Skip to main content
Download PDF

Recent advances in sperm maturation in the human epididymis

Andrologie volume 12, pages 38–51 (2002)Cite this article

Abstract

As spermatozoa move through the human epididymis they encounter a varied environment with respect to the proteins with which they come into contact. In the proximal epididymis sperm are subjected to the action of enzymes and exposure to proteins involved in membrane modification. In the middle region another set of proteins and enzymes predominates; those associated with sterol transport could modify the sperm membrane to permit the uptake of GPI-anchored zona binding proteins P34H and CD52. More distally sperm encounter increasing activities of lytic enzymes, proteins involved in both zona binding and oocyte fusion, the major maturation antigen CD52, antimicrobial activity and decapacitation factors, that help them to survive before ejaculation. Adherence of the proteins to different domains (e.g. anterior acrosome or equatorial acrosomal segment) may depend on the nature of the protein, the lipid composition of the particular membrane and the ionic environment in the epididymal lumen. The eventual location on a capacitated sperm (acrosomal membrane) or acrosome-reacted sperm (equatorial region) may dictate their role in, for example, zona-binding (P34H) or oocyte-binding (gp20). Both proteins and membranes may be modified during epididymal transit by the enzymes which may add to or remove carbo-hydrates and peptides from the sperm surface.

References

  1. AGERBERTH B., GUNNE H., ODEBERG J., KOGNER P., BOMAN H.G., GUDMUNDSSON G.H.: FALL-39, a putative human peptide antibiotic, is cysteine-free and expressed in bone marrow and testis. Proc. Nat. Acad. Sci. US., 1995, 92: 195–199.

    Article  CAS  Google Scholar 

  2. BATOVA I., KAMEDA K., HASEGAWA A., KOYAMA K., TSUJI Y., ISOJIMA S.: Monoclonal antibody recognising an apparent peptide epitope of human seminal plasma glycoprotein and exhibiting sperm immobilizing activity. J. Reprod. Immunol., 1990, 17: 1–6.

    Article  PubMed  CAS  Google Scholar 

  3. BEDFORD J.M., CALVIN H., COOPER G.W.: The maturation of spermatozoa in the human epididymis. J. Reprod. Fertil., 1973, Suppl 18: 199–213.

    CAS  Google Scholar 

  4. BOUÉ F., LASSALLE B., DUQUENNE C. et al.: Human sperm proteins from testicular and epididymal origin that participate is fertilization: modulation of sperm binding to zona-free hamster oocytes, using monoclonal antibodies. Mol. Reprod. Develop., 1992, 33: 470–480.

    Article  Google Scholar 

  5. BOUÉ F., BERUBÉ B., DE LAMIRANDE E., GAGNON C., SULLIVAN R.: Human sperm-zona pellucida interaction in inhibited by an antiserum against a hamster sperm protein. Biol. Reprod., 1994, 51: 577–587.

    Article  PubMed  Google Scholar 

  6. COHEN D.J., ELLERMAN D.A., BUSSO D. et al.: Evidence that human epididymal protein ARP plays a role in gamete fusion through complementary sites on the surface of the human egg. Biol. Reprod., 2001, 65: 1000–1005.

    Article  PubMed  CAS  Google Scholar 

  7. COOPER T.G.: Apologie de la fonction de l'épididyme dans l'espèce humaine. Contracept. Fertil. Sex., 1992, 20: 363–373.

    Google Scholar 

  8. COOPER T.G.: Interactions between epididymal secretions and spermatozoa.. J. Reprod. Fertil., 1998, Suppl 53: 119–136.

    CAS  Google Scholar 

  9. COOPER T.G., RACZEK S., YEUNG C.H., SCHWAB E., SCHULZE H., HERTLE L.: Composition of fluids obtained from human epididymal cysts. Urol. Res., 1992, 20: 275–280.

    Article  PubMed  CAS  Google Scholar 

  10. DELPECH S., LECOMTE P., LECOMTE C.: Étude in vitro chez l'homme de la liason des spermatozoïdes épididymaires à la zone pellucide. J. Gynecol. Obstet. Biol. Reprod., 1988, 17: 339–342.

    CAS  Google Scholar 

  11. DIEKMAN A.B., WESTBROOK-CASE V.A., NAABYHANSEN S., KLOTZ K.L., FLICKINGER C.J., HERR J.C.: Biochemical characterization of sperm agglutination antigen-1, a human sperm surface antigen implicated in gamete interactions. Biol. Reprod., 1997, 57: 1136–1144.

    Article  PubMed  CAS  Google Scholar 

  12. DIEKMAN A.B., NORTON E.J., WESTBROOK V.A., KLOTZ K.L., NAABY-HANSEN S., HERR J.C.: Anti-sperm antibodies from infertile patients and their cognate sperm antigens: a review. Identity between SAGA-1, the H6-3C4 antigen, and CD52. Am. J. Reprod. Immunol., 2000, 43: 134–43.

    Article  PubMed  CAS  Google Scholar 

  13. EDIRISINGHER W.R., JUNK S.M., MATSON P.L., YOVICH J.L.: Changes in motility patterns by in-vitro culture of fresh and frozen/thawed testicular and epididymal spermatozoa: implication for planning treatment by intracytoplasmic sperm injection. Human Reprod., 1996, 11: 2474–2476.

    Google Scholar 

  14. FINAZ C., LEFÈVRE A.: Gamete recognition in mammals: sperm and zona pellucida interactions. Contracept. Fertil. Sex., 1998, 26: 542–548.

    PubMed  CAS  Google Scholar 

  15. FINAZ C., MARTIN-RUIZ C., LEFÈVRE A.: Interaction des gamètes et protéines de reconnaissance. Médicine/Sciences, 1998, 14: 175–182.

    Google Scholar 

  16. FOCARELLI R., GIUFFRIDA A., CAPPARELLI S. et al.: Specific localization in the equatorial segment of gp20, a 20 kDa sialylglycoprotein of the capacitated human spermatozoon acquired during epididymal transit which is necessary to penetrate zona-free hamster eggs. Mol. Human Reprod., 1998, 4: 119–125.

    Article  CAS  Google Scholar 

  17. FOCARELLI R., FRANCAVILLA S., FRANCAVILLA F., GIOVAMPAOLA D.C., SANTUCCI A., ROSATI F.: gp20, a sialylglycoprotein of the human capacitated sperm surface is the homologue of the leukocyte CD52 antigen: analysis of the effect of anti-CD52 monoclonal antibody (CAMPATH-1) on capacitated sperm. Mol. Human Reprod., 1999, 5: 46–51.

    Article  CAS  Google Scholar 

  18. FOCARELLI R., GIOVAMPAOLA C.D., SERAGLIA R. et al.: Biochemical and MALDI analysis of the human sperm antigen gp20, homologue of leukocyte CD52. Biochem. Biophys. Res. Commun, 1999, 258: 639–643.

    Article  PubMed  CAS  Google Scholar 

  19. FOGDESTAM I., FALL M., NILSSON S.: Microsurgical epidi-dymovasostomy in the treatment of occlusive azoospermia. Fertil. Steril., 1986, 46: 925–929.

    PubMed  CAS  Google Scholar 

  20. FOURNIER-DELPECH A., GUÉRIN Y.: Interactions des spermatozoïdes avec le zone pellucide. Contracept. Fertil. Steril., 1991, 19: 825–832.

    Google Scholar 

  21. FRENETTE G., SULLIVAN R.: Prostasome-like particles are involved in the transfer of P25g from the bovine epididymal fluid to the sperm surface. Mol. Reprod. Develop., 2001, 59: 115–121.

    Article  CAS  Google Scholar 

  22. GAGO C., SOLER C., PEREZ-SANCHEZ F., YEUNG C.H., COOPER T.G.: Effect of cetrorelix on sperm morphology during migration through the epididymis in the cynomolgus macaque (Macaca fascicularis). Am. J. Primatol., 2000, 51: 103–17.

    Article  PubMed  CAS  Google Scholar 

  23. GOLAN R., COOPER T.G., OSCHRY Y. et al.: Changes in chromatin condensation of human spermatozoa during epididymal transit as determined by flow cytometry. Human Reprod., 1996, 11: 1457–1462.

    CAS  Google Scholar 

  24. HAMMANI-HAMZA S., DOUSSAU M., BERNARD J. et al.: Cloning and sequencing of SOB3, a human gene coding for a sperm protein homologous to an antimicrobial protein and potentially involved in zona pellucida binding. Mol. Human Reprod., 2001, 7: 625–632.

