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Effects of sorbitol on porcine oocyte maturation and embryo development in vitro

Published online by Cambridge University Press:  02 January 2014

Tao Lin
Affiliation:
Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University, Daejeon 305–764, Republic of Korea
Jin Yu Zhang
Affiliation:
Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University, Daejeon 305–764, Republic of Korea
Yun Fei Diao
Affiliation:
Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University, Daejeon 305–764, Republic of Korea
Jung Won Kang
Affiliation:
Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University, Daejeon 305–764, Republic of Korea
Dong-Il Jin*
Affiliation:
Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University, Daejeon 305–764, Republic of Korea Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University, Daejeon 305–764, Republic of Korea
*
All correspondence to: Dong-Il Jin. Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University, Daejeon 305–764, Republic of Korea. e-mail: dijin@cnu.ac.kr

Summary

In the present study, a porcine system was supplemented with sorbitol during in vitro maturation (IVM) or in vitro culture (IVC), and the effects of sorbitol on oocyte maturation and embryonic development following parthenogenetic activation were assessed. Porcine immature oocytes were treated with different concentrations of sorbitol during IVM, and the resultant metaphase II stage oocytes were activated and cultured in porcine zygote medium-3 (PZM-3) for 7 days. No significant difference was observed in cumulus expansion and the nuclear maturation between the control and sorbitol-treated groups, with the exception of the 100 mM group, which showed significantly decreased nuclear maturation and cumulus expansion. There was no significant difference in the intracellular reactive oxygen species (ROS) levels between oocytes matured with 10 or 20 mM sorbitol and control groups, but 50 and 100 mM groups had significantly higher ROS levels than other groups. The 20 mM group showed significant increases in intracellular glutathione and subsequent blastocyst formation rates following parthenogenetic activation compared with the other groups. During IVC, supplementation with sorbitol significantly reduced blastocyst formation and increased the apoptotic index compared with the control. The apoptotic index of blastocysts from the sorbitol-treated group for entire culture period was significantly higher than those of the partially sorbitol-exposed groups. Based on these findings, it can be concluded that the addition of a low concentration of sorbitol (20 mM) during IVM of porcine oocytes benefits subsequent blastocyst development and improves embryo quality, whereas sorbitol supplement during IVC has a negative effect on blastocyst formation.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

