Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-09T19:46:12.612Z Has data issue: false hasContentIssue false
  • English
  • Français

The epididymal influence on sperm maturation

Published online by Cambridge University Press:  03 June 2009

Trevor G Cooper
Trevor G Cooper*
Affiliation:
Institute of Reproductive Medicine of the University, Münster, Germany
*
Institute of Reproductive Medicine at the University, Steinfurter Strasse 107, D-48149 Münster, Germany.
Get access Rights & Permissions [Opens in a new window]

Extract

Consideration of the function of the epididymis has undergone profound changes over the last century during which it has moved from a largely neglected male reproductive organ to one that is an increasingly exploited source of sperm for assisted reproduction strategies. From histological studies in the lizard1 it was considered that, ‘…the cells lining the epididymal canal produce a material necessary for the spermatozoa during their passage through the organ …’ whereas a fertility study with guinea-pigs stated boldly that, ‘… changes undergone [by spermatozoa in the epididymis] are not conditioned by some specific action of epididymal secretion …’. The former view found favour in a review of the literature which concluded that, ‘… there are specific epididymal secretions necessary for sperm maturation and survival …’, although the nature of the secretions were not then known. However, this concept, currently held by most of those studying the epididymis of animals, was again contradicted on the basis of clinical work: ‘… it certainly is possible for sperm that have never passed through any length of the epididymis at all to mature on their own …’.

Type
Articles
Information
Reproductive Medicine Review , Volume 4 , Issue 3 , October 1995 , pp. 141 - 161
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1van der Stricht, O. La signification des cellules epitheliales de l'epididymis de Lacerta vivipara. CR Soc Biol 1893; 45: 799–801.Google Scholar
2Young, WC. 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 1931; 8: 151–62.CrossRefGoogle Scholar
3Orgebin-Crist, M-C, Danzo, BJ, Cooper, TG. Reexamination of the dependence of epididymal sperm viability on the epididymal environment. J Reprod Fertil 1976; (suppl 24): 115–28.Google Scholar
4Silber, SJ. Pregnancy caused by sperm from vasa efferentia. Fertil Steril 1988; 49: 373–75.CrossRefGoogle ScholarPubMed
5Adler, L, Makris, A. Successful artificial insemination with macerated testicular tissue. Fertil Steril 1951; 2: 459–61.CrossRefGoogle ScholarPubMed
6Craft, I, Bennet, V, Nicholson, N. Fertilising ability of testicular spermatozoa. Lancet 1993; 342: 864.CrossRefGoogle ScholarPubMed
7Hirsch, A, Montgomery, J, Mohan, P, Mills, C, Bekir, J, Tan, S-L. Fertilisation by testicular sperm with standard IVF techniques. Lancet 1993; 342: 1237–38.CrossRefGoogle Scholar
8Oates, RD, Honig, S, Berger, MJ, Harris, D. Microscopic epididymal sperm aspiration (MESA): a new option for treatment of the obstructive azoospermia associated with cystic fibrosis. J Assist Reprod Genet 1992; 9: 36–40.CrossRefGoogle Scholar
9Olar, TT, La, Nasa J, Dickey, RP, Taylor, SN, Curole, DN. Fertilization of human oocytes by microinjection of human sperm aspirated from the caput epididymidis of an individual with obstructive azoospenuia. J In Vitro Fert Embryo Transfer 1990; 7: 160–64.CrossRefGoogle Scholar
10Schoysman, R, Vanderzwalmen, P, Nijs, M et al. Pregnancy after fertilisation with human testicular spermatozoa. Lancet 1993; 342: 1236.CrossRefGoogle ScholarPubMed
11Schoysman, R, Vanderzwalmen, P, Nijs, M, van de Segal-Bertin, G, Casseye, M. Successful fertilization by testicular spermatozoa in an in vitro fertilization programme. Hum Reprod 1993; 8: 1339–40.CrossRefGoogle Scholar
12Tournaye, H, Nagy, Z, Devroey, P et al. Microsurgical epididymal sperm aspiration and intracytoplasmic sperm injection: a new effective approach to infertility as a result of congenital bilateral absence of the vas deferens. Fertil Steril 1994; 61: 1045–51.CrossRefGoogle ScholarPubMed
13Silber, SJ, Nagy, ZP, Liu, J et al. Conventional in vitro fertilization versus intracytoplasmic sperm injection for patients requiring microsurgical sperm aspiration. Hum Reprod 1994; 9: 1705–709.CrossRefGoogle ScholarPubMed
14Devroey, P, Liu, J, Nagy, Z et al. Normal fertilization of human oocytes after testicular sperm extraction and intracytoplasmic sperm injection. Fertil Steril 1994; 62: 639–41.CrossRefGoogle ScholarPubMed
