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The combined treatment of calcium ionophore with strontium improves the quality of ovine SCNT embryo development

Published online by Cambridge University Press:  22 November 2012

Inchul Choi ,
Jie Zhu  and
Keith H. S. Campbell
Inchul Choi*
Affiliation:
Developmental Epigenetics Laboratory, Department of Animal Science, Michigan State University, East Lansing, Michigan, USA. Animal Development and Biotechnology Group, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire, LE12 5RD, UK.
Jie Zhu
Affiliation:
Animal Development and Biotechnology Group, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire, LE12 5RD, UK.
Keith H. S. Campbell
Affiliation:
Animal Development and Biotechnology Group, School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire, LE12 5RD, UK.
*
All correspondence to: Inchul Choi. Developmental Epigenetics Laboratory, Department of Animal Science, Michigan State University, East Lansing, Michigan, USA. e-mail: icchoi@msu.edu
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Summary

Poor embryo quality is a major problem that contributes to the failure of pregnancy in somatic cell nuclear transfer (SCNT). The aims of this study were to improve the quality of ovine SCNT embryos by modifying the conventional activation protocol with the addition of SrCl2. In order to achieve this objective we conducted a series of experiments with in vitro-matured oocytes to optimize conditions for oocyte activation with strontium, and subsequently applied the protocol to SCNT embryos. The results showed that in vitro-matured oocytes could be activated effectively by 10 mM SrCl2 + 5 mg/ml cytochalasin B (CB) for 5 h in the absence of Ca2+ and that the blastocyst rate on day 7 (33.2%) was similar to that in the control group (31.0%) (5 M calcium ionophore [IP] A23187 for 5 min and cultured in CB/cycloheximide [CHX] for 5 h; P > 0.05). In SCNT experiments, the total cell number/blastocyst (104.12 ± 6.86) in the IP + SrCl2/CB-treatment group was, however, significantly higher than that in the control group (81.07 ± 3.39; P < 0.05). Apoptotic index (12.29 ± 1.22%) was significantly lower than the control (17.60 ± 1.39%; P < 0.05) when a combination of IP and SrCl2/CB was applied to SCNT embryos. In addition, karyotyping of the SCNT embryos showed that the percentage of diploid blastocysts in the IP + SrCl2/CB-treatment group was slightly higher than that in the control (P > 0.05). We conclude that the modified activation protocol with IP + SrCl2/CB can improve significantly the quality of ovine SCNT embryos in terms of total cell number, apoptosis and ploidy.

Keywords

ApoptosisEmbryo developmentOocyte activationSomatic cell nuclear transferStrontium
Type
Research Article
Information
Zygote , Volume 21 , Issue 2 , May 2013 , pp. 139 - 150
Copyright
Copyright © Cambridge University Press 2012

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References

Akagi, S., Takahashi, S., Adachi, N., Hasegawa, K., Sugawara, T., Tozuka, Y., Yamamoto, E., Shimizu, M. & Izaike, Y. (2003). In vitro and in vivo developmental potential of nuclear transfer embryos using bovine cumulus cells prepared in four different conditions. Cloning Stem Cells 5, 101–8.CrossRefGoogle ScholarPubMed
Akagi, S., Kaneyama, K., Adachi, N., Tsuneishi, B., Matsukawa, K., Watanabe, S., Kubo, M. & Takahashi, S. (2008). Bovine nuclear transfer using fresh cumulus cell nuclei and in vivo- or in vitro-matured cytoplasts. Cloning Stem Cells 10, 173–80.CrossRefGoogle ScholarPubMed
Alberio, R., Brero, A., Motlík, J., Cremer, T., Wolf, E. & Zakhartchenko, V. (2001). Remodeling of donor nuclei, DNA synthesis, and ploidy of bovine cumulus cell nuclear transfer embryos: effect of activation protocol. Mol. Reprod. Dev. 59, 371–9.CrossRefGoogle ScholarPubMed