Biswas, D. & Hyun, S.H. (2011). Supplementation with vascular endothelial growth factor during in vitro maturation of porcine cumulus–oocyte complexes and subsequent developmental competence after in vitro fertilization. Theriogenology 76, 153–60.CrossRefGoogle ScholarPubMed
Biswas, D., Jeon, Y.B., Kim, G.H., Jeung, E.B. & Hyun, S.H. (2011). Supplementation of vascular endothelial growth factor during in vitro maturation of porcine immature cumulus-oocyte complexes and subsequent developmental competence after parthenogenesis and somatic cell nuclear transfer. Reprod. Fert. Dev. 23, 165.Google Scholar
Campbell, K.H.S., Fisher, P., Chen, W.C., Choi, I., Kelly, R.D.W., Lee, J.H. & Xhu, J. (2007). Somatic cell nuclear transfer: Past, present and future perspectives. Theriogenology 68, S21431.Google Scholar
Colman, A. (1999). Somatic cell nuclear transfer in mammals: progress and applications. Cloning 1, 185200.Google Scholar
Fouladi-Nashta, A.A., Alberio, R., Kafi, M., Nicholas, B., Campbell, K.H. & Webb, R. (2005). Differential staining combined with TUNEL labelling to detect apoptosis in preimplantation bovine embryos. Reprod. Biomed. Online 10, 497502.Google Scholar
Funahashi, H. & Romar, R. (2004). Reduction of the incidence of polyspermic penetration into porcine oocytes by pretreatment of fresh spermatozoa with adenosine and a transient co-incubation of the gametes with caffeine. Reproduction 128, 789800.Google Scholar
Funahashi, H., Kim, N.H., Stumpf, T.T., Cantley, T.C. & Day, B.N. (1996). Presence of organic osmolytes in maturation medium enhances cytoplasmic maturation of porcine oocytes. Biol. Reprod. 54, 1412–9.CrossRefGoogle ScholarPubMed
Gomez, M.N., Kang, J.T., Koo, O.J., Kim, S.J., Kwon, D.K., Park, S.J., Atikuzzaman, M., Hong, S.G., Jang, G. & Lee, B.C. (2012). Effect of oocyte-secreted factors on porcine in vitro maturation, cumulus expansion and developmental competence of parthenotes. Zygote 20, 135–45.Google Scholar
Hao, Y., Lai, L., Mao, J., Im, G.S., Bonk, A. & Prather, R.S. (2004). Apoptosis in parthenogenetic preimplantation porcine embryos. Biol. Reprod. 70, 1644–9.CrossRefGoogle ScholarPubMed
Hu, J., Ma, X., Bao, J.C., Li, W., Cheng, D., Gao, Z., Lei, A., Yang, C. & Wang, H. (2011). Insulin-transferrin-selenium (ITS) improves maturation of porcine oocytes in vitro. Zygote 19, 191–7.CrossRefGoogle ScholarPubMed
Huang, Y., Tang, X., Xie, W., Zhou, Y., Li, D., Zhu, J., Yuan, T., Lai, L., Pang, D. & Ouyang, H. (2011). Vitamin C enhances in vitro and in vivo development of porcine somatic cell nuclear transfer embryos. Biochem. Biophys. Res. Commun. 411, 397401.Google Scholar
Hwang, I.S., Park, M.R., Moon, H.J., Shim, J.H., Kim, D.H., Yang, B.C., Ko, Y.G., Yang, B.S., Cheong, H.T. & Im, G.S. (2008). Osmolarity at early culture stage affects development and expression of apoptosis related genes (Bax-α and Bcl-xl) in pre-implantation porcine NT embryos. Mol. Reprod. Dev. 75, 464–71.Google Scholar
Im, G.S., Yang, B.S., Lai, L.X., Liu, Z.H., Hao, Y.H. & Prather, R.S. (2005). Fragmentation and development of preimplantation porcine embryos derived by parthenogenetic activation and nuclear transfer. Mol. Reprod. Dev. 71, 159–65.CrossRefGoogle ScholarPubMed
Jeong, Y.W., Park, S.W., Hossein, M.S., Kim, S., Kim, J.H., Lee, S.H., Kang, S.K., Lee, B.C. & Hwang, W.S. (2006). Antiapoptotic and embryotrophic effects of α-tocopherol and l-ascorbic acid on porcine embryos derived from in vitro fertilization and somatic cell nuclear transfer. Theriogenology 66, 2104–12.Google Scholar
Kikuchi, K., Nagai, T., Ding, J., Yamauchi, N., Noguchi, J. & Izaike, Y. (1999). Cytoplasmic maturation for activation of pig follicular oocytes cultured and arrested at metaphase I. J. Reprod. Fertil. 116, 143–56.Google Scholar
Kobayashi, M., Lee, E.S. & Fukui, Y. (2006). Cysteamine or β-mercaptoethanol added to a defined maturation medium improves blastocyst formation of porcine oocytes after intracytoplasmic sperm injection. Theriogenology 65, 1191–9.CrossRefGoogle ScholarPubMed
