Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017, Article ID 4371714, 14 pages
https://doi.org/10.1155/2017/4371714
Review Article

The Role of Antioxidant Enzymes in the Ovaries

1Department of Obstetrics and Gynecology, West China Second University Hospital, Sichuan University, Chengdu 610041, China
2Joint Laboratory of Reproductive Medicine, Sichuan University-The Chinese University of Hong Kong (SCU-CUHK), West China Second University Hospital, Sichuan University, Chengdu 610041, China

Correspondence should be addressed to Wenming Xu; moc.361@3791gnimnewux and Xinghui Liu; moc.361@uiliuhgnix

Received 30 May 2017; Accepted 19 July 2017; Published 24 September 2017

Academic Editor: Rodrigo Franco

Copyright © 2017 Shan Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. G. Allen and M. Tresini, “Oxidative stress and gene regulation,” Free Radical Biology & Medicine, vol. 28, pp. 463–499, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. A. U. Khan and T. Wilson, “Reactive oxygen species as cellular messengers,” Chemistry & Biology, vol. 2, pp. 437–445, 1995. View at Publisher · View at Google Scholar · View at Scopus
  3. T. Finkel, “Oxygen radicals and signaling,” Current Opinion in Cell Biology, vol. 10, pp. 248–253, 1998. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Valko, D. Leibfritz, J. Moncol, M. T. Cronin, M. Mazur, and J. Telser, “Free radicals and antioxidants in normal physiological functions and human disease,” The International Journal of Biochemistry & Cell Biology, vol. 39, pp. 44–84, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. B. Halliwell, “Tell me about free radicals, doctor: a review,” Journal of the Royal Society of Medicine, vol. 82, pp. 747–752, 1989. View at Google Scholar
  6. H. Kato, N. Sugino, S. Takiguchi, S. Kashida, and Y. Nakamura, “Roles of reactive oxygen species in the regulation of luteal function,” Reviews of Reproduction, vol. 2, pp. 81–83, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. N. Sugino, “Reactive oxygen species in ovarian physiology,” Reproductive Medicine and Biology, vol. 4, pp. 31–44, 2005. View at Publisher · View at Google Scholar
  8. A. Agarwal, S. Gupta, L. Sekhon, and R. Shah, “Redox considerations in female reproductive function and assisted reproduction: from molecular mechanisms to health implications,” Antioxidants & Redox Signaling, vol. 10, pp. 1375–1403, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. K. H. Al-Gubory, P. A. Fowler, and C. Garrel, “The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes,” The International Journal of Biochemistry & Cell Biology, vol. 42, pp. 1634–1650, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Agarwal, S. Gupta, and S. Sikka, “The role of free radicals and antioxidants in reproduction,” Current Opinion in Obstetrics & Gynecology, vol. 18, pp. 325–332, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. J. Avila, R. Gonzalez-Fernandez, D. Rotoli, J. Hernandez, and A. Palumbo, “Oxidative stress in granulosa-lutein cells from in vitro fertilization patients,” Reproductive Sciences, vol. 23, pp. 1656–1661, 2016. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Agarwal and S. S. Allamaneni, “Role of free radicals in female reproductive diseases and assisted reproduction,” Reproductive Biomedicine Online, vol. 9, pp. 338–347, 2004. View at Publisher · View at Google Scholar
  13. A. Agarwal, A. Aponte-Mellado, B. J. Premkumar, A. Shaman, and S. Gupta, “The effects of oxidative stress on female reproduction: a review,” Reproductive Biology and Endocrinology, vol. 10, p. 49, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. B. Halliwell, “Protection against tissue damage in vivo by desferrioxamine: what is its mechanism of action?” Free Radical Biology & Medicine, vol. 7, pp. 645–651, 1989. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Moncada, R. M. Palmer, and E. A. Higgs, “Nitric oxide: physiology, pathophysiology, and pharmacology,” Pharmacological Reviews, vol. 43, pp. 109–142, 1991. View at Google Scholar
  16. J. M. McCord, B. B. Keele Jr., and I. Fridovich, “An enzyme-based theory of obligate anaerobiosis: the physiological function of superoxide dismutase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 68, pp. 1024–1027, 1971. View at Publisher · View at Google Scholar
  17. B. Halliwell, “Superoxide-dependent formation of hydroxyl radicals in the presence of iron salts. Its role in degradation of hyaluronic acid by a superoxide-generating system,” FEBS Letters, vol. 96, pp. 238–242, 1978. View at Publisher · View at Google Scholar · View at Scopus
  18. J. P. Kehrer, “The Haber-Weiss reaction and mechanisms of toxicity,” Toxicology, vol. 149, pp. 43–50, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. S. J. Yoon, K. H. Choi, and K. A. Lee, “Nitric oxide-mediated inhibition of follicular apoptosis is associated with HSP70 induction and Bax suppression,” Molecular Reproduction and Development, vol. 61, pp. 504–510, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. B. C. Jee, S. H. Kim, and S. Y. Moon, “The role of nitric oxide on apoptosis in human luteinized granulosa cells. Immunocytochemical evidence,” Gynecologic and Obstetric Investigation, vol. 56, pp. 143–147, 2003. View at Publisher · View at Google Scholar · View at Scopus
  21. S. Preutthipan, S. H. Chen, J. L. Tilly, K. Kugu, R. R. Lareu, and A. M. Dharmarajan, “Inhibition of nitric oxide synthesis potentiates apoptosis in the rabbit corpus luteum,” Reproductive Biomedicine Online, vol. 9, pp. 264–270, 2004. View at Publisher · View at Google Scholar
  22. P. Ghafourifar and C. Richter, “Nitric oxide synthase activity in mitochondria,” FEBS Letters, vol. 418, pp. 291–296, 1997. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Giulivi, “Functional implications of nitric oxide produced by mitochondria in mitochondrial metabolism,” The Biochemical Journal, vol. 332, Part 3, pp. 673–679, 1998. View at Publisher · View at Google Scholar
