Sperm motility is lost in vitro as a consequence of mitochondrial free radical production and the generation of electrophilic aldehydes but can be significantly rescued by the presence of nucleophilic thiols

Biology of Reproduction

Volumn 87, Issue 5, 2012, Pages

  Aitken, R John ^a   Gibb, Zamira ^a   Mitchell, Lisa A ^a   Lambourne, Sarah R ^a   Connaughton, Haley S ^a   De Iuliis, Geoffry N ^a  

^a UNIVERSITY OF NEWCASTLE   (Australia)

Author keywords

Gamete biology; Mitochondria; Oxidative stress; Sperm; Sperm motility and transport

Indexed keywords

ACETYLCYSTEINE; ALDEHYDE; HOMOCYSTEINE; NUCLEOPHILE; PENICILLAMINE; REACTIVE OXYGEN METABOLITE; THIOL DERIVATIVE; THIOMALIC ACID;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIPID PEROXIDATION; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; SPERM PRESERVATION; SPERMATOZOON MOTILITY; SURVIVAL;

ALDEHYDES; ANIMALS; FREE RADICALS; HORSES; HUMANS; MALE; MITOCHONDRIA; OXIDATIVE STRESS; PENICILLAMINE; RATS; REACTIVE OXYGEN SPECIES; SEMEN PRESERVATION; SPERM MOTILITY; SPERMATOZOA; SULFHYDRYL COMPOUNDS;

EQUIDAE; RATTUS;

EID: 84869467151     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.112.102020     Document Type: Article

References (45)

