Skip to main content
Download PDF
  • Spermatogenèse
  • Published:

Estrogènes et spermatozoïdes

Estrogens and spermatozoa

Andrologie volume 9, pages 252–260 (1999)Cite this article

Resume

Les estrogènes sont depuis longtemps considérés comme des hormones sexuelles typiquement femelles; cependant ils semblent jouer un rôle éminent dans le testicule tout aussi important que leur fonction endocrine classique. L’aromatase (enzyme qui transforme irréversiblement les androgènes en estrogénes) est impliquée notamment dans le développement, la différenciation sexuelle et le comportement, la reproduction, les métabolismes osseux et lipidique, le fonctionnement du cerveau; son importance est donc capitale chez I’homme. Les données mettant en évidence au sein du testicule plusieurs types cellulaires opérationnels dans la production d’estrogènes, associés à la présence de récepteurs spécifiques (ERα et ERβ) à plusieurs niveaux du tractus génital mais aussi sur certaines cellules sexuelles, plaident donc fortement en faveur d’un rôle intrinsèque de ces hormones femelles en dehors de leur impact connu sur la secrétion gonadotrope. Un certain nombre de preuves et d’arguments permettent de penser qu’une (ou des) relation (s) existe (nt) entre estrogènes et infertilité, en particulier au niveau épididymaire où la composition du fluide luminal de la tête de l’épididyme (zone essentielle pour la maturation du spermatozoïde) serait modulée par ces hormones femelles. Chez I’homme, les sites de production et le rôle des estrogènes dans la spermatogenèse et la spermiogenèse ne sont pas encore totalement élucidés; cependant, dans l’étude des mécanismes physiopathologiques impliqués dans l’infertilité la participation des estrogènes est de plus en plus envisagée. En conséquence, les estrogènes se révèlent donc être essentiels pour la reproduction du mâle ce qui nous amènent à reconsidérer certaines notions de la physiologie de la reproduction masculine, avec non seulement des régulations androgéno-dépendantes mais aussi estrogéno-contrôlées.

Abstract

Aromatase is the terminal enzyme responsible for estrogen biosynthesis; it is present in the endoplasmic reticulum membrane of steroidogenic cells in vertebrates. This enzyme functions with the ubiquitous reductase as the electron donor. The aromatase gene is unique and its expression is regulated in a tissue and more precisely in a cell-specific fashion via the alternative use of several promoters located in the first exons.

This enzymatic complex is generally involved in development, reproduction, sexual differentiation and behaviour, but also in bone and lipid metabolism, brain functions and diseases such as breast and testicular tumors. The aromatase gene expression and its transduction in a fully active protein in testicular somatic cells and germ cells together with the widespread distribution of estrogen receptors (ERα & β) in the testis and the genital tract of the male, are clearly in favor of a physiological role for estrogens in the spermatogenesis processings especialy in sperm maturation. Therefore, we begin to understand the physiopathological roles of the estrogens in males indeed, the aromatase deficiency is associated, with severe bone maturation problems and sterility in man. Conversely, it is also obvious that estrogens in excess are responsible of the impaired spermatogenesis. These female hormones (or the ratio androgens/estrogens) do play a physiological role in the development and maintenance of male gonadal functions and obviously, several steps are concerned especially the sperm production and maturation.

References

  1. ARAI Y., MORI T., SUZUKI Y., BERN H.A. Longterm effects of perinatal exposure to sex steroids and diethylstilbestrol on the reproductive system of male mammals. Int. Rev. Cytol., 1983; 84: 235–268.

    Article  PubMed  CAS  Google Scholar 

  2. AUGER J., KUNSTMANN J.M., CZYGLIK F., JOUANNET P. Decline in semen quality among fertile men in Paris during the past 20 years. N. Engl. J. med., 1995; 332: 281–285.

    Article  PubMed  CAS  Google Scholar 

  3. BECK K.J., HERSCHEL S., HUNGERSHOFER R., SCHWINGER E. The effect of steroid hormones on motility and selective migration of X-and Y-bearing human spermatozoa. Fertil. Steril., 1976; 27: 407–412.

