Skip to main content
  • Environnement et Reproduction
  • Stress Oxydant et Spermatozoïdes
  • Published:

Composition lipidique des spermatozoides humains et susceptibilité au stress oxydant avant et après migration dans le mucus cervical

Human sperm lipid content and susceptibility to reactive oxygen species (ROS) before and after migration through human cervical mucus

Resume

L’intérêt porté aux effets physiopathologiques des dérivés actifs de l’oxygène (DAO) dans la fertilité masculine est de plus en plus important. Le spermatozoïde humain est une cellule très vulnérable au stress oxydant compte tenu de sa richesse en acides gras polyinsaturés. L’importance des dommages oxydatifs dans les spermatozoïdes dépend surtout de la capacité des fluides environnants à arrêter la chaîne de peroxydation lipidique membranaire. Les secrétions des tractus génitaux masculins et féminins constituent des microenvironnements qui jouent un rôle déterminant dans l’expression du pouvoir fécondant des spermatozoïdes via des échanges avec la membrane plasmique, et assurent une protection vis-à-vis d’un stress oxydant en maintenant l’équilibre de la balance prooxydants/antioxydants. Le déséquilibre de cette balance dans l’épididyme ou dans le sperme éjaculé, induit plusieurs dysfonctions spermatiques. En revanche, il existe de très rares données concernant les conséquences d’un stress oxydant au niveau du tractus génital féminin sur les caractéristiques spermatiques.

Après avoir abordé, sous forme d’une revue bibliographique, les modifications de la composition lipidique des spermatozoïdes au cours de leur maturation et les effets physiopathologiques des DAO sur les fonctions des spermatozoïdes humains, nous rapportons nos résultats concernant les modifications de la composition lipidique des spermatozoïdes humains après migration dans le mucus cervical et l’influence de la qualité de ce dernier sur les caractéristiques des spermatozoïdes sélectionnés après migration.

Nous avons démontré une baisse des lipides dans les spermatozoïdes humains après migration dans le mucus cervical (vitamine E, cholestérol, phospholipides diacyles, sphingomyéline et plasmalogènes). Cette baisse, associée à un enrichissement lipidique concomitant des mucus cervicaux, est en faveur d’un efflux actif des lipides membranaires des spermatozoïdes vers les glycoprotéines des mucus cervicaux. Par ailleurs, lorsque les mucus cervicaux contenaient des polynucléaires neutrrophiles (PNN), les taux de phospholipides et la quantité de DAO produite par les spermatozoïdes étaient significativement plus élevés que lorsque les spermatozoïdes avaient migré dans des mucus cervicaux dépourvus de PNN. L’infiltration des mucus cervicaux par les PNN joue un rôle possiblement délétère sur les structures et fonctions des spermatozoïdes et inhiberait l’interaction physiologique entre les spermatozoïdes et le mucus cervical.

Abstract

Spermatozoa are particularly susceptible to damage induced by ROS, especially as their plasma membrane contains large amounts of polyunsaturated fatty acids. Mammalian sperm cells develop the capacity to fertilise ova during transport in the male and female reproductive tracts. The nature and quality of the micro-environment of the female reproductive tract are important factors for sperm selection, capacitation and subsequent acrosome reaction.In vitro experiments using capacitating media have shown remodeling of the lipid composition of the sperm membrane during these steps and the same approaches have also shown that a low level of ROS was necessary. The oxidative status of the female genital tract is therefore certainly of primary importance for the physiological maturation of the sperm cell. It has been previously reported that an inappropriate oxidative balance in the male genital tract (ie, an excessive ROS production overwhelming all antioxidant strategies) impairs the structure and several functions of sperm cells. This phenomenon may arise in the female genital tract, but has never been investigated.

The present paper is a review of the literature on these subjects and also reports our results concerning the changes in semen lipid content during cervical mucus migration and the effect of cervical mucus polymorphonuclear (PMN) cells on sperm characteristics.

