Does resveratrol preserve the integrity of the sperm membrane in goats after thawing?
DOI:
https://doi.org/10.5433/1679-0359.2020v41n6Supl2p3189Keywords:
Antioxidants, Oxidative stress, Sperm, TRIS-egg yolk.Abstract
This study aimed to determine the effects of resveratrol in the trisaminomethane (TRIS)-egg yolk extender and its optimal inclusion level for goat semen cryopreservation. Five ejaculates of three Anglo Nubian goats were used, each divided into four 200 µL aliquots for use in four treatments: 0.00 (control), 0.04, 0.08 and 0.12 mg mL-1 resveratrol in the TRIS-egg yolk extender. We evaluated progressive sperm motility and sperm vigor post-dilution, post-cooling, and post thawing; membrane integrity (HOST); and acrosomal integrity and performed a slow thermoresistance test (STT). The data were submitted to a regression analysis at a 5% probability. There was no difference in progressive motility or sperm vigor in the post-dilution (89.5, 89.0, 88.7 and 88.3, and 4.9, 5.0, 4.9, and 4.9) or post-cooling (81.0, 82.0, 83.0, and 78.3; and 4.3, 4.3, 4.2, and 4.2) experiments (P > 0.05), or in the complementary acrosomal integrity test (42.0, 47.4, 42.2 and 38.2) (P > 0.05). However, the motility and vigor parameters decreased linearly in the post-thaw phase, as well as during the 2 hours of incubation on STT (P < 0.05). These factors increased quadratically when resveratrol was added to HOST, to an optimal level of 0.039 mg mL-1 resveratrol for a plasma membrane integrity of 52.55% (P < 0.05). The inclusion of resveratrol was effective in maintaining sperm viability; in particular, it was effective in maintaining plasmatic membrane integrity during the cryopreservation process up to 0.039 mg mL-1, meaning that it could be an alternative to conventionally used seminal extenders in goats.Downloads
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References
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Brito, L. S., Barbosa, L. P., Resende, M. V., Pinheiro, A. M., França, C. S., & Cardoso, R. C. (2017). Ácido ascórbico no diluidor para criopreservação de sêmen caprino. Ciência Animal Brasileira, 18(1-10), e-40117. doi: 10.1590/1089-6891v18e-40117
Bucak, M. N., Tuncer, P. B., Sariozkan, S., Ulutas, P. A., Coyan, K., Baspinar, N., & Ozkalp, B. (2009). Effects of hypotaurine, cysteamine and aminoacids solution on post-thaw microscopic and oxidative stress parameters of Angora goat semen. Research in Veterinary Science, 87(3), 468-472. doi: 10.1016/ j.rvsc.2009.04.014
Carrizzo, A., Forte, M., Damato, A., Trimarco, V., Salzano, F., Bartolo, M.,... Vecchione, C. (2013). Antioxidant effects of resveratrol in cardiovascular, cerebral and metabolic diseases. Food and Chemical Toxicology, 61(1), 215-226. doi: 10.1016/j.fct.2013.07.021
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Collodel, G., Federico, M. G., Geminiani, M., Martini, S., Bonechi, C., Rossi, C.,... Moretti, E. (2011). Effect of trans-resveratrol on induced oxidative stress in human sperm and in rat germinal cells. Reproductive Toxicology, 31(2), 239-246. doi: 10.1016/j.reprotox.2010.11.010
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Garcez, M. E., Branco, C. S., Lara, L. V., Pasqualotto, F. F., & Salvador, M. (2010). Effects of resveratrol supplementation on cryopreservation medium of human semen. Fertility and Sterility, 94(6), 2118-2121. doi: 10.1016/j.fertnstert.2010.01.058
Guerra, M. M. P., Evans, G., & Maxwell, W. M. C. (2004). Papel de oxidantes e antioxidantes na andrologia. Revista Brasileira de Reprodução Animal, 28(4), 187-195. Recovered from: http://www.cbra.org.br/ pages/publicacoes/rbra/download/v28n4.pdf
Henry, M., Neves, J. P., & Jobim, M. I. M. (2013). Manual para exame andrológico e avaliação de sêmen animal. In M. Henry, J. P. Neves, & M. I. M. Jobim, Caprinos (3a ed., pp. 39-42). Belo Horizonte: Colégio Brasileiro de Reprodução Animal.
