Monitoring the reactive oxygen species in spermatozoa during liquid storage of boar semen and its correlation with sperm motility, free thiol content and seasonality.


Journal

Andrologia
ISSN: 1439-0272
Titre abrégé: Andrologia
Pays: Germany
ID NLM: 0423506

Informations de publication

Date de publication:
Dec 2021
Historique:
revised: 09 08 2021
received: 26 02 2021
accepted: 24 08 2021
pubmed: 8 9 2021
medline: 4 11 2021
entrez: 7 9 2021
Statut: ppublish

Résumé

Oxidative stress is an important factor affecting the quality of spermatozoa during liquid storage of boar semen; however, monitoring of reactive oxygen species (ROS) that provides direct insight into the oxidative status is not yet attempted. This study aimed to monitor ROS in boar sperm during liquid semen storage to determine its correlation with sperm motility and free thiol (SH) content, and seasonality. Ejaculate was collected from mature Duroc boars in a commercial farm in autumn and spring, diluted in Mulberry III extender, stored at 15°C, and examined daily for sperm ROS level, SH content and motility. The ROS levels in spermatozoa prepared during autumn and spring were constantly low until days 4 and 5 of storage, respectively, which thereafter progressively increased in association with the loss of sperm motility. The increased sperm ROS level correlated with the higher SH level and lower motility, which was accentuated from day 4 of storage and was higher in September, or early autumn. This study indicates that increased sperm ROS levels during liquid storage results in oxidative damage, causing loss of sperm motility, presumably through decreased sperm viability, suggesting that sperm ROS monitoring effectively evaluates the quality of boar semen.

Identifiants

pubmed: 34490648
doi: 10.1111/and.14237
doi:

Substances chimiques

Reactive Oxygen Species 0
Sulfhydryl Compounds 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e14237

Subventions

Organisme : Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science
ID : 18H02327

Informations de copyright

© 2021 Wiley-VCH GmbH.