    PubMed  CAS  Google Scholar 

  4. BELMONTE S., MATURANO M., BERTINI F., PUSIOL E., SARTOR T., SOSA A. Changes in the content of rat epididymal fluid induced by prolonged treatment by tamoxifen. Andrologia, 1998; 30: 345–350.

    PubMed  CAS  Google Scholar 

  5. BERGH J.P. Oestrogens-essential for reproduction in males, too. Eur. J. Endocrinol., 1998, 138: 497–498.

    Article  Google Scholar 

  6. BULUN S.E. Aromatase deficiency in women and men: would you have predicted the phenotypes? J. Clin. Endocrinol. Metab., 1996; 81: 867–71.

    Article  PubMed  CAS  Google Scholar 

  7. BULUN S.E., NOBLE L.S., TAKAYAMA K. et al. Endocrine disorders associated with inappropriated high aromatase expression. J. Steroid. Biochem. Molec. Biol., 1997; 61: 133–139.

    Article  PubMed  CAS  Google Scholar 

  8. CARANI C., QIN K., SIMONI M., et al. Effect of testosterone and estradiol in a man with aromatase deficiency. N. Engl. J. Med., 1997; 337: 91–95.

    Article  PubMed  CAS  Google Scholar 

  9. CARREAU S. Germ cells-Sertoli cells interactions and Leydig cell function. In: Dufau M. L., Fabbri A., Isidori A., eds. Cell and Molecular Biology of the testis. Frontiers in Endocrinology 1994; 5: 137–48.

  10. CARREAU S. Paracrine control of human Leydig cell and Sertoli cell functions. Folia Histochem. Cytobiol. 1996; 34: 111–9.

    PubMed  CAS  Google Scholar 

  11. CARREAU S., LEVALLET J. L’aromatase testiculaire: du gène à la protéine. Andrologie, 1998; 8: 191–198.

    Article  Google Scholar 

  12. CARREAU S., BILINSKA B., LEVALLET J. Les cellules germinales mâles: une source nouvelle d’estrogènes dans le testicule des mammifères. Ann. Endocrinol., 1998b; 59: 79–92.

    CAS  Google Scholar 

  13. CARREAU S., GENISSEL C., BILINSKA B., LEVALLET J. The oestrogen sources in the testis and the reproductive tract of the male. Int. J. Androl., sous presse, 1999.

  14. CHAN S.Y.W., WANG C.C.L., TANG L.C.H. Effect of clomiphene citrate on human spermatozoa motility and fertilizing capacity in vitro. Fertil. Steril., 1985; 43: 773–776.

    PubMed  CAS  Google Scholar 

  15. CHENG C.Y., BOETTCHER B. The effect of steroids on the in vitro migration of washed human spermatozoa in modified tyrode’s solution or in fasting human blood serum. Fertil. Steril., 1979; 32: 566–570.

    PubMed  CAS  Google Scholar 

  16. CHEW P.C.T., LOGANATH A., PEH K.L., CHOW W.P., GUNASEGARAM R., RATNAM S.S. Concentrations of intracellular sex steroids in human spermatozoa. Arch. Androl., 1993; 30: 165–170.

    Article  PubMed  CAS  Google Scholar 

  17. COOKE P.S., YOUNG P., HESS R.A., CUNHA G.R. Estrogen receptor expression in developing epididymis, efferent ductules, and other male reproductive organs. Endocrinology, 1991; 128: 2874–2879.

    PubMed  CAS  Google Scholar 

  18. DANZO B.J. Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environ. Health Perspect., 1997; 105: 294–301.

    Article  PubMed  CAS  Google Scholar 

  19. DURKEE T.J., MUELLER M., ZINAMAN M. Identification of estrogen receptor protein and messenger ribonucleic acid in human spermatozoa. Am. J. Obstet. Gynecol., 1998; 178: 1288–1297.