Kao, S. H., Chao, H. T., Chen, H. W., Hwang, T. I. S., Liao, T. L., & Wei, Y. H. (2008). Increase of oxidative stress in human sperm with lower motility. Fertility and Sterility, 89(5), 1183-1190. doi: 10. 1016/j.fertnstert.2007.05.029
Kasdallah-Grissa, A., Mornagui, B., Aouani, E., Hammami, M., May, M. E., Gharbi, N.,… El-Fazaâ, S. (2007). Resveratrol, a red wine polyphenol, attenuates ethanol-induced oxidative stress in rat liver. Life Sciences, 80(11), 1033-1039. doi: 10.1016/j.lfs.2006.11.044
Kennedy, J. H., Korn, N., & Thurston, R. J. (2003). Prostaglandins levels in seminal plasma and sperm extracts of the domestic turkey, and the effects of cyclooxigenase inhibitors on sperm motility. Reproductive Biology and Endocrinology, 74(1), 1-7. doi: 10.1186/1477-7827-1-74
Longobardi, V., Zullo, G., Salzano, A., Canditiis, C., Cammarano, A., Luise, L.,... Gasparrini, B. (2017). Resveratrol prevents capacitation-like changes and improves in vitro fertilizing capability of buffalo frozen-thawed sperm. Theriogenology, 88(1), 1-8. doi: 10.1016/j.theriogenology.2016.09.046
Memon, A. A., Wahid, H., Rosnina, Y., Goh, Y. M., Ebrahimi, M., & Nadia, F. (2012). Effect of antioxidants on post thaw microscopic, oxidative stress parameter and fertility of Boer goat spermatozoa in Tris egg yolk glycerol extender. Animal Reproduction Science, 136(1-2), 55-60. doi: 10.1016/j. anireprosci.2012.10.020
Nickel, A., Kohlhaas, M., & Maack, C. (2014). Mitochondrial reactive oxygen species production and elimination. Journal of Molecular and Cellular Cardiology, 73(1), 26-33. doi: 10.1016/j.yjmcc.2014. 03.011
Ourique, G. M., Finamor, I. A., Saccol, E. M. H., Riffel, A. P. K., Pês, T. S., Gutierrez, K.,... Barreto, K. P. (2013). Resveratrol improves sperm motility, prevents lipid peroxidation and enhances antioxidant defences in the testes of hyperthyroid rats. Reproductive Toxicology, 37(1), 31-39. doi: 10.1016/j. reprotox.2013.01.006
Peris, S. I., Bilodeau, J.-F., Dufour, M., & Bailey, J. L. (2007). Impact of Cryopreservation and reactive oxygen species on DNA inetgrity, lipid peroxidation, and functional parameters in ram sperm. Molecular Reproduction and Development, 74(7), 878-892. doi: 10.1002/mrd.20686
Pope, C. E., Zhang, Y. Z., & Dresser, B. L. (1991). A simple staining method for valuating acrosomal status of cat spermatozoa. Journal of Zoo and Wildlife Medicine, 22(1), 87-95. Recovered from: https://www. jstor.org/stable/20095123
Purdy, P. H. (2006). A review on goat sperm cryopreservation. Small Ruminant Research, 63(3), 215-225. doi: 10.1016/j.smallrumres.2005.02.015
Resende, J., & Weitze, K. F. (1987). Congelamento de sêmen de caprino com diluente TRIS modificado. Anais da Reunião Anual da Sociedade Brasileira de Zootecnia. Anais do Simpósio Sobre Reprodução Animal, Brasília, DF, Brasil, 24, 4.
