Mechanism, measurement, and prevention of oxidative stress in male reproductive physiology

Indian Journal of Experimental Biology

Volumn 43, Issue 11, 2005, Pages 963-974

  Agarwal, Ashok ^a   Prabakaran, Sushil A ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Male fertility; Oxidative stress; Spermatozoa

Indexed keywords

ANTIOXIDANT; CYTOCHROME C; DNA; DYES, REAGENTS, INDICATORS, MARKERS AND BUFFERS; NITROBLUE TETRAZOLIUM; REACTIVE OXYGEN METABOLITE; THIOBARBITURIC ACID REACTIVE SUBSTANCE; UNSATURATED FATTY ACID;

ANIMAL; CHEMICAL MODEL; CHEMISTRY; FERTILITY; HUMAN; LIPID PEROXIDATION; MALE; MALE INFERTILITY; METABOLISM; OXIDATIVE STRESS; PATHOLOGY; REVIEW; SMOKING; SPERM; SPERMATOZOON;

ANIMALS; ANTIOXIDANTS; CYTOCHROMES C; DNA; FATTY ACIDS, UNSATURATED; FERTILITY; HUMANS; INDICATORS AND REAGENTS; INFERTILITY, MALE; LIPID PEROXIDATION; MALE; MODELS, CHEMICAL; NITROBLUE TETRAZOLIUM; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SEMEN; SMOKING; SPERMATOZOA; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 27644571053     PISSN: 00195189     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (128)

1. Purvis K & Christiansen E, Male infertility: Current concepts, Ann Med, 24 (1992) 259.
2. Carlsen E, Giwercman A, Keiding N et al., Evidence for decreasing quality of semen during past 50 years, Bmj, 305 (1992) 609.
3. Giwercman A, Carlsen E, Keiding N et al., Evidence for increasing incidence of abnormalities of the human testis: a review, Environ Health Perspect, 101 Suppl 2 (1993) 65.
4. Sikka S C, Rajasekaran M & Hellstrom W J, Role of oxidative stress and antioxidants in male infertility, J Androl, 16 (1995) 464.
5. Sharma R K & Agarwal A, Role of reactive oxygen species in male infertility, Urology, 48 (1996) 835.
6. de Lamirande E & Gagnon C, Reactive oxygen species and human spermatozoa. II. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility, J Androl, 13 (1992) 379.
7. Critical reviews of oxidative stress and aging. Advances in basic science, diagnostics and interventions, edited by R G Cutler and H Rodriguez (World Scientific/National Academic Press/Imperial College Press, New Jersey) 2002, 1700. Critical reviews of oxidative stress and aging.
8. Sikka S C, Relative impact of oxidative stress on male reproductive function, Curr Med Chem, 8 (2001) 851.
9. Darley-Usmar V, Wiseman H & Halliwell B, Nitric oxide and oxygen radicals: A question of balance, FEBS Lett, 369 (1995) 131.
10. Garrido N, Meseguer M, Simon C et al., Pro-oxidative and anti-oxidative imbalance in human semen and its relation with male fertility, Asian J Androl, 6 (2004) 59.
11. Aitken R J & Baker H W, Seminal leukocytes: Passengers, terrorists or good Samaritans?, Hum Reprod, 10 (1995) 1736.
12. Shalika S, Dugan K, Smith R D et al., The effect of positive semen bacterial and Ureaplasma cultures on in vitro fertilization success, Hum Reprod, 11 (1996) 2789.
13. Aitken R J, Fisher H M, Fulton N 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, 47 (1997) 468.
14. Hendin B N, Kolettis P N, Sharma R K et al., Varicocele is associated with elevated spermatozoal reactive oxygen species production and diminished seminal plasma antioxidant capacity, J Urol, 161 (1999) 1831.
15. Ochsendorf F R, Infections in the male genital tract and reactive oxygen species, Hum Reprod Update, 5 (1999) 399.
16. Pasqualotto F F, Sharma R K, Potts J M et al., Seminal oxidative stress in patients with chronic prostatitis, Urology, 55 (2000) 881.
