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Molecular biology of sperm maturation in the human epididymis

  • Christiane Kirchhoff (a1)

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Male infertility is a frequent cause of childlessness, and, indeed, a comparison of the contributions to conception failure made by male and female factors shows them to be equally frequent. In practice, male infertility appears to be resistant to most treatments. However, the major reason for this may be that often attempts are carried out without knowing the cause of the problem. Unlike in women, obstructions and hormonal disorders are rare in male infertility. Rather, it would appear that sperm disorders are the most common cause, reflecting a variety of pathogenetic mechanisms. Defects in sperm morphology, defective sperm movement, deficient development or functional failure of the acrosome, and the excessive generation of reactive oxygen species are changes that are often seen in infertile semen, but little is known about their aetiology. In 5–10% of men being treated for infertilty, an autoimmune reaction against spermatozoa is observed. Although the correlation between the presence of systemic antisperm antibodies and fertility potential is poor, the appearance of sperm-bound antibodies of immunoglobulin class IgA in semen seems to be closely associated with infertility. Studies in laboratory animals and humans have shown that complementary adhesion molecules are located on the surface of oocytes and spermatozoa. These molecules interact and lead to gamete fusion. Abnormalities in these molecules on the sperm surface might be expected to contribute to male infertility. However, their clinical significance has not yet been documented, and the molecular basis of human gamete interaction is far from being understood. Therefore, the key to understanding male infertility may lie in basic research which directly targets the fundamental cellular and molecular biology of the human spermatozoon.

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Corresponding author

IHF Institute for Hormone and Fertility Research at the University of Hamburg, Grandweg 64, D-22529 Hamburg, Germany

References

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1Jequier, AM. Male infertility. Br J Obstet Gynaecol 1993; 100: 612–14.
2Skakkebak, NE, Giwercman, A, de Kretser, D. Pathogenesis and management of male infertility. Lancet 1994; 343: 1473–79.
3Kruger, TF, Acosta, AA, Simmons, KF, Swanson, RJ, Matta, JF, Oehninger, S. Predictive value of abnormal sperm morphology in in vitro fertilization. Fertil Steril 1988; 49: 112–17.
4Yovich, JM, Edirisinghe, WR, Cummins, JM, Jovich, JL. Influence of pentoxifylline in severe male factor infertility. Fertil Steril 1990; 53: 715–22.
5Cummins, JM, Pember, SM, Jequier, AM, Yovich, JL, Hartmann, PE. A test of the human sperm acrosome reaction following ionophore challenge: relationship to fertility and other seminal parameters. J Androl 1991; 12: 98103.
6Liu, DY, Baker, HWG. Disordered acrosome reaction of human spermatozoa bound to the zona pellucida: a newly discovered sperm defect causing infertility with reduced sperm-zona pellucida penetration and reduced fertilization in vitro. Hum Reprod 1994; 9: 1694–700.
7Aitken, RJ. Pathophysiology of human spermatozoa. Curr Opin Obstet Gynecol 1994; 6: 128–35.
8Bronson, RA. Secretory IgA and anti sperm antibodies in the male and female reproductive tract. In: Griffin, PD, Johnson, PM eds. Local immunity in reproductive tract tissues. Oxford: Oxford University Press, 1993: 307–19.
9Wassarman, PM. Mouse gamete adhesion molecules. Biol Reprod 1992; 46: 186–91.
10O'Rand, MG, Widgren, EE, Nikolajczyk, BS, Richardson, RT, Shabanowitz, RB. Receptors for zona pellucida on human spermatozoa. In: Alexander, NJ, Griffin, D, Spieler, JM, Waites, GMH eds. Gamete interaction: prospects for immunocontraception. New York: Wiley-Liss, 1990: 213–24.
11Wilton, LJ, Temple-Smith, PD, Baker, HWG, de Kretser, DM. Human male infertility caused by degeneration and death of sperm in the epididymis. Fertil Steril 1988; 49: 1052–58.
12Bedford, JM. The status and the state of the human epididymis. Hum Reprod 1994; 9: 2187–99.
13Yanagimachi, R. Mammalian fertilization. In: Knobil, E, Neill, JD eds. The physiology of reproduction, second edition. New York: Raven Press; 1994: 189317.
