Role of the Epididymis in Mediating Changes in the Male Gamete during Maturation

  • T. G. Cooper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 377)


This article reviews recent knowledge about events occurring in the epididymis that are important for sperm to fertilise eggs. Well established concepts are stated without references (see Cooper, 1986 for older literature) but recent references are included where they throw light on mechanisms of epididymal function. During their sojourn in the epididymis spermatozoa acquire the capacity to move and to fertilise eggs; they are then stored in a quiescent state prior to ejaculation. The ability of sperm to undergo the events of fertilisation are developed as a result of interactions with certain epididymal secretions. Increases in our knowledge about the genes coding for epididymal secretions has not yet been matched by similar insight into the role that these secretions play in the maturation process. However, information about the changes that occur to the sperm cells during maturation permit certain scenarios to be sketched that may reflect reality. This review is one such attempt to bring the epididymal sperm-epithelial secretion into focus.


Sperm Cell Zona Pellucida Acrosome Reaction Epididymal Spermatozoon Testicular Spermatozoon 
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. Agmo A, The number of spermatozoa in spontaneous ejaculates of rats. J Reprod Fert 1976; 48: 405–407.Google Scholar
  2. Amann RP, Hammerstedt RH, Veeramachaneni DNR, The epididymis and sperm maturation: a perspective. Reprod Fertil Dev 1993; 5: 361–381.PubMedGoogle Scholar
  3. Anakwe OO, Sharma S, Hoff HB, Hardy DM, Gerton GL, Maturation of guinea pig sperm in the epididymis involves the modification of proacrosin oligosaccharide side chains. Molec Reprod Develop 1991; 29: 294–301.Google Scholar
  4. Araki Y, Vierula ME, Rankin TL, Tulsiani DRP, Orgebin-Crist M-C, Isolation and characterization of a 25-kilodalton protein form mouse testis: sequence homology with a phospholipid-binding protein. Biol Reprod 1992; 47: 832–843.PubMedGoogle Scholar
  5. Ariel M, Cedar H, McCarry J, Developmental changes in methylation of spermatogenesis-specific genes include reprogramming in the epididymis. Nature Genetics 1994; 7: 59–63.PubMedGoogle Scholar
  6. Barratt CLR, Cooke ID, Sperm loss in the urine of sexually rested men. Int J Androl 1988; 11: 201–207.PubMedGoogle Scholar
  7. Bearer EL, Friend DS, Morphology of mammalian sperm membranes during differentiation, maturation, and capacitation. J Elect Microscopy Technique 1990; 16: 281–297.Google Scholar
  8. Bedford JM. Sperm dynamics in the epididymis. In: Asch RA, Balmaceda JP, Johnston I, eds. Gamete Physiology. Serono Symposia, Norwell, 1990: 53–67).Google Scholar
  9. Bedford JM, Yanagimachi R, Epididymal storage at abdominal temperature reduces the time required for capacitation of hamster sprmatozoa. J Reprod Fert 1991; 91: 403–410.Google Scholar
  10. Biegler BE, Aarons DJ, George BC, Poirier GR, Induction of physiological acrosome reactions in caput epididymal spermatozoa of mice. J Reprod Fertil 1994; 100: 219–224.PubMedGoogle Scholar
  11. Blackmore PF, Lattanzio FA, Cell surface localization of a novel non-genomic progesterone receptor on the head of human sperm. Biochem Biophys Res Commun 1991; 181: 331–336.PubMedGoogle Scholar
  12. Block LJ, Bartlett JM, Bold-de-Vries J; Themmen AP, Brinkmann AO, Weinbauer GF, Nieschlag E, Grootegoed JA, Effect of testosterone deprivation on expression of the androgen receptor in rat prostate, epididymis and testis. Int J Androl 1992; 15: 182–198.Google Scholar