  24. W. H. Koppenol, J. J. Moreno, W. A. Pryor, H. Ischiropoulos, and J. S. Beckman, “Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxide,” Chemical Research in Toxicology, vol. 5, pp. 834–842, 1992. View at Publisher · View at Google Scholar
  25. C. Michiels, M. Raes, O. Toussaint, and J. Remacle, “Importance of Se-glutathione peroxidase, catalase, and Cu/Zn-SOD for cell survival against oxidative stress,” Free Radical Biology & Medicine, vol. 17, pp. 235–248, 1994. View at Publisher · View at Google Scholar · View at Scopus
  26. I. Fridovich, “Superoxide radical and superoxide dismutases,” Annual Review of Biochemistry, vol. 64, pp. 97–112, 1995. View at Publisher · View at Google Scholar
  27. H. R. Behrman, P. H. Kodaman, S. L. Preston, and S. Gao, “Oxidative stress and the ovary,” Journal of the Society for Gynecologic Investigation, vol. 8, pp. S40–S42, 2001. View at Google Scholar
  28. R. Sharma and A. Agarwal, “Role of reactive oxygen species in gynecologic diseases,” Reproductive Medicine and Biology, vol. 3, pp. 177–199, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. R. A. Weisiger and I. Fridovich, “Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization,” The Journal of Biological Chemistry, vol. 248, pp. 4793–4796, 1973. View at Google Scholar
  30. S. L. Marklund, “Human copper-containing superoxide dismutase of high molecular weight,” Proceedings of the National Academy of Sciences of the United States of America, vol. 79, pp. 7634–7638, 1982. View at Publisher · View at Google Scholar
  31. S. L. Marklund, E. Holme, and L. Hellner, “Superoxide dismutase in extracellular fluids,” Clinica Chimica Acta, vol. 126, pp. 41–51, 1982. View at Publisher · View at Google Scholar · View at Scopus
  32. G. C. Mills, “Hemoglobin catabolism. I. Glutathione peroxidase, an erythrocyte enzyme which protects hemoglobin from oxidative breakdown,” The Journal of Biological Chemistry, vol. 229, pp. 189–197, 1957. View at Google Scholar
  33. B. Chance, H. Sies, and A. Boveris, “Hydroperoxide metabolism in mammalian organs,” Physiological Reviews, vol. 59, pp. 527–605, 1979. View at Google Scholar
  34. J. D. Hayes and L. I. McLellan, “Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress,” Free Radical Research, vol. 31, pp. 273–300, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Kaplowitz, “Physiological significance of glutathione S-transferases,” The American Journal of Physiology, vol. 239, pp. G439–G444, 1980. View at Google Scholar
  36. H. Sies and W. Stahl, “Vitamins E and C, beta-carotene, and other carotenoids as antioxidants,” The American Journal of Clinical Nutrition, vol. 62, pp. 1315S–1321S, 1995. View at Google Scholar
  37. C. L. Rock, R. A. Jacob, and P. E. Bowen, “Update on the biological characteristics of the antioxidant micronutrients: vitamin C, vitamin E, and the carotenoids,” Journal of the American Dietetic Association, vol. 96, pp. 693–702, 1996. View at Publisher · View at Google Scholar
  38. W. J. Bettger, “Zinc and selenium, site-specific versus general antioxidation,” Canadian Journal of Physiology and Pharmacology, vol. 71, pp. 721–724, 1993. View at Publisher · View at Google Scholar
  39. S. I. Dashti, M. Thomson, and M. S. Mameesh, “Effects of copper deficiency and Cu complexes on superoxide dismutase in rats,” Nutrition, vol. 11, pp. 564–567, 1995. View at Google Scholar
  40. A. Scalbert, I. T. Johnson, and M. Saltmarsh, “Polyphenols: antioxidants and beyond,” The American Journal of Clinical Nutrition, vol. 81, pp. 215S–217S, 2005. View at Google Scholar
  41. K. Shkolnik, A. Tadmor, S. Ben-Dor, N. Nevo, D. Galiani, and N. Dekel, “Reactive oxygen species are indispensable in ovulation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, pp. 1462–1467, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Suzuki, N. Sugino, T. Fukaya et al., “Superoxide dismutase in normal cycling human ovaries: immunohistochemical localization and characterization,” Fertility and Sterility, vol. 72, pp. 720–726, 1999. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Tamate, K. Sengoku, and M. Ishikawa, “The role of superoxide dismutase in the human ovary and fallopian tube,” Journal of Obstetrics and Gynaecology (Tokyo, Japan), vol. 21, pp. 401–409, 1995. View at Publisher · View at Google Scholar
  44. J. Fujii, Y. Iuchi, and F. Okada, “Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system,” Reproductive Biology and Endocrinology, vol. 3, p. 43, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Geva and R. B. Jaffe, “Role of angiopoietins in reproductive tract angiogenesis,” Obstetrical & Gynecological Survey, vol. 55, pp. 511–519, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. J. D. Gordon, S. Mesiano, C. J. Zaloudek, and R. B. Jaffe, “Vascular endothelial growth factor localization in human ovary and fallopian tubes: possible role in reproductive function and ovarian cyst formation,” The Journal of Clinical Endocrinology and Metabolism, vol. 81, pp. 353–359, 1996. View at Publisher · View at Google Scholar
  47. E. D. Albrecht, J. S. Babischkin, Y. Lidor, L. D. Anderson, L. C. Udoff, and G. J. Pepe, “Effect of estrogen on angiogenesis in co-cultures of human endometrial cells and microvascular endothelial cells,” Human Reproduction, vol. 18, pp. 2039–2047, 2003. View at Publisher · View at Google Scholar · View at Scopus
  48. M. Ushio-Fukai and R. W. Alexander, “Reactive oxygen species as mediators of angiogenesis signaling: role of NAD(P)H oxidase,” Molecular and Cellular Biochemistry, vol. 264, pp. 85–97, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. J. S. Richards, “Hormonal control of gene expression in the ovary,” Endocrine Reviews, vol. 15, pp. 725–751, 1994. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Gougeon, “Human ovarian follicular development: from activation of resting follicles to preovulatory maturation,” Annales d'endocrinologie, vol. 71, pp. 132–143, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Miyazaki, K. Sueoka, A. M. Dharmarajan, S. J. Atlas, G. B. Bulkley, and E. E. Wallach, “Effect of inhibition of oxygen free radical on ovulation and progesterone production by the in-vitro perfused rabbit ovary,” Journal of Reproduction and Fertility, vol. 91, pp. 207–212, 1991. View at Publisher · View at Google Scholar
