Medium and time conservation affect follicular morphology and superoxide dismutase enzyme activity of bovine preantral follicles during storage at 4ºC
DOI:
https://doi.org/10.5433/1679-0359.2020v41n4p1227Keywords:
Ovary, Oxidative stress, Preservation.Abstract
The aim of this study was to evaluate the morphology and superoxide dismutase enzyme (SOD) activity of bovine preantral follicles (PFs) preserved in TCM 199, saline solution or PBS at different conservation periods. Cow ovaries (n=6) were divided into 7 fragments. One small piece of each ovarian fragment was randomly removed to evaluate SOD activity, while the remainder was immediately fixed for morphological evaluation as a control group. The other 6 fragments were randomly distributed in tubes containing TCM 199, saline solution, or PBS and maintained at 4ºC for 6 or 24 h. For histological evaluation, the fragments were fixed in Carnoy and stained with PAS-hematoxylin, following being classified PFs in relation to their follicular morphology in normal or degenerated. Determination of SOD activity was based on the ability to inhibit autoxidation of adrenaline in adrenochrome. Evaluation of follicular morphology showed that follicles preserved in TCM 199 for 6 h did not differ from the control (P > 0.05). In contrast, preservation in saline solution and PBS for 6 or 24 h and TCM 199 for 24 h decreased normal PFs compared to the control (P < 0.05). SOD showed a lower activity in ovarian cortical tissue kept in TCM 199 for 6 h and saline solution for 24 h than in the other groups. Our study shows that incubation using TCM 199 at 4°C for 6 h can be used to efficiently conserve female bovine PFs in situ.References
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Barberino, R. S., Silva, J. R. V., Figueiredo, J. R., & Matos, M. H. T. (2019). Transport of domestic and wild animal ovaries: a review of the effects of medium, temperature, and periods of storage on follicular viability. Biopreservation and Biobanking, 17(1), 84-90. doi: 10.1089/bio.2018.0057
Carvalho, F. C., Lucci, C. M., Silva, J. R., Andrade, E. R., Báo, S. N., & Figueiredo, J. R. (2001). Effect of Braun-Collins and Saline solutions at different temperatures and incubation times on the quality of goat preantral follicles preserved in situ. Animal Reproducion Science, 66(3-4), 195-208. doi: 10.1016/S0378-4320(01)00085-9
Celestino, J. J. H., Santos, R. R., Martins, F. S., Matos, M. H. T., Figueiredo, J. R., Costa, S. H. F.,... Rodrigues, A. P. R. (2007). Conservação de folículos pré-antrais bovinos em solução salina 0,9% ou TCM 199. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 59(3), 591-599. doi: 10.1590/S0102-09352007000300007
Combelles, C. M., Holick, E. A., Paolella, L. J., Walker, D. C., & Wu, Q. (2010). Profiling of superoxide dismutase isoenzymes in compartments of the developing bovine antral follicles. Reproduction, 139(5), 871-881. doi: 10.1530/REP-09-0390
Costa, S. H. F., Santos, R. R., Ferreira, M. A. L., Machado, V. P., Rodrigues, A. P. R., Ohashi, O. M., & Figueiredo, J. R. (2002). Preservation of goat preantral follicles in saline or coconut water solution. Brazilian Journal of Veterinary Research and Animal Science, 39(6), 324-330. doi: 10.1590/S1413-95962002000600009
Ferreira, M. A., Brasil, A. F., Silva, J. R., Andrade, E. R., Rodrigues, A. P., & Figueiredo, J. R. (2001). Effects of storage time and temperature on atresia of goat ovarian preantral follicles held in M199 with or without indole-3-acetic acid supplementation. Theriogenology, 55(8), 1607-1617. doi: 10.1016/s0093-691x(01)00506-4
Figueiredo, J. R., Rodrigues, A. P. R., & Amorin, C. A. (2008). Manipulação de oócitos inclusos em folículos ovarianos pré-antrais. In P. B. D. Gonçalves, J. R. Figueiredo & Freitas V. J. F. (Ed.), Biotécnicas aplicadas à reprodução animal (pp. 303-328). São Paulo: Roca.