15Silber, SJ, Van Steirteghem, AC, Liu, J, Nagy, Z, Tournaye, H, Devroey, P. High fertilisation and pregnancy rates after intracytoplasmic sperm injection with spermatids obtained from testicle biopsy. Hum Reprod 1995; 10: 148–52.CrossRefGoogle Scholar
16Bedford, JM. The status and state of the human epididymis. Hum Reprod 1994; 9: 2187–99.CrossRefGoogle ScholarPubMed
17Huszar, G. Sperm creatine kinase: a bridge among sperm maturity, morphology, Iipid peroxidation and fertility. Biochemist 1994; 16: 15–21.Google Scholar
18Porta, R, Esposito, C, De Santism, A et al. Sperm maturation in human semen: role of transglutaminase - mediated reactions. Biol Reprod 1986; 35: 965–70.CrossRefGoogle ScholarPubMed
19Babcock, DF, Singh, JP, Lardy, HA. Alteration of membrane permeability to calcium ions during maturation of bovine spermatozoa. Dev Biol 1979; 69: 85–93.CrossRefGoogle ScholarPubMed
20Cooper, TG. The epididymis, sperm maturation and fertilisation. Heidelberg: Springer Verlag, 1986.CrossRefGoogle Scholar
21Schirren, C. Gewebsentnahme aus dem Nebenhoden zu diagnostischen Zwecken? Andrologia 1982; 14: 461–62.CrossRefGoogle Scholar
22Fogdestam, I, Fall, M, Nilsson, S. Microsurgical epididymovasostomy in the treatment of occlusive azoospermia. Fertil Steril 1986; 46: 925–29.CrossRefGoogle ScholarPubMed
23Marshall, FF, Chang, T, Vindivich, D. Microsurgical vasoepididymostomy to corpus epididymidis in treatment of inflammatory obstructive azoospermia. Urology 1987; 30: 565–67.CrossRefGoogle ScholarPubMed
24Schmidt, SS, Schoysman, R, Stewart, BH. Surgical approaches to male infertility. In: Hafez, ESE ed. Human semen and fertility regulation in men. St Louis, MO: Moseby, 1976:476–93.Google Scholar
25Schoysman, RJ, Bedford, JM. The role of the human epididymis in sperm maturation and sperm storage as reflected in the consequences of epididymovasostomy. Fertil Steril 1986; 46: 293–99.CrossRefGoogle ScholarPubMed
26Silber, SJ. Results of microsurgical vasoepididymostomy: role of epididymis in sperm maturation. Hum Reprod 1989; 4: 298–303.CrossRefGoogle ScholarPubMed
27Silber, SJ. Role of epididymis in sperm maturation, Urology 1989; 33: 47–51.CrossRefGoogle ScholarPubMed
28Silber, SJ. Apparent fertility of human sperm from the caput epididymis. J Reprod Immunol 1988: 88: 895–900.Google Scholar
29Silber, SJ. Apparent fertility of human spermatozoa from the caput epididymidis. J Androl 1988; 10: 263–69.CrossRefGoogle Scholar
30Weiske, W-H.Pregnancy caused by sperm from the vasa efferentia. Fertil Steril 1994; 62: 642–43.CrossRefGoogle ScholarPubMed
31Schoysman, R. Clinical situations challenging the established concept of epididymal physiology in the human. Acta Eur Fertil 1993; 24: 55–60.Google ScholarPubMed
32Cooper, TG. The human epididymis - is it necessary? Int J Androl 1993; 16: 245–50.CrossRefGoogle ScholarPubMed
33Rajalakshmi, M, Kumar, BVR, Kapur, MM, Pal, PC. Ultrastructural changes in the efferent duct and epididymis of men with obstructive infertility. Anat Rec 1993; 237: 199–207.CrossRefGoogle ScholarPubMed
34Temple-Smith, PD, Southwick, GJ, Herrera, Castaneda E, Hamer, J, McClatchey, M. Surgical manipulation of the epididymis: an experimental approach to sperm maturation. In: Serio, M ed. Perspectives in andrology. New York, NY: Raven Press, 1989:281–90.Google Scholar
35Cooper, TG. In defense of a function for the human epididymis. Fertil Steril 1990; 90: 965–75.Google Scholar
36Wong, PYD, Tsang, AYF, Wang, C. Absence of a sperm coating protein after epididymovasostomy. J Androl 1982; 3: 205–208.CrossRefGoogle Scholar
37Cooper, TG, Yeung, CH, Nashan, D, Jockenhövel, F, Nieschlag, E. Improvement in the assessment of human epididymal function by the use of inhibitors in the assay of α-glucosidase in seminal plasma. Int J Androl 1990; 13: 297–305.CrossRefGoogle ScholarPubMed
38Kirchhoff, C, Habben, I, Ivell, R, Krull, N. A major human epididymis-specific cDNA encodes a protein with sequence homology to extracellular proteinase inhibitors. Biol Reprod 1991; 45: 350–57.CrossRefGoogle Scholar
39Hodges, RD, Hanley, HG. Epididymo-vasostomy: a microdissection study of two cases. Br J Urol 1966; 38: 534–41.CrossRefGoogle ScholarPubMed
40Silber, SJ, Ord, T, Balmaceda, J, Aschm, R, Borrero, C. Pregnancy with sperm aspiration from the proximal head of the epididymis: a treatment for congenital absence of the vas deferens. Fertil Steril 1988; 50: 525–28.CrossRefGoogle ScholarPubMed
41Silber, SJ, Ord, T, Balmaceda, J, Patrizio, P, Asch, RH. Congenital absence of the vas deferens. The fertilizing capacity of human epididymal sperm. N Engl J Med 1990; 323: 1788–92.CrossRefGoogle ScholarPubMed