  52. B. Du, K. Takahashi, G. M. Ishida, K. Nakahara, H. Saito, and H. Kurachi, “Usefulness of intraovarian artery pulsatility and resistance indices measurement on the day of follicle aspiration for the assessment of oocyte quality,” Fertility and Sterility, vol. 85, pp. 366–370, 2006. View at Publisher · View at Google Scholar · View at Scopus
  53. L. L. Espey, “Current status of the hypothesis that mammalian ovulation is comparable to an inflammatory reaction,” Biology of Reproduction, vol. 50, pp. 233–238, 1994. View at Publisher · View at Google Scholar
  54. R. L. Stouffer, F. Xu, and D. M. Duffy, “Molecular control of ovulation and luteinization in the primate follicle,” Frontiers in Bioscience, vol. 12, pp. 297–307, 2007. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Rizzo, M. T. Roscino, F. Binetti, and R. L. Sciorsci, “Roles of reactive oxygen species in female reproduction,” Reproduction in Domestic Animals, vol. 47, pp. 344–352, 2012. View at Publisher · View at Google Scholar · View at Scopus
  56. N. Sugino, “Roles of reactive oxygen species in the corpus luteum,” Animal Science Journal, vol. 77, pp. 556–565, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. J. C. Carlson, M. Sawada, D. L. Boone, and J. M. Stauffer, “Stimulation of progesterone secretion in dispersed cells of rat corpora lutea by antioxidants,” Steroids, vol. 60, pp. 272–276, 1995. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Sawada and J. C. Carlson, “Intracellular regulation of progesterone secretion by the superoxide radical in the rat corpus luteum,” Endocrinology, vol. 137, pp. 1580–1584, 1996. View at Publisher · View at Google Scholar
  59. B. J. Gulys and L. C. Yuan, “Microperoxisomes in the late pregnancy corpus luteum of rhesus monkeys (Macaca mulatta),” The Journal of Histochemistry and Cytochemistry, vol. 23, pp. 359–368, 1975. View at Publisher · View at Google Scholar
  60. Y. S. Park, S. Y. You, S. Cho et al., “Eccentric localization of catalase to protect chromosomes from oxidative damages during meiotic maturation in mouse oocytes,” Histochemistry and Cell Biology, vol. 146, pp. 281–288, 2016. View at Publisher · View at Google Scholar · View at Scopus
  61. M. B. Harvey, M. Y. Arcellana-Panlilio, X. Zhang, G. A. Schultz, and A. J. Watson, “Expression of genes encoding antioxidant enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo coculture,” Biology of Reproduction, vol. 53, pp. 532–540, 1995. View at Publisher · View at Google Scholar · View at Scopus
  62. S. L. Peterson and P. M. Stevenson, “Changes in catalase activity and concentration during ovarian development and differentiation,” Biochimica et Biophysica Acta, vol. 1135, pp. 207–214, 1992. View at Publisher · View at Google Scholar · View at Scopus
  63. R. Behl and R. S. Pandey, “FSH induced stimulation of catalase activity in goat granulosa cells in vitro,” Animal Reproduction Science, vol. 70, pp. 215–221, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. R. K. Parshad and S. S. Guraya, “Changes in catalase activity during follicular growth, atresia and luteinization in rat ovary,” Indian Journal of Experimental Biology, vol. 31, pp. 109–111, 1993. View at Google Scholar
  65. J. D. Neill and M. S. Smith, “Pituitary-ovarian interrelationships in the rat,” Current Topics in Experimental Endocrinology, vol. 2, pp. 73–106, 1974. View at Publisher · View at Google Scholar
  66. A. C. Enders and D. M. Nelson, “Pinocytotic activity of the uterus of the rat,” The American Journal of Anatomy, vol. 138, pp. 277–299, 1973. View at Publisher · View at Google Scholar · View at Scopus
  67. D. Singh and R. S. Pandey, “Changes in catalase activity and hydrogen peroxide level in rat ovary during estrous cycle and induction of catalase in rat ovary by estradiol-17 beta,” Indian Journal of Experimental Biology, vol. 36, pp. 421–423, 1998. View at Google Scholar
  68. K. H. El-Shahat and M. Kandil, “Antioxidant capacity of follicular fluid in relation to follicular size and stage of estrous cycle in buffaloes,” Theriogenology, vol. 77, pp. 1513–1518, 2012. View at Publisher · View at Google Scholar · View at Scopus
  69. G. Basini, B. Simona, S. E. Santini, and F. Grasselli, “Reactive oxygen species and anti-oxidant defences in swine follicular fluids,” Reproduction, Fertility, and Development, vol. 20, pp. 269–274, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. J. E. Fortune, “Ovarian follicular growth and development in mammals,” Biology of Reproduction, vol. 50, pp. 225–232, 1994. View at Publisher · View at Google Scholar
  71. S. P. Klinken and P. M. Stevenson, “Changes in enzyme activities during the artificially stimulated transition from follicular to luteal cell types in rat ovary,” European Journal of Biochemistry, vol. 81, pp. 327–332, 1977. View at Publisher · View at Google Scholar · View at Scopus
  72. V. H. Black and J. J. Russo, “Stereological analysis of the guinea pig adrenal: effects of dexamethasone and ACTH treatment with emphasis on the inner cortex,” The American Journal of Anatomy, vol. 159, pp. 85–120, 1980. View at Publisher · View at Google Scholar · View at Scopus
  73. J. J. Russo and V. H. Black, “Hormone-dependent changes in peroxisomal enzyme activity in guinea pig adrenal,” The Journal of Biological Chemistry, vol. 257, pp. 3883–3889, 1982. View at Google Scholar
