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Generation of parthenogenetic goat blastocysts: effects of different activation methods and culture media

Published online by Cambridge University Press:  10 January 2014

Hruda Nanda Malik
Affiliation:
Animal Biotechnology Center, National Dairy Research Institute, Karnal, India
Dinesh Kumar Singhal
Affiliation:
Animal Biotechnology Center, National Dairy Research Institute, Karnal, India
Shrabani Saugandhika
Affiliation:
Animal Biotechnology Center, National Dairy Research Institute, Karnal, India
Amit Dubey
Affiliation:
Animal Biotechnology Center, National Dairy Research Institute, Karnal, India
Ayan Mukherjee
Affiliation:
Animal Biotechnology Center, National Dairy Research Institute, Karnal, India
Raxita Singhal
Affiliation:
Animal Biotechnology Center, National Dairy Research Institute, Karnal, India
Sudarshan Kumar
Affiliation:
Animal Biotechnology Center, National Dairy Research Institute, Karnal, India
Jai Kumar Kaushik
Affiliation:
Animal Biotechnology Center, National Dairy Research Institute, Karnal, India
Ashok Kumar Mohanty
Affiliation:
Animal Biotechnology Center, National Dairy Research Institute, Karnal, India
Bikash Chandra Das
Affiliation:
Indian Veterinary Research Institute, Veterinary Physiology and Climatology, Izatnagar, Bareilly, India
Sadhan Bag
Affiliation:
Indian Veterinary Research Institute, Veterinary Physiology and Climatology, Izatnagar, Bareilly, India
Subrata Kumar Bhanja
Affiliation:
Central Avian Research Institute, Poultry Housing and Management, Izatnagar, Bareilly, India
Dhruba Malakar*
Affiliation:
Animal Biotechnology Center, National Dairy Research Institute, Karnal, India
*
All correspondence to: Dhruba Malakar. Animal Biotechnology Center, National Dairy Research Institute, Karnal, India. Tel: +91 9416741839. e-mail: dhrubamalakar@gmail.com

Summary

The present study was carried out to investigate the effects of different activation methods and culture media on the in vitro development of parthenogenetic goat blastocysts. Calcium (Ca2+) ionophore, ethanol or a combination of the two, used as activating reagents, and embryo development medium (EDM), modified Charles Rosenkrans (mCR2a) medium and research vitro cleave (RVCL) medium were used to evaluate the developmental competence of goat blastocysts. Quantitative expression of apoptosis, stress and developmental competence-related genes were analysed in different stages of embryos. In RVCL medium, the cleavage rate of Ca2+ ionophore-treated oocytes (79.61 ± 0.86) was significantly (P < 0.05) higher than in ethanol (74.90 ± 1.51) or in the combination of both Ca2+ ionophore and ethanol. In mCR2a or EDM, hatched blastocyst production rate of Ca2+ ionophore-treated oocytes (8.33 ± 1.44) was significantly higher than in ethanol (6.46 ± 0.11) or in the combined treatment (6.70 ± 0.24). In ethanol, the cleavage, blastocyst and hatched blastocyst production rates in RVCL medium (74.90 ± 1.51, 18.30 ± 1.52 and 8.24 ± 0.15, respectively) were significantly higher than in EDM (67.81 ± 3.21, 14.59 ± 0.27 and 5.59 ± 0.42) or mCR2a medium (65.09 ± 1.57, 15.36 ± 0.52 and 6.46 ± 0.11). The expression of BAX, Oct-4 and GlUT1 transcripts increased gradually from 2-cell stage to blastocyst-stage embryos, whereas the transcript levels of Bcl-2 and MnSOD were significantly lower in blastocysts. In addition, different activation methods and culture media had little effect on the pattern of variation and relative abundance of the above genes in different stages of parthenogenetic activated goat embryos. In conclusion, Ca2+ ionophore as the activating agent, and RVCL as the culture medium are better than other tested options for development of parthenogenetic activated goat blastocysts.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