14Eddy, EM, O'Brien, DA. The spermatozoon. In: Knobil, E, Neill, JD eds. The physiology of reproduction, second edition. New York: Raven Press; 1994: 2977.
15Robaire, B, Hermo, L. Efferent ducts, epididymis, and vas deferens: structure, functions, and their regulation. In: Knobil, E, Neill, JD eds. The physiology of reproduction. New York: Raven Press 1988:9991080.
16Vasquez, MH, DeLarminat, MA, Blaquier, JA. Effect of androgen on androgen receptors in cultured human epididymis. J Endocrinol 1986; 111: 343–48.
17Chang, C, Kokontis, J, Liao, S. Structural analysis of complementary DNA and amino acid sequences of human and rat androgen receptors. Proc Natl Acad Sci USA 1988; 85: 7211–15.
18Lubahn, DB, Joseph, DR, Sar, M et al. The human androgen receptor: complementary deoxyribonucleic acid cloning, sequence analysis and gene expression in prostate. Mol Endocrinol 1988; 2: 1265–75.
19Trapmann, J, Klaasen, P, Kuiper, GGJM et al. Cloning, structure and expression of a cDNA encoding the human androgen receptor. Biochem Biophys Res Commun 1988; 153: 241–48.
20Joseph, DR. Structure, function, and regulation of androgen-binding protein/sex hormone-binding globulin. Vitam Horm 1994; 49: 197280.
21Felden, F, Leheup, B, Fremont, S et al. The plasma membrane of epididymal epithelial cells has a specific receptor which binds to androgen-binding protein and sex steroid-binding protein. J Steroid Biochem Mol Biol 1992; 42: 279–85.
22Jones, RC. Membrane remodelling during sperm maturation in the epididymis. Oxf Rev Reprod Biol 1989; 11: 285337.
23Myles, DG. Sperm cell surface proteins of testicular origin: expression and localization in the testis and beyond. In: Desjardins, C, Ewing, LL eds. Cell and molecular biology of the testis. New York: Oxford University Press, 1993:452–73.
24Brooks, DE. Androgen-regulated epididymal secretory proteins associated with post-testicular sperm development. In: Orgebin-Crist MC, Danzo BJ eds. Cell biology of the testis and epididymis. Ann N Y Acad Sci 1987; 513: 179–94.
25Orgebin-Crist, MC. Post-testicular development of mammalian spermatozoa. In: Spera, G, deKretser, DM eds. Morphological basis of human reproductive function. New York: Plenum, 1987:155–74.
26Cooper, 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. Berlin: Springer Verlag, 1992:285318.
27Blaquier, J, Cameo, MS, Dawidowski, A, Gonzalez-Echeverria, F, Sanjuro, C. On the role of epididymal factors in sperm maturation in man. Serono Symp Pub 1989; 53: 3744.
28Rojas, FJ, La, A-H, Ord, T et al. Penetration of zonafree hamster oocytes using human sperm aspirated from the epididymis of men with congenital absence of the vas deferens: comparison with human in vitro fertilization. Fertil Steril 1992; 58: 10001005.
29Primakoff, P, Myles, DG. A map of the guinea pig sperm surface constructed with monoclonal antibodies. Dev Biol 1983; 98: 417–28.
30Primakoff, 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.
31Phelps, BM, Myles, DG. The guinea pig sperm plasma membrane protein, PH-20, reaches the surface via two transport pathways and becomes located to a domain after initial uniform distribution. Dev Biol 1987; 123: 6372.
32Blobel, CP, 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: 6978.
33Phelps, 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.
34Eddy, EM, Vernon, RB, Muller, CH, Hahnel, AC, Fenderson, BA. Immunodissection of sperm surface modifications during epididymal maturation. Am J Anat 1985; 174: 225–37.
35Wolfsberg, TG, Bazan, JF, Blobel, CP, Myles, DG, Primakoff, P. The precursor region of a protein active in sperm-egg fusion contains a metalloprotease and disintegrin domain: structural, functional, and evolutionary implications. Proc Natl Acad Sci USA 1993; 90: 10783–87.
36Lin, Y, Kimmel, LH, Myles, DG, Primakoff, P. Molecular cloning of the human and monkey sperm surface protein PH-20. Proc Natl Acad Sci USA 1993; 90: 10071–75.
