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Effect of anisomycin, a protein synthesis inhibitor, on the in vitro developmental potential, ploidy and embryo quality of bovine ICSI embryos

Published online by Cambridge University Press:  03 May 2016

María Elena Arias
Affiliation:
Laboratory of Reproduction, Centre of Reproductive Biotechnology (CEBIOR-BIOREN), Universidad de La Frontera, Temuco, Chile.
Raúl Sánchez
Affiliation:
Laboratory of Reproduction, Centre of Reproductive Biotechnology (CEBIOR-BIOREN), Universidad de La Frontera, Temuco, Chile.
Ricardo Felmer*
Affiliation:
Laboratory of Reproduction, Centre of Reproductive Biotechnology (CEBIOR-BIOREN), Department of Agricultural Sciences and Natural Resources, Faculty of Agriculture and Forestry, Universidad de La Frontera, Montevideo 0870, P.O. Box 54-D, Temuco, Chile. Department of Agricultural Sciences and Natural Resources, Faculty of Agriculture and Forestry, Universidad de La Frontera, Temuco, Chile.
*
All correspondence to: Ricardo Felmer. Laboratory of Reproduction, Centre of Reproductive Biotechnology (CEBIOR-BIOREN), Department of Agricultural Sciences and Natural Resources, Faculty of Agriculture and Forestry, Universidad de La Frontera, Montevideo 0870, P.O. Box 54-D, Temuco, Chile. Tel: +56 45 2325591. E-mail: [email protected]

Summary

Increasing the efficiency of intracytoplasmic sperm injection (ICSI) in domestic animals has been attempted by many researchers, however embryonic development to the blastocyst stage remains low compared with that of in vitro fertilization (IVF) embryos. One of the main problems observed in cattle is inadequate oocyte activation after ICSI. The present study compared the effect of cycloheximide (CHX), 6-dimethylaminopurine (DMAP), and anisomycin (ANY) on the fertilization rate, development, ploidy and quality of bovine embryos generated by ICSI. Although no differences were observed between treatments in terms of cleavage, higher blastocyst rates were observed for ANY (37.3%) compared with CHX (21.8%, P < 0.05) and DMAP (28.6%, P > 0.05) treatments. No differences were observed in the quality of embryos as assessed by the total number of cells, their distribution to the different embryo compartments [inner cell mass (ICM) and trophectoderm (TE)], the proportion of ICM cells to the total cell numbers and terminal deoxynucleotidyl transferase dUTP nick end labelling (TUNEL)-positive cells. Similarly, no differences were observed in the normal ploidy of embryos (56, 67, and 55%) for ANY, CHX and DMAP, respectively. However, higher fertilization rates were observed for ANY (75%) and CHX (87%) treatments compared with DMAP (35%). In conclusion, ANY showed a superior developmental rate compared with CHX treatment. Although no significant differences were observed compared with an improved protocol of DMAP (2Io-DMAP), the lower fertilization rate recorded with DMAP strongly suggests that ANY could be a better alternative for oocyte activation than traditional chemical compounds used currently in ICSI.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2016 

