Effect of Testosterone, Dihydrotestosterone, Estradiol and Cortisol on the Quality of Fresh and Cryopreserved Stallion Sperm
DOI:
https://doi.org/10.18006/2022.10(3).619.627Keywords:
Horse breeding, Cryopreservation, Sperm, Reproductive characteristics, Steroid hormonesAbstract
The effect of steroid hormones on the quality of fresh and cryopreserve sperm has not been fully understood. This study aimed to evaluate the effect of testosterone, dihydrotestosterone, estradiol, and cortisol on the quality of fresh and cryopreserved stallion sperm. The study was conducted on 40 Equus caballus stallions, including Arab (n=20), Oryol trotting (n=4), Standardbred (n=4), and Soviet Heavy Draft (n=12) breeds. The average age of the experimental animals was 9.9 ± 0.7 years. We determined standard quality indicators in fresh and cryopreserved sperm and the concentration of steroid hormones in the blood plasma of stallions. Results of the study suggested a negative correlation between the level of testosterone with total (r=-0.41; p<0.01) and progressive (r=-0.44; p<0.01) sperm motility in cryopreserved sperm as well as in fresh sperm (r=-0.38; p<0.05 and r=-0.39; p<0.05 correspondingly). While the level of estradiol showed a positive correlation with survival rate in cryopreserved (r=0.35; p<0.05) and in fresh (r=0.33; p<0.05) sperm. Further, the level of cortisol in the blood plasma of stallions did not show any statistically significant correlations with the qualitative characteristics of sperm. A positive relationship was found between the concentration of dihydrotestosterone with the volume of ejaculate (r=0.37; p<0.05) and the total number of sperm in the ejaculate (r=0.43; p<0.01). Results of the study can be concluded that steroid hormones have different effects on the quality indicators of fresh and cryopreserved sperm of stallions and their concentration in the blood should be considered when selecting stallions for cryopreservation of sperm.
References
Amory, J.K., Wang, C., & Swerdloff, R.S. (2007). The effect of 5alpha-reductase inhibition with dutasteride and finasteride on semen parameters and serum hormones in healthy men. The Journal of Clinical Endocrinology & Metabolism, 92, 1659–1665. https://doi.org/10.1210/jc.2006-2203 DOI: https://doi.org/10.1210/jc.2006-2203
Atroshchenko, M. M., Arkhangelskaya, E., Isaev, D. A., Stavitsky, S. B., et al. (2019a). Reproductive characteristics of thawed stallion sperm. Animals, 9 (12), 1099. DOI: https://doi.org/10.3390/ani9121099
Atroshchenko, M. M., Engalycheva, M. G., Kudlaeva, A. M., & Borodkina, E. Y. (2020). Effect of Blood Enzyme Activity on Stallion Sperm Quality and Cryostability. In XIX International Scientific and Practical Conference" Current Trends of Agricultural Industry in Global Economy" (pp. 1-8). DOI: https://doi.org/10.32743/agri.gl.econ.2020.1-8
Atroshchenko, M.M., Bragina, E.E., Zaitsev, A.M., et al. (2019b). Conservation of genetic resources in horse breeding and major structural damages of sperm during semen cryopreservation in stallions. Nature Conservation Research, 4(2), 78–82. https://dx.doi.org/10.24189/ncr.2019.024 DOI: https://doi.org/10.24189/ncr.2019.024
Atroshchenko, M.M., Kalaschnikov, V.V., Bragina, Y.Y., & Zaitsev, A.M. (2017). Comparative study of the structural integrity of spermatozoa in epididymal, ejaculated and cryopreserved semen of stallions. Sel’skokhozyaistvennayabiologiya [Agricultural Biology], 52(2), 274-281 DOI: 10.15389/agrobiology.2017.2.274eng DOI: https://doi.org/10.15389/agrobiology.2017.2.274eng
