Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Impact of oxidative stress SNPs on sperm DNA damage and male infertility in a south-east Iranian population

Zahra Miri Karam A B , Milad Baba Salari A , Ahmad Anjom Shoaa A , Somaye Dehghan Kouhestani C D , Asma Bahram Nejad E , Sareh Ashourzadeh F , Moahammad Reza Zangouyee A and Mohammad Reza Bazrafshani https://orcid.org/0000-0002-4391-2371 A G *
+ Author Affiliations
- Author Affiliations

A Department of Medical Genetics, Afzalipour School of Medicine, Kerman University of Medical Sciences, Kerman, Iran.

B Physiology Research Center, Institute of Neuropharmacology, Kerman University of Medical Sciences, Kerman, Iran.

C Department of Medical Biotechnology, Faculty of Medical Sciences, Tarbiat Moddares University, Tehran, Iran.

D Dr. Bazrafshani’s Medical Genetic Laboratory, Kerman, Iran.

E Higher Education Institute Rabe_Rashidi, Tabriz, Iran.

F Afzalipour Clinical Center for Infertility, Kerman University of Medical Sciences, Kerman, Iran.

G Centre for Integrated Genomic Medical Research (CIGMR), University of Manchester, Stopford Building, Oxford Road, Manchester M13 9PT, UK.

* Correspondence to: Bazr61@yahoo.co.uk

Handling Editor: Tod Fullston

Reproduction, Fertility and Development 34(8) 633-643 https://doi.org/10.1071/RD21305
Published online: 1 April 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Aim: We examined four single nucleotide polymorphisms in four antioxidant genes (PON1, CAT, GPx1 and SOD2) in 100 infertility cases and 100 controls from an Iranian population-based case–control study to confirm the assumption that polymorphisms in oxidative stress genes increase the risk of sperm DNA damage and idiopathic male infertility.

Methods: Restriction fragment length polymorphism and tetra-primer amplification refractory mutation system PCR were used to identify genotypes. Sperm DNA damage was assessed using the Sperm Chromatin Dispersion test (Halo Sperm), and the total antioxidant capacity of seminal fluid was determined using the FRAP assay.

Key results: Our findings demonstrated that alleles Arg-PON1 (rs662) and Ala-MnSOD (rs4880) variant genotypes were considerably linked with a higher risk of male infertility.

Conclusions: Linear regression analysis revealed that those with the PON1 Gln192Arg or SOD2 Val16Ala variants have significantly higher levels of sperm DNA fragmentation and lower levels of the total antioxidant capacity in seminal fluid.

Implications: These findings suggest that genetic differences in antioxidant genes may be linked to oxidative stress, sperm DNA damage, and idiopathic male infertility.

Keywords: DNA, enzyme, fertility, genotypying, oxidative stress, polymorphisms, semen, sperm.


References

Agarwal, A, and Said, TM (2003). Role of sperm chromatin abnormalities and DNA damage in male infertility. Human Reproduction Update 9, 331–345.
Role of sperm chromatin abnormalities and DNA damage in male infertility.Crossref | GoogleScholarGoogle Scholar | 12926527PubMed |

Agarwal, A, Virk, G, Ong, C, and du Plessis, SS (2014). Effect of oxidative stress on male reproduction. The World Journal of Men’s Health 32, 1–17.
Effect of oxidative stress on male reproduction.Crossref | GoogleScholarGoogle Scholar | 24872947PubMed |

Aitken, RJ (2013). Human spermatozoa: revelations on the road to conception. F1000Prime Reports 5, 39.
Human spermatozoa: revelations on the road to conception.Crossref | GoogleScholarGoogle Scholar | 24167720PubMed |

Aitken, J, and Fisher, H (1994). Reactive oxygen species generation and human spermatozoa: the balance of benefit and risk. BioEssays 16, 259–267.
Reactive oxygen species generation and human spermatozoa: the balance of benefit and risk.Crossref | GoogleScholarGoogle Scholar | 8031303PubMed |

