The Coming of Age of the Epididymis

  • B. Robaire
  • P. Syntin
  • K. Jervis
Part of the Ernst Schering Research Foundation Workshop book series (SCHERING FOUND, volume 6)


Several descriptive anatomical and histological studies of the testicular excurrent duct system from various species appeared at the beginning of the twentieth century. In the 1920’s, Benoit published a series of articles which culminated in a comprehensive treatise (Benoit, 1926) on the anatomy, cytology, and histophysiology of the efferent ducts, epididymis, and vas deferens. In that article, we can recognize easily our current view that a series of efferent ducts merge to form a single, highly convoluted, epididymal duct that is made up of several cell types, is under the influence of testicular substances, and is the site where spermatozoa acquire their potential for motility. The prevalent hypothesis in the 1920’s, that the epididymis plays an active role in the maturation of spermatozoa, their acquisition of motility, and their storage, was challenged by Young in a series of articles published between 1929 and 1931 (Young, 1929a,b, 1931). Relatively little research was done on the excurrent duct system during the ensuing three decades.


Initial Segment Principal Cell Postnatal Development Sperm Maturation Efferent Duct 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Abou-Haila A, Fain-Maurel MA (1985) Postnatal differentiation of the enzymatic activity of the mouse epididymis. Int J Androl 8: 441–458PubMedGoogle Scholar
  2. Akmal KM, Dufour JM, Kim KH (1996) Region-specific localization of retinoic acid receptor-alpha expression in the rat epididymis. Biol Reprod 54: 1111–1119PubMedGoogle Scholar
  3. Andersson S, Bishop RW, Russell DW (1989) Expression cloning and regulation of steroid 5a-reductase, an enzyme essential for male sexual differentiation. J Biol Chem 264: 16249–16255PubMedGoogle Scholar
  4. Andonian S, Badran H, Hermo L (1999a) Immunolocalization of acquaporins (AQPs) 6 and 9 in the adult rat vas deferens ( VD ). Cell Biol meeting 1610Google Scholar
  5. Andonian S, Hermo L (1999b) Cell-and region-specific localization of lysosomal and secretory proteins and endocytic receptors in epithelial cells of the cauda epididymidis and vas deferens of the adult rat. J Androl 20: 415–429PubMedGoogle Scholar
  6. Ashok BT, Ali R (1999) The aging paradox: free radical theory of aging. Exp Gerontol 34: 293–303PubMedGoogle Scholar
  7. Ayer-LeLievre C, Olson L, Ebendal T, Hallbook F, Persson H (1988) Nerve growth factor mRNA and protein in the testis and epididymis of mouse and rat. Proc Natl Acad Sci USA 85: 2628–2632PubMedGoogle Scholar
  8. Baker CS, Magargee SF, Hammerstedt RH (1993) Cholesterol transfer proteins from ram caudal epididymal and seminal plasma. Biol Reprod Suppl 48: 86Google Scholar
  9. Barbieri MA, Veisaga ML, Paolicchi F, Fornes MW, Sosa MA, Mayorga LS, Bustos-Obregon E, Bertini F (1996) Affinity sites for beta-glucuronidase on the surface of human spermatozoa. Andrologia 28: 327–333PubMedGoogle Scholar
  10. Bedford JM (1967) Effects of duct ligation on the fertilizing ability of spermatozoa from different regions of the rabbit epididymis. J Exp Zool 166: 271–282PubMedGoogle Scholar
  11. Belmonte S, Maturano M, Bertini MF, Pusiol E, Sartor T, Sosa MA (1998) Changes in the content of rat epididymal fluid induced by prolonged treatment with tamoxifen. Andrologia 30: 345–350PubMedGoogle Scholar
  12. Benoit J (1926) Recherches anatomiques, cytologiques et histophysiologiques sur les voies excretrices du testicule chez les mammifères. Arch Anat Histol Embryol (Strasb) 5: 175–412Google Scholar
  13. Berman DM, Russell DW (1993) Cell-type-specific expression of rat steroid 5a-reductase isozymes. Proc Natl Acad Sci USA 90: 9359–9363PubMedGoogle Scholar
  14. Bérubé B, Sullivan R (1994) Inhibition of in vivo fertilization by active immunization of male hamsters against a 26-kDa sperm glycoprotein. Biol Re-prod 51: 1255–1263Google Scholar
  15. Blanchard Y, Robaire B (1997) Le mode d’action des androgènes et la 5aréductase. Médecine/Sciences 13: 467–473Google Scholar
  16. Brooks DE (1981) Secretion of proteins and glycoproteins by the rat epididymis: regional differences, androgen-dependence, and effects of protease inhibitors, procaine, and tunycamycin. Biol Reprod 25: 1099–1117PubMedGoogle Scholar