We showed that the sperm levels of vitamin E, cholesterol, phospholipids, sphingomyelin and plasmalogen assessed by HPLC decreased after migration through cervical mucus. These modifications were observed in parallel with lipid enrichment of the cervical mucus, suggesting an efflux of cholesterol and lipids from sperm cells. The spermatozoa recovered postmigration in the cervical mucus were characterised by low levels of the various lipid classes.

Spermatozoa that migrated in cervical mucus samples with a considerable quantity of polymorphonuclear leukocytes (PMN) also showed significantly increased levels of sphingomyelin, diacyl phospholipids and plasmalogens in comparison to spermatozoa that migrated in cervical mucus devoid of PMN. Finally, we also found that PMA-induced ROS production was significantly increased for spermatozoa treated with cervical mucus containing PMN.

References

  1. AITKEN R.J.: The Amoroso Lecture. The human spermatozoon —a cell in crisis? J. Reprod. Fertil., 1999, 115: 1–7.

    PubMed  CAS  Google Scholar 

  2. AITKEN R.J.: Free radicals, lipid peroxydation and sperm function. Reprod. Fertil. Dev., 1995, 7: 659–669.

    Article  PubMed  CAS  Google Scholar 

  3. AITKEN R.J., BAKER H.W.G.: Seminal leucocytes: passengers, terrorists or good samaritans? Hum. Reprod., 1995, 10: 1736–1739.

    PubMed  CAS  Google Scholar 

  4. AITKEN R.J., CLARKSON J.S.: Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species. J. Reprod. Fertil., 1987, 81: 459–469.

    PubMed  CAS  Google Scholar 

  5. AITKEN R.J., CLARKSON J.S., FISHEL S.: Generation of reactive oxygen species, lipid peroxydation, and human sperm function. Biol. Reprod., 1989, 41: 183–197.

    Article  PubMed  CAS  Google Scholar 

  6. AITKEN R.J., FISHER H.M., FULTON M.et al.: 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: 468–482.

    Article  PubMed  CAS  Google Scholar 

  7. AITKEN R.J., GORDON E., HARKISS D.et al.: Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol. Reprod., 1998, 59: 1037–1046.

    Article  PubMed  CAS  Google Scholar 

  8. 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, c AMP-mediated inductionof tyrosine phosphorylation. J. Cell Sci., 1998, 111: 645–656.

    PubMed  CAS  Google Scholar 

  9. AITKEN RJ., KRAUSZ C.: Oxidative stress, DNA damage and the Y chromosome. Reproduction, 2001, 122: 497–506.

    Article  PubMed  CAS  Google Scholar 

  10. AITKEN R.J., PATERSON M., FISHER H., BUCKINGHAM D.W., 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: 2017–2025.

    PubMed  CAS  Google Scholar 

  11. AITKEN R.J., WEST K., BUCKINGHAM D.: Leukocytic infiltration into the human ejaculate and its association with semen quality, oxidative stress, and sperm function. J. Androl., 1994, 15: 343–352.

    PubMed  CAS  Google Scholar 

  12. ALVAREZ J.G., STOREY B.T.: Differential incorporation of fatty acids into and peroxidative loss of fatty acids from phospholipids of human spermatozoa. Mol. Reprod. Dev., 1995, 42: 334–346.

    Article  PubMed  CAS  Google Scholar 

  13. AMANN R.P., HAMMERSTEDT R.H., VEERAMACHANENI D.N.: The epididymis and sperm maturation: a perspective. Reprod. Fertil. Dev., 1993, 5: 361–381.

    Article  PubMed  CAS  Google Scholar 

  14. AMANN R.P., HAY S.R., HAMMERSTEDT R.H.: Yield, Characteristics, motility and cAMP content of sperm isolated from seven regions of ram epididymis. Biol. Reprod., 1982, 27: 723–733.

