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Évolution de la composante lipidique de la membrane plasmique des spermatozoïdes durant la maturation épididymaire

Changes in spermatozoa plasma membrane lipid composition during epididymal maturation

Résumé

Un des aspects de la maturation posttesticulaire des spermatozoïdes chez les mammifères est l’évolution progressive de la composition lipidique de la membrane plasmique des gamètes males qui permet à ces derniers d’acquérir des capacités fusogènes particulières déterminantes pour la fécondation. Une part importante de cette modification du contenu lipidique de la membrane des gamètes males est assurée lors de la descente des spermatozoïdes dans le tubule épididymaire. Les mouvements lipidiques seront ensuite poursuivis dans les voies génitales femelles au cours d’un processus dynamique, la capacitation, étape préalable indispensable à la réaction acrosomique, et donc, à la fécondation. Cette revue fait l’état des lieux des connaissances acquises par divers groupes de recherche dans le premier volet épididymaire de la maturation lipidique des gamètes males dans différents modèles de mammifères.

Abstract

One aspect of mammalian post-testicular sperm maturation is the progressive change in their plasma membrane lipid composition. These modifications in lipids allow sperm cells to fuse with oocytes during fertilization. A significant share of these sperm lipid changes occurs during their descent through the epididymal tubule. It then continues within the female genital tract during the capacitation process, an essential prerequisite for acrosomic reaction and hence fertilization. This review presents what is known concerning the sperm plasma membrane lipid changes during epididymal maturation in various mammalian models. In the first section, after a brief presentation of the classic eukaryotic cell plasma membrane lipid organization, the emphasis is on the particularities of sperm plasma membrane lipids. The second section presents the different changes occurring in the three major classes of lipids (i.e. phospholipids, sterols and fatty acids) during the sperm’s epididymal descent. The final section briefly describes the mechanisms by which these lipid changes might happen in the epididymal lumen environment. The role played by lipid-rich vesicles secreted by the epididymal epithelium via apocrine secretory processes is highlighted.

Abbreviations

AG:

acides gras

AGI:

acides gras insaturés

AGPI:

acides gras polyinsaturés

AGS:

acides gras saturés

AA:

acide arachidonique

Chol:

cholestérol

DHA:

acide docosahexaénoïque

DPA:

acide docosapentanoïque

EORs:

espèces oxygénées réactives

PC:

phosphatidylcholine

PE:

phosphatidyléthanolamine

PS:

phosphatidylsérine

PI:

phosphatidylinositol

PG:

phosphatidylglycérol

CL:

cardiolipine

DPG:

diphosphatidylglycérol

PL:

lysophospholipides

SM:

sphingomyéline

SOD:

superoxyde dismutase

GPX:

glutathion peroxydase

GPI:

glycosyl phosphatidylinositol

Références

  1. 1.

    Sinowatz F, Volgmayr JK, Gabius HJ, Friess AE (1989) Cytochemical analysis of mammalian sperm membranes. Prog Histochem Cytochem 19:1–74

    PubMed  CAS  Article  Google Scholar 

  2. 2.

    Peterson RN, Russell LD (1985) The mammalian spermatozoon: a model for the study of regional specificity in plasma membrane organization and function. Tissue Cell 17:769–791

    PubMed  CAS  Article  Google Scholar 

  3. 3.

    Adams CS, Johnson AD (1977) The lipid content of epididymal spermatozoa of Rattus norvegicus. Comp Biochem Physiol B 58:409–411

    PubMed  CAS  Article  Google Scholar 

  4. 4.

    Evans JP, Kopf GS, Schultz RM (1997) Characterization of the binding of recombinant mouse sperm fertilin beta subunit to mouse eggs: evidence for adhesive activity via an egg beta1 integrin-mediated interaction. Dev Biol 187:79–93

    PubMed  CAS  Article  Google Scholar 

  5. 5.

    Evans RW, Setchell BP (1979) Lipid changes in boar spermatozoa during epididymal maturation with some observations on the flow and composition of boar rete testis fluid. J Reprod Fertil 57:189–196

    PubMed  CAS  Article  Google Scholar 

  6. 6.

