Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-05T07:49:45.013Z Has data issue: false hasContentIssue false
  • English
  • Français

β-Mercaptoethanol in culture medium improves cryotolerance of in vitro-produced bovine embryos

Published online by Cambridge University Press:  23 September 2022

Karine de Mattos ,
Camilo Andrés Pena-Bello Open the ORCID record for Camilo Andrés Pena-Bello [Opens in a new window] ,
Karine Campagnolo ,
Gabriella Borba de Oliveira ,
Elvis Ticiani ,
César Augusto Pinzón-Osorio ,
Ana Laura da Silva Feijó ,
Higor da Silva Ferreira ,
José Luiz Rodrigues  and
Marcelo Bertolini
...Show all authors
Karine de Mattos
Affiliation:
School of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Camilo Andrés Pena-Bello
Affiliation:
School of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Karine Campagnolo
Affiliation:
School of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Gabriella Borba de Oliveira
Affiliation:
School of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Elvis Ticiani
Affiliation:
School of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
César Augusto Pinzón-Osorio
Affiliation:
School of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Ana Laura da Silva Feijó
Affiliation:
School of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Higor da Silva Ferreira
Affiliation:
School of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
José Luiz Rodrigues
Affiliation:
School of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Marcelo Bertolini
Affiliation:
School of Veterinary Medicine, Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil
Alceu Mezzallira
Affiliation:
Center of Agroveterinarian Sciences, Santa Catarina State University, Lages, SC, Brazil
Eduardo de Souza Ribeiro*
Affiliation:
Center of Agroveterinarian Sciences, Santa Catarina State University, Lages, SC, Brazil
*
Author for correspondence: Eduardo de Souza Ribeiro. Department of Animal Biosciences, University of Guelph, Guelph, ON, CanadaN1G 2W1. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The objective of this study was to investigate the effects of adding β-mercaptoethanol (βME) to culture medium of bovine in vitro-produced (IVP) embryos prior to or after vitrification on embryo development and cryotolerance. In Experiment I, Day-7 IVP blastocysts were vitrified and, after warming, cultured in medium containing 0, 50 or 100 μM βME for 72 h. Embryos cultured in 100 μM βME attained higher hatching rates (66.7%) than those culture in 0 (47.7%) and 50 (52.4%) μM βME. In Experiment II, IVP embryos were in vitro-cultured (IVC) to the blastocyst stage in 0 (control) or 100 μM βME, followed by vitrification. After warming, embryos were cultured for 72 h (post-warming culture, PWC) in 0 (control) or 100 μM βME, in a 2 × 2 factorial design: (i) CTRL–CTRL, control IVC and control PWC; (ii) CTRL–βME, control IVC and βME-supplemented PWC; (iii) βME–CTRL, βME-supplemented IVC and control PWC; or (iv) βME–βME, βME-supplemented IVC and βME-supplemented PWC. βME during IVC reduced embryo development (28.0% vs. 43.8%) but, following vitrification, higher re-expansion rates were seen in βME–CTRL (84.0%) and βME–βME (87.5%) than in CTRL–CTRL (71.0%) and CTRL–βME (73.1%). Hatching rates were higher in CTRL–βME (58.1%) and βME–βME (63.8%) than in CTRL–CTRL (36.6%) and βME–CTRL (42.0%). Total cell number in hatched blastocysts was higher in βME–βME (181.2 ± 7.4 cells) than CTRL–CTRL (139.0 ± 9.9 cells). Adding βME to the IVC medium reduced development but increased cryotolerance, whereas adding βME to the PWC medium improved embryo survival, hatching rates, and total cell numbers.