    Article  PubMed  CAS  Google Scholar 

  15. AUSTIN C.R.: Capacitation of spermatozoa. Int. J. Fertil., 1967, 12: 25–31.

    PubMed  CAS  Google Scholar 

  16. AUSTIN C.R.: Observations on the penetration of the sperm into the mammalian egg. Aust. J. Res., 1951, 4: 581–596.

    CAS  Google Scholar 

  17. AUSTIN C.R.: The capacitation of the mammalian sperm. Nature., 1952, 170: 326.

    Article  PubMed  CAS  Google Scholar 

  18. AVELDANO M.I., ROTSTEIN N.P., VERMOUTH N.T.: Lipid remodelling during epididymal maturation of rat spermatozoa. Enrichment in plasmenylcholines containing long-chain polyenoic fatty acids of the n-9 series. Biochem. J., 1992, 283: 235–241.

    PubMed  CAS  Google Scholar 

  19. AVELDANO M.I., ROTSTEIN N.P., VERMOUTH N.T.: Occurrence of long and very long polyenoic fatty acids of the n-9 series in rat spermatozoa. Lipids. 1992, 27: 676–680.

    Article  PubMed  CAS  Google Scholar 

  20. BARRATT C.L., COOKE I.D.: Sperm transport in the human female reproductive tract — a dynamic interaction. Int. J. Androl., 1991, 14: 394–411.

    Article  PubMed  CAS  Google Scholar 

  21. CHANG M.C.: Fertilization capacity of spermatozoa deposited into fallopian tubes. Nature, 1951, 168: 697–698.

    Article  PubMed  CAS  Google Scholar 

  22. CROSS N.L.: Role of cholesterol in sperm capacitation. Biol. Reprod., 1998, 159: 7–11.

    Article  Google Scholar 

  23. DELAMIRANDE E., GAGNON C.: Capacitation associated production of superoxide anion by human spermatozoa. Free Rad. Biol. Med., 1995, 18: 487–495.

    Article  CAS  Google Scholar 

  24. DELAMIRANDE E., GAGNON C.: Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Radic. Biol. Med., 1993, 14: 157–166.

    Article  CAS  Google Scholar 

  25. DE LAMIRANDE E., GAGNON C.: Reactive oxygen species and human spermatozoa. I. Effects on the motility of intact spermatozoa and on sperm axonemes. J. Androl., 1992, 13: 368–378.

    PubMed  Google Scholar 

  26. DE LAMIRANDE E., JIANG H., ZINI A., GAGNON C.: Reactive oxygen species and sperm physiology. Rev. Reprod., 1997, 2: 48–54.

    Article  PubMed  Google Scholar 

  27. DELAMIRANDE E., TSAI C., HARAKAT A., GAGNON C.: Involvement of reactive oxygen species in human sperm acrosome reaction induced by A23187, lysophosphatidylcholine, and biologic fluid ultrafiltrates. J. Androl., 1998, 19: 585–594.

    CAS  Google Scholar 

  28. FISHER H.M., AITKEN R.J.: Comparative analysis of the ability of precursor germ cells and epididymal spermatozoa to generate reactive oxygen metabolites. J. Exp. Zool. 1997, 277: 390–400.

    Article  PubMed  CAS  Google Scholar 

  29. FORCE A., GRISARD G., GIRAUD N., MOTTA C., SION B., BOUCHER D.: Membrane fluidity and lipid content of human spermatozoa selected by swim-up method. Int. J. Androl., 2001, 24: 327–334.

    Article  PubMed  CAS  Google Scholar 

  30. GAMZU R., YOGEV L., PAZ G., YAVETZ H., LICHTENBERG D.: Reduction of sperm cholesterol: phospholipid ratio is a possible mechanism for enhancement of human sperm binding to the zona pellucida following incubation with phosphatidylcholine liposomes. Biol. Reprod., 1997, 57: 539–546.

    Article  PubMed  CAS  Google Scholar 

  31. GIL-GUZMAN E., ORELLO M., LOPEZ M.C.et al.: Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. Hum. Reprod., 2001, 16: 1922–1930.

    Article  PubMed  CAS  Google Scholar 

  32. GO K.J., WOLF D.P.: Albumin-mediated changes in sperm sterol content during capacitation. Biol. Reprod., 1985, 32: 145–153.

