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http://dx.doi.org/10.5713/ajas.2010.10056

The Roles of Estrogens in the Efferent Ductules of the Male Reproductive System : A Review  

Min, Tae-Sun (National Research Foundation of Korea (NRF))
Lee, Ki-Ho (National Research Foundation of Korea (NRF))
Publication Information
Asian-Australasian Journal of Animal Sciences / v.23, no.8, 2010 , pp. 1118-1126 More about this Journal
Abstract
Male reproduction is influenced by a number of intrinsic and extrinsic factors, including environmental endocrine disruptors. Testosterone is a well recognized intrinsic regulator for development and function of the male reproductive tract, and thus male fertility. The testis and semen of many mammalians contain an unusually high concentration of estrogen. Testosterone is converted into estrogen by the enzymatic action of cytochrome P450 aromatase complex (Cyp19a1). Of the male reproductive tract, the efferent ductules (EDs) possess exceptionally elevated levels of estrogen receptors (ERs), ER${\alpha}$ and ER${\beta}$, indicating that estrogen, in addition to testosterone, would have a functional role in regulation of male reproduction. First, this review has focused on description and summary of what is currently known for functions of estrogen in the EDs. The biosynthetic pathway of estrogen occurring in the testis is briefly covered, following by detailed explanation of the morphology and physiology of EDs. In the next section, the sources and targets of estrogen in the male reproductive tract are highlighted, and possible functional roles of estrogen in the EDs are justified from the aspect of physiology, molecular biology, and morphology in adult animal models. Also, this section covers the importance of estrogen and ERs in maintaining normal function and morphology of the EDs during postnatal development. In the last part of this review, the effects of extrinsic factors, especially environmental endocrine-disruptors, on the EDs is summarized. The intent of this review is to emphasize the importance of estrogen for regulation of physiological function of the EDs, and thus male fertility.
Keywords
Estrogens; Efferent Ductules; Estrogen Receptors; Male Fertility; Environmental Endocrine Disruptor;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
Times Cited By Web Of Science : 1  (Related Records In Web of Science)
Times Cited By SCOPUS : 1
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1 Nilsson, S., S. Makela, E. Treuter, M. Tujague, J. Thomsen, G. Andersson, E. Enmark, K. Pettersson, M. Warner and J. A. Gustafsson. 2001. Mechanisms of estrogen action. Physiol. Rev. 81:1535-1565.
2 Nitta, H., D. Bunick, R. A. Hess, L. Janulis, S. C. Newton, C. F. Millette, Y. Osawa, Y. Shizuta, K. Toda and J. M. Bahr. 1993. Germ cells of the mouse testis express P450 aromatase. Endocrinology 132:1396-1401.   DOI   ScienceOn
3 Oliveira, A. G., L. F. Telles, R. A. Hess, G. A. B. Mahecha and C. A. Oliveira. 2007. Effects of the herbicide roundup on the epididymal region of drakes Anas platyrhynchos. Reprod. Toxicol. 23:182-191.   DOI   ScienceOn
4 Pudney, J. and D. W. Fawcett. 1984. Seasonal changes in fine structure of the ductuli efferentes of the ground squirrel, Citellus lateralis (Say). Anat. Rec. 208:383-399.   DOI   ScienceOn
5 Rago, V., B. Bilinska, A. Palma, S. Ando and A. Carpino. 2003. Evidence of aromatase localization in cytoplasmic droplet of human immature ejaculated spermatozoa. Folia Histochem. Cytobiol. 41:23-27.
6 Robaire, B. and L. Hermo. 1988. Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. In: The Physiology of Reproduction (Ed. E. Knobil and J. Neill). Raven Press, New York. pp. 999-1080.
7 Rommerts, F. F., F. H. de Jong, A. O. Brinkmann and H. J. van der Molen. 1982. Development and cellular localization of rat testicular aromatase activity. J. Reprod. Fertil. 65:281-288.   DOI   ScienceOn
8 Ruz, R., M. Gregory, C. E. Smith, D. G. Cyr, D. B. Lubahn, R. A. Hess and L. Hermo. 2006. Expression of aquaporins in the efferent ductules, sperm counts, and sperm motility in estrogen receptor-alpha deficient mice fed lab chow versus casein. Mol. Reprod. Dev. 73:226-237.   DOI   ScienceOn
9 Levine, N. and D. J. Marsh. 1971. Micropuncture studies of the electrolyte aspects of fluid and electrolyte transport in individual seminiferous tubules in the epididymis and the vas deferens in rats. J. Physiol. 213:557-579.   DOI
10 Linder, E. 1971. Fate of a kidney-specific mesonephric antigen during the differentiation of the epididymis. Ann. N.Y. Acad. Sci. 177:204-213.   DOI
11 Lubahn, D. B., J. S. Moyer, T. S. Golding, J. F. Couse, K. S. Korach and O. Smithies. 1993. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Nat. Acad. Sci. USA. 90:162-166.