Alberio, R., Brero, A., Motlik, 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.Google Scholar
Allen, N.D., Barton, S.C., Hilton, K., Norris, M.L. & Surani, M.A. (1994). A functional analysis of imprinting in parthenogenetic embryonic stem cells. Development 120, 1473–82.Google Scholar
Ayabe, T., Kopf, G. & Schultz, R.M. (1995). Regulation of mouse egg activation: presence of ryanodine receptors and effects of microinjected ryanodine and cyclic ADP ribose on uninseminated and inseminated eggs. Development 121, 2233–44.Google Scholar
Bogliolo, L., Calvia, P., Leoni, G., Loi, P., Ledda, S. & Moor, R.M. (1996). Uncoupling of histone Hl activity from cell cycle progression in parthenogenetically activated sheep oocytes. In Proceedings of the Society for the Study of Fertility Annual Meeting; Nottingham, UK. Abstract 39.Google Scholar
Booth, P.J., Tan, S.J., Reipurth, R., Holm, P. & Callesen, H. (2001). Simplification of bovine somatic cell nuclear transfer by application of a zona-free manipulation technique. Cloning Stem Cells 3, 139–50.Google Scholar
Bootman, M.D. & Berridge, M.J. (1995). The elementary principles of calcium signaling. Cell 83, 675–8.Google Scholar
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, 97105.Google Scholar
Carroll, J., Jones, K.T. & Whittingham, D.G. (1996). Ca2+ release and the development of Ca2+ release mechanisms during oocyte maturation: a prelude to fertilization. Rev. Reprod. 1, 137–43.Google Scholar
Cibelli, J.B., Grant, K.A., Chapman, K.B., Cunniff, K., Worst, T., Green, H.L., Walker, S.J., Gutin, P.H., Vilner, L., Tabar, V., Dominko, T., Kane, J., Wettstein, P.J., Lanza, R.P., Studer, L., Vrana, K.E. & West, M.D. (2002). Parthenogenetic stem cells in nonhuman primates. Science 295, 819.CrossRefGoogle ScholarPubMed
Collas, F., Fissore, R., Robl, J.M., Sullivan, E.J. & Barnes, F.L. (1993). Electrically induced calcium elevation, activation and parthenogenetic development of bovine oocytes. Mol. Reprod. Dev. 34, 212–23.Google Scholar
Das, S.K., Majumdar, A.C. & Sharma, G.T. (2003). In vitro development of reconstructed goat oocytes after somatic cell nuclear transfer with fetal fibroblast cells. Small Rumin. Res. 48, 217–25.Google Scholar
De, A.K., Malakar, D., Jena, M.K., Dutta, R., Garg, S. & Akshey, Y.S. (2012). Zona-free and with-zona parthenogenetic embryo production in goat (Capra hircus) – effect of activation methods, culture systems and culture media. Livest. Sci. 143, 3542.Google Scholar
Dobrinsky, J.R., Johnson, L.A. & Rath, D. (1996). Development of a culture medium (BECM-3) for porcine embryos: effect of bovine serum albumin and fetal bovine serum on embryo development. Biol. Reprod. 55, 1069–74.Google Scholar
Du, Y., Kragh, P.M., Zhang, Y., Li, J., Schmidt, M., Bogh, I.B., Zhang, X., Purup, S., Jorgensen, A.L., Pedersen, A.M., Villemoes, K., Yang, H., Bolund, L. & Vajta, G. (2007). Piglets born from handmade cloning, an innovative cloning method without micromanipulation. Theriogenology 68, 1104–10.Google Scholar
Grabiec, A., Max, A. & Tischner, M. (2007). Parthenogenetic activation of domestic cat oocytes using ethanol, calcium ionophore, cycloheximide and a magnetic field. Theriogenology 67, 795800.Google Scholar
Hoth, M. & Penner, R. (1992). Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355, 353–5.Google Scholar