Keywords

AntioxidantCattleCryopreservationCryosurvivalIVP embryo
Type
Research Article
Information
Zygote , Volume 30 , Issue 6 , December 2022 , pp. 830 - 840
Copyright
© The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

Present address: Department of Animal Biosciences, University of Guelph, Guelph, ON, Canada N1G 2W1

References

Abe, H., Yamashita, S., Satoh, T. and Hoshi, H. (2002). Accumulation of cytoplasmic lipid droplets in bovine embryos and cryotolerance of embryos developed in different culture systems using serum-free or serum-containing media. Molecular Reproduction and Development, 61(1), 57–66. doi: 10.1002/mrd.1131 CrossRefGoogle ScholarPubMed
Agarwal, A., Sharma, R. K., Nallella, K. P., Thomas, A. J., Alvarez, J. G. and Sikka, S. C. (2006). Reactive oxygen species as an independent marker of male factor infertility. Fertility and Sterility, 86(4), 878–885. doi: 10.1016/j.fertnstert.2006.02.111 CrossRefGoogle ScholarPubMed
Bain, N. T., Madan, P. and Betts, D. H. (2011). The early embryo response to intracellular reactive oxygen species is developmentally regulated. Reproduction, Fertility, and Development, 23(4), 561–575. doi: 10.1071/RD10148 CrossRefGoogle ScholarPubMed
Balakier, H., Sojecki, A., Motamedi, G., Bashar, S., Mandel, R. and Librach, C. (2012). Is the zona pellucida thickness of human embryos influenced by women’s age and hormonal levels? Fertility and Sterility, 98(1), 77–83. doi: 10.1016/j.fertnstert.2012.04.015 CrossRefGoogle ScholarPubMed
Barcroft, L. C., Hay-Schmidt, A., Caveney, A., Gilfoyle, E., Overstrom, E. W., Hyttel, P. and Watson, A. J. (1998). Trophectoderm differentiation in the bovine embryo: Characterization of a polarized epithelium. Journal of Reproduction and Fertility, 114(2), 327–339. doi: 10.1530/jrf.0.1140327 CrossRefGoogle ScholarPubMed
Budani, M. C. and Tiboni, G. M. (2020). Effects of supplementation with natural antioxidants on oocytes and preimplantation embryos. Antioxidants, 9(7), 612–637. doi: 10.3390/antiox9070612 CrossRefGoogle ScholarPubMed
Caamaño, J. N., Ryoo, Z. Y. and Youngs, C. R. (1998). Promotion of development of bovine embryos produced in vitro by addition of cysteine and β-mercaptoethanol to a chemically defined culture system. Journal of Dairy Science, 81(2), 369–374. doi: 10.3168/jds.S0022-0302(98)75586-9 CrossRefGoogle ScholarPubMed
Castillo-Martín, M., Yeste, M., Pericuesta, E., Morató, R., Gutiérrez-Adán, A. and Bonet, S. (2015). Effects of vitrification on the expression of pluripotency, apoptotic and stress genes in in vitro-produced porcine blastocysts. Reproduction, Fertility, and Development, 27(7), 1072–1081. doi: 10.1071/RD13405 CrossRefGoogle ScholarPubMed
Cleland, W. W. (1964). Dithiothreitol a new protective reagent for SH groups. Biochemistry, 3, 480–482. doi: 10.1021/bi00892a002 CrossRefGoogle ScholarPubMed
Cornell, N. W. and Crivaro, K. E. (1972). Stability constant for the zinc-dithiothreitol complex. Analytical Biochemistry, 47, 203–208. doi: 10.1016/0003-2697(72)90293-x CrossRefGoogle ScholarPubMed
de Castro e Paula, L. A. and Hansen, P. J. (2008). Modification of actions of heat shock on development and apoptosis of cultured preimplantation bovine embryos by oxygen concentration and dithiothreitol. Molecular Reproduction and Development, 75(8), 1338–1350. doi: 10.1002/mrd.20866 CrossRefGoogle ScholarPubMed
de Matos, D. G. and Furnus, C. C. (2000). The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development: Effect of b-mercaptoethanol, cysteine and cystine. Theriogenology, 53(3), 761–771. doi: 10.1016/S0093-691X(99)00278-2 CrossRefGoogle Scholar