17. Sharma R K, Pasqualotto A E, Nelson D R et al., Relationship between seminal white blood cell counts and oxidative stress in men treated at an infertility clinic, J Androl, 22 (2001) 575.
18. Saleh R A, Agarwal A, Kandirali E et al., Leukocytospermia is associated with increased reactive oxygen species production by human spermatozoa, Fertil Steril, 78 (2002) 1215.
19. Alvarez J G, Sharma R K, Ollero M et al., Increased DNA damage in sperm from leukocytospermic semen samples as determined by the sperm chromatin structure assay, Fertil Steril, 78 (2002) 319.
20. Aziz N, Agarwal A, Lewis-Jones I et al., Novel associations between specific sperm morphological defects and leukocytospermia, Fertil Steril, 82 (2004) 621.
21. Shekarriz M, Sharma R K, Thomas A J, Jr. et al., Positive myeloperoxidase staining (Endtz test) as an indicator of excessive reactive oxygen species formation in semen, J Assist Reprod Genet, 12 (1995) 70.
22. Potts J M, Sharma R, Pasqualotto F et al., Association of ureaplasma urealyticum with abnormal reactive oxygen species levels and absence of leukocytospermia, J Urol, 163 (2000) 1775.
23. Potts J M & Pasqualotto F F, Seminal oxidative stress in patients with chronic prostatitis, Andrologia, 35 (2003) 304.
24. Nallella K P, Allamaneni S S, Pasqualotto F F et al., Relationship of interleukin-6 with semen characteristics and oxidative stress in patients with varicocele, Urology, 64 (2004) 1010.
25. Gil-Guzman E, Ollero M, Lopez M C et al., Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation, Hum Reprod, 16 (2001) 1922.
26. Gomez E, Buckingham D W, Brindle J et al., Development of an image analysis system to monitor the retention of residual cytoplasm by human spermatozoa: Correlation with biochemical markers of the cytoplasmic space, oxidative stress, and sperm function, J Androl, 17 (1996) 276.
27. Gavella M & Lipovac V, NADH-dependent oxidoreductase (diaphorase) activity and isozyme pattern of sperm in infertile men, Arch Androl, 28 (1992) 135.
28. Pasqualotto F F, Sharma R K, Nelson D R et al., Relationship between oxidative stress, semen characteristics, and clinical diagnosis in men undergoing infertility investigation, Fertil Steril, 73 (2000) 459.
29. Lambert H, Overstreet J W, Morales P et al., Sperm capacitation in the human female reproductive tract, Fertil Steril, 43 (1985) 325.
30. de Lamirande E, Leclerc P & Gagnon C, Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization, Mol Hum Reprod, 3 (1997) 175.
31. de Lamirande E, Tsai C, Harakat A et al., Involvement of reactive oxygen species in human sperm arcosome reaction induced by A23187, lysophosphatidylcholine, and biological fluid ultrafiltrates, J Androl, 19 (1998) 585.
32. Zini A, De Lamirande E & Gagnon C, Low levels of nitric oxide promote human sperm capacitation in vitro, J Androl, 16 (1995) 424.
33. Sengoku K, Tamate K, Yoshida T et al., Effects of low concentrations of nitric oxide on the zona pellucida binding ability of human spermatozoa, Fertil Steril, 69 (1998) 522.
34. Yeoman R R, Jones W D & Rizk B M, Evidence for nitric oxide regulation of hamster sperm hyperactivation, J Androl, 19 (1998) 58.
35. Balercia G, Moretti S, Vignini A et al., Role of nitric oxide concentrations on human sperm motility, J Androl, 25 (2004) 245.
36. Donnelly E T, Lewis S E, Thompson W et al., Sperm nitric oxide and motility: The effects of nitric oxide synthase stimulation and inhibition, Mol Hum Reprod, 3 (1997) 755.
37. Garner B, van Reyk D, Dean R T et al., Direct copper reduction by macrophages. Its role in low density lipoprotein oxidation, J Biol Chem, 272 (1997) 6927.
38. +3, Neurodegeneration, 4 (1995) 329.
39. Benoff S, Hurley I R, Millan C et al., Seminal lead concentrations negatively affect outcomes of artificial insemination, Fertil Steril, 80 (2003) 517.