  74. R. C. Tuckey, Z. Kostadinovic, and P. M. Stevenson, “Ferredoxin and cytochrome P-450scc concentrations in granulosa cells of porcine ovaries during follicular cell growth and luteinization,” Journal of Steroid Biochemistry, vol. 31, pp. 201–205, 1988. View at Publisher · View at Google Scholar · View at Scopus
  75. S. G. Sligar, J. D. Lipscomb, P. G. Debrunner, and I. C. Gunsalus, “Superoxide anion production by the autoxidation of cytochrome P450cam,” Biochemical and Biophysical Research Communications, vol. 61, pp. 290–296, 1974. View at Publisher · View at Google Scholar · View at Scopus
  76. R. C. Tuckey and H. Kamin, “The oxyferro complex of adrenal cytochrome P-450scc. Effect of cholesterol and intermediates on its stability and optical characteristics,” The Journal of Biological Chemistry, vol. 257, pp. 9309–9314, 1982. View at Google Scholar
  77. J. W. Chu and T. Kimura, “Studies on adrenal steroid hydroxylases. Complex formation of the hydroxylase components,” The Journal of Biological Chemistry, vol. 248, pp. 5183–5187, 1973. View at Google Scholar
  78. K. Goda, J. Chu, T. Kimura, and A. P. Schaap, “Cytochrome c enhancement of singlet molecular oxygen production by the NADPH-dependent adrenodoxin reductase-adrenodoxin system: the role of singlet oxygen in damaging adrenal mitochondrial membranes,” Biochemical and Biophysical Research Communications, vol. 52, pp. 1300–1306, 1973. View at Publisher · View at Google Scholar · View at Scopus
  79. H. R. Behrman and R. F. Aten, “Evidence that hydrogen peroxide blocks hormone-sensitive cholesterol transport into mitochondria of rat luteal cells,” Endocrinology, vol. 128, pp. 2958–2966, 1991. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Shiotani, Y. Noda, K. Narimoto et al., “Immunohistochemical localization of superoxide dismutase in the human ovary,” Human Reproduction, vol. 6, pp. 1349–1353, 1991. View at Publisher · View at Google Scholar
  81. M. Laloraya, K. G. Pradeep, and M. M. Laloraya, “Changes in the levels of superoxide anion radical and superoxide dismutase during the estrous cycle of Rattus norvegicus and induction of superoxide dismutase in rat ovary by lutropin,” Biochemical and Biophysical Research Communications, vol. 157, pp. 146–153, 1988. View at Publisher · View at Google Scholar · View at Scopus
  82. M. Laloraya, G. P. Kumar, and M. M. Laloraya, “Histochemical study of superoxide dismutase in the ovary of the rat during the oestrous cycle,” Journal of Reproduction and Fertility, vol. 86, pp. 583–587, 1989. View at Publisher · View at Google Scholar
  83. C. M. Combelles, E. A. Holick, L. J. Paolella, D. C. Walker, and Q. Wu, “Profiling of superoxide dismutase isoenzymes in compartments of the developing bovine antral follicles,” Reproduction, vol. 139, pp. 871–881, 2010. View at Publisher · View at Google Scholar · View at Scopus
  84. F. Hozyen H, H. Ahmed H, G. E. Essawy, and S. I. Shalaby, “Seasonal changes in some oxidant and antioxidant parameters during folliculogenesis in Egyptian buffalo,” Animal Reproduction Science, vol. 151, pp. 131–136, 2014. View at Publisher · View at Google Scholar · View at Scopus
  85. L. Sabatini, C. Wilson, A. Lower, T. Al-Shawaf, and J. G. Grudzinskas, “Superoxide dismutase activity in human follicular fluid after controlled ovarian hyperstimulation in women undergoing in vitro fertilization,” Fertility and Sterility, vol. 72, pp. 1027–1034, 1999. View at Publisher · View at Google Scholar · View at Scopus
  86. M. L. Sutton, R. B. Gilchrist, and J. G. Thompson, “Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity,” Human Reproduction Update, vol. 9, pp. 35–48, 2003. View at Publisher · View at Google Scholar · View at Scopus
  87. H. Tatemoto, N. Muto, I. Sunagawa, A. Shinjo, and T. Nakada, “Protection of porcine oocytes against cell damage caused by oxidative stress during in vitro maturation: role of superoxide dismutase activity in porcine follicular fluid,” Biology of Reproduction, vol. 71, pp. 1150–1157, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. T. Ookawara, T. Kizaki, E. Takayama et al., “Nuclear translocation of extracellular superoxide dismutase,” Biochemical and Biophysical Research Communications, vol. 296, pp. 54–61, 2002. View at Google Scholar
  89. F. Johnson and C. Giulivi, “Superoxide dismutases and their impact upon human health,” Molecular Aspects of Medicine, vol. 26, pp. 340–352, 2005. View at Publisher · View at Google Scholar · View at Scopus
  90. I. A. Abreu and D. E. Cabelli, “Superoxide dismutases-a review of the metal-associated mechanistic variations,” Biochimica et Biophysica Acta, vol. 1804, pp. 263–274, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. E. Nozik-Grayck, H. B. Suliman, and C. A. Piantadosi, “Extracellular superoxide dismutase,” The International Journal of Biochemistry & Cell Biology, vol. 37, pp. 2466–2471, 2005. View at Publisher · View at Google Scholar · View at Scopus
  92. M. M. Matzuk, L. Dionne, Q. Guo, T. R. Kumar, and R. M. Lebovitz, “Ovarian function in superoxide dismutase 1 and 2 knockout mice,” Endocrinology, vol. 139, pp. 4008–4011, 1998. View at Publisher · View at Google Scholar
  93. P. C. Wong, D. Waggoner, J. R. Subramaniam et al., “Copper chaperone for superoxide dismutase is essential to activate mammalian Cu/Zn superoxide dismutase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, pp. 2886–2891, 2000. View at Publisher · View at Google Scholar · View at Scopus
  94. A. Kably Ambe, J. Ruiz Anguas, E. Carballo Mondragon, and S. Karchmer Krivitsky, “Intrafollicular levels of sexual steroids and their relation with the antioxidant enzymes on the oocyte quality in an in vitro fertilization program,” Ginecología y Obstetricia de México, vol. 73, pp. 19–27, 2005. View at Google Scholar
  95. P. S. LaPolt and L. S. Hong, “Inhibitory effects of superoxide dismutase and cyclic guanosine 3,5-monophosphate on estrogen production in cultured rat granulosa cells,” Endocrinology, vol. 136, pp. 5533–5539, 1995. View at Publisher · View at Google Scholar · View at Scopus
