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A combined treatment with ethanol and 6-dimethylaminopurine is effective for the activation and further embryonic development of oocytes from Sprague-Dawley and Wistar rats

Published online by Cambridge University Press:  01 February 2009

Daisuke Sano ,
Yuki Yamamoto ,
Tomo Samejima ,
Yasunari Seita ,
Tomo Inomata ,
Junya Ito  and
Naomi Kashiwazaki
Daisuke Sano
Affiliation:
Laboratory of Animal Reproduction, School of Veterinary Medicine, Azabu University.
Yuki Yamamoto
Affiliation:
Laboratory of Animal Reproduction, School of Veterinary Medicine, Azabu University.
Tomo Samejima
Affiliation:
Laboratory of Animal Reproduction, School of Veterinary Medicine, Azabu University.
Yasunari Seita
Affiliation:
Laboratory of Animal Reproduction, School of Veterinary Medicine, Azabu University.
Tomo Inomata
Affiliation:
Laboratory of Experimental Animal Science, School of Veterinary Medicine, Azabu University.
Junya Ito*
Affiliation:
Laboratory of Animal Reproduction, School of Veterinary Medicine, Azabu University, 1–17–71 Fuchinobe, Sagamihara, Kanagawa 229–8501, Japan. Laboratory of Animal Reproduction, School of Veterinary Medicine, Azabu University.
Naomi Kashiwazaki
Affiliation:
Laboratory of Animal Reproduction, School of Veterinary Medicine, Azabu University.
*
All correspondence to: Junya Ito. Laboratory of Animal Reproduction, School of Veterinary Medicine, Azabu University, 1–17–71 Fuchinobe, Sagamihara, Kanagawa 229–8501, Japan. Tel: +81 42 850 2484. Fax: +81 42 769 1762. e-mail: [email protected]
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Summary

In nuclear-transferred or round spermatid-injected oocytes, artificial activation is required for further development in mammals. Although strontium chloride is widely used as the reagent for inducing oocyte activation in mice, the optimal method for oocyte activation remains controversial in rats because ovulated rat oocytes are spontaneously activated in vitro before artificial activation is applied. In our previous study, we found that cytostatic factor activity, which is indispensable for arrest at the MII stage, is potentially low in rats and that this activity differs greatly between two outbred rats (Slc: Sprague-Dawley (SD) and Crj: Wistar). Therefore, it is necessary to establish an optimal protocol for oocyte activation independent of strains. Given that comparative studies of the in vitro development of oocytes activated by different activation protocols are very limited, we compared four different protocols for oocyte activation (ethanol, ionomycin, strontium and electrical pulses) in two different SD and Wistar rats. Our results show that oocytes derived from SD rats have significantly higher cleavage and blastocyst formation than those from Wistar rats independent of activation regimes. In both types of rat, ethanol treatment provided significantly higher developmental ability at cleavage and blastocyst formation compared to the other activation protocols. However, the initial culture in a fertilization medium (high osmolarity mR1ECM) for 24 h showed a detrimental effect on the further in vitro development of parthenogenetic rat oocytes. Taken together, our results show that ethanol treatment is the optimal protocol for the activation of rat oocytes in SD and Wistar outbred rats. Our data also suggest that high-osmolarity media are inadequate for the in vitro development of parthenogenetically activated oocytes compared with fertilized oocytes.

Keywords

DevelopmentEthanolOocytesParthenogenetic activationRat
Type
Research Article
Information
Zygote , Volume 17 , Issue 1 , February 2009 , pp. 29 - 36
Copyright
Copyright © Cambridge University Press 2008