  13. Brooks DE, Characterization of a 22kDa protein with widespread tissue distribution but which is uniquely present in secretions of the testis and epididymis and on the surface of spermatozoa. Biochem Biophys Acta 1985; 841: 59–70.PubMedGoogle Scholar
  14. Brown D, Verbavatz J-M, Valenta G, Lui B, Sablic I, Localization of the CHIP28 water channel in reabsorptive sgments of the rat male reproductive tract. Eur J Cell Biol 1993; 61: 264–273.PubMedGoogle Scholar
  15. Bunch D, Leyton L, Saling P. Sperm interaction with the zona pellucida: role of a tyrosine kinase receptor for ZP3 in fertilization. In: Nieschlag E, Habenicht U-F, eds. Spermatogenesis, Fertilization, Contraception. Molecular, cellular and endocrine events in male reproduction. Schering Foundation Workshop 4, Springer Verlag, Berlin, 1992: 367–381).Google Scholar
  16. Byers S, Graham R, Distribution of sodium-potassium ATPase in the rat testis and epididymis. Am J Anat 1990; 188: 31–43.PubMedGoogle Scholar
  17. Caflisch CR, DuBose TD, Direct evaluation of acidification by rat testis and epididymis: role of carbonic anhydrase. Am J Physiol 1990; 258:E143–E150.PubMedGoogle Scholar
  18. Carr DW; Usselman MC; Acott TS, Effects of pH, lactate, and viscoelastic drag on sperm motility: a species comparison. Biol Reprod 1985; 33: 588–595.PubMedGoogle Scholar
  19. Casillas ER, Accumulation of carnitine by bovine spermatozoa during maturation in the epididymis. J Biol Chem 1973; 248: 8227–8232.PubMedGoogle Scholar
  20. Cooper TG. The Epididymis, Sperm Maturation and Fertilisation. Springer Verlag, Heidelberg, 1986.Google Scholar
  21. Cooper TG, The epididymis as a site of contraceptive attack. In: Nieschlag, E; Habenicht, U-F (eds). Spermatogenesis, Fertilization, Contraception. Molecular, cellular and endocrine events in male reproduction. Schering Foundation Workshop 4, Springer Verlag, Berlin, 1992a:419–460.Google Scholar
  22. Cooper TG. Epididymal proteins and sperm maturation. In: Nieschlag E, Habenicht U-F, eds. Spermatogenesis, fertilization, contraception. Molecular, cellular and endocrine events in male reproduction. Schering Foundation Workshop 4, Springer Verlag, Berlin, 1992b:285–318.Google Scholar
  23. Cooper TG, Yeung CH, Bergmann M, Transcytosis in the epididymis studied by local arterial perfusion. Cell Tiss Res 1988; 253: 631–637.Google Scholar
  24. Cowan AE, Myles DG, Koppel DE, Lateral diffusion of the PH-20 protein on guinea pig sperm: evidence that barriers to diffusion maintain plasma membrane domains in mammalian sperm. J Cell Biol 1987; 104: 917–923.PubMedGoogle Scholar
  25. Craft I, Bennet V, Nicholson N, Fertilising ability of testicular spermatozoa. Lancet 1993; 342:864.PubMedGoogle Scholar
  26. Diaz-Perez E, Meizel S, Importance of mammalian sperm metalloendoprotease activity during the acrosome reaction to subsequent sperm-egg fusion. Inhibition studies with human sperm and zona-free hamster eggs. Molec Reprod Develop 1992; 31: 122–130.Google Scholar
  27. Erickson HP, Gene knockouts of c-src, transforming growth factor β1, and tenascin suggest superfluous, nonfunctional expression of proteins. J Cell Biol 1993; 120: 1079–1081.PubMedGoogle Scholar
  28. Frankel AI, Chapman JC, Nuclear androgen binding sites in the male rat.III. Late spermatid and spermatozoa in the testis with an introduction to epididymal spermatozoa. J Steroid Biochem 1984; 20: 1301–1311.Google Scholar
  29. Garrett JE, Garrett SH, Douglass J, A spermatozoa-associated factor regulates proenkephalin gene expression in the rat epididymis. Mol Endocrinol 1990; 4: 108–118.PubMedGoogle Scholar
  30. Garrett SH, Garrett JE, Douglass J, In situ histochemical analysis of region-specific gene expression in the adult rat epididymis. Molec Reprod Develop 1991; 30: 1–17.Google Scholar