Alexander, B., Coppola, G., Berardino, D.D., Rho, G.J., John, E.S., Betts, D.H. & King, W.A. (2006). The effect of 6-dimethylaminopurine (6-DMAP) and cycloheximide (CHX) on the development and chromosomal complement of sheep parthenogenetic and nuclear transfer embryos. Mol. Reprod. Dev. 73, 20–30.CrossRefGoogle ScholarPubMed
Alexopoulos, N.I. & French, A.J. (2009). The prevalence of embryonic remnants following the recovery of post-hatching bovine embryos produced in vitro or by somatic cell nuclear transfer. Anim. Reprod. Sci. 114, 43–53.CrossRefGoogle ScholarPubMed
Atabay, E.C., Katagiri, S., Nagano, M. & Takahashi, Y. (2003). Effect of activation treatments of recipient oocytes on subsequent development of bovine nuclear transfer embryos. Jpn J. Vet. Res. 50, 185–94.Google ScholarPubMed
Bhak, J.-S., Lee, S.-L., Ock, S.-A., Mohanakumar, B., Choe, S.-Y. & Rho, G.-J. (2006). Developmental rate and ploidy of embryos produced by nuclear transfer with different activation treatments in cattle. Anim. Reprod. Sci. 92, 37–49.CrossRefGoogle ScholarPubMed
Booth, P. J., Holm, P., Vajta, G., Greve, T. & Callesen, H. (2001). Effect of two activation treatments and age of blastomere karyoplasts on in vitro development of bovine nuclear transfer embryos. Mol. Reprod. Dev. 60, 377–83.CrossRefGoogle ScholarPubMed
Bos-Mikich, A., Swann, K. & Whittingham, D.G. (1995). Calcium oscillations and protein synthesis inhibition synergistically activate mouse oocytes. Mol. Reprod. Dev. 41, 84–90.CrossRefGoogle ScholarPubMed
Bos-Mikich, A., Whittingham, D.G. & Jones, K.T. (1997). Meiotic and mitotic Ca2+ oscillations affect cell composition in resulting blastocysts. Dev. Biol. 182, 172–9.CrossRefGoogle ScholarPubMed
Bos-Mikich, A., Mattos, A.L.G. & Ferrari, A.N. (2001). Early cleavage of human embryos: an effective method for predicting successful IVF/ICSI outcome. Hum. Reprod. 16, 2658–61.CrossRefGoogle ScholarPubMed
Brison, D.R. & Schultz, R.M. (1998). Increased incidence of apoptosis in transforming growth factor α-deficient mouse blastocysts. Biol. Reprod. 59, 136–44.CrossRefGoogle ScholarPubMed
Byrne, A.T., Southgate, J., Brison, D.R. & Leese, H.J. (1999). Analysis of apoptosis in the preimplantation bovine embryo using TUNEL. J. Reprod. Fertil. 117, 97–105.CrossRefGoogle ScholarPubMed
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, S214–31.CrossRefGoogle ScholarPubMed
Cervera, R., Silvestre, M., Marti, N., Garcia-Mengual, E., Moreno, R. & Stojkovic, M. (2009). Effects of different oocyte activation procedures on development and gene expression of porcine pre-implantation embryos. Reprod. Domest. Anim. 45, e12–20.Google Scholar
Cha, S.K., Kim, N.H., Lee, S.M., Baik, C.S., Lee, H.T. & Chung, K.S. (1997). Effect of cytochalasin B and cycloheximide on the activation rate, chromosome constituent and in vitro development of porcine oocytes following parthenogenetic stimulation. Reprod. Fertil. Dev. 9, 441–6.CrossRefGoogle ScholarPubMed
Che, L., Lalonde, A. & Bordignon, V. (2007). Chemical activation of parthenogenetic and nuclear transfer porcine oocytes using ionomycin and strontium chloride. Theriogenology 67, 1297–1304.CrossRefGoogle ScholarPubMed
Dai, X., Hao, J. & Zhou, Q. (2009). A modified culture method significantly improves the development of mouse somatic cell nuclear transfer embryos. Reprod. 138, 301–8.CrossRefGoogle ScholarPubMed
De La Fuente, R. & King, W.A. (1998). Developmental consequences of karyokinesis without cytokinesis during the first mitotic cell cycle of bovine parthenotes. Biol. Reprod. 58, 952–62.CrossRefGoogle ScholarPubMed
Ducibella, T., Huneau, D., Angelichio, E., Xu, Z., Schultz, R.M., Kopf, G.S., Fissore, R., Madoux, S. & Ozil, J.-P. (2002). Egg-to-embryo transition is driven by differential responses to Ca2+oscillation number. Dev. Biol. 250, 280–91.CrossRefGoogle Scholar