42Cooper, TG, Raczek, S, Yeung, CH, Schwab, E, Schulze, H, Hertle, L. Composition of fluids obtained from human epididymal spermatocoeles. Urol Res 1992; 20: 275–280.CrossRefGoogle Scholar
43Jow, WW, Steckel, J, Schlegel, PN, Magid, MS, Goldstein, M. Motile sperm in human testis biopsy specimens. J Androl 1993; 14: 194–98.CrossRefGoogle ScholarPubMed
44Patrizio, P, Ord, T, Silber, SJ, Asch, RH. Cystic fibrosis mutations impair the fertilization rate of epididymal sperm from men with congenital absence of the vas deferens. Hum Reprod 1993; 8: 1259–63.CrossRefGoogle ScholarPubMed
45Schlegel, PN, Alikani, M, Berkeley, AS et al. Epididymal micropuncture with in vitro fertilization and oocyte micromanipulation for the treatment of unreconstructable obstructive azoospermia. Fertil Steril 1994; 61: 895–901.CrossRefGoogle ScholarPubMed
46Patrizio, P, Ord, T, Silber, SJ, Asch, RH. Correlation between epididymal length and fertilization rate of men with congenital absence of the vas deferens. Fertil Steril 1994; 61: 265–68.CrossRefGoogle ScholarPubMed
47Aitken, RJ, Ross, A, Lees, ML. Analysis of sperm function in Kartagener's Syndrome. Fertil Steril 1983;40: 696–98.CrossRefGoogle ScholarPubMed
48Bedford, JM, Calvin, H, Cooper, GW. The maturation of spermatozoa in the human epididymis. J Reprod Fertil 1973; (suppl 18): 199–213.Google Scholar
49Haidl, G, Badura, B, Schill, W-B. Function of human epididymal spermatozoa. J Androl 1994; 15: 23S–27S.CrossRefGoogle ScholarPubMed
50Yeung, CH, Cooper, TG, Oberpenning, F, Schulze, H, Nieschlag, E. Changes in movement characteristics of human spermatozoa along the length of the epididymis. Biol Reprod 1993; 49: 274–80.CrossRefGoogle ScholarPubMed
51Mortimer, D. Laboratory standards in routine clinical andrology. Reprod Med Rev 1994, 3: 97–111.CrossRefGoogle Scholar
52Yeung, CH. Development of sperm motility. In: Hamamah, S, Mieusset, R, Dacheux, JL eds. Frontiers in endocrinology. Epididymis: role and importance in male infertility treatment. Rome: Ares Serono Symposia, 1995: 73–86.Google Scholar
53Rojas, FJ, Patrizio, P, Do, J et al. Evidence for a novel adenylyl cyclase in human epididymal sperm. Endocrinology 1993; 133: 3030–33.CrossRefGoogle ScholarPubMed
54Haidl, G, Badura, B, Hinsch, K-D, Ghyczy, M, Gareiß, J, Schill, W-B. Disturbances of sperm flagella due to failure of epididymal maturation and their possible relationship to phospholipids. Hum Reprod 1993; 8: 1070–73.CrossRefGoogle ScholarPubMed
55Chang, MC. The meaning of sperm capacitation: a historical perspective. J Androl 1984; 5: 45–50.CrossRefGoogle ScholarPubMed
56Bedford, JM. Significance of the need for sperm capacitation before fertilization in Eutherian mammals. Biol Reprod 1983; 28: 108–20.CrossRefGoogle ScholarPubMed
57Oliphant, G, Reynolds, AB, Thomas, TS. Sperm surface components involved in the control of the acrosome reaction. Am J Anat 1985; 174: 269–83.CrossRefGoogle ScholarPubMed
58Go, KJ, Wolf, DP. The role of sterols in sperm capacitation. Adv Lipid Res 1983; 20: 317–30.Google ScholarPubMed
59Parks, 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. Norwell: Serono Symposia, 1990:155–67.Google Scholar
60Hunter, RHF, Holtz, W, Henfrey, PJ. Epididymal function in the boar in relation to the fertilizing ability of spermatozoa. J Reprod Fertil 1976; 46: 463–66.CrossRefGoogle Scholar
61Yanagimachi, R. Zona-free hamster eggs: their use in assessing fertilizing capacity and examining chromosomes of human spermatozoa. Gamete Res 1984; 10: 187–232.CrossRefGoogle Scholar
62Cooper, TG. Functions of the human epdidymis. In: Hamamah, S, Mieusset, R, Dacheux, JL eds. Frontiers in endocrinology. Epididymis: role and importance in male infertility treatment. Rome: Ares Serono Symposia, 1995:1–12.Google Scholar
63Hoshi, K, Aita, T, Yangagida, K, Yoshimatsu, N, Sato, A. Variation in the cholesterol/phospholipid ratio in human spermatozoa and its relationship with capacitation. Hum Reprod, 1990; 5: 71–74.CrossRefGoogle ScholarPubMed
64Langlais, J, Zollinger, M, Plante, L et al. Localization of cholesteryl sulfate in human spermatozoa in support of a hypothesis for the mechanism of capacitation. Proc Natl Acad Sci USA 1981; 78: 7266–70.CrossRefGoogle ScholarPubMed
65Menezo, Y, Testart, J, Khatchadourian, C, Frydman, R. Human preovulatory follicular fluid: the lipids. Are they the trigger for capacitiation? Int J Fertil 1984; 29: 61–64.Google Scholar