  96. M. Ujihara, K. Yamamoto, K. Nomura et al., “Subunit-specific sulphation of oligosaccharides relating to charge-heterogeneity in porcine lutrophin isoforms,” Glycobiology, vol. 2, pp. 225–231, 1992. View at Publisher · View at Google Scholar · View at Scopus
  97. S. Kawaguchi, R. Sakumoto, and K. Okuda, “Induction of the expressions of antioxidant enzymes by luteinizing hormone in the bovine corpus luteum,” The Journal of Reproduction and Development, vol. 59, pp. 219–224, 2013. View at Publisher · View at Google Scholar
  98. K. H. Al-Gubory, J. C. Huet, J. C. Pernollet, J. Martal, and A. Locatelli, “Corpus luteum derived copper, zinc-superoxide dismutase serves as a luteinizing hormone-release inhibiting factor in sheep,” Molecular and Cellular Endocrinology, vol. 199, pp. 1–9, 2003. View at Publisher · View at Google Scholar · View at Scopus
  99. A. Meister and M. E. Anderson, “Glutathione,” Annual Review of Biochemistry, vol. 52, pp. 711–760, 1983. View at Publisher · View at Google Scholar
  100. B. Ketterer, B. Coles, and D. J. Meyer, “The role of glutathione in detoxication,” Environmental Health Perspectives, vol. 49, pp. 59–69, 1983. View at Publisher · View at Google Scholar
  101. H. Sies, “Glutathione and its role in cellular functions,” Free Radical Biology & Medicine, vol. 27, pp. 916–921, 1999. View at Publisher · View at Google Scholar · View at Scopus
  102. T. Kaneko, Y. Iuchi, S. Kawachiya et al., “Alteration of glutathione reductase expression in the female reproductive organs during the estrous cycle,” Biology of Reproduction, vol. 65, pp. 1410–1416, 2001. View at Publisher · View at Google Scholar
  103. U. Luderer, T. J. Kavanagh, C. C. White, and E. M. Faustman, “Gonadotropin regulation of glutathione synthesis in the rat ovary,” Reproductive Toxicology, vol. 15, pp. 495–504, 2001. View at Google Scholar
  104. S. Y. Lee, J. Y. Lee, S. J. Oh, H. C. Kim, and S. K. Kim, “Expression of hepatic and ovarian antioxidant enzymes during estrous cycle in rats,” Toxicology Letters, vol. 212, pp. 329–336, 2012. View at Publisher · View at Google Scholar · View at Scopus
  105. C. S. Gardiner and D. J. Reed, “Status of glutathione during oxidant-induced oxidative stress in the preimplantation mouse embryo,” Biology of Reproduction, vol. 51, pp. 1307–1314, 1994. View at Publisher · View at Google Scholar · View at Scopus
  106. E. C. Curnow, J. Ryan, D. Saunders, and E. S. Hayes, “Bovine in vitro oocyte maturation as a model for manipulation of the gamma-glutamyl cycle and intraoocyte glutathione,” Reproduction, Fertility, and Development, vol. 20, pp. 579–588, 2008. View at Publisher · View at Google Scholar · View at Scopus
  107. M. C. Sanchez, C. A. Sedo, V. L. Julianelli et al., “Dermatan sulfate synergizes with heparin in murine sperm chromatin decondensation,” Systems Biology in Reproductive Medicine, vol. 59, pp. 82–90, 2013. View at Publisher · View at Google Scholar · View at Scopus
  108. D. G. de Matos, C. C. Furnus, D. F. Moses, and H. Baldassarre, “Effect of cysteamine on glutathione level and developmental capacity of bovine oocyte matured in vitro,” Molecular Reproduction and Development, vol. 42, pp. 432–436, 1995. View at Publisher · View at Google Scholar · View at Scopus
  109. M. Takahashi, T. Nagai, S. Hamano, M. Kuwayama, N. Okamura, and A. Okano, “Effect of thiol compounds on in vitro development and intracellular glutathione content of bovine embryos,” Biology of Reproduction, vol. 49, pp. 228–232, 1993. View at Publisher · View at Google Scholar
  110. T. Paszkowski, A. I. Traub, S. Y. Robinson, and D. McMaster, “Selenium dependent glutathione peroxidase activity in human follicular fluid,” Clinica Chimica Acta, vol. 236, pp. 173–180, 1995. View at Publisher · View at Google Scholar · View at Scopus
  111. N. Clague, M. Sevcik, G. Stuart, M. Brannstrom, P. O. Janson, and J. F. Jarrell, “The effect of estrous cycle and buthionine sulfoximine on glutathione release from the in vitro perfused rat ovary,” Reproductive Toxicology, vol. 6, pp. 533–539, 1992. View at Publisher · View at Google Scholar · View at Scopus
  112. N. Maedomari, K. Kikuchi, M. Ozawa et al., “Cytoplasmic glutathione regulated by cumulus cells during porcine oocyte maturation affects fertilization and embryonic development in vitro,” Theriogenology, vol. 67, pp. 983–993, 2007. View at Publisher · View at Google Scholar · View at Scopus
  113. E. J. Schoevers, B. Colenbrander, and B. A. Roelen, “Developmental stage of the oocyte during antral follicle growth and cumulus investment determines in vitro embryo development of sow oocytes,” Theriogenology, vol. 67, pp. 1108–1122, 2007. View at Publisher · View at Google Scholar · View at Scopus
  114. A. M. Luciano, V. Lodde, M. S. Beretta, S. Colleoni, A. Lauria, and S. Modina, “Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus-oocyte complexes: role of cumulus cells, cyclic adenosine 3,5-monophosphate, and glutathione,” Molecular Reproduction and Development, vol. 71, pp. 389–397, 2005. View at Publisher · View at Google Scholar · View at Scopus
  115. A. M. Luciano, G. Goudet, F. Perazzoli, C. Lahuec, and N. Gerard, “Glutathione content and glutathione peroxidase expression in in vivo and in vitro matured equine oocytes,” Molecular Reproduction and Development, vol. 73, pp. 658–666, 2006. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Ozawa, T. Nagai, T. Somfai et al., “Cumulus cell-enclosed oocytes acquire a capacity to synthesize GSH by FSH stimulation during in vitro maturation in pigs,” Journal of Cellular Physiology, vol. 222, pp. 294–301, 2010. View at Publisher · View at Google Scholar · View at Scopus
  117. M. L. Sutton-McDowall, M. Purdey, H. M. Brown et al., “Redox and anti-oxidant state within cattle oocytes following in vitro maturation with bone morphogenetic protein 15 and follicle stimulating hormone,” Molecular Reproduction and Development, vol. 82, pp. 281–294, 2015. View at Publisher · View at Google Scholar · View at Scopus
