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BioMed Research International
Volume 2015, Article ID 513196, 10 pages
http://dx.doi.org/10.1155/2015/513196
Review Article

Variations in Antioxidant Genes and Male Infertility

Bolan Yu1,2 and Zhaofeng Huang3,4,5

1Key Laboratory for Major Obstetric Diseases of Guangdong Province, Third Affiliated Hospital of Guangzhou Medical University, Guangzhou 510150, China
2Key Laboratory of Reproduction and Genetics of Guangdong Higher Education Institutes, Third Affiliated Hospital of Guangzhou Medical University, Guangzhou 510150, China
3Institute of Human Virology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China
4Department of Biochemistry, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510080, China
5Key Laboratory of Tropical Diseases Control, Sun Yat-sen University, Ministry of Education in China, Guangzhou 510080, China

Received 21 May 2015; Revised 9 September 2015; Accepted 15 October 2015

Academic Editor: Katrien Stouffs

Copyright © 2015 Bolan Yu and Zhaofeng Huang. 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. B. Halliwell and C. E. Cross, “Oxygen-derived species: their relation to human disease and environmental stress,” Environmental Health Perspectives, vol. 102, supplement 10, pp. 5–12, 1994. View at Google Scholar · View at Scopus
  2. F. R. Ochsendorf, “Infections in the male genital tract and reactive oxygen species,” Human Reproduction Update, vol. 5, no. 5, pp. 399–420, 1999. View at Publisher · View at Google Scholar · View at Scopus
  3. G. Lavranos, M. Balla, A. Tzortzopoulou, V. Syriou, and R. Angelopoulou, “Investigating ROS sources in male infertility: a common end for numerous pathways,” Reproductive Toxicology, vol. 34, no. 3, pp. 298–307, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. H. Chen, H.-X. Zhao, X.-F. Huang et al., “Does high load of oxidants in human semen contribute to male factor infertility?” Antioxidants and Redox Signaling, vol. 16, no. 8, pp. 754–759, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. K. Tremellen, “Oxidative stress and male infertility—a clinical perspective,” Human Reproduction Update, vol. 14, no. 3, pp. 243–258, 2008. View at Publisher · View at Google Scholar · View at Scopus
  6. T. W. Kensler, N. Wakabayashi, and S. Biswal, “Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway,” Annual Review of Pharmacology and Toxicology, vol. 47, pp. 89–116, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. B. N. Nakamura, G. Lawson, J. Y. Chan et al., “Knockout of the transcription factor NRF2 disrupts spermatogenesis in an age-dependent manner,” Free Radical Biology and Medicine, vol. 49, no. 9, pp. 1368–1379, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. R. J. Aitken, D. W. Buckingham, A. Carreras, and D. S. Irvine, “Superoxide dismutase in human sperm suspensions: relationship with cellular composition, oxidative stress, and sperm function,” Free Radical Biology and Medicine, vol. 21, no. 4, pp. 495–504, 1996. View at Publisher · View at Google Scholar · View at Scopus
  9. C. Jeulin, J. C. Soufir, P. Weber, D. Laval-Martin, and R. Calvayrac, “Catalase activity in human spermatozoa and seminal plasma,” Gamete Research, vol. 24, no. 2, pp. 185–196, 1989. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Meseguer, J. A. Martínez-Conejero, L. Muriel, A. Pellicer, J. Remohí, and N. Garrido, “The human sperm glutathione system: a key role in male fertility and successful cryopreservation,” Drug Metabolism Letters, vol. 1, no. 2, pp. 121–126, 2007. View at Publisher · View at Google Scholar · View at Scopus
