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Prostasomes, dérivés actifs de l’oxygène et sperme humain
Prostasomes, reactive oxygen species and human semen
Andrologie volume 11, pages 33–48 (2001)
Résumé
Les prostasomes sont des vésicules lipidiques particulières sécrétées par la prostate humainne et retrouvées dans le sperme. Actuellement, aucune action spécifique ne leur a été attribuée. Cependant, les prostasomes semblent exercer un effet à différents niveaux. Par exemple, les prostasomes sont bénéfiques pour la mobilité des spermatozoïdesin-vitro et participent à l’immunomodulation exercée par le liquide séminal.
La production de dérivés actifs de l’oxygène (DAO) dans le sperme humain joue un rôle sur les capacités fonctionnelles des spermatozoïdes. La production de quantités faibles et contrôlées de DAO par les spermatozoïdes semble nécessaire à l’acquisition de leur capacités fonctionnelles. Par contre, la présence de leucocytes dans le sperme, associée à une forte production de DAO, peut se révéler néfaste pour les spermatozoïdes.
Après avoir abordé, sous forme d’une revue bibliographique, les caractéristiques structurales et fonctionnelles des prostasomes et le rôle des DAO dans le sperme humain, nous rapportons nos résultats concernant les effets des prostasomes sur la production des DAO et les conséquences sur les spermatozoïdes. Nous avons mis en évidence une fonction antioxydante des prostasomes dans le sperme humain. Elle s’exerce à la fois sur les polynucléaires neutrophiles et sur les spermatozoïdes. Le mode d’action des prostasomes est particulier puisqu’ils interviennent sur la production des DAO, en agissant notamment au niveau des membranes des polynucléaires neutrophiles. Ils entraînent une diminution de l’activité NADPH-oxydase de ces cellules associée à une rigidification de leur membrane plasmique. Au niveau des spermatozoïdes, les prostasomes protègent leurs capacités fonctionnelles lors d’un stress oxydant crée par la présence de NADPH dans le milieu.
Abstract
Prostasomes are particular lipid vesicles secreted by the human prostate and found in the semen. No specific action has yet been attributed to prostasomes, but they appear to act at various levels. For example, prostasomes enhance sperm motility in vitro and participate in the immunomodulation properties of seminal plasma.
Excessive production of reactive oxygen species (ROS) in human semen has a negative influence on the functional capacities of spermatozoa. The presence of leukocytes in semen is associated with increased production of ROS that can be harmful to sperm cells, under certain conditions. Previous results tend to suggest a possible role of prostasomes on ROS production in human semen.
After reviewing the literature concerning the structural and functional characteristics of prostasomes and the role of ROS in human semen, we report our results concerning the influence of prostasomes on ROS production and the consequences on semen. We have demonstrated that prostasomes exert an antioxidant function in human semen. This function is effective both on polymorphonuclear neutrophils and on sperm cells. The mechanism of action of prostasomes is unusual, as they act on ROS production mainly on the plasma membranes of neutrophils. They induce a decrease of NADPH-oxidase activity associated with rigidification of the plasma membrane. Prostasomes protect the functional capacities of spermatozoa during an oxidative stress created by the presence of NADPH in the incubation medium.
Références
AITKEN, R.J., CLARKSON, J.S.: Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil, 1987, 81: 459–69.
AITKEN, R.J., CLARKSON, J.S., FISHEL, S.: Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod, 1989, 41: 183–97.
AITKEN, R.J., WEST, K.M.: Analysis of the relationship between reactive oxygen species production and leucocyte infiltration in fractions of human semen separated on Percoll gradients. Int J Androl, 1990, 13: 433–51.
AITKEN, R.J., BUCKINGHAM, D.W., WEST, K.M.: Reactive oxygen species and human spermatozoa: analysis of the cellular mechanisms involved in luminol-and lucigenin-dependent chemiluminescence. J Cell Physiol, 1992, 151: 466–77.