    Article  PubMed  CAS  Google Scholar 

  20. EDDY E.M. WASHBURN T.F., BUNCH D.O. et al. Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 1996; 137: 4796–805.

    Article  PubMed  CAS  Google Scholar 

  21. ENMARK E., PELTO-HUIKKO M., GRANDIEN K. et al. Human estrogen receptor-β gene structure, chromosomal localization, and expression pattern. J. Clin. Endocrinol. Metab., 1997; 82: 4258–4265.

    Article  PubMed  CAS  Google Scholar 

  22. ERGUN S., UNGERFROREN H., HOLSTEIN A.F., DAVIDOFF M.S. Estrogen and progesterone receptors and estrogen receptor-related antigen (ER-D5) in human epididymis. Molec. Reprod. Dev., 1997; 47: 448–455.

    Article  PubMed  CAS  Google Scholar 

  23. FISHER C.R., GRAVES K.H., PARLOW A.F., SIMPSON E.R. Characterization of mice deficient in aromatase (ArKo) because of targeted disruption of thecyp 19 gene. Proc. Natl. Acad. Sci. (USA) 1998; 95: 6965–6970.

    Article  CAS  Google Scholar 

  24. FISHER J.S., MILLAR M.R., MADJIC G., SAUNDERS P.T.K., FRASER H.M., SHARPE R.M. Immunolocalisation of oestrogen receptor-α within the testis and excurrent ducts of the rat and marmoset monkey from perinatal life to adulthood. J. Endocrinol., 1997; 153: 485–495.

    Article  PubMed  CAS  Google Scholar 

  25. FISHER J.S., TURNER K.J., FRASER H.M., SAUNDERS P.T.K., BROWN D., SHARPE R.M. Immunoexpression of aquaporin-1 in the efferent ducts of the rat and marmoset monkey during development, its modulation by estrogens, and its possible role in fluid resorption. Endocrinology, 1998; 139: 3935–3945.

    Article  PubMed  CAS  Google Scholar 

  26. FOUCAULT P., DROSDOWSKY M.A., CARREAU S. Germ cell and Sertoli cell interactions in human testis: evidence for stimulatory and inhibitory effects. Human Reprod., 1994; 9: 2062–2068.

    CAS  Google Scholar 

  27. FREE M.J., JAFFE R.A. Collection of rete testis fluid from rats without previous efferent duct ligation. Biol. Reprod., 1979; 20: 269–278.

    Article  PubMed  CAS  Google Scholar 

  28. GILL-SHARMA M.K., GOPALKRISHNAN K., BALASINOR N., PARTE P., JAYARAMAN S., JUNEJA H.S. Effects of tamoxifen on the fertility of male rats. J. Reprod. Fertil., 1993; 99: 395–402.

    PubMed  CAS  Google Scholar 

  29. GOLDZEIHER J.W., ROBERTS I.S. Identification of estrogen in the human testis. J. Clin. Endocrinol. Metab., 1952; 12: 143–150.

    Google Scholar 

  30. GUNASEGARAM R., CHEW P.C.T., LOGANATH A., PEH K.L., RATNAM S.S. A Δ4-3-keto pathway for testosterone synthesis in the human spermatozoa. Arch. Androl., 1998a; 40: 49–57.

    Article  PubMed  CAS  Google Scholar 

  31. GUNASEGARAM R., PEH K.L., LOGANATH A., CHEW P.C.T., RATNAM S.S., ARULKUMARAN S. Cytochrome P-450 cholesterol side chain cleavage expression in human spermatozoa. Horm. Metab. Res., 1998; 30: 58–60.

    Article  PubMed  CAS  Google Scholar 

  32. HARRIS C.A., HENTTU P., PARKER M.G., SUMPTER J.P. The estrogenic activity of phthalate esters in vitro. Environ. Health Perspect., 1997; 105: 801–811.

    Article  Google Scholar 

  33. HENDRY W.F., PARSLOW J.M., STEDRONSKA J. Exploratory scrotomy in 168 azoospermic males. Br. J. Urol., 1983; 55: 785–791.