12 MacMillan, E. W. and R. G. Harrison. 1955. The rate of passage of radioplaque medium along the ductus epididymidis of the rat. Stud. Fert. 9:35-40.
13 Marshall, F. F., W. G. Reiner and B. S. Goldberg. 1979. The embryologic origin of the caput epididymis in the rat. Invest. Urol. 17:78-82.
14 Mason, K. E. and S. Shaver. 1952. Some functions of the caput epididymidis. Ann. NY Acad. Sci. 55:585-593.   DOI   ScienceOn
15 McKinnell, C., N. Atanasoova, K. Williams, J. S. Fisher, M. Walker, K. J. Turner, T. K. Saunders and R. M. Sharpe. 2001. Suppression of androgen action and the induction of gross abnormalities of the reproductive tract in male rats treated neonatally with diethylstilbestrol. J. Androl. 22:323-338.
16 Morales, C. and L. Hermo. 1983. Demonstration of fluid-phase endocytosis in epithelial cells of the male reproductive system by means of horseradish peroxidase-colloidal gold complex. Cell Tissue Res. 230:503-510.   DOI
17 Nakai, M., R. A. Hess, B. J. Moore, R. Guttroff, L. F. Strader and R. E. Linder. 1992. Acute and long-term effects of a single dose of the fungicide carbendazim (methyl 2-benzimidazolecarbamate) on the male reproductive system in the rat. J. Androl. 13:507-518.
18 Lee, K.-H., R. A. Hess, J. M. Bahr, D. B. Lubahn, J. Taylor and D. Bunick. 2000. Estrogen receptor ${\alpha}$ has a functional role in the mouse rete testis and efferent ductules. Biol. Reprod. 63:1873-1880.   DOI   ScienceOn
19 Kim, J.-Y., H.-J. Seo, O.-S. Kim, B.-J. Kim, S.-K. Lee, H.-W. Baik and K.-H. Lee. 2008. Analysis of differential expression of cytochrome P450 aromatase (Cyp19) in the efferent ductules and the epididymis of male rats during postnatal development. J. Anim. Sci. Technol. (Kor.) 50:783-792.   과학기술학회마을   DOI   ScienceOn
20 Krege, J. H., J. B. Hodgin, J. F. Course, E. Enmark, M. Warner, J. E. Mahler, M. Sar, K. S. Korach, J. A. Gustafsson and O. Smithies. 1998. Generation and reproductive phenotypes of mice lacking estrogen receptor ${\beta}$. Proc. Nat. Acad. Sci. USA. 95:15677-15682.   DOI
21 Lee, K.-H., C. Finnigan-Bunick, J. Bahr and D. Bunick. 2001. Estrogen regulation of ion transporter messenger RNA levels in mouse efferent ductules are mediated differentially through estrogen receptor (ER) ${\alpha}\;and\;ER{\beta}$. Biol. Reprod. 65:1534-1541.   DOI   ScienceOn
22 Lee, K.-H., D. Bunick, G. Lamprecht, I. Choi and J. M. Bahr. 2008. Differential expression of genes important to efferent ductules ion homeostasis across postnatal development in estrogen $receptor-{\alpha}$ knockout and wild-type mice. Asian-Aust. J. Anim. Sci. 21:510-522.   DOI
23 Lee, K.-H., J. H. Park, D. Bunick, D. B. Lubahn and J. M. Bahr. 2009. Morphological comparison of the testis and efferent ductules between wild-type and estrogen receptor alpha knockout mice during postnatal development. J. Anat. 214:916-925.   DOI   ScienceOn
24 Levallet, J., B. Bilinska, H. Mittre, C. Genissel, J. Fresnel and S. Carreau. 1998. Expression and immunolocalization of functional cytochrom P450 aromatase in mature rat testicular cells. Biol. Reprod. 58:919-926.   DOI   ScienceOn
25 Hinton, B. T. and T. T. Turner. 1988. Is the epididymis a kidney analogue? News Physiol. Sci. 3:28-31.
26 Hess, R. A., D. Bunick, K.-H. Lee, J. Bahr, J. A. Taylor, K. S. Korach and D. B. Lubahn. 1997a. A role for oestrogens in the male reproductive system. Nature 390:509-512.   DOI   ScienceOn
27 Hess, R. A., D. H. Gist, D. Bunick, D. B. Lubahn, A. Farrell, J. Bahr, P. S. Cooke and G. L. Greene. 1997b. Estrogen receptor $({\alpha}\;&\;{\beta})$ expression in the excurrent ducts of the adult male rat reproductive tract. J. Androl. 18:602-611.