Gigli, I., Byrd, D. D., & Fortune, J. E. (2006). Effects of oxygen tension and supplements to the culture medium on activation and development of bovine follicles in vitro. Theriogenology, 66(2), 344-353. doi: 10.1016/j.theriogenology.2005.11.021
Hulshof, S. C. J., Figueiredo, J. R., Beckers, J. F., Bevers, M. M., & Van Den Hurk, R. (1994). Isolation and characterization of preantral follicles from foetal bovine ovaries. The Veterinary Quarterly, 16(2), 78-80. doi: 10.1080/01652176.1994.9694423
Lima-Verde, I. B., Matos, M. H. T., Bruno, J. B., Martins, F. S., Santos, R. R., Báo, S. N.,… Lima, P. F. (2009). Effects of α-tocopherol and ternatin antioxidants on morphology and activation of goat preantral follicles in vitro cultured. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 61(1), 57-65. doi: 10.1590/S0102-09352009000100009
Lucci, C. M., Amorim, C. A., Rodrigues, A. P., Figueiredo, J. R., Báo, S. N., Silva, J. R., & Gonçalves, P. B. (1999). Study of preantral follicle population in situ and after mechanical isolation from caprine ovaries at different reproductive stages. Animal Reproduction Science, 56(3-4), 223-236. doi: 10.1016/s0378-4320(99)00045-7
Lucci, C. M., Kacinskis, M. A., Rumpf, R., & Báo, S. N. (2004). Effects of lowered temperatures and media on short-term preservation of zebu (Bos indicus) preantral ovarian follicles. Theriogenology, 61(2-3), 461-472. doi: 10.1016/s0093-691x(03)00226-7
Matos, M. H. T., Andrade, E. R., Lucci, C. M., Bao, C. N., Silva, J. R. V., Santos, R. R.,… Figueiredo, J. R. (2004). Morphological and ultrastructural analysis of sheep primordial follicles preserved in 0.9% saline solution and TCM 199. Theriogenology, 62(1-2), 65-80. doi: 10.1016/j.theriogenology.2003.07.025
Matzuk, M. M., Dionne, L., Guo, Q., Kumar, T. R., & Lebovitz, R. M. (1998). Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology, 139(9), 4008-4011. doi: 10.1210/endo.139.9.6289
Mclaughlin, M., Bromfield, J. J., Albertini, D. F., & Telfer, E. E. (2010). Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Molecular Human Reproduction, 16(9), 644-653. doi: 10.1093/molehr/gaq021
Migliorisi, G., Folkes, E., Pawlowski, N., & Cramer, E. B. (1987). In vitro studies of human monocyte migration across endothelium in response to leukotriene B4 and f-Met-Leu-Phe. The American Journal of Pathology, 127(1), 157-167.
Misra, H. P., & Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. The Journal of Biological Chemistry, 47(10), 3170-3175.
Missio, D., Rosa, F. Q., Guimarães, A. C. G., Leivas, F. G., & Brum, D. S. (2014). Conservação de folículos pré-antrais de felinos domésticos (Felis catus) refrigerados por 24 h em TCM 199 e PBS. Revista Brasileira de Reprodução Animal, 38(3), 176-181.
Paynter, S. J. (2000). Current status of the cryopreservation of human unfertilized oocytes. Human Reproducion Update, 6(5), 449-456. doi: 10.1093/humupd/6.5.449
Salehi, P., Spratlin, J., Chong, T. F., & Churchill, T. A. (2004). Beneficial effects of supplemental buffer and substrate on energy metabolism during small bowel storage. Cryobiology, 48(3), 245-253. doi: 10.1016/j.cryobiol.2004.01.008
Santos, R. R., Silva, J. R. V., Costa, S. H. F., Rodrigues, A. P. R., Lôbo, R. N. B., & Figueiredo, J. R. (2002). Effect of 0.9% saline solution and phosphate buffer saline at different temperatures and incubation times on the morphology of goat preantral follicles. Brazilian Journal of Veterinary Research and Animal Science, 39(5), 254-259. doi: 10.1590/S1413-95962002000500007
Sugino, N. (2007). The role of oxygen radical-mediated signaling pathways in endometrial function. Placenta, 28(Suppl.), 133-136. doi: 10.1016/j.placenta.2006.12.002
Sun, Y., Oberley, L. W., & Li, Y. (1998). A simple method for clinical assay of superoxide dismutase. Clinical Chemistry, 34(3), 497-500. doi: 10.1093/clinchem/34.3.497
Suzuki, T., Sugino, N., Fukaya, T., Sugiyama, S., Uda, T., Takaya, R.,… Sasano, H. (1999). Superoxide dismutase in normal cycling human ovaries: immunohistochemical localization and characterization. Fertility and Sterility, 72(4), 720-726.doi: 10.1016/s0015-0282(99)00332-5
Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T., Mazur, M., & Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. The International Journal of Biochemistry and Cell Biology, 39(1), 44-84. doi: 10.1016/j.biocel.2006.07.001
Wang, S., He, G., Cheng, M., Zuo, T., Xu, W., & Liu, X. (2017). The role of antioxidant enzymes in the ovaries. Oxidative Medicine and Cellular Longevity, 2017(2017), 1-14. doi: 10.1155/2017/4371714
Zhang, J. M., Wang, H. C., Wang, H. X., Ruan, L. H., Zhang, Y. M., Li, J. T.,… Zhang, Y. C. (2013). Oxidative stress and activities of caspase-8, -9, and -3 are involved in cryopreservation-induced apoptosis in granulosa cells. European Journal of Obstetrics and Gynecology and Reproductive Biology, 166(1), 52-55. doi: 10.1016/j.ejogrb.2012.09.011