    Article  PubMed  CAS  Google Scholar 

  34. HESS R.A., BUNICK D., BAHR J.M. Sperm, a source of estrogen. Environ. Health Perspect., 1995; 103: 59–62.

    Article  PubMed  Google Scholar 

  35. HESS R.A., GIST D.H., BUNICK D. et al. Estrogen receptor (α & β) expression in the excurrent ducts of the adult male rat reproductive tract. J. Androl., 1997; 18: 602–611.

    PubMed  CAS  Google Scholar 

  36. HESS R.A., BUNICK D., LEE K.H. et al. A role for estrogens in the male reproductive sytem. Nature, 1997; 390: 509–512.

    Article  PubMed  CAS  Google Scholar 

  37. IDAOMAR M., GUERIN J.F., LORNAGE J., CZYBA J.C. Stimulation of motility and energy metabolism of spermatozoa from asthenospermic patients by 17β-estradiol. Arch. Androl., 1989; 22: 197–202.

    Article  PubMed  CAS  Google Scholar 

  38. INKSTER S., YUE W., BRODIE A. Human testicular aromatase: immunocytochemical and biochemical studies. J. Clin. Endocrinol. Metab., 1995; 80: 1941–1947.

    Article  PubMed  CAS  Google Scholar 

  39. JANULIS L., HESS R.A., BUNICK D. et al. Mouse epididymal sperm contains active P450 aromatase which decreases as sperm traverse the epididymis. J. Androl., 1996; 17: 111–116.

    PubMed  CAS  Google Scholar 

  40. JANULIS L., BAHR J.M., HESS R.A., JANSEN S., OSAWA Y., BUNICK D. Rat testicular germ cells and epididymal sperm contain active P450 aromatase. J. Androl., 1998; 19: 65–71.

    PubMed  CAS  Google Scholar 

  41. JAYLE M.F., SCHOLLER R., SFIKAKIS A., HERON M. Excrétion des phénolstéroïdes et des 17-cétostéroïdes après administration de gonadotropines à des hommes. Clin. Chim. Acta, 1962; 7: 212–20.

    Article  PubMed  CAS  Google Scholar 

  42. JENKINS A.D., LECHENE C.P., HOWARDS S.S. The effect of estrogen administration in vivo on the elemental composition of the intraluminal fluids of the seminiferous tubules, rete testis and epididymis of tha rat. J. Androl., 1983; 4: 272–275.

    PubMed  CAS  Google Scholar 

  43. KUIPER G.G.J.M., CARLSSON B., GRANDIEN K. et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinology, 1997; 138: 863–870.

    Article  PubMed  CAS  Google Scholar 

  44. KUIPER G.G.J.M., GUSTAFSSON J.A. The novel estrogen receptor β subtype: potential role in the cell-and promoter-specific actions of estrogens and anti-estrogens. FEBS Lett., 1997; 410: 87–90.

    Article  PubMed  CAS  Google Scholar 

  45. KUIPER G.G.J.M., LEMMEN J.G., CARLSSON B. et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 1998; 139: 4252–4263.

    Article  PubMed  CAS  Google Scholar 

  46. KUMARI G.L., AALLAG I.S., DAS R.P., DATTA J.K. Regional differences in steroidogenesis and hormone levels in the epididymis and vas deferens of adult rats. Int. J. Androl., 1980; 3: 267–281.

    Article  PubMed  CAS  Google Scholar 

  47. LEACH R.B., MADDOCK W.O., TOKUYAMA I., PAULSEN C.A., NELSON W.O. Clinical studies of testicular hormone production. Recent Prog. Horm. Res., 1956; 12: 377–393.

    PubMed  CAS  Google Scholar 

  48. LEJEUNE H., SANCHEZ P., SAEZ J.M. Enhancement of long-term testosterone secretion, and steroidogenic enzyme expression in human Leydig cells by coculture with human Sertoli cellenriched preparations. Int. J. Androl., 1998; 21: 129–140.

    Article  PubMed  CAS  Google Scholar 

  49. LEVALLET J., CARREAU S. Expression in vitro du gène de l’aromatase dans les cellules testiculaires du rat. C. R. Acad. Sc. (Paris) 1997; 320: 123–129.