Références

Agarwal, A., Sharma, R. K., Nallella, K. P., Thomas, A. J. Jr, Alvarez, J. G., & Sikka, S. C. (2006). Reactive oxygen species as an independent marker of male factor infertility. Fertility and Sterility, 86(4), 878-885. https://doi.org/10.1016/j.fertnstert.2006.02.111
Aitken, R. J., Clarkson, J. S., & Fishel, S. (1989). Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biology of Reproduction, 41(1), 183-197. https://doi.org/10.1095/biolreprod41.1.183
Aitken, R. J., Gibb, Z., Baker, M. A., Drevet, J., & Gharagozloo, P. (2016). Causes and consequences of oxidative stress in spermatozoa. Reproduction, Fertility, and Development, 28(1-2), 1-10.
Bennetts, L. E., & Aitken, R. J. (2005). A comparative study of oxidative DNA damage in mammalian spermatozoa. Molecular Reproduction and Development, 71(1), 77-87. https://doi.org/10.1002/mrd.20285
Bondan, C., Zanella, E., Zanella, R., Poetini, M. R., Marques, M. G., & Soares, J. C. M. (2016). Oxidative status of boar semen during storage. American Journal of Biochemistry and Biotechnology, 12(2), 95-101. https://doi.org/10.3844/ajbbsp.2016.95.101
Cerolini, S., Maldjian, A., Surai, P., & Noble, R. (2000). Viability, susceptibility to peroxidation and fatty acid composition of boar semen during liquid storage. Animal Reproduction Science, 58(1-2), 99-111. https://doi.org/10.1016/S0378-4320(99)00035-4
Cornwall, G. A., Vindivich, D., Tillman, S., & Chang, T. S. K. (1988). The effect of sulfhydryl oxidation on the morphology of immature hamster epididymal spermatozoa induced to acquire motility in vitro. Biology of Reproduction, 39(1), 141-155.
Darbandi, M., Darbandi, S., Agarwal, A., Sengupta, P., Durairajanayagam, D., Henkel, R., & Sadeghi, M. R. (2018). Reactive oxygen species and male reproductive hormones. Reproductive Biology and Endocrinology, 16(1), 87. https://doi.org/10.1186/s12958-018-0406-2
de Lamirande, E., & Gagnon, C. (1992). Reactive oxygen species and human spermatozoa. II. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. Journal of Andrology, 13(5), 379-386.
Ferramosca, A., Pinto Provenzano, S., Montagna, D. D., Coppola, L., & Zara, V. (2013). Oxidative stress negatively affects human sperm mitochondrial respiration. Urology, 82(1), 78-83. https://doi.org/10.1016/j.urology.2013.03.058
Gavella, M., & Lipovac, V. (2013). Protective effects of exogenous gangliosides on ROS-induced changes in human spermatozoa. Asian Journal of Andrology, 15(3), 375-381. https://doi.org/10.1038/aja.2012.144
Iwasaki, A., & Gagnon, C. (1992). Formation of reactive oxygen species in spermatozoa of infertile patients. Fertility and Sterility, 57(2), 409-416.
Johnson, L. A., Weitze, K. F., Fiser, P., & Maxwell, W. M. (2000). Storage of boar semen. Animal Reproduction Science, 62(1-3), 143-172. https://doi.org/10.1016/S0378-4320(00)00157-3
Knox, R. V. (2016). Artificial insemination in pigs today. Theriogenology, 85(1), 83-93. https://doi.org/10.1016/j.theriogenology.2015.07.009
Ko, E. Y., Sabanegh, E. S. Jr, & Agarwal, A. (2014). Male infertility testing: Reactive oxygen species and antioxidant capacity. Fertility and Sterility, 102(6), 1518-1527. https://doi.org/10.1016/j.fertnstert.2014.10.020
Kohsaka, T. (2020). Testis, sperm and accessory glands. Textbook of reproduction and development (2nd ed., pp. 47-64). Tokyo: EDUWARD Press. ISBN:978-4-86671-110-2
Kohsaka, T., Minagawa, I., Morimoto, M., Yoshida, T., Sasanami, T., Yoneda, Y., Ikegaya, N., & Sasada, H. (2020). Efficacy of relaxin for cisplatin-induced testicular dysfunction and epididymal spermatotoxicity. Basic and Clinical Andrology, 30, 3. https://doi.org/10.1186/s12610-020-0101-y
Lenzi, A., Gandini, L., Maresca, V., Rago, R., Sgrò, P., Dondero, F., & Picardo, M. (2000). Fatty acid composition of spermatozoa and immature germ cells. Molecular Human Reproduction, 6(3), 226-321. https://doi.org/10.1093/molehr/6.3.226
Lopes, S., Jurisicova, A., Sun, J. G., & Casper, R. F. (1998). Reactive oxygen species: Potential cause for DNA fragmentation in human spermatozoa. Human Reproduction, 13(4), 896-900. https://doi.org/10.1093/humrep/13.4.896
Love, C. C., & Kenney, R. M. (1999). Scrotal heat stress induces altered sperm chromatin structure associated with a decrease in protamine disulfide bonding in the stallion. Biology of Reproduction, 60(3), 615-620. https://doi.org/10.1095/biolreprod60.3.615
Minagawa, I., Murata, Y., Terada, K., Shibata, M., Park, E. Y., Sasada, H., & Kohsaka, T. (2018). Evidence for the role of INSL3 on sperm production in boars by passive immunisation. Andrologia, 50(6), e13010. https://doi.org/10.1111/and.13010