  118. T. S. Hussein, J. G. Thompson, and R. B. Gilchrist, “Oocyte-secreted factors enhance oocyte developmental competence,” Developmental Biology, vol. 296, pp. 514–521, 2006. View at Publisher · View at Google Scholar · View at Scopus
  119. J. L. Crawford and K. P. McNatty, “The ratio of growth differentiation factor 9: bone morphogenetic protein 15 mRNA expression is tightly co-regulated and differs between species over a wide range of ovulation rates,” Molecular and Cellular Endocrinology, vol. 348, pp. 339–343, 2012. View at Publisher · View at Google Scholar · View at Scopus
  120. Y. S. Ho, J. L. Magnenat, R. T. Bronson et al., “Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia,” The Journal of Biological Chemistry, vol. 272, pp. 16644–16651, 1997. View at Publisher · View at Google Scholar · View at Scopus
  121. L. J. Yant, Q. Ran, L. Rao et al., “The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults,” Free Radical Biology & Medicine, vol. 34, pp. 496–502, 2003. View at Publisher · View at Google Scholar · View at Scopus
  122. M. Schneider, H. Forster, A. Boersma et al., “Mitochondrial glutathione peroxidase 4 disruption causes male infertility,” The FASEB Journal, vol. 23, pp. 3233–3242, 2009. View at Publisher · View at Google Scholar · View at Scopus
  123. M. Conrad, S. G. Moreno, F. Sinowatz et al., “The nuclear form of phospholipid hydroperoxide glutathione peroxidase is a protein thiol peroxidase contributing to sperm chromatin stability,” Molecular and Cellular Biology, vol. 25, pp. 7637–7644, 2005. View at Publisher · View at Google Scholar · View at Scopus
  124. W. Pretsch, “Glutathione reductase activity deficiency in homozygous Gr1a1Neu mice does not cause haemolytic anaemia,” Genetical Research, vol. 73, pp. 1–5, 1999. View at Publisher · View at Google Scholar · View at Scopus
  125. L. K. Rogers, C. M. Bates, S. E. Welty, and C. V. Smith, “Diquat induces renal proximal tubule injury in glutathione reductase-deficient mice,” Toxicology and Applied Pharmacology, vol. 217, pp. 289–298, 2006. View at Publisher · View at Google Scholar · View at Scopus
  126. L. K. Rogers, T. Tamura, B. J. Rogers, S. E. Welty, T. N. Hansen, and C. V. Smith, “Analyses of glutathione reductase hypomorphic mice indicate a genetic knockout,” Toxicological Sciences, vol. 82, pp. 367–373, 2004. View at Publisher · View at Google Scholar · View at Scopus
  127. T. R. Kumar, A. L. Wiseman, G. Kala, S. V. Kala, M. M. Matzuk, and M. W. Lieberman, “Reproductive defects in gamma-glutamyl transpeptidase-deficient mice,” Endocrinology, vol. 141, pp. 4270–4277, 2000. View at Publisher · View at Google Scholar
  128. M. W. Lieberman, A. L. Wiseman, Z. Z. Shi et al., “Growth retardation and cysteine deficiency in gamma-glutamyl transpeptidase-deficient mice,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, pp. 7923–7926, 1996. View at Publisher · View at Google Scholar · View at Scopus
  129. Y. Will, K. A. Fischer, R. A. Horton et al., “Gamma-glutamyltranspeptidase-deficient knockout mice as a model to study the relationship between glutathione status, mitochondrial function, and cellular function,” Hepatology, vol. 32, pp. 740–749, 2000. View at Publisher · View at Google Scholar
  130. G. Giordano, C. C. White, L. A. McConnachie, C. Fernandez, T. J. Kavanagh, and L. G. Costa, “Neurotoxicity of domoic acid in cerebellar granule neurons in a genetic model of glutathione deficiency,” Molecular Pharmacology, vol. 70, pp. 2116–2126, 2006. View at Publisher · View at Google Scholar · View at Scopus
  131. Y. Yang, M. Z. Dieter, Y. Chen, H. G. Shertzer, D. W. Nebert, and T. P. Dalton, “Initial characterization of the glutamate-cysteine ligase modifier subunit Gclm(−/−) knockout mouse. Novel model system for a severely compromised oxidative stress response,” The Journal of Biological Chemistry, vol. 277, pp. 49446–49452, 2002. View at Publisher · View at Google Scholar · View at Scopus
  132. T. P. Dalton, M. Z. Dieter, Y. Yang, H. G. Shertzer, and D. W. Nebert, “Knockout of the mouse glutamate cysteine ligase catalytic subunit (Gclc) gene: embryonic lethal when homozygous, and proposed model for moderate glutathione deficiency when heterozygous,” Biochemical and Biophysical Research Communications, vol. 279, pp. 324–329, 2000. View at Publisher · View at Google Scholar · View at Scopus
  133. Z. Z. Shi, J. Osei-Frimpong, G. Kala et al., “Glutathione synthesis is essential for mouse development but not for cell growth in culture,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, pp. 5101–5106, 2000. View at Publisher · View at Google Scholar · View at Scopus
  134. B. N. Nakamura, T. J. Fielder, Y. D. Hoang et al., “Lack of maternal glutamate cysteine ligase modifier subunit (Gclm) decreases oocyte glutathione concentrations and disrupts preimplantation development in mice,” Endocrinology, vol. 152, pp. 2806–2815, 2011. View at Publisher · View at Google Scholar · View at Scopus
  135. S. G. Lopez and U. Luderer, “Effects of cyclophosphamide and buthionine sulfoximine on ovarian glutathione and apoptosis,” Free Radical Biology & Medicine, vol. 36, pp. 1366–1377, 2004. View at Publisher · View at Google Scholar · View at Scopus
  136. S. Y. Chun, H. Billig, J. L. Tilly, I. Furuta, A. Tsafriri, and A. J. Hsueh, “Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous insulin-like growth factor I,” Endocrinology, vol. 135, pp. 1845–1853, 1994. View at Publisher · View at Google Scholar · View at Scopus
  137. S. Y. Chun, K. M. Eisenhauer, S. Minami, H. Billig, E. Perlas, and A. J. Hsueh, “Hormonal regulation of apoptosis in early antral follicles: follicle-stimulating hormone as a major survival factor,” Endocrinology, vol. 137, pp. 1447–1456, 1996. View at Publisher · View at Google Scholar