37Gmachl, M, Sagan, S, Ketter, S, Kreil, G. The human sperm protein PH-20 has hyaluronidase activity. FEBS Lett 1993; 336: 545–48.
38Gacesa, P, Civill, ND, Harrison, RA. PH-20 and sperm hyaluronidase: a conceptual conundrum in mammalian fertilization. Biochem J 1994; 303: 335–36.
39Phelps, BM, Primakoff, P, Koppel, DE, Low, MG, Myles, DG. Restricted lateral diffusion of PH-20, a Pl-anchored sperm membrane protein. Science 1988; 240: 1780–82.
40Primakoff, P, Lathrop, W, Woolman, L, Cowan, M, Myles, DG. Fully effective contraception in male and female guinea pigs immunized with the sperm protein PH-20. Na ire 1988; 335: 543–46.
41Lin, Y, Mahan, K, Lathrop, WF, Myles, DG, Primakoff, PA. 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: 1157–64.
42Blobel, 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 fusion. Nature 1992; 356: 248–52.
43Perry, ACF, Gichuhi, PM, Jones, R, Hall, L. Cloning and analysis of monkey fertilin reveals novel alpha subunits isoforms. Biochem J 1995; 307: 843–50.
44Perry, 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.
45Tulsiani, DRP, Skudlarek, MD, Holland, MK, Orgebin-Crist, MC. Glycosylation of rat sperm plasma membrane during epididymal maturation. Biol Reprod 1993; 48: 417–28.
46Tulsiani, DRP, Skudlarek, MD, Araki, Y, Orgebin-Crist, MC. Purification and characterization of two forms of β-D-galactosidase from rat epididymal luminal fluid: evidence for their role in the modification of sperm plasma membrane glycoprotein(s). Biochem J 1995; 305: 4150.
47Tulsiani, DRP, Skudlarek, MD, Orgebin-Crist, MC. Human sperm plasma membranes possess alpha-Dmannosidase activity but not galactosyltransferase activity. Biol Reprod 1990; 42: 843–58.
48Ross, 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.
49Cooper, TG, Yeung, CH, Nashan, D, Jockenhövel, F, Nieschlag, E. Improvement in the assessment of human epididymal function by the use of inhibitors on the assay of alpha-glucosidase in seminal plasma. Int J Androl 1990; 13: 297305.
50World Health Organization. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction, third edition. Cambridge: Cambridge University Press, 1992.
51Purvis, K, Egdetveit, I. Segmental distribution of alpha-glucosidase, ornithine decarboxylase and polyamines in the human epididymis. J Reprod Fertil 1993; 97: 575–80.
52Yeung, CH, Cooper, TG. Study of the role of epididymal alpha-glucosidase in the fertility of male rats by the administration of the enzyme inhibitor castanospermine. J Reprod Fertil 1994; 102: 401–10.
53Olson, GE, Hamilton, DW. Characterization of the surface glycoproteins of rat spermatozoa. Biol Reprod 1978; 19: 2635.
54Zeheb, R, Orr, GA. Characterization of a maturation-associated glycoprotein on the plasma membrane of rat caudal epididymal sperm. J Biol Chem 1984; 259: 839–48.
55Hamilton, DW, Wenstrom, JC, Baker, JB. Membrane glycoproteins from spermatozoa: partial characterization of an integral Mr = ~ 24,000 molecule from rat spermatozoa that is glycosylated during epididymal maturation. Biol Reprod 1986; 34; 925–36.
56Moore, A, White, TW, Ensrud, KM, Hamilton, DW (1989). The major maturation glycoprotein found on rat cauda epididymal sperm surface is linked to the membrane via phosphatidylinositol. Biochem Biophys Res Commun 1989; 160: 460–68.
57Eccleston, ED, White, TW, Howard, JB, Hamilton, DW. Characterization of a cell surface glycoprotein associated with maturation of rat spermatozoa. Mol Reprod Dev 1994; 37: 110–19.
58Hamilton, DW, Gould, RP. Preliminary observations on enzymatic galactosylation of glycoproteins on the surface of rat caput epididymal spermatozoa. Int J Androl 1982; 5 (supl): 7380.
