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Resveratrol protects boar sperm in vitro via its antioxidant capacity

Published online by Cambridge University Press:  02 June 2020

Linlin Sun ,
Xiaoteng Fan ,
Yao Zeng ,
Liqian Wang ,
Zhendong Zhu ,
Rongnan Li ,
Xiue Tian ,
Yongjun Wang ,
Yan Lin  and
De Wu
...Show all authors
Linlin Sun
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, China
Xiaoteng Fan
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, China
Yao Zeng
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, China
Liqian Wang
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, China
Zhendong Zhu
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, China
Rongnan Li
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, China
Xiue Tian
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, China
Yongjun Wang
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, China
Yan Lin
Affiliation:
Key Laboratory for Animal Disease Resistance Nutrition of the Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Ya’an, China
De Wu
Affiliation:
Key Laboratory for Animal Disease Resistance Nutrition of the Ministry of Education of China, Institute of Animal Nutrition, Sichuan Agricultural University, Ya’an, China
Wenxian Zeng*
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, China
*
Author for correspondence: Wenxian Zeng. College of Animal Science and Technology, Northwest A&F University, Yangling, China. E-mail: zengwenxian2015@126.com
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Summary

The objective of the present study was to elucidate whether resveratrol could facilitate the survival of boar sperm during liquid preservation and fast cooling processes. Boar semen were diluted with Modena extender containing different concentrations of resveratrol. Sperm motility was evaluated by visual estimation. Membrane integrity, acrosome integrity and mitochondrial membrane potentials were measured by SYBR-14/PI, FITC-PNA and JC-1 staining, respectively. Moreover, the levels of reactive oxygen species (ROS), malonaldehyde (MDA) and total antioxidant capacity (T-AOC) were measured using commercial assay kits. B-cell lymphoma protein-2 (BCL2) content was determined by western blotting. During liquid preservation at 17oC, the addition of 50 μM resveratrol to the Modena extender significantly improved sperm motility, membrane integrity, acrosome integrity, and sperm mitochondrial membrane potentials. Similar results were also observed in the 150 μM resveratrol group during the fast cooling process. Furthermore, addition of resveratrol led to a decrease of ROS and MDA, and an increase in the content of T-AOC and BCL2. These observations suggest that addition of resveratrol to Modena extender protects boar sperm against oxidative stress. The optimal concentrations of resveratrol are 50 μM and 150 μM during liquid preservation and fast cooling process, respectively.

Keywords

BoarFast coolingReactive oxygen speciesResveratrolSperm
Type
Research Article
Information
Zygote , Volume 28 , Issue 5 , October 2020 , pp. 417 - 424
Copyright
© The Author(s), 2020. Published by Cambridge University Press

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Footnotes

*

These authors contributed equally to this work.