  138. M. Tsai-Turton and U. Luderer, “Opposing effects of glutathione depletion and follicle-stimulating hormone on reactive oxygen species and apoptosis in cultured preovulatory rat follicles,” Endocrinology, vol. 147, pp. 1224–1236, 2006. View at Publisher · View at Google Scholar · View at Scopus
  139. Y. D. Hoang, B. N. Nakamura, and U. Luderer, “Follicle-stimulating hormone and estradiol interact to stimulate glutathione synthesis in rat ovarian follicles and granulosa cells,” Biology of Reproduction, vol. 81, pp. 636–646, 2009. View at Publisher · View at Google Scholar
  140. J. L. Tilly and K. I. Tilly, “Inhibitors of oxidative stress mimic the ability of follicle-stimulating hormone to suppress apoptosis in cultured rat ovarian follicles,” Endocrinology, vol. 136, pp. 242–252, 1995. View at Publisher · View at Google Scholar · View at Scopus
  141. E. D. Dubinskaia, A. S. Gasparov, T. A. Fedorova, and N. V. Lapteva, “Role of the genetic factors, detoxication systems and oxidative stress in the pathogenesis of endometriosis and infertility (review),” Vestnik Rossiĭskoĭ Akademii Meditsinskikh Nauk, vol. 8, pp. 14–19, 2013. View at Google Scholar
  142. J. J. Tarin, “Potential effects of age-associated oxidative stress on mammalian oocytes/embryos,” Molecular Human Reproduction, vol. 2, pp. 717–724, 1996. View at Publisher · View at Google Scholar
  143. P. Guerin, S. El Mouatassim, and Y. Menezo, “Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings,” Human Reproduction Update, vol. 7, pp. 175–189, 2001. View at Publisher · View at Google Scholar · View at Scopus
  144. T. Sabuncu, H. Vural, M. Harma, and M. Harma, “Oxidative stress in polycystic ovary syndrome and its contribution to the risk of cardiovascular disease,” Clinical Biochemistry, vol. 34, pp. 407–413, 2001. View at Publisher · View at Google Scholar · View at Scopus
  145. E. H. Ruder, T. J. Hartman, J. Blumberg, and M. B. Goldman, “Oxidative stress and antioxidants: exposure and impact on female fertility,” Human Reproduction Update, vol. 14, pp. 345–357, 2008. View at Publisher · View at Google Scholar · View at Scopus
  146. L. Qin, W. Xu, X. Li et al., “Differential expression profile of immunological cytokines in local ovary in patients with polycystic ovarian syndrome: analysis by flow cytometry,” European Journal of Obstetrics, Gynecology, and Reproductive Biology, vol. 197, pp. 136–141, 2016. View at Publisher · View at Google Scholar · View at Scopus
  147. L. Chen, W. M. Xu, and D. Zhang, “Association of abdominal obesity, insulin resistance, and oxidative stress in adipose tissue in women with polycystic ovary syndrome,” Fertility and Sterility, vol. 102, pp. 1167–1174.e1164, 2014. View at Publisher · View at Google Scholar · View at Scopus
  148. T. Zuo, M. Zhu, and W. Xu, “Roles of oxidative stress in polycystic ovary syndrome and cancers,” Oxidative Medicine and Cellular Longevity, vol. 2016, Article ID 8589318, 14 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  149. B. Fauser, “Consensus on diagnostic criteria and longterm health risks related to polycystic ovary syndrome,” in ESHRE/ASRM-Sponsored 3rd PCOS Consensus Workshop Group, Vol. 8, pp. 19–25, Fertil Steril, Rotterdam, 2004. View at Google Scholar
  150. V. M. Victor, M. Rocha, C. Banuls et al., “Induction of oxidative stress and human leukocyte/endothelial cell interactions in polycystic ovary syndrome patients with insulin resistance,” The Journal of Clinical Endocrinology and Metabolism, vol. 96, pp. 3115–3122, 2011. View at Publisher · View at Google Scholar · View at Scopus
  151. D. Zhang, W. Y. Luo, H. Liao, C. F. Wang, and Y. Sun, “The effects of oxidative stress to PCOS,” Sichuan Da Xue Xue Bao Yi Xue Ban, vol. 39, pp. 421–423, 2008. View at Google Scholar
  152. F. Gonzalez, N. S. Rote, J. Minium, and J. P. Kirwan, “Reactive oxygen species-induced oxidative stress in the development of insulin resistance and hyperandrogenism in polycystic ovary syndrome,” The Journal of Clinical Endocrinology and Metabolism, vol. 91, pp. 336–340, 2006. View at Publisher · View at Google Scholar · View at Scopus
  153. ASRM, “Definition of “infertility”,” Fertility and Sterility, vol. 82, Supplement 1, article S206, 2004. View at Publisher · View at Google Scholar
  154. A. DeCherney, L. Nathan, M. Eskandari, and M. Cadieux, Current Obstetric & Gynecologic Diagnosis & Treatment, pp. 979–990, 2003.
  155. G. Polak, M. Koziol-Montewka, R. Tarkowski, and J. Kotarski, “Peritoneal fluid and plasma 4-hydroxynonenal and malonyldialdehyde concentrations in infertile women,” Ginekologia Polska, vol. 72, pp. 1316–1320, 2001. View at Google Scholar
  156. G. Polak, R. Rola, M. Gogacz, M. Koziol-Montewka, and J. Kotarski, “Malonyldialdehyde and total antioxidant status in the peritoneal fluid of infertile women,” Ginekologia Polska, vol. 70, pp. 135–140, 1999. View at Google Scholar
  157. S. Gupta, N. Surti, L. Metterle, A. Chandra, and A. Agarwal, “Antioxidants and female reproductive pathologies,” Archives of Medical Science Special Issues, vol. 5, pp. 151–173, 2009. View at Google Scholar
  158. Y. Wang, R. Sharma, T. Falcone, J. Goldberg, and A. Agarwal, “Importance of reactive oxygen species in the peritoneal fluid of women with endometriosis or idiopathic infertility,” Fertility and Sterility, vol. 68, pp. 826–830, 1997. View at Publisher · View at Google Scholar · View at Scopus
  159. R. Sharma, K. R. Biedenharn, J. M. Fedor, and A. Agarwal, “Lifestyle factors and reproductive health: taking control of your fertility,” Reproductive Biology and Endocrinology, vol. 11, p. 66, 2013. View at Publisher · View at Google Scholar · View at Scopus
  160. S. K. Chaube, P. V. Prasad, S. C. Thakur, and T. G. Shrivastav, “Hydrogen peroxide modulates meiotic cell cycle and induces morphological features characteristic of apoptosis in rat oocytes cultured in vitro,” Apoptosis, vol. 10, pp. 863–874, 2005. View at Publisher · View at Google Scholar · View at Scopus