Aitken, RJ, Bu, DW, and West, KM (1992). Reactive oxygen species and human spermatozoa: analysis of the cellular mechanisms involved in luminol- and lucigenin-dependent chemiluminescence. Journal of Cellular Physiology 151, 466–477.
Reactive oxygen species and human spermatozoa: analysis of the cellular mechanisms involved in luminol- and lucigenin-dependent chemiluminescence.Crossref | GoogleScholarGoogle Scholar | 1338331PubMed |

Aitken, RJ, De Iuliis, GN, and McLachlan, RI (2009). Biological and clinical significance of DNA damage in the male germ line. International Journal of Andrology 32, 46–56.
Biological and clinical significance of DNA damage in the male germ line.Crossref | GoogleScholarGoogle Scholar | 19076252PubMed |

Aitken, RJ, Smith, TB, Jobling, MS, Baker, MA, and De Iuliis, GN (2014). Oxidative stress and male reproductive health. Asian Journal of Andrology 16, 31.
Oxidative stress and male reproductive health.Crossref | GoogleScholarGoogle Scholar | 24369131PubMed |

Aldridge, WN (1953). Serum esterases. 2. An enzyme hydrolysing diethyl p-nitrophenyl phosphate (E600) and its identity with the A-esterase of mammalian sera. Biochemical Journal 53, 117–124.
Serum esterases. 2. An enzyme hydrolysing diethyl p-nitrophenyl phosphate (E600) and its identity with the A-esterase of mammalian sera.Crossref | GoogleScholarGoogle Scholar |

Allamaneni, SSR, Naughton, CK, Sharma, RK, Thomas, AJ, and Agarwal, A (2004). Increased seminal reactive oxygen species levels in patients with varicoceles correlate with varicocele grade but not with testis size. Fertility and Sterility 82, 1684–1686.
Increased seminal reactive oxygen species levels in patients with varicoceles correlate with varicocele grade but not with testis size.Crossref | GoogleScholarGoogle Scholar |

Aseervatham, GSB, Sivasudha, T, Jeyadevi, R, and Ananth, DA (2013). Environmental factors and unhealthy lifestyle influence oxidative stress in humans – an overview. Environmental Science and Pollution Research 20, 4356–4369.
Environmental factors and unhealthy lifestyle influence oxidative stress in humans – an overview.Crossref | GoogleScholarGoogle Scholar |

Ávila Júnior, S, Possamai, FP, Budni, P, Backes, P, Parisotto, EB, Rizelio, VM, Torres, MA, Colepicolo, P, and Wilhelm Filho, D (2009). Occupational airborne contamination in South Brazil: 1. Oxidative stress detected in the blood of coal miners. Ecotoxicology 18, 1150–1157.
Occupational airborne contamination in South Brazil: 1. Oxidative stress detected in the blood of coal miners.Crossref | GoogleScholarGoogle Scholar | 19618269PubMed |

Bae, YS, Oh, H, Rhee, SG, and Yoo, YD (2011). Regulation of reactive oxygen species generation in cell signaling. Molecules and Cells 32, 491–509.
Regulation of reactive oxygen species generation in cell signaling.Crossref | GoogleScholarGoogle Scholar | 22207195PubMed |

Barratt, CLR, Aitken, RJ, Björndahl, L, Carrell, DT, de Boer, P, Kvist, U, Lewis, SEM, Perreault, SD, Perry, MJ, Ramos, L, Robaire, B, Ward, S, and Zini, A (2010). Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications – a position report. Human Reproduction 25, 824–838.
Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications – a position report.Crossref | GoogleScholarGoogle Scholar |

Behrouzi, S, Mashayekhi, F, and Bahadori, MH (2018). The association of PON1 192 Q/R polymorphism with the risk of idiopathic male infertility in Northern Iran. Avicenna Journal of Medical Biotechnology 10, 253.
| 30555659PubMed |

Benchaib, M, Braun, V, Lornage, J, Hadj, S, Salle, B, Lejeune, H, and Guérin, JF (2003). Sperm DNA fragmentation decreases the pregnancy rate in an assisted reproductive technique. Human Reproduction 18, 1023–1028.
Sperm DNA fragmentation decreases the pregnancy rate in an assisted reproductive technique.Crossref | GoogleScholarGoogle Scholar | 12721180PubMed |