References

Amidi, F, Pazhohan, A, Shabani Nashtaei, M, Khodarahmian, M and Nekoonam, S (2016). The role of antioxidants in sperm freezing: a review. Cell Tissue Bank 17, 745–56.CrossRefGoogle ScholarPubMed
Awda, BJ, Mackenzie-Bell, M and Buhr, MM (2009). Reactive oxygen species and boar sperm function. Biol Reprod 81, 553–61.CrossRefGoogle ScholarPubMed
Baumber, J, Ball, BA, Gravance, CG, Medina, V and Davies-Morel, MC (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.Google ScholarPubMed
Bennetts, LE and Aitken, RJ (2005). A comparative study of oxidative DNA damage in mammalian spermatozoa. Mol Reprod Dev 71, 77–87.CrossRefGoogle ScholarPubMed
Boise, L, González-García, M, Postema, C, Ding, L, Lindsten, T and Turka, L (1993). bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell Mol Life Sci 74, 597–608.Google ScholarPubMed
Brum, AM, Sabeur, K and Ball, BA (2008). Apoptotic-like changes in equine spermatozoa separated by density-gradient centrifugation or after cryopreservation. Theriogenology 69, 1041–55.CrossRefGoogle ScholarPubMed
Bucak, MN, Ataman, MB, Baspinar, N, Uysal, O, Taspinar, M, Bilgili, A, (2015). Lycopene and resveratrol improve post-thaw bull sperm parameters: sperm motility, mitochondrial activity and DNA integrity. Andrologia 47, 545–52.CrossRefGoogle ScholarPubMed
Buhr, MM, Fiser, P, Bailey, JL and Curtis, EF (2001). Cryopreservation in different concentrations of glycerol alters boar sperm and their membranes. J Androl 22, 961–9.CrossRefGoogle ScholarPubMed
Cerolini, S, Maldjian, A, Surai, P and Noble, R (2000). Viability, susceptibility to peroxidation and fatty acid composition of boar semen during liquid storage. Anim Reprod Sci 58(1–2), 99–111.CrossRefGoogle ScholarPubMed
Chuang, SY, Lin, CH and Fang, JY (2014). Natural compounds and aging: between autophagy and inflammasome. Biomed Res Int 2014, 297293.CrossRefGoogle ScholarPubMed
Cisternas, P and Moreno, RD (2006). Comparative analysis of apoptotic pathways in rat, mouse, and hamster spermatozoa. Mol Reprod Dev 73, 1318–25.CrossRefGoogle ScholarPubMed
Collodel, G, Federico, MG, Geminiani, M, Martini, S, Bonechi, C, Rossi, C, Figura, N and Moretti, E (2011). Effect of trans-resveratrol on induced oxidative stress in human sperm and in rat germinal cells. Reprod Toxicol 31, 239–46.CrossRefGoogle ScholarPubMed
Crowe, JH, Hoekstra, FA, Crowe, LM, Anchordoguy, TJ and Drobnis, E (1989). Lipid phase transitions measured in intact cells with Fourier transform infrared spectroscopy. Cryobiology 26, 76–84.CrossRefGoogle ScholarPubMed
De Lamirande, E and Gagnon, C (1992). Reactive oxygen species and human spermatozoa. II. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. J Androl 13, 379–86.Google ScholarPubMed
Delmas, D, Jannin, B and Latruffe, N (2005). Resveratrol: preventing properties against vascular alterations and ageing. Mol Nutr Food Res 49, 377–95.CrossRefGoogle ScholarPubMed
Gadani, B, Bucci, D, Spinaci, M, Tamanini, C and Galeati, G (2017). Resveratrol and epigallocatechin-3-gallate addition to thawed boar sperm improves in vitro fertilization. Theriogenology 90, 88–93.CrossRefGoogle ScholarPubMed
Garcez, ME, dos Santos Branco, C, Lara, LV, Pasqualotto, FF and Salvador, M (2010). Effects of resveratrol supplementation on cryopreservation medium of human serum. Fertil Steril 94, 2118–21.CrossRefGoogle Scholar
Gibb, Z and Aitken, RJ (2016). The impact of sperm metabolism during in vitro storage: the stallion as a model. Biomed Res Int 2016, 9380609.CrossRefGoogle Scholar
