Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-10T11:38:50.718Z Has data issue: false hasContentIssue false

In vitro development of goat parthenogenetic and somatic cell nuclear transfer embryos derived from different activation protocols

Published online by Cambridge University Press:  08 June 2009

Jitong Guo*
Affiliation:
Monash Immunology and Stem Cell Laboratories (MISCL), Building 75, Monash University, Wellington Road, Clayton, Victoria 3800, Australia. Monash Immunology and Stem Cell Laboratories (MISCL), Monash University, Wellington Road, Clayton, Victoria 3800, Australia.
Fengjun Liu
Affiliation:
Institute of Bioengineering, Northwest Science and Technology University of Agriculture and Forestry, Yangling, 712100, China.
Zekun Guo
Affiliation:
Institute of Bioengineering, Northwest Science and Technology University of Agriculture and Forestry, Yangling, 712100, China.
Yu Li
Affiliation:
Department of Biology, Inner Mongolia University, Huhhot, 010021, China.
Zhixing An
Affiliation:
Institute of Bioengineering, Northwest Science and Technology University of Agriculture and Forestry, Yangling, 712100, China.
Xuefeng Li
Affiliation:
College of Life Science, South China Normal University, Guangzhou, 510631, China.
Yuqiang Li
Affiliation:
Institute of Bioengineering, Northwest Science and Technology University of Agriculture and Forestry, Yangling, 712100, China.
Yong Zhang
Affiliation:
Institute of Bioengineering, Northwest Science and Technology University of Agriculture and Forestry, Yangling, 712100, China.
*
All correspondence to: J Guo. Monash Immunology and Stem Cell Laboratories (MISCL), Building 75, Monash University, Wellington Road, Clayton, Victoria 3800, Australia. Tel: +61 3 99050746. Fax: +61 3 99050680. e-mail: jitong.guo@med.monash.edu.au

Summary

Oocyte activation is an essential step in animal cloning to allow subsequent development of the reconstructed embryos. A special activation protocol is required for different animal species. The present study investigated low temperature, electrical pulses, ethanol, ionomycin and strontium for goat oocyte activation in order to optimize the protocols. We found, as a result, effective activation and parthenogenetic development of goat oocytes that had been derived from ionomycin, strontium and electrical pulse groups. Within each group 79.3–81.6%, 2.2–78.8% and 65.5% of the oocytes cleaved and 16.2–24.8%, 0–15.6% and 11.1% of the cleaved embryos developed into blastocysts when the oocytes were activated by ionomycin combined with 6-dimethylaminopurine, strontium plus cytochalasin B and electrical pulses combined with cytochalasin B, respectively. However, low temperature and ethanol were both unable to activate goat oocytes under our experimental conditions. When ionomycin combined with 6-dimethylaminopurine and strontium plus cytochalasin B was applied to activate somatic cell nuclear transfer embryos derived from cultured cumulus, 51.0% and 72.5% of the embryos cleaved, respectively. After transfer of 4-cell embryos into recipients, one (1/19 and 1/7) of the recipients from each group was found to be pregnant as detected by ultrasound, but both of these recipients lost the embryos between 45 and 60 days of pregnancy.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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

Apimeteetumrong, M., Thuangsanthia, A., Leingcharoen, N., Yiengvisavakul, V., Harintharanon, A., Kunavongkrit, A., Sumretprasong, J., Vignon, X. & Techakumphu, M. (2004). The effect of activation protocols on the development of cloned goat embryos. J. Vet. Med. Sci./Jap. Soc. Vet. Sci. 66, 1529–34.CrossRefGoogle ScholarPubMed