66Langlais, J, Kan, FWK, Granger, L et al. Identification of sterol acceptors that stimulate cholesterol efflux from human spermatozoa during in vitro capacitation. Gamete Res 1988; 20: 185–201.CrossRefGoogle ScholarPubMed
67Ravnik, AE, Zarutskie, PW, Muller, CH. Lipid transfer activity in human follicular fluid: relation to human sperm capacitation. J Androl 1990; 11: 216–26.CrossRefGoogle ScholarPubMed
68Ravnik, SE, Zarutskie, PW, Muller, CH. Purification and characterization of a human follicular fluid lipid transfer protein that stimulates human sperm capacitation. Biol Reprod 1992; 47: 1126–33.CrossRefGoogle ScholarPubMed
69Ravnik, SE, Albers, JJ, Muller, CH. A novel view of albumen-supported sperm capacitation: role of lipid transfer protein-I. Fertil Steril 1993; 59: 629–38.CrossRefGoogle ScholarPubMed
70Cross, NL, Morales, P, Overstreet, JW, Hanson, FW. Induction of acrosome reactions by the human zona pellucida. Biol Reprod 1988; 38: 235–44.CrossRefGoogle ScholarPubMed
71Phillips, DM. Structure and function of the zona pellucida. In: Familiari, G, Makabem, S, Motta, PM eds. Ultrastructure of the ovary. The Hague: Kluwer Academic Press, 1991: 63–72.CrossRefGoogle Scholar
72Wassarman, PM. Regulation of mammalian fertilization by gamete adhesion molecules. In: Nieschlag, E, Habenicht, U-F eds. Spermatogenesis, fertilization, contraception. Molecular, cellular and endocrine events in male reproduction. Berlin: Springer Verlag, 1992: 345–66.CrossRefGoogle Scholar
73Jones, R, Brown, CR. Identification of a zona-binding protein from boar spermatozoa as proacrosin. Exp Cell Res 1987; 171: 503–508.CrossRefGoogle ScholarPubMed
74Töpfer-Peterson, E, Henschen, A. Acrosin show zona and fucose binding, novel properties for a serine protease. FEBS Lett 1987; 226: 38–42.CrossRefGoogle Scholar
75Eberspächer, U, Donner, P. Characterization of inhibitory and stimulatory effects of zona pellucida glycoproteins on the proacrosin/acrosin system. In: Nieschlag, E, Habenicht, U-F eds. Spermatogenesis, fertilization, contraception. Molecular, cellular and endocrine events in male reproduction. Berlin: Springer, 1992: 383–94.CrossRefGoogle Scholar
76Tesarik, J, Drahorad, J, Peknicova, J. Subcellular immunochemical localization of acrosin in human spermatozoa during the acrosome reaction and zona pellucida penetration. Fertil Steril 1988; 50: 133–41.CrossRefGoogle ScholarPubMed
77Baba, T, Azuma, S, Kashiwabara, S-I, Toyada, Y. Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J Biol Chem 1994; 269: 31845–49.CrossRefGoogle ScholarPubMed
78Delpech, S, Lecomte, P, Lecomte, C. Étude in vitro chèz l'homme de la liason des spermatozoïdes èpididymaires à la zona pellucida. J Gynecol Obstet Biol Reprod (Paris) 1988; 17: 339–42.Google Scholar
79Sating, PM. Development of the ability to bind to zonae pellucidae during epididymal maturation: reversible immobilisation of mouse spermatozoa by lanthanum. Biol Reprod 1982; 26: 429–36.Google Scholar
80McLaughlin, JD, Shur, BD. Binding of caput epdidymal mouse sperm to the zona pellucida. Dev Biol 1987; 124: 557–61.CrossRefGoogle Scholar
81Kawai, 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 Pharmacol 1991; 14: 231–36.Google ScholarPubMed
82Biegler, BE, Aarons, DJ, George, BC, Poirier, GR. Induction of physiological acrosome reactions in caput epididymal spermatozoa of mice. J Reprod Fertil 1994; 100: 219–24.CrossRefGoogle ScholarPubMed
83Irwin, M, Nicholson, N, Haywood, JT, Poirier, GR. Immunological localization of a murine seminal vesicle proteinase inhibitor. Biol Reprod 1983; 28: 1201–206.CrossRefGoogle Scholar
84Poirier, GR, Robinson, R, Richardson, R, Hinds, K, Clayton, D. Evidence of a binding site on the sperm plasma membrane which recognises the murine zona pellucida: a binding site on the sperm plasma membrane. Gamete Res 1986; 14: 235–43.CrossRefGoogle Scholar
85Lopez, LC, Bayna, EM, Litoff, D et al. Receptor function of mouse sperm surface galactosyltransferase during fertilization. J Cell Biol 1985; 101: 1501–10.CrossRefGoogle ScholarPubMed
86Nagdas, SK, Araki, Y, Chayko, CA, Orgebin-Crist, MC, Tulsiani, RP. O-linked trisaccharide and relinked poly-N-acetyllactosaminyl glycans are present on mouse ZP2 and ZP3. Biol Reprod 1994; 51: 262–72.CrossRefGoogle Scholar
87Shur, BD, Hall, NG. A role for mouse sperm surface galactosyltransferase in sperm binding to the egg zona pellucida. J Cell Biol 1982; 95: 574–79.CrossRefGoogle Scholar
88Scully, NF, Shaper, JH, Shur, BD. Spatial and temporal expression of cell surface galactosyltransferase during mouse spermatogenesis and epididymal maturation. Dev Biol 1987; 124: 111–24.CrossRefGoogle ScholarPubMed