  31. Girotti M, Jones R, Emery DC, Chia W, Hall L, Structure and expression of the rat epididymal secretory protein I gene. An androgen-regulated member of the lipocalin superfamily with a rare splice donor site. Biochem J 1992; 281: 203–210.Google Scholar
  32. Glander HJ, Herrmann K, Haustam UF, The equatorial fibronecitin bound (EFB) on human spermatozoa-a diagnostic help in male fertility. Andrologia 1987; 19: 456–459.PubMedGoogle Scholar
  33. Gmachl M, Kreil G, Bee venom hyaluronidase is homologous to a membrane protein of mammalian sperm. Proc Natl Acad Sci US 1993; 90: 3569–3573.Google Scholar
  34. Grove K L, Speth RC, Rat epididymis contains functional angiotensin II receptors. Endocrinology 1989; 125: 223–230.PubMedGoogle Scholar
  35. Hall JC, Hadley J, Doman T, Correlation between changes in rat sperm membrane lipids, protein, and the membrane physical state during epididymal maturation. J Androl 1991; 12: 76–87.PubMedGoogle Scholar
  36. Hermo L, Dworkin J, Oko R, Role of epithelial clear cells of the rat epididymis in the disposal of the contents of cytoplasmic droplets detached from spermatozoa. Am J Anat 1988; 183: 107–124.PubMedGoogle Scholar
  37. Hermo L, Morales C, Oko R, Immunocytochemical localization of sulfated glycoprotein-1 (SGP-1) and identification of its transcripts in epithelial cells of the extratesticular duct system of the rat. Anat Rec 1992; 232: 401–422.PubMedGoogle Scholar
  38. Hermo L, Wright J, Oko R, Morales CR, Role of epithelial cells of the male ecurrent duct system of the rat in the endocytosis of secretion of sulfated glycoprotein-2 (clusterin). Biol Reprod 1991; 44:1115–1131.Google Scholar
  39. Hirsch A, Montgomery J, Mohan P, Mills C, Bekir J, Tan S-L, Fertilisation by testicular sperm with standard IVF techniques. Lancet 1993; 342: 1237–1238.Google Scholar
  40. Hoskins DD, Vijayaraghavan S. A new theory on the acquisition of sperm motility during epididymal transit. In: Gagnon C, ed. Controls of sperm motility; biological and clinical aspects. CRC Press, Boston, 1990: 53–62).Google Scholar
  41. Igdoura SA, Hermo L, Rosenthal A, Morales CR, Nonciliated cells of the rat efferent ducts endocytose testicular sulfated glycoprotein-1 (SGP-1) and synthesize SGP-1 derived saposins. Anatomical Record 1993; 235: 411–424.PubMedGoogle Scholar
  42. Irwin M, Nicholson N, Haywood JT, Poirier GR, Immunological localization of a murine seminal vesicle proteinase inhibitor. Biol Reprod 1983; 28: 1201–1206.PubMedGoogle Scholar
  43. Ivell R, “All that glisters is not gold” — common testis gene transcripts are not always what they seem. Int J Androl 1992; 15: 85–92.PubMedGoogle Scholar
  44. Jaakola U-M, Regional variations in transport of the luminal contents of the rat epididymis in vivo. J Reprod Fert 1983; 68: 465–470.Google Scholar
  45. Jeulin C, Dacheux JL, Soufir JC, Uptake and release of free L-carnitine by boar epididymal spermatozoa in vitro and subsequent acetylation rate. J Reprod Fert 1994; 100: 263–271.Google Scholar
  46. Jones R, Membrane remodelling during sperm maturation in the epididymis. Oxford Reviews of Reproductive Biology 1989; 11: 285–337.PubMedGoogle Scholar
  47. Jones R, Hall L, A 23kDa protein from rat sperm plasma membranes shows sequence similarity and phospholipid binding properties to a bovine brain cytosolic protein. Biochim Biophys Acta 1991; 1080: 78–892.PubMedGoogle Scholar
  48. Jones R, Brown CR, von Glos KI, Parker MG, Hormonal regulation of protein synthesis in the rat epididymis. Characterisation of androgen-dependent and testicular fluid-dependent proteins. Biochem J 1980; 188: 667–676.PubMedGoogle Scholar
  49. Jones R, Brown CR, Lancaster RT, Carbohydrate-binding properties of boar sperm proacrosin and assessment of its role in sperm-egg recognition and adhesion during fertilization. Development 1988; 102: 781–792.Google Scholar