AITKEN, R.J., HARKISS, D., BUCKINGHAM, D.: Relationship between iron-catalysed lipid peroxidation potential and human sperm function. J Reprod Fertil, 1993, 98: 257–65.
AITKEN, R.J., PATERSON, M., FISHER, H., BUCKINGHAM, D.W., VAN DUIN, M.: Redox regulation of tyrosine phosphorylation in human spermatozoa and its role in the control of human sperm function. J Cell Sci, 1995, 108: 2017–25.
AITKEN, R.J., FISHER, H.M., FULTON, N., GOMEZ, E., KNOX, E., LEWIS, B., IRVINE, S.: Reactive oxygen species generation by human spermatozoa is induced by exogenous NADPH and inhibited by the flavoprotein inhibitors diphenylene iodonium and quinacrine. Mol Reprod Dev, 1997, 47: 468–82.
AITKEN, R.J., HARKISS, D., KNOX, W., PATERSON, M., IRVINE, D.S.: A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation. J Cell Sci, 1998, 111: 645–56.
AITKEN, R.J.: The Amoroso Lecture. The human spermatozoon—a cell in crisis? J Reprod Fertil, 1999, 115: 1–7.
ALVAREZ, J.G., TOUCHSTONE, J.C., BLASCO, L., STOREY, B.T.: Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa. Superoxide dismutase as major enzyme protectant against oxygen toxicity. J Androl, 1987, 8: 338–48.
ALVAREZ, J.G., STOREY, B.T.: Role of glutathione peroxidase in protecting mammalian spermatozoa from loss of motility caused by spontaneous lipid peroxidation. Gamete Res, 1989, 23: 77–90.
ARIENTI, G., CARLINI, E., PALMERINI, C.A.: Fusion of human sperm to prostasomes at acidic pH. J Membr Biol, 1997, 155: 89–94.
ARIENTI, G., POLCI, A., CARLINI, E., PALMERINI, C.A.: Transfer of CD26/dipeptidyl peptidase IV (E.C. 3.5.4.4) from prostasomes to sperm. FEBS Lett, 1997, 410: 343–6.
ARIENTI, G., CARLINI, E., DE COSMO, A.M., DI PROFIO, P., PALMERINI, C.A.: Prostasome-like particles in stallion semen. Biol Reprod, 1998, 59: 309–13.
ARIENTI, G., CARLINI, E., POLCI, A., COSMI, E.V., PALMERINI, C.A.: Fatty acid pattern of human prostasome lipid. Arch Biochem Biophys, 1998, 358: 391–5.
ARIENTI, G., CARLINI, E., SACCARDI, C., PALMERINI, C.A.: Interactions between prostasomes and leukocytes. Biochim Biophys Acta, 1998, 1425: 36–40.
ARVIDSON, G., RONQUIST, G., WIKANDER, G., OJTEG, A.C.: Human prostasome membranes exhibit very high cholesterol/phospholipid ratios yielding high molecular ordering. Biochim Biophys Acta, 1989, 984: 167–73.
BARRAT, C.L.R., HORNBY, D.A. Induction of the human acrosome reaction by rhu-ZP3. In Human sperm acrosome reaction, Volume Colloque INSERM no 236 (P. Fénichel and J. Parinaud, eds), John Libbey Eurotext Ltd., 1995: 105–112.
BIELFELD, P., JEYENDRAN, R.S., ZANEVELD, L.J.: Human spermatozoa do not undergo the acrosome reaction during storage in the cervix. Int J Fertil, 1991, 36: 302–6.
BREITBART, H., RUBINSTEIN, S.: Characterization of Mg2+- and Ca2+-ATPase activity in membrane vesicles from ejaculated ram seminal plasma. Arch Androl, 1982, 9: 147–57.
BRODY, I., RONQUIST, G., GOTTFRIES, A.: Ultrastructural localization of the prostasome — an organelle in human seminal plasma. Ups J Med Sci, 1983, 88: 63–80.
CARLINI, E., PALMERINI, C.A., COSMI, E.V., ARIENTI, G.: Fusion of sperm with prostasomes: effects on membrane fluidity. Arch Biochem Biophys 1997, 343: 6–12.