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References

Barr, K.J., Garrill, A., Jones, D.H., Orlowski, J. & Kidder, G.M. (1998). Contributions of Na+/H+ exchanger isoforms to preimplantation development of the mouse. Mol. Reprod. Dev. 50, 146–53.3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Borsuk, E. (1991). Anucleate fragments of parthenogenetic eggs and of maturing oocytes contain complementary factors required for development of a male pronucleus. Mol. Reprod. Dev. 29, 150–6.CrossRefGoogle ScholarPubMed
Brind, S., Swann, K. & Carroll, J. (2000). Inositol 1,4,5-trisphosphate receptors are downregulated in mouse oocytes in response to sperm or adenophostin A but not to increases in intracellular Ca2+ or egg activation. Dev. Biol. 223, 251–65.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
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
Ducibella, T. (1998). Biochemical and cellular insights into the temporal window of normal fertilization. Theriogenology 49, 53–65.CrossRefGoogle ScholarPubMed
Hirabayashi, M., Kato, M., Ishikawa, A., Kaneko, R., Yagi, T. & Hochi, S. (2005). Factors affecting production of transgenic rats by ICSI-mediated DNA transfer, effects of sonication and freeze-thawing of spermatozoa, rat strains for sperm and oocyte donors and different constructs of exogenous DNA. Mol. Reprod. Dev. 70, 422–8.CrossRefGoogle ScholarPubMed
Inoue, K., Kohda, T., Lee, J., Ogonuki, N., Mochida, K., Noguchi, Y., Tanemura, K., Kaneko-Ishino, T., Ishino, F. & Ogura, A. (2002). Faithful expression of imprinted genes in cloned mice. Science 295, 297.CrossRefGoogle ScholarPubMed
Ito, J., Hirabayashi, M., Kato, M., Takeuchi, A., Ito, M., Shimada, M. & Hochi, S. (2005). Contribution of high p34cdc2 kinase activity to premature chromosome condensation of injected somatic cell nuclei in rat oocytes. Reproduction 129, 171–80.CrossRefGoogle ScholarPubMed
Ito, J., Shimada, M., Hochi, S. & Hirabayashi, M. (2007). Involvement of Ca2+-dependent proteasome in the degradation of both cyclin B1 and Mos during spontaneous activation of matured rat oocytes. Theriogenology 67, 475–85.CrossRefGoogle ScholarPubMed
Ito, J., Shimada, M. & Terada, T. (2003). Effect of protein kinase C activator on mitogen-activated protein kinase and p34cdc2 kinase activity during parthenogenetic activation of porcine oocytes by calcium ionophore. Biol. Reprod. 69, 1675–82.CrossRefGoogle ScholarPubMed
Ito, J., Shimada, M. & Terada, T. (2004). Mitogen-activated protein kinase kinase inhibitor suppresses cyclin B1 synthesis and reactivation of p34cdc2 kinase, which improves pronuclear formation rate in matured porcine oocytes activated by Ca2+ ionophore. Biol. Reprod. 70, 797–804.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Jiang, J.Y., Mizuno, S., Mizutani, E., Sasada, H. & Sato, E. (2002). Parthenogenetic activation and subsequent development of rat oocytes in vitro. Mol. Reprod. Dev. 61, 120–5.CrossRefGoogle ScholarPubMed
Kato, M., Hirabayashi, M., Aoto, T., Ito, K., Ueda, M. & Hochi, S. (2001). Strontium-induced activation regimen for art oocytes in somatic cell nuclear transplantation. J. Reprod. Dev. 48, 243–8.Google Scholar
Kato, M., Ishikawa, A., Hochi, S. & Hirabayashi, M. (2004). Effect of activation regimens for rat oocytes on full-term development after round spermatid injection. Contemp. Top. Lab. Anim. Sci. 43, 13–5.Google ScholarPubMed
Kawagishi, R., Tahara, M., Sawada, K., Morishige, K., Sakata, M., Tasaka, K. & Murata, Y. (2004). Na+/H+ exchanger-3 is involved in mouse blastocyst formation. J. Exp. Zoolog. A. Comp. Exp. Biol. 301, 767–75.CrossRefGoogle ScholarPubMed
Kishigami, S., Wakayama, S., Thuan, NV., Ohta, H., Mizutani, E., Hikichi, T., Bui, H.T., Balbach, S., Ogura, A., Boianim, M. & Wakayama, T. (2006). Production of cloned mice by somatic cell nuclear transfer. Nat. Protoc. 1, 125–38.CrossRefGoogle ScholarPubMed
Kurokawa, M., Sato, K., Wu, H., He, C., Malcuit, C., Black, S.J., Fukami, K. & Fissore, R.A. (2005). Functional, biochemical and chromatographic characterization of the complete [Ca2+]i oscillation-inducing activity of porcine sperm. Dev. Biol. 285, 376–92.CrossRefGoogle ScholarPubMed
Kurokawa, M., Yoon, S.Y., Alfandari, D., Fukami, K., Sato, K.I. & Fissore, R.A. (2007). Proteolytic processing of phospholipase Cζ and [Ca2+]i oscillations during mammalian fertilization. Dev. Biol. 312, 407–18.CrossRefGoogle ScholarPubMed
Lane, M., Baltz, J.M. & Bavister, B.D. (1998). Regulation of intracellular pH in hamster preimplantation embryos by the sodium hydrogen (Na+/H+) antiporter. Biol. Reprod. 59, 1483–90.CrossRefGoogle ScholarPubMed
Macháty, Z., Wang, W.H., Day, B.N. & Prather, R.S. (1997). Complete activation of porcine oocytes induced by the sulfhydryl reagent, thimerosal. Biol. Reprod. 57, 1123–7.CrossRefGoogle ScholarPubMed