89Youakim, HJ, Miller, DJ, Gong, X, Shuir, TD. Overexpressing sperm surface β1,4-galactosyltransferase in transgenic mice affects multiple aspects of sperm-egg interactions. J Cell Biol 1994; 126: 1573–83.CrossRefGoogle Scholar
90Ross, P, Vigneault, N, Provencher, S, Potier, M, Roberts, KD. Partial characterization of galactosyltransferase in human seminal plasma and its distribution in the human epididymis. J Reprod Fertil 1993; 98: 129–37.CrossRefGoogle ScholarPubMed
91Tulsiani, DRP, Skudlarek, MD, Orgebin-Crist, MC. Human sperm plasma membranes possess α-D-mannosidase activity but no galactosyltransferase activity. Biol Reprod 1990; 42: 843–58.CrossRefGoogle ScholarPubMed
92Tulsiani, DRP, Nagdas, SK, Cornwall, GA, Orgebin-Crist, M-C. Evidence for the presence of high-mannose/hybrid oligosaccharide chain(s) on the mouse ZP2 and ZP3. Biol Reprod 1992; 46: 93–100.CrossRefGoogle ScholarPubMed
93Cornwall, GA, Tulsiani, DRP, Orgebin-Crist, M-C. Inhibition of the mouse sperm surface α-D-mannosidase inhibits sperm-egg binding in vitro. Biol Reprod 1991; 44: 913–21.CrossRefGoogle ScholarPubMed
94Tulsiani, DRP, Cornwall, GA, Skudlarek, MD, Orgebin-Crist, M-C. Increase in sperm plasma membrane α-D-mannosidase correlates with the development of sperm binding ability. In: Baccetti, B ed. Comparative spermatology. New York, NY: Raven Pres, 1991:703–707.Google Scholar
95Primakoff, 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: 2239–44.CrossRefGoogle Scholar
96Lathrop, WF, Carmichael, EP, Myles, AG, Primakoff, D. cDNA cloning reveals the molecular structure of a sperm surface protein, PH-20, involved in spermegg adhesion and the wide distribution of its gene among mammals. J Cell Biol 1990; 111: 2939–49.CrossRefGoogle ScholarPubMed
97Gmachl, M, Kreil, G. Bee venom hyaluronidase is homologous to a membrane protein of mammalian sperm. Proc Natl Acad Sci USA; 90: 3569–73.CrossRefGoogle Scholar
98Gacesa, P, Civill, ND, Harrison, RAP. PH-20 and sperm hyaluronidase: a conceptual conundrum in mammalian fertilization. Biochem J 1994; 303: 335–36.CrossRefGoogle ScholarPubMed
99Lewin, LM, Nevo, Z, Gabsu, A, Weissenberg, R. The role of sperm-bound hyaluronidase in the dispersal of the cumulus oophorus surrounding rat ova. Int J Androl 1982; 5: 37–44.CrossRefGoogle ScholarPubMed
100Lin, 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: 1157–63.CrossRefGoogle ScholarPubMed
101Dandekar, P, Aggeler, J, Talbot, P. Structure, distribution and composition of the extracellular matrix of human occytes and cumulus masses. Hum Reprod 1992; 7: 391–98.CrossRefGoogle Scholar
102Talbot, P. Hyaluronidase dissolves a component in the hamster zona pellucida. J Exp Zool 1984; 229: 309–16.CrossRefGoogle ScholarPubMed
103Cooper, TG. Epididymal proteins and sperm maturation. In: Nieschlag, E, Habenicht, U-F eds. Spermatogenesis, fertilization, contraception. Molecular, cellular and endocrine events in male reproduction. Berlin: Springer Verlag, 1992: 285–318.CrossRefGoogle Scholar
104Phelps, 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: 1839–47.CrossRefGoogle ScholarPubMed
105Jones, R, Brown, CR, von Glos, KI, Gaunt, SJ. Development of a maturation antigen on the plasma membrane of rat spermatozoa in the epididymis and its fate during fertilization. Exp Cell Res 1985; 156: 31–44.CrossRefGoogle ScholarPubMed
106Kalabi, 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: 3810–17.CrossRefGoogle Scholar
107Bérubé, B, Sullivan, R. Inhibition of in vivo fertilization by active immunization of male hamsters against a 26-kDa sperm glycoprotein. Biol Reprod 1994; 51: 1255–63.CrossRefGoogle ScholarPubMed
108Boué, F, Bérubé, B, De Lamirande, E, Gagnon, C, Sullivan, R. Human sperm-zona pellucida interaction is inhibited by an antiserum against a hamster sperm protein. Biol Reprod 1994; 51: 577–87.CrossRefGoogle ScholarPubMed
109Fournier-Delpech, S, Holland, MK, Shudlarek, MD, Rankin, TL, Orgebin-Crist, MC, Courot, M. A ram epididymal secretory protein shares common antigenic determinants with rat epididymal proteins and human seminal plasma proteins. Reprod Nutr 1988; 28: 1283–99.CrossRefGoogle Scholar
110Orgebin-Crist, MC, Fournier-Delpech, S. Sperm-egg interactions. Evidence for maturational changes during epididymal transit. J Androl 1982; 3: 429–33.CrossRefGoogle Scholar
111Osterhoff, C, Kirchhoff, C, Krull, N, Ivell, R. Molecular cloning and characterization of a novel human sperm antigen (HE2) specifically expressed in the proximal epididymis. Biol Reprod 1994; 50: 516–25.CrossRefGoogle ScholarPubMed