Guthrie, HD and Welch, GR (2005). Impact of storage prior to cryopreservation on plasma membrane function and fertility of boar sperm. Theriogenology 63, 396–410.CrossRefGoogle ScholarPubMed
Guthrie, HD and Welch, GR (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, 2089–100.CrossRefGoogle ScholarPubMed
Jeong, YJ, Kim, MK, Song, HJ, Kang, EJ, Ock, SA, Kumar, BM, Balasubramanian, S and Rho, GJ (2009). Effect of alpha-tocopherol supplementation during boar semen cryopreservation on sperm characteristics and expression of apoptosis related genes. Cryobiology 58, 181–9.CrossRefGoogle ScholarPubMed
Johnson, L, Weitze, K, Fiser, P and Maxwell, W (2000). Storage of boar semen. Anim Reprod Sci 62(1–3), 143–72.CrossRefGoogle ScholarPubMed
Kumaresan, A, Kadirvel, G, Bujarbaruah, KM, Bardoloi, RK, Das, A, Kumar, S and Naskar, S (2009). Preservation of boar semen at 18C induces lipid peroxidation and apoptosis like changes in spermatozoa. Anim Reprod Sci 110, 162–71.CrossRefGoogle Scholar
Lehti, MS and Sironen, A (2017). Formation and function of sperm tail structures in association with sperm motility defects. Biol Reprod 97, 522–36.CrossRefGoogle ScholarPubMed
Li, CY, Zhao, YH, Hao, HS, Wang, HY, Huang, JM, Yan, CL, Du, WH, Pang, YW, Zhang, PP, Liu, Y, Zhu, HB and Zhao, XM (2018). Resveratrol significantly improves the fertilisation capacity of bovine sex-sorted semen by inhibiting apoptosis and lipid peroxidation. Sci Rep 8, 7603.CrossRefGoogle ScholarPubMed
Ma, H, Quan, F, Chen, D, Zhang, B and Zhang, Y (2010). Alterations in mitochondrial function and spermatozoal motility in goat spermatozoa following incubation with a human lysozyme plasmid. Anim Reprod Sci 121, 106–14.CrossRefGoogle ScholarPubMed
Martin, G, Sabido, O, Durand, P and Levy, R (2004). Cryopreservation induces an apoptosis-like mechanism in bull sperm. Biol Reprod 71, 28–37.CrossRefGoogle ScholarPubMed
Mojica-Villegas, MA, Izquierdo-Vega, JA, Chamorro-Cevallos, G and Sanchez-Gutierrez, M (2014). Protective effect of resveratrol on biomarkers of oxidative stress induced by iron/ascorbate in mouse spermatozoa. Nutrients 6, 489–503.CrossRefGoogle ScholarPubMed
Moustafa, MH, Sharma, RK, Thornton, J, Mascha, E, Abdel-Hafez, MA, Thomas, AJ Jr and Agarwal, A (2004). Relationship between ROS production, apoptosis and DNA denaturation in spermatozoa from patients examined for infertility. Hum Reprod 19, 129–38.CrossRefGoogle ScholarPubMed
Pervaiz, S and Holme, A (2009). Resveratrol: its biologic targets and functional activity. Antioxid Redox Signal 11, 2851–97.CrossRefGoogle ScholarPubMed
Revel, A, Raanani, H, Younglai, E, Xu, J, Han, R, Savouret, JF and Casper, RF (2001). Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects sperm from DNA damage and apoptosis caused by benzo(a)pyrene. Reprod Toxicol 15, 479–86.CrossRefGoogle ScholarPubMed
Salmon, VM, Leclerc, P and Bailey, JL (2016). Cholesterol-loaded cyclodextrin increases the cholesterol content of goat sperm to improve cold and osmotic resistance and maintain sperm function after cryopreservation. Biol Reprod 94, 85.CrossRefGoogle ScholarPubMed
Sarlós, P, Molnar, A, Kokai, M, Gabor, G and Ratky, J (2002). Comparative evaluation of the effect of antioxidants in the conservation of ram semen. Acta Vet Hung 50, 235–45.CrossRefGoogle ScholarPubMed
Sikka, SC (2001). Relative impact of oxidative stress on male reproductive function. Curr Med Chem 8, 851–62.CrossRefGoogle ScholarPubMed
Silva, EC, Cajueiro, JF, Silva, SV, Soares, PC and Guerra, MM (2012). Effect of antioxidants resveratrol and quercetin on in vitro evaluation of frozen ram sperm. Theriogenology 77, 1722–6.CrossRefGoogle ScholarPubMed