  17. Brooks DE (1983a) Influence of incubation conditions, tunicamycin and castration on incorporation of [3H]mannose and [3H]fucose into rat epididymal glycoproteins in vitro. J Reprod Fertil 67: 97–105PubMedGoogle Scholar
  18. Brooks DE (1983b) Effect of androgens on protein synthesis and secretion in various regions of the rat epididymis, as analysed by two-dimensional gel electrophoresis. Mol Cell Endocrinol 29: 255–270.PubMedGoogle Scholar
  19. Brooks DE, Means AR, Wright EJ, Singh SP, Tiver KK (1986) Molecular cloning of the cDNA for androgen-dependent sperm-coating glycoproteins secreted by the rat epididymis. Eur J Biochem 161: 13–18PubMedGoogle Scholar
  20. Byskov AG, Hßyer PE (1988) Embryology of mammalian gonads and ducts. In: Knobil E, Neill J (eds) The Physiology of Reproduction. Raven Press, New York, pp 265–302Google Scholar
  21. Cameo MS, Blaquier JA (1976) Androgen-controlled specific proteins in rat epididymis. J Endocrinol 69: 47–55PubMedGoogle Scholar
  22. Chaturapanich G, Jones RC, Culow J (1992) Protein synthesis and secretion by the epididymis of Tammar Wallaby, Macropus eugenii. Reprod Fert Dev 4: 533–545Google Scholar
  23. Chen MY, Carpenter D, Zhao GQ (1999) Expression of bone morphogenetic protein 7 in murine epididymis is developmentally regulated. Biol Reprod 60: 1503–1508PubMedGoogle Scholar
  24. Cheng CY, Mathur PP, Grima J (1988) Structural analysis of clusterin and its subunits in ram rete testis fluid. Biochemistry 27: 4079–4088PubMedGoogle Scholar
  25. Clermont Y, Flannery J (1970) Mitotic activity in the epithelium of the epididymis in young and old adult rats. Biol Reprod 3: 283–292PubMedGoogle Scholar
  26. Cohen J, Ooms MP, Vreeburg JTM (1981) Reduction of fertilizing capacity of epididymal spermatozoa by 5a-steroid reductase inhibitors. Experientia 37: 1031–1032PubMedGoogle Scholar
  27. Collins S, Quarmby V, French F, Lefkowitz RJ, Caron MG (1988) Regulation of the 132-adrenergic receptor in the rat ventral prostate by testosterone. FEBS Lett 233: 173–176PubMedGoogle Scholar
  28. Cooper TG (1990) In defense of a function for the human epididymis. Fert Steril 54: 965–975Google Scholar
  29. Cornwall GA, Hann SR (1995a) Transient appearance of CRES protein during spermatogenesis and caput epididymal sperm maturation. Mol Reprod Dev 41: 37–46PubMedGoogle Scholar
  30. Cornwall GA, Hann SR (1995b) Specialized gene expression in the epididymis. J Androl 16: 379–383PubMedGoogle Scholar
  31. Cornwall GA, Hsia N (1997) ADAM7, a member of the ADAM (a disintegrin and metalloprotease) gene family is specifically expressed in the mouse anterior pituitary and epididymis. Endocrinology 138: 4262–4272PubMedGoogle Scholar
  32. Cornwall GA, Orgebin-Crist MC, Hann SR (1992) 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 6: 1653–1664PubMedGoogle Scholar
  33. Cornwall GA, Tulsiani DR, Orgebin-Crist MC (1991) Inhibition of the mouse sperm surface alpha-D-mannosidase inhibits sperm-egg binding in vitro. Biol Reprod 44: 913–921PubMedGoogle Scholar
  34. Couse JF, Lindzey J, Grandien K, Gustafsson JA, Korach KS (1997) Tissue distribution and quantitative analysis of estrogen receptor-alpha (ERalpha) and estrogen receptor-beta ( ERbeta) messenger ribonucleic acid in the wild-type and ERalpha-knockout mouse. Endocrinology 138: 4613–1621Google Scholar
  35. Cyr DG, Hermo L, Blaschuk OW, Robaire B (1992) Distribution and regulation of epithelial cadherin messenger ribonucleic acid and immunocytochemical localization of epithelial cadherin in the rat epididymis. Endocrinology 130: 353–363PubMedGoogle Scholar
  36. Cyr DG, Hermo L, Egenberger N, Mertineit C, Trasler JM, Laird DW (1999) Cellular immunolocalization of occludin during embryonic and postnatal development of the mouse testis and epididymis. Endocrinology 140: 3815–3825PubMedGoogle Scholar
  37. Cyr DG, Hermo L, Robaire B (1993) Developmental-changes in epithelial cadherin messenger ribonucleic acid and immunocytochemical localization of epithelial cadherin during postnatal epididymal development in the rat. Endocrinology 132: 1115–1124PubMedGoogle Scholar
  38. Cyr DG, Robaire B (1992) Regulation of sulfated glycoprotein-2 (clusterin) messenger ribonucleic acid in the rat epididymis. Endocrinology 130: 2160–2166PubMedGoogle Scholar