40. Shekarriz M, DeWire D M, Thomas A J, Jr. et al., A method of human semen centrifugation to minimize the iatrogenic sperm injuries caused by reactive oxygen species, Eur Urol, 28 (1995) 31.
41. Halliwell B, Gutteridge J M & Blake D, Metal ions and oxygen radical reactions in human inflammatory joint disease, Philos Trans R Soc Lond B Biol Sci, 311 (1985) 659.
42. Davies K J, Delsignore M E & Lin S W, Protein damage and degradation by oxygen radicals. II. Modification of amino acids, J Biol Chem, 262 (1987) 9902.
43. Stadtman E R & Levine R L, Free radical-mediated oxidation of free amino acids and amino acid residues in proteins, Amino Acids, 25 (2003) 207.
44. Tominaga H, Kodama S, Matsuda N et al., Involvement of reactive oxygen species (ROS) in the induction of genetic instability by radiation, J Radiat Res (Tokyo), 45 (2004) 181.
45. Agarwal A & Saleh R A, Role of oxidants in male infertility: Rationale, significance, and treatment, Urol Clin North Am, 29 (2002) 817.
46. Aitken R J & Krausz C, Oxidative stress, DNA damage and the Y chromosome, Reproduction, 122 (2001) 497.
47. Lopes S, Jurisicova A, Sun J G et al., Reactive oxygen species: Potential cause for DNA fragmentation in human spermatozoa, Hum Reprod, 13 (1998) 896.
48. Imlay J A & Linn S, Bimodal pattern of killing of DNA-repair-defective or anoxically grown Escherichia coli by hydrogen peroxide, J Bacteriol, 166 (1986) 519.
49. Moustafa M H, Sharma R K, Thornton J et al., Relationship between ROS production, apoptosis and DNA denaturation in spermatozoa from patients examined for infertility, Hum Reprod, 19 (2004) 129.
50. Agarwal A & Allamaneni S S, The effect of sperm DNA damage on assisted reproduction outcomes. A review, Minerva Ginecol, 56 (2004) 235.
51. Agarwal A & Said T M, Role of sperm chromatin abnormalities and DNA damage in male infertility, Hum Reprod Update, 9 (2003) 331.
52. Saleh R A, Agarwal A, Nada E A et al., Negative effects of increased sperm DNA damage in relation to seminal oxidative stress in men with idiopathic and male factor infertility, Fertil Steril, 79 Suppl 3 (2003) 1597.
53. Twigg J, Fulton N, Gomez E et al., 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, 13 (1998) 1429.
54. Paasch U, Agarwal A, Gupta A K et al., Apoptosis signal transduction and the maturity status of human spermatozoa, Ann N Y Acad Sci, 1010 (2003) 486.
55. Hampton M B, Fadeel B & Orrenius S, Redox regulation of the caspases during apoptosis, Ann N Y Acad Sci, 854 (1998) 328.
56. Agarwal A, Saleh R A & Bedaiwy M A, Role of reactive oxygen species in the pathophysiology of human reproduction, Fertil Steril, 79 (2003) 829.
57. Wang X, Sharma R K, Sikka S C et al., Oxidative stress is associated with increased apoptosis leading to spermatozoa DNA damage in patients with male factor infertility, Fertil Steril, 80 (2003) 531.
58. Halliwell B, Antioxidant defence mechanisms: From the beginning to the end (of the beginning), Free Radic Res, 31 (1999) 261.
59. Padron O F, Brackett N L, Sharma R K et al., Seminal reactive oxygen species and sperm motility and morphology in men with spinal cord injury, Fertil Steril, 67 (1997) 1115.
60. Shekarriz M, Thomas A J, Jr. & Agarwal A, Incidence and level of seminal reactive oxygen species in normal men, Urology, 45 (1995) 103.
61. Esfandiari N, Saleh R A, Blaut A P et al., Effects of temperature on sperm motion characteristics and reactive oxygen species, Int J Fertil Womens Med, 47 (2002) 227.