  50. Kalabi P, Visconti P, Leclerc P, Kopf GS, p95, the major phosphotyrosine-containing protein in mouse spermatozoa, is a hexokinase with unique properties. J Biol Chem 1994; 269: 3810–3817.Google Scholar
  51. Kaufman S, Wright WW, Okret S, Wikstroem A-C, Gustafssonm, J-A, Shaper NL, Shaper JH, Evidence that rodent epididymal sperm contain the Mr-94,000 glucocorticoid receptor but lack the Mr-90,000 heat shock protein. Endocrinology 1992; 130: 3074–3084.Google Scholar
  52. Kawai Y, Yoshikawa K, Hama T, Mayumi T, Studies on egg zona pellucida-binding molecule (ligand) of mouse sperm. I. Sperm maturation and zona-binding ability. J Pharmacobio-Dyn 1991; 14: 231–236.PubMedGoogle Scholar
  53. Lakoski KA, Carron CP, Cabot CL, Saling PM, Epididymal maturation and the acrosome reaction in mouse sperm: response to zona pellucida coincident with modifications of M42 antigen. Biol Reprod 1988; 38: 221–233.PubMedGoogle Scholar
  54. Lathrop WF, Carmichael EP, Myles AG, Primakoff D, cDNA cloning reveals the molecular structure of a sperm surface protein, PH-20, involved in sperm-egg adhesion and the wide ditribution of its gene among mammals. J Cell Biol 1990; 111: 2939–29494.PubMedGoogle Scholar
  55. Lewin L, Nevo Z, Gabsu A, Weissenberg R, The role of sperm-bound hyaluronidase in the dispersal of the cumuls oophorus surrounding trat ova. Int J Androl 1982; 5: 37–44.PubMedGoogle Scholar
  56. Leyton L, Robinson A, Saling P, Relationship between the M42 antigen of mouse sperm and the acrosome reaction induced by ZP3. Develop Biol 1989; 133: 174–178.Google Scholar
  57. Lin Y, Mahan K, Lathrop WF, Myles DG, Primakoff P, A hyaluronidase activity of the sperm plasma membrane protein PH-20 enables sperm to penetrate the cumulus cell layer surrounding the egg. J Cell Biol 1994; 125: 1157–1163.PubMedGoogle Scholar
  58. Lopez A ML, de Souza W, Distribution of filipin-sterol complexes in the plasma membrane of stallion spermatozoa during the epididymal maturation process. Mol Reprod and Develop 1991; 28:158–168.Google Scholar
  59. Lopez LC, Shur BD, Redistribution of mouse sperm surface galactosyltransferase after the acrosome reaction. J Cell Biol 1987; 105: 1663–1670.PubMedGoogle Scholar
  60. Lopez LC, Bayna EM, Litoff D, Shaper NL, Shaper JH, Shur D, Receptor function of mouse sperm surface galactosyltransferase during fertilization. J Cell Biol 1985; 101: 1501–1510.PubMedGoogle Scholar
  61. Macek MB, Lopez LC, Shur BD, Aggregation of β-1,4-galactosyltransferase on mouse sperm induces the acrosome reaction. Developmental Biol 1991; 147: 440–444.Google Scholar
  62. McLaughlin JD, Shur BD, Binding of caput epididymal sperm to the zona pellucida. Developmental Biol 1987; 124: 557–561.Google Scholar
  63. Miranda PV, Tézon JG, Characterization of fibronectin as a marker for human epididymal sperm maturation. Molec Reprod Develop 1992; 33: 443–450.Google Scholar
  64. Mongkolsirikieat S, Boonsaeng V, Increase in sperm type hexokinase activity of rat spermatozoa during maturation. Int J Androl 1980; 3: 671–678.PubMedGoogle Scholar
  65. Nagdas SK, Skudlarek MD, Orgebin-Crist M-C, Tulsiani DRP, Biochemical alterations in the proacrosinacrosin system during epididymal maturation of the rat spermatozoa. J Androl 1992; 13: 36–43.PubMedGoogle Scholar
  66. 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.PubMedGoogle Scholar
  67. Okamura N, Tajima Y, Sugita Y, Decrease in bicarbonate transport activities during epididymal maturation of porcine sperm. Biochem Biophys Res Commun 1988; 157: 1280–1287.PubMedGoogle Scholar
  68. Okamura N, Onoe S, Sugita Y, Paquignon M, Dacheux F, Dacheux L, Water insoluble fraction of egg yolk maintains porcine sperm motility by activating adenylate cyclase. Mol Reprod and Develop 1991; 28: 136–142.Google Scholar
