DOI QR코드

DOI QR Code

Nitric oxide, 8-hydroxydeoxyguanosine, and total antioxidant capacity in human seminal plasma of infertile men and their relationship with sperm parameters

  • Gholinezhad, Maryam (Infertility and Reproductive Health Research Center, Health Research Institute, Babol University of Medical Sciences) ;
  • Aliarab, Azadeh (Department of Clinical Biochemistry, School of Medicine, Shahid Beheshti University of Medical Sciences) ;
  • Abbaszadeh-Goudarzi, Ghasem (Department of Medical Biotechnology, School of Medicine, Shahroud University of Medical Sciences) ;
  • Yousefnia-Pasha, Yousefreza (Infertility and Reproductive Health Research Center, Health Research Institute, Babol University of Medical Sciences) ;
  • Samadaian, Niusha (Department of Medical Genetics, School of Medicine, Tehran University of Medical Sciences) ;
  • Rasolpour-Roshan, Korush (Cellular and Molecular Biology Research Center, Babol University of Medical Sciences) ;
  • Aghagolzadeh-Haji, Hemat (Cellular and Molecular Biology Research Center, Babol University of Medical Sciences) ;
  • Mohammadoo-Khorasani, Milad (Department of Clinical Biochemistry, Faculty of Medicine, Gonabad University of Medical Sciences)
  • Received : 2019.07.12
  • Accepted : 2019.09.23
  • Published : 2020.03.31

Abstract

Objective: Oxidative stress plays a key role in the pathogenesis of male infertility. But, the adverse effects of oxidative biomarkers on sperm quality remain unclear. This study aimed to investigate the levels of nitric oxide (NO), 8-hydroxydesoxyguanosine (8-OHdG), and total antioxidant capacity (TAC) oxidative biomarkers in seminal plasma and their relationship with sperm parameters. Methods: A total of 77 volunteers participated in the study, including fertile (n = 40) and infertile men (n = 37). NO, 8-OHdG, and TAC levels were measured using the ferric reducing ability of plasma, Griess reagent method and an enzyme-linked immunosorbent assay kit, respectively. Results: The mean values of sperm parameters in the infertile group were significantly lower than those in the fertile group (p< 0.001). The mean 8-OHdG in the seminal plasma of infertile men was significantly higher (p= 0.013) than those of controls, while the mean TAC was significantly lower (p= 0.046). There was no significant difference in NO level between the two groups. The elevated seminal 8-OHdG levels were negatively correlated with semen volume, total sperm counts and morphology (p< 0.001, p= 0.001 and p= 0.052, respectively). NO levels were negatively correlated with semen volume, total sperm counts and morphology (p= 0.014, p= 0.020 and p= 0.060, respectively). Positive correlations between TAC and both sperm count and morphology (p= 0.043 and p= 0.025, respectively) were also found. Conclusion: These results suggested that increased levels of NO and 8-OHdG in seminal plasma could have a negative effect on sperm function by inducing damage to the sperm DNA hence their fertility potentials. Therefore, these biomarkers can be useful in the diagnosis and treatment of male infertility.