Santiani, A., Evangelista, S., Sepúlveda, N., Risopatrón, J., Villegas, J., & Sánchez, R. (2014). Addition of superoxide dismutase mimics during cooling process prevents oxidative stress and improves semen quality parameters in frozen/thawed ram spermatozoa. Theriogenology, 82(6), 884-889. doi: 10.1016/j. theriogenology.2014.07.002
Sarlós, P., Molnár, A., Kókai, M., Gábor, G., & Rátky, J. (2002). Comparative evaluation of the effect of antioxidants in the conservation of ram semen. Acta Veterinaria Hungarica, 50(2), 235-245. doi: 10. 1556/AVet.50.2002.2.13
Sassi, N., Mattarei, A., Azzolini, M., Szabò, I., Paradisi, C., Zoratti, M., & Biasutto, L. (2014). Cytotoxicity of mitochondria-targeted resveratrol derivatives: Interactions with respiratory chain complexes and ATP synthase. Biochimica et Biophysica Acta, 1837(10), 1781-1789. doi: 10.1016/j.bbabio.2014.06.010
Schmatz, R., Perreira, L. B., Stefanello, N., Mazzanti, C., Spanevello, R., Gutierres, J.,… Morsch, V. M. (2012). Effects of resveratrol on biomarkers of oxidative stress and on the activity of delta aminolevulinic acid dehydratase in liver and kidney of streptozotocin-induced diabetic rats. Biochimie, 94(2), 374-383. doi: 10.1016/j.biochi.2011.08.005
Shamsi, M. B., Kumar, R., Bhatt, A., Bamezai, R. N. K., Kumar, R., Gupta, N. P.,… Dada, R. (2008). Mitochondrial DNA Mutations in etiopathogenesis of male infertility. Indian Journal of Urology, 24(2), 150-154. doi: 10.4103/0970-1591.40606
Sicherle, C. C., Maia, M. S., Bicudo, S. D., Rodello, L., & Gallego, I. C. (2011). Lipid peroxidation and generation of hydrogen peroxide in frozen-thawed ram semen supplemented with catalase or Trolox. Small Ruminant Research, 95(2-3), 144-149. doi: 10.1016/j.smallrumres.2010.10.011
Silva, E. C. B., Cajueiro, J. F. P., Silva, S. V., Soares, P. C., & Guerra, M. M. P. (2012). Effect of antioxidants resveratrol and quercetin on in vitro viability of frozen ram sperm. Theriogenology, 77(8), 1722-1726. doi: 10.1016/j.theriogenology.2011.11.023
Statistical Analysis System Institute (2003). User’s guide. Version 9.1.3 for Windows. Cary, NC: USA.
