Skip to main content

Régulation des fonctions de l’épithélium épididymaire des mammifères: état des lieux

Current state of regulation of mammalian epididymal epithelial functions

Resume

Les gamètes mâles élaborés dans le testicule où se déroule la spermatogenèse poursuivent leur maturation hors de la gonade dans les conduits génitaux. L’épididyme est au centre de cette maturation post-testiculaire des spermatozoïdes responsable de l’acquisition de leur aptitude à se mouvoir ainsi qu’à reconnaître et à pénétrer un ovocyte, événements essentiels pour la fécondation.

Durant leur transit dans le canal épididymaire les gamètes évoluent dans un environnement luminal en perpétuel changement via le jeu complexe des activités de sécrétion et de réabsorption de l’épithélium épididymaire. Ces activités de sécrétion régulées dans l’espace et dans le temps ce qui fait de cet épithélium épididymaire un tissu d’une grande complexité soumis à un réseau élaboré de régulations croisées.

Outre les régulations classiques de type endocrine et paracrine, la région proximale de l’organe est soumise à des contrôles lumicrines par des facteurs d’origine testiculaire qui ajoutent à la complexité des réseaux de régulations mis en jeu. Le travail réalisé ci-dessous se veut être un état des lieux exhaustif des acteurs dont la littérature a montré qu’ils exerçaient une modulation de l’activité épididymaire.

Abstract

Male gametes formed in the testis, the site of spermatogenesis, continue their maturation outside of the gonad in the genital tract. The epididymis is at the centre of this process of post-testicular maturation of spermatozoa, responsible for acquisition of their mobility and their ability to recognize and penetrate an oocyte, essential events for fertilization.

During their transit in the epididymal ducts, gametes evolve in a perpetually changing luminal environment due to complex interactions of secretion and reabsorption activities of the epididymal epithelium. These numerous secretion and reabsorption activities are closely regulated in space and time, which makes this epididymal epithelium a very complex tissue subject to an elaborate network of cross-regulations.

Apart from classical endocrine and paracrine regulations, the proximal part of the epididymis is also subject to lumicrine regulation by testicular factors which increase the complexity of the regulation networks involved. The present study tries to present an exhaustive review of the factors demonstrated in the literature to exert a modulation of epididymal activity.

References

  1. 1.

    ABE K., TAKANO H., ITO T.: Interruption of the luminal flow in the epididymal duct of the corpus epididymidis in the mouse, with special reference to differentiation of the epididymal epithelium. Arch. Histol. Jpn, 1984, 47: 137–147.

    PubMed  CAS  Article  Google Scholar 

  2. 2.

    ABOU-HAILA A., FAIN-MAUREL M.A.: Regional differences of the proximal part of mouse epididymis: morphological and histochemical characterization. Anat. Rec., 1984, 209: 197–208.

    PubMed  CAS  Article  Google Scholar 

  3. 3.

    ABOU-HAILA A., FAIN-MAUREL M.A.: Postnatal differentiation of the enzymatic activity of the mouse epididymis. Int. J. Androl., 1985, 8: 441–458.

    PubMed  CAS  Article  Google Scholar 

  4. 4.

    AGRE P., KOZONO D.: Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett., 2003, 555: 72–78.

    PubMed  CAS  Article  Google Scholar 

  5. 5.

    ALARID E.T., CUNHA G.R., YOUNG P., NICOLL C.S.: Evidence for an organ- and sex-specific role of basic fibroblast growth factor in the development of the fetal mammalian reproductive tract. Endocrinology, 1991, 129: 2148–2154.

    PubMed  CAS  Google Scholar 

  6. 6.

    ANDERSON M.E., PAPARO A.A., MARTAN J.: Paraformaldehyde-induced fluorescence as a histochemical test for 5-hydroxytryptamine in the epididymis of the opossum. J. Anat., 1979, 129: 141–149.

    PubMed  CAS  Google Scholar 

  7. 7.

    ANDERSON R.A., CAMBRAY N., HARTLEY P.S., MCNEILLY A.S.: Expression and localization of inhibin alpha, inhibin/activin betaA and betaB and the activin type II and inhibin beta-glycan receptors in the developing human testis. Reproduction, 2002, 123: 779–788.

    PubMed  CAS  Article  Google Scholar 

  8. 8.

    ANDERSSON S., BERMAN D.M., JENKINS E.P., RUSSELL D.W.: Deletion of steroid 5 alpha-reductase 2 gene in male pseudohermaphroditism. Nature, 1991, 354: 159–161.

    PubMed  CAS  Article  Google Scholar 

  9. 9.

    ARAGONA C., FRIESEN H.G.: Specific prolactin binding sites in the prostate and testis of rats. Endocrinology, 1975, 97: 677–684.

    PubMed  CAS  Google Scholar 

  10. 10.

    ASSINDER S.J., CAREY M., PARKINSON T., NICHOLSON H.D.: Oxytocin and vasopressin expression in the ovine testis and epididymis: changes with the onset of spermatogenesis. Biol. Reprod., 2000, 63: 448–456.

    PubMed  CAS  Article  Google Scholar 

  11. 11.

    ASTRAUDO C., LEFEVRE A., BOUE F., DURR F., FINAZ C.: In vivo regulation of rat epididymal proteins by retinoids: analysis by two-dimensional electrophoresis. Arch. Androl., 1995, 35: 247–259.

    PubMed  CAS  Article  Google Scholar 

  12. 12.

    AU C.L., NGAI H.K., YEUNG C.H., WONG P.Y.: Effect of adrenalectomy and hormone replacement on sodium and water transport in the perfused rat cauda epididymidis. J. Endocrinol., 1978, 77: 265–266.

    PubMed  CAS  Article  Google Scholar 

  13. 13.

    AYER-LELIEVRE C., OLSON L., EBENDAL T., HALLBOOK F., PERSSON H.: Nerve growth factor mRNA and protein in the testis and epididymis of mouse and rat. Proc. Natl. Acad. Sci. U S A, 1988, 85: 2628–2632.

    PubMed  CAS  Article  Google Scholar 

  14. 14.

    BADRAN H.H., HERMO L.S.: Expression and regulation of aquaporins 1, 8, and 9 in the testis, efferent ducts, and epididymis of adult rats and during postnatal development. J. Androl., 2002, 23: 358–373.

    PubMed  CAS  Google Scholar 

  15. 15.

    BAHATHIQ A.O., STEWART R.L., BAXTER L., WELLS M., MOORE H.D., LEDGER W.L.: Tissue immunoexpression and messenger ribonucleic acid localization of inhibin/activin subunit in human epididymis. Fertil. Steril., 2005, 83: 78–85.

    PubMed  CAS  Article  Google Scholar 

  16. 16.

    BAKER J., HARDY M.P., ZHOU J. et al.: Effects of an Igf1 gene null mutation on mouse reproduction. Mol. Endocrinol., 1996, 10: 903–918.

    PubMed  CAS  Article  Google Scholar 

  17. 17.

    BAKER M.A., AITKEN R.J.: The importance of redox regulated pathways in sperm cell biology. Mol. Cell. Endocrinol., 2004, 216: 47–54.

    PubMed  CAS  Article  Google Scholar 

  18. 18.

    BAKER H.W.G., WORGUL T.J., SANTEN R.J., JEFFERSON L.S. BARDIN, C.W.: Effect of prolactin on nuclear androgens in perfused male sex accessory organs. In: Troen P., Nankin H.R. eds. The Testis in Normal and Infertile Men. New York, Raven Press, 1977: 379–385.

    Google Scholar 

  19. 19.

    BARTKE A.: Effects of prolactin on spermatogenesis in hypophysectomized mice. J. Endocrinol., 1971, 49: 311–316.

    PubMed  CAS  Article  Google Scholar 

  20. 20.

    BARTKE A., CROFT B.T., DALTERIO S.: Prolactin restores plasma testosterone levels and stimulates testicular growth in hamsters exposed to short day-length. Endocrinology, 1975, 97: 1601–1604.

    PubMed  CAS  Google Scholar 

  21. 21.

    BASCIANI S., MARIANI S., ARIZZI M. et al.: Expression of plateletderived growth factor (PDGF) in the epididymis and analysis of the epididymal development in PDGF-A, PDGF-B, and PDGF receptor beta deficient mice. Biol. Reprod., 2004, 70: 168–177.

    PubMed  CAS  Article  Google Scholar 

  22. 22.

    BERNARD D.J., CHAPMAN S.C., WOODRUFF, T.K.: An emerging role for co-receptors in inhibin signal transduction. Mol. Cell. Endocrinol., 2001, 180: 55–62.

    PubMed  CAS  Article  Google Scholar 

  23. 23.

    BINART N., MELAINE N., PINEAU C. et al.: Male reproductive function is not affected in prolactin receptor-deficient mice. Endocrinology, 2003, 144: 3779–3782.

    PubMed  CAS  Article  Google Scholar 

  24. 24.

    BLACKMORE P.F., NEULEN J., LATTANZIO F., BEEBE S.J.: Cell surface-binding sites for progesterone mediate calcium uptake in human sperm. J. Biol. Chem., 1991, 266: 18655–18659.

    PubMed  CAS  Google Scholar 

  25. 25.

    BLANER W.S., DAS K., MERTZ J.R., DAS S.R., GOODMAN D.S.: Effects of dietary retinoic acid on cellular retinol- and retinoic acid-binding protein levels in various rat tissues. J. Lipid. Res., 1986, 27: 1084–1088.

    PubMed  CAS  Google Scholar 

  26. 26.

    BLOMHOFF R., GREEN M.H., NORUM K.R.: VITAMIN A: physiological and biochemical processing. Annu. Rev. Nutr., 1992, 12: 37–57.

    PubMed  CAS  Article  Google Scholar 

  27. 27.

    BOMGARDNER D., WEHRENBERG U., RUNE G.M.: TGF-beta could be involved in paracrine actions in the epididymis of the marmoset monkey (Callithrix jacchus). J. Androl., 1999, 20: 375–383.

    PubMed  CAS  Google Scholar 

  28. 28.

    BOTTCHER R.T., NIEHRS C.: Fibroblast growth factor signaling during early vertebrate development. Endocr. Rev., 2005, 26: 63–77.

    PubMed  Article  CAS  Google Scholar 

  29. 29.

    BOULANGER V., ZHAO X., LACASSE P.: Protective effect of melatonin and catalase in bovine neutrophil-induced model of mammary cell damage. J. Dairy Sci., 2002, 85: 562–569.

    PubMed  CAS  Google Scholar 

  30. 30.

    BROCKMANN H.: Die Isolierung des antirachitischen Vitamins aus Thunfischleberol. Hoppe Seylers Z. Physiol. Chem., 1936, 241: 104–115.

    CAS  Google Scholar 

  31. 31.

    BROOKS D.E.: Influence of testicular secretions on tissue weight and on metabolic and enzyme activities in the epididymis of the rat. J. Endocrinol., 1979, 82: 305–313.

    PubMed  CAS  Article  Google Scholar 

  32. 32.

    BROOKS D.E.: Metabolic activity in the epididymis and its regulation by androgens. Physiol. Rev., 1981, 61: 515–555.

    PubMed  CAS  Google Scholar 

  33. 33.

    BRUMLOW W.B., ADAMS C.S.: Immunocytochemical detection of prolactin or prolactin-like immunoreactivity in epididymis of mature male mouse. Histochemistry, 1990, 93: 299–304.

    PubMed  CAS  Article  Google Scholar 

  34. 34.