Atroshchenko, M.M., Kudlaeva, A.M., Fomina, M.A., et al. (2019c). Analysis of seminal plasma biochemical parameters and sperm cryostability in different age groups of stallions. IOP Conference Series: Earth and Environmental Science, 341, 012162. doi:10.1088/1755-1315/341/1/012162 DOI: https://doi.org/10.1088/1755-1315/341/1/012162
Aurich, J., Kuhl, J., Tichy, A., & Aurich, C. (2020). Efficiency of semen cryopreservation in stallions. Animals, 10(6), 1033. https://doi.org/10.3390/ani10061033 DOI: https://doi.org/10.3390/ani10061033
Ballesteros, L.M., Delgado, N.M., Rosado, A., & Hernández, O. (1983). Effect of steroid hormones on membrane sugar transport in human spermatozoa. Archives of Andrology, 11(2), 1195–100. DOI: 10.3109/01485018308987467 DOI: https://doi.org/10.3109/01485018308987467
Basiru, A., Abdullahi, I. O., Adakole, A. S., Jimoh, A. G., Abdulfatai, A., & Mistura, A. O. (2022). Correlation between Testicular Biometrics and Serum Level of Reproductive Hormones of Crossed Arewa Breed of Stallions in Ilorin, Nigeria. Media Kedokteran Hewan, 33(2), 53-62. DOI: https://doi.org/10.20473/mkh.v33i2.2022.53-62
Bilinska, B., Wiszniewska, B., Kosiniak-Kamysz, K., et al. (2006). Hormonal status of male reproductive system: androgens and estrogens in the testis and epididymis. In vivo and in vitro approaches. Reproductive Biology, 6 (1), 43–58.
Bishop, J.D., Malven, P.V., Singleton, W.L., & Weesner, G.D. (1999). Hormonal and behavioral correlates of emotional states in sexually trained boars. Journal of Animal Science, 77, 3339-3345. https://doi.org/10.2527/1999.77123339x DOI: https://doi.org/10.2527/1999.77123339x
Borg, K.E., Esbenshade, K.L., & Johnson, B.H. (1991). Cortisol, growth hormone, and testosterone concentrations during mating behavior in the bull and boar. Journal of Animal Science, 69, 3230-3240. https://doi.org/10.2527/1991.6983230x DOI: https://doi.org/10.2527/1991.6983230x
Bóveda, P., Esteso, M. C., Velázquez, R., Castaño, C., et al. (2021). Influence of circulating testosterone concentration on sperm cryoresistance: The ibex as an experimental model. Andrology, 9 (4), 1242-1253.https://doi.org/10.1111/andr.12998 DOI: https://doi.org/10.1111/andr.12998
Cai, L., Fratianni, C.M., Gautier, T., & Imperato-McGinley, J. (1994). Dihydrotestosterone regulation of semen in male pseudohermaphrodites with 5a-reductase-2 deficiency. The Journal of Clinical Endocrinology & Metabolism, 79, 409–414. https://doi.org/10.1210/jcem.79.2.8045956 DOI: https://doi.org/10.1210/jcem.79.2.8045956
Calzada, L., Bernal, A, & Loustaunau, E. (1988). Effect of steroid hormones and capacitation on membrane potential of human spermatozoa. Archives of Andrology, 21, 121–128. https://doi.org/10.3109/01485018808986722 DOI: https://doi.org/10.3109/01485018808986722
Carreau, S., Delalande, C., & Galeraud-Denis, I. (2009). Mammalian sperm quality and aromatase expression. Microscopy Research and Technique, 72(8), 552-557. https://doi.org/10.1002/ jemt.20703 DOI: https://doi.org/10.1002/jemt.20703
Cheng, C.Y., Boettcher, B., Tinneberg, H.R., & Buxton, J. (1980). Activation of spermatozoal forward migration in vitro by hydrocortisone. International Journal of Andrology, 3(6), 654-670. https://doi.org/10.1111/j.1365-2605.1980.tb00153.x DOI: https://doi.org/10.1111/j.1365-2605.1980.tb00153.x
Claus, R., Wagner, A., & Lambert, T. (2005). Characterization of 11beta-hydroxysteroid dehydrogenase activity in testicular tissue of control and GnRH-immunized boars as a possible regulator of spermatogenesis. Experimental and Clinical Endocrinology & Diabetes, 113, 262–267. DOI: https://doi.org/10.1055/s-2005-837554