62. Aziz N, Saleh R A, Sharma R K et al., Novel association between sperm reactive oxygen species production, sperm morphological defects, and the sperm deformity index, Fertil Steril, 81 (2004) 349.
63. Traber M G, van der Vliet A, Reznick A Z et al., Tobacco-related diseases. Is there a role for antioxidant micronutrient supplementation?, Clin Chest Med, 21 (2000) 173.
64. Cross C E, Halliwell B, Borish E T et al., Oxygen radicals and human disease, Ann Intern Med, 107 (1987) 526.
65. Vine M F, Tse C K, Hu P et al., Cigarette smoking and semen quality, Fertil Steril, 65 (1996) 835.
66. Kunzle R, Mueller M D, Hanggi W et al., Semen quality of male smokers and non-smokers in infertile couples, Fertil Steril, 79 (2003) 287.
67. Saleh R A, Agarwal A, Sharma R K et al., Effect of cigarette smoking on levels of seminal oxidative stress in infertile men: a prospective study, Fertil Steril, 78 (2002) 491.
68. Pacifici R, Altieri I, Gandini L et al., Nicotine, cotinine, and trans-3-hydroxycotinine levels in seminal plasma of smokers: Efects on sperm parameters, Ther Drug Monit, 15 (1993) 358.
69. Goverde H J, Dekker H S, Janssen H J et al., Semen quality and frequency of smoking and alcohol consumption - an explorative study, Int J Fertil Menopausal Stud, 40 (1995) 135.
70. Marinelli D, Gaspari L, Pedotti P et al., Mini-review of studies on the effect of smoking and drinking habits on semen parameters, Int J Hyg Environ Health, 207 (2004) 185.
71. Abell A, Ernst E & Bonde J P, High sperm density among members of organic farmers' association, Lancet, 343 (1994) 1498.
72. Agarwal A, Ikemoto I & Loughlin K R, Relationship of sperm parameters with levels of reactive oxygen species in semen specimens, J Urol, 152 (1994) 107.
73. Shekarriz M, Thomas A J, Jr. & Agarwal A, Effects of time and sperm concentration on reactive oxygen species formation in human semen, Arch Androl, 34 (1995) 69.
74. McKinney K A, Lewis S E & Thompson W, Reactive oxygen species generation in human sperm: Luminol and lucigenin chemiluminescence probes, Arch Androl, 36 (1996) 119.
75. Aitken R J, Buckingham D W & West K M, Reactive oxygen species and human spermatozoa: Analysis of the cellular mechanisms involved in luminol- and lucigenin-dependent chemiluminescence, J Cell Physiol, 151 (1992) 466.
76. Said T M, Paasch U, Glander H J et al., Role of caspases in male infertility, Hum Reprod Update, 10 (2004) 39.
77. Ford W C, Regulation of sperm function by reactive oxygen species. Hum Reprod Update, 10 (2004) 387.
78. Esfandiari N, Sharma R K, Saleh R A et al., Utility of the nitroblue tetrazolium reduction test for assessment of reactive oxygen species production by seminal leukocytes and spermatozoa, J Androl, 24 (2003) 862.
79. Kirby T W & Fridovich I, A picomolar spectrophotometric assay for superoxide dismutase, Anal Biochem, 127 (1982) 435.
80. Elferink J G, Measurement of the metabolic burst in human neutrophils: A comparison between cytochrome c and NBT reduction, Res Commun Chem Pathol Pharmacol, 43 (1984) 339.
81. Weber G F, The measurement of oxygen-derived free radicals and related substances in medicine, J Clin Chem Clin Biochem, 28 (1990) 569.
82. Buettner G R, Spin trapping: ESR parameters of spin adducts, Free Radic Biol Med, 3 (1987) 259.
83. Kaur H, Edmonds S E, Blake D R et al., Hydroxyl radical generation by rheumatoid blood and knee joint synovial fluid, Ann Rheum Dis, 55 (1996) 915.
84. Kaur H & Halliwell B, Aromatic hydroxylation of phenylalanine as an assay for hydroxyl radicals. Measurement of hydroxyl radical formation from ozone and in blood from premature babies using improved HPLC methodology, Anal Biochem, 220 (1994) 11.
