Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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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))
  • Received : 2010.02.16
  • Accepted : 2010.03.16
  • Published : 2010.08.01
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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

References

  1. 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. https://doi.org/10.1073/pnas.0712029105
  2. Bretweld, R., M. Brouwers, I. Ebisch and Y. Roeleveld. 2007. Influence of pesticides on male fertilit. Scand. J. Work Environ. Health 33:13-28. https://doi.org/10.5271/sjweh.1060
  3. Carpino, A., F. Romeo and V. Rago. 2004. Aromatase immunolocalization in human ductuli efferentes and proximal ductus epididymis. J. Anat. 204:217-220. https://doi.org/10.1111/j.0021-8782.2004.00272.x
  4. 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. https://doi.org/10.1046/j.1365-2605.1999.00172.x
  5. 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. https://doi.org/10.1095/biolreprod52.1.192
  6. 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.
  7. 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. https://doi.org/10.1210/endo-128-6-2874
  8. 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. https://doi.org/10.1126/science.286.5448.2328
  9. 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. https://doi.org/10.1016/0303-7207(75)90051-9
  10. 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. https://doi.org/10.1210/en.137.11.4796
  11. 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. https://doi.org/10.1093/humrep/den503
  12. 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. https://doi.org/10.1677/joe.0.1530485
  13. 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. https://doi.org/10.1002/aja.1001520409
  14. 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.
  15. 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.
  16. 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. https://doi.org/10.1046/j.1365-2605.1997.00069.x
  17. Hermo, L. and C. Morales. 1984. Endocytosis in nonciliated epithelial cells of the ductuli efferentes in the rat. Am. J. Anat. 171:59-74. https://doi.org/10.1002/aja.1001710106
  18. Hess, R. A. 2000. Oestrogen in fluid transport in efferent ducts of the male reproductive tract. Rev. Reprod. 5:84-92. https://doi.org/10.1530/ror.0.0050084
  19. Hess, R. A. 2003. Estrogen in the adult male reproductive tract: a review. Reprod. Biol. Endocrinol. 1:52. https://doi.org/10.1186/1477-7827-1-52
  20. Hess, R. A., D. Bunick and J. M. Bahr. 1995. Sperm, a source of estrogen. Environ. Health. Perspec. 103:59-62. https://doi.org/10.1289/ehp.95103s459
  21. 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. https://doi.org/10.1016/S0303-7207(01)00412-9
  22. 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. https://doi.org/10.1038/37352
  23. 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.
  24. 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. https://doi.org/10.1016/0272-0590(91)90181-3
  25. Hinton, B. T. and T. T. Turner. 1988. Is the epididymis a kidney analogue? News Physiol. Sci. 3:28-31.
  26. 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. https://doi.org/10.1002/ar.1091750206
  27. 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.
  28. 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.
  29. Ilio, K. Y. and R. A. Hess. 1994. Structure and function of the ductuli efferentes: a review. Microsc. Res. Tech. 29:432-467. https://doi.org/10.1002/jemt.1070290604
  30. 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.
  31. 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. https://doi.org/10.1093/humrep/dem091
  32. 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. https://doi.org/10.5187/JAST.2008.50.6.783
  33. 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. https://doi.org/10.1073/pnas.95.26.15677
  34. 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. https://doi.org/10.1095/biolreprod63.6.1873
  35. 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. https://doi.org/10.1095/biolreprod65.5.1534
  36. 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. https://doi.org/10.5713/ajas.2008.70462
  37. 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. https://doi.org/10.1111/j.1469-7580.2009.01080.x
  38. 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. https://doi.org/10.1095/biolreprod58.4.919
  39. 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. https://doi.org/10.1113/jphysiol.1971.sp009400
  40. Linder, E. 1971. Fate of a kidney-specific mesonephric antigen during the differentiation of the epididymis. Ann. N.Y. Acad. Sci. 177:204-213. https://doi.org/10.1111/j.1749-6632.1971.tb35048.x
  41. 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.
  42. 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.
  43. 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.
  44. Mason, K. E. and S. Shaver. 1952. Some functions of the caput epididymidis. Ann. NY Acad. Sci. 55:585-593. https://doi.org/10.1111/j.1749-6632.1952.tb26578.x
  45. 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.
  46. 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. https://doi.org/10.1007/BF00216196
  47. 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.
  48. Nilsson, S. and J. A. Gustafsson. 2000. Estrogen receptor transcription and transactivation: basic aspects of estrogen action. Breast Cancer Res. 2:360-366. https://doi.org/10.1186/bcr81
  49. 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.
  50. 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. https://doi.org/10.1210/en.132.3.1396
  51. 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. https://doi.org/10.1016/j.reprotox.2006.11.004
  52. 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. https://doi.org/10.1002/ar.1092080309
  53. 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.
  54. 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.
  55. 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. https://doi.org/10.1530/jrf.0.0650281
  56. 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. https://doi.org/10.1002/mrd.20390
  57. 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. https://doi.org/10.1093/molehr/7.3.227
  58. Schlegel, P. N. 2009. Evaluation of male infertility. Minerva. Ginecol. 61:261-283.
  59. Sharpe, R. M. 1998. The roles of oestrogen in the male. TEM. 9:371-377.
  60. 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. https://doi.org/10.1196/annals.1336.008
  61. Sikka, S. C. and R. Wang. 2008. Endocrine disruptors and estrogenic effects on male reproductive axis. Asian J. Androl. 10:134-145. https://doi.org/10.1111/j.1745-7262.2008.00370.x
  62. Spring, K. R. 1999. Epithelial fluid transport-a century of investigation. News Physiol. Sci. 14:92-100.
  63. 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. https://doi.org/10.1002/ar.1091910409
  64. Takeuchi, S. 1992. Differentiation and maturation of excurrent duct system of the rat testis. Jap. J. Urol. 83:1043-1051. https://doi.org/10.5980/jpnjurol1989.83.1043
  65. 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. https://doi.org/10.1007/BF01012045
  66. 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. https://doi.org/10.1677/JOE-08-0257
  67. 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. https://doi.org/10.1210/endo-116-1-38
  68. Weniger, J. P. 1993. Estrogen production by fetal rat gonads. J. Steroid Biochem. Mol. Biol. 44:459-462. https://doi.org/10.1016/0960-0760(93)90250-Z
  69. Winet, H. 1980. On the mechanism for flow in the efferent ducts. J. Androl. 1:303-311.

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