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Boar seminal plasma improves sperm quality by enhancing its antioxidant capacity during liquid storage at 17°C

Published online by Cambridge University Press:  08 June 2022

Zhongyun Kou ,
Bingyan Hu ,
Yuqing Li ,
Rui Cai ,
Lei Gao ,
Guiyan Chu ,
Gongshe Yang  and
Weijun Pang Open the ORCID record for Weijun Pang [Opens in a new window]
Zhongyun Kou
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, China
Bingyan Hu
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, China
Yuqing Li
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, China
Rui Cai
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, China
Lei Gao
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, China
Guiyan Chu
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, China
Gongshe Yang
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, China
Weijun Pang*
Affiliation:
Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling Shaanxi 712100, China
*
Author for correspondence: Weijun Pang. No. 22 Xinong Road, Yangling, Shaanxi Province 712100, China. Tel: +86 29 87091017. Fax: +86 29 87092430. E-mail: [email protected]
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Summary

The objective of this study was to investigate the effects of different levels of seminal plasma (SP) on boar sperm quality, antioxidant capacity and bacterial concentrations during liquid storage at 17°C. Boar sperm was diluted with Beltsville Thawing Solution (BTS) consisting of 0, 25, 50 and 75% (v/v) of SP. Total motility, progressive motility and dynamic parameters were assessed by the computer assisted sperm analysis (CASA) system. Acrosome and plasma membrane integrity were measured by FITC-PNA/DAPI and SYBR-14/PI staining, respectively. In addition, total antioxidant capacity (T-AOC), malondialdehyde (MDA) content, and reactive oxygen species (ROS) levels were detected using commercial assay kits. Bacterial concentrations were assessed by turbidimetric assay. Our results showed that 25% SP markedly improved total motility, progressive motility, sperm dynamic parameters, acrosome integrity compared with 0, 50 and 75% SP (P < 0.05). In addition, 25% SP significantly increased T-AOC but decreased MDA content and ROS levels compared with 0, and 75% SP (P < 0.05). Moreover, 25% SP significantly decreased the bacterial concentrations in extended semen compared with 50% and 75% SP, however, which was higher than with 0% SP (P < 0.05). These results suggest that 25% SP can promote boar sperm quality through enhancing its antioxidant capacity during liquid storage.

Keywords

Bacterial contaminationLiquid storageOxidative stressSeminal plasmaSperm quality
Type
Research Article
Information
Zygote , Volume 30 , Issue 5 , October 2022 , pp. 695 - 703
Copyright
© The Author(s), 2022. Published by Cambridge University Press