Morielli, T., & O'Flaherty, C. (2015). Oxidative stress impairs function and increases redox protein modifications in human spermatozoa. Reproduction, 149(1), 113-123. https://doi.org/10.1530/REP-14-0240
Nazarewicz, R. R., Bikineyeva, A., & Dikalov, S. I. (2013). Rapid and specific measurements of superoxide using fluorescence spectroscopy. Journal of Biomolecular Screening, 18(4), 498-503. https://doi.org/10.1177/1087057112468765
Pérez-Crespo, M., Pintado, B., & Gutiérrez-Adán, A. (2008). Scrotal heat stress effects on sperm viability, sperm DNA integrity and the offspring sex ratio in mice. Molecular Reproduction and Development, 75(1), 40-47. https://doi.org/10.1002/mrd.20759
Rodríguez-Gil, J. E., & Estrada, E. (2013). Artificial insemination in boar reproduction. In S. Bonet, I. Casas, W. V. Holt, & M. Yeste (Eds.), Boar reproduction (pp. 589-608). Springer. https://doi.org/10.1007/978-3-642-35049-8_12
Rufas, O., Fisch, B., Seligman, J., Tadir, Y., Ovadia, J., & Shalgi, R. (1991). Thiol status in human sperm. Molecular Reproduction and Development, 29(3), 282-288. https://doi.org/10.1002/mrd.1080290311
Sagata, D., Minagawa, I., Kohriki, H., Pitia, A. M., Uera, N., Katakura, Y., & Kohsaka, T. (2015). The insulin-like factor 3 (INSL3)-receptor (RXFP2) network functions as a germ cell survival/anti-apoptotic factor in boar testes. Endocrinology, 156(4), 1523-1539. https://doi.org/10.1210/en.2014-1473
Sanocka, D., & Kurpisz, M. (2004). Reactive oxygen species and sperm cells. Reproductive Biology and Endocrinology, 2, 12. https://doi.org/10.1186/1477-7827-2-12
Seligman, J., Kosower, N. S., Weissenberg, R., & Shalgi, R. (1994). Thiol-disulfide status of human sperm proteins. Journal of Reproduction and Fertility, 101(2), 435-443. https://doi.org/10.1530/jrf.0.1010435
Shalgi, R., Seligman, J., & Kosower, N. S. (1989). Dynamics of the thiol status of rat spermatozoa during maturation: Analysis with the fluorescent labeling agent monobromobimane. Biology of Reproduction, 40(5), 1037-1045.
Sonderman, J. P., & Luebbe, J. J. (2008). Semen production and fertility issues related to differences in genetic lines of boars. Theriogenology, 70(8), 1380-1383. https://doi.org/10.1016/j.theriogenology.2008.08.009
Suleiman, S. A., Ali, M. E., Zaki, Z. M., el-Malik, E. M., & Nasr, M. A. (1996). Lipid peroxidation and human sperm motility: Protective role of vitamin E. Journal of Andrology, 17(5), 530-537.
Tsakmakidis, I., Lymberopoulos, A., & Khalifa, T. (2010). Relationship between sperm quality traits and field-fertility of porcine semen. Journal of Veterinary Science, 11(2), 151-154. https://doi.org/10.4142/jvs.2010.11.2.151
Vyt, P., Maes, D., Dejonckheere, E., Castryck, F., & Van Soom, A. (2004). Comparative study on five different commercial extenders for boar semen. Reproduction in Domestic Animals, 39(1), 8-12. https://doi.org/10.1046/j.1439-0531.2003.00468.x
Waterhouse, K. E., De Angelis, P. M., Haugan, T., Paulenz, H., Hofmo, P. O., & Farstad, W. (2004). Effects of in vitro storage time and semen-extender on membrane quality of boar sperm assessed by flow cytometry. Theriogenology, 62(9), 1638-1651. https://doi.org/10.1016/j.theriogenology.2004.03.001
Wei, S. M., Yan, Z. Z., & Zhou, J. (2007). Beneficial effect of taurine on testicular ischemia-reperfusion injury in rats. Urology, 70(6), 1237-1242. https://doi.org/10.1016/j.urology.2007.09.030
Zini, A., Kamal, K. M., & Phang, D. (2001). Free thiols in human spermatozoa: Correlation with sperm DNA integrity. Urology, 58(1), 80-84. https://doi.org/10.1016/S0090-4295(01)00997-9

Auteurs

Hoang Xuan Khoi (HX)

Department of Applied Life Science, Faculty of Agriculture, Shizuoka University, Shizuoka, Japan.

Kenji Shimizu (K)

Fuji Nojo Service, Fujinomiya, Japan.

Yoshitaka Yoneda (Y)

Tokuoka Ladies Clinic, Tokyo, Japan.

Itaru Minagawa (I)

Department of Applied Life Science, Faculty of Agriculture, Shizuoka University, Shizuoka, Japan.

Yasuyuki Abe (Y)

Department of Life Sciences, Faculty of Life and Environmental Sciences, Prefectural University of Hiroshima, Hiroshima, Japan.

Yasushi Kuwabara (Y)

Fuji Nojo Service, Fujinomiya, Japan.

Tomohiro Sasanami (T)

Department of Applied Life Science, Faculty of Agriculture, Shizuoka University, Shizuoka, Japan.

Tetsuya Kohsaka (T)

Department of Applied Life Science, Faculty of Agriculture, Shizuoka University, Shizuoka, Japan.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH