Skip to main content

Protection of Epididymal Spermatozoa from Oxidative Stress

  • Chapter
  • First Online:
Studies on Men's Health and Fertility
  • 1314 Accesses

Abstract

Mammalian spermatozoa leaving the testis via the rete testis and efferent ducts start a long journey through the epididymis. During their trip along this single tubule, fertilizing potential will gradually be acquired by these spermatozoa. In fine, for most mammals, spermatozoa are stored in the distal epididymal compartment for undetermined periods of time, obviously depending on the male sexual activity. During this phase of post-testicular spermatozoa maturation and storage, the silent nature of these highly differentiated cells renders them particularly fragile and susceptible to attacks, one of which being oxidative stress. It is one of the tasks of the epididymis to provide efficient protection to the male gametes against the deleterious effects of oxidative damage that, if not counteracted, could hamper its structures and function. This is done through the concerted actions of both nonenzymatic and enzymatic primary antioxidants. This chapter intends to give the reader an updated view of the means by which the mammalian epididymis protects transiting spermatozoa from oxidative injuries.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Jones R, Mann T, Sherins RJ. Adverse effects of peroxidized lipid on human spermatozoa. Proc R Soc Lond Biol Sci. 1978;201(1145):413–7.

    CAS  Google Scholar 

  2. Jones R, Mann T, Sherins RJ. Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma. Fertil Steril. 1979;31(5):531–7.

    PubMed  CAS  Google Scholar 

  3. Zalata AA, Chrostophe AB, Depuydt CE, et al. The fatty acid composition of phospholipids of spermatozoa from infertile patients. Mol Hum Reprod. 1998;4(2):11–118.

    Google Scholar 

  4. Halliwell B, Gutteridge JMC. Free radical in biology and medicine. Oxford, UK: Charendon Press; 1999.

    Google Scholar 

  5. Jrad-Lamine A, Henry-Berger J, Gourbeyre P, et al. Deficient-tryptophan catabolism along the kynurenine pathway reveals that the epididymis is in a unique tolerogenic state. J Biol Chem. 2011;286(10):8030–42.

    PubMed  CAS  Google Scholar 

  6. Drevet JR. Glutathione peroxidases expression in the mammalian epididymis and vas deferens. In: Francavilla F, Francavilla S, Forti G, editors. Andrology 2000. L’Aquila, Italy: Collana di “Study Abruzzesi”; 2000. p. 427–61.

    Google Scholar 

  7. Vernet P, Aitken RJ, Drevet JR. Antioxidant strategy in the epididymis. Mol Cell Endocrinol. 2004;216:31–9.

    PubMed  CAS  Google Scholar 

  8. Drevet JR. The antioxidant glutathione peroxidase family and spermatozoa: a complex story. Mol Cell Endocrinol. 2006;250:70–9.

    PubMed  CAS  Google Scholar 

  9. Chabory E, Damon C, Lenoir A, et al. Epididymis seleno-independent glutathione peroxidase 5 (GPx5) contributes to the maintenance of sperm DNA integrity. J Clin Invest. 2009;119:2074–85.

    PubMed  CAS  Google Scholar 

  10. Hinton BT, Palladino MA, Mattmueller DR, et al. Expression and activity of gamma-­glutamyl transpeptidase in the rat epididymis. Mol Reprod Dev. 1991;28(1):40–6.

    PubMed  CAS  Google Scholar 

  11. Zubkova EV, Robaire B. Effect of glutathione depletion on antioxidant enzymes in the epididymis, seminal vesicles, and liver and on spermatozoa motility in the aging brown Norway rat. Biol Reprod. 2004;71(3):1002–8.

    PubMed  CAS  Google Scholar 

  12. Potts RJ, Jefferies TM, Notarianni LJ. Antioxidant capacity of the epididymis. Hum Reprod. 1999;14(10):2513–6.

    PubMed  CAS  Google Scholar 

  13. Nordberg J, Arnér ES. Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med. 2001;31(11):1287–312.

    PubMed  CAS  Google Scholar 

  14. Arnér ES, Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem. 2000;267(20):6102–9.

    PubMed  Google Scholar 

  15. Miranda-Vizuete A, Ljung J, Damdimopoulos AE, et al. Characterization of Sptrx, a novel member of the thioredoxin family specifically expressed in human spermatozoa. J Biol Chem. 2001;276(34):31567–74.