    CAS  Google Scholar 

  50. LEVALLET J., BILINSKA B., MITTRE H., GENISSEL C., FRESNEL J., CARREAU S. Expression and immunolocalization of functional cytochrome P450 aromatase in mature rat testicular cells. Biol. Reprod., 1998; 58: 919–926.

    Article  PubMed  CAS  Google Scholar 

  51. LEVALLET J., DELARUE B., MITTRE H., CARREAU S. Alternative splicing events in the coding region of the P450 aromatase gene in male rat germ cells. J. Molec. Endocrinol., 1998; 20: 305–312.

    Article  CAS  Google Scholar 

  52. LI H., PAPADOPOULOS V., VIDIC B., DYM M., CULTY M. Regulation of rat testis gonocyte proliferation by platelet-derived growth factor and estradiol identification of signaling mechanisms involved. Endocrinology, 1997; 138: 1289–1298.

    Article  PubMed  CAS  Google Scholar 

  53. LUBAHN D.B., MOYER J.S., GOLDING T.S., COUSE J.F., KORACH K.S., SMITHIES O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. USA, 1993; 90: 11162–11166.

    Article  PubMed  CAS  Google Scholar 

  54. LUCONI M., BONACCORSI L., MAGGI M. et al. Identification and characterization of functional nongenomic progesterone receptors on human sperm membrane. J. Clin. Endocrinol. Metab., 1998; 83: 877–885.

    Article  PubMed  CAS  Google Scholar 

  55. MARIE E., VENDRELY E., de REVIERS M., CARREAU S. Stéroides plasmatiques et intratesticulaires: existe-t-il des correlations avec la spermatogenèse chez l’homme fertile et infécond. Ann. Endocrinol., 1995; 56: 337.

    Google Scholar 

  56. MARIE E., VENDRELY E, GALERAUD-DENIS I, de REVIERS M, CARREAU S. Increased testicular steroid concentrations in patients with idiopathic infertility and normal FSH levels. Andrologia, soumis.

  57. MEISTRICH M.L., HUGUES T.J., BRUCE W.R. Alteration of epididymal sperm transport and maturation in mice by oestrogen and testosterone. Nature 1975; 258: 145–147.

    Article  PubMed  CAS  Google Scholar 

  58. McCALMAN C.D., GETSIOS S., FAROOKHI R., BLASCHUK O.W. Estrogens potentiate the stimulatory effects of follicle stimulating hormone on N-cadherin messenger ribonucleic acid levels in cultured mouse Sertoli cells. Endocrinology, 1997; 138: 41–49.

    Article  Google Scholar 

  59. Mc LACHLAN R.I., WREFORD N.G., O’DONNELL L., de KRETSER D.M., ROBERTSON D.M. The endocrine regulation of spermatogenesis: independent roles for testosterone and FSH. J. Endocrinol., 1996; 148: 1–9.

    Article  Google Scholar 

  60. MORISHIMA A., GRUMBACH M.M., SIMPSON E.R., FISCHER C., QIN K. Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J. Clin. Endocrinol. Metab., 1995; 80: 3689–3698.

    Article  PubMed  CAS  Google Scholar 

  61. MORRISH D.W., VENNER P.M., SIY O., BARRON G., BHARDWAJ D., OUTHET D. Mechanisms of endocrine dysfunction in patients with testicular cancer. J. Natl. Cancer Inst. 1990; 82: 412–8.

    Article  PubMed  CAS  Google Scholar 

  62. MOSSELMAN S., POLMAN J., DIJKEMA R. ERβ: identification and characterization of a novel human estrogen receptor. FEBS Lett., 1996; 392: 49–53.

    Article  PubMed  CAS  Google Scholar 

  63. NAKAZUMI H., SASANO H., MAEHARA I., OZAKI M., TEZUKA F., ORIKASA S. Estrogen metabolism and impaired spermatogenesis in germ cell tumors of the testis. J. Clin. Endocrinol. Metab., 1996; 81: 1289–1295.