  39. Dacheux JL, Dacheux F, Paquignon M (1989) Changes in sperm surface membrane and lumina] protein fluid content during epididymal transit in the boar. Biol Reprod 40: 635–651PubMedGoogle Scholar
  40. Desai KV, Flanders KC, Kondaiah P (1998) Expression of transforming growth factor-beta isoforms in the rat male accessory sex organs and epididymis. Cell Tissue Res 294: 271–277PubMedGoogle Scholar
  41. Del-Rio AG (1979) Macromolecular secretion into various segments of the guinea pig epididymis. Arch Androl 3: 231–237PubMedGoogle Scholar
  42. Drevet JR, Lareyre JJ, Schwaab V, Vernet P, Dufaure JP (1998) The PEA3 protein of the Ets oncogene family is a putative transcriptional modulator of the mouse epididymis-specific glutathione peroxidase gene GPX5. Mol Re-prod Dev 49: 131–140Google Scholar
  43. Fan X, Robaire B (1998) Orchidectomy induces a wave of apoptotic cell death in the epididymis. Endocrinology 139: 2128–2136PubMedGoogle Scholar
  44. Fisher JS, Turner KJ, Fraser HM, Saunders PT, Brown D, Sharpe RM (1998) Immunoexpression of aquaporin- I in the efferent ducts of the rat and marmoset monkey during development, its modulation by estrogens, and its possible role in fluid resorption. Endocrinology 139: 3935–3945PubMedGoogle Scholar
  45. Flickinger CJ, Bush LA, Howards SS, Herr JC (1997) Distribution of leucocytes in the epithelium and interstitium of four regions of the Lewis rat epididymis. Anat Rec 248: 380–390PubMedGoogle Scholar
  46. Garrett JE, Garrett SH, Douglass J (1990) A spermatozoa-associated factor regulates proenkephalin gene expression in the rat epididymis. Mol Endocrinol 4: 108–118PubMedGoogle Scholar
  47. Ghyselinck NB, Jimenez C, Lefrancois AM, Dufaure JP (1990) Molecular cloning of a cDNA for androgen-regulated proteins secreted by the mouse epididymis. J Mol Endocrinol 4: 5–12PubMedGoogle Scholar
  48. Gloyna RE, Wilson JD (1969) A comparative study of the conversion of testosterone to 1713-hydroxy-5a-androstan-3-one (dihydrotestosterone) by rat prostate and epididymis. J Clin Endocrinol Metab 29: 970–977PubMedGoogle Scholar
  49. Hamilton DW (1980) UDP-galactose:N-acetylglucosamine galactosyltransferase in fluids from rat rete testis and epididymis. Biol Reprod 23: 377–385PubMedGoogle Scholar
  50. Hall JC, Perez FM, Kochins JG, Pettersen CA, Li Y, Tubbs CE, LaMarche MD (1996) Quantification and localization of N-acetyl-beta-D-hexosaminidase in the adult rat testis and epididymis. Biol Reprod 54: 914–929PubMedGoogle Scholar
  51. Hermo L, Barin K, Robaire B (1992a) Structural differentiation of the epithelial cells of the testicular excurrent duct system of rats during postnatal development. Anat Rec 233: 205–228PubMedGoogle Scholar
  52. Hermo L, Oko R, Robaire B (1992b) Epithelial cells of the epididymis show regional variations with respect to the secretion of endocytosis of immobilin as revealed by light and electron microscope immunocytochemistry. Anat Rec 232: 202–220PubMedGoogle Scholar
  53. Hermo L, Lustig M, Lefrancois S, Argraves WS, Morales CR (1999) Expression and regulation of LRP-2/megalin in epithelial cells lining the efferent ducts and epididymis during postnatal development. Mol Reprod Dev 53: 282–293PubMedGoogle Scholar
  54. Hermo L, Wright J, Oko R, Morales CR (1991) Role of epithelial cells of the male excurrent duct system of the rat in the endocytosis or secretion of sulfated glycoprotein-2 (clusterin). Biol Reprod 44: 1113–1131PubMedGoogle Scholar
  55. Hess RA, Gist DH, Bunick D, Lubahn DB, Farrell A, Bahr J, Cooke PS, Greene GL (1997) Estrogen receptor (alpha and beta) expression in the ex-current ducts of the adult male rat reproductive tract. J Androl 18: 602–611PubMedGoogle Scholar
  56. Hinton BT, Lan ZJ, Rudolph DB, Labus JC, Lye RJ (1998) Testicular regulation of epididymal gene expression. J Reprod Fertil Suppl 53: 47–57PubMedGoogle Scholar
  57. Hinton BT, Palladino MA, Rudolph D, Labus JC (1995) The epididymis as protector of maturing spermatozoa. Reprod Fertil Dev 7: 731–745PubMedGoogle Scholar
  58. Holland MK, Orgebin-Crist MC (1988) Characterization and hormonal regulation of protein synthesis by the murine epididymis. Biol Reprod 38: 487–496PubMedGoogle Scholar
  59. Igdoura SA, Herscovics A, Lal A, Moremen KW, Morales CR, Hermo L (1999) Alpha-mannosidases involved in N-glycan processing show cell specificity and distinct subcompartmentalization within the Golgi apparatus of cells in the testis and epididymis. Eur J Cell Biol 78: 441–452PubMedGoogle Scholar