112Hunter, DD, Porter, BE, Bulock, JW, Adams, SP, Merlie, JP, Sanes, JR. Primary sequence of a motorneuron selective adhesion site in the synaptic basal lamina protein s-laminin. Cell 1989; 59: 905–913.CrossRefGoogle Scholar
113Osterhoff, C, Lassalle, B, Finaz, C, Ivell, R, Kirchhoff, C. A secretory protein of the human epididymis appears to be involved in the gamete recognition process. J Reprod Fertil 1993; C31 (Abstract Series 12): 21.Google Scholar
114Yanagimachi, R, Phillips, DM. The status of acrosomal caps of hamster spermatozoa immediately before fertilization in vivo. Gamete Res 1984; 9: 1–19.CrossRefGoogle Scholar
115Anakwe, 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. Mol Reprod Dev 1991; 29: 294–301.CrossRefGoogle ScholarPubMed
116Nagdas, SK, Skudlarek, MD, Orgebin-Crist, M-C, Tulsiani, DRP. Biochemical alterations in the proacrosin-acrosin system during epididymal; maturation of the rat spermatozoa. J Androl 1992; 13: 36–43.CrossRefGoogle ScholarPubMed
117Meizel, S, Deamer, DW. The pH of the hamster sperm acrosome. J Histochem Cytochem 1978; 26: 98–105.CrossRefGoogle Scholar
118Singh, JP, Babcock, DF, Lardy, HA. Increased calcium -ion influx is a component is capacitation of spermatozoa. Biochem J 1978; 172: 549–56.CrossRefGoogle ScholarPubMed
119Lakoski, KA, Carron, CP, Cabot, CL, Saling, PM. Epididymal maturation and the acrosome reaction in mouse sperm: response to zona pellucida develops coincident with modifications of M42 antigen. Biol Reprod 1988; 38: 221–233.CrossRefGoogle ScholarPubMed
120Leyton, L, Saling, P. Evidence that aggregation of mouse sperm receptors by ZP3 triggers the acrosome reaction. J Cell Biol 1989; 108: 2163–68.CrossRefGoogle ScholarPubMed
121Aarons, D, Boettger-Tong, H, Holt, G, Poirier, GR. Acrosome reaction induced by immunoaggregation of a proteinase inhibitor bound to the murine sperm head. Mol Reprod Dev 1991; 30: 258–64.CrossRefGoogle Scholar
122Saling, 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. Norwell: Serono Symposia, 1990:239–52.Google Scholar
123Macek, MB, Lopez, LC, Shur, BD. Aggregation of β-1,4-galactosyltransferase on mouse sperm induces the acrosome reaction. Dev Biol 1991; 147: 440–44.CrossRefGoogle ScholarPubMed
124Williams, RM, Graham, JK, Hammerstedt, RH. Determination of the capacity of ram epididymal and ejaculated sperm to undergo the acrosome reaction and penetrate ova. Biol Reprod 1991; 44: 1080–91.CrossRefGoogle ScholarPubMed
125Graham, JK, Nolan, JP, Hammerstedt, RH. Effect of dilauroylphosphatidylcholine liposomes on motility, induction of the acrosome reaction and subsequent egg penetration of ram epididymal sperm. Biol Reprod 1991; 44: 1092–99.CrossRefGoogle ScholarPubMed
126Harayama, H, Kusunoki, H, Kato, S. Capacity of goat epididymal spermatozoa to undergo the acrosome reaction and subsequent fusion with the egg plasma membrane. Reprod Fertil Dev 1993; 7: a239–46.CrossRefGoogle Scholar
127Holt, WV, Dott, HM. Chemically induced fusion between ram spermatozoa and avian erythrocytes; an ultrastructural study. J Ultrastruct Res 1980; 71: 311–20.CrossRefGoogle ScholarPubMed
128Harayama, H, Kusonoki, H, Kato, S. Capacity of rete testicular and cauda epididymal boar spermatozoa to undergo the acrosome reaction and subsequent fusion with egg plasma membrane. Mol Reprod Dev 1993; 35: 62–68.CrossRefGoogle ScholarPubMed
129Sanchez, R, Töpfer-Peterson, E, Aitken, RJ, Schill, W-B. A new method for evaluation of the acrosome reaction in viable human spemiatozoa. Andrologia 1991; 23: 197–203.CrossRefGoogle Scholar
130Yanagimachi, R. Mammalian fertilization. In: Knobil, E, Neill, JD eds. The physiology of reproduction, second edition. New York, NY: Raven Press, 1994: 189–317.Google Scholar
131Lacham, O, Trounson, A. Fertilizing capacity of epididymal and testicular spermatozoa microinjected under the zona pellucida of the mouse oocyte. Mol Rep Dev 1991; 29: 85–93.CrossRefGoogle ScholarPubMed
132Hinrichsen, MJ, Blaquier, JA. Evidence supporting the existence of sperm maturation in the human epididymis. J Reprod Fertil 1980; 60: 291–94.CrossRefGoogle ScholarPubMed
133Sutherland, P, Maton, P, Moore, HDM et al. Clinical evaluation of the heterologous oocyte penetration (HOP) test. Br J Urol 1985; 57: 233–36.CrossRefGoogle ScholarPubMed
134Moore, HDM, Hartmann, TD, Pryor, JP. Development of the oocyte-penetrating capacity of spermatozoa in the human epididymis. Int J Androl 1983; 6: 310–18.CrossRefGoogle ScholarPubMed