Benzie, IFF, and Strain, JJ (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Analytical Biochemistry 239, 70–76.
The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay.Crossref | GoogleScholarGoogle Scholar |

Bhattacharyya, T, Nicholls, SJ, Topol, EJ, Zhang, R, Yang, X, Schmitt, D, Fu, X, Shao, M, Brennan, DM, and Ellis, SG (2008). Relationship of paraoxonase 1 (PON1) gene polymorphisms and functional activity with systemic oxidative stress and cardiovascular risk. JAMA 299, 1265–1276.
Relationship of paraoxonase 1 (PON1) gene polymorphisms and functional activity with systemic oxidative stress and cardiovascular risk.Crossref | GoogleScholarGoogle Scholar | 18349088PubMed |

Bilodeau, JF, Chatterjee, S, Sirard, MA, and Gagnon, C (2000). Levels of antioxidant defenses are decreased in bovine spermatozoa after a cycle of freezing and thawing. Molecular Reproduction and Development: Incorporating Gamete Research 55, 282–288.
Levels of antioxidant defenses are decreased in bovine spermatozoa after a cycle of freezing and thawing.Crossref | GoogleScholarGoogle Scholar |

Bousnane, NEH, May, S, Yahia, M, and Abu Alhaija, AA (2017). Association of CAT–262C/T with the concentration of catalase in seminal plasma and the risk for male infertility in Algeria. Systems Biology in Reproductive Medicine 63, 303–310.
Association of CAT–262C/T with the concentration of catalase in seminal plasma and the risk for male infertility in Algeria.Crossref | GoogleScholarGoogle Scholar | 28436704PubMed |

Castellazzi, M, Trentini, A, Romani, A, Valacchi, G, Bellini, T, Bonaccorsi, G, Fainardi, E, Cavicchio, C, Passaro, A, Zuliani, G, and Cervellati, C (2016). Decreased arylesterase activity of paraoxonase-1 (PON-1) might be a common denominator of neuroinflammatory and neurodegenerative diseases. The International Journal of Biochemistry & Cell Biology 81, 356–363.
Decreased arylesterase activity of paraoxonase-1 (PON-1) might be a common denominator of neuroinflammatory and neurodegenerative diseases.Crossref | GoogleScholarGoogle Scholar |

Cavalcanti Luna, MA, Rodrigues Vieira, E, Okada, K, Campos-Takaki, GM, and do Nascimento, AE (2015). Copper-induced adaptation, oxidative stress and its tolerance in Aspergillus niger UCP1261. Electronic Journal of Biotechnology 18, 418–427.
Copper-induced adaptation, oxidative stress and its tolerance in Aspergillus niger UCP1261.Crossref | GoogleScholarGoogle Scholar |

Collins, JA, Barnhart, KT, and Schlegel, PN (2008). Do sperm DNA integrity tests predict pregnancy with in vitro fertilization? Fertility and Sterility 89, 823–831.
Do sperm DNA integrity tests predict pregnancy with in vitro fertilization?Crossref | GoogleScholarGoogle Scholar | 17644094PubMed |

Costa, LG, Cole, TB, Jarvik, GP, and Furlong, CE (2003). Functional genomics of the paraoxonase (PON1) polymorphisms: effects on pesticide sensitivity, cardiovascular disease, and drug metabolism. Annual Review of Medicine 54, 371–392.
Functional genomics of the paraoxonase (PON1) polymorphisms: effects on pesticide sensitivity, cardiovascular disease, and drug metabolism.Crossref | GoogleScholarGoogle Scholar | 12525679PubMed |

de Lamirande, E, and O’Flaherty, C (2008). Sperm activation: role of reactive oxygen species and kinases. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics 1784, 106–115.
Sperm activation: role of reactive oxygen species and kinases.Crossref | GoogleScholarGoogle Scholar |

Evenson, DP (2016). The sperm chromatin structure assay (SCSA®) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility. Animal Reproduction Science 169, 56–75.
The sperm chromatin structure assay (SCSA®) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility.Crossref | GoogleScholarGoogle Scholar | 26919909PubMed |