de Matos, D. G., Furnus, C. C., Moses, D. F., Martinez, A. G. and Matkovic, M. (1996). Stimulation of glutathione synthesis of in vitro matured bovine oocytes and its effect on embryo development and freezability. Molecular Reproduction and Development, 45(4), 451–457. doi: 10.1002/(SICI)1098-2795(199612)45:4<451::AID-MRD7>3.0.CO;2-Q 3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Deleuze, S. and Goudet, G. (2010). Cysteamine supplementation of in vitro maturation media: A review. Reproduction in Domestic Animals, 45(6), e476–e482. doi: 10.1111/j.1439-0531.2010.01587.x CrossRefGoogle ScholarPubMed
Feugang, J. M., Van Langendonckt, A., Sayoud, H., Rees, J. F., Pampfer, S., Moens, A., Dessy, F. and Donnay, I. (2003). Effect of prooxidant agents added at the morula/blastocyst stage on bovine embryo development, cell death and glutathione content. Zygote, 11(2), 107–118. doi: 10.1017/s0967199403002144 CrossRefGoogle ScholarPubMed
Feugang, J. M., de Roover, R., Moens, A., Léonard, S., Dessy, F. and Donnay, I. (2004). Addition of β-mercaptoethanol or Trolox® at the morula/blastocyst stage improves the quality of bovine blastocysts and prevents induction of apoptosis and degeneration by prooxidant agents. Theriogenology, 61(1), 71–90. doi: 10.1016/S0093-691X(03)00191-2 CrossRefGoogle Scholar
Fleming, T. P., Warren, P. D., Chisholm, J. C. and Johnson, M. H. (1984). Trophectodermal processes regulate the expression of totipotency within the inner cell mass of the mouse expanding blastocyst. Journal of Embryology and Experimental Morphology, 84, 63–90. doi: 10.1242/dev.84.1.63 Google ScholarPubMed
Geshi, M., Yonai, M., Sakaguchi, M. and Nagai, T. (1999). Improvement of in vitro co-culture systems for bovine embryos using a low concentration of carbon dioxide and medium supplemented with beta-mercaptoethanol. Theriogenology, 51(3), 551–558. doi: 10.1016/s0093-691x(99)00009-6 CrossRefGoogle ScholarPubMed
Giorgi, V. S. I., Ferriani, R. A. and Navarro, P. A. (2021). Follicular fluid from infertile women with mild endometriosis impairs in vitro bovine embryo development: Potential role of oxidative stress. Revista Brasileira de Ginecologia e Obstetrícia: revista da Federação Brasileira das Sociedades de Ginecologia e Obstetrícia, 43(2), 119–125. doi: 10.1055/s-0040-1718443 Google ScholarPubMed
Goissis, M. D. and Cibelli, J. B. (2014). Functional characterization of CDX2 during bovine preimplantation development in vitro . Molecular Reproduction and Development, 81(10), 962–970. doi: 10.1002/mrd.22415 CrossRefGoogle ScholarPubMed
Gómez, E., Carrocera, S., Martín, D., Pérez-Jánez, J. J., Prendes, J., Prendes, J. M., Vázquez, A., Murillo, A., Gimeno, I. and Muñoz, M. (2020). Efficient one-step direct transfer to recipients of thawed bovine embryos cultured in vitro and frozen in chemically defined medium. Theriogenology, 146, 39–47. doi: 10.1016/j.theriogenology.2020.01.056 CrossRefGoogle ScholarPubMed
Goud, P. T., Goud, A. P., Joshi, N., Puscheck, E., Diamond, M. P. and Abu-Soud, H. M. (2014). Dynamics of nitric oxide, altered follicular microenvironment, and oocyte quality in women with endometriosis. Fertility and Sterility, 102(1), 151–159.e5. doi: 10.1016/j.fertnstert.2014.03.053 CrossRefGoogle ScholarPubMed
Guérin, P., El Mouatassim, S. and Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Human Reproduction Update, 7(2), 175–189. doi: 10.1093/humupd/7.2.175 CrossRefGoogle ScholarPubMed
