- Article de Revue
- Published:
Radicaux libres et spermatozoïdes humains: physiologie et physiopathologie
Free radicals and human spermatozoa: Physiology and physiopathology
Andrologie volume 5, pages 369–381 (1995)
Resume
Le mise en évidence de la toxicité de l’oxygène et de ses dérivés sur certaines fonctions du spermatozoïde humain apporte un éclairage nouveau dans le champ des explorations de la fertilité masculine. Des dérivés oxygénés sont détectés dans 40% des spermes provenant d’hommes inféconds. Du fait de la teneur importante de leurs membranes en acides gras polyinsaturés, les spermatozoïdes humains sont particulièrment sensibles à la peroxydation lipidique. Il existe deux sources majeures de dérivés oxygénés dans l’éjaculat, les spermatozoïdes eux mêmes et les leucocytes infiltrés dans le plasma séminal. Leur production dans l’éjaculat est corrélée de manière négative avec le potentiel de fécondation des spermatozoïdes aussi bien in vitro qu’in vivo. Si l’anion superoxyde apparaît comme le produit primaire du système générateur de dérivés oxygénés dans le sperme, le peroxyde d’hydrogène semble être le principal responsable des effets cytotoxiques engendrés par leur production excessive dans l’éjaculat. Cependant, à côté des effets potentiellement néfastes des dérivés oxygénés, il pourrait exister une production physiologique, contrôlée et bénéfique d’espèces radicalaires dans le sperme. A la fois l’anion superoxyde et le peroxyde d’hydrogène pourraint être nécessaires au processus de capacitation et/ ou de réaction acrosomique.
Abstract
The role of reactive oxygen species in the physiopathology of human sperm function has been emphasized in recent years. Their production in semen has been associated with loss of motility, decreased capacity for spermoocyte fusion and loss of fertility. In semen preparations, there are two major sources of reactive oxygen species: leucocytes and spermatozoa themselve. It has been proposed that reactive oxygen species production by human spermatozoa was dependent upon a membrane-bound NADPH oxidase or a mitochondrial diaphorase. Hydrogen peroxide produced by the dismutation of superoxide anion has been recognized as the most toxic oxidizing species for human spermatozoa. Owing to their high content of polyunsaturated fatty acids, it has been proposed that lipid peroxidation of the sperm plasma membrane is largely responsible for defective sperm function. Reactive oxygen species also affect the sperm axoneme as a result of ATP depletion, inhibit mitochondrial functions, and synthesis of DNA, RNA and proteins, produce cytoskeletal modifications and inhibit sperm-oocyte fusion. Human spermatozoa possess enzymatic defence systems such as superoxide dismutase, glutathion peroxidas/reductase and catalase to counteract the toxic effects induced by reactive oxygen species. Correlations have been reported between their effectiveness and the duration of sperm motility. If the excessive production of reactive oxygen species is detrimental for human spermatozoa, they could also participate in the physiological function of the spermatozoa when present at low concentrations. Indeed, reactive oxygen species have been shown to be involved in the activation of several enzymes. Furthermore, sperm capacitation, acrosome reaction and sperm-zona interaction would be enhanced by reactive oxygen species.
References
Aitken R. J., Paterson M., Van Duin M. (1994): Control of fertilization. Présenté au 10éme congrès de l’ESHRE, Bruxelles, 27–29 juin.
Aiken R. J., Ford W. C. L. (1988): Investigation of cellular mechanisms regulating the release of superoxide anion by human spermatozoa. Journal of Reproduction and Fertility, Abst Ser 1, 40.
Aitken R. J., Buckingham D., West K., Wu F. C., Zikopoulos K, Richardson DW (1992): Differential contribution of leucocytes and spermatozoa to the high levels of reactive oxygen species recorded in the ejaculates of oligozoospermic patients. Journal of Reproduction and Fertility, 94, 451–462.
Aitken R. J., Buckingham D. W., Harkiss D. (1993a): Use of a xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. Journal of Reproduction and Fertility, 97, 441–450.
Aitken R. J., Clarkson J. S. (1987): Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. Journal of Reproduction and Fertility, 81, 459–469.
Aitken R. J., Clarkson J. S. (1988): Significance of reactive oxygen species and antioxidants in defining the efficacy of sperm preparation techniques. Journal of Andrology, 9: 367–376.
Aitken R. J., Clarkson J. S., Fishel S. (1989a): Generation of reactive oxygen species, lipid peroxidation and human sperm function. Biology of Reproduction, 40, 183–197.
Aitken R. J., Clarkson J. S., Hargreave T. B., Irvine D. S., Wu F. W. C. (1989b): Analysis of the relationship between defective sperm function and the generation of reactive oxygen species in cases of oligozoospermia. Journal of Andrology, 10, 214–220.
Aitken R. J., Harkiss D., Buckingham D. W. (1993b): Relationship between iron-catalysed lipid peroxidation petential and human sperm function. Journal of Reproduction and Fertility, 98, 257–265.
Aitken R. J., Irvine D. S., Wu F. C. (1991): Prospective analysis of sperm-oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. American Journal of Obstetrics and Gynecology, 164, 542–551.