Stojanović, S., Sprinz, H., & Brede, O. (2001). Efficiency and mechanism of the antioxidant action of trans-resveratrol and its analogues in the radical liposome oxidation. Archives of Biochemistry and Biophysics, 391(1), 79-89. doi: 10.1006/abbi.2001.2388
Talini, R., Kozicki, L. E., Gaievski, F. R., Polo, G., Lima, L. G. F., Santiago, J.,... Galan, T. G. B. (2019). Bovine semen thermoresistance tests and their correlation with pregnancy rates after fixed-time artificial insemination. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 71(6), 2085-2092. doi: 10.1590/ 1678-4162-10994
Watson, P. F. (2000). The causes of reduced fertility with cryopreserved semen. Animal Reproduction Science, 60-61(1), 481-492. doi: 10.1016/S0378-4320(00)00099-3
Xiang, L., Xiao, L., Wang, Y., Li, H., Huang, Z., & He, X. (2014). Health benefits of wine: don’t expect resveratrol too much. Food Chemistry, 156(1), 258-263. doi: 10.1016/j.foodchem.2014.01.006
Aitken, R. J., Muscio, L., Whiting, S., Connaughton, H. S., Fraser, B. A., Nixon, B.,… De Iuliis, G. N. (2016). Analysis of the effects of polyphenols on human spermatozoa reveals unexpected impacts on mitochondrial membrane potential, oxidative stress and DNA integrity; implications for assisted reproductive technology. Biochemical Pharmacology, 121(1), 78-96. doi: 10.1016/j.bcp.2016.09.015
Bittencourt, R. F., Ribeiro, A. L. Fo, Santos, A. D. F., Chalhoub, M., Alves, S. G. G., Vasconcelos, M. F.,... Guimarães, J. D. (2005). Utilização do teste hiposmótico para avaliar a eficácia de diferentes protocolos de criopreservação do sêmen caprino. Ciência Animal Brasileira, 6(3), 213-218. Recovered from: https://www.revistas.ufg.br/vet/article/view/362
Brito, L. S., Barbosa, L. P., Resende, M. V., Pinheiro, A. M., França, C. S., & Cardoso, R. C. (2017). Ácido ascórbico no diluidor para criopreservação de sêmen caprino. Ciência Animal Brasileira, 18(1-10), e-40117. doi: 10.1590/1089-6891v18e-40117
Bucak, M. N., Tuncer, P. B., Sariozkan, S., Ulutas, P. A., Coyan, K., Baspinar, N., & Ozkalp, B. (2009). Effects of hypotaurine, cysteamine and aminoacids solution on post-thaw microscopic and oxidative stress parameters of Angora goat semen. Research in Veterinary Science, 87(3), 468-472. doi: 10.1016/ j.rvsc.2009.04.014
Carrizzo, A., Forte, M., Damato, A., Trimarco, V., Salzano, F., Bartolo, M.,... Vecchione, C. (2013). Antioxidant effects of resveratrol in cardiovascular, cerebral and metabolic diseases. Food and Chemical Toxicology, 61(1), 215-226. doi: 10.1016/j.fct.2013.07.021
Cézar, M. F., & Souza, W. H. (2006). Avaliação e utilização da condição corporal como ferramenta de melhoria da reprodução e produção de ovinos e caprinos de corte. Anais da Reunião Anual da Sociedade Brasileira de Zootecnia, João Pessoa, PB, Brasil, 43.
Collodel, G., Federico, M. G., Geminiani, M., Martini, S., Bonechi, C., Rossi, C.,... Moretti, E. (2011). Effect of trans-resveratrol on induced oxidative stress in human sperm and in rat germinal cells. Reproductive Toxicology, 31(2), 239-246. doi: 10.1016/j.reprotox.2010.11.010
Delmas, D., Jannin, B., & Latruffe, N. (2005). Resveratrol: Preventing properties against vascular alterations and ageing. Molecular Nutrition & Food Research, 49(5), 377-395. doi: 10.1002/mnfr.200400098
Garcez, M. E., Branco, C. S., Lara, L. V., Pasqualotto, F. F., & Salvador, M. (2010). Effects of resveratrol supplementation on cryopreservation medium of human semen. Fertility and Sterility, 94(6), 2118-2121. doi: 10.1016/j.fertnstert.2010.01.058
Guerra, M. M. P., Evans, G., & Maxwell, W. M. C. (2004). Papel de oxidantes e antioxidantes na andrologia. Revista Brasileira de Reprodução Animal, 28(4), 187-195. Recovered from: http://www.cbra.org.br/ pages/publicacoes/rbra/download/v28n4.pdf
Henry, M., Neves, J. P., & Jobim, M. I. M. (2013). Manual para exame andrológico e avaliação de sêmen animal. In M. Henry, J. P. Neves, & M. I. M. Jobim, Caprinos (3a ed., pp. 39-42). Belo Horizonte: Colégio Brasileiro de Reprodução Animal.