Dyban, A.P. (1983). An improved method for chromosome preparations from preimplantation mammalian embryos, oocytes or isolated blastomeres. Biotechnic. Histochem. 58, 69–72.Google ScholarPubMed
Escriba, M.J. & Garcia-Ximenez, F. (2000). Influence of sequence duration and number of electrical pulses upon rabbit oocyte activation and parthenogenetic in vitro development. Anim. Reprod. Sci. 59, 99–107.CrossRefGoogle ScholarPubMed
Garcia-Mengual, E., Alfonso, J., Salvador, I., Duque, C. C. & Silvestre, M.A. (2008). Oocyte activation procedures and influence of serum on porcine oocyte maturation and subsequent parthenogenetic and nuclear transfer embryo development. Zygote 16, 279–84.CrossRefGoogle ScholarPubMed
Gupta, M.K., Jang, J.M., Jung, J.W., Uhm, S.J., Kim, K.P. & Lee, H.T. (2009). Proteomic analysis of parthenogenetic and in vitro fertilized porcine embryos. Proteomics 9, 2846–60.CrossRefGoogle ScholarPubMed
Heytens, E., Soleimani, R., Lierman, S., De Meester, S., Gerris, J., Dhont, M., Van der Elst, J. & De Sutter, P. (2008). Effect of ionomycin on oocyte activation and embryo development in mouse. Reprod. Biomed. Online 17, 764–71.CrossRefGoogle Scholar
Holm, P., Booth, P.J. & Callesen, H. (2003). Developmental kinetics of bovine nuclear transfer and parthenogenetic embryos. Cloning Stem Cells 5, 133–42.CrossRefGoogle ScholarPubMed
Iager, A.E., Ragina, N.P., Ross, P.J., Beyhan, Z., Cunniff, K., Rodriguez, R.M. & Cibelli, J.B. (2008). Trichostatin A improves histone acetylation in bovine somatic cell nuclear transfer early embryos. Cloning Stem Cells 10, 371–9.CrossRefGoogle ScholarPubMed
Kishigami, S. & Wakayama, T. (2007a). Efficient strontium-induced activation of mouse oocytes in standard culture media by chelating calcium. J. Reprod. Dev. 53, 1207–15.CrossRefGoogle ScholarPubMed
Kishigami, S. & Wakayama, T. (2007b). Oocyte activation by strontium in the presence of calcium supports full term development of somatic cell cloned embryos. Biol. Reprod. 77, 163.CrossRefGoogle Scholar
Kishigami, S., Bui, H. T., Wakayama, S., Tokunaga, K., Van Thuan, N., Hikichi, T., Mizutani, E., Ohta, H., Suetsugu, R., Sata, T. & Wakayama, T. (2007). Successful mouse cloning of an outbred strain by trichostatin A treatment after somatic nuclear transfer. J. Reprod. Dev. 53, 165–70.CrossRefGoogle ScholarPubMed
Kline, D. & Kline, J.T. (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev. Biol. 149, 80–9.CrossRefGoogle ScholarPubMed
Krivokharchenko, A., Popova, E., Zaitseva, I., Vil'ianovich, L., Ganten, D. & Bader, M. (2003). Development of parthenogenetic rat embryos. Biol. Reprod. 68, 829–36.CrossRefGoogle ScholarPubMed
Levron, J., Cohen, J. & Willadsen, S. (1995). Highly effective method of human oocyte activation. Zygote 3, 157–61.CrossRefGoogle ScholarPubMed
Liu, L., Trimarchi, J.R. & Keefe, D.L. (2002). Haploidy but not parthenogenetic activation leads to increased incidence of apoptosis in mouse embryos. Biol. Reprod. 66, 204–10.CrossRefGoogle Scholar
Liu, S.Z., Jiang, M.X., Yan, L.Y., Jiang, Y., Ouyang, Y.C., Sun, Q.Y. & Chen, D.Y. (2005). Parthenogenetic and nuclear transfer rabbit embryo development and apoptosis after activation treatments. Mol. Reprod. Dev. 72, 48–53.CrossRefGoogle ScholarPubMed
Loi, P., Ledda, S., Fulka, J., Cappai, P. & Moor, R.M. (1998). Development of parthenogenetic and cloned ovine embryos: effect of activation protocols. Biol. Reprod. 58, 1177–87.CrossRefGoogle ScholarPubMed
Lonergan, P., Khatir, H., Piumi, F., Rieger, D., Humblot, P. & Boland, M.P. (1999). Effect of time interval from insemination to first cleavage on the developmental characteristics, sex ratio and pregnancy rate after transfer of bovine embryos. J. Reprod. Fertil. 117, 159–67.CrossRefGoogle ScholarPubMed