  11. D. T. Carrell and K. I. Aston, “The search for SNPs, CNVs, and epigenetic variants associated with the complex disease of male infertility,” Systems Biology in Reproductive Medicine, vol. 57, no. 1-2, pp. 17–26, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. B. Yu, J. Chen, D. Liu et al., “Cigarette smoking is associated with human semen quality in synergy with functional NRF2 polymorphisms,” Biology of Reproduction, vol. 89, no. 1, article 5, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. R. Peeker, L. Abramsson, and S. L. Marklund, “Superoxide dismutase isoenzymes in human seminal plasma and spermatozoa,” Molecular Human Reproduction, vol. 3, no. 12, pp. 1061–1066, 1997. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Revelli, G. Soldati, C. Costamagna et al., “Follicular fluid proteins stimulate nitric oxide (NO) synthesis in human sperm: a possible role for no in acrosomal reaction,” Journal of Cellular Physiology, vol. 178, no. 1, pp. 85–92, 1999. View at Google Scholar · View at Scopus
  15. A. Oakley, “Glutathione transferases: a structural perspective,” Drug Metabolism Reviews, vol. 43, no. 2, pp. 138–151, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. B. Ozkosem, S. I. Feinstein, A. B. Fisher, and C. O’Flaherty, “Advancing age increases sperm chromatin damage and impairs fertility in peroxiredoxin 6 null mice,” Redox Biology, vol. 5, pp. 15–23, 2015. View at Publisher · View at Google Scholar
  17. Y. Iuchi, F. Okada, S. Tsunoda et al., “Peroxiredoxin 4 knockout results in elevated spermatogenic cell death via oxidative stress,” Biochemical Journal, vol. 419, no. 1, pp. 149–158, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. J. R. Drevet, “The antioxidant glutathione peroxidase family and spermatozoa: a complex story,” Molecular and Cellular Endocrinology, vol. 250, no. 1-2, pp. 70–79, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. T. B. Smith, M. A. Baker, H. S. Connaughton, U. Habenicht, and R. J. Aitken, “Functional deletion of Txndc2 and Txndc3 increases the susceptibility of spermatozoa to age-related oxidative stress,” Free Radical Biology and Medicine, vol. 65, pp. 872–881, 2013. View at Publisher · View at Google Scholar · View at Scopus
  20. B. Yu, H. Lin, L. Yang et al., “Genetic variation in the Nrf2 promoter associates with defective spermatogenesis in humans,” Journal of Molecular Medicine, vol. 90, no. 11, pp. 1333–1342, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Tirumala Vani, N. Mukesh, B. Siva Prasad et al., “Role of glutathione S-transferase Mu-1 (GSTM1) polymorphism in oligospermic infertile males,” Andrologia, vol. 42, no. 4, pp. 213–217, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. S.-S. Chen, L. S. Chang, H.-W. Chen, and Y.-H. Wei, “Polymorphisms of glutathione S-transferase M1 and male infertility in Taiwanese patients with varicocele,” Human Reproduction, vol. 17, no. 3, pp. 718–725, 2002. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Aydemir, I. Onaran, A. R. Kiziler, B. Alici, and M. C. Akyolcu, “Increased oxidative damage of sperm and seminal plasma in men with idiopathic infertility is higher in patients with glutathione S-transferase Mu-1 null genotype,” Asian Journal of Andrology, vol. 9, no. 1, pp. 108–115, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. A. C. F. Finotti, R. C. P. C. E Silva, B. M. Bordin, C. T. X. Silva, and K. K. V. O. Moura, “Glutathione S-transferase M1 and T1 polymorphism in men with idiopathic infertility,” Genetics and Molecular Research, vol. 8, no. 3, pp. 1093–1098, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. O. H. Roshdy, T. M. Hussein, N. H. Zakaria, and A. A. Sabry, “Glutathione S-transferase Mu-1 gene polymorphism in Egyptian patients with idiopathic male infertility,” Andrologia, vol. 47, no. 5, pp. 587–593, 2015. View at Publisher · View at Google Scholar