CARLSSON, L., RONQUIST, G., STRIDSBERG, M., JOHANSSON, L.: Motility stimulant effects of prostasome inclusion in swim-up medium on cryopreserved human spermatozoa. Arch Androl, 1997, 38: 215–21.
CROSS, N.L.: Human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist, progesterone: cholesterol is the major inhibitor. Biol Reprod, 1996, 54: 138–45.
CROSS, N.L.: Effect of cholesterol and other sterols on human sperm acrosomal responsiveness. Mol Reprod Dev, 1996, 45: 212–7.
CROSS, N.L., MAHASRESHTI, P.: Prostasome fraction of human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist progesterone. Arch Androl, 1997, 39: 39–44.
DAVIS, B.K.: Inhibition of fertilizing capacity in mammalian spermatozoa by natural and synthetic vesicles. In The pharmacological Effects of lipids (K. JK, ed) JAOCS, Champaign, 1978: 145–157.
DE LAMIRANDE, E., GAGNON, C.: A positive role for the superoxide anion in triggering hyperactivation and capacitation of human spermatozoa. Int J Androl, 1993, 16: 21–5.
DE LAMIRANDE, E., GAGNON, C.: Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Radic Biol Med, 1993, 14: 157–66.
DE LAMIRANDE, E., EILEY, D., GAGNON, C.: Inverse relationship between the induction of human sperm capacitation and spontaneous acrosome reaction by various biological fluids and the superoxide scavenging capacity of these fluids. Int J Androl, 1993, 16: 258–66.
DE LAMIRANDE, E., GAGNON, C.: Capacitation-associated production of superoxide anion by human spermatozoa. Free Radic Biol Med, 1995, 18: 487–95.
DE LAMIRANDE, E., HARAKAT, A., GAGNON, C.: Human sperm capacitation induced by biological fluids and progesterone, but not by NADH or NADPH, is associated with the production of superoxide anion. J Androl, 1998, 19: 215–25.
FABIANI, R., JOHANSSON, L., LUNDKVIST, O., RONQUIST, G.: Enhanced recruitment of motile spermatozoa by prostasome inclusion in swim-up medium. Hum Reprod, 1994, 9: 1485–9.
FABIANI, R., JOHANSSON, L., LUNDKVIST, O., ULMSTEN, U., RONQUIST, G.: Promotive effect by prostasomes on normal human spermatozoa exhibiting no forward motility due to buffer washings. Eur J Obstet Gynecol Reprod Biol, 1994, 57: 181–8.
FERNANDEZ, J.A., HEEB, M.J., RADTKE, K.P., GRIFFIN, J.H.: Potent blood coagulant activity of human semen due to prostasome-bound tissue factor. Biol Reprod, 1997: 56: 757–63.
FORD, W.C., WHITTINGTON, K., WILLIAMS, A.C.: Reactive oxygen species in human sperm suspensions: production by leukocytes and the generation of NADPH to protect sperm against their effects. Int J Androl, 1997, 20: 44–9.
FORNES, M.W., DE ROSAS, J.C.: Interactions between rat epididymal epithelium and spermatozoa. Anat Rec, 1991, 231: 193–200.
FRENETTE, G., DUBE, J.Y., TREMBLAY, R.R.: Enzymatic characterization of arginine esterase from dog seminal plasma. Biochim Biophys Acta, 1985, 838: 270–6.
GOMEZ, E., BUCKINGHAM, D.W., BRINDLE, J., LANZAFAME, F., IRVINE, D.S., AITKEN, R.J.: Development of an image analysis system to monitor the retention of residual cytoplasm by human spermatozoa: correlation with biochemical markers of the cytoplasmic space, oxidative stress, and sperm function. J Androl, 1996, 17: 276–87.
GRIVEAU, J.F., RENARD, P., LE LANNOU, D.: An in vitro promoting role for hydrogen peroxide in human sperm capacitation. Int J Androl, 1994, 17: 300–7.
