Seminal plasma has limited counteracting effects following induction of oxidative stress in donkey spermatozoa
Marion Papas A , Jaime Catalan A , Sebastián Bonilla-Correal A , Sabrina Gacem A , Jordi Miró A C * and Marc Yeste
B C *
+ Author Affiliations
- Author Affiliations
A Equine Reproduction Service, Department of Animal Medicine and Surgery, Faculty of Veterinary Sciences, Autonomous University of Barcelona, E-08197 Bellaterra (Cerdanyola del Vallès), Barcelona, Spain.
B Biotechnology of Animal and Human Reproduction (TechnoSperm), Unit of Cell Biology, Department of Biology, Institute of Food and Agricultural Technology, Faculty of Sciences, University of Girona, E-17003 Girona, Spain.
C Corresponding authors. Email: marc.yeste@udg.edu; jordi.miro@uab.cat
Reproduction, Fertility and Development 32(6) 619-628 https://doi.org/10.1071/RD19192
Submitted: 23 May 2019 Accepted: 17 October 2019 Published: 22 January 2020
Abstract
The aim of this study was to evaluate the response of donkey spermatozoa to oxidative stress induced by hydrogen peroxide, and to determine whether the presence of seminal plasma modulates the sperm response to that stress. Nine ejaculates were collected, extended in skim milk extender and split into two aliquots. Seminal plasma was removed from the first but not second aliquot. Samples were subsequently split into four aliquots supplemented with different concentrations of commercial hydrogen peroxide (0, 100 and 250 µM and 50 mM). Aliquots were incubated at 37°C under aerobic conditions and several sperm parameters, namely motility, viability, intracellular levels of peroxides and superoxides and mitochondrial membrane potential, were evaluated at 0, 1 and 3 h. Exposure to hydrogen peroxide markedly decreased sperm motility but had much less of an effect on sperm viability, mitochondrial membrane potential and intracellular reactive oxygen species levels. A protective effect of seminal plasma against the loss of sperm motility was not apparent, but some kinetic parameters and relative levels of superoxides were better maintained when seminal plasma was present together with high concentration of hydrogen peroxide. In conclusion, oxidative stress induced by hydrogen peroxide reduces donkey sperm motility and has a less apparent effect on other sperm parameters. Finally, seminal plasma is only able to partially ameliorate the detrimental effect of this induced stress.
Additional keywords: catalase, glutathione peroxidase, hydrogen peroxide, reactive oxygen species, superoxide dismutase.
References
Aitken, R. J. (2017). Reactive oxygen species as mediators of sperm capacitation and pathological damage. Mol. Reprod. Dev. 84, 1039–1052.| Reactive oxygen species as mediators of sperm capacitation and pathological damage.Crossref | GoogleScholarGoogle Scholar | 28749007PubMed |
Aitken, R. J., Buckingham, D., and Harkiss, D. (1993). Use of a xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. J. Reprod. Fertil. 97, 441–450.
| Use of a xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa.Crossref | GoogleScholarGoogle Scholar | 8388958PubMed |
Aitken, R. J., De Iuliis, G. N., and Drevet, J. R. (2019). Role of oxidative stress in the etiology of male infertility and the potential therapeutic value of antioxidants. In ‘Oxidants, Antioxidants and Impact of the Oxidative Status in Male Reproduction’. (Eds R. Henkel, L. Samanta, and A. Agarwal.) pp. 91–100. (Elsevier.)
Alvarez, J. G., and Storey, B. T. (1989). Role of glutathione peroxidase in protecting mammalian spermatozoa from loss of motility caused by spontaneous lipid peroxidation. Gamete Res. 23, 77–90.
| Role of glutathione peroxidase in protecting mammalian spermatozoa from loss of motility caused by spontaneous lipid peroxidation.Crossref | GoogleScholarGoogle Scholar | 2545584PubMed |
Armstrong, J. S., Rajasekaran, M., Chamulitra, W., Gatti, P., Hellstrom, W., and Sikka, S. C. (1999). Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism. Free Radic. Biol. Med. 26, 869–880.
| Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism.Crossref | GoogleScholarGoogle Scholar | 10232830PubMed |
Baiardi, G., Ruiz, R. D., Fiol de Cuneo, M., Ponce, A. A., Lacuara, J. L., and Vincent, L. (1997). Differential effects of pharmacologically generated reactive oxygen species upon functional activity of epididymal mouse spermatozoa. Can. J. Physiol. Pharmacol. 75, 173–178.
| Differential effects of pharmacologically generated reactive oxygen species upon functional activity of epididymal mouse spermatozoa.Crossref | GoogleScholarGoogle Scholar | 9164698PubMed |
Ball, B. A. (2008). Oxidative stress, osmotic stress and apoptosis: Impacts on sperm function and preservation in the horse. Anim. Reprod. Sci. 107, 257–267.
