Low amounts and high thiol oxidation of peroxiredoxins in spermatozoa from infertile men

Journal of Andrology

Volumn 33, Issue 6, 2012, Pages 1342-1351

  Gong, Shasha ^a,b   Gabriel, Maria C San ^a,b   Zini, Armand ^a,b   Chan, Peter ^a,b   O'flaherty, Cristian ^a,b  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Antioxidants; Oxidative stress; Reactive oxygen species; Sperm dna damage; Sperm function; Thiol groups; Thioloxidized prdx

Indexed keywords

PEROXIREDOXIN 1; PEROXIREDOXIN 6; REACTIVE OXYGEN METABOLITE; THIOL;

ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LIPID PEROXIDATION; MAJOR CLINICAL STUDY; MALE; MALE INFERTILITY; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; SEMINAL PLASMA; SPERMATOZOON; SPERMATOZOON MOTILITY; VARICOCELE;

DNA DAMAGE; HUMANS; INFERTILITY, MALE; LIPID PEROXIDATION; MALE; OXIDATIVE STRESS; PEROXIREDOXIN VI; PEROXIREDOXINS; SEMEN; SPERMATOZOA; SULFHYDRYL COMPOUNDS; VARICOCELE;

EID: 84874443321     PISSN: 01963635     EISSN: 19394640     Source Type: Journal    
DOI: 10.2164/jandrol.111.016162     Document Type: Article

References (62)