135Primokoff, 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: 141–49.CrossRefGoogle Scholar
136Blobel, CR, Myles, DG, Primakoff, P, White, JM. Proteolytic processing of a protein involved in sperm-egg fusion correlates with acquisition of fertilization competence. J Cell Biol 1990; 111: 69–78.CrossRefGoogle ScholarPubMed
137Blobel, CP, Wolfsberg, TG, Turck, CW, Myles, DG, Primakoff, P, White, JM. A potential fusion peptide and an integrin ligand domain in a protein active in sperm-egg fusion. Nature 1992; 356: 248–52.CrossRefGoogle Scholar
138Perry, ACF, Jones, R, Barker, PJ, Hall, L. A mammalian epididymal protein with remarkable sequence similarity to snake venom haemorrhagic peptides. Biochem J 1992; 286: 671–75.CrossRefGoogle ScholarPubMed
139Bronson, RA, Fusi, F. Evidence that an Arg-Gly-Asp adhesion sequence plays a role in mammalian fertilization. Biol Reprod 1990; 43: 1019–25.CrossRefGoogle Scholar
140Fusi, FM, Vignall, M, Gailit, J, Bronson, RA. Mammalian oocytes exhibit specific recognition of RGD (arg-gly-asp) tripeptide and express oolemmal integrins. Mol Reprod Dev 1993; 36: 212–19.CrossRefGoogle ScholarPubMed
141Glander, H-J, Schaller, J. Expression von Adhäsionsmolekulen auf Humanspermien. Orientierende Untersuchungen. Fertilität 1992; 8: 136–40.Google Scholar
142Klentzeris, LD, Fishel, S, McDermott, H et al. A positive correlation between expression of pi-integrin cell adhesion molecules and fertilizing ability of human spermatozoa. Mol Hum Reprod 1995;10: 728–33.CrossRefGoogle ScholarPubMed
143Vuento, M, Kuusela, P, Virkki, M, Koskimies, A. Characterization of fibronectin on human spermatozoa. Hoppe Seylers Z Physiol Chem 1984; 365: 757–62.CrossRefGoogle ScholarPubMed
144Glander, HJ, Herrmann, K, Haustein, UF. The equatorial fibronectin bound (EFB) on human spermatozoa – a diagnostic help in male fertility. Andrologia 1987; 19: 456–59.CrossRefGoogle Scholar
145Fusi, FM, Bronson, RA. Sperm surface fibronectin. Expression following capacitation. J Androl 1992; 13: 28–31.CrossRefGoogle ScholarPubMed
146Fusi, FM, Lorenzetti, I, Vignali, M, Bronson, RA. Sperm surface proteins after capacitation. Expression of vitronectin on the spermatozoan head and laminin on the sperm tail. J Androl 1992; 13: 488–97.CrossRefGoogle ScholarPubMed
147Hoshi, K, Sasaki, H, Yanagida, K, Sato, A, Tsuiki, A. Localization of firbonectin on the surface of human spermatoyozoa and relation to the sperm-egg interaction. Fertil Steril 1994; 61: 542–47.CrossRefGoogle Scholar
148Lopez, LC, Shur, BD. Redistribution of mouse sperm surface galactosyltransferase after the acrosome reaction. J Cell Biol 1987; 105: 1663–70.CrossRefGoogle ScholarPubMed
149Cowan, AE, Primakoff, P, Myles, DG. Sperm exocytosis increases the amount of PH-20 antigen on the surface of guinea pig sperm. J Cell Biol 1986; 103: 1289–97.CrossRefGoogle ScholarPubMed
150Schaller, J, Glander, HJ, Dethloff, J. Evidence of β1 integrins and fibronectin on spermatogenic cells in human testis. Hum Reprod 1993; 8: 1873–78.CrossRefGoogle ScholarPubMed
151Miranda, PV, Tézon, JG. Characterization of fibronectin as a marker for human epididymal sperm maturation. Mol Reprod Dev 1992; 33: 443–50.CrossRefGoogle ScholarPubMed
152Rochwerger, L, Cuasnicú, PS. Redistribution of a rat sperm epididymal glycoprotein after in vitro and in vivo capacitation. Mol Reprod Dev 1992; 31: 34–41.CrossRefGoogle ScholarPubMed
153Kusunoki, H, Kato, S, Kanda, S. Induction of the acrosome reaction in goat spermatozoa in simple physiological salt solution. J Exp Zool 1989; 250: 346–48.CrossRefGoogle ScholarPubMed
154Free, MJ, Schluntz, GA, Jaffe, RA. Respiratory gas tensions in tissues and fluids of the male rat reproductive tract. Biol Reprod 1976; 14: 481–88.CrossRefGoogle ScholarPubMed
155Djakiew, D, Cardullo, R. Lower temperature of the cauda epididymidis facilitates the storage of sperm by enhancing oxygen availability. Gamete Res 1986; 15: 237–45.CrossRefGoogle Scholar
156Jones, R. Comparative biochemistry of mammalian epididymal plasma. Comp Biochem Physiol [B] 1978; 61B: 365–70.Google Scholar
157Yoseffi, S, Oschry, Y, Lewin, LM. Chromatin condensation in hamster sperm: a flow cytometric investigation. Mol Reprod Dev 1994; 37: 93–98.CrossRefGoogle Scholar
158Saowaros, W, Panyim, S. The formation of disulfide bonds in human protarnines during sperm maturation. Experientia 1979; 35: 191–92.CrossRefGoogle ScholarPubMed