Guo, Y., Mantel, C., Hromas, R. A. and Broxmeyer, H. E. (2008). Oct-4 is critical for survival/antiapoptosis of murine embryonic stem cells subjected to stress: Effects associated with Stat3/survivin. Stem Cells, 26(1), 30–34. doi: 10.1634/stemcells.2007-0401 CrossRefGoogle ScholarPubMed
Holm, P., Booth, P. J., Schmidt, M. H., Greve, T. and Callesen, H. (1999). High bovine blastocyst development in a static in vitro production system using SOFaa medium supplemented with sodium citrate and myo-inositol with or without serum proteins. Theriogenology, 52(4), 683–700. doi: 10.1016/S0093-691X(99)00162-4 CrossRefGoogle ScholarPubMed
Hosseini, S. M., Forouzanfar, M., Hajian, M., Asgari, V., Abedi, P., Hosseini, L., Ostadhosseini, S., Moulavi, F., Safahani Langrroodi, M., Sadeghi, H., Bahramian, H., Eghbalsaied, Sh and Nasr-Esfahani, M. H. (2009). Antioxidant supplementation of culture medium during embryo development and/or after vitrification-warming; which is the most important? Journal of Assisted Reproduction and Genetics, 26(6), 355–364. doi: 10.1007/s10815-009-9317-7 CrossRefGoogle ScholarPubMed
Jamil, M., Debbarh, H., Aboulmaouahib, S., Aniq Filali, O., Mounaji, K., Zarqaoui, M., Saadani, B., Louanjli, N. and Cadi, R. (2020). Reactive oxygen species in reproduction: harmful, essential or both? Zygote, 28(4), 255–269. doi: 10.1017/S0967199420000179 CrossRefGoogle ScholarPubMed
Johnson, M. H. and Nasr-Esfahani, M. H. (1994). Radical solutions and cultural problems: Could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 16(1), 31–38. doi: 10.1002/bies.950160105 CrossRefGoogle ScholarPubMed
Khanmohammadi, N., Movahedin, M., Safari, M., Sameni, H. R., Yousefi, B., Jafari, B. and Zarbakhsh, S. (2016). Effect of l-carnitine on in vitro developmental rate, the zona pellucida and hatching of blastocysts and their cell numbers in mouse embryos. International Journal of Reproductive Biomedicine, 14(10), 649–656. doi: 10.29252/ijrm.14.10.649 Google ScholarPubMed
Leme, L. O., Carvalho, J. O., Franco, M. M. and Dode, M. A. N. (2020). Effect of sex on cryotolerance of bovine embryos produced in vitro . Theriogenology, 141, 219–227. doi: 10.1016/j.theriogenology.2019.05.002 CrossRefGoogle ScholarPubMed
Lin, J. and Wang, L. (2020). Oxidative stress in oocytes and embryo development: Implications for in vitro systems. Antioxidants and Redox Signaling, 34, 1394–1406. doi: 10.1089/ars.2020.8209 CrossRefGoogle Scholar
Liu, L., Trimarchi, J. R. and Keefe, D. L. (1999). Thiol oxidation-induced embryonic cell death in mice is prevented by the antioxidant dithiothreitol. Biology of Reproduction, 61(4), 1162–1169. doi: 10.1095/biolreprod61.4.1162 CrossRefGoogle ScholarPubMed
Lonergan, P., Rizos, D., Gutierrez-Adan, A., Fair, T. and Boland, M. P. (2003). Oocyte and embryo quality: Effect of origin, culture conditions and gene expression patterns. Reproduction in Domestic Animals, 38(4), 259–267. doi: 10.1046/j.1439-0531.2003.00437.x CrossRefGoogle ScholarPubMed
Lopes, A. S., Lane, M. and Thompson, J. G. (2010). Oxygen consumption and ROS production are increased at the time of fertilization and cell cleavage in bovine zygotes. Human Reproduction, 25(11), 2762–2773. doi: 10.1093/humrep/deq221 CrossRefGoogle ScholarPubMed
Mori, M., Otoi, T., Wongsrikeao, P., Agung, B. and Nagai, T. (2006). Effects of beta-mercaptoethanol and cycloheximide on survival and DNA damage of bovine embryos stored at 4°C for 72 h. Theriogenology, 65(7), 1322–1332. doi: 10.1016/j.theriogenology.2005.07.018 CrossRefGoogle ScholarPubMed