GRIVEAU, J.F., DUMONT, E., RENARD, P., LE LANNOU, D.: Reactive oxygen species, lipid peroxidation and enzymatic defense systems in human spermatozoa. J Reprod Fertil, 1995, 103: 17–26.
GRIVEAU, J.F., RENARD, P., LE LANNOU, D.: Superoxide anion production by human spermatozoa as a part of the ionophore-induced acrosome reaction process. Int J Androl, 1995, 18: 67–74.
GRIVEAU, J.F., LE LANNOU, D.: Influence of oxygen tension on reactive oxygen species production and human sperm function. Int J Androl, 1997, 20: 195–200.
GRIZARD, G., SION, B., BAUCHART, D., BOUCHER, D.: Separation and quantification of cholesterol and major phospholipid classes in human semen by high-performance liquid chromatography and light-scattering detection. J Chrom B, 2000, 740: 101–107.
HALLIWELL, B., GUTTERIDGE, J.M.C.: Free Radicals in Biology and Medicine. Oxford: Clarendon Press, 1989.
HUGHES, C.M., LEWIS, S.E., MCKELVEY-MARTIN, V.J., THOMPSON, W.: A comparison of baseline and induced DNA damage in human spermatozoa from fertile and infertile men, using a modified comet assay. Mol Hum Reprod, 1996, 2: 613–9.
IRVINE, D.S., TWIGG, J.P., GORDON, E.L., FULTON, N., MILNE, P.A., AITKEN, R.J.: DNA integrity in human spermatozoa: relationships with semen quality. J Androl, 2000, 21: 33–44.
IWASAKI, A., GAGNON, C.: Formation of reactive oxygen species in spermatozoa of infertile patients. Fertil Steril, 1992, 57: 409–16.
JEULIN, C., SOUFIR, J.C., WEBER, P., LAVAL-MARTIN, D., CALVAYRAC, R.: Catalase activity in human spermatozoa and seminal plasma. Gamete Res, 1989, 24: 185–96.
KELLY, R.W.: Immunomodulators in human seminal plasma: a vital protection for spermatozoa in the presence of infection? Int J Androl, 1999, 22: 2–12.
KESSOPOULOU, E., TOMLINSON, M.J., BARRATT, C.L., BOLTON, A.E., COOKE, I.D.: Origin of reactive oxygen species in human semen: spermatozoa or leucocytes? J Reprod Fertil, 1992, 94: 463–70.
KOBAYASHI, T., MIYAZAKI, T., NATORI, M., NOZAWA, S.: Protective role of superoxide dismutase in human sperm motility: superoxide dismutase activity and lipid peroxide in human seminal plasma and spermatozoa. Hum Reprod, 1991, 6: 987–91.
KOBAYASHI, T., ROBINSON, J.M., SEGUCHI, H.: Identification of intracellular sites of superoxide production in stimulated neutrophils. J Cell Sci, 1998, 111: 81–91.
KODAMA, H., YAMAGUCHI, R., FUKUDA, J., KASAI, H., TANAKA, T.: Increased oxidative deoxyribonucleic acid damage in the spermatozoa of infertile male patients. Fertil Steril, 1997, 68: 519–24.
KRAUSZ, C., GERVASI, G., FORTI, G., BALDI, E.: Effect of platelet-activating factor on motility and acrosome reaction of human spermatozoa. Hum Reprod, 1994, 9: 471–6.
LECLERC, P., DE LAMIRANDE, E., GAGNON, C.: Interaction between Ca2+, cyclic 3′,5′ adenosine monophosphate, the superoxide anion, and tyrosine phosphorylation pathways in the regulation of human sperm capacitation. J Androl, 1998, 19: 434–43.
LETERRIER, F., GARY-BOBO, C. Biologie Membranaire: Structure et Dynamique des Membranes Biologiques. Hermann, 1989.
LINDAHL, M., TAGESSON, C., RONQUIST, G.: Phospholipase A2 activity in prostasomes from human seminal plasma. Urol Int, 1987, 42: 385–9.