Kwak, S.S., Cheong, S.A., Jeon, Y., Lee, E., Choi, K.C., Jeung, E.B. & Hyun, S.H. (2012). The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology 78, 86101.Google Scholar
Lai, L.X. & Prather, R.S. (2003). Production of cloned pigs by using somatic cells as donors. Cloning Stem Cells 5, 233–41.Google Scholar
Lai, L.X. & Prather, R.S. (2004). A method for producing cloned pigs by using somatic cells as donors. Methods Mol. Biol. 254, 149–64.Google Scholar
LaRosa, C. & Downs, S.M. (2006). Stress stimulates AMP-activated protein kinase and meiotic resumption in mouse oocytes. Biol. Reprod. 74, 585–92.Google Scholar
Long, C.R., Dobrinsky, J.R. & Johnson, L.A. (1999). In vitro production of pig embryos: Comparisons of culture media and boars. Theriogenology 51, 1375–90.Google Scholar
Martinez Diaz, M.A., Suzuki, M., Kagawa, M., Ikeda, K. & Takahashi, Y. (2003). Effects of cycloheximide treatment on in-vitro development of porcine parthenotes and somatic cell nuclear transfer embryos. Jpn J. Vet. Res. 50, 147–55.Google Scholar
de Matos, D.G. & Furnus, C.C. (2000). The importance of having high glutathione (GSH) level after bovine in vitro maturation on embryo development: effect of β-mercaptoethanol, cysteine and cystine. Theriogenology 53, 761–71.Google Scholar
Naruse, K., Kim, H.R., Shin, Y.M., Chang, S.M., Lee, H.R., Park, C.S. & Jin, D.I. (2007a). Low concentrations of MEM vitamins during in vitro maturation of porcine oocytes improves subsequent parthenogenetic development. Theriogenology 67, 407–12.Google Scholar
Naruse, K., Quan, Y.S., Choi, S.M., Park, C.S. & Jin, D.I. (2007b). Treatment of porcine oocytes with MEM vitamins during in vitro maturation improves subsequent blastocyst development following nuclear transfer. J. Reprod. Dev. 53, 679–84.Google Scholar
Naruse, K., Quan, Y.S., Kim, B.C., Lee, J.H., Park, C.S. & Jin, D.I. (2007c). Brief exposure to cycloheximide prior to electrical activation improves in vitro blastocyst development of porcine parthenogenetic and reconstructed embryos. Theriogenology 68, 709–16.Google Scholar
Polejaeva, I.A., Chen, S.H., Vaught, T.D., Page, R.L., Mullins, J., Ball, S., Dai, Y., Boone, J., Walker, S., Ayares, D.L., Colman, A. & Campbell, K.H. (2000). Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407, 8690.Google Scholar
Reed, M.L., Illera, M.J. & Petters, R.M. (1992). In vitro culture of pig embryos. Theriogenology 37, 95109.Google Scholar
Tao, Y., Zhou, B., Xia, G., Wang, F., Wu, Z. & Fu, M. (2004). Exposure to L-ascorbic acid or α-tocopherol facilitates the development of porcine denuded oocytes from metaphase I to metaphase II and prevents cumulus cells from fragmentation. Reprod. Domest. Anim. 39, 52–7.Google Scholar
Uhm, S.J., Gupta, M.K., Das, Z.C., Kim, N.H. & Lee, H.T. (2011). 3-Hydroxyflavone improves the in vitro development of cloned porcine embryos by inhibiting ROS production. Cell. Reprogram. 13, 441–9.Google Scholar
Wang, W.H., Abeydeera, L.R., Cantley, T.C. & Day, B.N. (1997). Effects of oocyte maturation media on development of pig embryos produced by in vitro fertilization. J. Reprod. Fertil. 111, 101–8.Google Scholar
Xie, Y., Zhong, W., Wang, Y., Trostinskaia, A., Wang, F., Puscheck, E.E. & Rappolee, D.A. (2007). Using hyperosmolar stress to measure biologic and stress-activated protein kinase responses in preimplantation embryos. Mol. Hum. Reprod. 13, 473–81.CrossRefGoogle ScholarPubMed
Yamauchi, N., Sasada, H., Soloy, E., Dominko, T., Kikuchi, K. & Nagai, T. (1999). Effects of hormones and osmolarity in the culture medium on germinal vesicle breakdown of porcine oocytes. Theriogenology 52, 153–62.Google Scholar
You, J., Kim, J., Lim, J. & Lee, E. (2010). Anthocyanin stimulates in vitro development of cloned pig embryos by increasing the intracellular glutathione level and inhibiting reactive oxygen species. Theriogenology 74, 777–85.Google Scholar
Zhang, J.Y., Diao, Y.F., Kim, H.R. & Jin, D.I. (2012). Inhibition of endoplasmic reticulum stress improves mouse embryo development. PLoS One 7, e40433.Google Scholar