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References

Abdalla, H., Shimoda, M., Hirabayashi, M. & Hochi, S. (2009). A combined treatment of ionomycin with ethanol improves blastocyst development of bovine oocytes harvested from stored ovaries and microinjected with spermatozoa. Theriogenology 72, 453–60.Google Scholar
Arias, M.E., Sanchez, R., Risopatron, J., Perez, L. & Felmer, R. (2014). Effect of sperm pretreatment with sodium hydroxide and dithiothreitol on the efficiency of bovine intracytoplasmic sperm injection. Reprod. Fertil. Dev. 26, 847–54.Google Scholar
Arias, M.E., Risopatrón, J., Sánchez, R. & Felmer, R. (2015). Intracytoplasmic sperm injection affects embryo developmental potential and gene expression in cattle. Reprod. Biol. 15, 3441.Google Scholar
Bevacqua, R.J., Pereyra-Bonnet, F., Fernandez-Martin, R. & Salamone, D.F. (2010). High rates of bovine blastocyst development after ICSI-mediated gene transfer assisted by chemical activation. Theriogenology 74, 922–31.Google Scholar
Bhak, J.S., Lee, S.L., Ock, S. A., Mohana Kumar, 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, 3749.Google Scholar
Catt, S.L., Catt, J.W., Gomez, M.C., Maxwell, W.M. & Evans, G. (1996). Birth of a male lamb derived from an in vitro matured oocyte fertilised by intracytoplasmic injection of a single presumptive male sperm. Vet. Rec. 139, 494–5.Google Scholar
Chung, J.T., Keefer, C.L. & Downey, B.R. (2000). Activation of bovine oocytes following intracytoplasmic sperm injection (ICSI). Theriogenology 53, 1273–84.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
Felmer, R. & Arias, M.E. (2015). Activation treatment of recipient oocytes affects the subsequent development and ploidy of bovine parthenogenetic and somatic cell nuclear transfer (SCNT) embryos. Mol. Reprod. Dev. 82, 441–9.Google Scholar
Felmer, R.N., Arias, M.E., Munoz, G.A. & Rio, J.H. (2011). Effect of different sequential and two-step culture systems on the development, quality, and RNA expression profile of bovine blastocysts produced in vitro . Mol. Reprod. Dev. 78, 403–14.CrossRefGoogle ScholarPubMed
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
Galli, C., Crotti, G., Notari, C. & Lazzari, G. (1999). High rate of activation and fertilisation following intracytoplasmic sperm injection (ICSI) in cattle. Theriogenology 51, 355.CrossRefGoogle Scholar
Galli, C., Vassiliev, I., Lagutina, I., Galli, A. & Lazzari, G. (2003). Bovine embryo development following ICSI: effect of activation, sperm capacitation and pre-treatment with dithiothreitol. Theriogenology 60, 1467–80.CrossRefGoogle ScholarPubMed
Garcia-Vazquez, F.A., Ruiz, S., Matas, C., Izquierdo-Rico, M.J., Grullon, L.A., De Ondiz, A., Vieira, L., Aviles-Lopez, K., Gutierrez-Adan, A. & Gadea, J. (2010). Production of transgenic piglets using ICSI-sperm-mediated gene transfer in combination with recombinase RecA. Reproduction 140, 259–72.Google Scholar
Goto, K., Kinoshita, A., Takuma, Y. & Ogawa, K. (1990). Fertilisation of bovine oocytes by the injection of immobilised, killed spermatozoa. Vet. Rec. 127, 517–20.Google Scholar
Hamano, K., Li, X., Qian, X.Q., Funauchi, K., Furudate, M. & Minato, Y. (1999). Gender preselection in cattle with intracytoplasmically injected, flow cytometrically sorted sperm heads. Biol. Reprod. 60, 1194–7.Google Scholar
Horiuch, T., Emuta, C., Yamauchi, Y., Oikawa, T., Numabe, T. & Yanagimachi, R. (2002). Birth of normal calves after intracytoplasmic sperm injection of bovine oocytes: a methodological approach. Theriogenology 57, 1013–24.Google Scholar
Joiakim, A., Mathieu, P.A., Elliott, A.A. & Reiners, J.J. Jr., (2004). Superinduction of CYP1A1 in MCF10A cultures by cycloheximide, anisomycin, and puromycin: a process independent of effects on protein translation and unrelated to suppression of aryl hydrocarbon receptor proteolysis by the proteasome. Mol. Pharmacol. 66, 936–47.Google Scholar
Kimura, Y. & Yanagimachi, R. (1995). Intracytoplasmic sperm injection in the mouse. Biol. Reprod. 52, 709–20.Google Scholar
Kumar, B.M., Jin, H.F., Kim, J.G., Ock, S.A., Hong, Y., Balasubramanian, S., Choe, S.Y. & Rho, G.J. (2007). Differential gene expression patterns in porcine nuclear transfer embryos reconstructed with fetal fibroblasts and mesenchymal stem cells. Dev. Dyn. 236, 435–46.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
Lazzari, G., Mari, G. & Galli, C. (2002). Synergistic effect of cicloheximide and 6-DMAP on activation of equine and bovine oocytes. Reprod. Fertil. Abst. Ser. 28, 73.Google Scholar
Li, X., Hamano, K., Qian, X.Q., Funauchi, K., Furudate, M. & Minato, Y. (1999). Oocyte activation and parthenogenetic development of bovine oocytes following intracytoplasmic sperm injection. Zygote 7, 233–7.Google Scholar
