and Cooke, P. S. (1999). Inhibin B levels in plasma of the male rat from birth to adulthood: effect of experimental manipulation of Sertoli cell number. J. Androl. 20, 94–101.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Stewart, P. A. (2000). Endothelial vesicles in the blood-brain barrier: are they related to permeability? Cell. Mol. Neurobiol. 20, 149–163.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Sullivan, M. H. F. , and Cooke, B. A. (1984). The role of calcium in luteinizing hormone-releasing hormone agonist (ICI 118630)-stimulated steroidogenesis in rat Leydig cells. Biochem. J. 218, 621–624.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Tao, L. , Zupp, J. L. , and Setchell, B. P. (2000). Effect of efferent duct ligation on the function of the blood–testis barrier in rats. J. Reprod. Fertil. 120, 13–18.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
![](../../media/share/OpenURL_Image.gif)
Tapanainen, J. , Kuopio, T. , Pelliniemi, L. J. , and Huhtaniemi, I. (1984). Rat testicular endogenous steroids and number of Leydig cells between the fetal period and sexual maturity. Biol. Reprod. 31, 1027–1035.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Tuck, R. R. , Setchell, B. P. , Waites, G. M. H. , and Young, J. A. (1970). The composition of fluid collected by micropuncture and catheterization from the seminiferous tubules and rete testis of rats. Pflugers Arch. 318, 225–243.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Turner, T. T. (1988). Transepithelial movement of 3H-androgen in seminiferous and epididymal tubules: a study using in vivo micropuncture and in vivo microperfusion. Biol. Reprod. 39, 399–408.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Turner, T. T. , and Rhoades, C. P. (1995). Testicular capillary permeability: the movement of luteinizing hormone from the vascular to the interstitial compartment. J. Androl. 16, 417–423.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Turner, T. T. , Cochran, R. C. , and Howards, S. S. (1981). Transfer of steroids across the hamster blood testis and blood epididymal barriers. Biol. Reprod. 25, 342–348.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Turner, T. T. , Jones, C. E. , Howards, S. S. , Ewing, L. L. , Zegeye, B. , and Gunsalus, G. L. (1984). On the androgen microenvironment of maturing spermatozoa. Endocrinology 115, 1925–1932.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Turner, T. T. , Ewing, L. L. , Jones, C. E. , Howards, S. S. , and Zegeye, B. (1985a). Androgens in male reproductive tract fluids: hypophysectomy and steroid replacement. Am. J. Physiol. 248, E274–E280.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Turner, T. T. , Ewing, L. L. , Jones, C. E. , Howards, S. S. , and Zegeye, B. (1985b). Androgens in various fluid compartments of the rat testis and epididymis after hypophysectomy and gonadotropin supplementation. J. Androl. 6, 353–358.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Voglmayr, J. K. , Roberson, C. , and Musto, N. A. (1980). Comparison of androgen levels in ram rete testis fluid, testicular lymph and spermatic venous blood plasma: evidence for a regulatory mechanism in the seminiferous tubules. Biol. Reprod. 23, 29–39.
| PubMed |
![](../../media/share/OpenURL_Image.gif)
Voglmayr, J. K. , Jolley, D. , Vale, W. , Willoughby, D. , Moser, A. , So, C.-K. , Chen, C.-L. , and Bardin, C. W. (1992). Effects of follicle-stimulating hormone on inhibin release by different testicular compartments in the adult ram. Biol. Reprod. 47, 573–581.
| PubMed |
![](../../media/share/OpenURL_Image.gif)