  60. Igdoura SA, Morales CR, Hermo L (1995) Differential expression of cathepsins B and D in testis and epididymis of adult rats. J Histochem Cytochem 43: 545–557PubMedGoogle Scholar
  61. Janulis L, Bahr JM, Hess RA, Janssen S, Osawa Y, Bunick D (1998) Rat testicular germ cells and epididymal sperm contain active P450 aromatase. J Androl 19: 65–71PubMedGoogle Scholar
  62. Jauhiainen A, Vanha-Perttula T (1985) Acid and neutral alpha-glucosidase in the reproductive organs and seminal plasma of the bull. J Reprod Fertil 74: 669–680PubMedGoogle Scholar
  63. Jeannotte L, Burbach JP, Drouin J (1987) Unusual proopiomelanocortin ribonucleic acids in extrapituitary tissues: intronless transcripts in testes and long poly(A) tails in hypothalamus. Mol Endocrinol 1: 749–757PubMedGoogle Scholar
  64. Jenkins E, Hsieh C-L, Milatovich A, Normington K, Berman DM, Francke U, Russell DW (1991) Characterization and chromosomal mapping of a human steroid 5a-reductase gene and pseudogene and mapping of the mouse homologue. Genomics 11: 1102–1112PubMedGoogle Scholar
  65. Jin YZ, Bannai S, Dacheux F, Dacheux JL, Okamura N (1997) Direct evidence for the secretion of lactoferrin and its binding to sperm in the porcine epididymis. Mol Reprod Dev 47: 490–496PubMedGoogle Scholar
  66. Kaunisto K, Fleming RE, Kneer J, Sly WS, Rajaniemi H (1999) Regional expression and androgen regulation of carbonic anhydrase IV and II in the adult rat epididymis. Biol Reprod 61: 1521–1526PubMedGoogle Scholar
  67. Kidroni G, Har-Nir R, Menezel J, Frutkoff 1W, Palti Z, Ron M (1983) Vitamin D3 metabolites in rat epididymis: high 24,25-dihydroxy vitamin D3 levels in the cauda region. Biochem Biophys Res Commun 113: 982–989Google Scholar
  68. Kirchhoff C (1999) Gene expression in the epididymis. Int Rev Cytol 188: 133–202PubMedGoogle Scholar
  69. Kirchhoff C, Habben I, Ivell R, Krull N (1991) A major human epididymisspecific cDNA encodes a protein with sequence homology to extracellular proteinase inhibitors. Biol Reprod 45: 350–357PubMedGoogle Scholar
  70. Kirchhoff C, Krull N, Pera I, Ive11 R (1993) A major mRNA of the human epididymal principal cells, HE5, encodes the leucocyte differentiation CDw52 antigen peptide backbone. Mol Reprod Dev 34: 8–15PubMedGoogle Scholar
  71. Kirchhoff C, Osterhoff C, Young L (1996) Molecular cloning and characterization of HEI, a major secretory protein of the human epididymis. Biol Reprod 54: 847–856PubMedGoogle Scholar
  72. Kistler MK, Ostrowski MC, Kistler WS (1981) Developmental regulation of secretory protein synthesis in the rat seminal vesicle. Proc Natl Acad Sci USA 78: 737–741PubMedGoogle Scholar
  73. Klinefelter GR, Amann RP (1980) Metabolism of testosterone by principal cells and basal cells isolated from the rat epididymal epithelium. Biol Re-prod 22: 1149–1154Google Scholar
  74. Labrie F, Sugimoto Y, Luu-The V, Simard J, Lachance Y, Bachvarov D, Leblanc G, Durocher F, Paquet N (1992) Structure of human type II 5a-reductase gene. Endocrinology 131: 1571–1573PubMedGoogle Scholar
  75. Lan ZJ, Labus JC, Hinton BT (1998) Regulation of gamma-glutamyl transpeptidase catalytic activity and protein level in the initial segment of the rat epididymis by testicular factors: role of basic fibroblast growth factor. Biol Reprod 58: 197–206PubMedGoogle Scholar
  76. Lan ZJ, Lye RJ, Holic N, Labus JC, Hinton BT (1999) Involvement of polyomavirus enhancer activator 3 in the regulation of expression of gamma-glutamyl transpeptidase messenger ribonucleic acid-1V in the rat epididymis. Biol Reprod 60: 664–673PubMedGoogle Scholar
  77. Lareyre JJ, Thomas TZ, Zheng WL, Kasper S, Ong DE, Orgebin-Crist MC, Matusik RI (1999) A 5-kilobase pair promoter fragment of the murine epididymal retinoic acid-binding protein gene drives the tissue-specific, cell-specific, and androgen-regulated expression of a foreign gene in the epididymis of transgenic mice. J Biol Chem 274: 8282–8290PubMedGoogle Scholar
  78. Lea OA, French FS (1981) Characterization of an acidic glycoprotein secreted by principal cells of the rat epididymis. Biochim Biophys Acta 668: 370–376PubMedGoogle Scholar
  79. Legaré C, Gaudreault C, St-Jacques S, Sullivan R (1999) P34H sperm protein is preferentially expressed by the human corpus epididymidis. Endocrinology 140: 3318–3327PubMedGoogle Scholar