Coloma, M.A., Go´mez-Brunet, A., Vela´zquez, R., et al. (2010). Freezability of Iberian ibex (Capra pyrenaica) sperm according to the glycerolization temperature and plasma testosterone concentration. Cryobiology, 61, 204–210. https://doi.org/10.1016/ j.cryobiol.2010.07.005 DOI: https://doi.org/10.1016/j.cryobiol.2010.07.005
Cooke, P. S., & Walker, W. H. (2022). Nonclassical androgen and estrogen signaling is essential for normal spermatogenesis. Seminars in Cell & Developmental biology, 121, 71–81. https://doi.org/10.1016/j.semcdb.2021.05.032 DOI: https://doi.org/10.1016/j.semcdb.2021.05.032
Deichsel, K., Pasing, S., & Erber, R. (2015). Increased cortisol release and transport stress do not influence semen quality and testosterone release in pony stallions. Theriogenology, 84(1), 70-75. https://doi.org/10.1016/j.theriogenology.2015.02.015 DOI: https://doi.org/10.1016/j.theriogenology.2015.02.015
Draper, N., & Stewart, P.M. (2005). 11beta-Hydroxysteroid dehydrogenase and the pre-receptor regulation of corticosteroid hormone action. Journal of Endocrinology, 186, 251–271. DOI: 10.1677/joe.1.06019 DOI: https://doi.org/10.1677/joe.1.06019
Elkina, Yu. L., Atroshchenko, M. M., Bragina, E. E., Muronetz, V. I., & Schmalhausen, E. V. (2011). Oxidation of glyceraldehydes-3-phosphate dehydrogenase decreases sperm motility. Biochemistry (Moscow), 76(2), 268-272. https://doi.org/10.1016/j.bbrc.2015.08.006 DOI: https://doi.org/10.1134/S0006297911020143
Ellerbrock, R. E., Podico, G., Scoggin, K. E., Ball, B. A., Carossino, M., & Canisso, I. F. (2021). Steroidogenic Enzyme and Steroid Receptor Expression in the Equine Accessory Sex Glands. Animals, 11(8), 2322. https://doi.org/10.3390/ani11082322 DOI: https://doi.org/10.3390/ani11082322
Greiser, T., Sieme, H., Martinsson, G., & Distl, O. (2020). Breed and stallion effects on frozen-thawed semen in warm blood, light and quarter horses. Theriogenology, 142, 8-14. https://doi.org/10.1016/j.theriogenology.2019.09.033 DOI: https://doi.org/10.1016/j.theriogenology.2019.09.033
Haffner, J.C., Fecteau, K.A., & Eiler, H. (2010). Blood steroid concentrations in domestic Mongolian horses. Journal of Veterinary Diagnostic Investigation, 22(4), 537-543. https://doi.org/10.1177/104063871002200407 DOI: https://doi.org/10.1177/104063871002200407
Hess, M.F., & Roser, J.F. (2004). Immunocytochemical localization of cytochrome P450 aromatase in the testis of prepubertal, pubertal, and postpubertal horses. Theriogenology, 61, 293–299. https://doi.org/10.1016/S0093-691X(03)00237-1 DOI: https://doi.org/10.1016/S0093-691X(03)00237-1
Hind, H., Farida, B. A., & Zoubir, B. (2021). Biometric Testicular and Hormonal Serum Profiles of Arabian Stallion during Breeding Season in Algeria. Animal Biotechnology, 59 (2), 137-142. 10.21608/assjm.2021.192149 DOI: https://doi.org/10.21608/assjm.2021.192149
Hoffmann, B., & Landeck, A. (1999). Testicular endocrine function, seasonality and semen quality of the stallion. Animal Reproduction Science, 57, 89-98. https://doi.org/10.1016/S0378-4320(99)00050-0 DOI: https://doi.org/10.1016/S0378-4320(99)00050-0
Holdcraft, R.W., & Braun, R.E. (2004). Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids. Development, 131, 459–467. doi: 10.1242/dev.00957 DOI: https://doi.org/10.1242/dev.00957
