The Protective Effects of Antioxidants Against Endogenous and Exogenous Oxidative Stress on Bull Sperm

Overview

Journal In Vitro Cell Dev Biol Anim

Publisher Springer

Specialties Biology
Cell Biology

Date 2024 Jul 30

PMID 39080183

Authors

Ali Md Younus

Takahiro Yamanaka

Masayuki Shimada

Affiliations

Soon will be listed here.

Abstract

Oxidative stress, caused by both endogenous and exogenous factors, affects sperm function by damaging morphology and reducing metabolic activity, leading to reduced fertilization ability. The purpose of this study was to investigate the effects of oxidative stress on bull sperm and to evaluate the efficacy of targeted antioxidants in mitigating these detrimental effects. Fresh bull semen samples were subjected to hydrogen peroxide (HO) and antimycin treatments to induce oxidative stress, and the antioxidants PQQ, ergothioneine, and vitamin C were applied to counteract the induced stress. Sperm motility, viability, and reactive oxygen species (ROS) levels in the cytoplasm and mitochondria of sperm were assessed using computer-assisted sperm analysis (CASA) and flow cytometry. The treatment with HO rapidly decreased sperm viability, and antimycin-induced mitochondrial ROS mainly decreased sperm motility; PQQ and vitamin C effectively reduced mitochondrial ROS, while ergothioneine and vitamin C reduced cytosolic ROS. In frozen-thawed sperm, oxidative stress was elevated in both cytoplasm and mitochondria, and all three antioxidants improved sperm motility by inhibiting ROS production. Furthermore, the localization of oxidized lipids (4-hydroxynonenal) in sperm was detected using immunofluorescence, indicating that oxidative stress affects the head and midpiece of sperm. These findings highlight the potential of targeted antioxidants to mitigate the detrimental effects of oxidative stress on bull sperm and provide valuable insights to improve semen quality and optimize the use of antioxidants in artificial insemination.

References

Agarwal A, Sekhon L . The role of antioxidant therapy in the treatment of male infertility. Hum Fertil (Camb). 2010; 13(4):217-25. DOI: 10.3109/14647273.2010.532279. View

Lewis S, Aitken R . DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res. 2005; 322(1):33-41. DOI: 10.1007/s00441-005-1097-5. View

Hu J, Tian W, Zhao X, Zan L, Wang H, Li Q . The cryoprotective effects of ascorbic acid supplementation on bovine semen quality. Anim Reprod Sci. 2010; 121(1-2):72-7. DOI: 10.1016/j.anireprosci.2010.04.180. View

Panner Selvam M, Agarwal A, Henkel R, Finelli R, Robert K, Iovine C . The effect of oxidative and reductive stress on semen parameters and functions of physiologically normal human spermatozoa. Free Radic Biol Med. 2020; 152:375-385. DOI: 10.1016/j.freeradbiomed.2020.03.008. View

Fayyaz M, Ahmad M, Ahmad N . Survival of buffalo bull spermatozoa: effect on structure and function due to alpha-lipoic acid and cholesterol-loaded cyclodextrin. Andrologia. 2016; 49(4). DOI: 10.1111/and.12652. View

Islam M, Umehara T, Tsujita N, Koyago M, Shimada M . Treatment with cholesterol just after thawing maintains the fertility of bull sperm. Mol Hum Reprod. 2023; 29(9). PMC: 10502238. DOI: 10.1093/molehr/gaad031. View

Aitken R, Gordon E, Harkiss D, Twigg J, Milne P, Jennings Z . Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod. 1998; 59(5):1037-46. DOI: 10.1095/biolreprod59.5.1037. View

Nagy S, Hallap T, Johannisson A, Rodriguez-Martinez H . Changes in plasma membrane and acrosome integrity of frozen-thawed bovine spermatozoa during a 4 h incubation as measured by multicolor flow cytometry. Anim Reprod Sci. 2004; 80(3-4):225-35. DOI: 10.1016/j.anireprosci.2003.08.003. View

Zhu B, Simonis U, Cecchini G, Zhou H, Li L, Teerlink J . Comparison of pyrroloquinoline quinone and/or metoprolol on myocardial infarct size and mitochondrial damage in a rat model of ischemia/reperfusion injury. J Cardiovasc Pharmacol Ther. 2006; 11(2):119-28. DOI: 10.1177/1074248406288757. View

10.

Pini T, Leahy T, de Graaf S . Sublethal sperm freezing damage: Manifestations and solutions. Theriogenology. 2018; 118:172-181. DOI: 10.1016/j.theriogenology.2018.06.006. View

11.

Chatterjee S, Gagnon C . Production of reactive oxygen species by spermatozoa undergoing cooling, freezing, and thawing. Mol Reprod Dev. 2001; 59(4):451-8. DOI: 10.1002/mrd.1052. View

12.

Ansari M, Rakha B, Andrabi S, Ullah N, Iqbal R, Holt W . Glutathione-supplemented tris-citric acid extender improves the post-thaw quality and in vivo fertility of buffalo (Bubalus bubalis) bull spermatozoa. Reprod Biol. 2012; 12(3):271-6. DOI: 10.1016/j.repbio.2012.10.001. View

13.

Khalil W, El-Harairy M, Zeidan A, Hassan M, Mohey-Elsaeed O . Evaluation of bull spermatozoa during and after cryopreservation: Structural and ultrastructural insights. Int J Vet Sci Med. 2019; 6(Suppl):S49-S56. PMC: 6161860. DOI: 10.1016/j.ijvsm.2017.11.001. View

14.

Ioannidou P, Papanikolaou D, Bosdou J, Goulis D, Lambropoulos A, Grimbizis G . Improvement in sperm quality by oral antioxidant supplementation in infertile men with varicocele who have not undergone surgical repair: Systematic review and meta-analysis. Andrologia. 2022; 54(10):e14533. DOI: 10.1111/and.14533. View

15.

Aitken R, Baker M . Oxidative stress, sperm survival and fertility control. Mol Cell Endocrinol. 2006; 250(1-2):66-9. DOI: 10.1016/j.mce.2005.12.026. View

16.

Zhu Z, Kawai T, Umehara T, Hoque S, Zeng W, Shimada M . Negative effects of ROS generated during linear sperm motility on gene expression and ATP generation in boar sperm mitochondria. Free Radic Biol Med. 2019; 141:159-171. DOI: 10.1016/j.freeradbiomed.2019.06.018. View

17.

John Morris G, Acton E, Murray B, Fonseca F . Freezing injury: the special case of the sperm cell. Cryobiology. 2011; 64(2):71-80. DOI: 10.1016/j.cryobiol.2011.12.002. View

18.

Agarwal A, Said T . Oxidative stress, DNA damage and apoptosis in male infertility: a clinical approach. BJU Int. 2005; 95(4):503-7. DOI: 10.1111/j.1464-410X.2005.05328.x. View

19.

Arjun V, Kumar P, Dutt R, Kumar A, Bala R, Verma N . Effect of mitochondria-targeted antioxidant on the regulation of the mitochondrial function of sperm during cryopreservation. Andrologia. 2022; 54(7):e14431. DOI: 10.1111/and.14431. View

20.

Lewis S, Sterling E, Young I, Thompson W . Comparison of individual antioxidants of sperm and seminal plasma in fertile and infertile men. Fertil Steril. 1997; 67(1):142-7. DOI: 10.1016/s0015-0282(97)81871-7. View