Kao, S. H., Chao, H. T., Chen, H. W., Hwang, T. I. S., Liao, T. L., & Wei, Y. H. (2008). Increase of oxidative stress in human sperm with lower motility. Fertility and Sterility, 89(5), 1183-1190. doi: 10. 1016/j.fertnstert.2007.05.029
Kasdallah-Grissa, A., Mornagui, B., Aouani, E., Hammami, M., May, M. E., Gharbi, N.,… El-Fazaâ, S. (2007). Resveratrol, a red wine polyphenol, attenuates ethanol-induced oxidative stress in rat liver. Life Sciences, 80(11), 1033-1039. doi: 10.1016/j.lfs.2006.11.044
Kennedy, J. H., Korn, N., & Thurston, R. J. (2003). Prostaglandins levels in seminal plasma and sperm extracts of the domestic turkey, and the effects of cyclooxigenase inhibitors on sperm motility. Reproductive Biology and Endocrinology, 74(1), 1-7. doi: 10.1186/1477-7827-1-74
Longobardi, V., Zullo, G., Salzano, A., Canditiis, C., Cammarano, A., Luise, L.,... Gasparrini, B. (2017). Resveratrol prevents capacitation-like changes and improves in vitro fertilizing capability of buffalo frozen-thawed sperm. Theriogenology, 88(1), 1-8. doi: 10.1016/j.theriogenology.2016.09.046
Memon, A. A., Wahid, H., Rosnina, Y., Goh, Y. M., Ebrahimi, M., & Nadia, F. (2012). Effect of antioxidants on post thaw microscopic, oxidative stress parameter and fertility of Boer goat spermatozoa in Tris egg yolk glycerol extender. Animal Reproduction Science, 136(1-2), 55-60. doi: 10.1016/j. anireprosci.2012.10.020
Nickel, A., Kohlhaas, M., & Maack, C. (2014). Mitochondrial reactive oxygen species production and elimination. Journal of Molecular and Cellular Cardiology, 73(1), 26-33. doi: 10.1016/j.yjmcc.2014. 03.011
Ourique, G. M., Finamor, I. A., Saccol, E. M. H., Riffel, A. P. K., Pês, T. S., Gutierrez, K.,... Barreto, K. P. (2013). Resveratrol improves sperm motility, prevents lipid peroxidation and enhances antioxidant defences in the testes of hyperthyroid rats. Reproductive Toxicology, 37(1), 31-39. doi: 10.1016/j. reprotox.2013.01.006
Peris, S. I., Bilodeau, J.-F., Dufour, M., & Bailey, J. L. (2007). Impact of Cryopreservation and reactive oxygen species on DNA inetgrity, lipid peroxidation, and functional parameters in ram sperm. Molecular Reproduction and Development, 74(7), 878-892. doi: 10.1002/mrd.20686
Pope, C. E., Zhang, Y. Z., & Dresser, B. L. (1991). A simple staining method for valuating acrosomal status of cat spermatozoa. Journal of Zoo and Wildlife Medicine, 22(1), 87-95. Recovered from: https://www. jstor.org/stable/20095123
Purdy, P. H. (2006). A review on goat sperm cryopreservation. Small Ruminant Research, 63(3), 215-225. doi: 10.1016/j.smallrumres.2005.02.015
Resende, J., & Weitze, K. F. (1987). Congelamento de sêmen de caprino com diluente TRIS modificado. Anais da Reunião Anual da Sociedade Brasileira de Zootecnia. Anais do Simpósio Sobre Reprodução Animal, Brasília, DF, Brasil, 24, 4.