MACLEOD, J.: The role of oxygen in the metabolism and motility of human spermatozoa. Am. J. Physiol, 1943, 138: 512–518.
MEIZEL, S., PILLAI, M., DIAZ-PEREZ, E., THOMAS, P.: Initiation of the human sperm acrosome reaction by components of follicular fluid and cumulus secretions including steroids. In Fertilization in mammals (B. D. Bavister, J. Cummins and E. R. S. Roldan, eds), Serono Symposia, Norwell, MA, USA, 1990: 205–202.
MINELLI, A., MORONI, M., MARTINEZ, E., MEZZASOMA, I., RONQUIST, G.: Occurrence of prostasome-like membrane vesicles in equine seminal plasma. J Reprod Fertil, 1998, 114: 237–43.
NILSSON, B.O., JIN, M., RONQUIST, G.: Immunolocalization of prostasomes in the human prostate. Ups J Med Sci, 1996, 101: 149–57.
OCHSENDORF, F.R., THIELE, J., FUCHS, J., SCHUTTAU, H., FREISLEBEN, H.J., BUSLAU, M., MILBRADT, R.: Chemiluminescence in semen of infertile men. Andrologia, 1994, 26: 289–93.
OCHSENDORF, F.R.: Infections in the male genital tract and reactive oxygen species. Hum Reprod Update, 1999, 5: 399–420.
OSHEROFF, J.E., VISCONTI, P.E., VALENZUELA, J.P., TRAVIS, A.J., ALVAREZ, J., KOPF, G.S.: Regulation of human sperm capacitation by a cholesterol efflux- stimulated signal transduction pathway leading to protein kinase A- mediated up-regulation of protein tyrosine phosphorylation. Mol Hum Reprod, 1999, 5: 1017–26.
PALMERINI, C.A., CARLINI, E., NICOLUCCI, A., ARIENTI, G.: Increase of human spermatozoa intracellular Ca2+ concentration after fusion with prostasomes. Cell Calcium, 1999, 25: 291–6.
PLANTE, M., DE LAMIRANDE, E., GAGNON, C.: Reactive oxygen species released by activated neutrophils, but not by deficient spermatozoa, are sufficient to affect normal sperm motility. Fertil Steril, 1994, 62: 387–93.
RENNEBERG, H., KONRAD, L., DAMMSHAUSER, I., SEITZ, J., AUMULLER, G.: Immunohistochemistry of prostasomes from human semen. Prostate, 1997, 30: 98–106.
RONQUIST, G., BRODY, I., GOTTFRIES, A., STEGMAYR, B.: An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid: part I. Andrologia, 1978, 10: 261–72.
RONQUIST, G., BRODY, I.: The prostasome: its secretion and function in man. Biochim Biophys Acta, 1985, 822: 203–18.
RONQUIST, G.: Zinc ion stimulation of ATP cleavage by prostasomes from human seminal plasma. Urol Int, 1988, 43: 334–40.
RONQUIST, G., NILSSON, B.O., HJERTEN, S.: Interaction between prostasomes and spermatozoa from human semen. Arch Androl, 1990, 24: 147–57.
RONQUIST, G., FABIANI, R., JIN, M., NILSSON, B.O., ELENBRING, K., HJERTEN, S. Adherence of human prostasomes to mouse spermatozoa and their displacement by monoclonal antibodies as revealed by free zone electrophoresis. Arch Androl, 1996, 36: 101–7.
ROONEY, I.A., ATKINSON, J.P., KRUL, E.S., SCHONFELD, G., POLAKOSKI, K., SAFFITZ, J.E., MORGAN, B.P.: Physiologic relevance of the membrane attack complex inhibitory protein CD59 in human seminal plasma: CD59 is present on extracellular organelles (prostasomes), binds cell membranes, and inhibits complement-mediated lysis. J Exp Med, 1993, 177: 1409–20.