85. Halliwell B & Kaur H, Hydroxylation of salicylate and phenylalanine as assays for hydroxyl radicals: A cautionary note visited for the third time, Free Radic Res, 27 (1997) 239.
86. Coudray C & Favier A, Determination of salicylate hydroxylation products as an in vivo oxidative stress marker, Free Radic Biol Med, 29 (2000) 1064.
87. Themann C, Teismann P, Kuschinsky K et al., Comparison of two independent aromatic hydroxylation assays in combination with intracerebral microdialysis to determine hydroxyl free radicals, J Neurosci Methods, 108 (2001) 57.
88. Li M, Carlson S, Kinzer J A et al., HPLC and LC-MS studies of hydroxylation of phenylalanine as an assay for hydroxyl radicals generated from Udenfriend's reagent, Biochem Biophys Res Commun, 312 (2003) 316.
89. Tubaro M, Cavallo G, Pensa V et al., Demonstration of the formation of hydroxyl radicals in acute myocardial infarction in man using salicylate as probe, Cardiology, 80 (1992) 246.
90. Iuliano L, Pratico D, Ghiselli A et al., Reaction of dipyridamole with the hydroxyl radical, Lipids, 27 (1992) 349.
91. Bass D A, Parce J W, Dechatelet L R et al., Flow cytometric studies of oxidative product formation by neutrophils: A graded response to membrane stimulation, J Immunol, 130 (1983) 1910.
92. Chirico S, Smith C, Marchant C et al., Lipid peroxidation in hyperlipidaemic patients. A study of plasma using an HPLC-based thiobarbituric acid test, Free Radic Res Commun, 19 (1993) 51.
93. Roberts L J & Morrow J D, Measurement of F(2)-isoprostanes as an index of oxidative stress in vivo, Free Radic Biol Med, 28 (2000) 505.
94. Fam S S & Morrow J D, The isoprostanes: Unique products of arachidonic acid oxidation - a review, Curr Med Chem, 10 (2003) 1723.
95. Tarpey M M, Wink D A & Grisham M B, Methods for detection of reactive metabolites of oxygen and nitrogen: In vitro and in vivo considerations, Am J Physiol Regul Integr Comp Physiol, 286 (2004) R431.
96. Said T M, Kattal N, Sharma R K et al., Enhanced chemiluminescence assay vs colorimetric assay for measurement of the total antioxidant capacity of human seminal plasma, J Androl, 24 (2003) 676.
97. Agarwal A, Allamaneni S S & Said T M, Chemiluminescence technique for measuring reactive oxygen species, Reprod Biomed Online, 9 (2004) 466.
98. Sharma R K, Pasqualotto F F, Nelson D R et al., The reactive oxygen species-total antioxidant capacity score is a new measure of oxidative stress to predict male infertility, Hum Reprod, 14 (1999) 2801.
99. Kolettis P N, Sharma R K, Pasqualotto F F et al., Effect of seminal oxidative stress on fertility after vasectomy reversal, Fertil Steril, 71 (1999) 249.
100. Jeulin C, Soufir J C, Weber P et al., Catalase activity in human spermatozoa and seminal plasma, Gamete Res, 24 (1989) 185.
101. Fraga C G, Motchnik P A, Shigenaga M K et al., Ascorbic acid protects against endogenous oxidative DNA damage in human sperm, Proc Natl Acad Sci USA, 88 (1991) 11003.
102. Thiele J J, Friesleben H J, Fuchs J et al., Ascorbic acid and urate in human seminal plasma: Determination and interrelationships with chemiluminescence in washed semen, Hum Reprod, 10 (1995) 110.
103. Aitken R J & Clarkson J S, Significance of reactive oxygen species and antioxidants in defining the efficacy of sperm preparation techniques, J Androl, 9 (1988) 367.
104. Lenzi A, Picardo M, Gandini L et al., Glutathione treatment of dyspermia: Effect on the lipoperoxidation process, Hum Reprod, 9 (1994) 2044.
105. Tauber P F, Zaneveld L J, Propping D et al., Components of human split ejaculates. I. Spermatozoa, fructose, immunoglobulins, albumin, lactoferrin, transferrin and other plasma proteins, J Reprod Fertil, 43 (1975) 249.