  80. Levy S, Robaire B (1999) Segment-specific changes in the expression of junctional proteins and the permeability of the blood-epididymis barrier with age. Biol Reprod 60: 1392–1401PubMedGoogle Scholar
  81. Li L, Xu JN, Wong YH, Wong JT, Pang SF, Shiu SY (1998) Molecular and cellular analyses of melatonin receptor-mediated cAMP signaling in rat corpus epididymis. J Pineal Res 25: 219–228PubMedGoogle Scholar
  82. Lindsey S, Wilkinson MF (1996) Homeobox genes and male reproductive development. J Assist Repro Genetics 13: 182–192Google Scholar
  83. Mattmueller DR, Hinton BT (1991) In vivo secretion and association of clusterin (SGP-2) in luminal fluid with spermatozoa in the rat testis and epididymis. Mol Reprod Dev 30: 62–69PubMedGoogle Scholar
  84. Mayorga LS, Bertini F (1985) The origin of some acid hydrolases of the fluid of the rat cauda epididymidis. J Androl 6: 243–245PubMedGoogle Scholar
  85. Miranda PV, Brandelli A, Tezon JG (1995) Characterization of beta-N-acetylglucosaminidase from human epididymis. Int J Androl 18: 263–270PubMedGoogle Scholar
  86. Mueller A, Hermo L, Robaire B (1998) The effects of aging on the expression of glutathione S-transferases in the testis and epididymis of the Brown Norway rat. J Androl 19: 450–465PubMedGoogle Scholar
  87. Normington K, Russell DW (1992) Tissue distribution and kinetic characteristics of rat steroid 5a-reductase isozymes. J Biol Chem 267: 19548–19554PubMedGoogle Scholar
  88. Oefelein M, Grapey D, Schaeffer T, Chin-Chance C, Bushman W (1996) Pax-2: a developmental gene constitutively expressed in the mouse epididymis and ductus deferens. J Urol 156: 1204–1207PubMedGoogle Scholar
  89. Okamura N, Dacheux F, Venien A, Onoe S, Huet JC, Dacheux JL (1992) Localization of a maturation-dependent epididymal sperm surface antigen recognized by a monoclonal antibody raised against a 135-kilodalton protein in porcine epididymal fluid. Biol Reprod 47: 1040–1052PubMedGoogle Scholar
  90. Okamura N, Iwaki Y, Hiramoto S, Tamba M, Bannai S, Sugita Y, Syntin P, Dacheux F, Dacheux JL (1997) Molecular cloning and characterization of the epididymis-specific glutathione peroxidase-like protein secreted in the porcine epididymal fluid. Biochim Biophys Acta 1336: 99–109PubMedGoogle Scholar
  91. Okamura N, Kiuchi S, Tamba M, Kashima T, Hiramoto S, Baba T, Dacheux F, Dacheux JL, Sugita Y, Jin YZ (1999) A porcine homolog of the major secretory protein of human epididymis, HE1, specifically binds cholesterol. Biochim Biophys Acta 1438: 377–387PubMedGoogle Scholar
  92. Okamura N, Tamba M, Liao HJ, Onoe S, Sugita Y, Dacheux F, Dacheux JL (1995b) Cloning of complementary DNA encoding a 135-kilodalton protein secreted from porcine corpus epididymis and its identification as an epididymis-specific alpha-mannosidase. Mol Reprod Dev 42: 141–148PubMedGoogle Scholar
  93. Okamura N, Tamba M, Uchiyama Y, Sugita Y, Dacheux F, Syntin P, Dacheux JL (I 995a) Direct evidence for the elevated synthesis and secretion of procathepsin L in the distal caput epididymis of boar. Biochim Biophys Acta 1245: 221–226Google Scholar
  94. Olson GE, Hinton BT (1985) Regional differences in luminal fluid polypeptides of the rat testis and epididymis revealed by two-dimensional gel electrophoresis. J Androl 6: 20–34PubMedGoogle Scholar
  95. Ong DE, Chytil F (1988) Presence of novel retinoic acid-binding proteins in the lumen of rat epididymis. Arch Biochem Biophys 267: 474–478PubMedGoogle Scholar
  96. Orgebin-Crist M-C (1967) Sperm maturation in rabbit epididymis. Nature 216: 816–818PubMedGoogle Scholar
  97. Orgebin-Crist MC, Djiane J (1979) Properties of a prolactin receptor from the rabbit epididymis. Biol Reprod 21: 135–139PubMedGoogle Scholar
  98. Orgebin-Crist M-C, Jahad N, Hoffman LH (1976) The effects of testosterone, 5a-dihydrotestosterone, 3a-androstandiol, and 313-androstandiol on the maturation of rabbit epididymal spermatozoa in organ culture. Cell Tissue Res 167: 515–525PubMedGoogle Scholar
  99. Osterhoff C, Kirchhoff C, Krull N, Ivell R (1994) Molecular cloning and characterization of a novel human sperm antigen (HE2) specifically expressed in the proximal epididymis. Biol Reprod 50: 516–525PubMedGoogle Scholar