Fanaei, H, Keshtgar, S, Bahmanpour, S, Ghannadi, A, and Kazeroni, M (2011). Beneficial effects of α-tocopherol against intracellular calcium overload in human sperm. Reproductive Sciences 18, 978–982.
Beneficial effects of α-tocopherol against intracellular calcium overload in human sperm.Crossref | GoogleScholarGoogle Scholar | 21478138PubMed |

Faure, C, Leveille, P, Dupont, C, Julia, C, Chavatte-Palmer, P, Group, A, Sutton, A, and Levy, R (2014). Are superoxide dismutase 2 and nitric oxide synthase polymorphisms associated with idiopathic infertility? Antioxidants & Redox Signaling 21, 565–569.
Are superoxide dismutase 2 and nitric oxide synthase polymorphisms associated with idiopathic infertility?Crossref | GoogleScholarGoogle Scholar |

Fujii, J, and Imai, H (2014). Redox reactions in mammalian spermatogenesis and the potential targets of reactive oxygen species under oxidative stress. Spermatogenesis 4, e979108.
Redox reactions in mammalian spermatogenesis and the potential targets of reactive oxygen species under oxidative stress.Crossref | GoogleScholarGoogle Scholar | 26413390PubMed |

Furlong, CE, Costa, LG, Hassett, C, Richter, RJ, Sundstrom, JA, Adler, DA, Disteche, CM, Omiecinski, CJ, Chapline, C, Crabb, JW, and Humbert, R (1993). Human and rabbit paraoxonases: purification, cloning, sequencing, mapping and role of polymorphism in organophosphate detoxification. Chemico-Biological Interactions 87, 35–48.
Human and rabbit paraoxonases: purification, cloning, sequencing, mapping and role of polymorphism in organophosphate detoxification.Crossref | GoogleScholarGoogle Scholar | 8393745PubMed |

García Rodríguez, A, de la Casa, M, Johnston, S, Gosálvez, J, and Roy, R (2019). Association of polymorphisms in genes coding for antioxidant enzymes and human male infertility. Annals of Human Genetics 83, 63–72.
Association of polymorphisms in genes coding for antioxidant enzymes and human male infertility.Crossref | GoogleScholarGoogle Scholar | 30191955PubMed |

Godbole, C, Thaker, S, Kerkar, P, Nadkar, M, Gogtay, N, and Thatte, U (2020). Association of PON1 gene polymorphisms and enzymatic activity with risk of coronary artery disease. Future Cardiology 17, 119–126.
Association of PON1 gene polymorphisms and enzymatic activity with risk of coronary artery disease.Crossref | GoogleScholarGoogle Scholar | 32583675PubMed |

Halliwell, B, and Whiteman, M (2004). Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? British Journal of Pharmacology 142, 231–255.
Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean?Crossref | GoogleScholarGoogle Scholar | 15155533PubMed |

Inhorn, MC, and Patrizio, P (2015). Infertility around the globe: new thinking on gender, reproductive technologies and global movements in the 21st Century. Human Reproduction Update 21, 411–426.
Infertility around the globe: new thinking on gender, reproductive technologies and global movements in the 21st Century.Crossref | GoogleScholarGoogle Scholar | 25801630PubMed |

Ji, G, Gu, A, Wang, Y, Huang, C, Hu, F, Zhou, Y, Song, L, and Wang, X (2012). 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 52, 775–780.
Genetic variants in antioxidant genes are associated with sperm DNA damage and risk of male infertility in a Chinese population.Crossref | GoogleScholarGoogle Scholar | 22206979PubMed |

Kesari, KK, Agarwal, A, and Henkel, R (2018). Radiations and male fertility. Reproductive Biology and Endocrinology 16, 118.
Radiations and male fertility.Crossref | GoogleScholarGoogle Scholar | 30445985PubMed |

Kothari, S, Thompson, A, Agarwal, A, and du Plessis, SS (2010). Free radicals: their beneficial and detrimental effects on sperm function. Indian Journal of Experimental Biology 48, 425–435.
| 20795359PubMed |