    BURNETT A.L., RICKER D.D., CHAMNESS S.L. et al.: Localization of nitric oxide synthase in the reproductive organs of the male rat. Biol. Reprod., 1995, 52: 1–7.

    PubMed  CAS  Article  Google Scholar 

  35. 35.

    BYYNY R.L., ORTH D.N., COHEN S.: Radioimmunoassay of epidermal growth factor. Endocrinology, 1972, 90: 1261–1266.

    PubMed  CAS  Google Scholar 

  36. 36.

    CANCILLA B., DAVIES A., FORD-PERRISS M., RISBRIDGER G.P.: Discrete cell- and stage-specific localisation of fibroblast growth factors and receptor expression during testis development. J. Endocrinol., 2000, 164: 149–159.

    PubMed  CAS  Article  Google Scholar 

  37. 37.

    CARPINO A., ROMEO F., RAGO V.: Aromatase immunolocalization in human ductuli efferentes and proximal ductus epididymis. J. Anat., 2004, 204: 217–220.

    PubMed  CAS  Article  Google Scholar 

  38. 38.

    CARR D.W., USSELMAN M.C., ACOTT T.S.: Effects of pH, lactate, and viscoelastic drag on sperm motility: a species comparison. Biol. Reprod., 1985, 33: 588–595.

    PubMed  CAS  Article  Google Scholar 

  39. 39.

    CARREAU S., GENISSEL C., BILINSKA B., LEVALLET J.: Sources of oestrogen in the testis and reproductive tract of the male. Int. J Androl., 1999, 22: 211–223.

    PubMed  CAS  Article  Google Scholar 

  40. 40.

    CATIZONE A., RICCI G., GALDIERI M.: Functional role of hepatocyte growth factor receptor during sperm maturation. J. Androl., 2002, 23: 911–918.

    PubMed  CAS  Google Scholar 

  41. 41.

    CAUSSANEL V., TABONE E., HENDRICK J.C., DACHEUX F., BENAHMED M.: Cellular distribution of transforming growth factor betas 1, 2, and 3 and their types I and II receptors during postnatal development and spermatogenesis in the boar testis. Biol. Reprod., 1997, 56: 357–367.

    PubMed  CAS  Article  Google Scholar 

  42. 42.

    CHAN H.C., KO W.H., ZHAO W., FU W.O., WONG P.Y.: Evidence for independent Cl- and HCO3- secretion and involvement of an apical Na(+)-HCO3-cotransporter in cultured rat epididymal epithelia. Exp. Physiol., 1996, 81: 515–524.

    PubMed  CAS  Google Scholar 

  43. 43.

    CHAO M.V.: Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci., 2003, 4: 299–309.

    PubMed  CAS  Article  Google Scholar 

  44. 44.

    CHAREST N.J., JOSEPH D.R., WILSON E.M., FRENCH F.S.: Molecular cloning of complementary deoxyribonucleic acid for an androgen-regulated epididymal protein: sequence homology with metalloproteins. Mol. Endocrinol., 1988, 2: 999–1004.

    PubMed  CAS  Article  Google Scholar 

  45. 45.

    CHENG F.P., FAZELI A.R., VOORHOUT W.F., TREMOLEDA J.L., BEVERS M.M., COLENBRANDER B.: Progesterone in mare follicular fluid induces the acrosome reaction in stallion spermatozoa and enhances in vitro binding to the zona pellucida. Int. J. Androl., 1998, 21: 57–66.

    PubMed  CAS  Article  Google Scholar 

  46. 46.

    CHENG F.P., GADELLA B.M., VOORHOUT W.F., FAZELI A., BEVERS M.M., COLENBRANDER B.: Progesterone-induced acrosome reaction in stallion spermatozoa is mediated by a plasma membrane progesterone receptor. Biol. Reprod., 1998, 59: 733–742.

    PubMed  CAS  Article  Google Scholar 

  47. 47.

    CHEUK B.L., LEUNG P.S., LO A.C., WONG P.Y.: Androgen control of cyclooxygenase expression in the rat epididymis. Biol. Reprod., 2000, 63: 775–780.

    PubMed  CAS  Google Scholar 

  48. 48.

    CHIKHI N., HOLIC N., GUELLAEN G., LAPERCHE Y.: Gammaglutamyl transpeptidase gene organization and expression: a comparative analysis in rat, mouse, pig and human species. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 1999, 122: 367–380.

    PubMed  CAS  Article  Google Scholar 

  49. 49.

    CHOW B.K., CHEUNG K.H., TSANG E.M., LEUNG M.C., LEE S.M., WONG P.Y.: Secretin controls anion secretion in the rat epididymis in an autocrine/paracrine fashion. Biol. Reprod., 2004, 70: 1594–1599.

    PubMed  CAS  Article  Google Scholar 

  50. 50.

    CLAPHAM D.E., RUNNELS L.W., STRUBING C.: The TRP ion channel family. Nat. Rev. Neurosci., 2001, 2: 387–396.

    PubMed  CAS  Article  Google Scholar 

  51. 51.

    CLULOW J., JONES R.C., HANSEN L.A.: 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., 1994, 79: 915–928.

    PubMed  CAS  Google Scholar 

  52. 52.

    CLULOW J., JONES R.C., HANSEN L.A., MAN S.Y.: Fluid and electrolyte reabsorption in the ductuli efferentes testis. J. Reprod. Fertil., 1998, Suppl 53: 1–14.

    CAS  Google Scholar 

  53. 53.

    COHEN J.P., HOFFER A.P., ROSEN S.: Carbonic anhydrase localization in the epidimymis and testis of the rat: histochemical and biochemical analysis. Biol. Reprod., 1976, 14: 339–346.

    PubMed  CAS  Article  Google Scholar 

  54. 54.

    COOPER T.G., WAGENFELD A., CORNWALL G.A. et al.: Gene and protein expression in the epididymis of infertile c-ros receptor tyrosine kinase-deficient mice. Biol. Reprod., 2003, 69: 1750–1762.

    PubMed  CAS  Article  Google Scholar 

  55. 55.

    CORNWALL G.A., COLLIS R., XIAO Q., HSIA N., HANN S.R.: BMyc, a proximal caput epididymal protein, is dependent on androgens and testicular factors for expression. Biol. Reprod., 2001, 64: 1600–1607.

    PubMed  CAS  Article  Google Scholar 

  56. 56.

    CORNWALL G.A., ORGEBIN-CRIST M.C., HANN S.R.: The CRES gene: a unique testis-regulated gene related to the cystatin family is highly restricted in its expression to the proximal region of the mouse epididymis. Mol. Endocrinol., 1992, 6: 1653–1664.

    PubMed  CAS  Article  Google Scholar 

  57. 57.

    COSTA S.L., BOEKELHEIDE K., VANDERHYDEN B.C., SETH R., MCBURNEY M.W.: Male infertility caused by epididymal dysfunction in transgenic mice expressing a dominant negative mutation of retinoic acid receptor alpha. Biol. Reprod., 1997, 56: 985–990.

    PubMed  CAS  Article  Google Scholar 

  58. 58.

    CREPIEUX P., COLL J., STEHELIN D.: The Ets family of proteins: weak modulators of gene expression in quest for transcriptional partners. Crit. Rev. Oncog., 1994, 5: 615–638.

    PubMed  CAS  Google Scholar 

  59. 59.

    CUTHBERT A.W., WONG P.Y.: Electrogenic anion secretion in cultured rat epididymal epithelium. J. Physiol., 1986, 378: 335–345.

    PubMed  CAS  Google Scholar 

  60. 60.

    Dahia C.L., Rao A.J.: Demonstration of follicle-stimulating hormone receptor in cauda epididymis of rat. Biol. Reprod., 2006.

  61. 61.

    DANZO B.J., ORGEBIN-CRIST M.C., ELLER B.C.: Changes in 5alpha-dihydrotestosterone binding to epididymal cytosol during sexual maturation in rabbits: correlation with morphological changes in the testis and epididymis. Mol. Cell. Endocrinol., 1975, 3: 203–220.

    PubMed  CAS  Article  Google Scholar 

  62. 62.

    DEL RIO A.G., BLANCO A.M., PIGNATARO O., NIEPOMNISZCZE H., JUVENAL G., PISAREV M.A.: High-affinity binding of T3 to epididymis nuclei. Arch. Androl., 2000, 44: 187–191.

    PubMed  Article  Google Scholar 

  63. 63.

    DEL RIO A.G., VALDEZ TOLEDO C.L., QUIROS M.C.: Thyroid gland and epididymal function in rats—histological study. Arch. Androl., 1979, 3: 19–22.

    PubMed  Article  Google Scholar 

  64. 64.

    DESAI K.V., FLANDERS K.C., KONDAIAH P.: Expression of transforming growth factor-beta isoforms in the rat male accessory sex organs and epididymis. Cell Tissue Res., 1998, 294: 271–277.

    PubMed  CAS  Article  Google Scholar 

  65. 65.

    DESAI K.V., KONDAIAH P.: Androgen ablation results in differential regulation of transforming growth factor-beta isoforms in rat male accessory sex organs and epididymis. J. Mol. Endocrinol., 2000, 24: 253–260.

    PubMed  CAS  Article  Google Scholar 

  66. 66.

    DIERICH A., SAIRAM M.R., MONACO L. et al.: Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc. Natl. Acad. Sci. U S A, 1998, 95: 13612–13617.

    PubMed  CAS  Article  Google Scholar 

  67. 67.

    DOMBROWICZ D., SENTE B., CLOSSET J., HENNEN G.: Dose-dependent effects of human prolactin on the immature hypophysectomized rat testis. Endocrinology, 1992, 130: 695–700.

    PubMed  CAS  Article  Google Scholar 

  68. 68.

    DREVET J.R., LAREYRE J.J., SCHWAAB V., VERNET P., DUFAURE J.P.: The PEA3 protein of the Ets oncogene family is a putative transcriptional modulator of the mouse epididymis-specific glutathione peroxidase gene gpx5. Mol. Reprod. Dev., 1998, 49: 131–140.

    PubMed  CAS  Article  Google Scholar 

  69. 69.

    DUFAURE J.P., LAREYRE J.J., SCHWAAB V., MATTEI M.G., DREVET J.R.: Structural organization, chromosomal localization, expression and phylogenetic evaluation of mouse glutathione peroxidase encoding genes. C. R. Acad. Sci. III, 1996, 319: 559–568.

    PubMed  CAS  Google Scholar 

  70. 70.

    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: 4796–4805.

    PubMed  CAS  Article  Google Scholar 

  71. 71.

    EINSPANIER A., IVELL R.: Oxytocin and oxytocin receptor expression in reproductive tissues of the male marmoset monkey. Biol. Reprod., 1997, 56: 416–422.

    PubMed  CAS  Article  Google Scholar 

  72. 72.

    ELKJAER M., VAJDA Z., NEJSUM L.N. et al.: Immunolocalization of AQP9 in liver, epididymis, testis, spleen, and brain. Biochem. Biophys. Res. Commun., 2000, 276: 1118–1128.

    PubMed  CAS  Article  Google Scholar 

  73. 73.

    ELSON S.D., BROWNE C.A., THORBURN G.D.: Identification of epidermal growth factor-like activity in human male reproductive tissues and fluids. J. Clin. Endocrinol. Metab., 1984, 58: 589–594.

    PubMed  CAS  Google Scholar 

  74. 74.