28 Hess, R. A., B. J. Moore, J. Forrer, R. E. Linder and A. A. Abuel-Atta. 1991. The fungicide benomyl (methyl 1-(butylcarbamoyl)-2-benzimidazolecarbamate) causes testicular dysfunction by inducing the sloughing of germ cells and occlusion of efferent ductules. Fundam. Appl. Toxicol. 17:733-745.   DOI   ScienceOn
29 Hoffer, A. P., D. W. Hamilton and D. W. Fawcett. 1973. The ultrastructural pathology of the rat epididymis after administration of a-chlorhydrin (U-5897). Anat. Rec. 175:203-220.   DOI   ScienceOn
30 Hoffer, A. P. and D. W. Hamilton. 1974. Phagocytosis of sperm by the epithelial cells in ductuli efferentes of experimental rats. Anat. Rec. 178:376-377.
31 Iguchi, T., Y. Uesugi, T. Sato, Y. Ohta and N. Takasugi. 1991. Developmental pattern of estrogen receptor expression in male mouse genital organs. Mol. Androl. 3:109-119.
32 Ilio, K. Y. and R. A. Hess. 1994. Structure and function of the ductuli efferentes: a review. Microsc. Res. Tech. 29:432-467.   DOI   ScienceOn
33 Jones, R. C. and K. M. Jurd. 1987. Structural differentiation and fluid reabsorption in the ductuli efferentes testis of the rat. Aust. J. Biol. Sci. 40:79-90.
34 Goyal, H. O., A. Eljack and S. Mobini. 1988. Regional differences in the morphology of ductuli efferentes of the goat. J. Vet. MEd. C. 17:369. Abstract.
35 Kahnia, B., L. C. Maria, G.-M. Anne, Y. Jacques, L. Marc and M. Geri. 2007. Human fetal testis: source of estrogen and target of estrogen action. Hum. Reprod. 22:1885-1892.   DOI   ScienceOn
36 Fisher, J. S., M. R. Millar, G. Majdic, P. T. Saunders, H. M. Fraser and R. M. Sharpe. 1997. Immunolocalisation of oestrogen receptor-alpha within the testis and excurrent ducts of the rat and marmoset monkey from perinatal life to adulthood. J. Endocrinol. 153:485-495.   DOI   ScienceOn
37 Flickinger, J. A., S. S. Howards and H. F. English. 1978. Ultrastructural differences in the efferent ducts and several regions of the epididymis of the hamster. Am. J. Anat. 152:557-586.   DOI   ScienceOn
38 Hamilton, D. W. 1975. Structure and function of the epithelium lining the ductuli efferentes, ductus epididymis, and ductus deferens in the rat. In: Handbook of Physiology (Ed. D. W. Hamilton and R. O. Greep). American Physiology Society, Washington DC, pp. 259-300.
39 Hansen, L. A., J. Clulow and R. C. Jones. 1997. Perturbation of fluid resorption in the efferent ducts of the rat by testosterone propionate, $17{\beta}-oestradiol$ 3-benzoate, flutamide and tamoxifen. Int. J. Androl. 20:265-273.   DOI   ScienceOn
40 Hermo, L. and C. Morales. 1984. Endocytosis in nonciliated epithelial cells of the ductuli efferentes in the rat. Am. J. Anat. 171:59-74.   DOI   ScienceOn
41 Hess, R. A. 2000. Oestrogen in fluid transport in efferent ducts of the male reproductive tract. Rev. Reprod. 5:84-92.   DOI
42 Hess, R. A. 2003. Estrogen in the adult male reproductive tract: a review. Reprod. Biol. Endocrinol. 1:52.   DOI   ScienceOn
43 Carreau, S., C. Genissel, B. Bilinska and J. Levallet. 1999. Sources of oestrogen in the testis and reproductive tract of the male. Int. J. Androl. 22:211-223.   DOI
44 Hess, R. A., D. Bunick and J. M. Bahr. 1995. Sperm, a source of estrogen. Environ. Health. Perspec. 103:59-62.   DOI
45 Hess, R. A., D. Bunick and J. M. Bahr. 2001. Oesterogen, its receptors and function in the male reproductive tract-a review. Mol. Cell. Endocrinol. 178:29-38.   DOI   ScienceOn
46 Carpino, A., F. Romeo and V. Rago. 2004. Aromatase immunolocalization in human ductuli efferentes and proximal ductus epididymis. J. Anat. 204:217-220.   DOI   ScienceOn
47 Chan, H. C., K. B. Lai, W. O. Fu, Y. W. Chung, P. S. Chan and P. Y. Wong. 1995. Regional differences in bioelectrical properties and anion secretion in cultured epithelia from rat and human male excurrent ducts. Biol. Reprod. 52:192-198.   DOI   ScienceOn
48 Clulow, J., R. C. Jones and L. A. Hansen. 1994. Micropuncture and cannulation studies of fluid composition and transport in the ductuli efferentes testis of the rat: comparisons with the homologous metanephric proximal tubule. Exp. Physiol. 81:633-644.