Santiani, A., Evangelista, S., Sepúlveda, N., Risopatrón, J., Villegas, J., & Sánchez, R. (2014). Addition of superoxide dismutase mimics during cooling process prevents oxidative stress and improves semen quality parameters in frozen/thawed ram spermatozoa. Theriogenology, 82(6), 884-889. doi: 10.1016/j. theriogenology.2014.07.002
Sarlós, P., Molnár, A., Kókai, M., Gábor, G., & Rátky, J. (2002). Comparative evaluation of the effect of antioxidants in the conservation of ram semen. Acta Veterinaria Hungarica, 50(2), 235-245. doi: 10. 1556/AVet.50.2002.2.13
Sassi, N., Mattarei, A., Azzolini, M., Szabò, I., Paradisi, C., Zoratti, M., & Biasutto, L. (2014). Cytotoxicity of mitochondria-targeted resveratrol derivatives: Interactions with respiratory chain complexes and ATP synthase. Biochimica et Biophysica Acta, 1837(10), 1781-1789. doi: 10.1016/j.bbabio.2014.06.010
Schmatz, R., Perreira, L. B., Stefanello, N., Mazzanti, C., Spanevello, R., Gutierres, J.,… Morsch, V. M. (2012). Effects of resveratrol on biomarkers of oxidative stress and on the activity of delta aminolevulinic acid dehydratase in liver and kidney of streptozotocin-induced diabetic rats. Biochimie, 94(2), 374-383. doi: 10.1016/j.biochi.2011.08.005
Shamsi, M. B., Kumar, R., Bhatt, A., Bamezai, R. N. K., Kumar, R., Gupta, N. P.,… Dada, R. (2008). Mitochondrial DNA Mutations in etiopathogenesis of male infertility. Indian Journal of Urology, 24(2), 150-154. doi: 10.4103/0970-1591.40606
Sicherle, C. C., Maia, M. S., Bicudo, S. D., Rodello, L., & Gallego, I. C. (2011). Lipid peroxidation and generation of hydrogen peroxide in frozen-thawed ram semen supplemented with catalase or Trolox. Small Ruminant Research, 95(2-3), 144-149. doi: 10.1016/j.smallrumres.2010.10.011
Silva, E. C. B., Cajueiro, J. F. P., Silva, S. V., Soares, P. C., & Guerra, M. M. P. (2012). Effect of antioxidants resveratrol and quercetin on in vitro viability of frozen ram sperm. Theriogenology, 77(8), 1722-1726. doi: 10.1016/j.theriogenology.2011.11.023
Statistical Analysis System Institute (2003). User’s guide. Version 9.1.3 for Windows. Cary, NC: USA.
Stojanović, S., Sprinz, H., & Brede, O. (2001). Efficiency and mechanism of the antioxidant action of trans-resveratrol and its analogues in the radical liposome oxidation. Archives of Biochemistry and Biophysics, 391(1), 79-89. doi: 10.1006/abbi.2001.2388
Talini, R., Kozicki, L. E., Gaievski, F. R., Polo, G., Lima, L. G. F., Santiago, J.,... Galan, T. G. B. (2019). Bovine semen thermoresistance tests and their correlation with pregnancy rates after fixed-time artificial insemination. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 71(6), 2085-2092. doi: 10.1590/ 1678-4162-10994
Watson, P. F. (2000). The causes of reduced fertility with cryopreserved semen. Animal Reproduction Science, 60-61(1), 481-492. doi: 10.1016/S0378-4320(00)00099-3
Xiang, L., Xiao, L., Wang, Y., Li, H., Huang, Z., & He, X. (2014). Health benefits of wine: don’t expect resveratrol too much. Food Chemistry, 156(1), 258-263. doi: 10.1016/j.foodchem.2014.01.006
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2020-11-06
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Brito, L. S., Barbosa, L. P., Pinheiro, A. M., Resende, M. V., Costa, N. G. de L., Machado, W. M., … Cardoso, R. de C. (2020). Does resveratrol preserve the integrity of the sperm membrane in goats after thawing?. Semina: Ciências Agrárias, 41(6Supl2), 3189–3198. https://doi.org/10.5433/1679-0359.2020v41n6Supl2p3189
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