    ERGUN S., KILIC N., FIEDLER W., MUKHOPADHYAY A.K.: Vascular endothelial growth factor and its receptors in normal human testicular tissue. Mol. Cell. Endocrinol., 1997, 131: 9–20.

    PubMed  CAS  Article  Google Scholar 

  75. 75.

    ERGUN S., LUTTMER W., FIEDLER W., HOLSTEIN A.F.: Functional expression and localization of vascular endothelial growth factor and its receptors in the human epididymis. Biol. Reprod., 1998, 58: 160–168.

    PubMed  CAS  Article  Google Scholar 

  76. 76.

    EZER N., ROBAIRE B.: Gene expression is differentially regulated in the epididymis after orchidectomy. Endocrinology, 2003, 144: 975–988.

    PubMed  CAS  Article  Google Scholar 

  77. 77.

    FAN X., ROBAIRE B.: Orchidectomy induces a wave of apoptotic cell death in the epididymis. Endocrinology, 1998, 139: 2128–2136.

    PubMed  CAS  Article  Google Scholar 

  78. 78.

    FILIPPI S., LUCONI M., GRANCHI S. et al.: Estrogens, but not androgens, regulate expression and functional activity of oxytocin receptor in rabbit epididymis. Endocrinology, 2002, 143: 4271–4280.

    PubMed  CAS  Article  Google Scholar 

  79. 79.

    FILIPPI S., MORELLI A., VIGNOZZI L. et al.: Oxytocin mediates the estrogen-dependent contractile activity of endothelin-1 in human and rabbit epididymis. Endocrinology, 2005, 146: 3506–3517.

    PubMed  CAS  Article  Google Scholar 

  80. 80.

    FILIPPI S., VANNELLI G.B., GRANCHI S. et al.: Identification, localization and functional activity of oxytocin receptors in epididymis. Mol. Cell. Endocrinol., 2002, 193: 89–100.

    PubMed  CAS  Article  Google Scholar 

  81. 81.

    FIRNBERG N., NEUBUSER A.: FGF signaling regulates expression of Tbx2, Erm, Pea3, and Pax3 in the early nasal region. Dev. Biol., 2002, 247: 237–250.

    PubMed  CAS  Article  Google Scholar 

  82. 82.

    FORESTA C., CARETTO A., VAROTTO A., ROSSATO M., SCANDELLARI C.: Epidermal growth factor receptors (EGFR) localization in human testis. Arch. Androl., 1991, 27: 17–24.

    PubMed  CAS  Article  Google Scholar 

  83. 83.

    GARRETT J.E., GARRETT S.H., DOUGLASS J.: A spermatozoa-associated factor regulates proenkephalin gene expression in the rat epididymis. Mol. Endocrinol., 1990, 4: 108–118.

    PubMed  CAS  Article  Google Scholar 

  84. 84.

    GAUTAM R., PEREIRA B.M.: The effect of ovine prolactin on the epididymal sialic acid concentration in male rats. Clin. Exp. Pharmacol. Physiol., 1992, 19: 495–501.

    PubMed  CAS  Article  Google Scholar 

  85. 85.

    GAUTAM R., PEREIRA B.M.: Modulation in activity of some epididymal glycosidases by prolactin. Indian J. Exp. Biol., 1993, 31: 410–413.

    PubMed  CAS  Google Scholar 

  86. 86.

    GHYSELINCK N.B., DUFAURE I., LAREYRE J.J., RIGAUDIERE N., MATTEI M.G., DUFAURE J.P.: Structural organization and regulation of the gene for the androgen-dependent glutathione peroxidase-like protein specific to the mouse epididymis. Mol. Endocrinol., 1993, 7: 258–272.

    PubMed  CAS  Article  Google Scholar 

  87. 87.

    GILBERT E., MOREL A., TULLIEZ M. et al.: In vivo effects of activated H-ras oncogene expressed in the liver and in urogenital tissues. Int. J. Cancer, 1997, 73: 749–756.

    PubMed  CAS  Article  Google Scholar 

  88. 88.

    GOSS G.D., MCBURNEY M.W.: Physiological and clinical aspects of vitamin A and its metabolites. Crit. Rev. Clin. Lab. Sci., 1992, 29: 185–215.

    PubMed  CAS  Article  Google Scholar 

  89. 89.

    GOYAL H.O.: Morphology of the bovine epididymis. Am. J. Anat., 1985, 172: 155–172.

    PubMed  CAS  Article  Google Scholar 

  90. 90.

    GRIMBERG A., COHEN P.: Role of insulin-like growth factors and their binding proteins in growth control and carcinogenesis. J. Cell. Physiol., 2000, 183: 1–9.

    PubMed  CAS  Article  Google Scholar 

  91. 91.

    GRISWOLD M.D., BISHOP P.D., KIM K.H., PING R., SIITERI J.E., MORALES C.: Function of vitamin A in normal and synchronized seminiferous tubules. Ann. N. Y. Acad. Sci., 1989, 564: 154–172.

    PubMed  CAS  Article  Google Scholar 

  92. 92.

    Grove K.L., Speth R.C.: Rat epididymis contains functional angiotensin II receptors. Endocrinology, 1989, 125: 223–230.

    PubMed  CAS  Google Scholar 

  93. 93.

    GROVER A., SAIRAM M.R., SMITH C.E., HERMO L.: Structural and functional modifications of sertoli cells in the testis of adult follicle-stimulating hormone receptor knockout mice. Biol. Reprod., 2004, 71: 117–129.

    PubMed  CAS  Article  Google Scholar 

  94. 94.

    GROVER A., SMITH C.E., GREGORY M., CYR D.G., SAIRAM M.R., HERMO, L.: Effects of FSH receptor deletion on epididymal tubules and sperm morphology, numbers, and motility. Mol. Reprod. Dev., 2005, 72: 135–144.

    PubMed  CAS  Article  Google Scholar 

  95. 95.

    GUNASEKAR P.G., KUMARAN B., GOVINDARAJULU P.: Prolactin and Leydig cell steroidogenic enzymes in the bonnet monkey (Macaca radiata). Int. J. Androl., 1988, 11: 53–59.

    PubMed  CAS  Article  Google Scholar 

  96. 96.

    HAIR W.M., GUBBAY O., JABBOUR H.N., LINCOLN G.A.: Prolactin receptor expression in human testis and accessory tissues: localization and function. Mol. Hum. Reprod., 2002, 8: 606–611.

    PubMed  CAS  Article  Google Scholar 

  97. 97.

    HANSSON H.A., NILSSON A., ISGAARD J. et al.: Immunohistochemical localization of insulin-like growth factor I in the adult rat. Histochemistry, 1988, 89: 403–410.

    PubMed  CAS  Article  Google Scholar 

  98. 98.

    HARNEIT S., ERGUN S., PAUST H.J., MUKHOPADHYAY A.K., HOLSTEIN A.F.: Endothelin-1 and its receptors in the human epididymis. Adv. Exp. Med. Biol., 1997, 424: 191–192.

    PubMed  CAS  Google Scholar 

  99. 99.

    HARRIS G.C., FRAYNE J., NICHOLSON H.D.: Epididymal oxytocin in the rat: its origin and regulation. Int. J. Androl., 1996, 19: 278–286.

    PubMed  CAS  Article  Google Scholar 

  100. 100.

    HAUSSLER M.R.: Vitamin D receptors: nature and function. Annu. Rev. Nutr., 1986, 6: 527–562.

    PubMed  CAS  Article  Google Scholar 

  101. 101.

    HENRY H.L., NORMAN A.W.: Vitamin D: metabolism and biological actions. Annu. Rev. Nutr., 1984, 4: 493–520.

    PubMed  CAS  Article  Google Scholar 

  102. 102.

    HERMO L., KRZECZUNOWICZ D., RUZ R.: Cell specificity of aquaporins 0, 3, and 10 expressed in the testis, efferent ducts, and epididymis of adult rats. J. Androl., 2004, 25: 494–505.

    PubMed  CAS  Google Scholar 

  103. 103.

    HERMO L., ROBAIRE B.: Epididymal cell types and their functions. In: Hinton R.A. ed. The epididymis: from molecules to clinical practice. New York, Kluwer Academic-Plenum Publishers, 2002: 81–102.

    Google Scholar 

  104. 104.

    HERRERO M.B., PEREZ MARTINEZ S., VIGGIANO J.M., POLAK J.M., DE GIMENO M.F.: Localization by indirect immunofluorescence of nitric oxide synthase in mouse and human spermatozoa. Reprod. Fertil. Dev., 1996, 8: 931–934

    PubMed  CAS  Article  Google Scholar 

  105. 105.

    HERRERO M.B., VIGGIANO J.M., PEREZ MARTINEZ S., DE GIMENO M.F.: Evidence that nitric oxide synthase is involved in progesterone-induced acrosomal exocytosis in mouse spermatozoa. Reprod. Fertil. Dev., 1997, 9: 433–439.

    PubMed  CAS  Article  Google Scholar 

  106. 106.

    HESS R.A.: The efferent ductules: structure and functions. In: Robaire B, Hinton B.T. eds. The Epididymis: from Molecules to clinical practice. New-York, Kluwer Academic-Plenum Publishers, 2002: 49–80.

    Google Scholar 

  107. 107.

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

    PubMed  CAS  Article  Google Scholar 

  108. 108.

    HESS R.A., BUNICK D., LUBAHN D.B., ZHOU Q., BOUMA J.: Morphologic changes in efferent ductules and epididymis in estrogen receptor-alpha knockout mice. J. Androl., 2000, 21: 107–121.

    PubMed  CAS  Google Scholar 

  109. 109.

    HESS R.A., ZHOU Q., NIE R.: The role of estrogens in the endocrine and paracrines regulation of the efferent ductules, epididymis and vas deferens. Robaire B., Hinton B.T. eds. New-York, Kluwer Academic-Plenum Publishers, 2002: 317–338.

    Google Scholar 

  110. 110.

    HIB J.: The in vitro effects of oxytocin and vasopressin on spontaneous contractility of the mouse cauda epididymidis. Biol. Reprod., 1974, 11, 436–439.

    PubMed  CAS  Article  Google Scholar 

  111. 111.

    HIB J.: The ‘in vivo’ effects of oxytocin and vasopressin on spontaneous contractility of the rat epididymis. Int. J. Fertil., 1977, 22: 63–64.

    PubMed  CAS  Google Scholar 

  112. 112.

    HINTON B.T.: The testicular and epididymal luminal amino acid microenvironment in the rat. J. Androl., 1990, 11: 498–505.

    PubMed  CAS  Google Scholar 

  113. 113.

    HINTON B.T., KEEFER D.A.: Binding of [3H]aldosterone to a single population of cells within the rat epididymis. J. Steroid. Biochem., 1985, 23: 231–233.

    PubMed  CAS  Article  Google Scholar 

  114. 114.

    HINTON B.T., KIRBY J.L., RODRIGUEZ C.M., LYE R.J., TROAN B.V., YANG L.: Signal transduction pathways to gene expression. In: Hinton B.T., Turner T.T. eds. Third International Conference on the Epididymis. Charlottesville, Virginia, USA. The Van Doren Company, 2003.

    Google Scholar 

  115. 115.

    HINTON B.T., LAN Z.J., RUDOLPH D.B., LABUS J.C., LYE R.J.: Testicular regulation of epididymal gene expression. J. Reprod. Fertil., 1998, Suppl 53: 47–57.

    CAS  Google Scholar 

  116. 116.

    HINTON B.T., PALLADINO M.A., RUDOLPH D., LABUS, J.C.: The epididymis as protector of maturing spermatozoa. Reprod. Fertil. Dev., 1995, 7: 731–745.