Moussa, M., Yang, C. Y., Zheng, H. Y., Li, M. Q., Yu, N. Q., Yan, S. F., Huang, J. X. and Shang, J. H. (2019). Vitrification alters cell adhesion related genes in pre-implantation buffalo embryos: Protective role of β-mercaptoethanol. Theriogenology, 125, 317–323. doi: 10.1016/j.theriogenology.2018.11.013 CrossRefGoogle ScholarPubMed
Nada, A. M., El-Noury, A., Al-Inany, H., Bibars, M., Taha, T., Salama, S., Hassan, F. and Zein, E. (2018). Effect of laser-assisted zona thinning, during assisted reproduction, on pregnancy outcome in women with endometriosis: Randomized controlled trial. Archives of Gynecology and Obstetrics, 297(2), 521–528. doi: 10.1007/s00404-017-4604-5 CrossRefGoogle ScholarPubMed
Nedambale, T. L., Du, F., Yang, X. and Tian, X. C. (2006). Higher survival rate of vitrified and thawed in vitro produced bovine blastocysts following culture in defined medium supplemented with β-mercaptoethanol. Animal Reproduction Science, 93(1–2), 61–75. doi: 10.1016/j.anireprosci.2005.06.027 CrossRefGoogle ScholarPubMed
Nganvongpanit, K., Müller, H., Rings, F., Gilles, M., Jennen, D., Hölker, M., Tholen, E., Schellander, K. and Tesfaye, D. (2006). Targeted suppression of E-cadherin gene expression in bovine preimplantation embryo by RNA interference technology using double-stranded RNA. Molecular Reproduction and Development, 73(2), 153–163. doi: 10.1002/mrd.20406 CrossRefGoogle ScholarPubMed
Nikseresht, M., Toori, M. A., Rahimi, H. R., Fallahzadeh, A. R., Kahshani, I. R., Hashemi, S. F., Bahrami, S. and Mahmoudi, R. (2017). Effect of antioxidants (β-mercaptoethanol and cysteamine) on assisted reproductive technology in vitro . Journal of Clinical and Diagnostic Research, 11(2), BC10–BC14. doi: 10.7860/JCDR/2017/21778.9298 Google ScholarPubMed
Rashidipour, N., Karami-Mohajeri, S., Mandegary, A., Mohammadinejad, R., Wong, A., Mohit, M., Salehi, J., Ashrafizadeh, M., Najafi, A. and Abiri, A. (2020). Where ferroptosis inhibitors and paraquat detoxification mechanisms intersect, exploring possible treatment strategies. Toxicology, 433–434, 152407. doi: 10.1016/j.tox.2020.152407 CrossRefGoogle ScholarPubMed
Ray, P. D., Huang, B. W. and Tsuji, Y. (2012). Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cellular Signaling, 24(5), 981–990. doi: 10.1016/j.cellsig.2012.01.008 CrossRefGoogle ScholarPubMed
Ribeiro, E. S., Gerger, R. P., Ohlweiler, L. U., Ortigari, I., Jr., Mezzalira, J. C., Forell, F., Bertolini, L. R., Rodrigues, J. L., Ambrósio, C. E., Miglino, M. A., Mezzalira, A. and Bertolini, M. (2009). Developmental potential of bovine hand-made clone embryos reconstructed by aggregation or fusion with distinct cytoplasmic volumes. Cloning and Stem Cells, 11(3), 377–386. doi: 10.1089/clo.2009.0022 CrossRefGoogle ScholarPubMed
Ribeiro, E. S., Galvão, K. N., Thatcher, W. W. and Santos, J. E. P. (2012). Economic aspects of applying reproductive technologies to dairy herds. Animal Reproduction, 9, 370–387.Google Scholar
Rizos, D., Ward, F., Duffy, P., Boland, M. P. and Lonergan, P. (2002). Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: Implications for blastocyst yield and blastocyst quality. Molecular Reproduction and Development, 61(2), 234–248. doi: 10.1002/mrd.1153 CrossRefGoogle ScholarPubMed
Rocha-Frigoni, N. A., Leão, B. C., Nogueira, É., Accorsi, M. F. and Mingoti, G. Z. (2014). Reduced levels of intracellular reactive oxygen species and apoptotic status are not correlated with increases in cryotolerance of bovine embryos produced in vitro in the presence of antioxidants. Reproduction, Fertility, and Development, 26(6), 797–805. doi: 10.1071/RD12354 CrossRefGoogle Scholar