    PubMed  CAS  Google Scholar 

  16. Sadek CM, Damdimopoulos AE, Pelto-Huikko M, et al. Sptrx-2, a fusion protein composed of one thioredoxin and three tandemly repeated NDP-kinase domains is expressed in human testis germ cells. Genes Cells. 2001;6(12):1077–90.

    PubMed  CAS  Google Scholar 

  17. Lewis SE, Sterling ES, Young IS, et al. Comparison of individual antioxidants of sperm and seminal plasma in fertile and infertile men. Fertil Steril. 1997;67(1):142–7.

    PubMed  CAS  Google Scholar 

  18. Regoli F, Winston GW. Quantification of total oxidant scavenging capacity of antioxidants for peroxynitrite, peroxyl radicals, and hydroxyl radicals. Toxicol Appl Pharmacol. 1999;156(2):96–105.

    PubMed  CAS  Google Scholar 

  19. Aitken RJ, Ryan AL, Baker MA, et al. Redox activity associated with the maturation and capacitation of mammalian spermatozoa. Free Radic Biol Med. 2004;36(8):994–1010.

    PubMed  CAS  Google Scholar 

  20. Pruneda A, Yeung CH, Bonet S, et al. Concentrations of carnitine, glutamate and myo-inositol in epididymal fluid and spermatozoa from boars. Anim Reprod Sci. 2007;97:344–55.

    PubMed  CAS  Google Scholar 

  21. Chiu Ming NG, Blackman MR, Wang C, et al. The role of carnitine in the male reproductive system. Ann N Y Acad Sci. 2004;1033:177–88.

    Google Scholar 

  22. Vicari E, Calogero AE. Effects of treatment with carnitines in infertile patients with prostato-vesiculo-epididymitis. Hum Reprod. 2001;16(11):2338–42.

    PubMed  CAS  Google Scholar 

  23. Abd-Allah AR, Helal GK, Al-Yahya AA, et al. Pro-inflammatory and oxidative stress pathways which compromise sperm motility and survival may be altered by l-carnitine. Oxid Med Cell Longev. 2009;2(2):73–81.

    PubMed  Google Scholar 

  24. Wright CE, Tallan HH, Lin YY, et al. Taurine: biological update. Annu Rev Biochem. 1986;55:427–53.

    PubMed  CAS  Google Scholar 

  25. Mrsny RJ, Waxman L, Meizel S. Taurine maintains and stimulates motility of hamster sperm during capacitation in vitro. J Exp Zool. 1979;210(1):123–8.

    PubMed  CAS  Google Scholar 

  26. Alvarez JG, Storey BT. Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility. Biol Reprod. 1983;29(3):548–55.

    PubMed  CAS  Google Scholar 

  27. Hinton BT. The testicular and epididymal luminal amino acid microenvironment in the rat. J Androl. 1990;11(6):498–505.

    PubMed  CAS  Google Scholar 

  28. Aruoma OI, Halliwell B, Hoey BM, et al. The antioxidant action of taurine, hypotaurine and their metabolic precursors. Biochem J. 1988;256(1):251–5.

    PubMed  CAS  Google Scholar 

  29. Schaffer SW, Azuma J, Mozaffari M. Role of antioxidant activity of taurine in diabetes. Can J Physiol Pharmacol. 2009;87:91–9.

    PubMed  CAS  Google Scholar 

  30. Vohra BP, Hui X. Taurine protects against carbon tetrachloride toxicity in the cultured neurons and in vivo. Arch Physiol Biochem. 2001;109(1):90–4.

    PubMed  CAS  Google Scholar 

  31. Wu H, Jin Y, Wei J, Jin H, et al. Mode of action of taurine as a neuroprotector. Brain Res. 2005;1038(2):123–31.

    PubMed  CAS  Google Scholar 

  32. Suzuki T, Suzuki T, Wada T, et al. Taurine as a constituent of mitochondrial tRNAs: new insights into the functions of taurine and human mitochondrial diseases. EMBO J. 2002;21(23):6581–9.

    PubMed  CAS  Google Scholar 

  33. Dacheux JL, Belghazi M, Lanson Y, et al. Human epididymal secretome and proteome. Mol Cell Endocrinol. 2006;250(1–2):36–42.

    PubMed  CAS  Google Scholar 

  34. Roche M, Rondeau P, Singh NR, et al. The antioxidant properties of serum albumin. FEBS Lett. 2008;582:1783–7.

    PubMed  CAS  Google Scholar 

  35. Halliwell B. Albumin—an important extracellular antioxidant? Biochem Pharmacol. 1988;37(4):569–71.

    PubMed  CAS  Google Scholar 

  36. Quinlan GJ, Martin GS, Evans TW. Albumin: biochemical properties and therapeutic potential. Hepatology. 2005;41(6):1211–9.

