Influence of thermal stress during in vitro maturation on the developmental competence of oocytes and embryos and the expression of Sirtuins in cumulus oocyte complexes in cattle
DOI:
https://doi.org/10.5433/1679-0359.2025v46n1p149Keywords:
Sirtuins, Temperature, IVP, Bos taurus, Heat stress.Abstract
Sirtuins are of central importance in many cellular functions and promote cell survival under stress. However, little information is available regarding the relationship between sirtuins and female reproductive biology, especially in response to thermal stress. This study investigated the influence of moderately high (40°C) and low (37°C) thermal stress during in vitro maturation on the development competence of bovine oocytes and embryos. The expression and abundance of sirtuins and other proteins involved in stress response were also studied. The cumulus-oocyte complexes (COCs) of Simmental (Bos taurus) cows underwent in vitro maturation (IVM) at different temperatures (37°C, 38.5°C and 40°C). Before maturation, the oocytes were stained with Brilliant Cresyl Blue (BCB) and categorized as labeled (BCB+) or unlabeled (BCB-). Embryo production was analyzed at the different IVM temperatures. Polar body extrusion was evaluated following IVM, and the mRNA and protein abundance of sirtuins and P53 in oocytes and cumulus cells were analyzed. The differing temperatures during IVM did not significantly alter polar body extrusion and cleavage rates; however, significant differences in blastocyst production were observed. COCs matured at 38.5°C (control, 37.3%) had the highest blastocyst rate, in contrast to those matured at 37°C (33.2%) and 40°C (21.5%). In all groups, the blastocyst rates were higher for BCB+ oocytes than for BCB- oocytes. In BCB+ oocytes, the expression of SIRT1, SIRT2, SIRT3, and SIRT5 genes was higher after maturation than that before maturation and in most of the cases, the expression was higher when IVM was performed at 38.5°C. In the cumulus cells of BCB+ COCs, only SIRT2 remained unaffected by the maturation temperature. In summary, the temperature change of ±1.5°C for 24 h during bovine oocyte maturation impaired in vitro embryo development. This lead to several cellular biochemical alterations in oocytes and granulosa cells from COCs with higher developmental competence (BCB+). Thus, SIRT1 is important for in vitro embryonic development and may protect against cold and heat stress.
Downloads
References
Adamkova, K., Yi, Y.-J., Petr, J., Zalmanova, T., Hoskova, K., Jelinkova, P., Moravec, J., Kralickova, M., Sutovsky, M., Sutovsky, P., & Nevoral, J. (2017). SIRT1-dependent modulation of methylation and acetylation of histone H3 on lysine 9 (H3K9) in the zygotic pronuclei improves porcine embryo development. Journal of Animal Science and Biotechnology, 8(83), 1-12. doi: 10.1186/s40104-017-0214-0 DOI: https://doi.org/10.1186/s40104-017-0214-0
Alm, H., Torner, H., Löhrke, B., Viergutz, T., Ghoneim, I. M., & Kanitz, W. (2005). Bovine blastocyst development rate in vitro is influenced by selection of oocytes by brillant cresyl blue staining before IVM as indicator for glucose-6-phosphate dehydrogenase activity. Theriogenology, 63(8), 2194-2205. doi: 10.1016/j.theriogenology.2004.09.050 DOI: https://doi.org/10.1016/j.theriogenology.2004.09.050
Andrade Melo-Sterza, F. de, & Poehland, R. (2021). Lipid metabolism in bovine oocytes and early embryos under in vivo, in vitro, and stress conditions. International Journal of Molecular Sciences, 22(7), 3421. doi: 10.3390/ijms22073421 DOI: https://doi.org/10.3390/ijms22073421
Aubrey, B. J., Kelly, G. L., Janic, A., Herold, M. J., & Strasser, A. (2018). How does p53 induce apoptosis and how does this relate to p53-mediated tumour suppression? Cell Death & Differentiation, 25(1), 104-113. doi: 10.1038/cdd.2017.169 DOI: https://doi.org/10.1038/cdd.2017.169
Bai, W., & Zhang, X. (2016). Nucleus or cytoplasm? The mysterious case of SIRT1’s subcellular localization. Cell Cycle, 15(24), 3337-3338. doi: 10.1080/15384101.2016.1237170 DOI: https://doi.org/10.1080/15384101.2016.1237170