  26. M. R. Safarinejad, N. Shafiei, and S. Safarinejad, “The association of glutathione-S-transferase gene polymorphisms (GSTM1, GSTT1, GSTP1) with idiopathic male infertility,” Journal of Human Genetics, vol. 55, no. 9, pp. 565–570, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Tang, W. Xue, Y. Xing et al., “Genetic polymorphisms of glutathione S-transferase M1, T1, and P1, and the assessment of oxidative damage in infertile men with varicoceles from northwestern China,” Journal of Andrology, vol. 33, no. 2, pp. 257–263, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. X.-B. Xu, S.-R. Liu, H.-Q. Ying, and A. Zhou-Cun, “Null genotype of GSTM1 and GSTT1 may contribute to susceptibility to male infertility with impaired spermatogenesis in Chinese population,” Biomarkers, vol. 18, no. 2, pp. 151–154, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. Q. Wu, J. Xing, W. Xue, J. Sun, X. Wang, and X. Jin, “Influence of polymorphism of glutathione S-transferase T1 on Chinese infertile patients with varicocele,” Fertility and Sterility, vol. 91, no. 3, pp. 960–962, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. Q.-F. Wu, J.-P. Xing, K.-F. Tang et al., “Genetic polymorphism of glutathione S-transferase T1 gene and susceptibility to idiopathic azoospermia or oligospermia in northwestern China,” Asian Journal of Andrology, vol. 10, no. 2, pp. 266–270, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. D. K. Xiong, H. Chen, X. Ding, S. Zhang, and J. Zhang, “Association of polymorphisms in glutathione S-transferase genes (GSTM1, GSTT1, GSTP1) with idiopathic azoospermia or oligospermia in Sichuan, China,” Asian Journal of Andrology, vol. 17, no. 3, pp. 481–486, 2014. View at Publisher · View at Google Scholar
  32. K. Ichioka, K. Nagahama, K. Okubo, T. Soda, O. Ogawa, and H. Nishiyama, “Genetic polymorphisms in glutathione S-transferase T1 affect the surgical outcome of varicocelectomies in infertile patients,” Asian Journal of Andrology, vol. 11, no. 3, pp. 333–341, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. D. Hering, M. Lecewicz, W. Kordan, A. Majewska, and S. Kaminski, “Missense mutation in glutathione-S-transferase M1 gene is associated with sperm motility and ATP content in frozen-thawed semen of Holstein-Friesian bulls,” Animal Reproduction Science, vol. 159, pp. 94–97, 2015. View at Publisher · View at Google Scholar
  34. N. Lakpour, A. Mirfeizollahi, S. Farivar et al., “The association of seminal plasma antioxidant levels and sperm chromatin status with genetic variants of GSTM1 and GSTP1 (Ile105Val and Ala114Val) in infertile men with oligoasthenoteratozoospermia,” Disease Markers, vol. 34, no. 3, pp. 205–210, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. V. Paracchini, S.-S. Chang, R. M. Santella, S. Garte, P. Pedotti, and E. Taioli, “GSMT1 deletion modifies the levels of polycyclic aromatic hydrocarbon-DNA adducts in human sperm,” Mutation Research, vol. 586, no. 2, pp. 97–101, 2005. View at Publisher · View at Google Scholar · View at Scopus
  36. S. L. Yarosh, E. V. Kokhtenko, M. I. Churnosov, M. A. Solodilova, and A. V. Polonikov, “Joint effect of glutathione S-transferase genotypes and cigarette smoking on idiopathic male infertility,” Andrologia, vol. 47, no. 9, pp. 980–986, 2015. View at Publisher · View at Google Scholar
  37. S. E. Aydos, M. Taspinar, A. Sunguroglu, and K. Aydos, “Association of CYP1A1 and glutathione S-transferase polymorphisms with male factor infertility,” Fertility and Sterility, vol. 92, no. 2, pp. 541–547, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Yan, J. Liu, S. Wu, S. Zhang, G. Ji, and A. Gu, “Seminal superoxide dismutase activity and its relationship with semen quality and SOD gene polymorphism,” Journal of Assisted Reproduction and Genetics, vol. 31, no. 5, pp. 549–554, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. J. I. Ruiz-Sanz, I. Aurrekoetxea, R. Matorras, and M. B. Ruiz-Larrea, “Ala16Val SOD2 polymorphism is associated with higher pregnancy rates in in vitro fertilization cycles,” Fertility and Sterility, vol. 95, no. 5, pp. 1601–1605, 2011. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Faure, P. Leveille, C. Dupont et al., “Are superoxide dismutase 2 and nitric oxide synthase polymorphisms associated with idiopathic infertility?” Antioxidants and Redox Signaling, vol. 21, no. 4, pp. 565–569, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. G. Ji, A. Gu, Y. Wang et al., “Genetic variants in antioxidant genes are associated with sperm DNA damage and risk of male infertility in a Chinese population,” Free Radical Biology and Medicine, vol. 52, no. 4, pp. 775–780, 2012. View at Publisher · View at Google Scholar · View at Scopus