    PubMed  CAS  Article  Google Scholar 

  117. 117.

    HINTON B.T., PALLADINO M.A., RUDOLPH D.B., LAN Z.J., LABUS J.C.: The role of the epididymis in the protection of spermatozoa. In: Pederson R.A., Schatten G.P. eds. Current Topics in Developmental Biology. New York, Academic Press, 1996, Vol. 33: 61–102.

    Google Scholar 

  118. 118.

    HOLLAND M.K., ORGEBIN-CRIST M.C.: Characterization and hormonal regulation of protein synthesis by the murine epididymis. Biol. Reprod., 1988, 38: 487–496.

    PubMed  CAS  Article  Google Scholar 

  119. 119.

    HOTTEN G., NEIDHARDT H., SCHNEIDER C., POHL J.: Cloning of a new member of the TGF-beta family: a putative new activin beta C chain. Biochem. Biophys. Res. Commun., 1995, 206: 608–613.

    Article  Google Scholar 

  120. 120.

    HUANG S.J., FU W.O., CHUNG Y.W., ZHOU T.S., WONG P.Y.: Properties of cAMP-dependent and Ca(2+)-dependent whole cell Cl-conductances in rat epididymal cells. Am. J. Physiol., 1993, 264: C794–802.

    PubMed  CAS  Google Scholar 

  121. 121.

    HUANG S.J., LEUNG A.Y., FU W.O. et al.: Electrophysiological studies of anion secretion in cultured human epididymal cells. J. Physiol., 1992, 455: 455–469.

    PubMed  CAS  Google Scholar 

  122. 122.

    HURKADLI K.S., JOSEPH R., GARDE S.V., SHETH A.R.: De novo biosynthesis and localization of inhibin in marmoset (Callithrix jacchus) and rat epididymis. Indian J. Exp. Biol., 1991, 29: 715–720.

    PubMed  CAS  Google Scholar 

  123. 123.

    IGARASHI-MIGITAKA J., TAKESHITA A., KOIBUCHI N., YAMADA S., OHTANI-KANEKO R., HIRATA K.: Differential expression of p160 steroid receptor coactivators in the rat testis and epididymis. Eur. J. Endocrinol., 2005, 153: 595–604.

    PubMed  CAS  Article  Google Scholar 

  124. 124.

    ILIO K.Y., HESS R.A.: Structure and function of the ductuli efferentes: a review. Microsc. Res. Tech., 1994, 29: 432–467.

    PubMed  CAS  Article  Google Scholar 

  125. 125.

    ISAACS J.T.: Antagonistic effect of androgen on prostatic cell death. Prostate, 1984, 5: 545–557.

    PubMed  CAS  Article  Google Scholar 

  126. 126.

    JANULIS L., BAHR J.M., HESS R.A., JANSSEN 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 

  127. 127.

    JELKMANN W.: Erythropoietin: structure, control of production, and function. Physiol. Rev., 1992, 72: 449–489.

    PubMed  CAS  Google Scholar 

  128. 128.

    JENKINS A.D., LECHENE C.P., HOWARDS S.S.: The effect of spironolactone on the elemental composition of the intraluminal fluids of the seminiferous tubules, rete testis and epididymis of the rat. J. Urol., 1983, 129: 851–854.

    PubMed  CAS  Google Scholar 

  129. 129.

    JOHNSON G.L., LAPADAT R.: Mitogen-activated protein kinase pathways mediated by ERK, JNK, and p38 protein kinases. Science, 2002, 298: 1911–1912.

    PubMed  CAS  Article  Google Scholar 

  130. 130.

    JOHNSON J.A., GRANDE J.P., ROCHE P.C., KUMAR R.: Immunohistochemical detection and distribution of the 1,25-dihydroxyvitamin D3 receptor in rat reproductive tissues. Histochem. Cell. Biol., 1996, 105: 7–15.

    PubMed  CAS  Article  Google Scholar 

  131. 131.

    JOHNSTON D.S., JELINSKY S.A., BANG H.J. et al.: The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol. Reprod., 2005, 73: 404–413.

    PubMed  CAS  Article  Google Scholar 

  132. 132.

    JONES R., BROWN C.R., VON GLOS K.I., PARKER M.G.: Hormonal regulation of protein synthesis in the rat epididymis. Characterization of androgen-dependent and testicular fluid-dependent proteins. Biochem. J., 1980, 188: 667–676.

    PubMed  CAS  Google Scholar 

  133. 133.

    JUNGNICKEL J., CLAUS P., GRANSALKE K., TIMMER M., GROTHE C.: Targeted disruption of the FGF-2 gene affects the response to peripheral nerve injury. Mol. Cell. Neurosci., 2004, 25: 444–452.

    PubMed  CAS  Article  Google Scholar 

  134. 134.

    KECK P.J., HAUSER S.D., KRIVI G. et al.: Vascular permeability factor, an endothelial cell mitogen related to PDGF. Science, 1989, 246: 1309–1312.

    PubMed  CAS  Article  Google Scholar 

  135. 135.

    KHACHIGIAN L.M., TAKUWA Y., COLLINS T.: Mechanisms of angiotensin II-induced platelet-derived growth factor gene expression. Mol. Cell. Biochem., 2000, 212: 183–186.

    PubMed  CAS  Article  Google Scholar 

  136. 136.

    KHOLKUTE S.K., RODRIQUEZ J., DUKELOW W.R.: In vitro fertilization and the effect of progesterone and 17 alpha-hydroxyprogesterone on acrosome reaction of mouse epididymal spermatozoa. Int. J. Androl., 1995, 18: 146–150.

    PubMed  CAS  Article  Google Scholar 

  137. 137.

    KINUTA K., TANAKA H., MORIWAKE T., AYA K., KATO S., SEINO Y.: Vitamin D is an important factor in estrogen biosynthesis of both female and male gonads. Endocrinology, 2000, 141: 1317–1324.

    PubMed  CAS  Article  Google Scholar 

  138. 138.

    KIRBY J.L., YANG L., LABUS J.C., HINTON B.T.: Characterization of fibroblast growth factor receptors expressed in principal cells in the initial segment of the rat epididymis. Biol. Reprod., 2003, 68: 2314–2321.

    PubMed  CAS  Article  Google Scholar 

  139. 139.

    KIRCHHOFF C.: Gene expression in the epididymis. Int. Rev. Cytol., 1999, 188: 133–202.

    PubMed  CAS  Article  Google Scholar 

  140. 140.

    KIRCHHOFF C., KRULL N., PERA I., IVELL R.: A major mRNA of the human epididymal principal cells, HE5, encodes the leucocyte differentiation CDw52 antigen peptide backbone. Mol. Reprod. Dev., 1993, 34: 8–15.

    PubMed  CAS  Article  Google Scholar 

  141. 141.

    KOBAYASHI T., YANASE H., IWANAGA T., SASAKI R., NAGAO M.: Epididymis is a novel site of erythropoietin production in mouse reproductive organs. Biochem. Biophys. Res. Commun., 2002, 296: 145–151.

    PubMed  CAS  Article  Google Scholar 

  142. 142.

    KORPELAINEN E.I., KARKKAINEN M.J., TENHUNEN A. et al.: Overexpression of VEGF in testis and epididymis causes infertility in transgenic mice: evidence for nonendothelial targets for VEGF. J. Cell. Biol., 1998, 143: 1705–1712.

    PubMed  CAS  Article  Google Scholar 

  143. 143.

    KRISHNAMURTHY H., BABU P.S., MORALES C.R., SAIRAM M.R.: Delay in sexual maturity of the follicle-stimulating hormone receptor knockout male mouse. Biol. Reprod., 2001, 65: 522–531.

    PubMed  CAS  Article  Google Scholar 

  144. 144.

    KRISHNAMURTHY H., KATS R., DANILOVICH N., JAVESHGHANI D., SAIRAM M.R.: Intercellular communication between Sertoli cells and Leydig cells in the absence of follicle-stimulating hormone-receptor signaling. Biol. Reprod., 2001, 65: 1201–1207.

    PubMed  CAS  Article  Google Scholar 

  145. 145.

    KUMAR P.N., ARULDHAS M.M., JUNEJA S.C.: Influence of hyperthyroidism induced at prepuberty on the epididymal lipids, number and motility of spermatozoa in rats. Reprod. Fertil. Dev., 1996, 8: 373–378.

    PubMed  CAS  Article  Google Scholar 

  146. 146.

    KUMAR T.R., VARANI S., WREFORD N.G., TELFER N.M., DE KRETSER D.M., MATZUK M.M.: Male reproductive phenotypes in double mutant mice lacking both FSHbeta and activin receptor IIA. Endocrinology, 2001, 142: 3512–3518.

    PubMed  CAS  Article  Google Scholar 

  147. 147.

    LAI K.B., FU W.O., KO W.H., CHAN H.C., WONG P.Y.: The effect of [Arg8]vasopressin on electrogenic chloride secretion in cultured rat epididymal epithelia. Am. J. Physiol., 1994, 267: C607–616.

    PubMed  CAS  Google Scholar 

  148. 148.

    LAN Z.J., LABUS J.C., HINTON B.T.: Regulation of gamma-glutamyl transpeptidase catalytic activity and protein level in the initial segment of the eat epididymis by testicular factors: role of basic fibroblast growth factor. Biol. Reprod., 1998, 58: 197–206.

    PubMed  CAS  Article  Google Scholar 

  149. 149.

    LAN Z.J., LYE R.J., HOLIC N., LABUS J.C., HINTON B.T.: Involvement of polyomavirus enhancer activator 3 in the regulation of expression of gamma-glutamyl transpeptidase messenger ribonucleic acid-IV in the rat epididymis. Biol. Reprod., 1999, 60: 664–673.

    PubMed  CAS  Article  Google Scholar 

  150. 150.

    LAN Z.J., PALLADINO M.A., RUDOLPH D.B., LABUS J.C., HINTON B.T.: Identification, expression, and regulation of the transcriptional factor polyomavirus enhancer activator 3, and its putative role in regulating the expression of gamma-glutamyl transpeptidase mRNA-IV in the rat epididymis. Biol. Reprod., 1997, 57: 186–193.

    PubMed  CAS  Article  Google Scholar 

  151. 151.

    LAREYRE J.J., CLAESSENS F., ROMBAUTS W., DUFAURE J.P., DREVET J.R.: Characterization of an androgen response element within the promoter of the epididymis-specific murine glutathione peroxidase 5 gene. Mol. Cell. Endocrinol., 1997, 129: 33–46.

    PubMed  CAS  Article  Google Scholar 

  152. 152.

    LAREYRE J.J., REID K., NELSON C. et al.: Characterization of an androgen-specific response region within the 5′ flanking region of the murine epididymal retinoic acid binding protein gene. Biol. Reprod., 2000, 63: 1881–1892.

    PubMed  CAS  Article  Google Scholar 

  153. 153.

    LAREYRE J.J., WINFREY V.P., KASPER S. et al.: Gene duplication gives rise to a new 17-kilodalton lipocalin that shows epididymal region-specific expression and testicular factor(s) regulation. Endocrinology, 2001, 142: 1296–1308.

    PubMed  CAS  Article  Google Scholar 

  154. 154.

    LEHEUP B.P., GRIGNON G.: Immunohistochemical localization of insulin-like growth factor I (IGF-I) in the rat epididymis. J. Androl., 1993, 14: 159–163.