1. Aitken RJ, Curry BJ. Redox regulation of human sperm function: from the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line. Antioxid Redox Signal 2011; 14: 367-381.
2. Jones R, Mann T, Sherins RJ. Peroxidative breakdown of phospholipids in human spermatozoa: spermicidal effects of fatty acid peroxides and protective action of seminal plasma. Fertil Steril 1979; 31:531-537.
3. Sawyer DE, Mercer BG, Wiklendt AM, Aitken RJ. Analysis of genespecific DNA damage and single-strand DNA breaks induced by prooxidant treatment of human spermatozoa in vitro. Mutat Res 2003; 529: 21-34.
4. Vernet P, Aitken RJ, Drevet JR. Antioxidant strategies in the epididymis. Mol Cell Endocrinol 2004; 216:31-39.
5. Rhemrev JP, van Overveld FW, Haenen GR, Teerlink T, Bast A, Vermeiden JP. Quantification of the nonenzymatic fast and slow TRAP in a post-addition assay in human seminal plasma and the antioxidant contributions of various seminal compounds. J Androl 2000; 21:913-920.
6. Koppers AJ, De Iuliis GN, Finnie JM, McLaughlin EA, Aitken RJ. Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J Clin Endocrinol Metab 2008; 93: 3199-3207.
7. Krausz C, Mills C, Rogers S, Tan SL, Aitken RJ. Stimulation of oxidant generation by human sperm suspensions using phorbol esters and formyl peptides: relationships with motility and fertilization in vitro. Fertil Steril 1994; 62:599-605.
8. Henkel R, Kierspel E, Hajimohammad M, Stalf T, Hoogendijk C, Mehnert C, Menkveld R, Schill WB, Kruger TF. DNA fragmentation of spermatozoa and assisted reproduction technology. Reprod Biomed Online 2003; 7:477-484.
9. Gomez E, Aitken RJ. Impact of in vitro fertilization culture media on peroxidative damage to human spermatozoa. Fertil Steril 1996; 65: 880-882.
10. Alvarez JG, Touchstone JC, Blasco L, Storey BT. Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa. J Androl 1987; 8:338-348.
11. MacLeod J. Sulfhydryl groups in relation to the metabolism and motility of human spermatozoa. J Gen Physiol 1951; 34:705-714.
12. Hughes LM, Griffith R, Carey A, Butler T, Donne SW, Beagley KW, Aitken RJ. The spermostatic and microbicidal actions of quinones and maleimides: toward a dual-purpose contraceptive agent. Mol Pharmacol 2009; 76:113-124.
13. Cabrillana ME, Monclus MA, Sáez Lancellotti TE, Boarelli PV, Clementi MA, Vincenti AE, Yunes RF, Fornés MW. Characterization of flagellar cysteine-rich sperm proteins involved in motility, by the combination of cellular fractionation, fluorescence detection, and mass spectrometry analysis. Cytoskeleton (Hoboken) 2011; 68:491-500.
14. Aitken RJ, Whiting S, De Iuliis GN, McClymont S, Mitchell LA, Baker MA. Electrophilic aldehydes generated by sperm metabolism activate mitochondrial reactive oxygen species generation and apoptosis by targeting succinate dehydrogenase. J Biol Chem 2012; 287:33048-33060.
15. Diezel W, Engel S, Sönnichsen N, Höhne WE. Lipid peroxidation products in human spermatozoa: detection and pathogenic significance. Andrologia 1980; 12:167-171.
16. Biggers JD, Whitten WK, Whittingham DG. The culture of mouse embryos in vitro. In: Daniels JC (ed.), Methods in Mammalian Embryology. San Francisco: Freeman; 1971:86-116.
17. Aitken RJ, Ryan AL, Curry BJ, Baker MA. Multiple forms of redox activity in populations of human spermatozoa. Mol Hum Reprod 2003; 9: 645-661.
18. Kenney RM, Bergman RV, Cooper WL, Morse GW. Minimal contamination techniques for breeding mares: techniques and preliminary findings. In: Proceedings of the 21st annual convention of the American Association of Equine Practitioners; 1975:327.
19. Stewart JJ. Optimization of parameters for semiempirical methods V: modification of NDDO approximations and application to 70 elements. J Mol Model 2007; 13:1173-1213.
20. Koppers AJ, Mitchell LA, Wang P, Lin M, Aitken RJ. Phosphoinositide 3-kinase signalling pathway involvement in a truncated apoptotic cascade associated with motility loss and oxidative DNA damage in human spermatozoa. Biochem J 2011; 436:687-698.
21. Aitken RJ, Wingate JK, De Iuliis GN, Koppers AJ, McLaughlin EA. Cisunsaturated fatty acids stimulate reactive oxygen species generation and lipid peroxidation in human spermatozoa. J Clin Endocrinol Metab 2006; 91:4154-4163.
22. Koppers AJ, Garg ML, Aitken RJ. Stimulation of mitochondrial reactive oxygen species production by unesterified, unsaturated fatty acids in defective human spermatozoa. Free Radic Biol Med 2010; 48:112-119.
23. Chen ZH, Niki E. 4-hydroxynonenal (4-HNE) has been widely accepted as an inducer of oxidative stress. Is this the whole truth about it or can 4-HNE also exert protective effects? IUBMB Life 2006; 58:372-373.
24. Uchida K. 4-Hydroxy-2-nonenal: a product and mediator of oxidative stress. Prog Lipid Res 2003; 42:318-343.
25. Doorn JA, Petersen DR. Covalent modification of amino acid nucleophiles by the lipid peroxidation products 4-hydroxy-2-nonenal and 4-oxo-2-nonenal. Chem Res Toxicol 2002; 15:1445-1450.
26. Pujianto DA, Curry BJ, Aitken RJ. Prolactin exerts a prosurvival effect on human spermatozoa via mechanisms that involve the stimulation of Akt phosphorylation and suppression of caspase activation and capacitation. Endocrinology 2010; 151:1269-1279.
27. O WS, Chen H, Chow PH. Male genital tract antioxidant enzymes-their ability to preserve sperm DNA integrity. Mol Cell Endocrinol 2006; 250: 80-83.
28. Musset B, Clark RA, DeCoursey TE, Petheo GL, Geiszt M, Chen Y, Cornell JE, Eddy CA, Brzyski RG, El Jamali A. NOX5 in human spermatozoa: expression, function, and regulation. J Biol Chem 2012; 287: 9376-9388.
29. Storey BT. Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol 2008; 52:427-437.
30. Gomez E, Irvine DS, Aitken RJ. Evaluation of a spectrophotometric assay for the measurement of malondialdehyde and 4-hydroxyalkenals in human spermatozoa: relationships with semen quality and sperm function. Int J Androl 1998; 21:81-94.
31. Griveau JF, Le Lannou D. Reactive oxygen species and human spermatozoa: physiology and pathology. Int J Androl 1997; 20:61-69.
32. Koterba AP, Smolen S, Joseph A, Basista MH, Brecher AS. Coagulation protein function. II. Influence of thiols upon acetaldehyde effects. Alcohol 1995; 12:49-57.
33. Blanusa M, Varnai VM, Piasek M, Kostial K. Chelators as antidotes of metal toxicity: therapeutic and experimental aspects. Curr Med Chem 2005; 12:2771-2794.
34. Storey BT. Biochemistry of the induction and prevention of lipoperoxidative damage in human spermatozoa. Mol Hum Reprod 1997; 3: 203-213.
35. Durmaz A, Dikmen N. Homocysteine effects on cellular glutathione peroxidase (GPx-1) activity under in vitro conditions. J Enzyme Inhib Med Chem 2007; 22:733-738.
36. Mehta R, Wong L, O'Brien PJ. Cytoprotective mechanisms of carbonyl scavenging drugs in isolated rat hepatocytes. Chem Biol Interact 2009; 178:317-323.
37. Althaus JS, Oien TT, Fici GJ, Scherch HM, Sethy VH, VonVoigtlander PF. Structure activity relationships of peroxynitrite scavengers an approach to nitric oxide neurotoxicity. Res Commun Chem Pathol Pharmacol 1994; 83:243-254.
38. Singh IN, Sullivan PG, Hall ED. Peroxynitrite-mediated oxidative damage to brain mitochondria: protective effects of peroxynitrite scavengers. J Neurosci Res 2007; 85:2216-2223.
39. Aitken RJ. The capacitation-apoptosis highway: oxysterols and mammalian sperm function. Biol Reprod 2011; 85:9-12.
40. Szabó C, Ohshima H. DNA damage induced by peroxynitrite: subsequent biological effects. Nitric Oxide 1997; 1:373-385.
41. Bravard A, Vacher M, Gouget B, Coutant A, de Boisferon FH, Marsin S, Chevillard S, Radicella JP. Redox regulation of human OGG1 activity in response to cellular oxidative stress. Mol Cell Biol 2006; 26:7430-7436.
42. Wakabayashi K, King SM. Modulation of Chlamydomonas reinhardtii flagellar motility by redox poise. J Cell Biol 2006; 173:743-754.
43. Pavlok A. D-penicillamine and granulosa cells can effectively extend the fertile life span of bovine frozen-thawed spermatozoa in vitro: effect on fertilization and polyspermy. Theriogenology 2000; 53:1135-1146.
44. Pavlok A, Kubelka M, Peknicová J. The effect of various capacitation active compounds and capacitation time on the in vitro fertility and protein tyrosine phosphorylation profiles of bovine sperm. Zygote 2001; 9:25-38.
45. Bavister BD. Substitution of a synthetic polymer for protein in a mammalian gamete culture system. J Exp Zool 1981; 217:45-51.