| Oxidative stress, osmotic stress and apoptosis: Impacts on sperm function and preservation in the horse.Crossref | GoogleScholarGoogle Scholar | 18524506PubMed |
Ball, B. A., Gravance, C. G., Medina, V., Baumber, J., and Liu, I. K. M. (2000). Catalase activity in equine semen. Am. J. Vet. Res. 61, 1026–1030.
| Catalase activity in equine semen.Crossref | GoogleScholarGoogle Scholar | 10976731PubMed |
Ball, B. A., Vo, A. T., and Baumber, J. (2001). Generation of reactive oxygen species by equine spermatozoa. Am. J. Vet. Res. 62, 508–515.
| Generation of reactive oxygen species by equine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 11327456PubMed |
Baumber, J., and Ball, B. A. (2005). Determination of glutathione peroxidase and superoxide dismutase-like activities in equine spermatozoa, seminal plasma, and reproductive tissue. Am. J. Vet. Res. 66, 1415–1419.
| Determination of glutathione peroxidase and superoxide dismutase-like activities in equine spermatozoa, seminal plasma, and reproductive tissue.Crossref | GoogleScholarGoogle Scholar | 16173486PubMed |
Baumber, J., Ball, B. A., Gravance, C. G., Medina, V., and Davies-Morel, M. C. G. (2000). The effect of reactive oxygen species on equine sperm motility, viability, acrosomal integrity, mitochondrial membrane potential, and membrane lipid peroxidation. J. Androl. 21, 895–902.
| 11105916PubMed |
Baumber, J., Vo, A. T., Sabeur, K., and Ball, B. A. (2002). Generation of reactive oxygen species by equine neutrophils and their effect on motility of equine spermatozoa. Theriogenology 57, 1025–1033.
| Generation of reactive oxygen species by equine neutrophils and their effect on motility of equine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 12041897PubMed |
Bilodeau, J. F., Blanchette, S., Cormier, N., and Sirard, M. A. (2002). Reactive oxygen species-mediated loss of bovine sperm motility in egg yolk Tris extender: protection by pyruvate, metal chelators and bovine liver or oviductal fluid catalase. Theriogenology 57, 1105–1122.
| Reactive oxygen species-mediated loss of bovine sperm motility in egg yolk Tris extender: protection by pyruvate, metal chelators and bovine liver or oviductal fluid catalase.Crossref | GoogleScholarGoogle Scholar | 12041904PubMed |
de Lamirande, E., and Gagnon, C. (1992). Reactive oxygen species and human spermatozoa I. Effects on the motility of intact spermatozoa and on sperm axonemes. J. Androl. 13, 368–378.
| 1331006PubMed |
Garg, A., Kumaresan, A., and Ansari, M. R. (2009). Effects of hydrogen peroxide (H2O2) on fresh and cryopreserved buffalo sperm functions during incubation at 37°C in vitro. Reprod. Domest. Anim. 44, 907–912.
| Effects of hydrogen peroxide (H2O2) on fresh and cryopreserved buffalo sperm functions during incubation at 37°C in vitro.Crossref | GoogleScholarGoogle Scholar | 18992123PubMed |
Garner, D. L., and Johnson, L. A. (1995). Viability assessment of mammalian sperm using SYBR-14 and propidium iodide. Biol. Reprod. 53, 276–284.
| Viability assessment of mammalian sperm using SYBR-14 and propidium iodide.Crossref | GoogleScholarGoogle Scholar | 7492679PubMed |
Gavriliouk, D., and Aitken, R. J. (2015). Damage to sperm DNA mediated by reactive oxygen species: its impact on human reproduction and the health trajectory of offspring. In ‘The Male Role in Pregnancy Loss and Embryo Implantation Failure’. (Ed. R. Bronson.) pp. 23–47. (Springer International Publishing: Basel, Switzerland)
Guthrie, H. D., and Welch, G. R. (2006). Determination of intracellular reactive oxygen species and high mitochondrial membrane potential in Percoll-treated viable boar sperm using fluorescence-activated flow cytometry. J. Anim. Sci. 84, 2089–2100.
| Determination of intracellular reactive oxygen species and high mitochondrial membrane potential in Percoll-treated viable boar sperm using fluorescence-activated flow cytometry.Crossref | GoogleScholarGoogle Scholar | 16864869PubMed |
Guthrie, H. D., and Welch, G. R. (2012). Effects of reactive oxygen species on sperm function. Theriogenology 78, 1700–1708.
| Effects of reactive oxygen species on sperm function.Crossref | GoogleScholarGoogle Scholar | 22704396PubMed |
Kawai, G. K. V., Gurgel, J. R. C., Losano, J. D. A., Dalmazzo, A., Rocha, C. C., Tsunoda, R. H., de Araújo Góes, P. A., Rui, B. R., Angrimani, D. S. R., Assumpçao, M. E. O. A., Mendes, C. M., Barnabe, V. H., and Nichi, M. (2017). Susceptibility of stallion spermatozoa to different oxidative challenges: role of seminal plasma. J. Equine Vet. Sci. 55, 76–83.
| Susceptibility of stallion spermatozoa to different oxidative challenges: role of seminal plasma.Crossref | GoogleScholarGoogle Scholar |
Maehly, A. C., and Chance, B. (1954). The assay of catalases and peroxidases. Methods Biochem. Anal. 1, 357–424.
| 13193536PubMed |
Maia, M. S., Bicudo, S. D., and Rodello, L. (2014). Effect of hydrogen peroxide on thawed ovine sperm motility. Anim. Reprod. 11, 119–123.