    PubMed  CAS  Google Scholar 

  155. 155.

    LEI Z.M., MISHRA S., ZOU W., XU B., FOLTZ M., LI X., RAO C.V.: Targeted disruption of luteinizing hormone/human chorionic gonadotropin receptor gene. Mol. Endocrinol., 2001, 15: 184–200.

    PubMed  CAS  Article  Google Scholar 

  156. 156.

    LEUNG A.Y., LEUNG P.Y., CHENG-CHEW S.B., WONG P.Y.: The role of calcitonin gene-related peptide in the regulation of anion secretion by the rat and human epididymis. J. Endocrinol., 1992, 133: 259–268.

    PubMed  CAS  Article  Google Scholar 

  157. 157.

    LEUNG A.Y., WONG P.Y., YANKASKAS J.R., BOUCHER R.C.: cAMP-but not Ca(2+)-regulated Cl-conductance is lacking in cystic fibrosis mice epididymides and seminal vesicles. Am. J. Physiol., 1996, 271: C188–193.

    PubMed  CAS  Google Scholar 

  158. 158.

    LEUNG A.Y.H., WONG, P.Y.D.: The epididymis as a chloride secreting organ. News Physiol. Sci., 1994, 9: 31–35.

    Google Scholar 

  159. 159.

    LEUNG D.W., CACHIANES G., KUANG W.J., GOEDDEL D.V., FERRARA N.: Vascular endothelial growth factor is a secreted angiogenic mitogen. Science, 1989, 246: 1306–1309.

    PubMed  CAS  Article  Google Scholar 

  160. 160.

    LEUNG G.P., CHEUNG K.H., LEUNG C.T., TSANG M.W., WONG P.Y.: 2004 Regulation of epididymal principal cell functions by basal cells: role of transient receptor potential (Trp) proteins and cyclooxygenase-1 (COX-1). Mol. Cell. Endocrinol., 216: 5–13.

    PubMed  CAS  Article  Google Scholar 

  161. 161.

    LEUNG G.P., DUN S.L., DUN N.J., WONG P.Y.: Serotonin via 5-HT1B and 5-HT2B receptors stimulates anion secretion in the rat epididymal epithelium. J. Physiol., 1999, 519 Pt 3: 657–667.

    PubMed  CAS  Article  Google Scholar 

  162. 162.

    LEUNG P.S., CHAN H.C., FU L.X., LEUNG P.Y., CHEW S.B., WON P.Y.: Angiotensin II receptors: localization of type I and type II in rat epididymides of different developmental stages. J. Membr. Biol., 1997, 157: 97–103.

    PubMed  CAS  Article  Google Scholar 

  163. 163.

    LEUNG P.S., CHAN H.C., FU L.X., ZHOU W.L., WONG P.Y.: Angiotensin II receptors, AT1 and AT2 in the rat epididymis. Immunocytochemical and electrophysiological studies. Biochim. Biophys. Acta, 1997, 1357: 65–72.

    PubMed  CAS  Article  Google Scholar 

  164. 164.

    LEUNG P.S., WONG T.P., LAM S.Y., CHAN H.C., WONG P.Y.: Testicular hormonal regulation of the renin-angiotensin system in the rat epididymis. Life Sci., 2000, 66: 1317–1324.

    PubMed  CAS  Article  Google Scholar 

  165. 165.

    LEUNG P.S., WONG T.P., SERNIA C.: Angiotensinogen expression by rat epididymis: evidence for an intrinsic, angiotensin-generating system. Mol. Cell. Endocrinol., 1999, 155: 115–122.

    PubMed  CAS  Article  Google Scholar 

  166. 166.

    LEUNG P.S., YAO X.Q., CHAN H.C., FU L.X., WONG P.Y.: Differential gene expression of angiotensin II receptor subtypes in the epididymides of mature and immature rats. Life Sci., 1998, 62: 461–468

    PubMed  CAS  Article  Google Scholar 

  167. 167.

    LEVEEN P., PEKNY M., GEBRE-MEDHIN S., SWOLIN B., LARSSON E., BETSHOLTZ C.: Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes. Dev., 1994, 8: 1875–1887.

    PubMed  CAS  Article  Google Scholar 

  168. 168.

    LI L., WONG J.T., PANG S.F., SHIU S.Y.: Melatonin-induced stimulation of rat corpus epididymal epithelial cell proliferation. Life Sci., 1999, 65: 1067–1076.

    PubMed  CAS  Article  Google Scholar 

  169. 169.

    LI L., XU J.N., WONG Y.H., WONG J.T., PANG S.F., SHIU S.Y.: Molecular and cellular analyses of melatonin receptor-mediated cAMP signaling in rat corpus epididymis. J. Pineal. Res., 1998, 25: 219–228.

    PubMed  CAS  Article  Google Scholar 

  170. 170.

    LLANOS M.N., ANABALON M.C.: Studies related to progesterone-induced hamster sperm acrosome reaction. Mol. Reprod. Dev., 1996, 45: 313–319.

    PubMed  CAS  Article  Google Scholar 

  171. 171.

    LOVELAND K.L., MCFARLANE J.R., DE KRETSER D.M.: Expression of activin beta C subunit mRNA in reproductive tissues. J. Mol. Endocrinol., 1996, 17: 61–65.

    PubMed  CAS  Article  Google Scholar 

  172. 172.

    MANGELSDORF D.J., UMESONO K., EVANS R.M.: The retinoid receptors. In: Sporn M.B., Roberts A.B., Goodman D.S. eds. The Retinoids, 2nd ed. New-York, Raven Press, 1994: 319–349.

    Google Scholar 

  173. 173.

    MARAN R.R., PRIYADARSINI D., UDHAYAKUMAR R.C., ARUNAKARAN J., ARULDHAS M.M.: Differential effect of hyperthyroidism on rat epididymal glycosidases. Int. J. Androl., 2001, 24: 206–215.

    PubMed  CAS  Article  Google Scholar 

  174. 174.

    MASON K.E.: Relation of the vitamins to the sex glands. In: Allen E., Danforth C.H., Doisy E.A. eds. Sex and internal Secretions. Baltimore, Williams & Wilkins, 1939, 2nd ed.: 153–239.

    Google Scholar 

  175. 175.

    MASON A.J., HAYFLICK J.S., LING N. et al.: Complementary DNA sequences of ovariant follicular fluid inhibin show precursor structure and homology with transforming growth factor-beta. Nature, 1985, 318: 659–663.

    PubMed  CAS  Article  Google Scholar 

  176. 176.

    MATZUK M.M., KUMAR T.R., BRADLEY A.: Different phenotypes for mice deficient in either activins or activin receptor type II. Nature, 1995, 374: 356–360.

    PubMed  CAS  Article  Google Scholar 

  177. 177.

    MCALLISTER B.S., LEEB-LUNDBERG L.M., JAVORS M.A., OLSON M.S.: Bradykinin receptors and signal transduction pathways in human fibroblasts: integral role for extracellular calcium. Arch. Biochem. Biophys., 1993, 304: 294–301.

    PubMed  CAS  Article  Google Scholar 

  178. 178.

    MEIZEL S.: Amino acid neurotransmitter receptor/chloride channels of mammalian sperm and the acrosome reaction. Biol. Reprod., 1997, 56: 569–574.

    PubMed  CAS  Article  Google Scholar 

  179. 179.

    MELIN P.: Effects in vivo of neurohypophysial hormones on the contractile activity of accessory sex organs in male rabbits. J. Reprod. Fertil., 1970, 22: 283–292.

    PubMed  CAS  Google Scholar 

  180. 180.

    MERCIER-BODARD C., ALFSEN A., BAULIEU E.E.: Sex steroid binding plasma protein (SBP). Acta Endocrinol. Suppl. (Copenh), 1970, 147: 204–224.

    CAS  Google Scholar 

  181. 181.

    MINGHETTI P.P., NORMAN A.W.: 1,25(OH)2-vitamin D3 receptors: gene regulation and genetic circuitry. Faseb J., 1988, 2: 3043–3053.

    PubMed  CAS  Google Scholar 

  182. 182.

    MISAO R., NIWA K., MORISHITA S., FUJIMOTO J., NAKANISHI Y., TAMAYA T.: Immunohistochemical detection of estrogen and progesterone receptors in spermatozoa of infertile men. Int. J. Fertil. Womens Med., 1997, 42: 421–425.

    PubMed  CAS  Google Scholar 

  183. 183.

    MONCADA S., PALMER R.M., HIGGS E.A.: Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev., 1991, 43: 109–142.

    PubMed  CAS  Google Scholar 

  184. 184.

    MOORE H.D., BEDFORD J.M.: The differential absorptive activity of epithelial cells of the rat epididymus before and after castration. Anat. Rec., 1979, 193: 313–327.

    PubMed  CAS  Article  Google Scholar 

  185. 185.

    MOORE X.L., HOONG I., COLE T.J.: Expression of the 11beta-hydroxysteroid dehydrogenase 2 gene in the mouse. Kidney Int., 2000, 57: 1307–1312.

    PubMed  CAS  Article  Google Scholar 

  186. 186.

    NAG S., SANYAL S., GHOSH K.K., BISWAS N.M.: Prolactin suppression and spermatogenic developments in maturing rats. A quantitative study. Horm. Res., 1981, 15: 72–77.

    PubMed  CAS  Article  Google Scholar 

  187. 187.

    NAIR N., BEDWAL R.S., MATHUR R.S.: Effect of adrenalectomy on rat epididymidis. Asian J. Androl., 2002, 4: 273–279.

    PubMed  CAS  Google Scholar 

  188. 188.

    NAPOLI J.: The biogenesis of retinoic acid: a physiologically significant promoter of differentiation. In: Dawson M.I., Okamura W.H. eds. Chemistry and biology of synthetic retinoids. Boca Raton, FL, CRC Press, 1990: 229–249.

    Google Scholar 

  189. 189.

    NAZ R.K., JOSEPH A., LEE Y., AHMAD K., BHARGAVA M.M.: Expression of scatter factor/hepatocyte growth factor is regionally correlated with the initiation of sperm motility in murine male genital tract: is scatter factor/hepatocyte growth factor involved in initiation of sperm motility? Mol. Reprod. Dev., 1994, 38: 431–439.

    PubMed  CAS  Article  Google Scholar 

  190. 190.

    NICANDER L., OOSMAN D.I., PLOEN L., BUGGE H.P., KVISGAARD K.N.: Early effects of efferent ductule ligation on the proximal segment of the rat epididymis. Int. J. Androl., 1983, 6: 91–102.

    PubMed  CAS  Article  Google Scholar 

  191. 191.

    NICHOLSON H.D., GULDENAAR S.E., BOER G.J., PICKERING B.T.: Testicular oxytocin: effects of intratesticular oxytocin in the rat. J. Endocrinol., 1991, 130: 231–238.

    PubMed  CAS  Article  Google Scholar 

  192. 192.

    NICHOLSON H.D., JENKIN L.: 5 alpha-réductase activity is increased by oxytocin in the rat testis. In: Barke A. ed. Function of Somatic cells in the Testis. New York, Springer Verlag, 1994: 278–285.

    Google Scholar 

  193. 193.

    NIEMI M., KORMANO M.: Contractility of the Seminiferous Tubule of the Postnatal Rat Testis and Its Response to Oxytocin. Ann. Med. Exp. Biol. Fenn., 1965, 43: 40–42.

    PubMed  CAS  Google Scholar 

  194. 194.