Inoue, J., Cerbito, W.A., Oguri, N., Matsuzawa, T., & Sato, K. (1993). Serum levels of testosterone and oestrogens in normal and infertile stallions. International Journal of Andrology, 16, 155-158. https://doi.org/10.1111/j.1365-2605.1993.tb01169.x DOI: https://doi.org/10.1111/j.1365-2605.1993.tb01169.x
Jarow, J.P., & Zirkin, B.R. (2005). The androgen microenvironment of the human testis and hormonal control of spermatogenesis. Annals of the New York Academy of Sciences, 1061, 208–220 https://doi.org/10.1196/annals.1336.023 DOI: https://doi.org/10.1196/annals.1336.023
Jeremy, M., Gurusubramanian, G., Roy, V. K., & Kharwar, R. K. (2021). Co-treatment of testosterone and estrogen mitigates heat-induced testicular dysfunctions in a rat model. The Journal of Steroid Biochemistry and Molecular Biology, 214, 106011. https://doi.org/10.1016/j.jsbmb.2021.106011 DOI: https://doi.org/10.1016/j.jsbmb.2021.106011
Kang, H., Imperato-MсGinley J., Zhu Y., & Rosenwaks Z. (2014). The effect of 5α-reductase-2 deficiency on human fertility. Fertility and Sterility, 101(2), 310-316. https://doi.org/10.1016/ j.fertnstert.2013.11.128 DOI: https://doi.org/10.1016/j.fertnstert.2013.11.128
Khan, I. M., Cao, Z., Liu, H., Khan, A., et al. (2021). Impact of cryopreservation on spermatozoa freeze-thawed traits and relevance omics to assess sperm cryo-tolerance in farm animals. Frontiers in Veterinary Science, 8, 139.https://doi.org/10.3389/ fvets.2021.609180 DOI: https://doi.org/10.3389/fvets.2021.609180
Lambard, S., Galeraud-Denis, I., Martin, G., Levy, R., & Carreau, S. (2004). Analysis and significance of mRNA in human ejaculated sperm from normozoospermic donors: Relationship to sperm motility and capacitation. Molecular Human Reproduction, 10, 535–541. https://doi.org/10.1093/molehr/gah064 DOI: https://doi.org/10.1093/molehr/gah064
Larose, H., Kent, T., Ma, Q., Shami, A. N., et al. (2020). Regulation of meiotic progression by Sertoli-cell androgen signaling. Molecular Biology of the Cell, 31(25), 2841-2862. https://doi.org/10.1091/mbc.E20-05-0334 DOI: https://doi.org/10.1091/mbc.E20-05-0334
Leahy, T., Rickard, J. P., Pini, T., Gadella, B. M., & de Graaf, S. P. (2020). Quantitative proteomic analysis of seminal plasma, sperm membrane proteins, and seminal extracellular vesicles suggests vesicular mechanisms aid in the removal and addition of proteins to the ram sperm membrane. Proteomics, 20(12), 1900289. https://doi.org/10.1002/pmic.201900289 DOI: https://doi.org/10.1002/pmic.201900289
Martínez-Fresneda, L., O'Brien, E., LópezSebastián, A., et al. (2019). In vitro supplementation of testosterone and prolactin affects spermatozoa freezability in small ruminants. Domestic Animal Endocrinology, 72 (106372), 1-9. DOI: 10.1016/j.domaniend.2019.06.004 DOI: https://doi.org/10.1016/j.domaniend.2019.06.004
Meng, J., Holdcraft, R.W., Shima, J.E., Griswold, M.D., & Braun, R.E. (2005). Androgens regulate the permeability of the blood–testis barrier. The Proceedings of the National Academy of Sciences U.S.A., 102, 16696–16700. https://doi.org/10.1073/ pnas.0506084102 DOI: https://doi.org/10.1073/pnas.0506084102
Mesbah, M., Forouzanfar, M., & Eghbalsaied, S. (2022). Supplementation of Estradiol Into Semen Extender Improved Goat Sperm Cryopreservation. Biopreservation and Biobanking, 20(1), 59-66. https://doi.org/10.1089/bio.2020.0169 DOI: https://doi.org/10.1089/bio.2020.0169
Naumenkov, A.I., & Roman’kova, N.K. (1971). The method for stallion semen cryopreservation. In Theoretical and Practical Aspects of Horse Breeding: Scientific reports of Russian Institute of Horse Breeding; Russian Institute of Horse Breeding: Divovo, Russia, XXV, 128–132.