Keywords

References

  1. Agarwal A, Virk G, Ong C, du Plessis SS. Effect of oxidative stress on male reproduction. World J Mens Health 2014;32:1-17. https://doi.org/10.5534/wjmh.2014.32.1.1
  2. Bansal AK, Bilaspuri GS. Impacts of oxidative stress and antioxidants on semen functions. Vet Med Int 2010;2010:686137.
  3. Layali I, Tahmasbpour E, Joulaei M, Jorsaraei SG, Farzanegi P. Total antioxidant capacity and lipid peroxidation in semen of patient with hyperviscosity. Cell J 2015;16:554-9.
  4. Saleh RA, Agarwal A. Oxidative stress and male infertility: from research bench to clinical practice. J Androl 2002;23:737-52.
  5. Jeng HA, Pan CH, Chao MR, Lin WY. Sperm DNA oxidative damage and DNA adducts. Mutat Res Genet Toxicol Environ Mutagen 2015;794:75-82. https://doi.org/10.1016/j.mrgentox.2015.09.002
  6. Buzadzic B, Vucetic M, Jankovic A, Stancic A, Korac A, Korac B, et al. New insights into male (in)fertility: the importance of NO. Br J Pharmacol 2015;172:1455-67. https://doi.org/10.1111/bph.12675
  7. Balercia G, Moretti S, Vignini A, Magagnini M, Mantero F, Boscaro M, et al. Role of nitric oxide concentrations on human sperm motility. J Androl 2004;25:245-9. https://doi.org/10.1002/j.1939-4640.2004.tb02784.x
  8. Uribe P, Boguen R, Treulen F, Sanchez R, Villegas JV. Peroxynitritemediated nitrosative stress decreases motility and mitochondrial membrane potential in human spermatozoa. Mol Hum Reprod 2015;21:237-43. https://doi.org/10.1093/molehr/gau107
  9. Du Plessis SS, McAllister DA, Luu A, Savia J, Agarwal A, Lampiao F. Effects of H(2)O(2) exposure on human sperm motility parameters, reactive oxygen species levels and nitric oxide levels. Andrologia 2010;42:206-10. https://doi.org/10.1111/j.1439-0272.2009.00980.x
  10. Belen Herrero M, Chatterjee S, Lefievre L, de Lamirande E, Gagnon C. Nitric oxide interacts with the cAMP pathway to modulate capacitation of human spermatozoa. Free Radic Biol Med 2000;29:522-36. https://doi.org/10.1016/S0891-5849(00)00339-7
  11. Badade G, More K, Narshetty G, Badade VZ, Yadav BK. Human seminal oxidative stress: correlation with antioxidants and sperm quality parameters. Ann Biol Res 2011;2:351-9.
  12. Bianco B, Ghirelli-Filho M, Cavalheiro CM, Cavalcanti V, Peluso C, Gava MM, et al. Variants in endothelial nitric oxide synthase (eNOS) gene in idiopathic infertile Brazilian men. Gene 2013;519:13-7. https://doi.org/10.1016/j.gene.2013.02.001
  13. Song P, Zou S, Chen T, Chen J, Wang Y, Yang J, et al. Endothelial nitric oxide synthase (eNOS) T-786C, 4a4b, and G894T polymorphisms and male infertility: study for idiopathic asthenozoospermia and meta-analysis. Biol Reprod 2015;92:38. https://doi.org/10.1095/biolreprod.114.123240
  14. Khosravi F, Valojerdi MR, Amanlou M, Karimian L, Abolhassani F. Relationship of seminal reactive nitrogen and oxygen species and total antioxidant capacity with sperm DNA fragmentation in infertile couples with normal and abnormal sperm parameters. Andrologia 2014;46:17-23. https://doi.org/10.1111/and.12034
  15. Cambi M, Tamburrino L, Marchiani S, Olivito B, Azzari C, Forti G, et al. Development of a specific method to evaluate 8-hydroxy, 2-deoxyguanosine in sperm nuclei: relationship with semen quality in a cohort of 94 subjects. Reproduction 2013;145:227-35. https://doi.org/10.1530/REP-12-0404
  16. World Health Organization. Laboratory manual of the WHO for the examination of human semen and sperm-cervical mucus interaction. Ann Ist Super Sanita 2001;37:I-XII,1-123.
  17. Kruger TF, Menkveld R, Stander FS, Lombard CJ, Van der Merwe JP, van Zyl JA, et al. Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil Steril 1986;46:1118-23. https://doi.org/10.1016/S0015-0282(16)49891-2
  18. Yousefniapasha Y, Jorsaraei G, Gholinezhadchari M, Mahjoub S, Hajiahmadi M, Farsi M. Nitric oxide levels and total antioxidant capacity in the seminal plasma of infertile smoking men. Cell J 2015;17:129-36.