    Article  Google Scholar 

  25. HAIDL G., BADURA B., HINSCH K.D., GHYCZY M., GAREI B.J., SCHILL W.B.: Disturbances of sperm flagella due to failure of epididymal maturation and their possible relationship to phospholipids. Human Reprod., 1993, 8: 1070–1073.

    CAS  Google Scholar 

  26. HAIDL G., BADURA B., SCHILL W.B.: Function of human epididymal spermatozoa. J. Androl., 1994, 15: 23S-27S.

    PubMed  Google Scholar 

  27. HE X., SHEN L., BJARTELL A., MALM J., LILJA H., DAHLBÄCK, B.: The gene encoding vitamin K-dependent anticoagulant protein C is expressed in human male reproductive tissues. J. Histochem. Cytochem., 1995, 43: 563–570.

    PubMed  CAS  Google Scholar 

  28. HUTTER H., HAMMER A., BLASCHITZ A. et al.: The monoclonal antibody GZS-1 detects a maturation-associated antigen of human spermatozoa that is also present on the surface of human mononuclear blood cells. J. Reprod. Immunol., 1996, 30: 115–32.

    Article  PubMed  CAS  Google Scholar 

  29. JEAN M., DACHEUX J.L., DACHEUX F., SAGOT P., LOPES P., BARRIERE P.: Increased zona-binding ability after incubation of spermatozoa with proteins extracted from spermatozoa of fertile men. J. Reprod. Fertil., 1995, 105: 43–48.

    PubMed  CAS  Google Scholar 

  30. JOW W.W., STECKEL J., SCHLEGEL P.N., MAGID M.S., GOLDSTEIN M.: Motile sperm in human testis biopsy specimens. J. Androl., 1993, 14: 194–198.

    PubMed  CAS  Google Scholar 

  31. KAMEDA K., TAKADA Y., HASEGAWA A., TSUJI Y., KOYAMA K., ISOJIMA S.: Sperm immobilizing and fertilization-blocking monoclonal antibody 2C6 to human seminal plasma and characterization of the antigen epitope corresponding to the monoclonal antibody. J. Reprod. Immunol., 1991, 20: 27–41.

    Article  PubMed  CAS  Google Scholar 

  32. KAMEDA K., TSUJI Y., KOYOMA K., ISOJIMA S.: Comparative studies of the antigens recognised by sperm-immobilising monoclonal antibodies. Biol. Reprod., 1992, 46: 349–357.

    Article  PubMed  CAS  Google Scholar 

  33. KIRCHHOFF C.: Molecular characterization of epididymal proteins. Rev. Reprod., 1998, 3: 86–95.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  35. KRÄTZSCHMAR J., HAENDLER B., EBERSPAECHER U., ROOSTERMAN D., DONNER P., SCHLEUNING W.D.: The human cysteine-rich secretory protein (CRISP) family. Primary structure and tissue distribution of CRISP-1, CRISP-2 and CRISP-3. Europ J. Biochem., 1996, 236: 827–836.

    Article  PubMed  Google Scholar 

  36. MAHONY M.C., ALEXANDER N.J.: Sites of antisperm antibody action. Human Reprod., 1991, 6: 1426–1430.

    CAS  Google Scholar 

  37. MALM J., SORENSEN O., PERSSON T. et al.: The human cationic antimicrobial protein (hCAP-18) is expressed in the epithelium of human epididymis, is present in seminal plasma at high concentrations, and is attached to spermatozoa. Infect. Immun., 2000, 68: 4297–302.

    Article  PubMed  CAS  Google Scholar 

  38. MATHIEU C., GUÉRIN J.F., COGNAT M., LEJEUNE H., PINATEL M.C., LORNAGE J.: Motility and fertilizing capacity of epididymal human spermatozoa in normal and pathological cases. Fertil. Steril., 1992, 57: 871–876.

    PubMed  CAS  Google Scholar 

  39. MOORE H.D.M., CURRY M.R., PENFOLD L.M., PRYOR J.P.: The culture of human epididymal epithelium and in vitro maturation of epididymal spermatozoa. Fertil. Steril., 1992, 58: 776–783.

    PubMed  CAS  Google Scholar 

  40. MOORE, H.D.M., HARTMANN T.D., PRYOR J.P.: Development of the oocyte-penetrating capacity of spermatozoa in the human epididymis. Int. J. Androl., 1983, 6: 310–318.