    Johnson LA, Gerrits RJ, Young EP (1969) The fatty acid composition of porcine spermatozoa phospholipids. Biol Reprod 1:330–334

    PubMed  CAS  Article  Google Scholar 

  7. 7.

    Poulos A, Brown-Woodman PD, White IG, Cox RI (1975) Changes in phospholipids of ram spermatozoa during migration through the epididymis and possible origin of prostaglandin F2alpha in testicular and epididymal fluid. Biochim Biophys Acta 388:12–18

    PubMed  CAS  Article  Google Scholar 

  8. 8.

    Poulos A, White IG (1973) The phospholipid composition of human spermatozoa and seminal plasma. J Reprod Fertil 35:265–272

    PubMed  CAS  Article  Google Scholar 

  9. 9.

    Agrawal P, Magargee SF, Hammerstedt RH (1988) Isolation and characterization of the plasma membrane of rat cauda epididymal spermatozoa. J Androl 9:178–189

    PubMed  CAS  Article  Google Scholar 

  10. 10.

    Hall JC, Hadley J, Doman T (1991) Correlation between changes in rat sperm membrane lipids, protein, and the membrane physical state during epididymal maturation. J Androl 12:76–87

    PubMed  CAS  Google Scholar 

  11. 11.

    Nikolopoulou M, Soucek DA, Vary JC (1985) Changes in the lipid content of boar sperm plasma membranes during epididymal maturation. Biochim Biophys Acta 815:486–498

    PubMed  CAS  Article  Google Scholar 

  12. 12.

    Parks JE, Arion JW, Foote RH (1987) Lipids of plasma membrane and outer acrosomal membrane from bovine spermatozoa. Biol Reprod 37:1249–1258

    PubMed  CAS  Article  Google Scholar 

  13. 13.

    Parks JE, Hammerstedt RH (1985) Development changes occurring in the lipids of ram epididymal spermatozoa plasma membrane. Biol Reprod 32:653–668

    PubMed  CAS  Article  Google Scholar 

  14. 14.

    Rana AP, Majumder GC, Misra S, Ghosh A (1991) Lipid changes of goat sperm plasma membrane during epididymal maturation. Biochim Biophys Acta 1061:185–196

    PubMed  CAS  Article  Google Scholar 

  15. 15.

    Rana AP, Misra S, Majumder GC, Ghosh A (1993) Phospholipid asymmetry of goat sperm plasma membrane during epididymal maturation. Biochim Biophys Acta 1210:1–7

    PubMed  CAS  Article  Google Scholar 

  16. 16.

    Alvarez JG, Storey BT (1995) Differential incorporation of fatty acids into and peroxidative loss of fatty acids from phospholipids of human spermatozoa. Mol Reprod Dev 42:334–346

    PubMed  CAS  Article  Google Scholar 

  17. 17.

    Aveldaño MI, Rotstein NP, Vermouth NT (1992) Lipid remodelling during epididymal maturation of rat spermatozoa. Enrichment in plasmenylcholines containing long-chain polyenoic fatty acids of the n-9 series. Biochem J 283(Pt 1):235–241

    PubMed  PubMed Central  Article  Google Scholar 

  18. 18.

    Awano M, Kawaguchi A, Mohri H (1993) Lipid composition of hamster epididymal spermatozoa. J Reprod Fertil 99:375–383

    PubMed  CAS  Article  Google Scholar 

  19. 19.

    Touchstone JC, Alvarez JG, Levin SS, Storey BT (1985) Evidence for diplasmalogen as the major component of rabbit sperm phosphatidylethanolamine. Lipids 20:869–875

    PubMed  CAS  Article  Google Scholar 

  20. 20.

    Murray RK, Mayes PA, Granner DK, Rodwell WR (eds) (1999) Harper’s Biochemistry. 24th ed, London.

  21. 21.

    Shechter E (2000) Fluidité membranaire. In: Schecter E, Rossignol B (eds) Biochimie et biophysique des membranes. Aspects structuraux et fonctionnels. Masson, Paris, pp. 97–121

    Google Scholar 

  22. 22.