Liang, Y.Y., Ye, D.N., Laowtammathron, C., Phermthai, T., Nagai, T., Somfai, T. & Parnpai, R. (2011). Effects of chemical activation treatment on development of swamp buffalo (Bubalus bubalis) oocytes matured in vitro and fertilized by intracytoplasmic sperm injection. Reprod. Domest. Anim. 46, e67–73.CrossRefGoogle ScholarPubMed
Malcuit, C., Maserati, M., Takahashi, Y., Page, R. & Fissore, R.A. (2006). Intracytoplasmic sperm injection in the bovine induces abnormal [Ca2+]i responses and oocyte activation. Reprod. Fertil. Dev. 18, 3951.CrossRefGoogle ScholarPubMed
Montag, M., Koster, M., van der Ven, K., Bohlen, U. & van der Ven, H. (2012). The benefit of artificial oocyte activation is dependent on the fertilization rate in a previous treatment cycle. Reprod. Biomed. Online 24, 521–6.Google Scholar
Nasr-Esfahani, M. H., Deemeh, M. R. & Tavalaee, M. (2010). Artificial oocyte activation and intracytoplasmic sperm injection. Fertil. Steril. 94, 520–6.Google Scholar
Ock, S.A., Bhak, J.S., Balasubramanian, S., Lee, H.J., Choe, S.Y. & Rho, G.J. (2003). Different activation treatments for successful development of bovine oocytes following intracytoplasmic sperm injection. Zygote 11, 6976.Google Scholar
Oikawa, T., Takada, N., Kikuchi, T., Numabe, T., Takenaka, M. & Horiuchi, T. (2005). Evaluation of activation treatments for blastocyst production and birth of viable calves following bovine intracytoplasmic sperm injection. Anim. Reprod. Sci. 86, 187–94.Google Scholar
Palermo, G.D., Schlegel, P.N., Colombero, L.T., Zaninovic, N., Moy, F. & Rosenwaks, Z. (1996). Aggressive sperm immobilization prior to intracytoplasmic sperm injection with immature spermatozoa improves fertilization and pregnancy rates. Hum. Reprod. 11, 1023–9.CrossRefGoogle ScholarPubMed
Perry, A.C., Wakayama, T., Kishikawa, H., Kasai, T., Okabe, M., Toyoda, Y. & Yanagimachi, R. (1999). Mammalian transgenesis by intracytoplasmic sperm injection. Science 284, 1180–3.Google Scholar
Probst, S. & Rath, D. (2003). Production of piglets using intracytoplasmic sperm injection (ICSI) with flow cytometrically sorted boar semen and artificially activated oocytes. Theriogenology 59, 961–73.Google Scholar
Rho, G.J., Kawarsky, S., Johnson, W.H., Kochhar, K. & Betteridge, K.J. (1998a). Sperm and oocyte treatments to improve the formation of male and female pronuclei and subsequent development following intracytoplasmic sperm injection into bovine oocytes. Biol. Reprod. 59, 918–24.Google Scholar
Rho, G.J., Wu, B., Kawarsky, S., Leibo, S.P. & Betteridge, K.J. (1998b). Activation regimens to prepare bovine oocytes for intracytoplasmic sperm injection. Mol. Reprod. Dev. 50, 485–92.Google Scholar
Rodger, J.C., Paris, D.B., Czarny, N.A., Harris, M.S., Molinia, F.C., Taggart, D.A., Allen, C.D. & Johnston, S.D. (2009). Artificial insemination in marsupials. Theriogenology 71, 176–89.Google Scholar
Ross, P.J., Rodriguez, R.M., Iager, A.E., Beyhan, Z., Wang, K., Ragina, N.P., Yoon, S.Y., Fissore, R.A. & Cibelli, J.B. (2009). Activation of bovine somatic cell nuclear transfer embryos by PLCZ cRNA injection. Reproduction 137, 427–37.Google Scholar
Salamone, D., Baranao, L., Santos, C., Bussmann, L., Artuso, J., Werning, C., Prync, A., Carbonetto, C., Dabsys, S., Munar, C., Salaberry, R., Berra, G., Berra, I., Fernandez, N., Papouchado, M., Foti, M., Judewicz, N., Mujica, I., Munoz, L., Alvarez, S.F., Gonzalez, E., Zimmermann, J., Criscuolo, M. & Melo, C. (2006). High level expression of bioactive recombinant human growth hormone in the milk of a cloned transgenic cow. J. Biotechnol. 124, 469–72.Google Scholar
Suttner, R., Zakhartchenko, V., Stojkovic, P., Muller, S., Alberio, R., Medjugorac, I., Brem, G., Wolf, E. & Stojkovic, M. (2000). Intracytoplasmic sperm injection in bovine: effects of oocyte activation, sperm pretreatment and injection technique. Theriogenology 54, 935–48.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
Tesarik, J. & Sousa, M. (1995). Key elements of a highly efficient intracytoplasmic sperm injection technique: Ca2+ fluxes and oocyte cytoplasmic dislocation. Fertil. Steril. 64, 770–6.Google Scholar
van Soom, A., Ysebaert, M.T. & de Kruif, A. (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, 4756.Google Scholar
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, 292301.CrossRefGoogle ScholarPubMed
Wei, H. & Fukui, Y. (2002). Births of calves derived from embryos produced by intracytoplasmic sperm injection without exogenous oocyte activation. Zygote 10, 149–53.Google Scholar
Wells, D.N., Misica, P.M. & Tervit, H.R. (1999). Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biol. Reprod. 60, 9961005.CrossRefGoogle ScholarPubMed
Yanagimachi, R. (1994). Mammalian fertilization. In The Physiology of Reproduction, 2nd edn (ed. Knobil, E.N.J.) pp. 189317. New York: Raven Press.Google Scholar