49 Cooke, P. S., P. Young, R. A. Hess and G. R. Cunha. 1991. Estrogen receptor expression in developing epididymis, efferent ductules and other male reproductive organs. Endocrinology 128:2874-2879.   DOI   ScienceOn
50 Couse, J. F., S. C. Hewitt, D. O. Bunch, M. Sar, V. R. Walker, B. J. Davis and K. S. Korach. 1999. Postnatal sex reversal of the ovaries in mice lacking estrogen receptors ${\alpha}\;and\;{\beta}$. Science 286:2328-2331.   DOI   ScienceOn
51 Danzo, B. J., B. C. Eller, L. A. Judy, J. R. Trautman and M. C. Orgebin-Crist. 1975. Estradiol binding in cytosol from epididymides of immature rabbits. Mol. Cell. Endocrinol. 2:91-105.   DOI   ScienceOn
52 Sharpe, R. M. 1998. The roles of oestrogen in the male. TEM. 9:371-377.
53 Eddy, E. M., T. F. Washburn, D. O. Bunch, E. H. Goulding, B. C. Gladen, D. B. Lubahn and K. S. Korach. 1996. Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 137:4796-4805.   DOI   ScienceOn
54 Eshere task force on ethics and law, G. Pennings, G. de Wert, F. Shenfield, J. Cohen, B. Tarlatzis and P. Devroey. 2009. Providing infertility treatment in resource-poor countries. Hum. Reprod. 24:1008-1011.   DOI   ScienceOn
55 Antal, M. C., A. Krust, P. Chambon and M. Mark. 2008. Sterility and absent of histopathological defects in nonreproductive organs of a mouse $ER{\beta}-null$ mutant. Proc. Nat. Acad. Sci. USA. 105:2433-2438.   DOI   ScienceOn
56 Bretweld, R., M. Brouwers, I. Ebisch and Y. Roeleveld. 2007. Influence of pesticides on male fertilit. Scand. J. Work Environ. Health 33:13-28.   DOI   ScienceOn
57 Weniger, J. P. 1993. Estrogen production by fetal rat gonads. J. Steroid Biochem. Mol. Biol. 44:459-462.   DOI   ScienceOn
58 Winet, H. 1980. On the mechanism for flow in the efferent ducts. J. Androl. 1:303-311.
59 Saunders, P. T., R. M. Sharpe, K. Williams, S. Macpherson, H. Urquart, D. S. Irvine and M. R. Millar. 2001. Differential expression of oestrogen receptor alpha and beta proteins in the testes and male reproductive system of human and non-human primates. Mol. Hum. Reprod. 7:227-236.   DOI   ScienceOn
60 Schlegel, P. N. 2009. Evaluation of male infertility. Minerva. Ginecol. 61:261-283.
61 Sierens, J. E., S. F. Sneddon, F. Collins, M. R. Millar and P. T. K. Saunders. 2005. Estrogens in testis biology. Ann. NY Acad. Sci. 1061:65-76.   DOI   ScienceOn
62 Sikka, S. C. and R. Wang. 2008. Endocrine disruptors and estrogenic effects on male reproductive axis. Asian J. Androl. 10:134-145.   DOI   ScienceOn
63 Spring, K. R. 1999. Epithelial fluid transport-a century of investigation. News Physiol. Sci. 14:92-100.
64 Suzuki, F. and T. Nagano. 1978. Regional differentiation of cell junctions in the excurrent duct epithelium of the rat testis as revealed by freeze-fracture. Anat. Rec. 191:503-520.   DOI   ScienceOn
65 Takeuchi, S. 1992. Differentiation and maturation of excurrent duct system of the rat testis. Jap. J. Urol. 83:1043-1051.   DOI
66 Tingari, M. D. 1973. Histochemical localization of $3{\beta}-\;and\;17{\beta}-hydroxysteroid$ dehydrogenases in the male reproductive tract of the domestic fowl (Gallus domesticus). Histochem. J. 5:57-65.   DOI
67 Toda, K., T. Okada, Y. Hayashi and T. Saibara. 2008. Preserved tissue structure of efferent ductules in aromatase-deficient mice. J. Endocrinol. 199:137-146.   DOI   ScienceOn
68 Tsai-Morris, C. H., D. R. Aquilano and M. L. Dufau. 1985. Cellular localization of rat testicular aromatase activity during development. Endocrinology 116:38-46.   DOI   ScienceOn
69 Nilsson, S. and J. A. Gustafsson. 2000. Estrogen receptor transcription and transactivation: basic aspects of estrogen action. Breast Cancer Res. 2:360-366.   DOI