Ma, S.-F., Liu, X.-Y., Miao, D.-Q., Han, Z.-B., Zhang, X., Miao, Y.-L., Yanagimachi, R. & Tan, J.-H. (2005). Parthenogenetic activation of mouse oocytes by strontium chloride: a search for the best conditions. Theriogenology 64, 1142–57.CrossRefGoogle ScholarPubMed
Ma, Y., Li, Y., Wei, H., Li, Q., Fang, R., Zhao, R., Zhang, K., Xue, K., Lou, Y., Dai, Y., Lian, L. & Li, N. (2009). Effects of chemical activation and season on birth efficiency of cloned pigs. Science in China Series C: Life Sciences 52, 657–64.Google ScholarPubMed
McKiernan, S.H. & Bavister, B.D. (1994). Fertilization and early embryology: timing of development is a critical parameter for predicting successful embryogenesis. Hum. Reprod. 9, 2123–9.CrossRefGoogle Scholar
Meo, S.C., Yamazaki, W., Leal, C.L.V., de Oliveira, J.A. & Garcia, J.M. (2005). Use of strontium for bovine oocyte activation. Theriogenology 63, 2089–102.CrossRefGoogle ScholarPubMed
Meo, S.C., Yamazaki, W., Ferreira, C.R., Perecin, F., Saraiva, N.Z., Leal, C.L.V. & Garcia, J.M. (2007). Parthenogenetic activation of bovine oocytes using single and combined strontium, ionomycin and 6-dimethylaminopurine treatments. Zygote 15, 295–306.CrossRefGoogle ScholarPubMed
Minamihashi, A., Watson, A.J., Watson, P.H., Church, R.B. & Schultz, G.A. (1993). Bovine parthenogenetic blastocysts following in vitro maturation and oocyte activation with ethanol. Theriogenology 40, 63–76.CrossRefGoogle ScholarPubMed
Mohammed, A.A., Karasiewicz, J. & Modlinski, J.A. (2008). Development potential of selectively enucleated immature mouse oocytes upon nuclear transfer. Mol. Reprod. Dev. 75, 1269–80.CrossRefGoogle ScholarPubMed
Nussbaum, D.J. & Prather, R.S. (1995). Differential effects of protein synthesis inhibitors on porcine oocyte activation. Mol. Reprod. Dev. 41, 70–5.CrossRefGoogle ScholarPubMed
Ogura, A., Inoue, K., Ogonuki, N., Noguchi, A., Takano, K., Nagano, R., Suzuki, O., Lee, J., Ishino, F. & Matsuda, J. (2000). Production of male cloned mice from fresh, cultured, and cryopreserved immature Sertoli cells. Biol. Reprod. 62, 1579–84.CrossRefGoogle ScholarPubMed
Ono, Y., Shimozawa, N., Ito, M. & Kono, T. (2001). Cloned mice from fetal fibroblast cells arrested at metaphase by a serial nuclear transfer. Biol. Reprod. 64, 44–50.CrossRefGoogle ScholarPubMed
Ozil, J.-P., Markoulaki, S., Toth, S., Matson, S., Banrezes, B., Knott, J.G., Schultz, R.M., Huneau, D. & Ducibella, T. (2005). Egg activation events are regulated by the duration of a sustained [Ca2+]cyt signal in the mouse. Dev. Biol. 282, 39–54.CrossRefGoogle ScholarPubMed
Prather, R.S., Sutovsky, P. & Green, J.A. (2004). Nuclear remodeling and reprogramming in transgenic pig production. Exp. Biol. Med. (Maywood) 229, 1120–6.CrossRefGoogle ScholarPubMed
Presicce, G.A. & Yang, X. (1994). Nuclear dynamics of parthenogenesis of bovine oocytes matured in vitro for 20 and 40 hours and activated with combined ethanol and cycloheximide treatment. Mol. Reprod. Dev. 37, 61–8.CrossRefGoogle ScholarPubMed
Rhoton-Vlasak, A., Lu, P.Y., Barud, K.M., Dewald, G.W. & Hammitt, D.G. (1996). Efficacy of calcium ionophore A23187 oocyte activation for generating parthenotes for human embryo research. J. Assist. Reprod. Genet. 13, 793–6.CrossRefGoogle ScholarPubMed
Ribas, R., Oback, B., Ritchie, W., Chebotareva, T., Taylor, J., Mauricio, A.C., Sousa, M. & Wilmut, I. (2006). Modifications to improve the efficiency of zona-free mouse nuclear transfer. Cloning Stem Cells 8, 10–5.CrossRefGoogle ScholarPubMed
Rideout, W.M., Wakayama, T., Wutz, A., Eggan, K., Jackson-Grusby, L., Dausman, J., Yanagimachi, R. & Jaenisch, R. (2000). Generation of mice from wild-type and targeted ES cells by nuclear cloning. Nat. Genet. 24, 109–10.CrossRefGoogle ScholarPubMed