59Kirchhoff, C, Krull, N, Pera, I, Ivell, R. A major mRNA of the human epididymal principal cells, HE5, encodes the leucocyte differentiation CDw52 antigen peptide backbone. Mol Reprod Dev 1993; 34: 815.
60Kirchhoff, C. A major messenger ribonucleic acid of the rodent epididymis encodes a small glycosylphosphatidylinositol-anchored lymphocyte surface antigen. Biol Reprod 1994; 50: 896902.
61Tezon, JG, Vasquez, MH, Pineiro, L, De Laminat, M, Blaquier, JA. Identification of androgen-induced proteins in the human epididymis. Biol Reprod 1985; 32: 584–90.
62Tezon, JG, Ramella, E, Cameo, MS, Vasquez, MH, Blaquier, JA. Immunochemical localization of secretory antigens in the human epididymis and their association with spermatozoa. Biol Reprod 1985; 32: 591–97.
63Ross, P, Kan, FWK, Antaki, P, Vigneault, N, Chapdelaine, A, Roberts, KD. Protein synthesis and secretion in the human epididymis and immunoreactivity with sperm antibodies. Mol Reprod Dev 1990; 26: 1223.
64Dacheux, JL, Chevrier, C, Lanson, Y. Motility and surface transformations of human spermatozoa during epididymal transit. Ann NY Acad Sci 1987; 513: 560–63.
65Boué, F, Lasalle, B, Duquenne, C et al. Human sperm proteins from testicular and epididymal origin that participate in fertilization: modulation of sperm binding to zona-free hamster oocytes, using monoclonal antibodies. Mol Reprod Dev 1992; 33: 470–80.
66Schauer, R. Sialic acids and their role as biological masks. Trends Biochem Sci 1985; 10: 357–60.
67Lasalle, B, Testart, J. Human zona pellucida recognition associated with removal of sialic acid from human sperm surface. J Reprod Fertil 1994; 101: 703–11.
68Brooks, DE, Means, AR, Wright, EJ, Singh, SP, Tiver, KK. Molecular cloning of the cDNA for androgendependent sperm-coating glycoproteins secreted by the rat epididymis. Eur J Biochem 1986; 161: 1318.
69Brooks, DE, Means, AR, Wright, JE, Singh, SP, Tiver, KK. Molecular cloning of the cDNA for two major androgen-dependent secretory proteins of 18.5 kilodaltons synthesized by the rat epididymis. J Biol Chem 1986; 261: 4956–61.
70Mizuki, N, Kasahara, M. Mouse submandibular glands express an androgen-regulated transcript encoding an acidic epididymal glycoprotein-like molecule. Mol Cell Endocrinol 1992; 89: 2532.
71Rankin, TL, Tsuruta, KJ, Holland, MK, Griswold, MD, Orgebin-Crist, MC. Isolation, immunolocalization, and sperm-association of three proteins of 18,25, and 29 kilodaltons secreted by the mouse epididymis. Biol Reprod 1992; 46: 747–66.
72Kirchhoff, C, Osterhoff, C, Habben, I, Ivell, R, Cloning and analysis of mRNAs expressed specifically in the human epdidymis. Int J Androl 1990; 13: 155–67.
73Kirchhoff, 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.
74Kirchhoff, C, Pera, I, Rust, W, Ivell, R. A major human epididymis-specific gene product, HE3, is the first representative of a novel gene family. Mol Reprod Dev 1994; 37: 130–37.
75Osterhoff, 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.
76Krull, N, Ivell, R, Osterhoff, C, Kirchhoff, C. Regionspecific variation of gene expression in the human epididymis as revealed by in situ hybridization with tissue-specific cDNAs. Mol Reprod Dev 1993; 34: 1624.
77Schoysmann, R, 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.
78Silber, SJ. Role of epididymis in sperm maturation. Urology 1989; 33: 4751.
79Uhlenbruck, F, Sinowatz, F, Amselgruber, W, Kirchhoff, C, Ivell, R. Tissue-specific gene expression as an indicator of epididymis-specific functional status in the boar, bull and stallion. Int J Androl 1993; 16: 5361.
80Ellerbrock, K, Pera, I, Hartung, S, Ivell, R. Gene expression in the dog epididymis: a model for human epididymal function. Int J Androl 1994; 17: 314–23.