  69. Oliphant G, Reynolds AB, Thomas TS, Sperm surface components involved in the control of the acrosome reaction. Am J Anat 1985; 174: 269–283.PubMedGoogle Scholar
  70. Olson LM, Zhou X, Schreiber JR, Immunolocalization of apolipoprotein E in the testis and epididymis of the rat. Biol Reprod 1994, 50:535–542.PubMedGoogle Scholar
  71. Ong DE, Chytil F, Presence of novel retinoic acid-binding proteins in the lumen of rat epididymis. Arch Biochem Biophys 1988; 267: 474–478.PubMedGoogle Scholar
  72. Paris F, Weinbauer GF, Blüm V, Nieschlag E. The effect of androgens and antiandrogens on the immunohistochemical localization of the androgen receptor in accessory reproductive organs of male rats. J Steroid Biochem Molec Biol 1994; 48: 129–137.PubMedGoogle Scholar
  73. Parks JE, Ehrenwald E. Cholesterol efflux from mammalian sperm and its potential role in capacitation. In: Bavister BD, Cummins J, Roldan ERS, eds. Fertilization in mammals. Serono Symposia, Norwell, 1990: 155–167).Google Scholar
  74. Parkkila S, Kauisto K, Kellokumpu S, Rajaniemi H, A high activity carbonic anhydrase isoenzyme (CAII) is present in mammalian spermatozoa. Histochemistry 1991; 95: 477–482.PubMedGoogle Scholar
  75. Perry ACF, Jones R, Hall L, Sequence analysis of monkey acrosin-trypsin inhibitor transcripts and their abundant expression in the epididymis. Biochem Biophys Acta 1993; 1172: 159–160.PubMedGoogle Scholar
  76. Perry ACF, Hall L, Bell AE, Jones R, Spermatozoa are the source of a phospholipid binding protin (PBP) found in rat rete testis fluid and epididymal secretions. J Reprod Fert, Abstract Series Number 13, 1994; abstract 99.Google Scholar
  77. Phelps BM, Myles DG, The guinea pig sperm plasma membrane protein, PH-20, reaches the surface via two transport pathways and becomes localized to a domain after an initial uniform distribution. Developmental Biology 1987; 123: 63–72.PubMedGoogle Scholar
  78. Phelps BM, Koppel DE, Primakoff P, Myles DG, Evidence that proteolysis of the surface is an initial step in the mechanism of formation of sperm cell surface domains. J Cell Biol 1990; 111: 1839–1847.PubMedGoogle Scholar
  79. Poirier GR, Robinson R, Richardson R, Hinds K, Clayton D, Evidence for a binding site on the sperm plasma membrane which recognises the murine zona pellucoda: a binding site on the sperm plasma membrane. Gamete Res 1986; 14: 235–243.Google Scholar
  80. Porter SB, Ong DE, Chytil F, Orgebin-Crist MC, Localization of cellular retinol-binding protein and cellular retinoic acid binding protein in the rat testis and epididymis. J Androl 1985; 6: 197–212.PubMedGoogle Scholar
  81. Pöllänen P, Cooper TG, Immunology of the testicular excurrent ducts. J Reprod Immunol 1994; 26: 167–216.PubMedGoogle Scholar
  82. Primakoff P, Hyatt H, Myles DG, A role for the migrating sperm surface antigen PH-20 in guinea pig sperm binding to the egg zona pellucida. J Cell Biol 1985; 101: 2239–2244.PubMedGoogle Scholar
  83. Primakoff P, Hyatt H, Tredick-Kline J, Identification and purification of a sperm surface protein with a potential role in sperm-egg membrane fusion. J Cell Biol 1987; 104: 141–149.PubMedGoogle Scholar
  84. Prins GS, Zaneveld LJD, Contractions of the rabbit vas deferens following sexual activity: a mechanism for proximal transport of spermatozoa. Biol Reprod 1980; 23: 904–909.PubMedGoogle Scholar
  85. Rodriguez-Martinez H, Ekstedt E, Einarsson S, Acidification of epididymal fluid in the boar. Int J Androl 239-243:1990.Google Scholar
  86. Saling PM, Development of the ability to bind to zonae pellucidae during epididymal maturation: reversible immobilisation of mouse spermatozoa by lanthanum. Biol Reprod 1982; 26: 429–436.PubMedGoogle Scholar