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References

Althouse, G. C. and Lu, K. G. (2005). Bacteriospermia in extended porcine semen. Theriogenology, 63(2), 573–584. doi: 10.1016/j.theriogenology.2004.09.031 CrossRefGoogle ScholarPubMed
Ammar, O., Houas, Z. and Mehdi, M. (2019). The association between iron, calcium, and oxidative stress in seminal plasma and sperm quality. Environmental Science and Pollution Research International, 26(14), 14097–14105. doi: 10.1007/s11356-019-04575-7 CrossRefGoogle ScholarPubMed
Barranco, I., Padilla, L., Tvarijonaviciute, A., Parrilla, I., Martínez, E. A., Rodriguez-Martinez, H., Yeste, M. and Roca, J. (2019). Levels of activity of superoxide dismutase in seminal plasma do not predict fertility of pig AI-semen doses. Theriogenology, 140, 18–24. doi: 10.1016/j.theriogenology.2019.08.010 CrossRefGoogle Scholar
Barranco, I., Tvarijonaviciute, A., Padilla, L., Rodriguez-Martinez, H., Roca, J. and Lucas, X. (2021). Delays in processing and storage of pig seminal plasma alters levels of contained antioxidants. Research in Veterinary Science, 135, 416–423. doi: 10.1016/j.rvsc.2020.10.027 CrossRefGoogle ScholarPubMed
Breininger, E., Dubois, D., Pereyra, V. E., Rodriguez, P. C., Satorre, M. M. and Cetica, P. D. (2017). Participation of phosphofructokinase, malate dehydrogenase and isocitrate dehydrogenase in capacitation and acrosome reaction of boar spermatozoa. Reproduction in Domestic Animals, 52(5), 731–740. doi: 10.1111/rda.12973 CrossRefGoogle ScholarPubMed
Bussalleu, E., Yeste, M., Sepúlveda, L., Torner, E., Pinart, E. and Bonet, S. (2011). Effects of different concentrations of enterotoxigenic and verotoxigenic E. coli on boar sperm quality. Animal Reproduction Science, 127(3–4), 176–182. doi: 10.1016/j.anireprosci.2011.07.018 CrossRefGoogle ScholarPubMed
Eghbali, M., Alavi-Shoushtari, S. M. and Rezaii, S. A. (2008). Effects of copper and superoxide dismutase content of seminal plasma on buffalo semen characteristics. Pakistan Journal of Biological Sciences, 11(15), 1964–1968. doi: 10.3923/pjbs.2008.1964.1968 CrossRefGoogle ScholarPubMed
Feng, C., Zhu, Z., Bai, W., Li, R., Zheng, Y., Tian, X., Wu, D., Lu, H., Wang, Y. and Zeng, W. (2020). Proline protects boar sperm against oxidative stress through proline dehydrogenase-mediated metabolism and the amine structure of pyrrolidine. Animals (Basel), 10(9), 1549. doi: 10.3390/ani10091549 CrossRefGoogle ScholarPubMed
Gadea, J. (2003). Semen extenders used in the artificial insemination of swine. Spanish Journal of Agricultural Research, 1(2), 17–28.CrossRefGoogle Scholar
Ghiselli, A., Serafini, M., Natella, F. and Scaccini, C. (2000). Total antioxidant capacity as a tool to assess redox status: Critical view and experimental data. Free Radical Biology and Medicine, 29(11), 1106–1114. doi: 10.1016/s0891-5849(00)00394-4 CrossRefGoogle ScholarPubMed
Griveau, J. F., Dumont, E., Renard, P., Callegari, J. P. and Le Lannou, D. (1995). Reactive oxygen species, lipid peroxidation and enzymatic defence systems in human spermatozoa. Journal of Reproduction and Fertility, 103(1), 17–26. doi: 10.1530/jrf.0.1030017 CrossRefGoogle ScholarPubMed
He, Y., Li, D., Zhang, W., Tian, X., Pang, W., Du, R., Yang, G. and Yu, T. (2020). Boar sperm quality and oxidative status as affected by rosmarinic acid at 17°C. Tropical Animal Health and Production, 52(4), 2169–2177. doi: 10.1007/s11250-020-02246-1 CrossRefGoogle ScholarPubMed
Hensel, B., Jakop, U., Scheinpflug, K., Mühldorfer, K., Schröter, F., Schäfer, J., Greber, K., Jung, M. and Schulze, M. (2020). Low temperature preservation of porcine semen: Influence of short antimicrobial lipopeptides on sperm quality and bacterial load. Scientific Reports, 10(1), 13225. doi: 10.1038/s41598-020-70180-1 CrossRefGoogle ScholarPubMed