1. Agarwal A, Gupta S, Sikka S. The role of free radicals and antioxidants in reproduction. Curr Opin Obstet Gynecol. 2006;18: 325-332.
2. Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol. 2008;59:2-11.
3. Aitken RJ, Baker MA. Oxidative stress, sperm survival and fertility control. Mol Cell Endocrinol. 2006;250:66-69.
4. Aitken RJ, Buckingham D, West K, Wu FC, Zikopoulos K, Richardson DW. Differential contribution of leucocytes and spermatozoa to the generation of reactive oxygen species in the ejaculates of oligozoospermic patients and fertile donors. J Reprod Fertil. 1992;94:451-462.
5. Aitken RJ, Buckingham DW, Carreras A, Irvine DS. Superoxide dismutase in human sperm suspensions: relationship with cellular composition, oxidative stress, and sperm function. Free Radic Biol Med. 1996;21:495-504.
6. Aitken RJ, De Iuliis GN, Finnie JM, Hedges A, McLachlan RI. Analysis of the relationships between oxidative stress, DNA damage and sperm vitality in a patient population: development of diagnostic criteria. Hum Reprod. 2010;25:2415-2426.
7. Aitken RJ, Harkiss D, Buckingham DW. Analysis of lipid peroxidation mechanisms in human spermatozoa. Mol Reprod Dev. 1993;35:302-315.
8. Banmeyer I, Marchand C, Verhaeghe C, Vucic B, Rees JF, Knoops B. Overexpression of human peroxiredoxin 5 in subcellular compartments of chinese hamster ovary cells: effects on cytotoxicity and DNA damage caused by peroxides. Free Radic Biol Med. 2004;36:65-77.
9. Baty JW, Hampton MB, Winterbourn CC. Proteomic detection of hydrogen peroxide-sensitive thiol proteins in Jurkat cells. Biochem J. 2005;389:785-795.
10. Biggers JD, Whitten WK, Whittngham DG. The culture of mouse embryos in vitro. In: Daniel JC, ed. Methods in Mammalian Embryology. San Francisco, CA: Freeman; 1971:86-116.
11. Blumer CG, Fariello RM, Restelli AE, Spaine DM, Bertolla RP, Cedenho AP. Sperm nuclear DNA fragmentation and mitochondrial activity in men with varicocele. Fertil Steril. 2008;90:1716-1722.
12. Carrell DT, Liu L, Peterson CM, Jones KP, Hatasaka HH, Erickson L, Campbell B. Sperm DNA fragmentation is increased in couples with unexplained recurrent pregnancy loss. Arch Androl. 2003; 49:49-55.
13. Cavallini G. Male idiopathic oligoasthenoteratozoospermia. Asian J Androl. 2006;8:143-157.
14. Conrad M, Moreno SG, Sinowatz F, Ursini F, Kolle S, Roveri A, Brielmeier M, Wurst W, Maiorino M, Bornkamm GW. The nuclear form of phospholipid hydroperoxide glutathione peroxidase is a protein thiol peroxidase contributing to sperm chromatin stability. Mol Cell Biol. 2005;25:7637-7644.
15. Cox AG, Hampton MB. Bcl-2 over-expression promotes genomic instability by inhibiting apoptosis of cells exposed to hydrogen peroxide. Carcinogenesis. 2007;28:2166-2171.
16. De Iuliis GN, Thomson LK, Mitchell LA, Finnie JM, Koppers AJ, Hedges A, Nixon B, Aitken RJ. 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;81:517-524.
17. de Kretser DM, Baker HWG. Infertility in men: recent advances and continuing controversies. J Clin Endocrinol Metab. 1999;84: 3443-3450.
18. de Lamirande E, Gagnon C. Impact of reactive oxygen species on spermatozoa: a balancing act between beneficial and detrimental effects. Hum Reprod. 1995;10(suppl 1):15-21.
19. de Lamirande E, Leduc BE, Iwasaki A, Hassouna M, Gagnon C. Increased reactive oxygen species formation in semen of patients with spinal cord injury. Fertil Steril. 1995;63:637-642.
20. Dubuisson M, Vander Stricht D, Clippe A, Etienne F, Nauser T, Kissner R, Koppenol WH, Rees JF, Knoops B. Human peroxiredoxin 5 is a peroxynitrite reductase. FEBS Lett. 2004;571: 161-165.
21. Evenson DP, Larson KL, Jost LK. Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility comparisons with other techniques. J Androl. 2002; 23:25-43.
22. Gagnon C, Iwasaki A, de Lamirande E, Kovalski N. Reactive oxygen species and human spermatozoa. Ann N Y Acad Sci. 1991;637: 436-444.
23. Halliwell B. Oxidative stress and neurodegeneration: where are we now? J Neurochem. 2006;97:1634-1658.
24. Halliwell B, Gutteridge J. Antioxidant defences: endogenous and diet derived. In: Halliwell B, Gutteridge J, eds. Free Radicals in Biology and Medicine. New York, NY: Oxford University Press; 2007a: 79-186.
25. Halliwell B, Gutteridge J. Cellular responses to oxidative stress: adaptation, damage, repair, senescence and death. In: Halliwell B, Gutteridge J, eds. Free Radicals in Biology and Medicine. New York, NY: Oxford University Press; 2007b:187-267.
26. Imai H, Hakkaku N, Iwamoto R, Suzuki J, Suzuki T, Tajima Y, Konishi K, Minami S, Ichinose S, Ishizaka K, Shioda S, Arata S, Nishimura M, Naito S, Nakagawa Y. Depletion of selenoprotein GPx4 in spermatocytes causes male infertility in mice. J Biol Chem. 2009;284:32522-32532.
27. Immenschuh S, Baumgart-Vogt E, Tan M, Iwahara Si, Ramadori G, Fahimi HD. Differential cellular and subcellular localization of heme-binding protein 23/peroxiredoxin I and heme oxygenase-1 in rat liver. J Histochem Cytochem. 2003;51:1621-1631.
28. Iwasaki A, Gagnon C. Formation of reactive oxygen species in spermatozoa of infertile patients. Fertil Steril. 1992;57:409-416.