  161. A. Tripathi, K. V. PremKumar, A. N. Pandey et al., “Melatonin protects against clomiphene citrate-induced generation of hydrogen peroxide and morphological apoptotic changes in rat eggs,” European Journal of Pharmacology, vol. 667, pp. 419–424, 2011. View at Publisher · View at Google Scholar · View at Scopus
  162. A. Tripathi, T. G. Shrivastav, and S. K. Chaube, “An increase of granulosa cell apoptosis mediates aqueous neem (Azadirachta Indica) leaf extract-induced oocyte apoptosis in rat,” International Journal of Applied and Basic Medical Research, vol. 3, pp. 27–36, 2013. View at Publisher · View at Google Scholar
  163. S. K. Chaube, T. G. Shrivastav, M. Tiwari, S. Prasad, A. Tripathi, and A. K. Pandey, “Neem (Azadirachta Indica L.) leaf extract deteriorates oocyte quality by inducing ROS-mediated apoptosis in mammals,” SpringerPlus, vol. 3, p. 464, 2014. View at Publisher · View at Google Scholar · View at Scopus
  164. A. Agarwal, T. M. Said, M. A. Bedaiwy, J. Banerjee, and J. G. Alvarez, “Oxidative stress in an assisted reproductive techniques setting,” Fertility and Sterility, vol. 86, pp. 503–512, 2006. View at Publisher · View at Google Scholar · View at Scopus
  165. A. Iborra, J. R. Palacio, and P. Martinez, “Oxidative stress and autoimmune response in the infertile woman,” Chemical Immunology and Allergy, vol. 88, pp. 150–162, 2005. View at Publisher · View at Google Scholar · View at Scopus
  166. M. C. Carbone, C. Tatone, S. Delle Monache et al., “Antioxidant enzymatic defences in human follicular fluid: characterization and age-dependent changes,” Molecular Human Reproduction, vol. 9, pp. 639–643, 2003. View at Publisher · View at Google Scholar · View at Scopus
  167. J. Lim and U. Luderer, “Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary,” Biology of Reproduction, vol. 84, pp. 775–782, 2011. View at Publisher · View at Google Scholar · View at Scopus
  168. H. Y. Lian, Y. Gao, G. Z. Jiao et al., “Antioxidant supplementation overcomes the deleterious effects of maternal restraint stress-induced oxidative stress on mouse oocytes,” Reproduction, vol. 146, pp. 559–568, 2013. View at Publisher · View at Google Scholar · View at Scopus
  169. H. Tamura, A. Takasaki, I. Miwa et al., “Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate,” Journal of Pineal Research, vol. 44, pp. 280–287, 2008. View at Publisher · View at Google Scholar · View at Scopus
  170. O. G. Eryilmaz, A. Devran, E. Sarikaya, F. N. Aksakal, L. Mollamahmutoglu, and N. Cicek, “Melatonin improves the oocyte and the embryo in IVF patients with sleep disturbances, but does not improve the sleeping problems,” Journal of Assisted Reproduction and Genetics, vol. 28, pp. 815–820, 2011. View at Publisher · View at Google Scholar · View at Scopus
  171. A. S. Batioglu, U. Sahin, B. Gurlek, N. Ozturk, and E. Unsal, “The efficacy of melatonin administration on oocyte quality,” Gynecological Endocrinology, vol. 28, pp. 91–93, 2012. View at Publisher · View at Google Scholar · View at Scopus
  172. M. Liu, Y. Yin, X. Ye et al., “Resveratrol protects against age-associated infertility in mice,” Human Reproduction, vol. 28, pp. 707–717, 2013. View at Publisher · View at Google Scholar · View at Scopus
  173. J. Mier-Cabrera, T. Aburto-Soto, S. Burrola-Mendez et al., “Women with endometriosis improved their peripheral antioxidant markers after the application of a high antioxidant diet,” Reproductive Biology and Endocrinology, vol. 7, p. 54, 2009. View at Publisher · View at Google Scholar · View at Scopus
  174. J. Mier-Cabrera, M. Genera-Garcia, J. De la Jara-Diaz, O. Perichart-Perera, F. Vadillo-Ortega, and C. Hernandez-Guerrero, “Effect of vitamins C and E supplementation on peripheral oxidative stress markers and pregnancy rate in women with endometriosis,” International Journal of Gynaecology and Obstetrics, vol. 100, pp. 252–256, 2008. View at Publisher · View at Google Scholar · View at Scopus
  175. I. A. Cotgreave, “N-Acetylcysteine: pharmacological considerations and experimental and clinical applications,” Advances in Pharmacology, vol. 38, pp. 205–227, 1997. View at Publisher · View at Google Scholar · View at Scopus
  176. G. S. Kelly, “Clinical applications of N-acetylcysteine,” Alternative Medicine Review, vol. 3, pp. 114–127, 1998. View at Google Scholar
  177. A. F. Amin, O. M. Shaaban, and M. A. Bediawy, “N-Acetyl cysteine for treatment of recurrent unexplained pregnancy loss,” Reproductive Biomedicine Online, vol. 17, pp. 722–726, 2008. View at Publisher · View at Google Scholar
  178. A. Rumbold, L. Duley, C. Crowther, and R. Haslam, “Antioxidants for preventing pre-eclampsia,” Cochrane Database of Systematic Reviews, vol. 4, article CD004227, 2005. View at Publisher · View at Google Scholar
  179. L. Poston, A. L. Briley, P. T. Seed, F. J. Kelly, A. H. Shennan, and Vitamins in Pre-eclampsia (VIP) Trial Consortium, “Vitamin C and vitamin E in pregnant women at risk for pre-eclampsia (VIP trial): randomised placebo-controlled trial,” Lancet, vol. 367, pp. 1145–1154, 2006. View at Publisher · View at Google Scholar · View at Scopus
  180. J. M. Roberts, L. Myatt, C. Y. Spong et al., “Vitamins C and E to prevent complications of pregnancy-associated hypertension,” The New England Journal of Medicine, vol. 362, pp. 1282–1291, 2010. View at Publisher · View at Google Scholar · View at Scopus
  181. H. Xu, R. Perez-Cuevas, X. Xiong et al., “An international trial of antioxidants in the prevention of preeclampsia (INTAPP),” American Journal of Obstetrics and Gynecology, vol. 202, pp. 239.e1–239.e10, 2010. View at Publisher · View at Google Scholar · View at Scopus
  182. G. S. Aseervatham, T. Sivasudha, R. Jeyadevi, and D. Arul Ananth, “Environmental factors and unhealthy lifestyle influence oxidative stress in humans—an overview,” Environmental Science and Pollution Research International, vol. 20, pp. 4356–4369, 2013. View at Publisher · View at Google Scholar · View at Scopus