Rogers, N.T., Halet, G., Piao, Y., Carroll, J., Ko, M.S.H. & Swann, K. (2006). The absence of a Ca2+ signal during mouse egg activation can affect parthenogenetic preimplantation development, gene expression patterns, and blastocyst quality. Reproduction 132, 45–57.CrossRefGoogle ScholarPubMed
Stice, S.L., Keefer, C.L. & Matthews, L. (1994). Bovine nuclear transfer embryos: oocyte activation prior to blastomere fusion. Mol. Reprod. Dev. 38, 61–8.CrossRefGoogle ScholarPubMed
Susko-Parrish, J.L., Leibfried-Rutledge, M.L., Northey, D.L., Schutzkus, V. & First, N.L. (1994). Inhibition of protein kinases after an induced calcium transient causes transition of bovine oocytes to embryonic cycles without meiotic completion. Dev. Biol. 166, 729–39.CrossRefGoogle ScholarPubMed
Tao, T., Machaty, Z., Abeydeera, L.R., Day, B.N. & Prather, R.S. (2000). Optimisation of porcine oocyte activation following nuclear transfer. Zygote 8, 69–77.CrossRefGoogle ScholarPubMed
van Soom, A., Ysebaert, M.-T. & Kruif, A.D. (1997). Relationship between timing of development, morula morphology, and cell allocation to inner cell mass and trophectoderm in in vitro-produced bovine embryos. Mol. Reprod. Dev. 47, 47–56.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Wang, Z.G., Wang, W., Yu, S.D. & Xu, Z.R. (2008). Effects of different activation protocols on preimplantation development, apoptosis and ploidy of bovine parthenogenetic embryos. Anim. Reprod. Sci. 105, 292–301.CrossRefGoogle ScholarPubMed
Ware, C.B., Barnes, F.L., Maiki-Laurila, M. & First, N.L. (1989). Age dependence of bovine oocyte activation. Gamete Res. 22, 265–75.CrossRefGoogle ScholarPubMed
Whitworth, K.M., Li, R., Spate, L.D., Wax, D.M., Rieke, A., Whyte, J.J., Manandhar, G., Sutovsky, M., Green, J.A., Sutovsky, P. & Prather, R.S. (2009). Method of oocyte activation affects cloning efficiency in pigs. Mol. Reprod. Dev. 76, 490–500.CrossRefGoogle ScholarPubMed
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J. & Campbell, K.H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–3.CrossRefGoogle ScholarPubMed
Windt, M.L., Kruger, T.F., Coetzee, K. & Lombard, C.J. (2004). Comparative analysis of pregnancy rates after the transfer of early dividing embryos versus slower dividing embryos. Hum. Reprod. 19, 1155–62.CrossRefGoogle ScholarPubMed
Winger, Q.A., Fuente, R.D.L., King, W.A., Armstrong, D.T. & Watson, A.J. (1997). Bovine parthenogenesis is characterized by abnormal chromosomal complements: Implications for maternal and paternal co-dependence during early bovine development. Dev. Genet. 21, 160–6.3.0.CO;2-5>CrossRefGoogle ScholarPubMed
Wrenzycki, C., Wells, D., Herrmann, D., Miller, A., Oliver, J., Tervit, R. & Niemann, H. (2001). Nuclear transfer protocol affects messenger RNA expression patterns in cloned bovine blastocysts. Biol. Reprod. 65, 309–17.CrossRefGoogle ScholarPubMed
Yamazaki, W., Ferreira, C.R., Meo, S.C., Leal, C.L.V., Meirelles, F.V. & Garcia, J.M. (2005). Use of strontium in the activation of bovine oocytes reconstructed by somatic cell nuclear transfer. Zygote 13, 295–302.CrossRefGoogle ScholarPubMed
Yang, X., Kubota, C., Suzuki, H., Taneja, M., Bols, P.E.J. & Presicce, G.A. (1998). Control of oocyte maturation in cows—biological factors. Theriogenology 49, 471–82.CrossRefGoogle ScholarPubMed
Yang, X.-Y., Li, H., Ma, Q.-W., Yan, J.-B., Zhao, J.-G., Li, H.-W., Shen, H.-Q., Liu, H.-F., Huang, Y., Huang, S.-Z., Zeng, Y.-T. & Zeng, F. (2006). Improved efficiency of bovine cloning by autologous somatic cell nuclear transfer. Reproduction 132, 733–9.CrossRefGoogle ScholarPubMed
Zhang, D., Pan, L., Yang, L.-H., He, X.-K., Huang, X.-Y. & Sun, F.-Z. (2005). Strontium promotes calcium oscillations in mouse meiotic oocytes and early embryos through InsP3 receptors, and requires activation of phospholipase and the synergistic action of InsP3. Hum. Reprod. 20, 3053–61.CrossRefGoogle ScholarPubMed