Liu, H, Zhao, J, Xu, J, Zhu, P, Yu, M, Jiang, W, Zhang, J, Li, W, Wu, Q, and Li, Z (2018). Correlation of the single nucleotide polymorphism rs662 of PON1 with the risk of male infertility. Zhonghua nan ke xue – National Journal of Andrology 24, 708–712.
| 30173430PubMed |

Luo, Z, Pu, L, Muhammad, I, Chen, Y, and Sun, X (2018). Associations of the PON1 rs662 polymorphism with circulating oxidized low-density lipoprotein and lipid levels: a systematic review and meta-analysis. Lipids in Health and Disease 17, 281.
Associations of the PON1 rs662 polymorphism with circulating oxidized low-density lipoprotein and lipid levels: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 30545386PubMed |

Malakooti, SJ, Tonkaboni, SZS, Noaparast, M, Ardejani, FD, and Naseh, R (2014). Characterisation of the Sarcheshmeh copper mine tailings, Kerman province, southeast of Iran. Environmental Earth Sciences 71, 2267–2291.
Characterisation of the Sarcheshmeh copper mine tailings, Kerman province, southeast of Iran.Crossref | GoogleScholarGoogle Scholar |

Malakootian, M, Jafari Mansourian, H, Mousavi, S, and Danesh Pajooh, M (2013). Performance evaluation of fenton process to remove chromium, cod and turbidity from electroplating industry wastewater. Journal of Water and Wastewater – Ab va Fazilab (in Persian) 24, 2–10.

Masoumi, I, Kamali, G, Asghari, O, and Emery, X (2020). Assessing the impact of geologic contact dilution in ore/waste classification in the Gol-Gohar iron ore mine, southeastern Iran. Minerals 10, 336.
Assessing the impact of geologic contact dilution in ore/waste classification in the Gol-Gohar iron ore mine, southeastern Iran.Crossref | GoogleScholarGoogle Scholar |

Mazjin, MA, Salehi, Z, Mashayekhi, F, and Bahadori, M (2016). Evaluation of GPx1 Pro198Leu polymorphism in idiopathic male infertility. Molecular Biology 50, 77–80.
Evaluation of GPx1 Pro198Leu polymorphism in idiopathic male infertility.Crossref | GoogleScholarGoogle Scholar |

Mousavi, SM, Yaghmaei, S, Vossoughi, M, Jafari, A, and Roostaazad, R (2006). Zinc extraction from Iranian low-grade complex zinc–lead ore by two native microorganisms: Acidithiobacillus ferrooxidans and sulfobacillus. International Journal of Mineral Processing 80, 238–243.
Zinc extraction from Iranian low-grade complex zinc–lead ore by two native microorganisms: Acidithiobacillus ferrooxidans and sulfobacillus.Crossref | GoogleScholarGoogle Scholar |

O’Flaherty, C (2014). The enzymatic antioxidant system of human spermatozoa. Advances in Andrology 2014, 626374.
The enzymatic antioxidant system of human spermatozoa.Crossref | GoogleScholarGoogle Scholar |

Ott, M, Gogvadze, V, Orrenius, S, and Zhivotovsky, B (2007). Mitochondria, oxidative stress and cell death. Apoptosis 12, 913–922.
Mitochondria, oxidative stress and cell death.Crossref | GoogleScholarGoogle Scholar | 17453160PubMed |

Patra, DK, Pradhan, C, and Patra, HK (2019). Chromium bioaccumulation, oxidative stress metabolism and oil content in lemon grass Cymbopogon flexuosus (Nees ex Steud.) W. Watson grown in chromium rich over burden soil of Sukinda chromite mine, India. Chemosphere 218, 1082–1088.
Chromium bioaccumulation, oxidative stress metabolism and oil content in lemon grass Cymbopogon flexuosus (Nees ex Steud.) W. Watson grown in chromium rich over burden soil of Sukinda chromite mine, India.Crossref | GoogleScholarGoogle Scholar | 30609487PubMed |

Rowe PJ, Comhaire FH, Hargreave TB, Mahmoud AM (2000) ‘WHO Manual for the Standardized Investigation and Diagnosis of the Infertile Male.’ (Cambridge University Press: Cambridge, UK)