Andrade, E. R., Amorim, C. A., Costa, S. H. F., Ferreira, M. A. L., Rodrigues, A. R. R., Dode, M. A. N., & Figueiredo, J. R. (2002). Preliminary study of short-term preservation of ovine ovarian tissue containing preantral follicles in saline solution of TCM199. The Veterinary Record, 151(15), 452-453. doi: 10.1136/vr.151.15.452
Barberino, R. S., Silva, J. R. V., Figueiredo, J. R., & Matos, M. H. T. (2019). Transport of domestic and wild animal ovaries: a review of the effects of medium, temperature, and periods of storage on follicular viability. Biopreservation and Biobanking, 17(1), 84-90. doi: 10.1089/bio.2018.0057
Carvalho, F. C., Lucci, C. M., Silva, J. R., Andrade, E. R., Báo, S. N., & Figueiredo, J. R. (2001). Effect of Braun-Collins and Saline solutions at different temperatures and incubation times on the quality of goat preantral follicles preserved in situ. Animal Reproducion Science, 66(3-4), 195-208. doi: 10.1016/S0378-4320(01)00085-9
Celestino, J. J. H., Santos, R. R., Martins, F. S., Matos, M. H. T., Figueiredo, J. R., Costa, S. H. F.,... Rodrigues, A. P. R. (2007). Conservação de folículos pré-antrais bovinos em solução salina 0,9% ou TCM 199. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 59(3), 591-599. doi: 10.1590/S0102-09352007000300007
Combelles, C. M., Holick, E. A., Paolella, L. J., Walker, D. C., & Wu, Q. (2010). Profiling of superoxide dismutase isoenzymes in compartments of the developing bovine antral follicles. Reproduction, 139(5), 871-881. doi: 10.1530/REP-09-0390
Costa, S. H. F., Santos, R. R., Ferreira, M. A. L., Machado, V. P., Rodrigues, A. P. R., Ohashi, O. M., & Figueiredo, J. R. (2002). Preservation of goat preantral follicles in saline or coconut water solution. Brazilian Journal of Veterinary Research and Animal Science, 39(6), 324-330. doi: 10.1590/S1413-95962002000600009
Ferreira, M. A., Brasil, A. F., Silva, J. R., Andrade, E. R., Rodrigues, A. P., & Figueiredo, J. R. (2001). Effects of storage time and temperature on atresia of goat ovarian preantral follicles held in M199 with or without indole-3-acetic acid supplementation. Theriogenology, 55(8), 1607-1617. doi: 10.1016/s0093-691x(01)00506-4
Figueiredo, J. R., Rodrigues, A. P. R., & Amorin, C. A. (2008). Manipulação de oócitos inclusos em folículos ovarianos pré-antrais. In P. B. D. Gonçalves, J. R. Figueiredo & Freitas V. J. F. (Ed.), Biotécnicas aplicadas à reprodução animal (pp. 303-328). São Paulo: Roca.
Gigli, I., Byrd, D. D., & Fortune, J. E. (2006). Effects of oxygen tension and supplements to the culture medium on activation and development of bovine follicles in vitro. Theriogenology, 66(2), 344-353. doi: 10.1016/j.theriogenology.2005.11.021
Hulshof, S. C. J., Figueiredo, J. R., Beckers, J. F., Bevers, M. M., & Van Den Hurk, R. (1994). Isolation and characterization of preantral follicles from foetal bovine ovaries. The Veterinary Quarterly, 16(2), 78-80. doi: 10.1080/01652176.1994.9694423
Lima-Verde, I. B., Matos, M. H. T., Bruno, J. B., Martins, F. S., Santos, R. R., Báo, S. N.,… Lima, P. F. (2009). Effects of α-tocopherol and ternatin antioxidants on morphology and activation of goat preantral follicles in vitro cultured. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 61(1), 57-65. doi: 10.1590/S0102-09352009000100009
Lucci, C. M., Amorim, C. A., Rodrigues, A. P., Figueiredo, J. R., Báo, S. N., Silva, J. R., & Gonçalves, P. B. (1999). Study of preantral follicle population in situ and after mechanical isolation from caprine ovaries at different reproductive stages. Animal Reproduction Science, 56(3-4), 223-236. doi: 10.1016/s0378-4320(99)00045-7
Lucci, C. M., Kacinskis, M. A., Rumpf, R., & Báo, S. N. (2004). Effects of lowered temperatures and media on short-term preservation of zebu (Bos indicus) preantral ovarian follicles. Theriogenology, 61(2-3), 461-472. doi: 10.1016/s0093-691x(03)00226-7
Matos, M. H. T., Andrade, E. R., Lucci, C. M., Bao, C. N., Silva, J. R. V., Santos, R. R.,… Figueiredo, J. R. (2004). Morphological and ultrastructural analysis of sheep primordial follicles preserved in 0.9% saline solution and TCM 199. Theriogenology, 62(1-2), 65-80. doi: 10.1016/j.theriogenology.2003.07.025
Matzuk, M. M., Dionne, L., Guo, Q., Kumar, T. R., & Lebovitz, R. M. (1998). Ovarian function in superoxide dismutase 1 and 2 knockout mice. Endocrinology, 139(9), 4008-4011. doi: 10.1210/endo.139.9.6289
Mclaughlin, M., Bromfield, J. J., Albertini, D. F., & Telfer, E. E. (2010). Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Molecular Human Reproduction, 16(9), 644-653. doi: 10.1093/molehr/gaq021
Migliorisi, G., Folkes, E., Pawlowski, N., & Cramer, E. B. (1987). In vitro studies of human monocyte migration across endothelium in response to leukotriene B4 and f-Met-Leu-Phe. The American Journal of Pathology, 127(1), 157-167.