  100. Palladino MA, Hinton BT (1994) 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 manner. Endocrinology 135: 1146–1156PubMedGoogle Scholar
  101. Papp S, Robaire B, Hermo L (1995) Immunocytochemical localization Ya, Yc, Ybi, and Yb2 subunits of glutathione S-transferases in the testis and epididymis of adult rats. Micro Res Tech 30: 1–23Google Scholar
  102. Pera I, Den P, Yeung CH, Cooper TG, Kirchhoff C (1997) Regionalized expression of CD52 in rat epididymis is related to mRNA poly(A) tail length. Mol Reprod Dev 48: 433–441PubMedGoogle Scholar
  103. Perry AC, Jones R, Barker PJ, Hall L (1992) A mammalian epididymal protein with remarkable sequence similarity to snake haemorrhagic peptides. Biochem J 286: 671–675PubMedGoogle Scholar
  104. Perry AC, Jones R, Hall L (1993a) 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 293: 21–25PubMedGoogle Scholar
  105. Perry AC, Jones R, Hall L (1993b) Sequence analysis of monkey acrosin-trypsin inhibitor transcripts and their abundant expression in the epididymis. Biochim Biophys Acta 1172: 159–160PubMedGoogle Scholar
  106. Podlasek CA, Seo RM, Clemens JQ, Ma L, Maas RL, Bushman W (1999) Hoxa-10 deficient male mice exhibit abnormal development of the accessory sex organs. Dev Dynamics 214: 1–12Google Scholar
  107. Porter SB, Ong DE, Chytil F, Orgebin-Crist MC (1985) Localization of cellular retinol-binding protein and cellular retinoic acid-binding protein in the rat testis and epididymis. J Androl 6: 197–212PubMedGoogle Scholar
  108. Rankin TL, Tsuruta KJ, Holland MK, Griswold MD, Orgebin-Crist MC (1992) Isolation, immunolocalization, and sperm-association of three proteins of 18, 25, and 29 kilodaltons secreted by the mouse epididymis. Biol Reprod 46: 747–766Google Scholar
  109. Ravet V, Depeiges A, Morel F, Dufaure JP (1991) Synthesis and post-translational modifications of an epididymal androgen dependent protein family. Gen Comp Endocrinol 84: 104–114PubMedGoogle Scholar
  110. Robaire B (1979) Effects of unilateral orchidectomy on rat epididymal A4–5areductase and 3a-hydroxysteroid dehydrogenase. Can J Physiol Pharmol 57: 998–100Google Scholar
  111. Robaire B, Ewing LL, Zirkin BR, Irby DC (1977) Steroid A4–5a-reductase and 3a-hydroxysteroid dehydrogenase in the rat epididymis. Endocrinology 101: 1379–1390PubMedGoogle Scholar
  112. Robaire B, Hermo L (1988) Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. In: Knobil E, Neill J (eds) The Physiology of Reproduction. Raven Press, New York, pp 999–1080Google Scholar
  113. Robaire B, Scheer H, Hachey C (1981) Regulation of epididymal steroid metabolizing enzymes. In: Jagiello G, Vogel HJ (eds) Bioregulators of Reproduction. Academic Press, New York, pp 487–498Google Scholar
  114. Robaire B, Viger R (1995) Regulation of epididymal epithelial cell functions. Biol Reprod 52: 226–236PubMedGoogle Scholar
  115. Robaire B, Zirkin BR (1981) Hypophysectomy and simultaneous testosterone replacement: effects on male rat reproductive tract and epididymal A4–5areductase and 3a-hydroxysteroid dehydrogenase. Endocrinology 109: 1225–1233PubMedGoogle Scholar
  116. Rockwerger I, Cohen D, Cuasnicu PS (1992) Mammalian sperm-egg fusiom: the rat egg has complementary sites for a sperm protein that mediate gamete fusion. Dev Biol 153: 83–90Google Scholar
  117. Ruiz-Bravo N (1988) Tissue and cell specificity of immobilin biosynthesis. Biol Reprod 39: 901–911PubMedGoogle Scholar
  118. Scheer H, Robaire B (1980) Steroid A4–5a-reductase and 3a-hydroxysteroid dehydrogenase in the rat epididymis during postnatal development. Endocrinology 107: 948–953PubMedGoogle Scholar
  119. Scheer H, Robaire B (1983) Subcellular distribution of steroid A4–5a-reductase and 3a-hydroxysteroid dehydrogenase in the rat epididymis during sexual maturation. Biol Reprod 29: 1–10PubMedGoogle Scholar
  120. Schleicher G, Privette TH, Stumpf WE (1989) Distribution of soltriol [1,25(OH)2-vitamin D3] binding sites in male sex organs of the mouse: an autoradiographic study. J Histochem Cytochem 37: 1083–1096PubMedGoogle Scholar
  121. Schwaab V, Faure J, Dufaure JP, Drevet JR (1998) GPx3: the plasma-type glutathione peroxidase is expressed under androgenic control in the mouse epididymis and vas deferens. Mol Reprod Dev 51: 362–372PubMedGoogle Scholar
  122. Serre V, Robaire B (1998a) Segment specific morphological changes in the aging Brown Norway rat epididymis. Biol Reprod 58: 497–513PubMedGoogle Scholar