  42. I. Reveillaud, J. Phillips, B. Duyf, A. Hilliker, A. Kongpachith, and J. E. Fleming, “Phenotypic rescue by a bovine transgene in a Cu/Zn superoxide dismutase-null mutant of Drosophila melanogaster,” Molecular and Cellular Biology, vol. 14, no. 2, pp. 1302–1307, 1994. View at Publisher · View at Google Scholar · View at Scopus
  43. T. Ishii, S. Matsuki, Y. Iuchi et al., “Accelerated impairment of spermatogenic cells in SOD1-knockout mice under heat stress,” Free Radical Research, vol. 39, no. 7, pp. 697–705, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. S. Sabouhi, Z. Salehi, M. H. Bahadori, and M. Mahdavi, “Human catalase gene polymorphism (CAT C-262T) and risk of male infertility,” Andrologia, vol. 47, no. 1, pp. 97–101, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. H.-Q. Ying, X.-Y. Pu, S.-R. Liu, and Z.-C. A, “Genetic variants of eNOS gene may modify the susceptibility to idiopathic male infertility,” Biomarkers, vol. 18, no. 5, pp. 412–417, 2013. View at Publisher · View at Google Scholar
  46. T. Mostafa, L. A. Rashed, N. Nabil, H. Fouad, D. Sabry, and D. M. El-Saied, “Endothelial nitric oxide synthase gene polymorphism relationship with semen parameters and oxidative stress in infertile oligoasthenoteratozoospermic men,” Urology, vol. 85, no. 5, pp. 1058–1061, 2015. View at Publisher · View at Google Scholar
  47. M. R. Safarinejad, N. Shafiei, and S. Safarinejad, “The role of endothelial nitric oxide synthase (eNOS) T-786C, G894T, and 4a/b gene polymorphisms in the risk of idiopathic male infertility,” Molecular Reproduction and Development, vol. 77, no. 8, pp. 720–727, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. E. Buldreghini, R. Z. Mahfouz, A. Vignini et al., “Single nucleotide polymorphism (SNP) of the endothelial nitric oxide synthase (eNOS) gene (Glu298Asp variant) in infertile men with asthenozoospermia,” Journal of Andrology, vol. 31, no. 5, pp. 482–488, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. Q. Yu, Y. Zhang, Y. Xia et al., “Analysis of endothelial nitric oxide synthase (eNOS) G894T polymorphism and semen parameters in a Chinese Han population,” Andrologia, vol. 46, no. 5, pp. 541–546, 2014. View at Publisher · View at Google Scholar · View at Scopus
  50. L. Yan, W. Guo, S. Wu et al., “Genetic variants in nitric oxide synthase genes and the risk of male infertility in a Chinese population: a case-control study,” PLoS ONE, vol. 9, no. 12, Article ID e115190, 2014. View at Publisher · View at Google Scholar · View at Scopus
  51. Y.-J. Yun, J.-H. Park, S.-H. Song, and S. Lee, “The association of 4a4b polymorphism of endothelial nitric oxide synthase (eNOS) gene with the sperm morphology in Korean infertile men,” Fertility and Sterility, vol. 90, no. 4, pp. 1126–1131, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Schneider, H. Förster, A. Boersma et al., “Mitochondrial glutathione peroxidase 4 disruption causes male infertility,” The FASEB Journal, vol. 23, no. 9, pp. 3233–3242, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. H. Pfeifer, M. Conrad, D. Roethlein et al., “Identification of a specific sperm nuclei selenoenzyme necessary for protamine thiol cross-linking during sperm maturation,” The FASEB Journal, vol. 15, no. 7, pp. 1236–1238, 2001. View at Google Scholar · View at Scopus
  54. E. Chabory, C. Damon, A. Lenoir et al., “Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice,” Journal of Clinical Investigation, vol. 119, no. 7, pp. 2074–2085, 2009. View at Google Scholar · View at Scopus