Méo, 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
Miyazaki, S. (2006). Thirty years of calcium signals at fertilization. Semin. Cell. Dev. Biol. 17, 233–43.CrossRefGoogle ScholarPubMed
Miyoshi, K., Abeydeera, L.R., Okuda, K. & Niwa, K. (1995). Effects of osmolarity and amino acids in a chemically defined medium on development of rat one-cell embryos. J. Reprod. Fertil. 103, 27–32.CrossRefGoogle Scholar
Miyoshi, K., Funahashi, H., Okuda, K. & Niwa, K. (1994). Development of rat one-cell embryos in a chemically defined medium, effects of glucose, phosphate and osmolarity. J. Reprod. Fertil. 100, 21–6.CrossRefGoogle Scholar
Miyoshi, K., Inoue, S., Himaki, T., Mikawa, S. & Yoshida, M. (2007). Birth of cloned miniature pigs derived from somatic cell nuclear transferred embryos activated by ultrasound treatment. Mol. Reprod. Dev. 74, 1568–74.CrossRefGoogle ScholarPubMed
Mizutani, E., Jiang, J.Y., Mizuno, S., Tomioka, I., Shinozawa, T., Kobayashi, J., Sasada, H. & Sato, E. (2004). Determination of optimal conditions for parthenogenetic activation and subsequent development of rat oocytes in vitro. J. Reprod. Dev. 50, 139–46.CrossRefGoogle ScholarPubMed
Nagai, T. (1987). Parthenogenetic activation of cattle follicular oocytes in vitro with ethanol. Gamete Res. 16, 243–9.CrossRefGoogle ScholarPubMed
Naito, K., Dean, F.P. & Toyoda, Y. (1992). Comparison of histon H1 kinase activity during meiotic maturation between two types of porcine oocytes matured in different media in vitro. Biol. Reprod. 47, 43–7.CrossRefGoogle ScholarPubMed
Nakai, M., Saito, E., Takizawa, A., Akamatsu, Y., Koichi, M., Hisamatsu, S., Inomata, T., Shino, M. & Kashiwazaki, N. (2005). Offspring derived from intracytoplasmic injection of sonicated rat sperm heads. J. Mamm. Ova. Res. 22, 159–62.CrossRefGoogle Scholar
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
Ogura, A., Matsuda, J. & Yanagimachi, R. (1994). Birth of normal young after electrofusion of mouse oocytes with round spermatids. Proc. Natl. Acad. Sci. USA 91, 7460–2.CrossRefGoogle ScholarPubMed
Oh, S.H., Miyoshi, K. & Funahashi, H. (1998). Rat oocytes fertilized in modified rat 1-cell embryo culture medium containing a high sodium chloride concentration and bovine serum albumin maintain developmental ability to the blastocyst stage. Biol. Reprod. 59, 884–9.CrossRefGoogle Scholar
Roh, S., Guo, J., Malakooti, N., Morrison, J.R., Trounson, A.O. & Du, Z.T. (2003). Birth of rats following nuclear exchange at the 2-cell stage. Zygote 11, 317–21.CrossRefGoogle Scholar
Ross, P.J., Yabuuchi, A. & Cibelli, JB. (2006). Oocyte spontaneous activation in different rat strains. Cloning Stem Cells. 8, 275–82.CrossRefGoogle ScholarPubMed
Ruddock, N.T., Macháty, Z., Milanick, M. & Prather, R.S. (2000). Mechanism of intracellular pH increase during parthenogenetic activation of In vitro matured porcine oocytes. Biol. Reprod. 63, 488–92.CrossRefGoogle ScholarPubMed
Schultz, R.M. & Kopf, G.S. (1995). Molecular basis of mammalian egg activation. Curr. Top. Dev. Biol. 30, 21–62.CrossRefGoogle ScholarPubMed
Shinozawa, T., Mizutani, E., Tomioka, I., Kawahara, M., Sasada, H., Matsumoto, H. & Sato, E. (2004). Differential effect of recipient cytoplasm for microtubule organization and preimplantation development in rat reconstituted embryos with two-cell embryonic cell nuclear transfer. Mol. Reprod. Dev. 68, 313–8.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
Tse, C.M., Levine, S.A., Yun, C.H., Khurana, S. & Donowitz, M. (1994). Na+/H+ exchanger-2 is an O-linked but not an N-linked sialoglycoprotein. Biochemistry 33, 12954–61.CrossRefGoogle ScholarPubMed
Tunquist, B.J., Maller, J.L. (2003). Under arrest, cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev. 17, 683–710.CrossRefGoogle ScholarPubMed
Wakayama, T., Perry, A.C., Zuccotti, M., Johnson, K.R. & Yanagimachi, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394, 369–74.CrossRefGoogle ScholarPubMed
Whittingham, D.G. (1971). Culture of mouse ova. J. Reprod. Fertil. Suppl. 14, 7–21.Google ScholarPubMed
Yamanaka, K., Sugimura, S., Wakai, T., Shoji, T., Kobayashi, J., Sasada, H. & Sato, E. (2007). Effect of activation treatments on actin filament distribution and in vitro development of miniature pig somatic cell nuclear transfer embryos. J. Reprod. Dev. 53, 791–800.CrossRefGoogle ScholarPubMed
Yamauchi, N., Sasada, H., Sugawara, S. & Nagai, T. (1996). Effect of culture conditions on artificial activation of porcine oocytes matured in vitro. Reprod. Fertil. Dev. 8, 1153–6.CrossRefGoogle ScholarPubMed
Yun, C.H., Tse, C.M., Nath, S.K., Levine, S.A., Brant, S.R. & Donowitz, M. (1995). Mammalian Na+/H+ exchanger gene family, structure and function studies. Am. J. Physiol. 269, G1–11.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