Hsieh, Y.C., Intawicha, P., Lee, K.H., Chiu, Y.T., Lo, N.W. & Ju, J.C. (2011). LIF and FGF cooperatively support stemness of rabbit embryonic stem cells derived from parthenogenetically activated embryos. Cell. Reprogram. 13, 241–55.Google Scholar
Jellerette, T., Melican, D., Butler, R., Nims, S., Ziomek, C., Fissore, R. & Gavin, W. (2006). Characterization of calcium oscillation patterns in caprine oocytes induced by IVF or an activation technique used in nuclear transfer. Theriogenology 65, 1575–86.Google Scholar
Jena, M.K., Malakar, D., De, A.K., Garg, S., Akshey, Y.S., Dutta, R., Sahu, S., Mohanty, A.K. & Kaushik, J.K. (2012). Handmade cloned and parthenogenetic goat embryos – a comparison of different culture media and donor cells. Small Ruminant Res. 105, 255–62.Google Scholar
Jurisicova, A., Latham, K.E., Casper, R.F. & Varmuza, S.L. (1998). Expression and regulation of genes associated with cell death during murine preimplantation embryo development. Mol. Reprod. Dev. 51, 243–53.Google Scholar
Kim, N.H., Simerly, C., Funahashi, H., Schatten, G., & Day, B.N. (1996). Microtubule organization in porcine oocytes during fertilization and parthenogenesis. Biol. Reprod. 54, 1397–404.Google Scholar
Kline, D. & Kline, J. (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev. Biol. 149, 80–9.Google Scholar
Lagutina, I., Lazzari, G., Duchi, R., Turini, P., Tessaro, I., Brunetti, D., Colleoni, S., Crotti, G. & Galli, C. (2007). Comparative aspects of somatic cell nuclear transfer with conventional and zona-free method in cattle, horse, pig and sheep. Theriogenology 67, 90–8.Google Scholar
Liu, L., Ju, J.C. & Yang, X. (1998). Differential inactivation of maturation promoting factor and mitogen-activated protein kinase following parthenogenetic activation in bovine oocytes. Biol. Reprod. 59, 537–45.CrossRefGoogle ScholarPubMed
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–8.Google Scholar
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.Google Scholar
Malakar, D., Das, S.K. & Goswami, S.L. (2008). Goat kids born from in vitro matured and fertilized goat embryos after transfer to surrogate mother using laparoscopy technique. Indian J. Dairy Sci. 61, 136–40.Google Scholar
Miyazaki, S. (1990). Cell signaling at fertilization of hamster eggs. J. Reprod. Fertil. Suppl. 42, 163–75.Google Scholar
Miyazaki, S., Shirakawa, K., Nakada, K. & Honda, Y. (1993). Essential role of the inositol 1,4,5 trisphosphate receptor Ca2+ release channels in Ca2+ waves and Ca2+ oscillation at fertilization in mammalian eggs. Dev. Biol. 158, 6278.Google Scholar
Moore, G.D., Kopf, G.S. & Schultz, R.M. (1995). Differential effect of activators of protein kinase C on cytoskeleton changes in mouse and hamster eggs. Dev. Biol. 170, 519–30.Google Scholar
Pashaias, L.M., Khodadadi, K., Holland, M.K. & Verma, P.J. (2010). The efficient generation of cell lines from bovine parthenotes. Cell. Reprogram. 12, 571–9.Google Scholar
Petters, R.M. & Wells, K.D. (1993). Culture of pig embryos. J. Reprod. Fertil. 48, 6173.Google Scholar
Revazova, E.S., Turovets, N.A., Kochetkova, O.D., Kindarova, L.B., Kuzmichev, L.N., Janus, J.D. & Pryzhkova, M.V. (2007). Patient-specific stem cell lines derived from human parthenogenetic blastocysts. Cloning and Stem Cells 9, 432–49.Google Scholar
Rinaudo, P., Pepperell, J.R., Buradgunta, S., Massobrio, M. & Keefe, D.L. (1997). Dissociation between intracellular calcium elevation and development of human oocytes treated with calcium ionophore. Fertil. Steril. 68, 1086–92.Google Scholar
Sato, K., Yoshida, M. & Miyoshi, K. (2005). Utility of ultrasound stimulation for activation of pig oocytes matured in vitro . Mol. Reprod. Dev. 72, 396403.Google Scholar