  55. T. Nguyen, P. J. Sherratt, and C. B. Pickett, “Regulatory mechanisms controlling gene expression mediated by the antioxidant response element,” Annual Review of Pharmacology and Toxicology, vol. 43, pp. 233–260, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. N. Garrido, M. Meseguer, J. Alvarez, C. Simón, A. Pellicer, and J. Remohí, “Relationship among standard semen parameters, glutathione peroxidase/glutathione reductase activity, and mRNA expression and reduced glutathione content in ejaculated spermatozoa from fertile and infertile men,” Fertility and Sterility, vol. 82, supplement 3, pp. 1059–1066, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. A. C. Williams and W. C. L. Ford, “Functional significance of the pentose phosphate pathway and glutathione reductase in the antioxidant defenses of human sperm,” Biology of Reproduction, vol. 71, no. 4, pp. 1309–1316, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. X. Wang, D. J. Tomso, B. N. Chorley et al., “Identification of polymorphic antioxidant response elements in the human genome,” Human Molecular Genetics, vol. 16, no. 10, pp. 1188–1200, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. R. Holland and J. C. Fishbein, “Chemistry of the cysteine sensors in kelch-like ECH-associated protein 1,” Antioxidants and Redox Signaling, vol. 13, no. 11, pp. 1749–1761, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. T. Prestera and P. Talalay, “Electrophile and antioxidant regulation of enzymes that detoxify carcinogens,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 19, pp. 8965–8969, 1995. View at Publisher · View at Google Scholar · View at Scopus
  61. M. B. Sporn and K. T. Liby, “Cancer chemoprevention: scientific promise, clinical uncertainty,” Nature Clinical Practice Oncology, vol. 2, no. 10, pp. 518–525, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. M.-K. Kwak, N. Wakabayashi, K. Itoh, H. Motohashi, M. Yamamoto, and T. W. Kensler, “Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway: identification of novel gene clusters for cell survival,” Journal of Biological Chemistry, vol. 278, no. 10, pp. 8135–8145, 2003. View at Publisher · View at Google Scholar · View at Scopus
  63. D. D. Zhang and M. Hannink, “Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress,” Molecular and Cellular Biology, vol. 23, no. 22, pp. 8137–8151, 2003. View at Publisher · View at Google Scholar · View at Scopus
  64. P. Chelikani, I. Fita, and P. C. Loewen, “Diversity of structures and properties among catalases,” Cellular and Molecular Life Sciences, vol. 61, no. 2, pp. 192–208, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Moncada and A. Higgs, “The L-arginine-nitric oxide pathway,” The New England Journal of Medicine, vol. 329, no. 27, pp. 2002–2012, 1993. View at Publisher · View at Google Scholar · View at Scopus
  66. G. R. Drummond, H. Cai, M. E. Davis, S. Ramasamy, and D. G. Harrison, “Transcriptional and posttranscriptional regulation of endothelial nitric oxide synthase expression by hydrogen peroxide,” Circulation Research, vol. 86, no. 3, pp. 347–354, 2000. View at Publisher · View at Google Scholar · View at Scopus
  67. J. Kanner, S. Harel, and G. Rina, “Nitric oxide as an antioxidant,” Archives of Biochemistry and Biophysics, vol. 289, no. 1, pp. 130–136, 1991. View at Publisher · View at Google Scholar · View at Scopus
  68. N. V. Gorbunov, J. C. Yalowich, A. Gaddam et al., “Nitric oxide prevents oxidative damage produced by tert-butyl hydroperoxide in erythroleukemia cells via nitrosylation of heme and non-heme iron. Electron paramagnetic resonance evidence,” The Journal of Biological Chemistry, vol. 272, no. 19, pp. 12328–12341, 1997. View at Publisher · View at Google Scholar · View at Scopus
  69. D. J. Stuehr, “Mammalian nitric oxide synthases,” Biochimica et Biophysica Acta, vol. 1411, no. 2-3, pp. 217–230, 1999. View at Publisher · View at Google Scholar · View at Scopus
  70. R. Udomsinprasert, S. Pongjaroenkit, J. Wongsantichon et al., “Identification, characterization and structure of a new Delta class glutathione transferase isoenzyme,” Biochemical Journal, vol. 388, no. 3, pp. 763–771, 2005. View at Publisher · View at Google Scholar · View at Scopus