Baufeld, A., Koczan, D., & Vanselow, J. (2019). L-lactate induces specific genome wide alterations of gene expression in cultured bovine granulosa cells. BMC Genomics, 20(273), 1-11. doi: 10.1186/s12864-019-5657-6 DOI: https://doi.org/10.1186/s12864-019-5657-6
Baur, J. A., Ungvari, Z., Minor, R. K., Le Couteur, D. G., & Cabo, R. de. (2012). Are sirtuins viable targets for improving healthspan and lifespan? Nature Reviews. Drug Discovery, 11(6), 443-461. doi: 10.1038/nrd3738 DOI: https://doi.org/10.1038/nrd3738
Bhojwani, S., Alm, H., Torner, H., Kanitz, W., & Poehland, R. (2007). Selection of developmentally competent oocytes through brilliant cresyl blue stain enhances blastocyst development rate after bovine nuclear transfer. Theriogenology, 67(2), 341-345. doi: 10.1016/j.theriogenology.2006.08.006 DOI: https://doi.org/10.1016/j.theriogenology.2006.08.006
Blondin, P., & Sirard, M. A. (1995). Oocyte and follicular morphology as determining characteristics for developmental competence in bovine oocytes. Molecular Reproduction and Development, 41(1), 54-62. doi: 10.1002/mrd.1080410109 DOI: https://doi.org/10.1002/mrd.1080410109
Cao, Y., Zhao, H., Wang, Z., Zhang, C., Bian, Y., Liu, X., Zhang, C., Zhang, X., & Zhao, Y. (2020). Quercetin promotes in vitro maturation of oocytes from humans and aged mice. Cell Death & Disease, 11(11), 965. doi: 10.1038/s41419-020-03183-5 DOI: https://doi.org/10.1038/s41419-020-03183-5
Chen, B., Zang, W., Wang, J., Huang, Y., He, Y., Yan, L., Liu, J., & Zheng, W. (2015). The chemical biology of sirtuins. Chemical Society Reviews, 44(15), 5246-5264. doi: 10.1039/c4cs00373j DOI: https://doi.org/10.1039/C4CS00373J
Conti, M., & Franciosi, F. (2018). Acquisition of oocyte competence to develop as an embryo: integrated nuclear and cytoplasmic events. Human Reproduction Update, 24(3), 245-266. doi: 10.1093/humupd/dmx040 DOI: https://doi.org/10.1093/humupd/dmx040
Da Broi, M. G., Giorgi, V. S. I., Wang, F., Keefe, D. L., Albertini, D., & Navarro, P. A. (2018). Influence of follicular fluid and cumulus cells on oocyte quality: clinical implications. Journal of Assisted Reproduction and Genetics, 35(5), 735-751. doi: 10.1007/s10815-018-1143-3 DOI: https://doi.org/10.1007/s10815-018-1143-3
Edwards, J. L., & Hansen, P. J. (1997). Differential responses of bovine oocytes and preimplantation embryos to heat shock. Molecular Reproduction and Development, 46(2), 138-145. doi: 10.1002/(SICI)1098-2795(199702)46:2<138::AID-MRD4>3.0.CO;2-R DOI: https://doi.org/10.1002/(SICI)1098-2795(199702)46:2<138::AID-MRD4>3.0.CO;2-R
Grabowska, W., Sikora, E., & Bielak-Zmijewska, A. (2017). Sirtuins, a promising target in slowing down the ageing process. Biogerontology, 18(4), 447-476. doi: 10.1007/s10522-017-9685-9 DOI: https://doi.org/10.1007/s10522-017-9685-9
Halvaei, I., Khalili, M. A., Soleimani, M., & Razi, M. H. (2011). Evaluating the role of first polar body morphology on rates of fertilization and embryo development in ICSI cycles. International Journal of Fertility & Sterility, 5(2), 110-115. PMID: 24963368; PMCID: PMC4059947
Hori, Y. S., Kuno, A., Hosoda, R., & Horio, Y. (2013). Regulation of FOXOs and p53 by SIRT1 modulators under oxidative stress. PloS One, 8(9), e73875. doi: 10.1371/journal.pone.0073875 DOI: https://doi.org/10.1371/journal.pone.0073875
Ju, J. C., Parks, J. E., & Yang, X. (1999). Thermotolerance of IVM-derived bovine oocytes and embryos after short-term heat shock. Molecular Reproduction and Development, 53(3), 336-340. doi: 10.1002/(SICI)1098-2795(199907)53:3<336::AID-MRD9>3.0.CO;2-M DOI: https://doi.org/10.1002/(SICI)1098-2795(199907)53:3<336::AID-MRD9>3.3.CO;2-D
Leibfried, L., & First, N. L. (1979). Characterization of bovine follicular oocytes and their ability to mature in vitro. Journal of Animal Science, 48(1), 76-86. doi: 10.2527/jas1979.48176x DOI: https://doi.org/10.2527/jas1979.48176x