81Fröhlich, O, Young, LG. Cloning and analysis of EPI-1, the major secretory protein in chimpanzee cauda epididymal fluid. Submitted to Biol Reprod.
82Young, LG, Gould, KG, Hinton, BT. Changes in binding of a 27-kilodalton chimpanzee cauda epididymal protein glycoprotein component to chimpanzee sperm. Gamete Res 1987; 18: 163–78.
83Kirchhoff, C, Osterhoff, C, Young, LG. Molecular cloning and characterization of HE1, a (the?) major secretory protein of the human epididymis. Submitted to Biol Reprod.
84Drenth, J, Low, BW, Richardson, JS, Wright, CS. The toxin-agglutinin fold. A new group of small protein structures organized around a four-disulfide core. J Biol Chem 1980; 255: 2652–55.
85Stetler, G, Brewer, M, Thompson, RC. Isolation and sequence of a human gene encoding a protent inhibitor of leukocyte proteases. Nucleic Acids Res 1986; 14: 7883–96.
86Seemüller, U, Arnold, M, Fritz, H et al. The acid-stabile protease inhibitor of human mucous secretions. FEBS Lett 1986; 199: 4348.
87Xia, MQ, Tone, M, Packman, L, Hale, G, Waldmann, H. Characterization of the CAMPATH-1 (CDw52) antigen: biochemical analysis and cDNA cloning reveal an unusually small peptide backbone. Eur J Immunol 1991; 21: 1677–84.
88Treumann, A, Lifely, MR, Schneider, P, Ferguson, MAJ. Primary structure of CD52. J Biol Chem 1995; 270: 6088–99.
89Perry, ACF, Jones, R, Hall, L. Identification of an abundant monkey epididymal transcript encoding a homologue of human CAMPATH-1 antigen precursor. Biochem Biophys Acta 1992; 1171: 122–24.
90Jentoft, N. Why are proteins O-glycosylated. Trends Biochem Sci 1990; 15: 291–94.
91Hinton, BT, Palladino, MA. Epididymal epithelium: its contribution to the formation of a luminal fluid microenvironment. Microsc Res Tech 1995; 30: 6781.
92Hale, G, Rye, PD, Warford, A, Lauder, I, Brito-Babapulle, A. The GPI-anchored lymphocyte antigen CDw52 is associated with the epididymal maturation of human spermatozoa. J Reprod Immunol 1993; 23: 189205.
93Boettger-Tong, H, Aarons, D, Biegler, B, Lee, T, Poirier, GR. Competition between zonae pellucidae and a proteinase inhibitor for sperm binding. Biol Reprod 1992; 47: 716–22.
94Coronel, CE, San, Agustin J, Lardy, HA. Purification and structure of caltrin-like proteins from seminal vesicle of the guinea pig. J Biol Chem 1990; 265: 6854–59.
95McConville, MJ, Ferguson, MJA. The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasite protozoa and higher eukaryotes. Biochem J 1993; 294: 305–24.
96Kirchhoff, C, Hale, G. Cell-to-cell transfer of glycosylphosphatidylinositol-anchored membrane proteins during sperm maturation. Submitted to Hum Reprod.
97Hirsch, T, Havemann, K, Krause, W, Neumann, K, Ziegler, A, Uchanska-Ziegler, B. Use of human spermatozoa and small-cell lung cancer cell lines to characterize mAb directed against NK and non-lineage antigens. In: Knapp, W ed. Leucocyte typing TV, white blood cell differentiation antigens. Oxford: Oxford University Press, 1989: 657.
98Yeung, CH, Cooper, TG, Oberpennig, F, Schulze, H, Nieschlag, E. Changes in movement characteristics of human spermatozoa along the length of the epididymis. Biol Reprod 1993; 49: 274–80.
99Moore, HDM, Hartman, TD, Pryor, JP. Fertilizing capacity of human epididymal spermatozoa. Int J Androl 1983; 6: 310–18.
100Hale, G, Xia, MQ, Tighe, HP, Dyer, MJS, Waldmann, H. The CAMPATH-1 antigen (CDw52). Tissue Antigens 1990; 35: 118–27.
101Robinson, PJ. Phosphatidylinositol membrane anchors and T-cell activation. Immunol Today 1990; 12: 3541.