Aitken R. J., West K. M. (1990): Analysis of the relationship between reactive oxygen species production and leucocyte infiltration in fractions of human semen separated on Percoll gradients. International Journal of Andrology, 13, 433–451.
Alvarez J. G., Storey B. T. (1989): Role of glutathione peroxidase in protecting mammalian spermatozoa from loss of motility caused by spontaneous lipid. Gamete Research, 23, 77–90.
Alvarez J. G., Touchstone J. C., Blasco I., Storey B. T. (1987): Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa. Journal of Andrology, 8, 338–348.
Beapark T., Savemini D., Sneddon J. M., Vane J. R. (1988): Endothélium-derived relaxing factor (EDRF) and superoxide anions modulate platelet adhesion to endothelial cells. Journal of Physiology, 339, 12 P.
Bendich A., Machlin L. J., Scandurro O. (1986): The antioxidant role of vitamin C. Advance in Free radicals Biology and Medicine, 2, 419–444.
Bielski B. J. H., Arudi R. L., Sutherland M. W. (1983): A study of the reactivity of HO2/O2-with unsaturated fatty acids. Journal of Biological Chemistry, vol 258, 8, 4759–4761.
Biemond P., Van Eijk H. G., Swaak A. J. G., Koster J. F. (1984): Iron mobilization from ferritin by superoxide derived from stimulated polymorphonuclear leukocytes: possible mechanism in inflammation. Journal of Clinical Investigation, 73, 1576–1579.
Bize I., Santander G., Cabello P., Driscoll D., Sharpe C. (1991): Hydrogen peroxide is involved in hamster sperm capacitation in vitro. Biology of Reproduction, 44, 398–403.
Block E. R. (1991): Hydrogen peroxide alters the physical state and function of the plasma membrane of pulmonary artery endothelial cells. Journal of Cellular Physiology, 20, 362–369
Chow C. K. (1991): Vitamin E and oxidative stress. Free Radicals Biology and Medicine, 11, 215–232.
Chun Y. S., Kim J. H., Lee H. T., Chung K. S. (1994): Effect of superoxide dismutase on the development of preimplantation mouse embryos. Therigenology, 41, 511–520.
Cillard J., Morel I., Cillard P., Lescoat G., Gicquel M. (1989): Flavonoïds as free radicals scavengers. In: Flavonoïds in Biology and Medicine.
Cillard J., Cillard P. (1987): Antioxidant activity of associated alpha-tocopherol and ascorbic acid in aqueaous media. Revue Française des Corps Gras, 34, 271–274.
Comporti M. (1989): Three models of free radical-induced cell injury. Chemical and Biological interactions, 72, 1–56.
Corey E. J., Mehrotra M. M., Khan A. U. (1987): Water induced dismutation of superoxide anion generates singlet molecular oxygen. Biochemical and Biophysical Research Communication, Vol. 145, 2, 842–846.
De Lamirande E., Gagnon C. (1992a): Reactive oxygen species and human spermatozoa. I-Effects on the motility of intact Spermatozoa and on sperm axonemes. Journal of Andrology, Vol. 13, no 5, 368–378.
De Lamirande E., Gagnon C. (1993a): A positive role for the superoxide anion in triggering hyperactivation and capacitation of human spermatozoa. International Journal of Andrology, 16, 21–25.
De Lamirande E., Gagnon C. (1993b): Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Radicals Biology and Medicine, 14, 157–166.
De Lamirande E., Gagnon C. (1992b): Reactive oxygen species and human spermatozoaII — Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. Journal of Andrology, Vol. 13, no 5, 379–386.
Deby C., Boes M., Pincemail J., Bourdon-Neuray J., Deby-Dupont G. (1990): degradation of membrane phospholipids by a direct nucleophilic action of superoxide anion. Free Radicals, Lipoproteins and Membrane lipids, Eds A Crastes de Paulet, L Douste-Blazy et R paoletti. Plenum Press, New-York, pp 105–113.
Doba T., Burton G. W., Igold K. U. (1985): Antioxidant and co-antioxidant activity of vitamine C. Biochemical Biophysical Acta, 835, 298–303.
Esterbauer H., Shaur R. J., Zollner H. (1991): Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radicals in Biology and Medicine, 11, 81–128.
Evans H., Bishop K. S. (1922): on the existence of a hitherto unrecognised dietary factor essential for reproduction. Science, 56, 650–651.
Fenton H. (1984): Oxidation of tartaric acid in the presence of iron. Journal of Chemical Society, 65, 899–903.
Gopalakrishna R., Anderson W. B. (1989): Ca2+ and phospholipid-independent activation of protein kinase C by the selective oxidative modification of the regulatory domain. Proceeding of the National Academy of Science, USA, 86, 6758–6762.
Griveau J. F., Renard P., Le Lannou D. (1994): An in vitro promoting role of human sperm capacitation for hydrogen peroxide. International Journal of Andrology, 17, 300–307.