  19. Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Anal Biochem 1996;239:70-6. https://doi.org/10.1006/abio.1996.0292
  20. Amiri I, Sheikh N, Najafi R. Nitric oxide level in seminal plasma and its relation with sperm DNA damages. Iran Biomed J 2007;11:259-64.
  21. Aksoy Y, Ozbey I, Aksoy H, Polat O, Akcay F. Seminal plasma nitric oxide concentration in oligo- and/or asthenozoospermic subjects with/without varicocele. Arch Androl 2002;48:181-5. https://doi.org/10.1080/01485010252869261
  22. Huang I, Jones J, Khorram O. Human seminal plasma nitric oxide: correlation with sperm morphology and testosterone. Med Sci Monit 2006;12:CR103-6.
  23. Revelli A, Bergandi L, Massobrio M, Lindblom B, Bosia A, Ghigo D. The concentration of nitrite in seminal plasma does not correlate with sperm concentration, sperm motility, leukocytospermia, or sperm culture. Fertil Steril 2001;76:496-500. https://doi.org/10.1016/S0015-0282(01)01958-6
  24. Herrero MB, de Lamirande E, Gagnon C. Tyrosine nitration in human spermatozoa: a physiological function of peroxynitrite, the reaction product of nitric oxide and superoxide. Mol Hum Reprod 2001;7:913-21. https://doi.org/10.1093/molehr/7.10.913
  25. Hibbs JB Jr, Vavrin Z, Taintor RR. L-arginine is required for expression of the activated macrophage effector mechanism causing selective metabolic inhibition in target cells. J Immunol 1987;138:550-65.
  26. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007;87:315-424. https://doi.org/10.1152/physrev.00029.2006
  27. Sheikh N, Amiri I, Najafi R, Goodarzi MT. The correlation between total antioxidant capacity and nitric oxide concentration in seminal plasma with sperm DNA damage. Afr J Biotechnol 2010;9:5739-45.
  28. Hosen MB, Islam MR, Begum F, Kabir Y, Howlader MZ. Oxidative stress induced sperm DNA damage, a possible reason for male infertility. Iran J Reprod Med 2015;13:525-32.
  29. Guz J, Gackowski D, Foksinski M, Rozalski R, Zarakowska E, Siomek A, et al. Comparison of oxidative stress/DNA damage in semen and blood of fertile and infertile men. PLoS One 2013;8:e68490. https://doi.org/10.1371/journal.pone.0068490
  30. Kao SH, Chao HT, Chen HW, Hwang TI, Liao TL, Wei YH. Increase of oxidative stress in human sperm with lower motility. Fertil Steril 2008;89:1183-90. https://doi.org/10.1016/j.fertnstert.2007.05.029
  31. Aitken RJ, Koppers AJ. Apoptosis and DNA damage in human spermatozoa. Asian J Androl 2011;13:36-42. https://doi.org/10.1038/aja.2010.68
  32. Mishra S, Kranthi V, Kumar R, Malhotra N, Mohanty K, Pathak V, et al. Oxidative damage to sperm DNA: clinical implications. Andrology 2014;3:10000116.
  33. Fazeli F, Salimi S. Correlation of seminal plasma total antioxidant capacity and malondialdehyde levels with sperm parameters in men with idiopathic infertility. Avicenna J Med Biochem 2016;4:e29736.
  34. Roychoudhury S, Sharma R, Sikka S, Agarwal A. Diagnostic application of total antioxidant capacity in seminal plasma to assess oxidative stress in male factor infertility. J Assist Reprod Genet 2016;33:627-35. https://doi.org/10.1007/s10815-016-0677-5
  35. Amiri I, Karimi J, Piri H, Goodarzi MT, Tavilani H, Khodadadi I, et al. Association between nitric oxide and 8-hydroxydeoxyguanosine levels in semen of diabetic men. Syst Biol Reprod Med 2011;57:292-5. https://doi.org/10.3109/19396368.2011.621508
  36. Agarwal A, Majzoub A. Role of antioxidants in assisted reproductive techniques. World J Mens Health 2017;35:77-93. https://doi.org/10.5534/wjmh.2017.35.2.77

Cited by

  1. Current mechanistic perspectives on male reproductive toxicity induced by heavy metals vol.38, pp.3, 2020, https://doi.org/10.1080/26896583.2020.1782116
  2. Effects of hazelnut supplemented diet on doxorubicin‐induced damage of reproductive system in male rats vol.45, pp.11, 2020, https://doi.org/10.1111/jfbc.13973