Baguisi, A., Behboodi, E., Melican, D.T., Pollock, J.S., Destrempes, M.M., Cammuso, C., Williams, J.L., Nims, S.D., Porter, C.A., Midura, P., Palacios, M.J., Ayres, S.L., Denniston, R.S., Hayes, M.L., Ziomek, C.A., Meade, H.M., Godke, R.A., Gavin, W.G., Overstrom, E.W. & Echelard, Y. (1999). Production of goats by somatic cell nuclear transfer. Nat. Biotechnol. 17, 456–61.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, 8490.CrossRefGoogle ScholarPubMed
Chang, M.C. (1954). development of parthenogenetic rabbit blastocysts induced by low temperature storage of unfertilized ova. J. Exp. Zool. 125, 127–9.CrossRefGoogle Scholar
Che, L., Lalonde, A. & Bordignon, V. (2007). Chemical activation of parthenogenetic and nuclear transfer porcine oocytes using ionomycin and strontium chloride. Theriogenology 67, 1297–304.CrossRefGoogle ScholarPubMed
Cheng, W.M., Sun, X.L., An, L., Zhu, S.E., Li, X.H., Li, Y. & Tian, J.H. (2007). Effect of different parthenogenetic activation methods on the developmental competence of in vitro matured porcine oocytes. Anim. Biotechnol. 18, 131–41.CrossRefGoogle ScholarPubMed
Collas, P., Fissore, R., Robl, J.M., Sullivan, E.J. & Barnes, F.L. (1993a). Electrically induced calcium elevation, activation and parthenogenetic development of bovine oocytes. Mol. Reprod. Dev. 34, 212–23.CrossRefGoogle ScholarPubMed
Collas, P., Sullivan, E.J. & Barnes, F.L. (1993b). Histone H1 kinase activity in bovine oocytes following calcium stimulation. Mol. Reprod. Dev. 34, 224–31.CrossRefGoogle ScholarPubMed
Cuthbertson, K.S. (1983). Parthenogenetic activation of mouse oocytes in vitro with ethanol and benzyl alcohol. J. Exp. Zool. 226, 311–4.CrossRefGoogle ScholarPubMed
Cuthbertson, K.S., Whittingham, D.G. & Cobbold, P.H. (1981). Free Ca2+ increases in exponential phases during mouse oocyte activation. Nature 294, 754–7.CrossRefGoogle ScholarPubMed
Das, S.K. & Majumdar, A.C. (2003). Effect of different electric impulses on development of in-vitro matured goat oocytes reconstructed with fetal fibroblast cell. Indian J. Anim. Sci. 73, 1219–23.Google Scholar
Didion, B.A., Martin, M.J. & Markert, C.L. (1990). Parthenogenetic activation of mouse and pig oocytes matured in vitro. Theriogenology 33, 1165–75.CrossRefGoogle Scholar
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 ScholarPubMed
Fraser, L.R. (1987). Strontium supports capacitation and the acrosome reaction in mouse sperm and rapidly activates mouse eggs. Gamete Res. 18, 363–74.CrossRefGoogle ScholarPubMed
Fukui, Y., Sawai, K., Furudate, M., Sato, N., Iwazumi, Y. & Ohsaki, K. (1992. Parthenogenetic development of bovine oocytes treated with ethanol and cytochalasin B after in vitro maturation. Mol. Reprod. Dev. 33, 357–62.CrossRefGoogle ScholarPubMed
Grupen, C.G., Verma, P.J., Du, Z.T., McIlfatrick, S.M., Ashman, R.J. & Nottle, M.B. (1999). Activation of in vivo- and in vitro-derived porcine oocytes by using multiple electrical pulses. Reprod. Fertil. Dev. 11, 457–62.CrossRefGoogle ScholarPubMed
Guo, J.T., An, Z.X., Yu, L., Li, X.F., Li, Y.Q., Guo, Z.K. & Zhang, Y. (2002). Cloned goats (Capra hircus) from adult ear cells. Science in China Series C – Life Sciences 45, 260–7.CrossRefGoogle ScholarPubMed
Jones, K.T., Carroll, J. & Whittingham, D.G. (1995). Ionomycin, thapsigargin, ryanodine and sperm induced Ca2+ release increase during meiotic maturation of mouse oocytes. J. Biol. Chem. 270, 6671–7.CrossRefGoogle ScholarPubMed
Kaufman, M.H. (1983). Early Mammalian Development: Parthenogenetic Studies. Cambridge: Cambridge University Press.Google Scholar
Keefer, C.L., Baldassarre, H., Keyston, R., Wang, B., Bhatia, B., Bilodeau, A.S., Zhou, J.F., Leduc, M., Downey, B.R., Lazaris, A. & Karatzas, C.N. (2001). Generation of dwarf goat (Capra hircus) clones following nuclear transfer with transfected and nontransfected fetal fibroblasts and in vitro-matured oocytes. Biol. Reprod. 64, 849–56.CrossRefGoogle ScholarPubMed