    PubMed  CAS  Google Scholar 

  37. Forman HJ, Maiorino M, Ursini F. Signaling functions of reactive oxygen species. Biochemistry. 2010;49(5):835–42.

    PubMed  CAS  Google Scholar 

  38. Bartz RR, Piantadosi CA. Clinical review: oxygen as a signaling molecule. Crit Care. 2010;14(5):234.

    PubMed  Google Scholar 

  39. Conrad M, Sandin A, Förster H, et al. 12/15-lipoxygenase-derived lipid peroxides control receptor tyrosine kinase signaling through oxidation of protein tyrosine phosphatases. Proc Natl Acad Sci USA. 2010;107(36):15774–9.

    PubMed  CAS  Google Scholar 

  40. Delaunay A, Pflieger D, Barrault MB, et al. A thiol peroxidase is an H2O2 receptor and redox-transducer in gene activation. Cell. 2002;111:471–81.

    PubMed  CAS  Google Scholar 

  41. Jervis KM, Robaire B. Dynamic changes in gene expression along the rat epididymis. Biol Reprod. 2001;65(3):696–703.

    PubMed  CAS  Google Scholar 

  42. Perry AC, Jones R, Hall L. 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. 1993;293(Pt 1):21–5.

    PubMed  CAS  Google Scholar 

  43. Lewis B, Aitken RJ. Impact of epididymal maturation on the tyrosine phosphorylation patterns exhibited by rat spermatozoa. Biol Reprod. 2001;64(5):1545–56.

    PubMed  CAS  Google Scholar 

  44. O’Flaherty C, de Lamirande E, Gagnon C. Positive role of reactive oxygen species in mammalian sperm capacitation: triggering and modulation of phosphorylation events. Free Radic Biol Med. 2006;41(4):528–40.

    PubMed  Google Scholar 

  45. de Lamirande E, O’Flaherty C. Sperm activation: role of reactive oxygen species and kinases. Biochim Biophys Acta. 2008;1784(1):106–15.

    PubMed  Google Scholar 

  46. Alvarez JG, Storey BT. Role of glutathione peroxidase in protecting mammalian spermatozoa from the loss of motility caused by spontaneous lipid peroxidation. Gamete Res. 1989;2:77–90.

    Google Scholar 

  47. Imai H, Suzuki K, Ishizaka K, et al. Failure of the expression of phospholipid hydroperoxide glutathione peroxidase in the spermatozoa of human infertile males. Biol Reprod. 2001;64:674–83.

    PubMed  CAS  Google Scholar 

  48. Foresta C, Flohé L, Garolla A, et al. Male infertility is linked to the selenoprotein phospholipid hydroperoxide glutathione peroxidase. Biol Reprod. 2002;67:967–71.

    PubMed  CAS  Google Scholar 

  49. Conrad M, Moreno SG, Sinowatz F, et al. The nuclear form of phospholipids hydroperoxide glutathione is a protein thiol peroxidase contributing to sperm chromatin stability. Mol Cell Biol. 2005;25:7637–44.

    PubMed  CAS  Google Scholar 

  50. Imai HN, Hakkaku R, Iwamoto J, et al. Depletion of Selenoprotein GPx4 in spermatocytes causes male infertility in mice. J Biol Chem. 2009;284(47):32009–522.

    Google Scholar 

  51. Liang H, Yoo SH, Na R, et al. Short form glutathione peroxidase 4 is the essential isoform required for survival and somatic mitochondrial functions. J Biol Chem. 2009;284(45):30836–44.

    PubMed  CAS  Google Scholar 

  52. Schneider M, Förster H, Boersma A, et al. Mitochondrial glutathione peroxidase 4 disruption causes male infertility. FASEB J. 2009;23(9):3233–42.

    PubMed  CAS  Google Scholar 

  53. Vernet P, Rigaudiere N, Ghyselinck NB, et al. In vitro expression of a mouse tissue specific glutathione-peroxidase-like protein lacking the selenocysteine can protect stably transfected mammalian cells against oxidative damage. Biochem Cell Biol. 1996;74:125–31.