Griveau J. F., Dumont E., Renard P., Le Lannou D. (1995): Reactive oxygen species, lipid peroxidation and enzymatic defense systems in human spermatozoa. Journal of Reproduction and Fertility, 103, 17–26.
Griveau J. F., Renard, P., Le Lannou D. (1995): Superoxide anion production by human spermatozoa as a part of the ionophore-induced acrosome reaction in vitro. Internal Journal of Andrology, sous presse.
Griveau J. F., Le Lannou D. (1994): Effects of antioxidants on human sperm preparation techniques. International Journal of Andrology, 17, 225–231.
Iwasaki A., Gagnon C. (1992): Formation of reactive oxygen species in spermatozoa of infertile patients. Fertility and Sterility, 57, no 2, 409–416.
Jeulin C., Soufir J. C., Weber P., Laval-Martin D., Calvayrac R. (1989): Catalase activity in human spermatozoa and seminal plasma. Gamete Research, 24, 185–196.
Jones R., Mann T., Sherins R. J. (1979): Peroxidative breakdown of phospholipids in human spermatozoa: spermicidal effects of fatty acid peroxides and protective action of seminal plasma. Fertility and Sterility, 31, 531–537.
Kessopoulou E., Tomlison M. J., Barrat C. R. L., Bolton A. E., Cooke L. D. (1993): Origin of reactive oxygen species in human semen: spermatozoa or leucocytes? Journal of Reproduction and Fertility, 94, 463–470.
Kinnaird A. A. A., Choy P. C., Man R. Y. K. (1988): Lysophosphatidylcholine accumulation in the ischemic canine heart. Lipids, 23, 32–35.
Koppenol W. H. (1976): reactions involving singlet oxygen and the superoxide anion. Nature, 262, 420–421.
Koshio O., Akanuma Y., Kasuga M. (1988): Hydrogen peroxide stimulates tyrosine phosphorylation of the insulin receptor and its tyrosine kinase activity in intact cells. Biochemical journal, 250, 95–101.
Kovalski N. N., De Lamirand E., Gagnon C. (1992): Reactive oxygen species generated by human neutrophils inhibit sperm motility: protective effect of seminal plasma and scavengers. Fertility and Sterility, vol. 58, 4, 809–816.
Kwenang A., Krous M. J., Koster J. F., Van Eijk H. G. (1987): Iron, ferritin and copper in seminal plasma. Human Reproduction, 2, 387–388.
Mc Cay P. B. (1985): Vitamin E: interactions with free radicals and ascorbate. Annual Revue of Nutrition, 5, 323–340.
Mc Leod J. (1943): The role of oxygen in the metabolism and motility of human spermatozoa. American Journal of Physiology, 138, 512–518.
Mennela M. R. F., Jones R. (1980): Properties of spermatozoal superoxide dismutase and lack of involment of superoxides in metal-iron-catalysed lipid-peroxidation reactions in semen. Biochemical Journal, 191, 289–297.
Niki E., Tsuchiya J., Tanimura R., Kamiya Y. (1982): Role of vitamin C as an antioxidant. Chemistry Letters, 6, 789–792.
Nissen H. P. andKreysel H. W. (1983): Superoxide dismutase in human semen. Klinische Wochenschrift, 61, 63–65.
OHYASHIKI T., TSUKA T., MOHRI T. (1988): Increase of the molecular rigidity of the protein conformation in the intestinal brush-border membranes by lipid peroxidation. Biochemical and Biophysical Acta, 939, 383–392.
Rosen G. M., Barber M. J., Rauckman E. J. (1983): Discription of erythrocyte membranal organization by superoxide. Journal of Biological Chemistry, Vol. 258, 4, 2225–2228.
Salo D. C., Pacifici R. E., Lin S. W., Giulivi C., Davies K. J. (1990): A superoxide dismutase undergoes proteolysis and fragmentation following oxidative modification and inactivation. Journal of Biological Chemistry, 265, 11919–11927.
Selley M. L., Mc Guiness J. A., Jenjin L. A., Bartlett M. R., Ardlie N. G. (1988): Effect of 4+hydroxy-2,3-trans-nonenal on platelet function. Thrombose Haemostase, 59, 143–146.
Selley M. L., Lacey M. J., Bartlett M. R., Copeland C. M., Ardlie N. G. (1991): Content of significant amounts of a cytotoxic end-product of lipid peroxidation in human semen. Journal of Reproduction and Fertility, 92, 291–298.
Sevanian A., Wratten M., Mc Leod L. L., Kim E. (1988): Lipid peroxidation and phospholipase A2 activity in liposomes composed of unsaturated phospholipids: a structural basisfor enzymes activation. Biochemical Biophysical Acta, 961, 316–327.
Valentine J. S., Curtis A. B. (1975): A convenient preparation of solution of superoxide anion and the reaction of superoxide anion with copper (II) complex. Journal of the American Chemical Society, 97, 224–226.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Griveau, J.F., Le Lannou, D. Radicaux libres et spermatozoïdes humains: physiologie et physiopathologie. Androl. 5, 369–381 (1995). https://doi.org/10.1007/BF03034342
Issue Date:
DOI: https://doi.org/10.1007/BF03034342