  87. Saling PM, Bunch DO, Guen PL, Leyton L. ZP3-induced acrosomal exocytosis: a new model for triggering. In: Bavister BD, Cummins J, Roldan ERS, eds. Fertilization in mammals. Serono Symposia, Norwell, 1990: 239–252).Google Scholar
  88. Schlegel RA Hammerstedt R, Cofer GP, Kozarsky K, Freidus D, Williams P, Changes in the organization of the lipid bilayer of the plasma membrane during spermatogenesis and epididymal maturation. Biol Reprod 1986; 34: 379–391.PubMedGoogle Scholar
  89. Schoysman R, Vanderzwalmen P, Nijs M, Segal L, Segal-Bertin G, Geerts L, van Roosendaal E, Schoysman D, Pregnancy after fertilisation with human testicular spermatozoa. Lancet 1993a; 342:1236.Google Scholar
  90. Schoysman R, Vanderzwalmen P, Nijs M, Segal-Bertin G, van de, Casseye M, Successful fertilization by testicular spermatozoa in an in vitro fertilization programme. Human Reproduction 1993b; 8:1339–1340.PubMedGoogle Scholar
  91. Scully NF, Shaper JH, Shur BD, Spatial and temporal expresion of cell surface galactosyltransferase during mouse spermatogenesis and epididymal maturation. Develop Biol 1987; 124: 111–124.PubMedGoogle Scholar
  92. Seligman J, Kosower NS, Shalgi R, Effects of caput ligation of rat sperm and epididymis: protein thiols and fertilizing ability. Biol Reprod 1992; 43: 301–308.Google Scholar
  93. Shur BD, Hall NG, A role for mouse sperm surface galactosyltransferase in sperm binding to the egg zona pellucida. J Cell Biol 1982; 95: 574–579.PubMedGoogle Scholar
  94. Singh JP, Babcock DF, Lardy HA, Increased calcium-ion influx is a component is capacitation of spermatozoa. Biochem J 1978; 172: 549–556.PubMedGoogle Scholar
  95. Sosa MA, Barbieri MA, Bertini F, Binding of β-galactosidase from rat epididymal fluid to the sperm surface by high-affinity sites different from phosphomannosyl receptors. J Reprod Fert 1991; 93: 279–285.Google Scholar
  96. Suarez SS, Varosi SM, Dai XB, Intracellular calcium increases with hyperactivation in intact, moving hamster sperm and oscillates with the flagellar beat cycle. Proc Natl Acad Sci US 1993; 90: 4660–4664.Google Scholar
  97. Sujarit S, Jones RC, Setchell BP, Chaturapanich G, Lin M, Clulow J, Stimulation of protein secretion in the initial segment of the rat epididymis by fluid from the ram rete testis. J Reprod Fert 1990; 88: 315–321.Google Scholar
  98. Suzuki F, Changes in the distribution of intramembranous particles and filipin-sterol complexes during epididymal maturation of golden hamster spermatozoa. J Ultrastructure and Molec Struct Res 1988; 100: 39–54.Google Scholar
  99. Takano H, Yanagimachi R, Urch UA, Evidence that acrosin activity is important for the development of fusibility of mammalian spermatozoa with the oolemma: inhibitor studies using the golden hamster. Zygote 1993; 1: 79–91.PubMedGoogle Scholar
  100. Talo A, In-vitro electrical activity of rat efferent ductules. J Reprod Fert 1981; 63: 17–20.Google Scholar
  101. Töpfer-Peterson E, Henschen A, Zona pellucida-binding and fucose binding of boar sperm acrosin is not correlated with proteolytic activity. Bioch Chem Hoppe-Seyler 1988; 369: 69–76.Google Scholar
  102. Toshimori K, Higashi R, Oura C, Distribution of intramembranous particles and filipin-sterol complexes in mouse sperm membranes: polyene antibiotic filipin treatment. Am J Anat 1985; 174: 455–470.PubMedGoogle Scholar
  103. Toshimori K, Higashi R, Oura C, Filipin-sterol complexes in golden hamster sperm membranes with special reference to epididymal maturation. Cell Tiss Res 1987; 250: 673–680.Google Scholar
  104. Turner TT, Gleavy JL, Harris JM, Fluid movement in the lumen of the rat epididymis: effect of vasectomy and subsequent vasovasostomy. J Androl 1990; 11: 422–428.PubMedGoogle Scholar