    PubMed  CAS  Google Scholar 

  54. Vernet P, Rock E, Mazur A, et al. Selenium-independent epididymis-restricted glutathione peroxidase 5 protein (GPX5) can back up failing Se-dependent GPXs in mice subjected to selenium deficiency. Mol Reprod Dev. 1999;54:362–70.

    PubMed  CAS  Google Scholar 

  55. Herbette S, Roeckel-Drevet P, Drevet JR. Seleno-independent glutathione peroxidases. More than simple antioxidant scavengers. FEBS J. 2007;274:2163–80.

    PubMed  CAS  Google Scholar 

  56. Belleannée C, Labas V, Teixeira-Gomes AP, et al. Identification of luminal and secreted ­proteins in bull epididymis. J Proteomics. 2011;74(1):59–78.

    PubMed  Google Scholar 

  57. Hall L, Williams K, Perry AC, et al. The majority of human glutathione peroxidase type 5 (GPX5) transcripts are incorrectly spliced: implications for the role of GPX5 in the male reproductive tract. Biochem J. 1998;333(Pt 1):5–9.

    PubMed  CAS  Google Scholar 

  58. Pontius JU, Wagner L, Schuller GD, Pontius JU, Wagner L, Schuller GD. UniGene a unified view of the transcriptome. In: McEntyre J, Ostell J, editors. The NCBI Handbook. Bethesda, MD: National Center for Biotechnology Information; 2003.

    Google Scholar 

  59. Pushpa-Rebka TR, Bursdall AI, Oleksa M, et al. Rat phospholipids hydroxyperoxide glutathione peroxidase. cDNA cloning and identification of multiple transcription and translation start sites. J Biol Chem. 1995;270:26993–9.

    Google Scholar 

  60. Godeas C, Tramer F, Micali F, et al. Distribution and possible novel role of phospholipid hydroperoxide glutathione peroxidase in rat epididymal spermatozoa. Biol Reprod. 1997;57:1502–8.

    PubMed  CAS  Google Scholar 

  61. Pfeifer HM, Conrad M, Roethlein D, et al. Identification of a specific sperm nuclei selenoenzyme necessary for protamine thiol cross-linking during sperm maturation. FASEB J. 2001;15:1236–8.

    PubMed  CAS  Google Scholar 

  62. Moreno SG, Laux G, Brielmeier M, et al. Testis-specific expression of the nuclear form of phospholipid hydroperoxide glutathione peroxidase (PHGPx). J Biol Chem. 2003;384:635–43.

    CAS  Google Scholar 

  63. Maiorino M, Scapin M, Ursini F, et al. Distinct promoters determine alternative transcription of GPx4 into phospholipids-hydroperoxide glutathione peroxides variants. J Biol Chem. 2003;278:34286–90.

    PubMed  CAS  Google Scholar 

  64. Ursini F, Heim S, Kiess M, et al. Dual function of the selenoprotein PHGPx during sperm maturation. Science. 1999;285:1393–6.

    PubMed  CAS  Google Scholar 

  65. Kleene KC. The mitochondrial capsule selenoprotein-a structural protein in the mitochondrial capsule of mammalian sperm. In: Burk RF, editor. Selenium in biology and human health. New York, NY: Springer; 1994. p. 135–48.

    Google Scholar 

  66. Sivashanmugam P, Rajalakshmi M. Sperm mauration in rhesus monkey: changes in ultrastructure, chromatin condensation, and organization of lipid bilayer. Anat Rec. 1997;247:25–32.

    PubMed  CAS  Google Scholar 

  67. Mammoto A, Matsumoto N, Tahara M, et al. Involvement of s sperm protein sensitive to sulfhydryl-depleting reagents in mouse sperm-egg fusion. J Exp Zool. 1997;278:178–88.

    PubMed  CAS  Google Scholar 

  68. Francavilla S, Cordeschi G, Gabriele A, et al. Chromatin defects in normal and malformed human ejaculated and epididymal spermatozoa: a cytochemical ultrastructural study. J Reprod Fertil. 1996;106(2):259–68.

    PubMed  CAS  Google Scholar 

  69. Mate KE, Kosower NS, White IG, et al. Fluorescent localization of thiols and disulfides in marsupial spermatozoa by brombimane labelling. Mol Reprod Dev. 1994;37:318–25.

    PubMed  CAS  Google Scholar 

  70. Cummins JM, Fleming AD, Crozet N, et al. Labelling of living mammalian spermatozoa with the fluorescent thiol alkylating agent, monobromobimane (MB): immobilization upon exposure to ultraviolet light and analysis of acrosomal status. J Exp Zool. 1986;237: 375–82.