Soleas, G J, Diamandis, EP and Goldberg, DM (1997) Resveratrol: a molecule whose time has come? And gone? Clinical biochemistry, 30, 91–113.CrossRefGoogle ScholarPubMed
Stojanovic, S, Sprinz, H and Brede, O (2001). Efficiency and mechanism of the antioxidant action of trans-resveratrol and its analogues in the radical liposome oxidation. Arch Biochem Biophys 391, 79–89.CrossRefGoogle ScholarPubMed
Thomson, LK, Fleming, SD, Aitken, RJ, De Iuliis, GN, Zieschang, JA and Clark, AM (2009). Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Hum Reprod 24, 2061–70.CrossRefGoogle ScholarPubMed
Tvrdá, E, Kovacik, A, Tusimova, E, Massanyi, P and Lukac, N (2015). Resveratrol offers protection to oxidative stress induced by ferrous ascorbate in bovine spermatozoa. J Environ Sci Health A Tox Hazard Subst Environ Eng 50, 1440–51.CrossRefGoogle ScholarPubMed
Ungvari, Z, Labinskyy, N, Mukhopadhyay, P, Pinto, JT, Bagi, Z, Ballabh, P, Zhang, C, Pacher, P and Csiszar, A (2009). Resveratrol attenuates mitochondrial oxidative stress in coronary arterial endothelial cells. Am J Physiol Heart Circ Physiol 297, H1876–81.CrossRefGoogle ScholarPubMed
Ungvari, Z, Sonntag, WE, De Cabo, R, Baur, JA and Csiszar, A (2011). Mitochondrial protection by resveratrol. Exerc Sport Sci Rev 39, 128–32.CrossRefGoogle ScholarPubMed
Vireque, AA, Tata, A, Silva, OF, Loturco, EG, Azzolini, A, Ferreira, CR, Dantas, MH, Ferriani, RA and Reis, RM (2016). Effects of n-6 and n-3 polyunsaturated acid-rich soybean phosphatidylcholine on membrane lipid profile and cryotolerance of human sperm. Fertil Steril 106, 273–83 e276.CrossRefGoogle ScholarPubMed
Wang, A, Zhang, H, Ikemoto, I, Anderson, D and Loughlin, K (1997). Reactive oxygen species generation by seminal cells during cryopreservation. Urology 49, 921–5.CrossRefGoogle ScholarPubMed
Wang, S, Sun, M, Wang, N, Yang, K, Guo, H, Wang, J, Zhang, Y, Yue, S and Zhou, J (2018). Effects of l-glutamine on boar sperm quality during liquid storage at 17C. Anim Reprod Sci 191, 76–84.CrossRefGoogle Scholar
Wang, X (2001). The expanding role of mitochondria in apoptosis. Genes Dev 15, 2922–33.Google ScholarPubMed
White, IG (1993). Lipids and calcium uptake of sperm in relation to cold shock and preservation: a review. Reprod Fertil Dev 5, 639–58.CrossRefGoogle ScholarPubMed
Zeng, W and Terada, T (2001). Protection of boar spermatozoa from cold shock damage by 2-hydroxypropyl-beta-cyclodextrin. Theriogenology 55, 615–27.CrossRefGoogle ScholarPubMed
Zhu, Z, Fan, X, Lv, Y, Zhang, N, Fan, C, Zhang, P and Zeng, W (2015). Vitamin E analogue improves rabbit sperm quality during the process of cryopreservation through its antioxidative action. PLoS One 10, e0145383.CrossRefGoogle ScholarPubMed
Zhu, Z, Fan, X, Lv, Y, Lin, Y, Wu, and Zeng, W (2017a). Glutamine protects rabbit spermatozoa against oxidative stress via glutathione synthesis during cryopreservation. Reprod Fertil Dev 29, 2183–94.CrossRefGoogle ScholarPubMed
Zhu, Z, Ren, Z, Fan, X, Pan, Y, Lv, S, Pan, C, Lei, A and Zeng, W (2017b). Cysteine protects rabbit spermatozoa against reactive oxygen species-induced damages. PLoS One 12, e0181110.CrossRefGoogle ScholarPubMed
Zini, R, Morin, C, Bertelli, A, Bertelli, A and Tillement, J (1999). Effects of resveratrol on the rat brain respiratory chain. Drugs Exp Clin Res 25(2–3), 87–97.Google ScholarPubMed
Zhu, Z, Li, R, Fan, X, Lv, Y, Zheng, Y, Hoque, SAM, Wu, D and Zeng, W (2109). Resveratrol improves boar sperm quality via 5’AMP-activated protein kinase activation during cryopreservation. Oxid Med Cell Longev 2019, 5921503.Google Scholar
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