    Article  PubMed  CAS  Google Scholar 

  64. NITTA H., BUNICK D., HESS R.A. et al. Germ cells of the mouse testis express P450 aromatase. Endocrinology, 1993; 132: 1396–1401.

    Article  PubMed  CAS  Google Scholar 

  65. O’MARCAIGH A., LEDGER G.A., ROCHE P.C., PARISI J.E., ZIMMERMAN D. Aromatase ex-pression in human germinomas with possible biological effects. J. Clin. Endocrinol. Metab. 1996; 80: 3763–6.

    Article  Google Scholar 

  66. PAPADOPOULOS V., DROSDOWSKY M.A., CARREAU S. On the existence of two Leydig cell populations in aged human testis. Ann. NY. Acad. Sci., 1987; 513: 356–359.

    Article  Google Scholar 

  67. PAYNE A.H., KELCH R.P., MUSICH S.S., HALPERN M.E. Intratesticular site of aromatization in the human. J. Clin. Endocrinol. Metab., 1976; 42: 1081–1087.

    Article  PubMed  CAS  Google Scholar 

  68. PURVIS K., LANDGREN B.M., CEKAN Z., DICZFALUSY E. Indices of gonadal function in the human male. Seminal plasma levels of steroids in normal and pathological conditions. Clin. Endocrinol., 1975; 4: 247–258.

    Article  CAS  Google Scholar 

  69. REPKE K.R., MATTHES E. Tamoxifen is a Na+ antagonistic inhibitor of Na+/K+ transporting ATPase from tumor and normal cells. J. Enzyme Inhib., 1994; 8: 207–212.

    Article  PubMed  CAS  Google Scholar 

  70. RAESIDE J.J. (1969) The isolation of estrone sulphate and estradiol-17β sulphate from stallion testis. Can. J. Biochem., 1969; 47; 811–815.

    Article  PubMed  CAS  Google Scholar 

  71. SAEZ J.M. Leydig cells: endocrine, paracrine and autocrine regulation. Endocr. Rev., 1994; 15: 574–626.

    PubMed  CAS  Google Scholar 

  72. SAUNDERS P.T.K., FISHER J.S., SHARPE R.M., MILLAR M.R. Expression of oestrogen receptor beta (ERβ) occurs in multiple cell types, including some germ cells, in the rat testis. J. Endocrinol., 1998; 156: R13-R17.

    Article  PubMed  CAS  Google Scholar 

  73. SHARPE R.M. Do males rely on female hormones. Nature, 1997; 390: 447–448

    Article  PubMed  CAS  Google Scholar 

  74. SHARPE R.M. The roles of oestrogen in the male. TEM, 1998; 9: 371–377

    PubMed  CAS  Google Scholar 

  75. SIMPSON E.R., MAHENDROO M.S., MEANS G.D. et al. Aromatase cytochrome P450, the enzyme responsible for estrogen biosynthesis. Endocr. Rev., 1994; 15: 342–355.

    PubMed  CAS  Google Scholar 

  76. SIMPSON E.R., MICHAEL M.D., AGARWAL V.R., HINSHELWOOD M.M., BULUN S.E., ZHAO Y. Expression of the CYP 19 (aromatase) gene: an unusual case of alternative promoter usage. FASEB J., 1997; 11: 29–36.

    PubMed  CAS  Google Scholar 

  77. SHETTY G., KRISHNAMURTHY H., KRISHNAMURTHY H.N., BHATNAGAR S., MOUDGAL R.N. Effect of estrogen deprivation on the reproductive physiology of male and female primates. J. Steroid Biochem. Molec. Biol. 1997; 61: 157–166.

    Article  PubMed  CAS  Google Scholar 

  78. SHETTY G., KRISHNAMURTHY H., KRISHNAMURTHY H.N. et al. Effect of long term treatment with aromatase inhibitor on testicular function of adult male bonnet monkeys. Steroids, 1998; 63: 414–420.