    PubMed  CAS  Google Scholar 

  71. Huang TT, Kosower NK, Yanagimachi R. Localization of thiol and disulfide groups in guinea pig spermatozoa during maturation and capacitation using bimane fluorescent labels. Biol Reprod. 1984;31:797–809.

    PubMed  CAS  Google Scholar 

  72. Imai H, Hirao F, Sakamoto T, et al. Early embryonic lethality caused by targeted disruption of the mouse PHGPx gene. Biochem Biophys Res Commun. 2003;305(2):278–86.

    PubMed  CAS  Google Scholar 

  73. Yant LJ, Ran Q, Rao L, et al. The selenoprotein GPx4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radic Biol Med. 2003;34:496–502.

    PubMed  CAS  Google Scholar 

  74. Flohé L. Selenium in mammalian spermiogenesis. Biol Chem. 2007;388(10):987–95.

    PubMed  Google Scholar 

  75. Shalini S, Bansal MP. Dietary selenium deficiency as well as excess supplementation induces multiple defects in mouse epididymal spermatozoa: understanding the role of selenium in male fertility. Int J Androl. 2008;31(4):438–49.

    PubMed  CAS  Google Scholar 

  76. Weiss K. Importins and exportins: how to get in and out of the nucleus. Trends Biochem Sci. 1998;23(5):185–9.

    Google Scholar 

  77. Maiorino M, Aumann KD, Brigelius-Flohe R, et al. Probing the presumed catalytic triad of selenium-containing peroxidases by mutational analysis of phospholipid hydroperoxide glutathione peroxidase (PHGPx). Biol Chem Hoppe Seyler. 1995;376:651–60.

    PubMed  CAS  Google Scholar 

  78. Manadhar G, Miranda-Vizuete A, Pedrajas JR, et al. Peroxiredoxin 2 and peroxidase enzymatic activity of mammalian spermatozoa. Biol Reprod. 2009;80:1168–77.

    Google Scholar 

  79. O’Flaherty C, de Souza AR. Hydrogen peroxide modifies human sperm peroxiredoxins in a dose-dependent manner. Biol Reprod. 2011;84(2):238–47.

    PubMed  Google Scholar 

  80. Koppers AJ, De Iuliis GN, Nixon B, et al. Significance of mitochondrial reactive oxygen ­species in the generation of oxidative stress in spermatozoa. J Clin Endocrinol Metab. 2008;93(8):3199–207.

    PubMed  CAS  Google Scholar 

  81. Aitken RJ, De Iuliis GN. On the possible origins of DNA damage in human spermatozoa. Mol Hum Reprod. 2009;6(1):3–13.

    Google Scholar 

  82. Aitken RJ. GPx5 protects the family jewels. J Clin Invest. 2009;119:1849–51.

    PubMed  CAS  Google Scholar 

  83. De Iullis GN, Thompson LK, Mitchell LA, et al. DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-2′-deoxyguanosine, a marker of oxidative stress. Biol Reprod. 2009;81:517–24.

    Google Scholar 

  84. Tesarik J, Greco E, Mendoza C. Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum Reprod. 2004;19:611–5.

    PubMed  CAS  Google Scholar 

  85. Tesarik J, Mendoza-Tesarik R, Mendoza C. Sperm nuclear DNA damage: update on the mechanism, diagnosis and treatment. Reprod Biomed Online. 2006;12:715–21.

    PubMed  CAS  Google Scholar 

  86. Baker MA, Aitken RJ. Reactive oxygen species in spermatozoa: methods for monitoring and significance for the origins of genetic disease and infertility. Reprod Biol Endocrinol. 2005;29:3–67.

    Google Scholar 

  87. Aitken RJ, De Iuliis GN, McLachlan RI. Biological and clinical significance of DNA damage in the male germ line. Int J Androl. 2008;32:46–56.

    PubMed  Google Scholar 

  88. Thompson LK, Fleming SD, Aitken RJ, et al. Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Hum Reprod. 2009;24:1061–2070.

    Google Scholar 

  89. Gu W, Hecht NB. Developmental expression of glutathione peroxidase, catalase, and manganese superoxide dismutase mRNAs during spermatogenesis in the mouse. J Androl. 1996;17(3):256–62.