  105. Uehora T, Yanagimachi R, Behaviour of nuclei of testicular, caput and cauda epididymal spermatozoa injected into hamster eggs. Biol Reprod 1977; 16: 315–321.Google Scholar
  106. Vanderhaeghen P, Schurmans S, Vassart G, Parmentier M, Olfactory receptors are displayed on dog mature sperm cells. J Cell Biol 1993; 123: 1441–1452.PubMedGoogle Scholar
  107. Velazquez A, Rosado A, Rosado A, Participation of vitamin A in the maturation of rabbit spermatozoa. Int J Fert 1975; 20: 151–155.Google Scholar
  108. Vierula ME, Araki Y, Rankiin TL, Tulsiani DRP, Orgebin-Crist M-C, Immunolocalization of a 25-kilodalton protein in mouse testis and epididymis. Biol Reprod 1992; 47: 844–856.PubMedGoogle Scholar
  109. Weyand I, Goddie M, Frings S, Weiner J, Mueller F, Altenhofen, Hatt H, Kaupp B, Cloning and functional expression of a cyclic-nucleotide-gated channel from mammalian sperm. Nature 1994; 368: 859–863.PubMedGoogle Scholar
  110. Winet H, On the mechanism for flow in the efferent ducts. J Androl 1980; 1: 304–311.Google Scholar
  111. Wolf DE, Voglmayr JK, Diffusion and regionalization in membranes of maturing ram spermatozoa. J Cell Biol 1984; 98: 1678–1684.PubMedGoogle Scholar
  112. Wolf DE, McKinton CA, Leyton L, Lakoski LK, Saling PM, Protein dynamics in sperm membranes: implications for sperm function during gamete interaction. Molec Reprod Develop 1992; 33: 228–234.Google Scholar
  113. Wong PYD, Lee WM, Tsang AYF, The effects of extracellular sodium on acid release and motility initiation on rat caudal epididymal spermatozoa in vitro. Exp Cell Res 1981; 131: 97–104.PubMedGoogle Scholar
  114. Wong PYD, Control of anion and fluid secretion by apical P2-purinoceptors in the rat epididymis. Br J Pharm 1988; 95: 1315–1321.Google Scholar
  115. Wong PYD, Physiology and pathophysiology of electrolytes transport in the epididymis. In: Nieschlag, E; Habenicht, U-F (eds). Spermatogenesis, Fertilization, Contraception. Molecular, cellular and endocrine events in male reproduction. Schering Foundation Workshop 4, Springer Verlag, Berlin, 1992: 319–344.Google Scholar
  116. Wong PYD, Uchendu CN, The role of angiotensin-converting enzyme in the rat epididymis. J Endocrinol 1990; 125: 457–465.PubMedGoogle Scholar
  117. Wong PYD, Uchendu CN, Studies on the renin-angiotensin system in primary monolayer cell cultures of the rat epididymis. J Endocrinol 1991; 131: 287–293.PubMedGoogle Scholar
  118. Wong PYD, Fu WO, Huang SJ, Law WK, Effect of angiotensins on electrogenic anion transport in monolayer cultures of rat epididymis. J Endocrinol 1990; 125: 449–456.PubMedGoogle Scholar
  119. Yanagida K, Bedford JM, Yanagimachi R, Cleavage of rabbit eggs after microsurgical injection of testicular spermatozoa. Human Reproduction 1991; 6: 277–279.PubMedGoogle Scholar
  120. Yeung CH, Cooper TG, Bergmann M, Schulze H, Organization of tubules in the human caput epididymidis and the ultrastructure of their epithelia. Am J Anat 1991; 191:261–279.PubMedGoogle Scholar
  121. Yeung CH, Nashan D, Cooper TG, Sorg C, Oberpenning F, Schulze H, Nieschlag E. Basal cells of the human epididymis — antigenic and ultrastructural similarities to tissue-fixed macrophages. Biol Reprod 1994; 50: 917–926.PubMedGoogle Scholar
  122. Zimmerman KJ, Crabo BG, Moore R, Weisberg S, Diebel FC, Graham EF, Movements of sodium and potassium into epididymal boar spermatozoa. Biol Reprod 1979; 21: 173–179.PubMedGoogle Scholar
  123. Zoppi S, Lechuga M, Motta M, Selective inhibition of the 5α-reductase of the rat epididymis. J Steroid Biochem 1992; 42: 509–514.Google Scholar

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© Springer Science+Business Media New York 1995

Authors and Affiliations

  • T. G. Cooper
    • 1
  1. 1.Institute of Reproductive Medicine of the UniversityMünsterGermany

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