Kishigami, S. & Wakayama, T. (2007). Efficient strontium-induced activation of mouse oocytes in standard culture media by chelating calcium. J. Reprod. Dev. 53, 1207–15.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
Kubiak, J., Paldi, A., Weber, M. & Maro, B. (1991). Genetically identical parthenogenetic mouse embryos produced by inhibition of the first meiotic cleavage with cytochalasin D. Development 111, 763–9.CrossRefGoogle ScholarPubMed
Lan, G.C., Han, D., Wu, Y.G., Han, Z.B., Ma, S.F., Liu, X.Y., Chang, C.L. & Tan, J.H. (2005). Effects of duration, concentration and timing of ionomycin and 6-dimethylaminopurine (6-DMAP) treatment on activation of goat oocytes. Mol. Reprod. Dev. 71, 380–8.CrossRefGoogle ScholarPubMed
Lan, G.C., Chang, Z.L., Luo, M.J., Jiang, Y.L., Han, D., Wu, Y.G., Han, Z.B., Ma, S.F. & Tan, J.H. (2006). Production of cloned goats by nuclear transfer of cumulus cells and long-term cultured fetal fibroblast cells into abattoir-derived oocytes. Mol. Reprod. Dev. 73, 834–40.CrossRefGoogle ScholarPubMed
Ledda, S., Loi, P., Bogliolo, L., Moor, R.M. & Fulka, J. Jr (1996). The effect of 6-dimethylaminopurine (6-DMAP) on DNA synthesis in activated mammalian oocytes. Zygote 4, 79.CrossRefGoogle ScholarPubMed
Li, X., An, Z., Guo, J. & Zhang, Y. (2002). Effect of different chemical activations on the development of bovine parthenogenetic embryos. J. Northwest Sci-Tech Univ. Agricul. Forest. (Natural Science Edition) 30, 43–7.Google Scholar
Loi, P., Ledda, S., Fulka, J. Jr., Cappai, P. & Moor, R.M. (1998). Development of parthenogenetic and cloned ovine embryos: effect of activation protocols. Biol. Reprod. 58, 1177–87.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
Melican, D., Butler, R., Hawkins, N., Chen, L.H., Hayden, E., Destrempes, M., Williams, J., Lewis, T., Behboodi, E., Ziomek, C., Meade, H., Echelard, Y. & Gavin, W. (2005). Effect of serum concentration, method of trypsinization and fusion/activation utilizing transfected fetal cells to generate transgenic dairy goats by somatic cell nuclear transfer. Theriogenology 63, 1549–63.CrossRefGoogle ScholarPubMed
Meo, S.C., Leal, C.L. & Garcia, J.M. (2004). Activation and early parthenogenesis of bovine oocytes treated with ethanol and strontium. Anim. Reprod. Sci. 81, 3546.CrossRefGoogle ScholarPubMed
Meo, S.C., Yamazaki, W., Leal, C.L., 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. & Garcia, J.M. (2007). Parthenogenetic activation of bovine oocytes using single and combined strontium, ionomycin and 6-dimethylaminopurine treatments. Zygote 15, 295306.CrossRefGoogle ScholarPubMed
Moor, R.M. & Crosby, I.M. (1985). Temperature-induced abnormalities in sheep oocytes during maturation. J. Reprod. Fertil. 75, 467–73.CrossRefGoogle ScholarPubMed
Nagai, T. (1987). Parthenogenetic activation of cattle follicular oocytes in vitro with ethanol. Gamete Res. 16, 243–9.CrossRefGoogle ScholarPubMed
O'Neill, G.T., Rolfe, L.R. & Kaufman, M.H. (1991). Developmental potential and chromosome constitution of strontium-induced mouse parthenogenones. Mol. Reprod. Dev. 30, 214–9.CrossRefGoogle ScholarPubMed
Ongeri, E.M., Bormann, C.L., Butler, R.E., Melican, D., Gavin, W.G., Echelard, Y., Krisher, R.L. & Behboodi, E. (2001). Development of goat embryos after in vitro fertilization and parthenogenetic activation by different methods. Theriogenology 55, 1933–45.CrossRefGoogle ScholarPubMed
Onodera, M. & Tsunoda, Y. (1989). Parthenogenetic activation of mouse and rabbit eggs by electric stimulation in vitro. Gamete Res. 22, 277–83.CrossRefGoogle ScholarPubMed