    Yeagle P (1982) The structure of biological membranes. In: Yeagle P (ed), CRC Press, Boca Raton, pp. 175–210

    Google Scholar 

  23. 23.

    Yeagle P (1993) The membranes of cells. Academic Press, San Diego

    Google Scholar 

  24. 24.

    Ladha S (1998) Lipid heterogeneity and membrane fluidity in a highly polarized cell, the mammalian spermatozoon. J Membr Biol 165:1–10

    PubMed  CAS  Article  Google Scholar 

  25. 25.

    Alberts B, Bray D, Lewis J, et al (1994) Membrane structure. Part. III, Chapter 10. In: Molecular biology of the cell. 3rd ed, Garland Publishing, New York, pp. 478–524

    Google Scholar 

  26. 26.

    Jones R (1998) Plasma membrane structure and remodelling during sperm maturation in the epididymis. J Reprod Fertil Suppl 53:73–84

    PubMed  CAS  Google Scholar 

  27. 27.

    Selivonchick DP, Schmid PC, Natarajan V, Schmid HH (1980) Structure and metabolism of phospholipids in bovine epididymal spermatozoa. Biochim Biophys Acta 618:242–254

    PubMed  CAS  Article  Google Scholar 

  28. 28.

    Wolf DE, Lipscomb AC, Maynard VM (1988) Causes of nondiffusing lipid in the plasma membrane of mammalian spermatozoa. Biochemistry 27:860–865

    PubMed  CAS  Article  Google Scholar 

  29. 29.

    Ollero M, Powers RD, Alvarez JG (2000) Variation of docosahexaenoic acid content in subsets of human spermatozoa at different stages of maturation: implications for sperm lipoperoxidative damage. Mol Reprod Dev 55:326–324

    PubMed  CAS  Article  Google Scholar 

  30. 30.

    Cross NL (1996) Human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist, progesterone: cholesterol is the major inhibitor. Biol Reprod 54:138–145

    PubMed  CAS  Article  Google Scholar 

  31. 31.

    Rejraji H, Sion B, Prensier G, et al (2006) Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation. Biol Reprod 74:1104–1113

    PubMed  CAS  Article  Google Scholar 

  32. 32.

    Christova Y, James P, Mackie A, et al (2004) Molecular diffusion in sperm plasma membranes during epididymal maturation. Mol Cell Endocrinol 216:41–46

    PubMed  CAS  Article  Google Scholar 

  33. 33.

    James PS, Wolfe CA, Ladha S, Jones R (1999) Lipid diffusion in the plasma membrane of ram and boar spermatozoa during maturation in the epididymis measured by fluorescence recovery after photobleaching. Mol Reprod Dev 52:207–215

    PubMed  CAS  Article  Google Scholar 

  34. 34.

    Rana AP, Majumder GC (1990) Changes in the fluidity of the goat sperm plasma membrane in transit from caput to cauda epididymis. Biochem Int 21:797–803

    PubMed  CAS  Google Scholar 

  35. 35.

    Hinkovska VT, Dimitrov GP, Koumanov KS (1986) Phospholipid composition and phospholipid asymmetry of ram spermatozoa plasma membranes. Int J Biochem 18:1115–1121

    PubMed  CAS  Article  Google Scholar 

  36. 36.

    Perry AC, Jones R, Hall L (1993) Isolation and characterization of a rat cDNA clone encoding a secreted superoxide dismutase reveals the epididymis to be a major site of its expression. Biochem J 293(Pt 1):21–25

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  37. 37.

    Drevet JR (2000) Glutathione peroxydases expression in the mammalian epididymis and vas deferens. In: Francavilla F, Francavilla S, Forti G (eds) Andrology. L’Aquilla, Italy, pp. 427–461

    Google Scholar 

  38. 38.

    Drevet JR (2006) The antioxidant glutathione peroxidase family and spermatozoa: a complex story. Mol Cell Endocrinol 250:70–79

    PubMed  CAS  Article  Google Scholar 

  39. 39.