    Article  PubMed  CAS  Google Scholar 

  33. GOMEZ E., BUCKINGHAM D., BRINDLE J., LANZAFAME F., IRVINE S.D., AITKEN R.J.: Development of image analysis system to monitor the retention of residual cytoplasm by human spermatozoa: correlation with biochemical markers of cytoplasmic space, oxidative stress and sperm function. J. Androl., 1996, 17: 276–287.

    PubMed  CAS  Google Scholar 

  34. GOULD J.E., OVERSTREET J.W., HANSON F.W.: Assessment of human sperm function after recovery from the female reproductive tract. Biol. Reprod., 1984, 31: 888–894.

    Article  PubMed  CAS  Google Scholar 

  35. GRIVEAU J.F., DUMONT E., RENARD P., CALLEGARI J.P., LE LANNOU D.: Reactive oxygen species, lipid peroxidation and enzymatic defence systems in human spermatozoa. J. Reprod. Fertil., 1995, 103: 17–26.

    PubMed  CAS  Google Scholar 

  36. GRIVEAU J.F., LELANNOU D.: Reactive oxygen species and human spermatozoa: physiology and pathology. Int. J. Androl., 1997, 20: 61–69.

    Article  PubMed  CAS  Google Scholar 

  37. GRIVEAU J.F., RENARD P., LE LANNOU D.: Anin vitro promoting role for hydrogen peroxide in human sperm capacitation. Int. J. Androl., 1994, 17: 300–307.

    Article  PubMed  CAS  Google Scholar 

  38. 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.

    Article  PubMed  CAS  Google Scholar 

  39. GRIZARD G., BAUCHART D., BOUCHER D.: Separation and quantification of cholesterol and major phopholipid classes in human semen by high-performance liquid chromatography and light scattering detection. J. Chromatography B, 2000, 740: 101–107.

    Article  CAS  Google Scholar 

  40. HAIDL G., OPPER C.: Changes in lipids and membrane anisotropy in human spermatozoa during epididymal maturation. Hum. Reprod., 1997, 12: 2720–2723.

    Article  PubMed  CAS  Google Scholar 

  41. HAMAMAH S., LANSON, M., BARTHELEMY, C.et al.: Analysis of the lipid content and the motility of human sperm after follicular fluid treatment. Andrologia, 1995, 27: 91–97.

    Article  PubMed  CAS  Google Scholar 

  42. HOSHI K., AITA T., YANAGIDA 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.

    PubMed  CAS  Google Scholar 

  43. HUSZAR G., SBARACIA M., VIGUE L., MILLER D.J., SHUR B.D.: Sperm plasma membrane remodeling during spermiogenetic maturation in men: relationship among plasma membrane beta 1, 4-galactosyltransferase, cytoplasmic creatine phosphokinase, and creatine phosphokinase isoform ratios. Biol. Reprod., 1997, 56: 1020–1024.

    Article  PubMed  CAS  Google Scholar 

  44. 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.

    PubMed  CAS  Google Scholar 

  45. JONES R.: Plasma membrane structure and remodelling during sperm maturation in the epididymis. J. Reprod. Fertil. Suppl., 1998, 53: 73–84.

    PubMed  CAS  Google Scholar 

  46. JONES R., MANN T., SHERINS R.: Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal propreties of fatty acid peroxides and protective action of seminal plasma. Fertil. Steril., 1979, 31: 531–537.

    PubMed  CAS  Google Scholar 

  47. JONES R., MANN T.: Lipid peroxides in spermatozoa; formation, role, of plasmalogen and physiological significance. Proc. Roy. Soc. London B, 1976, 193: 317–333.

    Article  CAS  Google Scholar 

  48. KATZ D.F., DROBNIS E.Z., OVERSTREET J.W.: Factors regulating mammalian sperm migration through the female reproductive tract and oocyte vestments. Gamete Res., 1989, 22: 443–469.