102Xia, MQ, Hale, G, Lifely, MR. Structure of the CAMPATH-1 antigen, a glycosylphosphatidylinositol-anchored glycoprotein which is an exceptionally good target for complement lysis. Biochem J 1993; 293: 633–40.
103Rooney, IA, Davies, A, Morgan, BP. Membrane attack complex (MAC)-mediated damage to spermatozoa: protection of the cells by the presence on their membranes of MAC inhibitory proteins. Immunology 1992; 75: 499506.
104D'Cruz, OJ, Haas, GG. The expression of the complement regulators CD46, CD55, and CD59 by human sperm does not protect them from antisperm antibody- and complement-mediated injury. Fertil Steril 1993; 59: 876–84.
105Bozas, SE, Kirszbaum, L, Sparrow, RL, Walker, ID. Several vascular complement inhibitors are present on human sperm. Biol Reprod 1993; 48: 503–11.
106Simpson, KL, Holmes, CH. Differential expression of complement regulatory proteins decay-accelerating factor (CD55), membrane cofactor protein (CD46) and CD59 during human spermatogenesis. Immunology 1994; 81: 452–61.
107Rooney, IA, Atkinson, JP, Krul, ES et al. Physiologic relevance of the membrane attack complex inhibitory protein CD59 in human seminal plasm: CD59 is present on extracellular organelles (prostasomes), binds cell membranes, and inhibits complement-mediated lysis. J Exp Med 1993; 177: 1409–20.
108Fenichel, P, Cervoni, F, Hofmann, P et al. Expression of the complement regulatory protein CD59 on human spermatozoa: characterization and role in gametic interaction. Mol Reprod Dev 1994; 38: 338–46.
109Zimmermann, H. 5'-Nucleotidase: molecular structure and functional aspects. Biochem J 1992; 285: 345–65.
110Aumüller, G, Riva, A. Morphology and functions of the human seminal vesicle. Andrologia 1992; 24: 183–96.
111Schiemann, PJ, Aliante, M, Wennemuth, G, Fini, C, Aumüller, G. Distribution of endogenous and exogenous 5'-nucleotidase on bovine spermatozoa. Histochemistry 1994; 101: 253–62.
112Barclay, AN, Birkeland, ML, Brown, MH et al. The leucocyte antigen facts book. London: Academic Press; Cleveland, OH: Harcourt Brace Jovanovich, 1993; 263.
113Manin, M, Lecher, P, Martinez, A, Tournadre, S, Jean, CI. Exportation of mouse vas deferens protein, a protein without a signal peptide, from mouse vas deferens epithelium: a model of apocrine secretion. Biol Reprod 1995; 52: 5062.
114Ronquist, G, Brody, I. The prostasome: its secretion and function in man. Biochim Biophys Acta 1985; 822: 203–18.
115Ronquist, G, Nilsson, BO, Hjerten, S. Interaction between prostasomes and spermatozoa from human semen. Arch Androl 1990; 24: 147–57.
116Kelly, RW, Holland, P, Skibinski, G et al. Extracellular organelles (prostasomes) are immunosuppressive components of human semen. Clin Exp Immunol 1991; 86: 550–56.
117Fornes, MW, Barbieri, A, Sosa, MA, Bertini, F. First observations on enzymatic activity and protein content of vesicles separated from rat epididymal fluid. Andrologia 1991; 23: 347–51.
118Schoysman, R, Vanderzwalmen, P, Nijs, M, Segal-Bertin, G, van de Casseye, M. Successful fertilization by testicular spermatozoa in an in vitro fertilization programme. Hum Reprod 1993; 8: 1339–440.
119Ogura, A, Matsuda, J, Yanagimachi, R. Birth of normal young following electrofusion of mouse oocytes with round spermatids. Proc Natl Acad Sci USA 1994; 91: 7460–62.
120Asch, RH, Silber, SJ. Microsurgical epididymal sperm aspiration and assisted reproductive techniques. Ann NY Acad Sci 1991; 626: 101–10.
121Esponda, P, Bedford, JM. Epididymal fluid macromolecules do not act as auto- or alloantigens. J Androl 1985; 6: 359–64.

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Molecular biology of sperm maturation in the human epididymis

  • Christiane Kirchhoff (a1)

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