159Uehora, T, Yanagimachi, R. Behaviour of nuclei of testicular, caput and cauda epididymal spermatozoa injected into hamster eggs. Biol Reprod 1977; 16: 315–21.CrossRefGoogle Scholar
160Yanagida, K, Bedford, JM, Yanagimachi, R. Cleavage of rabbit eggs after microsurgical injection of testicular spermatozoa. Hum Reprod 1991; 6: 277–79.CrossRefGoogle ScholarPubMed
161Van Steirteghem, AC, Nagy, Z, Liu, J et al. Embryo development after ICSI using testicular, epididymal and ejaculated spermatozoa. In: Hamamah, S, Mieusset, R, Dacheux, JL eds. Frontiers in endocrinology. Epididymis: role and importance in male infertility treatment. Rome: Ares Serono Symposia, 1995:141–47.Google Scholar
162Silber, SJ, Devroey, P, Van Steirteghem, AC. Fertilizing capacity of epididymal and testicular sperm with ICSI. In: Hamamah, S, Mieusset, R, Dacheux, JL eds. Frontiers in endocrinology. Epididymis: role and importance in male infertility treatment. Rome: Ares Serono Symposia, 1995: 129–40.Google Scholar
163Mieusset, R. Spermatozoa and embryo development. In: Hamamah, S, Mieusset, R, Dacheux, JL eds. Frontiers in endocrinology. Epididymis: role and importance in male infertility treatment. Rome: Ares Serono Symposia, 1995:105–28.Google Scholar
164Ariel, M, Cedar, H, McCarry, J. Developmental changes in methylation of spermatogenesis-specific genes include reprogramming in the epididymis. Nature Genetics 1994; 7: 59–63.CrossRefGoogle ScholarPubMed
165Liebaers, J, Bonduelle, M, Legein, J et al. Malformation rates from IVF and/or assisted fertilization with epididymal spermatozoa. In: Hamamah, S, Mieusset, R, Dacheux, JL eds. Frontiers in endocrinology. Epididymis: role and importance in male infertility treatment. Rome: Ares Serono symposia, 1995:169–74.Google Scholar
166Orgebin-Crist, M-C, NagDas, SK, Tulsiani, DRP. Modifications of putative sperm binding proteins for the zona pellucida during sperm maturation. In: Dufau, ML, Fabbri, A, Isidori, A eds. Cell and molecular biology of the testis. Rome: Ares Serono Symposia, 1994: 211–16.Google Scholar
167O'Brien, JS, Kishimoto, Y. Saposin proteins: structure, function, and role in human lysosomal storage disorders. FASEB J 1991; 5: 301–303.CrossRefGoogle ScholarPubMed
168Kirszbaum, L, Sharpe, JA, Murphy, B et al. Molecular cloning and characterization of the novel, human complement-associated protein, SP-40,40: a link between the complement and reproductive systems. EMBO J 1989; 8: 711–18.CrossRefGoogle ScholarPubMed
169Hermo, L, Oko, R, Morales, CR. Secretion and endocytosis in the male reproductive tract: role in sperm maturation. Int Rev Cytol 1994; 154: 105–89.CrossRefGoogle ScholarPubMed
170Jones, 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: 78–82.CrossRefGoogle Scholar
171Perry, ACF, Hall, L, Bell, AE, Jones, R. Sequence analysis of a mammalian phospholipid-binding protein from testis and epididymis and its distribution between spermatozoa and extracellular secretions. Biochem J 1994; 301: 235–42.CrossRefGoogle ScholarPubMed
172Girotti, 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: 203–10.CrossRefGoogle ScholarPubMed
173Newcomer, ME. Structure of the epididymal retinoic acid binding protein at 2.1 Å resolution. Structure 1993; 1: 7–18.CrossRefGoogle ScholarPubMed
174Mattmueller, DH, Hinton, BT. In vivo secretion and association of clusterin (SGP-2) in luminal fluid with spermatozoa in the rat testis and epididymis. Mol Reprod Dev 1991; 30: 62–69.CrossRefGoogle ScholarPubMed
175Olson, LM, Zhou, X, Schrieber, JR. Immunolocalization of apolipoprotein E in the testis and epididymis of the rat. Biol Reprod 1994; 50: 535–42.CrossRefGoogle ScholarPubMed
176Olson, LM, Zhou, X, Schreiber, JR. Cell-specific localization of apolipoprotein E messenger ribonucleic acid in the testis and epididymis of the rat. Biol Reprod 1995; 52: 1003–11.CrossRefGoogle ScholarPubMed
177Yeung, CH, Nashan, D, Cooper, TG et al. Basal cells of the human epididymis – antigenic and ultrastructural similarities to tissue-fixed macrophages. Biol Reprod 1994; 50: 917–26.CrossRefGoogle ScholarPubMed
178O'Bryan, MK, Mallidas, C, Murphy, BF, Baker, HWG. Immunohistological localization of clusterin in the male genital tract in humans and marmosets. Biol Reprod 1994; 50: 502–509.CrossRefGoogle ScholarPubMed
179von Lanz, T, Neuhauser, G. Morphometrische Analyse des menschlichen Nebenhodens. Z Anat Entwicklungsgesch 1964; 124: 126–52.CrossRefGoogle Scholar
180Johnson, L, Varner, DD. Effect of daily sperm production but not age on transit time of spermatozoa through the human epididymis. Biol Reprod 1988; 39: 812–17.CrossRefGoogle Scholar