ROONEY, I.A., HEUSER, J.E., ATKINSON, J.P.: GPI-anchored complement regulatory proteins in seminal plasma. An analysis of their physical condition and the mechanisms of their binding to exogenous cells. J Clin Invest, 1996, 97: 1675–86.
SAEZ, F., MOTTA, C., BOUCHER, D. aND GRIZARD, G.: Antioxidant capacity of prostasomes in human semen. Mol Hum Reprod, 1998, 4: 667–672.
SAEZ, F., MOTTA, C., BOUCHER, D. aND GRIZARD, G.: Prostasomes inhibit the NADPH-oxidase activity of human neutrophils. Mol Hum Reprod, 2000, 6: 883–891.
SKIBINSKI, G., KELLY, R.W., HARKISS, D., JAMES, K.: Immunosuppression by human seminal plasma—extracellular organelles (prostasomes) modulate activity of phagocytic cells. Am J Reprod Immunol, 1992, 28: 97–103.
STEGMAYR, B., RONQUIST, G.: Promotive effect on human sperm progressive motility by prostasomes. Urol Res, 1982, 10: 253–7.
STRIDSBERG, M., FABIANI, R., LUKINIUS, A., RONQUIST, G.: Prostasomes are neuroendocrine-like vesicles in human semen. Prostate, 1996, 29: 287–95.
SUKCHAROEN, N., KEITH, J., IRVINE, D.S., AITKEN, R.J.: Predicting the fertilizing potential of human sperm suspensions in vitro: importance of sperm morphology and leukocyte contamination. Fertil Steril, 1995, 63: 1293–300.
SUN, J.G., JURISICOVA, A., CASPER, R.F.: Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod, 1997, 56: 602–7.
THOMAS, J., FISHEL, S.B., HALL, J.A., GREEN, S., NEWTON, T.A., THORNTON, S.J.: Increased polymorphonuclear granulocytes in seminal plasma in relation to sperm morphology. Hum Reprod, 1997, 12: 2418–21.
TWIGG, J., FULTON, N., GOMEZ, E., IRVINE, D.S., AITKEN, R.J.: Analysis of the impact of intracellular reactive oxygen species generation on the structural and functional integrity of human spermatozoa: lipid peroxidation, DNA fragmentation and effectiveness of antioxidants. Hum Reprod, 1998, 13: 1429–36.
VAISSIERE, C., LE CABEC, V., MARIDONNEAU-PARINI, I.: NADPH oxidase is functionally assembled in specific granules during activation of human neutrophils. J Leukoc Biol, 1999, 65: 629–34.
VICARI, E.: Seminal leukocyte concentration and related specific reactive oxygen species production in patients with male accessory gland infections. Hum Reprod, 1999, 14: 2025–30.
WHITTINGTON, K., FORD, W.C.: Relative contribution of leukocytes and of spermatozoa to reactive oxygen species production in human sperm suspensions. Int J Androl, 1999, 22: 229–35.
WOLFF, H.: The biologic significance of white blood cells in semen. Fertil Steril, 1995, 63: 1143–57.
ZALATA, A., HAFEZ, T., COMHAIRE, F.: Evaluation of the role of reactive oxygen species in male infertility. Hum Reprod, 1995, 10: 1444–51.
ZALATA, A.A., CHRISTOPHE, A.B., DEPUYDT, C.E., SCHOONJANS, F., COMHAIRE, F.H.: White blood cells cause oxidative damage to the fatty acid composition of phospholipids of human spermatozoa. Int J Androl, 1998, 21: 154–62.
ZINI, A., DE LAMIRANDE, E., GAGNON, C.: Reactive oxygen species in semen of infertile patients: levels of superoxide dismutase- and catalase-like activities in seminal plasma and spermatozoa. Int J Androl, 1993, 16: 183–8.
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Saez, F., Grizard, G. & Boucher, D. Prostasomes, dérivés actifs de l’oxygène et sperme humain. Androl. 11, 33–48 (2001). https://doi.org/10.1007/BF03034393
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DOI: https://doi.org/10.1007/BF03034393