Ruiz-Sanz, JI, Aurrekoetxea, I, Matorras, R, and Ruiz-Larrea, MB (2011). Ala16Val SOD2 polymorphism is associated with higher pregnancy rates in in vitro fertilization cycles. Fertility and Sterility 95, 1601–1605.
Ala16Val SOD2 polymorphism is associated with higher pregnancy rates in in vitro fertilization cycles.Crossref | GoogleScholarGoogle Scholar | 21130430PubMed |

Schröder P, Krutmann J (2005) Environmental oxidative stress – environmental sources of ROS. In ‘Reactions, Processes’. (Ed. T Grune) pp. 19–31.

Seli, E, Gardner, DK, Schoolcraft, WB, Moffatt, O, and Sakkas, D (2004). Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization. Fertility and Sterility 82, 378–383.
Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 15302287PubMed |

Seydi, E, Soltani, M, Ramazani, M, Zarei, MH, and Pourahmad, J (2020). Occupational exposure in lead and zinc mines induces oxidative stress in miners lymphocytes: role of mitochondrial/lysosomal damage. Main Group Metal Chemistry 43, 154–163.
Occupational exposure in lead and zinc mines induces oxidative stress in miners lymphocytes: role of mitochondrial/lysosomal damage.Crossref | GoogleScholarGoogle Scholar |

Shahabpour, J, Doorandish, M, and Abbasnejad, A (2005). Mine-drainage water from coal mines of Kerman region, Iran. Environmental Geology 47, 915–925.
Mine-drainage water from coal mines of Kerman region, Iran.Crossref | GoogleScholarGoogle Scholar |

Sharma, RK, and Agarwal, A (1996). Role of reactive oxygen species in male infertility. Urology 48, 835–850.
Role of reactive oxygen species in male infertility.Crossref | GoogleScholarGoogle Scholar | 8973665PubMed |

Shimoda-Matsubayashi, S, Matsumine, H, Kobayashi, T, Nakagawa-Hattori, Y, Shimizu, Y, and Mizuno, Y (1996). Structural dimorphism in the mitochondrial targeting sequence in the human manganese superoxide dismutase gene: a predictive evidence for conformational change to influence mitochondrial transport and a study of allelic association in Parkinson’s Disease. Biochemical and Biophysical Research Communications 226, 561–565.
Structural dimorphism in the mitochondrial targeting sequence in the human manganese superoxide dismutase gene: a predictive evidence for conformational change to influence mitochondrial transport and a study of allelic association in Parkinson’s Disease.Crossref | GoogleScholarGoogle Scholar | 8806673PubMed |

Shirinzadeh, H, Eren, B, Gurer-Orhan, H, Suzen, S, and Özden, S (2010). Novel indole-based analogs of melatonin: synthesis and in vitro antioxidant activity studies. Molecules 15, 2187–2202.
Novel indole-based analogs of melatonin: synthesis and in vitro antioxidant activity studies.Crossref | GoogleScholarGoogle Scholar | 20428037PubMed |

Soran, N, Altindag, O, Çakir, H, Çelik, H, Demirkol, A, and Aksoy, N (2008). Assessment of paraoxonase activities in patients with knee osteoarthritis. Redox Report 13, 194–198.
Assessment of paraoxonase activities in patients with knee osteoarthritis.Crossref | GoogleScholarGoogle Scholar | 18796237PubMed |

Sutton, A, Khoury, H, Prip-Buus, C, Cepanec, C, Pessayre, D, and Degoul, F (2003). The Ala16Val genetic dimorphism modulates the import of human manganese superoxide dismutase into rat liver mitochondria. Pharmacogenetics and Genomics 13, 145–157.
The Ala16Val genetic dimorphism modulates the import of human manganese superoxide dismutase into rat liver mitochondria.Crossref | GoogleScholarGoogle Scholar |