29. Jacobson G, Karsnas P. Important parameters in semi-dry electrophoretic transfer. Electrophoresis. 1990;11:46-52.
30. 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;68:519-524.
31. Kovalski N, de Lamirande E, Gagnon C. Determination of neutrophil concentration in semen by measurement of superoxide radical formation. Fertil Steril. 1991;56:946-953.
32. Lewis SE, Aitken RJ. DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res. 2005;322:33-41.
33. Li T. The glutathione and thiol content of mammalian spermatozoa and seminal plasma. Biol Reprod. 1975;12:641-646.
34. Liu G, Feinstein SI, Wang Y, Dodia C, Fisher D, Yu K, Ho YS, Fisher AB. Comparison of glutathione peroxidase 1 and peroxiredoxin 6 in protection against oxidative stress in the mouse lung. Free Radic Biol Med. 2010;49:1172-1181.
35. Low FM, Hampton MB, Peskin AV, Winterbourn CC. Peroxiredoxin 2 functions as a noncatalytic scavenger of low-level hydrogen peroxide in the erythrocyte. Blood. 2007;109:2611-2617.
36. Marchetti C, Obert G, Deffosez A, Formstecher P, Marchetti P. Study of mitochondrial membrane potential, reactive oxygen species, DNA fragmentation and cell viability by flow cytometry in human sperm. Hum Reprod. 2002;17:1257-1265.
37. Montjean D, Menezo Y, Benkhalifa M, Cohen M, Belloc S, Cohen-Bacrie P, de Mouzon J. Malonaldehyde formation and DNA fragmentation: two independent sperm decays linked to reactive oxygen species. Zygote. 2010;18:265-268.
38. Oberley TD, Verwiebe E, Zhong W, Kang SW, Rhee SG. Localization of the thioredoxin system in normal rat kidney. Free Radic Biol Med. 2001;30:412-424.
39. O'Brien J, Zini A. Sperm DNA integrity and male infertility. Urology. 2005;65:16-22.
40. O'Flaherty C, de Souza AR. Hydrogen peroxide modifies human sperm peroxiredoxins in a dose-dependent manner. Biol Reprod. 2011;84:238-247.
41. 2 is not reflected in its reaction with other oxidants and thiol reagents. J Biol Chem. 2007;282:11885-11892.
42. 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;62:387-393.
43. 2, a necessary evil for cell signaling. Science. 2006;312:1882-1883.
44. Rhee SG, Chae HZ, Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic Biol Med. 2005a;38:1543-1552.
45. Rhee SG, Kang SW, Jeong W, Chang TS, Yang KS, Woo HA. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol. 2005b;17: 183-189.
46. Saba M, Morales CR, de Lamirande E, Gagnon C. Morphological and biochemical changes following acute unilateral testicular torsion in prepubertal rats. J Urol. 1997;157:1149-1154.
47. Sakkas D, Alvarez JG. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril. 2010;93:1027-1036.
48. Schneider M, Forster H, Boersma A, Seiler A, Wehnes H, Sinowatz F, Neumuller C, Deutsch MJ, Walch A, Hrabe de Angelis M, Wurst W, Ursini F, Roveri A, Maleszewski M, Maiorino M, Conrad M. Mitochondrial glutathione peroxidase 4 disruption causes male infertility. FASEB J. 2009;23:3233-3242.
49. Schremmer B, Manevich Y, Feinstein SI, Fisher AB. Peroxiredoxins in the lung with emphasis on peroxiredoxin VI. Subcell Biochem. 2007;44:317-344.
50. Seo MS, Kang SW, Kim K, Baines IC, Lee TH, Rhee SG. Identification of a new type of mammalian peroxiredoxin that forms an intramolecular disulfide as a reaction intermediate. J Biol Chem. 2000;275:20346-20354.
51. Sharma RK, Agarwal A. Role of reactive oxygen species in male infertility. Urology. 1996;48:835-850.
52. Thannickal VJ, Fanburg BL. Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol. 2000;279:L1005-L1028.
53. Tremellen K. Oxidative stress and male infertility: a clinical perspective. Hum Reprod Update. 2008;14:243-258.
54. Turner TT, Lysiak JJ. Oxidative stress: a common factor in testicular dysfunction. J Androl. 2008;29:488-498.
55. Twigg J, Fulton N, Gomez E, Irvine DS, Aitken RJ. 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.
56. Ursini F, Heim S, Kiess M, Maiorino M, Roveri A, Wissing J, Flohe L. Dual function of the selenoprotein PHGPx during sperm maturation. Science. 1999;285:1393-1396.
57. World Health Organization (WHO). WHO Laboratory Manual for Examination of Human Semen and Semen-Cervical Mucus Interaction. Cambridge, United Kingdom: University Press Cambridge; 1999:1-20.
58. Williams K, Frayne J, Hall L. Expression of extracellular glutathione peroxidase type 5 (GPX5) in the rat male reproductive tract. Mol Hum Reprod. 1998;4:841-848.
59. Woo HA, Kang SW, Kim HK, Yang KS, Chae HZ, Rhee SG. Reversible oxidation of the active site cysteine of peroxiredoxins to cysteine sulfinic acid. Immunoblot detection with antibodies specific for the hyperoxidized cysteine-containing sequence. J Biol Chem. 2003;278:47361-47364.
60. Wood ZA, Poole LB, Karplus PA. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science. 2003a;300: 650-653.
61. Wood ZA, Schroder E, Robin Harris J, Poole LB. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci. 2003b;28:32-40.
62. Zini A, de Lamirande E, Gagnon C. Reactive oxygen species in semen of infertile patients: levels of superoxide dismutase- and catalaselike activities in seminal plasma and spermatozoa. Int J Androl. 1993;16:183-188.