Misra, H. P., & Fridovich, I. (1972). The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. The Journal of Biological Chemistry, 47(10), 3170-3175.
Missio, D., Rosa, F. Q., Guimarães, A. C. G., Leivas, F. G., & Brum, D. S. (2014). Conservação de folículos pré-antrais de felinos domésticos (Felis catus) refrigerados por 24 h em TCM 199 e PBS. Revista Brasileira de Reprodução Animal, 38(3), 176-181.
Paynter, S. J. (2000). Current status of the cryopreservation of human unfertilized oocytes. Human Reproducion Update, 6(5), 449-456. doi: 10.1093/humupd/6.5.449
Salehi, P., Spratlin, J., Chong, T. F., & Churchill, T. A. (2004). Beneficial effects of supplemental buffer and substrate on energy metabolism during small bowel storage. Cryobiology, 48(3), 245-253. doi: 10.1016/j.cryobiol.2004.01.008
Santos, R. R., Silva, J. R. V., Costa, S. H. F., Rodrigues, A. P. R., Lôbo, R. N. B., & Figueiredo, J. R. (2002). Effect of 0.9% saline solution and phosphate buffer saline at different temperatures and incubation times on the morphology of goat preantral follicles. Brazilian Journal of Veterinary Research and Animal Science, 39(5), 254-259. doi: 10.1590/S1413-95962002000500007
Sugino, N. (2007). The role of oxygen radical-mediated signaling pathways in endometrial function. Placenta, 28(Suppl.), 133-136. doi: 10.1016/j.placenta.2006.12.002
Sun, Y., Oberley, L. W., & Li, Y. (1998). A simple method for clinical assay of superoxide dismutase. Clinical Chemistry, 34(3), 497-500. doi: 10.1093/clinchem/34.3.497
Suzuki, T., Sugino, N., Fukaya, T., Sugiyama, S., Uda, T., Takaya, R.,… Sasano, H. (1999). Superoxide dismutase in normal cycling human ovaries: immunohistochemical localization and characterization. Fertility and Sterility, 72(4), 720-726.doi: 10.1016/s0015-0282(99)00332-5
Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T., Mazur, M., & Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. The International Journal of Biochemistry and Cell Biology, 39(1), 44-84. doi: 10.1016/j.biocel.2006.07.001
Wang, S., He, G., Cheng, M., Zuo, T., Xu, W., & Liu, X. (2017). The role of antioxidant enzymes in the ovaries. Oxidative Medicine and Cellular Longevity, 2017(2017), 1-14. doi: 10.1155/2017/4371714
Zhang, J. M., Wang, H. C., Wang, H. X., Ruan, L. H., Zhang, Y. M., Li, J. T.,… Zhang, Y. C. (2013). Oxidative stress and activities of caspase-8, -9, and -3 are involved in cryopreservation-induced apoptosis in granulosa cells. European Journal of Obstetrics and Gynecology and Reproductive Biology, 166(1), 52-55. doi: 10.1016/j.ejogrb.2012.09.011
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2020-05-13
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Ramos, M. A. G., Leivas, F. G., Missio, D., Cibin, F. W. S., Guimarães, A. C. G., & Brum, D. dos S. (2020). Medium and time conservation affect follicular morphology and superoxide dismutase enzyme activity of bovine preantral follicles during storage at 4ºC. Semina: Ciências Agrárias, 41(4), 1227–1236. https://doi.org/10.5433/1679-0359.2020v41n4p1227
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