  71. J. D. Hayes, J. U. Flanagan, and I. R. Jowsey, “Glutathione transferases,” Annual Review of Pharmacology and Toxicology, vol. 45, pp. 51–88, 2005. View at Publisher · View at Google Scholar · View at Scopus
  72. E. S. J. Arnér and A. Holmgren, “Physiological functions of thioredoxin and thioredoxin reductase,” European Journal of Biochemistry, vol. 267, no. 20, pp. 6102–6109, 2000. View at Publisher · View at Google Scholar · View at Scopus
  73. A. Holmgren, “Thioredoxin and glutaredoxin: small multi-functional redox proteins with active-site disulphide bonds,” Biochemical Society Transactions, vol. 16, no. 2, pp. 95–96, 1988. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Holmgren, “Thioredoxin and glutaredoxin systems,” Journal of Biological Chemistry, vol. 264, no. 24, pp. 13963–13966, 1989. View at Google Scholar · View at Scopus
  75. J. M. Hansen, Y.-M. Go, and D. P. Jones, “Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling,” Annual Review of Pharmacology and Toxicology, vol. 46, pp. 215–234, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. W. H. Watson and D. P. Jones, “Oxidation of nuclear thioredoxin during oxidative stress,” FEBS Letters, vol. 543, no. 1–3, pp. 144–147, 2003. View at Publisher · View at Google Scholar · View at Scopus
  77. W. Gu and N. B. Hecht, “Developmental expression of glutathione peroxidase, catalase, and manganese superoxide dismutase mRNAs during spermatogenesis in the mouse,” Journal of Andrology, vol. 17, no. 3, pp. 256–262, 1996. View at Google Scholar · View at Scopus
  78. K. Chen, Z. Mai, Y. Zhou, X. Gao, and B. Yu, “Low NRF2 mRNA expression in spermatozoa from men with low sperm motility,” Tohoku Journal of Experimental Medicine, vol. 228, no. 3, pp. 259–266, 2012. View at Publisher · View at Google Scholar · View at Scopus
  79. C.-N. An, H. Jiang, Q. Wang et al., “Down-regulation of DJ-1 protein in the ejaculated spermatozoa from Chinese asthenozoospermia patients,” Fertility and Sterility, vol. 96, no. 1, pp. 19–23.e2, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. C. M. Clements, R. S. McNally, B. J. Conti, T. W. Mak, and J. P.-Y. Ting, “DJ-1, a cancer- and Parkinson's disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 41, pp. 15091–15096, 2006. View at Publisher · View at Google Scholar · View at Scopus
  81. O. Moscovitz, G. Ben-Nissan, I. Fainer, D. Pollack, L. Mizrachi, and M. Sharon, “The Parkinson's-associated protein DJ-1 regulates the 20S proteasome,” Nature Communications, vol. 6, article 6609, 2015. View at Publisher · View at Google Scholar
  82. X. Song, Y. Zhao, Q. Cai, Y. Zhang, and Y. Niu, “Association of the glutathione S-transferases M1 and T1 polymorphism with male infertility: a meta-Analysis,” Journal of Assisted Reproduction and Genetics, vol. 30, no. 1, pp. 131–141, 2013. View at Publisher · View at Google Scholar · View at Scopus
  83. H.-Q. Ying, Y. Qi, X.-Y. Pu, S.-R. Liu, and A. Zhou-Cun, “Association of GSTM1 and GSTT1 genes with the susceptibility to male infertility: result from a meta-analysis,” Genetic Testing and Molecular Biomarkers, vol. 17, no. 7, pp. 535–542, 2013. View at Publisher · View at Google Scholar · View at Scopus
  84. W. Wu, J. Lu, Q. Tang et al., “GSTM1 and GSTT1 null polymorphisms and male infertility risk: an updated meta-analysis encompassing 6934 subjects,” Scientific Reports, vol. 3, article 2258, 2013. View at Publisher · View at Google Scholar
  85. M. Tang, S. Wang, W. Wang et al., “The glutathione-S-transferase gene polymorphisms (GSTM1 and GSTT1) and idiopathic male infertility risk: a meta-analysis,” Gene, vol. 511, no. 2, pp. 218–223, 2012. View at Publisher · View at Google Scholar · View at Scopus
  86. W. W. Jow, P. N. Schlegel, Z. Cichon, D. Phillips, M. Goldstein, and C. W. Bardin, “Identification and localization of copper-zinc superoxide dismutase gene expression in rat testicular development,” Journal of Andrology, vol. 14, no. 6, pp. 439–447, 1993. View at Google Scholar · View at Scopus