Jelezarsky, L., Vaisberg, Ch, Chaushev, T. and Sapundjiev, E. (2008). Localization and characterization of glutathione peroxidase (GPx) in boar accessory sex glands, seminal plasma, and spermatozoa and activity of GPx in boar semen. Theriogenology, 69(2), 139–145. doi: 10.1016/j.theriogenology.2007.08.016 CrossRefGoogle ScholarPubMed
Johnson, L. A., Weitze, K. F., Fiser, P. and Maxwell, W. M. (2000). Storage of boar semen. Animal Reproduction Science, 62, 143–172. doi: 10.1016/s0378-4320(00)00157-3 CrossRefGoogle ScholarPubMed
Juyena, N. S. and Stelletta, C. (2012). Seminal plasma: An essential attribute to spermatozoa. Journal of Andrology, 33(4), 536–551. doi: 10.2164/jandrol.110.012583 CrossRefGoogle ScholarPubMed
Kuster, C. E. and Althouse, G. C. (2016). The impact of bacteriospermia on boar sperm storage and reproductive performance. Theriogenology, 85(1), 21–26. doi: 10.1016/j.theriogenology.2015.09.049 CrossRefGoogle ScholarPubMed
Lopes, V. R., Strømme, M. and Ferraz, N. (2020). In vitro biological impact of nanocellulose fibers on human gut bacteria and gastrointestinal cells. Nanomaterials, 10(6), 1159. doi: 10.3390/nano10061159 CrossRefGoogle ScholarPubMed
Mårdh, P. A. and Colleen, S. (1975). Antimicrobial activity of human seminal fluid. Scandinavian Journal of Urology and Nephrology, 9(1), 17–23. doi: 10.3109/00365597509139907 CrossRefGoogle ScholarPubMed
Maxwell, W. M., Welch, G. R. and Johnson, L. A. (1996). Viability and membrane integrity of spermatozoa after dilution and flow cytometric sorting in the presence or absence of seminal plasma. Reproduction, Fertility, and Development, 8(8), 1165–1178. doi: 10.1071/rd9961165 CrossRefGoogle ScholarPubMed
Pan, C., Wu, Y., Yang, Q. and Ye, J. (2018). Effects of seminal plasma concentration on sperm motility and plasma and acrosome membrane integrity in chilled canine spermatozoa. Polish Journal of Veterinary Sciences, 21(1), 133–138. doi: 10.24425/119031 Google ScholarPubMed
Parrilla, I., Martinez, E. A., Gil, M. A., Cuello, C., Roca, J., Rodriguez-Martinez, H. and Martinez, C. A. (2020). Boar seminal plasma: Current insights on its potential role for assisted reproductive technologies in swine. Animal Reproduction, 17(3), e20200022. doi: 10.1590/1984-3143-AR2020-0022 CrossRefGoogle ScholarPubMed
Pei, Y., Yang, L., Wu, L., He, H., Geng, G., Xu, D., Chen, H. and Li, Q. (2018). Combined effect of apigenin and ferulic acid on frozen–thawed boar sperm quality. Animal Science Journal, 89(7), 956–965. doi: 10.1111/asj.13009 CrossRefGoogle ScholarPubMed
Pezo, F., Romero, F., Zambrano, F. and Sánchez, R. S. (2019). Preservation of boar semen: An update. Reproduction in Domestic Animals, 54(3), 423–434. doi: 10.1111/rda.13389 CrossRefGoogle ScholarPubMed
Pinart, E., Domènech, E., Bussalleu, E., Yeste, M. and Bonet, S. (2017). A comparative study of the effects of Escherichia coli and Clostridium perfringens upon boar semen preserved in liquid storage. Animal Reproduction Science, 177, 65–78. doi: 10.1016/j.anireprosci.2016.12.007 CrossRefGoogle ScholarPubMed
Recuero, S., Fernandez-Fuertes, B., Bonet, S., Barranco, I. and Yeste, M. (2019). Potential of seminal plasma to improve the fertility of frozen–thawed boar spermatozoa. Theriogenology, 137, 36–42. doi: 10.1016/j.theriogenology.2019.05.035 CrossRefGoogle ScholarPubMed
Rowe, M., Czirják, G. Á., Lifjeld, J. T. and Giraudeau, M. (2013). Lysozyme-associated bactericidal activity in the ejaculate of a wild passerine. Biological Journal of the Linnean Society, 109(1), 92–100. doi: 10.1111/bij.12044 CrossRefGoogle Scholar
Sabeti, P., Pourmasumi, S., Rahiminia, T., Akyash, F. and Talebi, A. R. (2016). Etiologies of sperm oxidative stress. International Journal of Reproductive Biomedicine, 14(4), 231–240. doi: 10.29252/ijrm.14.4.231 Google ScholarPubMed