Nixon, B., De Iuliis, G. N., Hart, H. M., Zhou, W., et al. (2019). Proteomic profiling of mouse epididymosomes reveals their contributions to post-testicular sperm maturation. Molecular & Cellular Proteomics, 18, S91-S108. https://doi.org/10.1074/ mcp.RA118.000946 DOI: https://doi.org/10.1074/mcp.RA118.000946
O’Donnell, L., Robertson, K.M., Jones, M.E., & Simpson, E.R. (2001). Estrogen and spermatogenesis. Endocrine Reviewes, 22, 289–318. https://doi.org/10.1210/edrv.22.3.0431 DOI: https://doi.org/10.1210/edrv.22.3.0431
Pearl, C.A., Mason, H., & Roser,J.F. (2011). Immunolocalization of estrogen receptor alpha, estrogen receptor beta and androgen receptor in the pre-, peri- and post-pubertal stallion testis. Animal Reproduction Science,125(1-4), 103-111. https://doi.org/10.1016/ j.anireprosci.2011.03.007 DOI: https://doi.org/10.1016/j.anireprosci.2011.03.007
Purohit, S.B., Saxena, D., Laloraya, M., & Kumar, G.P. (2000). Altered molecular dynamics and antioxidant status in the spermatozoa in testosterone-induced oligospermia in mouse. Molecular Reproduction and Development, 55, 316–325. https://doi.org/10.1002/(SICI)1098-2795(200003)55:3<316::AID-MRD10>3.0.CO;2-G DOI: https://doi.org/10.1002/(SICI)1098-2795(200003)55:3<316::AID-MRD10>3.0.CO;2-G
Rengarajan, S., & Balasubramanian, K. (2007). Corticosterone has direct inhibitory effect on the expression of peptide hormone receptors, 11betaHSD and glucose oxidation in cultured adult rat Leydig cells. Molecular and Cellular Endocrinology, 279, 52–62. https://doi.org/10.1016/j.mce.2007.09.001 DOI: https://doi.org/10.1016/j.mce.2007.09.001
Robertson, K.M., O’Donnell, L., & Jones, M.E. (1999). Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. The Proceedings of the National Academy of Sciences U.S.A., 96, 7986–7991. https://doi.org/ 10.1073/pnas.96.14.7986 DOI: https://doi.org/10.1073/pnas.96.14.7986
Rochira, V., Granata, A., & Madeo, B. (2005). Estrogens in males: What we have learned in last 10 years? Asian Journal of Andrology, 7, 3–20. https://doi.org/10.1111/j.1008-862X.2005.00018.x DOI: https://doi.org/10.1111/j.1745-7262.2005.00018.x
Roser, J.F. (2008). Regulation of testicular function in the stallion: An intricate network of endocrine, paracrine and autocrine systems. Animal Reproduction Science, 107, 3–4, 179-196. https://doi.org/10.1016/j.anireprosci.2008.05.004 DOI: https://doi.org/10.1016/j.anireprosci.2008.05.004
Roser, J.F., & Hughes, J.P. (1992). Seasonal effects on seminal quality, plasma hormone concentrations and GnRH-induced LH response in fertile and subfertile stallions. Journal of Andrology, 13, 214-223. https://doi.org/10.1002/j.1939-4640.1992.tb00304.x
Seale, J. (2010). Analysis of estronesulphate, testosterone, and cortisol concentrations around time of ejaculation and potential correlation to sexual behavior and sperm characteristics in stallions. Unpublished Ph.D. thesis submitted to the Texas A & M University.