106. Alvarez J G & Storey B T, Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility, Biol Reprod, 29 (1983) 548.
107. de Lamirande E & Gagnon C, Capacitation-associated production of superoxide anion by human spermatozoa, Free Radic Biol Med, 18 (1995) 487.
108. Peeker R, Abramsson L & Marklund S L, Superoxide dismutase isoenzymes in human seminal plasma and spermatozoa, Mol Hum Reprod, 3 (1997) 1061.
109. Baker H W, Brindle J, Irvine D S et al., Protective effect of antioxidants on the impairment of sperm motility by activated polymorphonuclear leukocytes, Fertil Steril, 65 (1996) 411.
110. Zini A, Fischer M A, Mak V et al., Catalase-like and superoxide dismutase-like activities in human seminal plasma, Urol Res, 30 (2002) 321.
111. Sikka S C, Role of oxidative stress and antioxidants in andrology and assisted reproductive technology, J Androl, 25 (2004) 5.
112. Wang X, Falcone T, Attaran M et al., Vitamin C and vitamin E supplementation reduce oxidative stress-induced embryo toxicity and improve the blastocyst development rate, Fertil Steril, 78 (2002) 1272.
113. Burton G W, Joyce A & Ingold K U, First proof that vitamin E is major lipid-soluble, chain-breaking antioxidant in human blood plasma, Lancet, 2 (1982) 327.
114. Agarwal A, Nallella K P, Allamaneni S S et al., Role of antioxidants in treatment of male infertility: An overview of the literature, Reprod Biomed Online, 8 (2004) 616.
115. Lutsenko E A, Carcamo J M & Golde D W, Vitamin C prevents DNA mutation induced by oxidative stress, J Biol Chem, 277 (2002) 16895.
116. Irvine D S, Glutathione as a treatment for male infertility, Rev Reprod, 1 (1996) 6.
117. Yoda Y, Nakazawa M, Abe T et al., Prevention of doxorubicin myocardial toxicity in mice by reduced glutathione, Cancer Res, 46 (1986) 2551.
118. Hansen J C & Deguchi Y, Selenium and fertility in animals and man - A review, Acta Vet Scand, 37 (1996) 19.
119. Ursini F, Heim S, Kiess M et al., Dual function of the selenoprotein PHGPx during sperm maturation, Science, 285 (1999) 1393.
120. Lenzi A, Gandini L, Picardo M et al., Lipoperoxidation damage of spermatozoa polyunsaturated fatty acids (PUFA): Scavenger mechanisms and possible scavenger therapies, Front Biosci, 5 (2000) E1.
121. Lenzi A, Gandini L, Lombardo F et al., Polyunsaturated fatty acids of germ cell membranes, glutathione and blutathione-dependent enzyme-PHGPx: from basic to clinic, Contraception, 65 (2002) 301.
122. Lenzi A, Lombardo F, Gandini L et al., Glutathione therapy for male infertility, Arch Androl, 29 (1992) 65.
123. Oeda T, Henkel R, Ohmori H et al., Scavenging effect of N-acetyl-L-cysteine against reactive oxygen species in human semen: A possible therapeutic modality for male factor infertility?, Andrologia, 29 (1997) 125.
124. Sies H & Stahl W, Vitamins E and C, beta-carotene, and other carotenoids as antioxidants, Am J Clin Nutr, 62 (1995) 1315S.
125. Frei B, Kim M C & Ames B N, Ubiquinol-10 is an effective lipid-soluble antioxidant at physiological concentrations, Proc Natl Acad Sci USA, 87 (1990) 4879.
126. Mellors A & Tappel A L, The inhibition of mitochondrial peroxidation by ubiquinone and ubiquinol, J Biol Chem, 241 (1966) 4353.
127. Lewin A & Lavon H, The effect of coenzyme Q10 on sperm motility and function, Mol Aspects Med, 18 Suppl (1997) S213.
128. Agarwal A & Said T M, Carnitines and male infertility, Reprod Biomed Online, 8 (2004) 376.