Rodríguez-González, E., López-Bejar, M., Mertens, M. J. and Paramio, M. T. (2003). Effects on in vitro embryo development and intracellular glutathione content of the presence of thiol compounds during maturation of prepubertal goat oocytes. Molecular Reproduction and Development, 65(4), 446–453. doi: 10.1002/mrd.10316 CrossRefGoogle ScholarPubMed
Sakurai, N., Takahashi, K., Emura, N., Fujii, T., Hirayama, H., Kageyama, S., Hashizume, T. and Sawai, K. (2016). The necessity of OCT-4 and CDX2 for early development and gene expression involved in differentiation of inner cell mass and trophectoderm lineages in bovine embryos. Cell Reprogram, 18(5), 309–318. doi: 10.1089/cell.2015.0081 CrossRefGoogle ScholarPubMed
Schreck, R., Rieber, P. and Baeuerle, P. A. (1991). Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO Journal, 10(8), 2247–2258. doi: 10.1002/j.1460-2075.1991.tb07761.x CrossRefGoogle ScholarPubMed
Seidel, G. E. (2006). Modifying oocytes and embryos to improve their cryopreservation. Theriogenology, 65(1), 228–235. doi: 10.1016/j.theriogenology.2005.09.025 CrossRefGoogle ScholarPubMed
Sies, H. (1997). Oxidative stress: Oxidants and antioxidants. Experimental Physiology, 82(2), 291–295. doi: 10.1113/expphysiol.1997.sp004024 CrossRefGoogle ScholarPubMed
Stevens, R., Stevens, L. and Price, N. C. (1983). The stabilities of various thiol compounds used in protein purifications. Biochemical Education, 11(2), 70. doi: 10.1016/0307-4412(83)90048-1 CrossRefGoogle Scholar
Stojkovic, M., Machado, S. A., Stojkovic, P., Zakhartchenko, V., Hutzler, P., Gonçalves, P. B. and Wolf, E. (2001). Mitochondrial distribution and adenosine triphosphate content of bovine oocytes before and after in vitro maturation: Correlation with morphological criteria and developmental capacity after in vitro fertilization and culture. Biology of Reproduction, 64(3), 904–909. doi: 10.1095/biolreprod64.3.904 CrossRefGoogle ScholarPubMed
Stringfellow, D. A. and Givens, M. D. (2010). Manual of the International Embryo Transfer Society: A procedural guide and general information for the use of embryo transfer technology emphasizing sanitary procedures, 4th edn. Savory, Ill.: International Embryo Transfer Society.Google Scholar
Sudano, M. J., Paschoal, D. M., Rascado, Tda S., Magalhães, L. C., Crocomo, L. F., de Lima-Neto, J. F. and Landim-Alvarenga, Fda C. (2011) Lipid content and apoptosis of in vitro-produced bovine embryos as determinants of susceptibility to vitrification. Theriogenology, 75(7), 1211–1220. doi: 10.1016/j.theriogenology.2010.11.033 CrossRefGoogle ScholarPubMed
Takahashi, M., Nagai, T., Hamano, S., Kuwayama, M., Okamura, N. and Okano, A. (1993). Effect of thiol compounds on in vitro development and intracellular glutathione content of bovine embryos. Biology of Reproduction, 49(2), 228–232. doi: 10.1095/biolreprod49.2.228 CrossRefGoogle ScholarPubMed
Takahashi, H., Kuwayama, M., Hamano, S., Takahashi, M., Okano, A., Kadokawa, H., Kariya, T. and Nagai, T. (1996). Effect of b-mercaptoethanol on the viability of IVM/IVF/IVC bovine embryos during long-distance transportation in plastic straws. Theriogenology, 46(6), 1009–1015. doi: 10.1016/s0093-691x(96)00265-8 CrossRefGoogle ScholarPubMed
Takeichi, M. (1988). The cadherins: cell–cell adhesion molecules controlling animal morphogenesis. Development, 102(4), 639–655. doi: 10.1242/dev.102.4.639 CrossRefGoogle ScholarPubMed
Takeo, T., Horikoshi, Y., Nakao, S., Sakoh, K., Ishizuka, Y., Tsutsumi, A., Fukumoto, K., Kondo, T., Haruguchi, Y., Takeshita, Y., Nakamuta, Y., Tsuchiyama, S. and Nakagata, N. (2015). Cysteine analogs with a free thiol group promote fertilization by reducing disulfide bonds in the zona pellucida of mice. Biology of Reproduction, 92(4), 90. doi: 10.1095/biolreprod.114.125443 CrossRefGoogle ScholarPubMed
Tarín, J. J., Ten, J., Vendrell, F. J. and Cano, A. (1998). Dithiothreitol prevents age-associated decrease in oocyte/conceptus viability in vitro . Human Reproduction, 13(2), 381–386. doi: 10.1093/humrep/13.2.381 CrossRefGoogle ScholarPubMed
Truong, T. and Gardner, D. K. (2017). Antioxidants improve IVF outcome and subsequent embryo development in the mouse. Human Reproduction, 32(12), 2404–2413. doi: 10.1093/humrep/dex330 CrossRefGoogle ScholarPubMed
Truong, T. T. and Gardner, D. K. (2020). Antioxidants increase blastocyst cryosurvival and viability post-vitrification. Human Reproduction, 35(1), 12–23. doi: 10.1093/humrep/dez243 CrossRefGoogle ScholarPubMed
Truong, T. T., Soh, Y. M. and Gardner, D. K. (2016). Antioxidants improve mouse preimplantation embryo development and viability. Human Reproduction, 31(7), 1445–1454. doi: 10.1093/humrep/dew098 CrossRefGoogle ScholarPubMed
Tsuzuki, Y., Saigoh, Y. and Ashizawa, K. (2005). Effects of β-mercaptoethanol on ATP contents in cumulus cell-enclosed bovine oocytes matured in vitro and sequential development of resultant embryos from in vitro fertilization. Journal of Mammalian Ova Research, 22(1), 33–39. doi: 10.1274/jmor.22.33 CrossRefGoogle Scholar
Vajta, G., Holm, P., Greve, T. and Callesen, H. (1997). The submarine incubation system, a new tool for in vitro embryo culture: A technique report. Theriogenology, 48(8), 1379–1385. doi: 10.1016/S0093-691X(97)00379-8 CrossRefGoogle Scholar
Van Soom, A., Yuan, Y. Q., Peelman, L. J., de Matos, D. G., Dewulf, J., Laevens, H. and de Kruif, A. (2002). Prevalence of apoptosis and inner cell allocation in bovine embryos cultured under different oxygen tensions with or without cysteine addition. Theriogenology, 57(5), 1453–1465. doi: 10.1016/S0093-691X(01)00726-9 CrossRefGoogle ScholarPubMed
Velez-Pardo, C., Morales, A. T., Del Rio, M. J. and Olivera-Angel, M. (2007). Endogenously generated hydrogen peroxide induces apoptosis via mitochondrial damage independent of NF-kappaB and p53 activation in bovine embryos. Theriogenology, 67(7), 1285–1296. doi: 10.1016/j.theriogenology.2007.01.018 CrossRefGoogle ScholarPubMed
Viana, J. (2020). 2019 Statistics of embryo production and transfer in domestic farm animals. Embryo Technology Newsletter IETS, 38, 7–26.Google Scholar
Werlich, D. E., Barreta, M. H., Martins, L. T., Vieira, A. D., Moraes, A. N. and Mezzalira, A. (2006). Bovine IVP embryos vitrified in different cryoprotectant solutions, using or not super cooled nitrogen. Acta Scientiae Veterinariae, 34, 77–82.CrossRefGoogle Scholar
Willert, K. and Nusse, R. (1998). Beta-catenin: A key mediator of Wnt signaling. Current Opinion in Genetics and Development, 8(1), 95–102. doi: 10.1016/s0959-437x(98)80068-3 CrossRefGoogle ScholarPubMed
Wong, S., Kirkland, J. L., Schwanz, H. A., Simmons, A. L., Hamilton, J. A., Corkey, B. E. and Guo, W. (2014). Effects of thiol antioxidant β-mercaptoethanol on diet-induced obese mice. Life Sciences, 107(1–2), 32–41. doi: 10.1016/j.lfs.2014.04.031 CrossRefGoogle ScholarPubMed