Shah, R.A., George, A., Singh, M.K., Kumar, D., Chauhan, M.S., Manik, R., Palta, P. & Singla, S.K. (2008). Hand-made cloned buffalo (Bubalus bubalis) embryos: comparison of different media and culture systems. Cloning and Stem Cells 10, 435–42.Google Scholar
Shiina, Y., Kaneda, M., Matsuyama, K., Tanaka, K., Hiroi, M. & Doi, K. (1993). Role of the extracellular Ca2+ on the intracellular Ca2+ changes in fertilized and activated mouse oocytes. J. Reprod. Fertil. 97, 143–50.Google Scholar
Simon, L., Veerapandian, C., Balasubramanian, S. & Subramanian, A. (2006). Somatic cell nuclear transfer in buffalos: effect of the fusion and activation protocols and embryo culture system on preimplantation embryo development. Reprod. Fertil. Dev. 18, 439–45.CrossRefGoogle ScholarPubMed
Simone, C.M., Claudia, L.V.L. & Joaquim, M.G. (2004). Activation and early parthenogenesis of bovine oocytes treated with ethanol and strontium. Ani. Reprod. Sci. 81, 3546.Google Scholar
Sun, F.J., Hoyland, J., Huang, X., Mason, W. & Moor, R.M. (1991). A comparison of intracellular changes in porcine eggs after fertilization and electroactivation. Development 115, 947–56.Google Scholar
Swann, K. & Ozil, J.P. (1994). Dynamics of the calcium signal that triggers mammalian egg activation. Int. Rev. Cytol. 1152, 183222.Google Scholar
Szollosi, M.S., Kubiak, J.Z., Debey, P., de Pennart, H., Szollosi, D. & Maro, B. (1993). Inhibition of protein kinases by 6-dimethylaminopurine accelerates the transition to interphase in activated mouse oocytes. J. Cell. Sci. 104, 861–72.Google Scholar
Tomashov-Matar, R., Tchetchik, D., Eldar, A., Kaplan-Kraicer, R., Oron, Y. & Shalgi, R. (2005). Strontium-induced rat egg activation. Reproduction 130, 467–74.Google Scholar
Varga, E., Pataki, R., Lörincz, Z., Koltai, J. & Papp, A.B. (2008). Parthenogenetic development of in vitro matured porcine oocytes treated with chemical agents. Anim. Reprod. Sci. 105, 226–33.CrossRefGoogle ScholarPubMed
Vrana, K.E., Hipp, J.D., Goss, A.M., McCool, B.A., Riddle, D.R., Walker, S.J., Wettstein, P.J., Studer, L.P., Tabar, V., Cunniff, K., Chapman, K., Vilner, L., West, M.D., Grant, K.A. & Cibelli, J.B. (2003). Nonhuman primate parthenogenetic stem cells. Proc. Natl. Acad. Sci. USA 100, 11911–6.Google Scholar
Wei, Q., Sun, Z., He, X., Tan, T., Lu, B., Guo, X., Su, B. & Ji, W. (2011). Derivation of rhesus monkey parthenogenetic embryonic stem cells and its microRNA signature. PLoS One 6, e25052.Google Scholar
White, K.L. & Yue, C. (1996). Intracellular receptors and agents that induce activation in bovine oocytes. Theriogenology 45, 91100.Google Scholar
Wright, R.W. Jr (1977). Successful culture in vitro of swine embryos to the blastocyst stage. J. Anim. Sci. 44, 854–8.Google Scholar
Xu, X.M., Hua, J.L., Jia, W.W., Huang, W., Yang, C.R. & Dou, Z.Y. (2007). Parthenogenetic activation of porcine oocytes and isolation of embryonic stem cells-like derived from parthenogenetic blastocysts. Asian-Aust. J. Anim. Sci. 20, 1510–6.Google Scholar
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I.M. & Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–9.Google Scholar
Yu, S.M., Yan, X.R, Chen, D.M., Cheng, X. & Dou, Z.Y. (2011). Isolation and characterization of parthenogenetic embryonic stem (pES) cells containing genetic background of the kunming mouse strain. Asian-Aust. J. Anim. Sci. 24, 3744.Google Scholar
Zhang, L., Hua, S. & Zhang, Y. (2007). Optimization of culture measure for bovine–bovine and goat–bovine cloned embryos in vitro . Sheng. Wu. Gong. Cheng. Xue. Bao. 23, 662–6.Google Scholar