    NOBUNAGA T., TOKUGAWA Y., HASHIMOTO K. et al.: Elevated nitric oxide concentration in the seminal plasma of infertile males: nitric oxide inhibits sperm motility. Am. J. Reprod. Immunol., 1996, 36: 193–197.

    PubMed  CAS  Google Scholar 

  195. 195.

    NORMAN A.W., ROTH J., ORCI L.: The vitamin D endocrine system: steroid metabolism, hormone receptors, and biological response (calcium binding proteins). Endocr. Rev., 1982, 3: 331–366.

    PubMed  CAS  Article  Google Scholar 

  196. 196.

    NOY N., BLANER W.S.: Interactions of retinol with binding proteins: studies with rat cellular retinol-binding protein and with rat retinol-binding protein. Biochemistry, 1991, 30: 6380–6386.

    PubMed  CAS  Article  Google Scholar 

  197. 197.

    ODA S., NISHIMATSU S., MURAKAMI K., UENO N.: Molecular cloning and functional analysis of a new activin beta subunit: a dorsal mesoderm-inducing activity in Xenopus. Biochem. Biophys. Res. Commun., 1995, 210: 581–588.

    PubMed  CAS  Article  Google Scholar 

  198. 198.

    O’HAGAN R.C., TOZER R.G., SYMONS M., MCCORMICK F., HASSELL J.A.: The activity of the Ets transcription factor PEA3 is regulated by two distinct MAPK cascades. Oncogene, 1996, 13: 1323–1333.

    PubMed  CAS  Google Scholar 

  199. 199.

    OKAMURA N., TAJIMA Y., SOEJIMA A., MASUDA H., SUGITA Y.: Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylate cyclase. J. Biol. Chem., 1985, 260: 9699–9705.

    PubMed  CAS  Google Scholar 

  200. 200.

    OKAMURA N., TAMBA M., UCHIYAMA Y. et al.: Direct evidence for the elevated synthesis and secretion of procathepsin L in the distal caput epididymis of boar. Biochim. Biophys. Acta, 1995, 1245: 221–226.

    PubMed  Google Scholar 

  201. 201.

    OLIVEIRA C.A., CARNES K., FRANCA L.R., HERMO L., HESS R.A.: Aquaporin-1 and-9 are differentially regulated by oestrogen in the efferent ductule epithelium and initial segment of the epididymis. Biol. Cell., 2005, 97: 385–395.

    PubMed  CAS  Article  Google Scholar 

  202. 202.

    OLIVEIRA C.A., ZHOU Q., CARNES K. et al.: ER function in the adult male rat: short- and long-term effects of the antiestrogen ICI 182,780 on the testis and efferent ductules, without changes in testosterone. Endocrinology, 2002, 143: 2399–2409.

    PubMed  CAS  Article  Google Scholar 

  203. 203.

    ONG D.E., NEWCOMER M.E., CHYTIL F.: Cellular retinoid-binding proteins. In: Sporn M.B., Roberts B.A., Goodman D.S. eds. The Retinoids: Biology, Chemistry, and Medicine. New-York, Raven Press, 1994, 2nd ed.: 283–317.

    Google Scholar 

  204. 204.

    ORGEBIN-CRIST M.C.: Androgens and epididymal function. In: Blasin D., Gabelnick H.L., Spieler J.M., Swerdloff R.S., Wang C. eds. Pharmacology, Biology and Clinical Applications of Androgens. New York, Wiley-Liss, 1996: 27–38.

    Google Scholar 

  205. 205.

    ORGEBIN-CRIST M.C.: Sperm maturation in rabbit epididymis. Nature, 1967, 216: 816–818.

    PubMed  CAS  Article  Google Scholar 

  206. 206.

    ORGEBIN-CRIST M.C., DAVIES J.: Functional and morphological effects of hypophysectomy and androgen replacement in the rabbit epididymis. Cell Tissue Res., 1974, 148: 183–201.

    PubMed  CAS  Article  Google Scholar 

  207. 207.

    ORGEBIN-CRIST M.C., DJIANE J.: Properties of a prolactin receptor from the rabbit epididymis. Biol. Reprod., 1979, 21: 135–139.

    PubMed  CAS  Article  Google Scholar 

  208. 208.

    ORTH J.M.: The role of follicle-stimulating hormone in controlling Sertoli cell proliferation in testes of fetal rats. Endocrinology, 1984, 115: 1248–1255.

    PubMed  CAS  Google Scholar 

  209. 209.

    PAKARAINEN T., ZHANG F.P., MAKELA S., POUTANEN M., HUHTANIEMI I.: Testosterone replacement therapy induces spermatogenesis and partially restores fertility in luteinizing hormone receptor knockout mice. Endocrinology, 2005, 146: 596–606.

    PubMed  CAS  Article  Google Scholar 

  210. 210.

    PALLADINO M.A., HINTON B.T.: Expression of multiple gamma-glutamyl transpeptidase messenger ribonucleic acid transcripts in the adult rat epididymis is differentially regulated by androgens and testicular factors in a region-specific manne. Endocrinology, 1994, 135: 1146–1156.

    PubMed  CAS  Article  Google Scholar 

  211. 211.

    PALLADINO M.A., LAPERCHE Y., HINTON B.T.: Multiple forms of gamma-glutamyl transpeptidase messenger ribonucleic acid are expressed in the adult rat testis and epididymis. Biol. Reprod., 1994, 50: 320–328.

    PubMed  CAS  Article  Google Scholar 

  212. 212.

    PALLADINO M.A., POWELL J.D., KORAH N., HERMO L.: Expression and localization of hypoxia-inducible factor-1 subunits in the adult rat epididymis. Biol. Reprod., 2004, 70: 1121–1130.

    PubMed  CAS  Article  Google Scholar 

  213. 213.

    PALMER R.M., ASHTON D.S., MONCADA S.: Vascular endothelial cells synthesize nitric oxide from L-arginine. Nature, 1988, 333: 664–666.

    PubMed  CAS  Article  Google Scholar 

  214. 214.

    PANESAR N.S., HUANG N.J.: Effect of hCG on intracellular chloride concentration in rat epididymal cells. Clin. Biochem. Rev., 1993, 14: abstract PS255.

  215. 215.

    PASTOR-SOLER N., ISNARD-BAGNIS C., HERAK-KRAMBERGER C. et al. Expression of aquaporin 9 in the adult rat epididymal epithelium is modulated by androgens. Biol. Reprod., 2002, 66: 1716–1722.

    PubMed  CAS  Article  Google Scholar 

  216. 216.

    PATRIZIO P., SALAMEH W.A.: Expression of the cystic fibrosis transmembrane conductance regulator (CFTR) mRNA in normal and pathological adult human epididymis. J. Reprod. Fertil., 1998, Suppl 53: 261–270.

    CAS  Google Scholar 

  217. 217.

    PEARCE P.T., LIPKEVICIUS O.R., FUNDER J.W.: High affinity (type 1) aldosterone-binding sites in rat epididymis. Endocrinology, 1986, 118: 2072–2075.

    PubMed  CAS  Google Scholar 

  218. 218.

    PEREYRA-MARTINEZ A.C., ROSELLI C.E., STADELMAN H.L., RESKO J.A.: Cytochrome P450 aromatase in testis and epididymis of male rhesus monkeys. Endocrine, 2001, 16: 15–19.

    PubMed  CAS  Article  Google Scholar 

  219. 219.

    PERI A., FANTONI G., GRANCHI S. et al.: Gene expression of endothelin-1, endothelin-converting enzyme-1, and endothelin receptors in human epididymis. J. Clin. Endocrinol. Metab., 1997, 82: 3797–3806.

    PubMed  CAS  Article  Google Scholar 

  220. 220.

    PERI A., FANTONI G., GRANCHI S. et al.: Endothelin-1 is synthesized and biologically active in human epididymis via a paracrine mode of actior. Steroids, 1998, 63: 294–298.

    PubMed  CAS  Article  Google Scholar 

  221. 221.

    PERRY A.C., JONES R., HALL L.: Isolation and characterization of a rat cDNA clone encoding a secreted superoxide dismutase reveals the epididymis to be a major site of its expression. Biochem. J., 1993, 293: 21–25.

    PubMed  CAS  Google Scholar 

  222. 222.

    PETKOVICH M., BRAND N.J., KRUST A., CHAMBON P.: A human retinoic acid receptor which belongs to the family of nuclear receptors. Nature, 1987, 330: 444–450.

    PubMed  CAS  Article  Google Scholar 

  223. 223.

    PIETROBON E.O., MONCLUS MDE L., ALBERDI A.J., FORNES M.W.: Progesterone receptor availability in mouse spermatozoa during epididymal transit and capacitation: ligand blot detection of progesterone-binding protein. J. Androl., 2003, 24: 612–620.

    PubMed  CAS  Google Scholar 

  224. 224.

    Porter S.B., Fraker L.D., Chytil F., Ong, D.E.: Localization of cellular retinol-binding protein in several rat tissues. Proc. Natl Acad. Sci. USA, 1983, 80: 6586–6590.

    PubMed  CAS  Article  Google Scholar 

  225. 225.

    PORTER S.B., ONG D.E., CHYTIL F., ORGEBIN-CRIST M.C.: Localization of cellular retinol-binding protein and cellular retinoic acidbinding protein in the rat testis and epididymis. J. Androl., 1985, 6: 197–212.

    PubMed  CAS  Google Scholar 

  226. 226.

    PURVIS K., CLAUSEN O.P., OLSEN A., HAUG E., HANSSON V.: Prolactin and Leydig cell responsiveness to LH/hCG in the rat. Arch. Androl., 1979, 3: 219–230.

    PubMed  CAS  Article  Google Scholar 

  227. 227.

    PUUSTINEN R., SARVILINNA N., MANNINEN T., TUOHIMAA P., YLIKOMI T.: Localization of glucocorticoid receptor interacting protein 1 in murine tissues using two novel polyclonal antibodies. Eur. J. Endocrinol., 2001, 145: 323–333.

    PubMed  CAS  Article  Google Scholar 

  228. 228.

    RADHAKRISHNAN B., SUAREZ-QUIAN C.A.: Characterization of epidermal growth factor receptor in testis, epididymis and vas deferens of non-human primates. J. Reprod. Fertil., 1992, 96: 13–23.

    PubMed  CAS  Google Scholar 

  229. 229.

    RAIBLE F., BRAND M.: Tight transcriptional control of the ETS domain factors Erm and Pea3 by Fgf signaling during early zebrafish development. Mech. Dev., 2001, 107: 105–117.

    PubMed  CAS  Article  Google Scholar 

  230. 230.

    RIGAUDIERE N., GHYSELINCK N.B., FAURE J., DUFAURE J.P.: Regulation of the epididymal glutathione peroxidase-like protein in the mouse: dependence upon androgens and testicular factors. Mol. Cell. Endocrinol., 1992, 89: 67–77.

    PubMed  CAS  Article  Google Scholar 

  231. 231.

    ROBAIRE B., EWING L.L., ZIRKIN B.R., IRBY D.C.: Steroid delta4-5alpha-reductase and 3alpha-hydroxysteroid dehydrogenase in the rat epididymis. Endocrinology, 1977, 101: 1379–1390.

    PubMed  CAS  Google Scholar 

  232. 232.

    ROBAIRE B., HERMO L.: Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. In: Knobil E., Neill J. eds. The Physiology of Reproduction. New-York, Raven Press, 1988: 999–1080.

    Google Scholar 

  233. 233.