Shivaji, S., & Jagannadham, M.V. (1992). Steroid-induced perturbations of membranes and its relevance to sperm acrosome reaction. Biochimicaet Biophysica Acta, 1108, 99-109. https://doi.org/10.1016/0005-2736(92)90119-7 DOI: https://doi.org/10.1016/0005-2736(92)90119-7
Tamanini, C., Giordano, N., Chiesa, F., & Seren, E. (1983). Plasma cortisol variations induced in the stallion by mating. Acta Endocrinologica, 102, 447-450. DOI: https://doi.org/10.1530/ acta.0.1020447 DOI: https://doi.org/10.1530/acta.0.1020447
Turner, T.T., Jones C.E., & Howards S.S. (1984). On the androgen microenvironment of maturing spermatozoa. Endocrinology, 115, 1925–1932. https://doi.org/10.1210/endo-115-5-1925 DOI: https://doi.org/10.1210/endo-115-5-1925
Varner D., Moraes C., Teague S., Cortopassi G., Datta S., & Meyers S. (2016). Lactate and pyruvate are major sources of energy for stallion sperm with dose effects on mitochondrial
function, motility, and ROS production. Biology of Reproduction, 95(2), 1-11. doi: 10.1095/biolreprod.116.140707. DOI: https://doi.org/10.1095/biolreprod.116.140707
Villani, M., Cairoli, F., & Kindahl, H. (2006). Effects of mating on plasma concentrations of testosterone, cortisol, oestronesulphate and PGF2a in stallions. Reproduction in Domestic Animals, 41, 544–548. https://doi.org/10.1111/j.1439-0531.2006.00711.x DOI: https://doi.org/10.1111/j.1439-0531.2006.00711.x
Walker, W.H. (2011). Testosterone signaling and the regulation of spermatogenesis. Spermatogenesis, 1(2), 116-120. https://doi.org/ 10.4161/spmg.1.2.16956 DOI: https://doi.org/10.4161/spmg.1.2.16956
Watson, P.F. (2000). The causes of reduced fertility with cryopreserved semen. Animal Reproduction Science, 6061, 481–92. https://doi.org/10.1016/S0378-4320(00)00099-3 DOI: https://doi.org/10.1016/S0378-4320(00)00099-3
Weerakoon, W. W. P. N., Sakase, M., Kohama, N., & Kawate, N. (2020). Plasma estradiol-17β, cortisol, and insulin concentrations and serum biochemical parameters surrounding puberty in Japanese Black beef bulls with normal and abnormal semen. Theriogenology, 148, 18-26. https://doi.org/10.1016/j. theriogenology.2020.02.035 DOI: https://doi.org/10.1016/j.theriogenology.2020.02.035
Wiest, J.J., Thompson, D.L., McNeill-Wiest, D.R., Garza, F., & Mitchell, P.S. (1988). Effect of administration of adrenocorticotropic hormone on plasma concentrations of testosterone, luteinizing hormone, follicle stimulating hormone and cortisol in stallions. Journal of Equine Veterinary Science, 8, 168-170. https://doi.org/10.1016/S0737-0806(88)80043-1 DOI: https://doi.org/10.1016/S0737-0806(88)80043-1
Wilson, J. D. (2001). The role of 5-reduction in steroid hormone physiology. Reproduction, Fertility and Development, 13, 673. https://doi.org/10.1071/RD01074 DOI: https://doi.org/10.1071/RD01074
Downloads
Published
How to Cite
License
Copyright (c) 2022 Journal of Experimental Biology and Agricultural Sciences
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.