Ozil, J.P. (1990). The parthenogenetic development of rabbit oocytes after repetitive pulsatile electrical stimulation. Development 109, 117–27.CrossRefGoogle ScholarPubMed
Powell, R. & Barnes, F.L. (1992). The kinetics of oocyte activation and polar body formation in bovine embryo clones. Mol. Reprod. Dev. 33, 53–8.CrossRefGoogle ScholarPubMed
Presicce, G.A. & Yang, X. (1994). Parthenogenetic development of bovine oocytes matured in vitro for 24 hr and activated by ethanol and cycloheximide. Mol. Reprod. Dev. 38, 380–5.CrossRefGoogle ScholarPubMed
Rosenkrans, C.F. Jr. & First, N.L. (1994). Effect of free amino acids and vitamins on cleavage and developmental rate of bovine zygotes in vitro. J. Anim. Sci. 72, 434–7.CrossRefGoogle ScholarPubMed
Rosenkrans, C.F. Jr., Zeng, G.Q., GT, M.C., Schoff, P.K. & First, N.L. (1993). Development of bovine embryos in vitro as affected by energy substrates. Biol. Reprod. 49, 459–62.CrossRefGoogle ScholarPubMed
Shen, P.C., Lee, S.N., Wu, J.S., Huang, J.C., Chu, F.H., Chang, C.C., Kung, J.C., Lin, H.H., Chen, L.R., Shiau, J.W., Yen, N.T. & Cheng, W.T. (2006). The effect of electrical field strength on activation and development of cloned caprine embryos. Anim. Reprod. Sci. 92, 310–20.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
Tacitus, C. (1937). Histories and Annals (transl. Moore, C.H. & Jackson, J.). Cambridge: Harvard University Press.Google Scholar
Tateno, H. & Kamiguchi, Y. (1997). Parthenogenetic activation of Chinese hamster oocytes by chemical stimuli and its cytogenetic evaluation. Mol. Reprod. Dev. 47, 72–8.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Tesarik, J. & Sousa, M. (1995). More than 90% fertilization rates after intracytoplasmic sperm injection and artificial induction of oocyte activation with calcium ionophore. Fertil. Steril. 63, 343–9.CrossRefGoogle ScholarPubMed
Tomashov-Matar, R., Tchetchik, D., Eldar, A., Kaplan-Kraicer, R., Oron, Y. & Shalgi, R. (2005). Strontium-induced rat egg activation. Reproduction 130, 467–74.CrossRefGoogle ScholarPubMed
Vitullo, A.D. & Ozil, J.P. (1992). Repetitive calcium stimuli drive meiotic resumption and pronuclear development during mouse oocyte activation. Dev. Biol. 151, 128–36.CrossRefGoogle ScholarPubMed
Wang, W.H., Machaty, Z., Abeydeera, L.R., Prather, R.S. & Day, B.N. (1998). Parthenogenetic activation of pig oocytes with calcium ionophore and the block to sperm penetration after activation. Biol. Reprod. 58, 1357–66.CrossRefGoogle ScholarPubMed
Winston, N.J. & Maro, B. (1995). Calmodulin-dependent protein kinase II is activated transiently in ethanol-stimulated mouse oocytes. Dev. Biol. 170, 350–2.CrossRefGoogle ScholarPubMed
Winston, N., Johnson, M., Pickering, S. & Braude, P. (1991). Parthenogenetic activation and development of fresh and aged human oocytes. Fertil. Steril. 56, 904–12.CrossRefGoogle ScholarPubMed
Yamazaki, W., Ferreira, C.R., Meo, S.C., Leal, C.L., Meirelles, F.V. & Garcia, J.M. (2005). Use of strontium in the activation of bovine oocytes reconstructed by somatic cell nuclear transfer. Zygote 13, 295302.CrossRefGoogle ScholarPubMed
Yang, X., Presicce, G.A., Moraghan, L., Jiang, S.E. & Foote, R.H. (1994). Synergistic effect of ethanol and cycloheximide on activation of freshly matured bovine oocytes. Theriogenology 41, 395403.CrossRefGoogle ScholarPubMed
Zakhartchenko, V., Alberio, R., Stojkovic, M., Prelle, K., Schernthaner, W., Stojkovic, P., Wenigerkind, H., Wanke, R., Duchler, M., Steinborn, R., Mueller, M., Brem, G. & Wolf, E. (1999). Adult cloning in cattle: potential of nuclei from a permanent cell line and from primary cultures. Mol. Reprod. Dev. 54, 264–72.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed