Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T08:47:34.843Z Has data issue: false hasContentIssue false

Effects of gaseous atmosphere and antioxidants on the development and cryotolerance of bovine embryos at different periods of in vitro culture

Published online by Cambridge University Press:  16 September 2013

Nathália Alves de Souza Rocha-Frigoni
Affiliation:
School of Veterinary Medicine, Laboratory of Reproductive Physiology, UNESP–Universidade Estadual Paulista, Araçatuba, SP 16050–680, Brazil.
Beatriz Caetano da Silva Leão
Affiliation:
School of Veterinary Medicine, Laboratory of Reproductive Physiology, UNESP–Universidade Estadual Paulista, Araçatuba, SP 16050–680, Brazil.
Ériklis Nogueira
Affiliation:
Brazilian Agricultural Research Corporation, EMBRAPA Pantanal, Corumbá, MS 79320–900, Brazil.
Mônica Ferreira Accorsi
Affiliation:
School of Veterinary Medicine, Laboratory of Reproductive Physiology, UNESP–Universidade Estadual Paulista, Araçatuba, SP 16050–680, Brazil.
Gisele Zoccal Mingoti*
Affiliation:
School of Veterinary Medicine, Department of Animal Health, UNESP–Universidade Estadual Paulista, Araçatuba 16050–680, São Paulo, Brazil.
*
All correspondence to: G.Z. Mingoti, School of Veterinary Medicine, Department of Animal Health, UNESP–Universidade Estadual Paulista, Araçatuba 16050–680, São Paulo, Brazil. Tel: +55 18 3636 1375. Fax: +55 18 3636 1352. E-mail: gmingoti@fmva.unesp.br

Summary

This study examined the effects of antioxidant supplementation and O2 tension on embryo development, cryotolerance and intracellular reactive oxygen species (ROS) levels. The antioxidant supplementation consisted of 0.6 mM cysteine (CYST); 0.6 mM cysteine + 100 μM cysteamine (C+C); 100 IU catalase (CAT) or 100 μM β-mercaptoethanol (β-ME) for 3 or 7 days of in vitro culture (IVC). Two O2 tensions (20% O2 [5% CO2 in air] or 7% O2, 5% CO2 and 88% N2 [gaseous mixture]) were examined. After 7 days of antioxidant supplementation, the blastocyst frequencies were adversely affected (P < 0.05) by CYST (11.2%) and C+C (1.44%), as well as by low O2 tension (17.2% and 11.11% for 20% and 7% O2, respectively) compared with the control (26.6%). The blastocyst re-expansion rates were not affected (P > 0.05) by the treatments (range, 66–100%). After 3 days of antioxidant supplementation, the blastocyst frequencies were not affected (P > 0.05) by any of the antioxidants (range, 43.6–48.5%), but they were reduced by low O2 tension (P < 0.05) (52.1% and 38.4% for 20% and 7% O2, respectively). The intracellular ROS levels, demonstrated as arbitrary fluorescence units, were not affected (P > 0.05) by antioxidant treatment (range, 0.78 to 0.95) or by O2 tension (0.86 and 0.88 for 20% and 7% O2, respectively). The re-expansion rates were not affected (P > 0.05) by any of the treatments (range, 63.6–93.3%). In conclusion, intracellular antioxidant supplementation and low O2 tension throughout the entire IVC period were deleterious to embryo development. However, antioxidant supplementation up to day 3 of IVC did not affect the blastocyst frequencies or intracellular ROS levels.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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.)

References

Ali, A.A., Bilodeau, J.F. & Sirard, M.A. (2003). Antioxidant requirements for bovine oocytes varies during in vitro maturation, fertilization and development. Theriogenology 59, 939–49.Google Scholar
Arias, M.E., Sanchez, R. & Felmer, R. (2011). Evaluation of different culture systems with low oxygen tension on the development, quality and oxidative stress-related genes of bovine embryos produced in vitro. Zygote 20, 209–17.CrossRefGoogle ScholarPubMed
Bain, N.T., Madan, P. & Betts, D.H. (2011). The early embryo to intracellular reactive oxygen species is developmentally regulated. Reprod. Fertil. Dev. 23, 561–75.Google Scholar
Betts, D.H. & Madan, P. (2008). Permanent embryo arrest: molecular and cellular concepts. Mol. Hum. Reprod. 14, 445–53.Google Scholar
Carolan, C., Lonergan, P., Van Langendonckt, A. & Mermillod, P. (1995). Factors affecting bovine embryo development in synthetic oviduct fluid following oocyte maturation and fertilization in vitro. Theriogenology 43, 1115–28.CrossRefGoogle ScholarPubMed
Corrêa, G.A., Rumpf, R., Mundim, T.C.D., Franco, M.M. & Dode, M.A.N. (2008). Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim. Reprod. Sci. 104, 132–42.CrossRefGoogle ScholarPubMed
Deleuze, S. & Goudet, G. (2010). Cysteamine supplementation of in vitro maturation media: a review. Reprod. Dom. Anim. 45, 476–82.Google Scholar
De Matos, D.G., Herrera, C., Cortvrindt, R., Smitz, J., Van Soom, A., Nogueira, D. & Pasqualini, R.S. (2002). Cysteamine supplementation during in vitro maturation and embryo culture: a useful tool for increasing the efficiency of bovine in vitro embryo production. Mol. Reprod. Dev. 62, 203–9.CrossRefGoogle ScholarPubMed
Fugitani, Y., Kasai, K., Ohtani, S., Nishimura, K., Yamada, M. & Utsumi, K. (1997). Effect of oxygen concentration and free radicals on in vitro development of in vitro-produced bovine embryos. J. Anim. Sci. 75, 483–92.CrossRefGoogle Scholar
Fukui, Y. & Oyamada, T. (2004). Oxygen tension and medium supplements for in vitro maturation of bovine oocytes cultured individually in a chemically defined medium. J. Reprod. Dev. 50, 107–17.Google Scholar
Gonçalves, F.S., Barreto, L.S.S., Arruda, R.P., Perri, S.H.V. & Mingoti, G.Z. (2010). Effect of antioxidants during bovine in vitro fertilization procedures on spermatozoa and embryo development. Reprod. Domest. Anim. 45, 129135.Google Scholar
Goto, Y., Noda, Y., Mori, T. & Nakano, M. (1993). Increased generation of reactive oxygen species in embryo cultured in vitro. Free. Radic. Biol. Med. 15, 6975.CrossRefGoogle ScholarPubMed
Guérin, P., Mouatassim, S.E.L. & Ménézo, Y. (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7, 175189.CrossRefGoogle ScholarPubMed
Harvey, M.B., Arcellana-Panlilio, M.Y., Zhang, X., Schultz, G.A. & Watson, A.J. (1995). Expression of genes encoding antioxidants enzymes in preimplantation mouse and cow embryos and primary bovine oviduct cultures employed for embryo co-cultured. Biol. Reprod. 53, 532572.CrossRefGoogle Scholar
Harvey, A.J. (2007). The role of oxygen in ruminant preimplantation embryo development and metabolism. Anim. Reprod. Sci. 98, 113–28.Google Scholar
Hosseini, S.M., Forouzanfar, M., Hajian, M., Asgari, V., Abedi, P. & Hosseini, L. (2009). Antioxidant supplementation of culture medium during embryo development and/or after vitrification-warming: which is the most important? J. Assist. Reprod. Genet. 26, 355–64.CrossRefGoogle ScholarPubMed
Imai, K., Matoba, S., Dochi, O. & Shimohira, I. (2002). Different factors affect developmental competence and cryotolerance in in vitro produced bovine embryo. Theriogenology 64, 887891.Google Scholar
Iwata, H., Akamatsu, S., Minami, N. & Yamada, M. (1998). Effects of antioxidants on the development of bovine IVM/IVF embryos in various concentrations of glucose. Theriogenology 50, 365–75.CrossRefGoogle ScholarPubMed
Khurana, N.K. & Niemann, H. (2000). Effect of oocyte quality, oxygen tension, embryo density, cumulus cells and energy substrate on cleavage and morula/blastocysts formation of bovine embryos. Theriogenology 54, 741–56.CrossRefGoogle Scholar
Kitagawa, Y., Suzukib, K., Yonedaa, A, & Watanabea, T. (2004). Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation on porcine embryos. Theriogenology 62, 11861283.Google Scholar
Kouridakis, K. & Gardner, D.K. (1995). Pyruvate in embryo culture media acts as an antioxidant. Proc. Fertil. Soc. Aus. 14, 29.Google Scholar
Leminska, A., Wnuk, M., Slota, E. & Bartosz, G. (2007). Total antioxidant capacity of cell culture media. Clin. Exp. Pharmacol. Physiol. 34, 781–86.Google Scholar
Lim, J.M., Reggio, B.C., Godke, R.A. & Hansel, W. (1999). Development of in vitro-derived bovine embryos cultured in 5% CO2 in air or in 5% O2, 5% de CO2 and 90% N2. Hum. Reprod. 14, 458–64.Google Scholar
Lonergan, P., Rizos, D., Gutierrez-Adan, A., Fair, T. & Boland, M.P. (2003). Oocytes and embryos quality: effect of origin, culture conditions and gene expression patterns. Reprod. Dom. Anim. 38, 259–67.CrossRefGoogle ScholarPubMed
Lopes, A.S., Lane, M. & Thompson, J.G. (2010). Oxygen consumption and ROS production are increased at the time of fertilization in cell cleavage in bovine zygotes. Hum. Reprod. 25, 2763–72.Google Scholar
Martín-Romero, F.J., Miguel-Lasobras, E.M., Domínguez-Arroyo, J.A., González-Carrera, E. & Álvarez, I.S. (2008). Contribution of culture media to oxidative stress and its effects on human oocytes. Reprod. Biomed. Online 17, 652661Google Scholar
Mingoti, G.Z., Caiado Castro, V.S.D., Méo, S.C., Barreto, L.S.S. & Garcia, J.M. (2009). The effect of interaction between macromolecule supplement and oxygen tension on bovine oocytes and embryos cultured in vitro. Zygote 17, 321328.CrossRefGoogle ScholarPubMed
Nars-Esfahani, M.H., Aitken, J.R. & Johnson, M.H. (1990). Hydrogen peroxide levels in mouse oocytes and early cleavage stages embryos developed in vitro or in vivo. Development 109, 501–8.Google Scholar
Nedambale, T., Du, F., Yang, X. & Tian, X. (2006). Higher survival rate of vitrified and thawed in vitro produced bovine blastocysts following culture in defined medium supplemented with beta-mercaptoethanol. Anim. Reprod. Sci. 93, 6175.Google Scholar
Noda, Y., Matsumoto, H., Maoka, H., Tatsumi, K., Kishi, J. & Mori, T. (1991). Involvement of superoxide radicals in the mouse 2-cell block. Mol. Reprod. Dev. 28, 356–60.Google Scholar
Orsi, N.M. & Leese, H.J. (2001). Protection against reactive oxygen species during mouse preimplantation embryo development: role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Mol. Reprod. Dev. 59, 4453.CrossRefGoogle ScholarPubMed
Parrish, J.J., Susko-Parrish, J., Winer, M.A. & First, N.L. (1988). Capacitation of bovine sperm by heparin. Biol. Reprod. 38, 1171–88.Google Scholar
Rizos, D., Ward, F., Boland, M.P. & Lonergan, P. (2001). Effect of culture system on the yield and quality of bovine blastocysts as assessed by survival after vitrification. Theriogenology 56, 116.CrossRefGoogle ScholarPubMed
Rocha, N.A.S., Leão, B.C.S., Nogueira, E. & Mingoti, G.Z. (2012a). Intracellular reactive oxygen species in bovine embryos cultured in vitro with catalase under various oxygen tensions. Reprod. Fertil. Dev. 24, 157158 [Abstract].Google Scholar
Rocha, N.A.S., Leão, B.C.S., Nogueira, E. & Mingoti, G.Z. (2012b). Supplementation with antioxidants during maturation increases resistance to oxidative stress in bovine embryos produced in vitro but not improves cryotolerance. Anim. Reprod. 9, 681. [Abstract].Google Scholar
Somfai, T., Inaba, Y., Aikawa, Y., Ohtake, M., Kobayashi, S., Konishi, K., Nagai, T. & Imai, K. (2010). Development of bovine embryos cultured in CR1aa and IDV101 media using different oxygen tension and culture systems. Acta Vet. Hung. 58, 465–74.Google Scholar
Takahashi, M., Nagai, T., Hamano, S., Kuwayama, M., Okamura, N. & Okano, A. (1993). Effect of thiol compounds on in vitro development and intracellular glutathione content of bovine embryos. Biol. Reprod. 49, 228–64.CrossRefGoogle ScholarPubMed
Takahashi, M., Keisho, H., Takahashi, H., Ogawa, H., Schultz, R.M. & Okano, A. (2000). Effect of oxidative stress on development and DNA damage in in vitro-cultured bovine embryos by comet assay. Theriogenology 54, 137–45.Google Scholar
Takahashi, M., Nagai, T., Okamura, N., Takahashi, H. & Okano, A. (2002). Promoting effect of beta-mercaptoethanol on in vitro development under oxidative stress and cystine uptake of bovine embryos. Biol. Reprod. 66, 562–69.Google Scholar
Thompson, J.G.E., Simpson, A.C., Pugh, P.A., Donnely, P.E. & Tervit, H.R. (1990). Effect of oxygen concentration on in vitro development of preimplantation sheep and cattle embryos. J. Reprod. Fertil. 89, 573–78.Google Scholar
Ufer, C., Wang, C.C., Borchert, B., Heydeck, D. & Kuhn, H. (2010). Redox control in mammalian embryo development. Antioxid. Redox. Signal. 13, 836–75.Google Scholar
Vajta, G., Rindom, N., Peura, T.T., Holm, P., Greve, T. & Callesen, H. (1999). The effect of media, serum and temperature on in vitro survival of bovine blastocysts after open pulled straw (OPS) vitrification. Theriogenology 52, 939–48.Google Scholar
Van Der Westerlaken, L.A.J., Van Der Vlugt, J.J., Dewit, A.A.C. & Van Der Schans, A. (1992). The effect of oxygen tension on in vitro fertilization and embryonic development. Theriogenology 37, 312.CrossRefGoogle Scholar
Van Soom, A., Yuan, Y.Q., Peelman, L.J., De Matos, D.G., Dewulf, J., Laevens, H. & 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, 1453–65.CrossRefGoogle ScholarPubMed
Voelkel, S.A. & Hu, Y.V. (1992). Effect of gas atmosphere on the development of one-cell bovine embryos in two culture systems. Theriogenology 37, 1117–31.CrossRefGoogle ScholarPubMed