Madison, V., Avery, B., & Greve, T. (1992). Selection of immature bovine oocytes for developmental potential in vitro. Animal Reproduction Science, 27(1), 1-11. doi: 10.1016/0378-4320(92)90065-L DOI: https://doi.org/10.1016/0378-4320(92)90065-L
Nabenishi, H., Ohta, H., Nishimoto, T., Morita, T., Ashizawa, K., & Tsuzuki, Y. (2012a). The effects of cysteine addition during in vitro maturation on the developmental competence, ROS, GSH and apoptosis level of bovine oocytes exposed to heat stress. Zygote, 20(3), 249-259. doi: 10.1017/S0967199411000220 DOI: https://doi.org/10.1017/S0967199411000220
Nabenishi, H., Takagi, S., Kamata, H., Nishimoto, T., Morita, T., Ashizawa, K., & Tsuzuki, Y. (2012b). The role of mitochondrial transition pores on bovine oocyte competence after heat stress, as determined by effects of cyclosporin A. Molecular Reproduction and Development, 79(1), 31-40. doi: 10.1002/mrd.21401 DOI: https://doi.org/10.1002/mrd.21401
Nakagawa, T., & Guarente, L. (2011). Sirtuins at a glance. Journal of Cell Science, 124(6), 833-838. doi: 10.1242/jcs.081067 DOI: https://doi.org/10.1242/jcs.081067
Ong, A. L. C., & Ramasamy, T. S. (2018). Role of Sirtuin1-p53 regulatory axis in aging, cancer and cellular reprogramming. Ageing Research Reviews, 43, 64-80. doi: 10.1016/j.arr.2018.02.004 DOI: https://doi.org/10.1016/j.arr.2018.02.004
Paula-Lopes, F. F., Lima, R. S., Satrapa, R. A., & Barros, C. M. (2013). Physiology and endocrinology symposium: influence of cattle genotype (Bos indicus vs. Bos taurus) on oocyte and preimplantation embryo resistance to increased temperature. Journal of Animal Science, 91(3), 1143-1153. doi: 10.2527/jas.2012-5802 DOI: https://doi.org/10.2527/jas.2012-5802
Pujol, M., López-Béjar, M., & Paramio, M. T. (2004). Developmental competence of heifer oocytes selected using the brilliant cresyl blue (BCB) test. Theriogenology, 61(4), 735-744. doi: 10.1016/s0093-691x(03)00250-4 DOI: https://doi.org/10.1016/S0093-691X(03)00250-4
Rato, L., Alves, M. G., Silva, B. M., Sousa, M., & Oliveira, P. F. (2016). Sirtuins: novel players in male reproductive health. Current Medicinal Chemistry, 23(11), 1084-1099. doi: 10.2174/0929867323666160229114248 DOI: https://doi.org/10.2174/0929867323666160229114248
Reader, K. L., Stanton, J.-A. L., & Juengel, J. L. (2017). The role of oocyte organelles in determining developmental competence. Biology, 6(35), 1-22. doi: 10.3390/biology6030035 DOI: https://doi.org/10.3390/biology6030035
Ren, F., Yang, M., Liu, G., Qi, Y., Li, A., Li, J., & Zheng, L. (2024). SIRT5-mediated PRKAA2 succinylation ameliorates apoptosis of human placental trophoblasts in hypertensive disorder complicating pregnancy. Clinical and Experimental Hypertension, 46(1), 2358030. doi: 10.1080/10641963.2024.2358030 DOI: https://doi.org/10.1080/10641963.2024.2358030
Rispoli, L. A., Payton, R. R., Gondro, C., Saxton, A. M., Nagle, K. A., Jenkins, B. W., Schrick, F. N., & Edwards, J. L. (2013). Heat stress effects on the cumulus cells surrounding the bovine oocyte during maturation: altered matrix metallopeptidase 9 and progesterone production. Reproduction, 146(2), 193-207. doi: 10.1530/REP-12-0487 DOI: https://doi.org/10.1530/REP-12-0487
Rodríguez-González, E., López-Béjar, M., Velilla, E., & Paramio, M. T. (2002). Selection of prepubertal goat oocytes using the brilliant cresyl blue test. Theriogenology, 57(5), 1397-1409. doi: 10.1016/s0093-691x(02)00645-3 DOI: https://doi.org/10.1016/S0093-691X(02)00645-3
Roth, Z., & Hansen, P. J. (2005). Disruption of nuclear maturation and rearrangement of cytoskeletal elements in bovine oocytes exposed to heat shock during maturation. Reproduction, 129(2), 235-244. doi: 10.1530/rep.1.00394 DOI: https://doi.org/10.1530/rep.1.00394
Salviano, M. B., Collares, F. J. F., Becker, B. S., Rodrigues, B. A., & Rodrigues, J. L. (2016). Bovine non-competent oocytes (BCB-) negatively impact the capacity of competent (BCB+) oocytes to undergo in vitro maturation, fertilisation and embryonic development. Zygote, 24(2), 245-251. doi: 10.1017/S09671 99415000118 DOI: https://doi.org/10.1017/S0967199415000118