    ROBAIRE B., JERVIS K.M., EZER N.: Cell dynamics and cell death in the epididymal epithelium. In: Hinton B. T., Turner T.T. eds. Third International Conference on the Epididymis. Charlottesville. The Van Doren Company, 2003: 35–49.

    Google Scholar 

  234. 234.

    ROBAIRE B., SYNTIN P., JERVIS K.: The coming of the epididymis. In: Jégou B., Pineau C., Saez J. eds. Testis, Epididymis and Technologies in the year 2000. New-York, Springer-Verlag, 2000: 229–262.

    Google Scholar 

  235. 235.

    ROBERTS K.P., HOFFMAN L.B., ENSRUD K.M., HAMILTON D.W. Expression of crisp-1 mRNA splice variants in the rat epididymis, and comparative analysis of the rat and mouse crisp-1 gene regulatory regions. J. Androl., 2001, 22: 157–163.

    PubMed  CAS  Google Scholar 

  236. 236.

    ROBERTS, V.J.: Tissue-specific expression of inhibin/activin subunit and follistatin mRNAs in mid-to late-gestational age human fetal testis and epididymis. Endocrine, 1997, 6: 85–90.

    PubMed  CAS  Article  Google Scholar 

  237. 237.

    ROBINSON A.G.: The neurohypophysis: recent developments. J. Lab. Clin. Med., 1987, 109: 336–345.

    PubMed  CAS  Google Scholar 

  238. 238.

    ROEHL H., NUSSLEIN-VOLHARD C.: Zebrafish pea3 and erm are general targets of FGF8 signaling. Curr. Biol., 2001, 11: 503–507.

    PubMed  CAS  Article  Google Scholar 

  239. 239.

    ROLDAN E.R., MURASE T., SHI Q.X.: Exocytosis in spermatozoa in response to progesterone and zona pellucida. Science, 1994, 266: 1578–1581.

    PubMed  CAS  Article  Google Scholar 

  240. 240.

    RUBIN R.T., POLAND R.E., TOWER B.B.: Prolactin-related testosterone secretion in normal adult men. J. Clin. Endocrinol. Metab., 1976, 42: 112–116.

    PubMed  CAS  Article  Google Scholar 

  241. 241.

    SCHAEFFER H.J., WEBER M.J.: Mitogen-activated protein kinases: specific messages from ubiquitous messengers. Mol. Cell. Biol., 1999, 19: 2435–2444.

    PubMed  CAS  Google Scholar 

  242. 242.

    SCHLEICHER G., PRIVETTE T.H., STUMPF W.E.: Distribution of soltriol [1,25(OH)2-vitamin D3] binding sites in male sex organs of the mouse: an autoradiographic study. J. Histochem. Cytochem., 1989, 37: 1083–1086.

    PubMed  CAS  Google Scholar 

  243. 243.

    SCHLESSINGER J.: Cell signaling by receptor tyrosine kinases. Cell, 2000, 103: 211–225.

    PubMed  CAS  Article  Google Scholar 

  244. 244.

    SCHUBERT D., KIMURA H., LACORBIERE M., VAUGHAN J., KARR D., FISCHER W.H.: Activin is a nerve cell survival molecule. Nature, 1990, 344: 868–870.

    PubMed  CAS  Article  Google Scholar 

  245. 245.

    SCHULTZ R., ISOLA J., PARVINEN M. et al.: Localization of the glucocorticoid receptor in testis and accessory sexual organs of male rat. Mol. Cell. Endocrinol., 1993, 95: 115–120.

    PubMed  CAS  Article  Google Scholar 

  246. 246.

    SCHWAAB V., LAREYRE J.J., VERNET P., PONS E., FAURE J., DUFAURE J.P., DREVET J.R.: Characterization, regulation of the expression and putative roles of two glutathione peroxidase proteins found in the mouse epididymis. J. Reprod. Fertil., Suppl., 1998, 53: 157–162.

    CAS  Google Scholar 

  247. 247.

    SCHWIDETZKY U., SCHLEUNING W.D., HAENDLER B.: Isolation and characterization of the androgen-dependent mouse cysteine-rich secretory protein-1 (CRISP-1) gene. Biochem. J., 1997, 321: 325–332.

    PubMed  Google Scholar 

  248. 248.

    SETCHELL B.P., SCOTT T.W., VOGLMAYR J.K., WAITES G.M.: Characteristics of testicular spermatozoa and the fluid which transports them into the epididymis. Biol. Reprod., 1969, 1: Suppl 1: 40–66.

    PubMed  Article  Google Scholar 

  249. 249.

    SHAYU D., RAO A.J.: Expression of functional aromatase in the epididymis: Role of androgens and LH in modulation of expression and activity. Mol. Cell. Endocrinol., 2006, 249: 40–50.

    PubMed  CAS  Google Scholar 

  250. 250.

    SHI Y., MASSAGUE J.: Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell, 2003, 113: 685–700.

    PubMed  CAS  Article  Google Scholar 

  251. 251.

    SHINGLETON J.L., SKINNER M.K., ONG D.E.: Characteristics of retinol accumulation from serum retinol-binding protein by cultured Sertoli cells. Biochemistry, 1989, 28: 9641–9647.

    PubMed  CAS  Article  Google Scholar 

  252. 252.

    SHIU S.Y., CHOW P.H., YU Z.H., TANG F., PANG S.F.: Autoradiographic distribution and physiological regulation of 2-[125]iodomelatonin binding in rat epididymis. Life Sci., 1996, 59: 1165–1174.

    PubMed  CAS  Article  Google Scholar 

  253. 253.

    SHIU S.Y., LI L., SIU S.W., XI S.C., FONG S.W., PANG S.F.: Biological basis and possible physiological implications of melatonin receptor-mediated signaling in the rat epididymis. Biol. Signals Recept., 2000, 9: 172–187.

    PubMed  CAS  Article  Google Scholar 

  254. 254.

    SIMONI M., GROMOLL J., NIESCHLAG E.: The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev., 1997, 18: 739–773.

    PubMed  CAS  Article  Google Scholar 

  255. 255.

    SMITHWICK E.B., YONG L.G.: Histological effects of androgen deprivation on the adult chimpanzee epididymis. Tissue Cell, 2001, 33: 450–461.

    PubMed  CAS  Article  Google Scholar 

  256. 256.

    SONNENBERG E., GODECKE A., WALTER B., BLADT F., BIRCHMEIER C.: Transient and locally restricted expression of the ros1 protooncogene during mouse development. Embo. J., 1991, 10: 3693–3702.

    PubMed  CAS  Google Scholar 

  257. 257.

    SONNENBERG-RIETHMACHER E., WALTER B., RIETHMACHER D., GODECKE S., BIRCHMEIER C.: The c-ros tyrosine kinase receptor controls regionalization and differentiation of epithelial cells in the epididymis. Genes. Dev., 1996, 10: 1184–1193.

    PubMed  CAS  Article  Google Scholar 

  258. 258.

    SOPRANO D.R., BLANER W.S.: Plasma retinol-binding protein. In: Sporn M.B., Roberts A.B., Goodman D.S. eds. The Retinoids: Biology, Chemistry, and Medicine. 2nd ed. New-York, Raven Press, 1994: 257–281.

    Google Scholar 

  259. 259.

    SORIANO P.: Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice. Genes. Dev., 1994, 8: 1888–1896.

    PubMed  CAS  Article  Google Scholar 

  260. 260.

    SRIRAMAN V., SAIRAM M.R., RAO A.J.: Evaluation of relative roles of LH and FSH in regulation of differentiation of Leydig cells using an ethane 1,2-dimethylsulfonate-treated adult rat model. J. Endocrinol., 2003, 176: 151–161.

    PubMed  CAS  Article  Google Scholar 

  261. 261.

    SRIVASTAVA S., DESAI P., COUTINHO E., GOVIL G.: Protective effect of L-arginine against lipid peroxidation in goat epididymal spermatozoa. Physiol. Chem. Phys. Med. NMR, 2000, 32: 127–135.

    PubMed  CAS  Google Scholar 

  262. 262.

    Srivastava S., Desai P., Coutinho E., Govil G.: Mechanism of Action of L-Arginine on the Vitality of Spermatozoa is Primarily Through Increased Biosynthesis of Nitric Oxide. Biol Reprod., 2006.

  263. 263.

    ST-PIERRE N., DUFRESNE J., ROONEY A.A., CYR D.G.: Neonatal hypothyroidism alters the localization of gap junctional protein connexin 43 in the testis and messenger RNA levels in the epididymis of the rat. Biol. Reprod., 2003, 68: 1232–1240.

    PubMed  CAS  Article  Google Scholar 

  264. 264.

    STUDDARD P.W., STEIN J.L., COSENTINO M.J.: The effects of oxytocin and arginine vasopressin in vitro on epididymal contractility in the rat. Int. J. Androl., 2002, 25: 65–71.

    PubMed  CAS  Article  Google Scholar 

  265. 265.

    SUAREZ-QUIAN C.A., DAI M.Z., ONODA M., KRISS R.M., DYM M.: Epidermal growth factor receptor localization in the rat and monkey testes. Biol. Reprod., 1989, 41: 921–932.

    PubMed  CAS  Article  Google Scholar 

  266. 266.

    SUAREZ-QUIAN C.A., NIKLINSKI W.: Immunocytochemical localization of the epidermal growth factor receptor in mouse testis. Biol. Reprod., 1990, 43: 1087–1097.

    PubMed  CAS  Article  Google Scholar 

  267. 267.

    SUAREZ-QUIAN C.A., OKE B.O., RADHAKRISHNAN B.: Relationship between submandibular gland epidermal growth factor, and spermatogenesis in C3H mice. Tissue Cell, 1994, 26: 285–298.

    PubMed  CAS  Article  Google Scholar 

  268. 268.

    SUELDO C.E., OEHNINGER S., SUBIAS E. et al.: Effect of progesterone on human zona pellucida sperm binding and oocyte penetrating capacity. Fertil. Steril., 1993, 60: 137–140.

    PubMed  CAS  Google Scholar 

  269. 269.

    SUJARIT S., PHOLPRAMOOL C.: Enhancement of sperm transport through the rat epididymis after castration. J. Reprod. Fertil., 1985, 74: 497–502.

    PubMed  CAS  Article  Google Scholar 

  270. 270.

    SUVANTO O., KORMANO M.: The relation between in vitro contractions of the rat seminferous tubules and the cyclic stage of the seminiferous epithelium. J. Reprod. Fertil., 1970, 21: 227–232.

    PubMed  CAS  Google Scholar 

  271. 271.

    TAO Y.X., LEI Z.M., RAO CH.V.: Human epididymis contains luteinizing hormone/chorionic gonadotropin receptors. In: Program of the 10th International Congress of Endocrinology; San Francisco, CA. 1996: Abstract OR21-2.

  272. 272.

    TAO Y.X., LEI Z.M., RAO CH.V.: Novel expression of luteinizing hormone (LH)/human chorionic gonadotropin (hCG) receptor gene in rat epididymis. Biol. Reprod., 1995, 52 (suppl 1): abstract 338 (14.1)

    Google Scholar 

  273. 273.

    TESSAROLLO L., NAGARAJAN L., PARADA L.F.: c-ros: the vertebrate homolog of the sevenless tyrosine kinase receptor is tightly regulated during organogenesis in mouse embryonic development. Development, 1992, 115: 11–20.

    PubMed  CAS  Google Scholar 

  274. 274.

    TOMSIG J.L., TURNER T.T.: Growth factors and the epididymis. J. Androl., 2006, 27: 348–357.