    PubMed  CAS  Google Scholar 

  90. Zini A, Schlegel PN. Catalase mRNA expression in the male rat reproductive tract. J Androl. 1996;17(5):473–80.

    PubMed  CAS  Google Scholar 

  91. Zini A, Schlegel PN. Identification and characterization of antioxidant enzyme mRNAs in the rat epididymis. Int J Androl. 1997;20(2):86–91.

    PubMed  CAS  Google Scholar 

  92. Okuda S, Nishiyama N, Saito H, et al. Hydrogen peroxide-mediated neuronal cell death induced by an endogenous neurotoxin, 3-hydroxykynurenine. Proc Natl Acad Sci USA. 1996;93(22):12553–8.

    PubMed  CAS  Google Scholar 

  93. Okuda S, Nishiyama N, Saito H, et al. 3-Hydroxykynurenine, an endogenous oxidative stress generator, causes neuronal cell death with apoptotic features and region selectivity. J Neurochem. 1998;70(1):299–307.

    PubMed  CAS  Google Scholar 

  94. Wei H, Leeds P, Chen RW, et al. Neuronal apoptosis induced by pharmacological concentrations of 3-hydroxykynurenine: characterization and protection by dantrolene and Bcl-2 overexpression. J Neurochem. 2000;75(1):81–90.

    PubMed  CAS  Google Scholar 

  95. Goldstein LE, Leopold MC, Huang X, et al. 3-Hydroxykynurenine and 3-hydroxyanthranilic acid generate hydrogen peroxide and promote alpha-crystallin cross-linking by metal ion reduction. Biochemistry. 2000;39(24):7266–75.

    PubMed  CAS  Google Scholar 

  96. Lee HJ, Bach JH, Chae HS, et al. Mitogen-activated protein kinase/extracellular signal-­regulated kinase attenuates 3-hydroxykynurenine-induced neuronal cell death. J Neurochem. 2004;88(3):647–56.

    PubMed  CAS  Google Scholar 

  97. Christen S, Peterhans E, Stocker R. Antioxidant activities of some tryptophan metabolites: possible implication for inflammatory diseases. Proc Natl Acad Sci USA. 1990;87(7):2506–10.

    PubMed  CAS  Google Scholar 

  98. Christen S, Thomas SR, Garner B, et al. Inhibition by interferon-gamma of human mononuclear cell-mediated low density lipoprotein oxidation. Participation of tryptophan metabolism along the kynurenine pathway. J Clin Invest. 1994;93(5):2149–58.

    PubMed  CAS  Google Scholar 

  99. Luthra M, Balasubramanian D. 3-Hydroxykynurenine and 3-hydroxyanthranilic acid may act as endogenous antioxidants in the eye lens. Exp Eye Res. 1992;55(4):641–3.

    PubMed  CAS  Google Scholar 

  100. Leipnitz G, Schumacher C, Dalcin KB, et al. In vitro evidence for an antioxidant role of 3-hydroxykynurenine and 3-hydroxyanthranilic acid in the brain. Neurochem Int. 2007;50(1):83–94.

    PubMed  CAS  Google Scholar 

  101. Kanai T, Takahashi K, Inoue H. Three distinct-type glutathione S-transferases from Escherichia coli important for defense against oxidative stress. J Biochem. 2006;140(5):703–11.

    PubMed  CAS  Google Scholar 

  102. Mueller A, Hermo L, Robaire B. The effects of aging on the expression of glutathione S-transferases in the testis and epididymis of the Brown Norway rat. J Androl. 1998;19(4):450–65.

    PubMed  CAS  Google Scholar 

  103. Andonian S, Hermo L. Immunocytochemical localization of the Ya, Yb1, Yc, Yf, and Yo subunits of glutathione S-transferases in the cauda epididymidis and vas deferens of adult rats. J Androl. 1999;20(1):145–57.

    PubMed  CAS  Google Scholar 

  104. Hemachand T, Gopalakrishnan B, Salunke DM, et al. Sperm plasma-membrane-associated glutathione S-transferases as gamete recognition molecules. J Cell Sci. 2002;115(Pt 10):2053–65.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Joël R. Drevet PhD .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Drevet, J.R. (2012). Protection of Epididymal Spermatozoa from Oxidative Stress. In: Agarwal, A., Aitken, R., Alvarez, J. (eds) Studies on Men's Health and Fertility. Oxidative Stress in Applied Basic Research and Clinical Practice. Humana Press. https://doi.org/10.1007/978-1-61779-776-7_5

Download citation

Publish with us

Policies and ethics