  87. T. R. Pushpa-Rekha, A. L. Burdsall, L. M. Oleksa, G. M. Chisolm, and D. M. Driscoll, “Rat phospholipid-hydroperoxide glutathione peroxidase. cDNA cloning and identification of multiple transcription and translation start sites,” The Journal of Biological Chemistry, vol. 270, no. 45, pp. 26993–26999, 1995. View at Publisher · View at Google Scholar · View at Scopus
  88. H. Imai, N. Hakkaku, R. Iwamoto et al., “Depletion of selenoprotein GPx4 in spermatocytes causes male infertility in mice,” Journal of Biological Chemistry, vol. 284, no. 47, pp. 32522–32532, 2009. View at Publisher · View at Google Scholar · View at Scopus
  89. D. Hering, M. Lecewicz, W. Kordan, and S. Kamiński, “Association between ETFA genotype and activity of superoxide dismutase, catalase and glutathione peroxidase in cryopreserved sperm of Holstein-Friesian bull,” Reproduction in Domestic Animals, vol. 50, no. 1, pp. 168–171, 2014. View at Publisher · View at Google Scholar · View at Scopus
  90. H. Imai, K. Suzuki, K. Ishizaka et al., “Failure of the expression of phospholipid hydroperoxide glutathione peroxidase in the spermatozoa of human infertile males,” Biology of Reproduction, vol. 64, no. 2, pp. 674–683, 2001. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Diaconu, Y. Tangat, D. Böhm et al., “Failure of phospholipid hydroperoxide glutathione peroxidase expression in oligoasthenozoospermia and mutations in the PHGPx gene,” Andrologia, vol. 38, no. 4, pp. 152–157, 2006. View at Publisher · View at Google Scholar · View at Scopus
  92. E. Kawakami, A. Takemura, M. Sakuma et al., “Superoxide dismutase and catalase activities in the seminal plasma of normozoospermic and asthenozoospermic beagles,” Journal of Veterinary Medical Science, vol. 69, no. 2, pp. 133–136, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. L. Storgaard, J. P. Bonde, E. Ernst et al., “Genetic and environmental correlates of semen quality: a twin study,” Epidemiology, vol. 17, no. 6, pp. 674–681, 2006. View at Publisher · View at Google Scholar · View at Scopus
  94. K. I. Aston, C. Krausz, I. Laface, E. Ruiz-Castané, and D. T. Carrell, “Evaluation of 172 candidate polymorphisms for association with oligozoospermia or azoospermia in a large cohort of men of European descent,” Human Reproduction, vol. 25, no. 6, pp. 1383–1397, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. G. Kosova, N. M. Scott, C. Niederberger, G. S. Prins, and C. Ober, “Genome-wide association study identifies candidate genes for male fertility traits in humans,” American Journal of Human Genetics, vol. 90, no. 6, pp. 950–961, 2012. View at Publisher · View at Google Scholar · View at Scopus
  96. Z. Hu, Y. Xia, X. Guo et al., “A genome-wide association study in Chinese men identifies three risk loci for non-obstructive azoospermia,” Nature Genetics, vol. 44, no. 2, pp. 183–186, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. Z. Hu, Z. Li, J. Yu et al., “Association analysis identifies new risk loci for non-obstructive azoospermia in Chinese men,” Nature Communications, vol. 5, article 3857, 2014. View at Publisher · View at Google Scholar
  98. K. I. Aston, “Genetic susceptibility to male infertility: news from genome-wide association studies,” Andrology, vol. 2, no. 3, pp. 315–321, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. D. M. Hering, K. Oleński, A. Ruść, and S. Kaminski, “Genome-wide association study for semen volume and total number of sperm in Holstein-Friesian bulls,” Animal Reproduction Science, vol. 151, no. 3-4, pp. 126–130, 2014. View at Publisher · View at Google Scholar · View at Scopus
  100. D. M. Hering, K. Olenski, and S. Kaminski, “Genome-wide association study for sperm concentration in Holstein-Friesian bulls,” Reproduction in Domestic Animals, vol. 49, no. 6, pp. 1008–1014, 2014. View at Publisher · View at Google Scholar
  101. D. M. Hering, K. Olenski, and S. Kaminski, “Genome-wide association study for poor sperm motility in Holstein-Friesian bulls,” Animal Reproduction Science, vol. 146, no. 3-4, pp. 89–97, 2014. View at Publisher · View at Google Scholar · View at Scopus