  123. Serre V, Robaire B (1998b) Paternal age affects fertility and progeny outcome in the Brown Norway rat. Fertil Steril 70: 625–31PubMedGoogle Scholar
  124. Serre V, Robaire, B., (1999) The distribution of immune cells in the epithelium of the epididymis of the aging brown norway rat is segment-specific and related to the luminal content. Biol Reprod 61: 705–714PubMedGoogle Scholar
  125. Shiu SY, Chow PH, Yu ZH, Tang F, Pang SF (1996) Autoradiographic distribution and physiological regulation of 2-[1251]iodomelatonin binding in rat epididymis. Life Sci 59: 1165–1174PubMedGoogle Scholar
  126. Silber SJ (1989) Results of microsurgical vasoepididymostomy: role of epididymis in sperm maturation. Hum Reprod 4: 298–303PubMedGoogle Scholar
  127. Sonnenberg-Riethmacher E, Walter B, Riethmacher D, Godecke S, Birchmeier C (1996) The c-ros tyrosine kinase receptor controls regionalization and differentiation of epithelial cells in the epididymis. Genes Dev 10: 1184–1193PubMedGoogle Scholar
  128. Sun EL, Flickinger CJ (1979) Development of cell types and of regional differences in the postnatal rat epididymis. Am J Anat 154: 27–55PubMedGoogle Scholar
  129. Sutton KA, Maiti S, Tribley WA, Lindsey JS, Meistrich ML, Bucana CD, Sanborn BM, Joseph DR, Griswold MD, Cornwall GA, Wilkinson MF (1998) Androgen regulation of the Pem homeodomain gene in mice and rat Sertoli and epididymal cells. J Androl 19: 21–30PubMedGoogle Scholar
  130. Sylvester SR, Morales C, Oko R, Griswold MD (1991) Localization of sulfated glycoprotein-2 (clusterin) on spermatozoa and in the reproductive tract of the male rat. Biol Reprod 45: 195–207PubMedGoogle Scholar
  131. Sylvester SR, Skinner MK, Griswold MD (1984) A sulfated glycoprotein synthesized by Sertoli cells and by epididymal cells is a component of the sperm membrane. Biol Reprod 31: 1087–1101PubMedGoogle Scholar
  132. Syntin P, Dacheux JL, Dacheux F (1999) Postnatal development and regulation of proteins secreted in the boar epididymis. Biol Reprod 61: 1622–1635PubMedGoogle Scholar
  133. Syntin P, Dacheux F, Druart X, Gatti JL, Okamura N, Dacheux JL (1996) Characterization and identification of proteins secreted in the various regions of the adult boar epididymis. Biol Reprod 55: 956–974PubMedGoogle Scholar
  134. Takada M, Yonezawa N, Yoshizawa M, Noguchi S, Hatanaka Y, Nagai T, Kikuchi K, Aoki H, Nakano M (1994) pH-sensitive dissociation and association of beta-N-acetylhexosaminidase from boar sperm acrosome. Biol Reprod 50: 860–868Google Scholar
  135. Thigpen AE, Davis DL, Milatovich A, Mendonca BB, Imperato-McGinley J, Griffin JE, Francke U, Wilson JD, Russell DW (1992) Molecular genetics of steroid 5a-reductase 2 deficiency. J Clin Invest 90: 799–809PubMedGoogle Scholar
  136. Tindall DJ, French FS, Nayfeh SN (1972) Androgen uptake and binding in rat epididymal nuclei, in vivo. Biochem Biophys Res Commun 49: 1391–1397PubMedGoogle Scholar
  137. Tomomasa H, Waguri S, Umeda T, Koiso K, Kominami E, Uchiyama Y (1994) Lysosomal cysteine proteinases in rat epididymis. J Histochem Cytochem 42: 417–425PubMedGoogle Scholar
  138. Tulsiani DR, NagDas SK, Skudlarek MD, Orgebin-Crist MC (1995b) Rat sperm plasma membrane mannosidase: localization and evidence for proteolytic processing during epididymal maturation. Dev Biol 167: 584–595PubMedGoogle Scholar
  139. Tulsiani DR, Orgebin-Crist MC, Skudlarek MD (1998) Role of luminal fluid glycosyltransferases and glycosidases in the modification of rat sperm plasma membrane glycoproteins during epididymal maturation. J Reprod Fertil Suppl 53: 85–97PubMedGoogle Scholar
  140. Tulsiani DR, Skudlarek MD, Araki Y, Orgebin-Crist MC (1995a) Purification and characterization of two forms of beta-D-galactosidase from rat epididymal luminal fluid: evidence for their role in the modification of sperm plasma membrane glycoprotein(s). Biochem J 305: 41–50PubMedGoogle Scholar
  141. Tulsiani DR, Skudlarek MD, Holland MK, Orgebin-Crist MC (1993b) Glycosylation of rat sperm plasma membrane during epididymal maturation. Biol Reprod 48: 417–428PubMedGoogle Scholar
  142. Tulsiani DR, Skudlarek MD, Nagdas SK, Orgebin-Crist MC (1993a) Purification and characterization of rat epididymal-fluid alpha-D-mannosidase: similarities to sperm plasma-membrane alpha-D-mannosidase. Biochem J 290: 427–436PubMedGoogle Scholar