    Article  PubMed  CAS  Google Scholar 

  41. PATRIZIO P., ORD T., SILBER S.J., ASCH R.H.: Correlation between epididymal length and fertilization rate of men with congenital absence of the vas deferens. Fertil. Steril., 1994, 61: 265–268.

    PubMed  CAS  Google Scholar 

  42. ROCHWERGER L., CUASNICÚ P.S.: Redistribution of a rat sperm epididymal glycoprotein after in vitro and in vivo capacitation. Mol. Reprod. Develop., 1992, 31: 34–41.

    Article  CAS  Google Scholar 

  43. ROSS P., VIGNEAULT N., PROVENCHER S., POTIER M., ROBERTS K.D.: Partial characterization of galactosyltransferase in human seminal plasma and its distribution in the human epididymis. J. Reprod. Fertil., 1993, 98: 129–137.

    PubMed  CAS  Google Scholar 

  44. SANJURJO C., DAWIDOWSKY A.R., CAMEO M.S., GONZALÉZ ECHEVERRÍA F., BLAQUIER J.A.: Participation of human epididymal sperm coating antigens in fertilization. J. Androl., 1990, 11: 476–483.

    PubMed  CAS  Google Scholar 

  45. SCHIRREN C.: Gewebsentnahme aus dem Nebenhoden zu diagnostischen Zwecken? Andrologia, 1982, 14: 461–462.

    Article  PubMed  CAS  Google Scholar 

  46. SCHMIDT S.S., SCHOYSMAN R., STEWART B.H.: Surgical approaches to male infertility. In: Hafez, E.S.E. eds. Human Semen and Fertility Regulation in Men., 1976: 476–493.

  47. SOLER C., PÉREZ-SÁNCHEZ F., SCHULZE H., BERGMANN M., OBERPENNING F., YEUNG C., COOPER T.G.: Objective evaluation of the morphology of human epididymal sperm heads. Int. J. Androl., 2000, 23: 77–84.

    Article  PubMed  CAS  Google Scholar 

  48. TEZÓN J.G., RAMELLA E., CAMEO M.S., VAZQUEZ M.H., BLAQUIER J.A.: Immunocytochemical localization of secretion antigens in the human epididymis and their association with spermatozoa. Biol. Reprod., 1985, 32: 591–597.

    Article  PubMed  Google Scholar 

  49. YEUNG C.H., COOPER T.G., SENGE T.: Histochemical localization and quantification of α-glucosidase in the epididymis of men and laboratory animals. Biol. Reprod., 1990, 42: 669–676.

    Article  PubMed  CAS  Google Scholar 

  50. YEUNG C.H., COOPER T.G., 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.

    Article  PubMed  CAS  Google Scholar 

  51. YEUNG C.H., COOPER T.G., OBERPENNING F., SCHULZE H., NIESCHLAG E.: Changes in movement characteristics of human spermatozoa along the length of the epididymis. Biol. Reprod., 1993, 49: 274–280.

    Article  PubMed  CAS  Google Scholar 

  52. YEUNG C.H., PEREZ-SANCHEZ F., SOLER C., POSER D., KLIESCH S., COOPER T.G.: Maturation of human spermatozoa (from selected epididymides of prostatic carcinoma patients) with respect to their morphology and ability to undergo the acrosome reaction. Hum. Reprod. Update, 1997, 3: 205–13.

    Article  PubMed  CAS  Google Scholar 

  53. YEUNG C.H., SCHRÖTER S., WAGENFELD A. et al.: Interaction of the human epididymal protein CD52 (HE5) with epididymal spermatozoa from men and cynomolgus monkeys. Mol. Reprod. Develop., 1997, 48: 267–275.

    Article  CAS  Google Scholar 

  54. WIESE K., HAIDL G., OPPER C., SCHILL W.B.: Erhöhte Membranrigidität bei Spermatozoen mit mangelnder Nebenhodenausreifung. Fertilität, 1996, 12: 91–94.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Reproductive Medicine of the University, Münster, Domagkstraße 11, D-48129, Münster, Germany

    Trevor G. Cooper

Authors
  1. Trevor G. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Trevor G. Cooper.

Additional information

Communication au XVIII° Congrès de la Société d'Andrologie de Langue Française, Montpellier, 13–15 décembre 2001.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cooper, T.G. Recent advances in sperm maturation in the human epididymis. Androl. 12, 38–51 (2002). https://doi.org/10.1007/BF03034947

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03034947

Key words

Basic and Clinical Andrology

ISSN: 2051-4190