    Article  PubMed  CAS  Google Scholar 

  49. KIM J.G., PARTHASARATHY S.: Oxidation and the spermatozoa. Sem. Reprod. Endocrinol., 1998, 16: 235–239.

    Article  CAS  Google Scholar 

  50. KRAUSZ C., MILLIS C., ROGERS S., TAN S.L., AITKEN R.J.: Stimulation of oxidant generation by human sperm suspensions using phorbol esters and formyl peptides: Relation ships with motility and fertilizationin vitro. Fertil. Steril., 1994, 62: 599–605.

    PubMed  CAS  Google Scholar 

  51. LAMBERT H., OVERSTREET J.W., MORALES P.et al.: Sperm capacitation in the human female reproductive tract. Fertil. Steril., 1985, 43: 325–327.

    PubMed  CAS  Google Scholar 

  52. LANGLAIS J., KAN F.W., GRANGER L., RAYMOND L., BLEAU G., ROBERTS K.D.: Identification of sterol acceptors that stimulate cholesterol efflux from human spermatozoa duringin vitro capacitation. Gamete Res., 1988, 20: 185–201.

    Article  PubMed  CAS  Google Scholar 

  53. LECLERC P., DELAMIRANDE E., GAGNON C.: Regulation of protein-tyrosine phosphorylation and human sperm capacitation by reactive oxygen derivatives. Free Radic. Biol. Med., 1997, 22: 643–656.

    Article  PubMed  CAS  Google Scholar 

  54. LENZI A., GANDINI L., MARESCA V.et al.: Fatty acid composition of spermatozoa and immature germ cells. Mol. Hum. Reprod., 2000, 6: 226–231.

    Article  PubMed  CAS  Google Scholar 

  55. LIN Y., KAN F.W.: Regionalization and redistribution of membrane phospholipids and cholesterol in mouse spermatozoa duringin vitro capacitation. Biol. Reprod., 1996, 55: 1133–1146.

    Article  PubMed  CAS  Google Scholar 

  56. LIN D.S., CONNOR W.E., WOLF D.P., NEURINGER M., HACHEY D.L.: Unique lipids of primate spermatozoa: desmosterol and docosahexaenoic acid. J. Lipid Res., 1993, 34: 491–499.

    PubMed  Google Scholar 

  57. OLLERO M., GIL-GUZMAN E., LOPEZ M.C.et al.: Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum. Reprod., 2001, 16: 1912–1921.

    Article  PubMed  CAS  Google Scholar 

  58. OLLERO M., POWERS R.D., ALVAREZ J.G.: Variation of docosahexaenoic acid content in subsets of human spermatozoa at different stages of maturation: implications for sperm lipoperoxidative damage. Mol. Reprod. Dev., 2000, 55: 326–334.

    Article  PubMed  CAS  Google Scholar 

  59. OSHEROFF J.E., VISCONTI P.E., VALENZUELA J.P., TRAVIS A.J., ALVAREZ J., KOPF G.S.: Regulation of human sperm capacitation by cholesterol efflux stimulated signal transduction pathway leading to protein kinase A mediated up regulation of protein tyrosine phosphorylation. Mol. Hum. Reprod., 1999, 5: 1017–1026.

    Article  PubMed  CAS  Google Scholar 

  60. PARKS J.E., HAMMERSTEDT R.H.: Development changes occurring in the lipids of ram epididymal spermatozoa plasma membrane. Biol. Reprod., 1985, 32: 653–668.

    Article  PubMed  CAS  Google Scholar 

  61. POULOS A., DARIN-BENNETT A., WHITE I.G.: The phospholipids-bound fatty acids and aldehydes of mammalian spermatozoa. Comp. Biochem. Physiol., 1973, 46: 541–549.

    Article  CAS  Google Scholar 

  62. RAMOS L., WETZELS A.: Low rates of DNA fragmentation in selected motile human spermatozoa assessed by the TUNEL assay. Hum. Reprod., 2001, 16: 1703–1707.

    Article  PubMed  CAS  Google Scholar 

  63. RICHER S.C., FORD W.C.A.: Critical investigation of NADPH oxidase activity in human spermatozoa. Mol. Hum. Reprod., 2001, 3: 237–244.