  143. Turner TT, Jones CE, Howards SS, Ewing LL, Zegeye B, Gunsalus GL (1984) On the androgen microenvironment of maturing spermatozoa. Endocrinology 115: 1925–1932PubMedGoogle Scholar
  144. Turner TT, Miller DW, Avery EA (1995) Protein synthesis and secretion by the rat caput epididymis in vivo: influence of the luminal microenvironment. Biol Reprod 52: 1012–1019PubMedGoogle Scholar
  145. Ueda H, Hirano T, Fujimoto S (1990) Changes in proteins secretion patterns during the development of the rat epididymis. Zool Sci 55: 119–125Google Scholar
  146. Veri JP, Hermo L, Robaire B (1993) Immunocytochemical localization of the Yf subunit of glutathione S-transferase P shows regional variation in the staining of epithelial cells of the testis, efferent ducts and epididymis of the male rat. J Androl 14: 23–44PubMedGoogle Scholar
  147. Vierula ME, Rankin TL, Orgenin-Crist M-C (1995) Electron microscopic immunolocalization of the 18 and 29 kilodalton secretory proteins in the mouse epididymis: evidence for differential uptake by clear cells. Micro Res Tech 30: 24–36Google Scholar
  148. Viger RS, Robaire B (1991) Differential regulation of steady state 4-ene steroid 5a-reductase messenger ribonucleic acid levels along the rat epididymis. Endocrinology 128: 2407–2414PubMedGoogle Scholar
  149. Viger RS, Robaire B (1992) Expression of 4-ene steroid 5a-reductase messenger ribonucleic acid in the rat epididymis during postnatal development. Endocrinology 131: 1534–1540PubMedGoogle Scholar
  150. Viger RS, Robaire B (1994) Immunocytochemical localization of 4-ene steroid 5a-reductase type 1 along the rat epididymis during postnatal development. Endocrinology 134: 2298–2306PubMedGoogle Scholar
  151. Viger RS, Robaire B (1995) Gene expression in the aging Brown Norway rat epididymis. J Androl 16: 108–117PubMedGoogle Scholar
  152. Viger RS, Robaire B (1996) The mRNAs for the steroid 5a-reductase isozymes, type 1 and type 2, are differentially regulated in the rat epididymis. J Androl 17: 27–34PubMedGoogle Scholar
  153. Wichmann L, Vaalasti A, Vaalasti T, Tuohimaa P (1989) Localization of lactoferrin in the male reproductive tract. Int J Androl 12: 179–186PubMedGoogle Scholar
  154. Winer MA, Wolgemuth DJ (1995) The segment-specific pattern of A-raf expression in the mouse epididymis is regulated by testicular factors. Endocrinology 136: 2561–2572PubMedGoogle Scholar
  155. Wong PY, Chan HC, Leung PS, Chung YW, Wong YL, Lee WM, Ng V, Dun NJ (1999) Regulation of anion secretion by cyclo-oxygenase and prostanoids in cultured epididymal epithelia from the rat. J Physiol 514: 809–820PubMedGoogle Scholar
  156. Wright WW, Fiore C, Zirkin BR. (1993) The effect of aging on the seminiferous epithelium of the Brown Norway rat. J Androl 14: 110–117PubMedGoogle Scholar
  157. Xu W, Ensrud KM, Hamilton DW (1997) The 26 kD protein recognized on rat cauda epididymal sperm by monoclonal antibody 4E9 has internal peptide sequence that is identical to the secreted form of epididymal protein E. Mol Reprod Dev 46: 377–382Google Scholar
  158. Young WC (1929a) A study of the function of the epididymis. I. Is the attainment of full spermatozoon maturity attributable to some specific action of the epididymal secretion? J Morphol Physiol 47: 479–495Google Scholar
  159. Young WC (1929b) A study of the function of the epididymis. II. The importance of an aging process in sperm for the length of the period during which fertilizing capacity is retained by sperm isolated in the epididymis of the guinea-pig. J Morphol Physiol 48: 475–491Google Scholar
  160. Young WC (1931) A study of the function of the epididymis. III. Functional changes undergone by spermatozoa during their passage through the epididymis and vas deferens in the guinea pig. J Exp Biol 8: 151–162Google Scholar
  161. Yu LC, Chen (1993) The developmental profile of lactoferrin in mouse epididymis. Biochem J 296: 107–111Google Scholar
  162. Zhao GQ, Liaw L, Hogan BL (1998) Bone morphogenetic protein 8 A plays a role in the maintenance of spermatogenesis and the integrity of the epididymis. Development 125: 1103–1112PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2000

Authors and Affiliations

  • B. Robaire
  • P. Syntin
  • K. Jervis

There are no affiliations available

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