Tavilani, H, Fattahi, A, Esfahani, M, Khodadadi, I, Karimi, J, Bahrayni, E, Vatannejad, A, Vaisi-Raygani, A, Ghorbani, M, and Latifi, Z (2014). Genotype and phenotype frequencies of paraoxonase 1 in fertile and infertile men. Systems Biology in Reproductive Medicine 60, 361–366.
Genotype and phenotype frequencies of paraoxonase 1 in fertile and infertile men.Crossref | GoogleScholarGoogle Scholar | 25264968PubMed |

Tefik, T, Kucukgergin, C, Sanli, O, Oktar, T, Seckin, S, and Ozsoy, C (2013). Manganese superoxide dismutase Ile58Thr, catalase C-262T and myeloperoxidase G-463A gene polymorphisms in patients with prostate cancer: relation to advanced and metastatic disease. BJU International 112, E406–E414.
Manganese superoxide dismutase Ile58Thr, catalase C-262T and myeloperoxidase G-463A gene polymorphisms in patients with prostate cancer: relation to advanced and metastatic disease.Crossref | GoogleScholarGoogle Scholar | 23773345PubMed |

Usui, S, Oveson, BC, Iwase, T, Lu, L, Lee, SY, Jo, Y-J, Wu, Z, Choi, E-Y, Samulski, RJ, and Campochiaro, PA (2011). Overexpression of SOD in retina: need for increase in H2O2-detoxifying enzyme in same cellular compartment. Free Radical Biology and Medicine 51, 1347–1354.
Overexpression of SOD in retina: need for increase in H2O2-detoxifying enzyme in same cellular compartment.Crossref | GoogleScholarGoogle Scholar | 21736939PubMed |

Valko, M, Leibfritz, D, Moncol, J, Cronin, MTD, Mazur, M, and Telser, J (2007). Free radicals and antioxidants in normal physiological functions and human disease. The International Journal of Biochemistry & Cell Biology 39, 44–84.
Free radicals and antioxidants in normal physiological functions and human disease.Crossref | GoogleScholarGoogle Scholar |

Veiga, L, Silva-Nunes, J, Melão, A, Oliveira, A, Duarte, L, and Brito, M (2011). Q192R polymorphism of the paraoxonase-1 gene as a risk factor for obesity in Portuguese women. European Journal of Endocrinology 164, 213–218.
Q192R polymorphism of the paraoxonase-1 gene as a risk factor for obesity in Portuguese women.Crossref | GoogleScholarGoogle Scholar | 21078685PubMed |

Volk, M, Jaklič, H, Zorn, B, and Peterlin, B (2011). Association between male infertility and genetic variability at the PON1/2 and GSTM1/T1 gene loci. Reproductive BioMedicine Online 23, 105–110.
Association between male infertility and genetic variability at the PON1/2 and GSTM1/T1 gene loci.Crossref | GoogleScholarGoogle Scholar | 21561808PubMed |

Wu, JQ, Kosten, TR, and Zhang, XY (2013). Free radicals, antioxidant defense systems, and schizophrenia. Progress in Neuro-Psychopharmacology and Biological Psychiatry 46, 200–206.
Free radicals, antioxidant defense systems, and schizophrenia.Crossref | GoogleScholarGoogle Scholar | 23470289PubMed |

Yin, Y, Zhu, P, Luo, T, and Xia, X (2020). Association of single-nucleotide polymorphisms in antioxidant genes and their gene–gene interactions with risk of male infertility in a Chinese population. Biomedical Reports 13, 49–54.
Association of single-nucleotide polymorphisms in antioxidant genes and their gene–gene interactions with risk of male infertility in a Chinese population.Crossref | GoogleScholarGoogle Scholar | 32494361PubMed |

Zhu, P-R, Wu, Q-Y, Yu, M-M, Zhang, M-C, Ni, M-X, Liu, S-M, Jiang, W-J, Zhang, J, Li, W-W, and Cao, J (2017). Nucleotide polymorphism rs4880 of the SOD2 gene and the risk of male infertility. Zhonghua nan ke xue – National Journal of Andrology 23, 137–141.
| 29658251PubMed |

Zini, A, Boman, JM, Belzile, E, and Ciampi, A (2008). Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Human Reproduction 23, 2663–2668.
Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 18757447PubMed |