    Article  Google Scholar 

  64. SALEH R.A., AGARWAL A., KANDIRALI E.et al.: Leukocytospermia is associated with increased reactive oxygen species production by human spermatozoa. Fertil. Steril., 2002, 78: 1215–1224.

    Article  PubMed  Google Scholar 

  65. THEROND P., COUTURIER M., DEMELIER J.F., LEMONNIER F.: Simultaneous determination of the main molecular species of soybean phosphatidylcholine or phosphatidylethanolamine and their corresponding hydroperoxides obtained by lipoxygenase treatment. Lipids, 1993, 28: 245–249.

    Article  PubMed  CAS  Google Scholar 

  66. 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: 2418–2421.

    Article  PubMed  CAS  Google Scholar 

  67. TOMLINSON M.J., BARRATT C.L., COOKE I.D.: Prospective study of leukocytes and leukocyte subpopulations in semen suggests they are not a cause of male infertility. Fertil. Steril., 1993, 60: 1069–1075.

    PubMed  CAS  Google Scholar 

  68. TOMLINSON M.J., WHITE A., BARRATT C.L., BOLTON A.E., COOKE I.D.: The removal of morphologically abnormal sperm forms by phagocytes: a positive role for seminal leukocytes? Hum. Reprod., 1992, 7: 517–522.

    PubMed  CAS  Google Scholar 

  69. TOSHIMORI K.: Maturation of mammalian spermatozoa: modifications of the acrosome and plasma membrane leading to fertilization. Cell Tissue Res., 1998, 293: 177–187.

    Article  PubMed  CAS  Google Scholar 

  70. MICHAEL L., AITKEN R.J.: Iatrogenic DNA damage induced in human spermatozoa during sperm preparation: protective significance of seminal plasma. Mol. Hum. Reprod., 1998, 4: 439–445.

    Article  PubMed  Google Scholar 

  71. 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: 1429–1436.

    Article  PubMed  CAS  Google Scholar 

  72. 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: 229–235.

    Article  PubMed  CAS  Google Scholar 

  73. WOLFF H.: The biologic significance of white blood cells in semen. Fertil. Steril., 1995, 63: 1143–1157.

    PubMed  CAS  Google Scholar 

  74. WORLD HEALTH ORGANISATION (WHO): Laboratory manual for the examination of human semen and semen-cervical mucus interaction. 2nd ed. Cambridge, United Kingdom, The press syndicate of the University of Cambridge, 1999.

    Google Scholar 

  75. YANAGIMACHI R.: Fertility of mammalian spermatozoa: its development and relativity. Zygote, 1994, 2: 371–372.

    PubMed  CAS  Google Scholar 

  76. ZALATA A.A., CHRISTOPHE A.B., DEPUYDT C.E., SCHOONJANS F., COMHAIRE F.H.: The fatty acid composition of phospholipids of spermatozoa from infertile patients. Mol. Hum. Reprod., 1998, 4: 111–118.

    Article  PubMed  CAS  Google Scholar 

  77. ZALATA A.A., CHRISTOPHE A.B., DEPUYDT C.E., SCHOONJANS F., COMHAIRE F.H.: White blood cells cause oxidative damage to fatty acid composition of phospholipids of human spermatozoa. Int. J. Androl., 1998, 21: 154–162.

    Article  PubMed  CAS  Google Scholar 

  78. ZHU J., BARRATT C.L., LIPPES J.et al.: The sequential effects of human cervical mucus, oviductal fluid, and follicular fluid on sperm function. Fertil. Steril., 1994, 61: 1129–1135.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nozha Chakroun Feki.

Additional information

Prix DEA, SALF 2002.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chakroun Feki, N., Therond, P., Jouannet, P. et al. Composition lipidique des spermatozoides humains et susceptibilité au stress oxydant avant et après migration dans le mucus cervical. Androl. 13, 381–392 (2003). https://doi.org/10.1007/BF03035205

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03035205

Mots clés

Key words