Silva, D. S., Rodriguez, P., Galuppo, A., Arruda, N. S., & Rodrigues, J. L. (2013). Selection of bovine oocytes by brilliant cresyl blue staining: Effect on meiosis progression, organelle distribution and embryo development. Zygote, 21(3), 250-255. doi: 10.1017/S0967199411000487 DOI: https://doi.org/10.1017/S0967199411000487
Singh, C. K., Chhabra, G., Ndiaye, M. A., Garcia-Peterson, L. M., Mack, N. J., & Ahmad, N. (2018). The role of sirtuins in antioxidant and redox signaling. Antioxidants & Redox Signaling, 28(8), 643-661. doi: 10.1089/ars.2017.7290 DOI: https://doi.org/10.1089/ars.2017.7290
Tatone, C., Di Emidio, G., Vitti, M., Di Carlo, M., Santini, S., D’Alessandro, A. M., Falone, S., & Amicarelli, F. (2015). Sirtuin functions in female fertility: possible role in oxidative stress and aging. Oxidative Medicine and Cellular Longevity, 2015(659687), 1-11. doi: 10.1155/2015/659687 DOI: https://doi.org/10.1155/2015/659687
Thompson, J. G., Lane, M., & Gilchrist, R. B. (2007). Metabolism of the bovine cumulus-oocyte complex and influence on subsequent developmental competence. Society of Reproduction and Fertility Supplement, 64, 179-190. doi: 10.5661/rdr-vi-179 DOI: https://doi.org/10.5661/RDR-VI-179
Vousden, K. H. (2000). p53: death star. Cell, 103(5), 691-694. doi: 10.1016/s0092-8674(00)00171-9 DOI: https://doi.org/10.1016/S0092-8674(00)00171-9
Wang, H., Jo, Y.-J., Oh, J. S., & Kim, N.-H. (2017). Quercetin delays postovulatory aging of mouse oocytes by regulating SIRT expression and MPF activity. Oncotarget, 8(24), 38631-38641. doi: 10.18632/oncotarget.16219 DOI: https://doi.org/10.18632/oncotarget.16219
Yenuganti, V. R., & Vanselow, J. (2017). Cultured bovine granulosa cells rapidly lose important features of their identity and functionality but partially recover under long-term culture conditions. Cell and Tissue Research, 368(2), 397-403. doi: 10.1007/s00441-017-2571-6 DOI: https://doi.org/10.1007/s00441-017-2571-6
Yi, J., & Luo, J. (2010). SIRT1 and p53, effect on cancer, senescence and beyond. Biochimica et Biophysica Acta, 1804(8), 1684-1689. doi: 10.1016/j.bbapap.2010.05.002 DOI: https://doi.org/10.1016/j.bbapap.2010.05.002
Zeng, H., He, X., Tuo, Q.-H., Liao, D.-F., Zhang, G.-Q., & Chen, J.-X. (2016). LPS causes pericyte loss and microvascular dysfunction via disruption of Sirt3/angiopoietins/Tie-2 and HIF-2α/Notch3 pathways.Scientific Reports, 6(20931), 1-13. doi: 10.1038/srep20931 DOI: https://doi.org/10.1038/srep20931
Zhang, Q., Siyuan, Z., Xing, C., & Ruxiu, L. (2024). SIRT3 regulates mitochondrial function: a promising star target for cardiovascular disease therapy. Biomedicine & Pharmacotherapy, 170(116004). doi: 10.1016/j.biopha.2023.116004 DOI: https://doi.org/10.1016/j.biopha.2023.116004
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2024 Ralf Pöhland, Mirela Brochado Souza-Cáceres, Tirtha Kumar Datta, Jens Vanselow, Wilian Aparecido Leite da Silva, Christopher Junior Tavares Cardoso, Fabiana de Andrade Melo Sterza
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Semina: Ciências Agrárias adopts the CC-BY-NC license for its publications, the copyright being held by the author, in cases of republication we recommend that authors indicate first publication in this journal.
This license allows you to copy and redistribute the material in any medium or format, remix, transform and develop the material, as long as it is not for commercial purposes. And due credit must be given to the creator.
The opinions expressed by the authors of the articles are their sole responsibility.
The magazine reserves the right to make normative, orthographic and grammatical changes to the originals in order to maintain the cultured standard of the language and the credibility of the vehicle. However, it will respect the writing style of the authors. Changes, corrections or suggestions of a conceptual nature will be sent to the authors when necessary.
Funding data
-
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Grant numbers 88881.068117/2014-01 -
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Grant numbers 001