Miró, J., Taberner, E., Rivera, M., Peña, A., Medrano, A., Rigau, T., and Peñalba, A. (2009). Effect of dilution and centrifugation on the survival of spermatozoa and the structure of motile sperm cell subpopulations in refrigerated Catalonian donkey semen. Theriogenology 72, 1017–1022.
| Effect of dilution and centrifugation on the survival of spermatozoa and the structure of motile sperm cell subpopulations in refrigerated Catalonian donkey semen.Crossref | GoogleScholarGoogle Scholar | 19747718PubMed |
Misro, M. M., Choudhury, L., Upreti, K., Gautam, D., Chaki, S. P., Mahajan, A. S., and Babbar, R. (2004). Use of hydrogen peroxide to assess the sperm susceptibility to oxidative stress in subjects presenting a normal semen profile. Int. J. Androl. 27, 82–87.
| Use of hydrogen peroxide to assess the sperm susceptibility to oxidative stress in subjects presenting a normal semen profile.Crossref | GoogleScholarGoogle Scholar | 15149465PubMed |
Morrell, J. M., Winblad, C., Georgakas, A., Stuhtmann, G., Humblot, P., and Johannisson, A. (2013). Reactive oxygen species in stallion semen can be affected by season and colloid centrifugation. Anim. Reprod. Sci. 140, 62–69.
| Reactive oxygen species in stallion semen can be affected by season and colloid centrifugation.Crossref | GoogleScholarGoogle Scholar | 23778304PubMed |
Muiño-Blanco, T., Pérez-Pé, R., and Cebrián-Pérez, J. A. (2008). Seminal plasma proteins and sperm resistance to stress. Reprod. Domest. Anim. 43, 18–31.
| Seminal plasma proteins and sperm resistance to stress.Crossref | GoogleScholarGoogle Scholar | 18803753PubMed |
Papas, M., Arroyo, L., Bassols, A., Catalán, J., Bonilla-Correal, S., Gacem, S., Yeste, M., and Miró, J. (2019). Activities of antioxidant seminal plasma enzymes (SOD, CAT, GPX and GSR) are higher in jackasses than in stallions and are correlated with sperm motility in jackasses. Theriogenology 140, 180–187.
| Activities of antioxidant seminal plasma enzymes (SOD, CAT, GPX and GSR) are higher in jackasses than in stallions and are correlated with sperm motility in jackasses.Crossref | GoogleScholarGoogle Scholar | 31479834PubMed |
Sharma, A. (2015). Investigation on the effects of exogenous H2O2 on sperm motility, LPO, catalase and SOD levels in seminal plasma. Health Sci. J. 10, 1–5.
Shi, T. Y., Chen, G., Huang, X., Yuan, Y., Wu, X., Wu, B., Li, Z., Shun, F., Chen, H., and Shi, H. (2012). Effects of reactive oxygen species from activated leucocytes on human sperm motility, viability and morphology. Andrologia 44, 696–703.
| Effects of reactive oxygen species from activated leucocytes on human sperm motility, viability and morphology.Crossref | GoogleScholarGoogle Scholar | 22097888PubMed |
Vilés, K., Rabanal, R., Rodríguez-Prado, M., and Miró, J. (2013). Influence of seminal plasma on leucocyte migration and amount of COX-2 protein in the jenny endometrium after insemination with frozen–thawed semen. Anim. Reprod. Sci. 143, 57–63.
| Influence of seminal plasma on leucocyte migration and amount of COX-2 protein in the jenny endometrium after insemination with frozen–thawed semen.Crossref | GoogleScholarGoogle Scholar | 24280633PubMed |
Woodward, E. M., and Troedsson, M. H. T. (2015). Inflammatory mechanisms of endometritis. Equine Vet. J. 47, 384–389.
| Inflammatory mechanisms of endometritis.Crossref | GoogleScholarGoogle Scholar | 25537084PubMed |
Zini, A., de Lamirande, E., and Gagnon, C. (1993). Reactive oxygen species in semen of infertile patients: levels of superoxide dismutase- and catalase-like activities in seminal plasma and spermatozoa. Int. J. Androl. 16, 183–188.
| Reactive oxygen species in semen of infertile patients: levels of superoxide dismutase- and catalase-like activities in seminal plasma and spermatozoa.Crossref | GoogleScholarGoogle Scholar | 8359932PubMed |