    PubMed  CAS  Article  Google Scholar 

  275. 275.

    TRAMER F., ROCCO F., MICALI F., SANDRI G., PANFILI E.: Antioxidant systems in rat epididymal spermatozoa. Biol. Reprod., 1998, 59: 753–758.

    PubMed  CAS  Article  Google Scholar 

  276. 276.

    TSUCHIDA K., VALE W., SUZUKI N., NISHIMURA E., SHINIHARA M., KATAOKA H. et al.: Activin signal transduction and the role of TGF-b superfamily in cell differentiation. In: Aono T., Sugino H., Vale W. eds. Inhibin, activin, and follistatin regulatory functions in system and cell biology. Norwell, MA, Serono Symposia USA, 1997: 254–263.

  277. 277.

    TUOHIMAA P., LYAKHOVICH A., AKSENOV N. et al.: Vitamin D and prostate cancer. J. Steroid. Biochem. Mol. Biol., 2001, 76: 125–134.

    PubMed  CAS  Article  Google Scholar 

  278. 278.

    TURNER T.T.: Necessity’s potion: Inorganic ions and small organic molecules in the epididymal lumen. In: Robaire B., Hinton B.T. eds. The epididymis: From molecules to clinical practice. New York, Kluwer Academic/Plenum Publishers, 2002: 131–150.

    Google Scholar 

  279. 279.

    TURNER T.T., CESARINI D.M.: The ability of the rat epididymis to concentrate spermatozoa. Responsiveness to aldosterone. J. Androl., 1983, 4: 197–202.

    PubMed  CAS  Google Scholar 

  280. 280.

    TURNER T.T., MILLER D.W.: On the synthesis and secretion of rat seminiferous tubule proteins in vivo after ischemia and germ cell loss. Biol. Reprod., 1997, 57: 1275–1284.

    PubMed  CAS  Article  Google Scholar 

  281. 281.

    TURNER T.T., RILEY T.A.: p53 independent, region-specific epithelial apoptosis is induced in the rat epididymis by deprivation of luminal factors. Mol. Reprod. Dev., 1999, 53: 188–197.

    PubMed  CAS  Article  Google Scholar 

  282. 282.

    WADDELL B.J., HISHEH S., KROZOWSKI Z.S., BURTON P.J.: Localization of 11beta-hydroxysteroid dehydrogenase types 1 and 2 in the male reproductive tract. Endocrinology, 2003, 144: 3101–3106.

    PubMed  CAS  Article  Google Scholar 

  283. 283.

    WILKINSON M.G., MILLAR J.B.: Control of the eukaryotic cell cycle by MAP kinase signaling pathways. Faseb J., 2000, 14: 2147–2157.

    PubMed  CAS  Article  Google Scholar 

  284. 284.

    WINER M.A., WADEWITZ A.G., WOLGEMUTH D.J.: Members of the raf gene family exhibit segment-specific patterns of expression in mouse epididymis. Mol. Reprod. Dev., 1993, 35: 16–23.

    PubMed  CAS  Article  Google Scholar 

  285. 285.

    WINER M.A., WOLGEMUTH D.J.: The segment-specific pattern of A-raf expression in the mouse epididymis is regulated by testicular factors. Endocrinology, 1995, 136: 2561–2572.

    PubMed  CAS  Article  Google Scholar 

  286. 286.

    WISE H., JONES R.L.: An introduction to prostacyclin and its receptors. Prostacyclin and its Receptors. Wise H., Jones R.L. eds. New York, Kluwer Academic/Plenum, 2000: 1–27.

    Google Scholar 

  287. 287.

    WISZNIEWSKA B., KURZAWA R., CIECHANOWICZ A., MACHALINSKI B.: Inducible nitric oxide synthase in the epithelial epididymal cells of the rat. Reprod. Fertil. Dev., 1997, 9: 789–794.

    PubMed  CAS  Article  Google Scholar 

  288. 288.

    WOLBACH S.B., HOWE P.R.: Tissue changes following deprivation of fat soluble A vitamin. J. Exp. Med., 1925, 42: 753–777.

    CAS  Article  PubMed  Google Scholar 

  289. 289.

    WONG P.Y., CHAN H.C., LEUNG P.S., CHUNG Y.W., WONG Y.L., LEE W.M., NG V., DUN N.J.: Regulation of anion secretion by cyclo-oxygenase and prostanoids in cultured epididymal epithelia from the rat. J. Physiol., 1999, 514 (Pt 3): 809–820.

    PubMed  CAS  Article  Google Scholar 

  290. 290.

    WONG P.Y., FU W.O., HUANG S.J.: Endothelin stimulates short circuit current in a cultured epithelium. Br. J. Pharmacol., 1989, 98: 1191–1196.

    PubMed  CAS  Google Scholar 

  291. 291.

    WONG P.Y., FU W.O., HUANG S.J., LAW W.K.: Effect of angiotensins on electrogenic anion transport in monolayer cultures of rat epididymis. J. Endocrinol., 1990, 125: 449–456.

    PubMed  CAS  Article  Google Scholar 

  292. 292.

    WONG P.Y.D., GONG, X.D., LEUNG, G.P.H., CHEUK B.L.: Formation of the epididymal fluid environment. In: Robaire B., Hinton B. eds. The Epididymis: From Molecules to Clinical Practice. Kluwer Plenum Press, New York 2001: 119–130.

    Google Scholar 

  293. 293.

    WONG P.Y., UCHENDU C.N.: The role of angiotensin-converting enzyme in the rat epididymis. J. Endocrinol., 1990, 125: 457–465.

    PubMed  CAS  Article  Google Scholar 

  294. 294.

    WONG P.Y., UCHENDU C.N.: Studies on the renin-angiotensin system in primary monolayer cell cultures of the rat epididymis. J. Endocrinol., 1991, 131: 287–293.

    PubMed  CAS  Article  Google Scholar 

  295. 295.

    XU J., LI Q.: Review of the in vivo functions of the p160 steroid receptor coactivator family. Mol. Endocrinol., 2003, 17: 1681–1692.

    PubMed  CAS  Article  Google Scholar 

  296. 296.

    YAMAMOTO H., OCHIYA T., TAKAHAMA Y., ISHII Y. et al.: Detection of spatial localization of Hst-1/Fgf-4 gene expression in brain and testis from adult mice. Oncogene, 2000, 19: 3805–3810.

    PubMed  CAS  Article  Google Scholar 

  297. 297.

    YAMAMOTO S., MIKAMI T., KONISHI M., ITOH N.: Stage-specific expression of a novel isoform of mouse FGF-14 (FHF-4) in spermatocytes. Biochim. Biophys. Acta, 2000, 1490: 121–124.

    PubMed  CAS  Google Scholar 

  298. 298.

    YAMASHITA S.: Localization of estrogen and androgen receptors in male reproductive tissues of mice and rats. Anat. Rec. A Discov. Mol. Cell. Evol. Biol., 2004, 279: 768–778.

    PubMed  Article  CAS  Google Scholar 

  299. 299.

    YEUNG C.H., WAGENFELD A., NIESCHLAG E., COOPER T.G.: The cause of infertility of male c-ros tyrosine kinase receptor knockout mice. Biol. Reprod., 2000, 63: 612–618.

    PubMed  CAS  Article  Google Scholar 

  300. 300.

    YU X., GUPTA A., WANG Y. et al.: Foxa1 and foxa2 interact with the androgen receptor to regulate prostate and epididymal genes differentially. Ann. N. Y. Acad. Sci., 2005, 1061: 77–93.

    PubMed  CAS  Article  Google Scholar 

  301. 301.

    ZHANG F.P., PAKARAINEN T., ZHU F., POUTANEN M., HUHTANIEMI I.: Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice. Endocrinology, 2004, 145: 1453–1463.

    PubMed  CAS  Article  Google Scholar 

  302. 302.

    ZHANG F.P., POUTANEN M., WILBERTZ J., HUHTANIEMI I.: Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Mol. Endocrinol., 2001, 15: 172–183.

    PubMed  CAS  Article  Google Scholar 

  303. 303.

    ZHANG T., GUO C.X., HU Z.Y., LIU Y.X.: Localization of plasminogen activator and inhibitor, LH and androgen receptors and inhibin subunits in monkey epididymis. Mol. Hum. Reprod., 1997, 3: 945–952.

    PubMed  CAS  Article  Google Scholar 

  304. 304.

    ZHAO W., LEUNG P.Y., CHEW S.B., CHAN H.C., WONG P.Y.: Localization and distribution of angiotensin II in the rat epididymis. J. Endocrinol., 1996, 149: 217–222.

    PubMed  CAS  Article  Google Scholar 

  305. 305.

    ZHOU Q., NIE R., PRINS G.S., SAUNDERS P.T., KATZENELLENBOGEN B.S., HESS R.A.: Localization of androgen and estrogen receptors in adult male mouse reproductive tract. J. Androl., 2002, 23: 870–881.

    PubMed  CAS  Google Scholar 

  306. 306.

    ZHOU H.M., ZHANG T., LIU Y.X.: Rat epididymis expresses luteinizing hormone receptor (LHR). Chinese Sci. Bull., 1996, 41: 1608–1610.

    Google Scholar 

  307. 307.

    ZHU L.J., HARDY M.P., INIGO I.V., HUHTANIEMI I., BARDIN C.W., MOO-YOUNG A.J.: Effects of androgen on androgen receptor expression in rat testicular and epididymal cells: a quantitative immunohistochemical study. Biol. Reprod., 2000, 63: 368–376.

    PubMed  CAS  Article  Google Scholar 

  308. 308.

    ZIMMERMAN E.A., ROBINSON A.G., HUSAIN M.K., ACOSTA M., FRANTZ A.G., SAWYER W.H.: Neurohypophysial peptides in the bovine hypothalamus: the relationship of neurophysin 1 to oxytocin, and neurophysin II to vasopressin in supraoptic and paraventricular regions. Endocrinology, 1974, 95: 931–936.

    PubMed  CAS  Google Scholar 

  309. 309.

    ZINI A., DE LAMIRANDE E., GAGNON C.: Low levels of nitric oxide promote human sperm capacitation in vitro. J. Androl., 1995, 16: 424–431.

    PubMed  CAS  Google Scholar 

  310. 310.

    ZINI A., O’BRYAN M.K., MAGID M.S., SCHLEGEL P.N.: Immunohistochemical localization of endothelial nitric oxide synthase in human testis, epididymis, and vas deferens suggests a possible role for nitric oxide in spermatogenesis, sperm maturation, and programmed cell death. Biol. Reprod., 1996, 55: 935–941.

    PubMed  CAS  Article  Google Scholar 

  311. 311.

    ZIPF W.B., PAYNE A.H., KELCH R.P.: Prolactin, growth hormone, and luteinizing hormone in the maintenance of testicular luteinizing hormone receptors. Endocrinology, 1978, 103: 595–600.

    PubMed  CAS  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Aurore Britan.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Britan, A., Drevet, J.R. Régulation des fonctions de l’épithélium épididymaire des mammifères: état des lieux. Androl. 16, 197–228 (2006). https://doi.org/10.1007/BF03034859

Download citation

Mots clés

  • spermatozoïdes
  • maturation post-testiculaire
  • fertilité
  • contrôles endocrines
  • lumicrines
  • autocrines et paracrines

Key Words

  • spermatozoa
  • post-testicular maturation
  • fertility
  • endocrine
  • lumicrine
  • autocrine and paracrine regulation