Schulze, M., Ammon, C., Schaefer, J., Luther, A. M., Jung, M. and Waberski, D. (2017). Impact of different dilution techniques on boar sperm quality and sperm distribution of the extended ejaculate. Animal Reproduction Science, 182, 138–145. doi: 10.1016/j.anireprosci.2017.05.013 CrossRefGoogle ScholarPubMed
Schulze, M., Czirják, G. Á., Müller, K., Bortfeldt, R., Jung, M. and Jakop, U. (2019). Antibacterial defense and sperm quality in boar ejaculates. Journal of Reproductive Immunology, 131, 13–20. doi: 10.1016/j.jri.2018.11.001 CrossRefGoogle ScholarPubMed
Schulze, M., Jakop, U., Schröter, F., Herrmann, C., Leiding, C., Müller, K., Jung, M. and Czirják, G. Á. (2020). Antibacterial defense in bull and boar semen: A putative link to the microbiome and reproductive strategy? Theriogenology, 157, 335–340. doi: 10.1016/j.theriogenology.2020.07.033 CrossRefGoogle Scholar
Sezonov, G., Joseleau-Petit, D. and D’Ari, R. (2007). Escherichia coli physiology in Luria-Bertani broth. Journal of Bacteriology, 189(23), 8746–8749. doi: 10.1128/JB.01368-07 CrossRefGoogle ScholarPubMed
Shaoyong, W., Li, Q., Ren, Z., Xiao, J., Diao, Z., Yang, G. and Pang, W. (2019a). Effects of kojic acid on boar sperm quality and anti-bacterial activity during liquid preservation at 17C. Theriogenology, 140, 124–135. doi: 10.1016/j.theriogenology.2019.08.020 CrossRefGoogle ScholarPubMed
Shaoyong, W., Li, Q., Ren, Z. Q., Wei, C. S., Chu, G. Y., Dong, W. Z., Yang, G. S. and Pang, W. J. (2019b). Evaluation of ϵ-polylysine as antimicrobial alternative for liquid-stored boar semen. Theriogenology, 130, 146–156. doi: 10.1016/j.theriogenology.2019.03.005 CrossRefGoogle ScholarPubMed
Strzeżek, J., Hopfer, E. and Zaborniak, A. (1987). Zinc ion-dependent protein in boar semen. II. Effects on sperm motility and antibacterial properties. Animal Reproduction Science, 13(2), 133–142. doi: 10.1016/0378-4320(87)90125-4 CrossRefGoogle Scholar
Sun, L., Fan, X., Zeng, Y., Wang, L., Zhu, Z., Li, R., Tian, X., Wang, Y., Lin, Y., Wu, D. and Zeng, W. (2020). Resveratrol protects boar sperm in vitro via its antioxidant capacity. Zygote, 28(5), 417–424. doi: 10.1017/S0967199420000271 CrossRefGoogle Scholar
Tavilani, H., Goodarzi, M. T., Vaisi-raygani, A., Salimi, S. and Hassanzadeh, T. (2008). Activity of antioxidant enzymes in seminal plasma and their relationship with lipid peroxidation of spermatozoa. International Brazilian Journal of Urology, 34(4), 485–491. doi: 10.1590/s1677-55382008000400011 CrossRefGoogle ScholarPubMed
Tian, X., Li, D., He, Y., Zhang, W., He, H., Du, R., Pang, W., Yang, G. and Yu, T. (2019). Supplementation of salvianic acid A to boar semen extender to improve seminal quality and antioxidant capacity. Animal Science Journal, 90(9), 1142–1148. doi: 10.1111/asj.13263 CrossRefGoogle Scholar
Ubeda, J. L., Ausejo, R., Dahmani, Y., Falceto, M. V., Usan, A., Malo, C. and Perez-Martinez, F. C. (2013). Adverse effects of members of the Enterobacteriaceae family on boar sperm quality. Theriogenology, 80(6), 565–570. doi: 10.1016/j.theriogenology.2013.05.02 CrossRefGoogle ScholarPubMed
Zeng, W. X. and Terada, T. (2001). Protection of boar spermatozoa from cold shock damage by 2-hydroxypropyl-beta-cyclodextrin. Theriogenology, 55(2), 615–627. doi: 10.1016/s0093-691x(01)00430-7 CrossRefGoogle ScholarPubMed
Žura Žaja, I., Samardžija, M., Vince, S., Vilić, M., Majić-Balić, I., Đuričić, D. and Milinković-Tur, S. (2016). Differences in seminal plasma and spermatozoa antioxidative systems and seminal plasma lipid and protein levels among boar breeds and hybrid genetic traits. Animal Reproduction Science, 170, 75–82. doi: 10.1016/j.anireprosci.2016.04.006 CrossRefGoogle ScholarPubMed