    Ghyselinck NB, Dufaure I, Lareyre JJ, et al (1993) Structural organization and regulation of the gene coding for the androgendependent glutathione peroxidase-like protein specific to the mouse epididymis. Mol Endocrinol 7:258–272

    PubMed  CAS  Google Scholar 

  40. 40.

    Rejraji H, Drevet JR (2004) Sécrétions apocrines dans le tractus génital male: rôles potentiels dans la maturation des spermatozoïdes. Andrologie 14:22–33

    Article  Google Scholar 

  41. 41.

    Saez F, Frenette G, Sullivan R (2003) Epididymosomes and prostasomes: their roles in posttesticular maturation of the sperm cells. J Androl 24:149–154

    PubMed  Article  Google Scholar 

  42. 42.

    Frenette G, Lessard C, Sullivan R (2002) Selected proteins of “prostasome-like particles” from epididymal cauda fluid are transferred to epididymal caput spermatozoa in bull. Biol Reprod 67:308–313

    PubMed  CAS  Article  Google Scholar 

  43. 43.

    Girouard J, Frenette G, Sullivan R (2008) Seminal plasma proteins regulate the association of lipids and proteins within detergentresistant membrane domains of bovine spermatozoa. Biol Reprod 78:921–931

    PubMed  CAS  Article  Google Scholar 

  44. 44.

    Rooney IA, Heuser JE, Atkinson JP (1996) 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 97:1675–1686

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  45. 45.

    Kirchhoff C, Pera I, Derr P, et al (1997) The molecular biology of the sperm surface. Post-testicular membrane remodelling. Adv Exp Med Biol 424:221–232

    PubMed  CAS  Article  Google Scholar 

  46. 46.

    Rooney IA, Atkinson JP, Krul ES, et al (1993) 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 177:1409–1420

    PubMed  CAS  Article  Google Scholar 

  47. 47.

    Gaudreault C, El Alfy M, Légaré C, Sullivan R (2001) Expression of the hamster sperm protein P26h during spermatogenesis. Biol Reprod 65:79–86

    PubMed  CAS  Article  Google Scholar 

  48. 48.

    Gaudreault C, Montfort L, Sullivan R (2002) Effect of immunization against recombinant P26h on fertility rates. Reproduction 123:307–313

    PubMed  CAS  Article  Google Scholar 

  49. 49.

    Gaudreault C, Légaré C, Bérubé B, Sullivan R (1999) Hamster sperm protein, p26h: a member of the short-chain dehydrogenasereductase superfamily. Biol Reprod 61:264–273

    PubMed  CAS  Article  Google Scholar 

  50. 50.

    Légaré C, Thabet M, Picard S, Sullivan R (2001) Effect of vasectomy on P34H messenger ribonucleic acid expression along the human excurrent duct: a reflection on the function of the human epididymis. Biol Reprod 64:720–727

    PubMed  Article  Google Scholar 

  51. 51.

    Madore N, Smith KL, Graham CH, et al (1999) Functionally different GPI proteins are organized in different domains on the neuronal surface. Embo J 18:6917–6926

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  52. 52.

    Rietveld A, Simons K (1998) The differential miscibility of lipids as the basis for the formation of functional membrane rafts. Biochim Biophys Acta 1376:467–469

    PubMed  CAS  Article  Google Scholar 

  53. 53.

    Kirchhoff C (1998) Molecular characterization of epididymal proteins. Rev Reprod 3:86–95

    PubMed  CAS  Article  Google Scholar 

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Correspondence to J. -R. Drevet.

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Rejraji, H., Saez, F. & Drevet, J.-. Évolution de la composante lipidique de la membrane plasmique des spermatozoïdes durant la maturation épididymaire. Basic Clin. Androl. 19, 17–28 (2009). https://doi.org/10.1007/s12610-008-0006-7

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Mots clés

  • Spermatozoïdes
  • Maturation posttesticulaire
  • Mammifères
  • Lipides

Keywords

  • Spermatozoa
  • Post-testicular maturation
  • Mammals
  • Lipids