    Article  PubMed  CAS  Google Scholar 

  79. SMITH EP, BOYD J, FRANK GR et al. Oestrogen resistance caused by a mutation in the oestrogen receptor gene in man. New Engl. J. Med., 1994; 331: 1056–1061.

    Article  PubMed  CAS  Google Scholar 

  80. SONG W.C., QIAN Y., SUN X., NEGISHI M. Cellular localization and regulation of expression of testicular estrogen sulfotransferase. Endocrinology, 1997; 138: 5006–5012.

    Article  PubMed  CAS  Google Scholar 

  81. TASH J.S., MEANS A.R. Regulation of protein phosphorylation and motility by cyclic adenosine monophosphate. Biol. Reprod., 1982; 26: 745–763.

    Article  PubMed  CAS  Google Scholar 

  82. TASH J.S., MEANS A.R. Ca2+ regulation of sperm axonemal motility. Methods Enzymol., 1987; 139: 808–823.

    Article  PubMed  CAS  Google Scholar 

  83. TEA N.T., CASTANIER M., GRENIER J., SCHOLLER R. Taux d’oestrogènes dans le plasma séminal; comparaison avec le spermogramme. Ann. Endocrinol., 1972; 33: 297–298.

    CAS  Google Scholar 

  84. TONEY W.T., DANZO B.J. Developmental changes and hormonal regulation of estrogen and androgen receptors present in the rabbit epididymis. Biol. Reprod., 1988; 39: 818–828.

    Article  PubMed  CAS  Google Scholar 

  85. TOPPARI J., LARSEN J.C., CHRISTIANSEN P et al. Male reproductive health and environmental xenoestrogens. Environ. Health Perspect., 1996; 104: 741–803.

    Article  PubMed  CAS  Google Scholar 

  86. TSUBOTA T., NITTA H., OSAWA Y et al. Immunolocalization of steroidogenic enzymes, P450scc, 3β-HSD, P450c17, and P450arom in the hokkaido brown bear (Ursus arctos yesoensis) testis. Gen. Comp. Endocrinol., 1993; 92: 439–444.

    Article  PubMed  CAS  Google Scholar 

  87. TSUTSUMI I., FUGIMORI K., NAKAMURA R.M., MATHER J.P., ONO T., DIZEREGA G.S. Disruption of seminiferous epithelial function in the rat by ovarian protein. Biol. Reprod., 1987; 36: 451–461.

    Article  PubMed  CAS  Google Scholar 

  88. van PELT A.M.M., de ROOIJ D.G., van der BURG B., van der SAAG P.T., GUSTAFSSON J.A., KUIPER G.G.J.M. Ontogeny of estrogen receptor-β expression in rat testis. Endocrinology, 1999; 140: 478–483.

    Article  PubMed  Google Scholar 

  89. VORNBERGER W., PRINS G., MUSTO N.A., SUAREZ-QUIAN C.A. Androgen receptor distribution in rat testis: new implications for androgen regulation of spermatogenesis. Endocrinology, 1994; 134: 2307–2316.

    Article  PubMed  CAS  Google Scholar 

  90. YOUNG J., BULUN S.E., AGARWAL V. et al. Aromatase expression in a feminizing adrenocortical tumor. J. Clin. Endocrinol. Metab., 1996; 81: 3173–3176.

    Article  PubMed  CAS  Google Scholar 

  91. ZONDEK B. Mass excretion of oestrogenic hormone in the urine of the stallion. Nature, 1934; 193: 209–210.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Clinique de Reproduction Humaine, CHRU Clémenceau, Caen

    I. Galeraud-Denis & E. Marie

  2. Laboratoire de Biochimie-IRBA, UPRES EA 2608, Université, 14032, CAEN Cédex

    S. Carreau

Authors
  1. I. Galeraud-Denis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. Marie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Carreau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. Galeraud-Denis.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Galeraud-Denis, I., Marie, E. & Carreau, S. Estrogènes et spermatozoïdes. Androl. 9, 252–260 (1999). https://doi.org/10.1007/BF03035237

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03035237

Mots-clés

Key words

Basic and Clinical Andrology

ISSN: 2051-4190