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Analysis of specific factors generating 2-cell block in AKR mouse embryos

Published online by Cambridge University Press:  01 May 2006

Akihiro Yoneda ,
Aki Okada ,
Teruhiko Wakayama ,
Junji Ueda  and
Tomomasa Watanabe
Akihiro Yoneda*
Affiliation:
Laboratory of Animal Breeding and Reproduction, Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589, Japan.
Aki Okada
Affiliation:
Laboratory of Animal Breeding and Reproduction, Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589, Japan.
Teruhiko Wakayama
Affiliation:
Center for Developmental Biology RIKEN Kobe, 2-2-3 Minatojima-minaminachi, Kobe 650-0047, Japan.
Junji Ueda
Affiliation:
Laboratory of Animal Breeding and Reproduction, Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589, Japan.
Tomomasa Watanabe
Affiliation:
Laboratory of Animal Breeding and Reproduction, Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589, Japan.
*
All correspondence to: A. Yoneda, Laboratory of Animal Breeding and Reproduction, Graduate School of Agriculture, Hokkaido University, Sapporo, 060-8589, Japan. e-mail: ayoneda@anim.agr.hokudai.ac.jp
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Summary

The phenomenon of the developmental arrest at the 2-cell stage of 1-cell embryos from some mouse strains during in vitro culture is known as the 2-cell block. We investigated the specific factors involved in the 2-cell block of AKR embryos by means of a modified culture system, the production of reconstructed embryos by pronuclear exchange and a cross experiment. In a culture medium with phosphate, 94.6% of 1-cell embryos from the C57BL mouse strain developed to the blastocyst stage, but 95.7% of embryos from the AKR mouse strain showed 2-cell block. Phosphate-free culture medium rescued the 2-cell block of AKR embryos and accelerated the first cell cycle of the embryos. Co-culture with BRL cells and a BRL-conditioned medium fractionated below 30 kDa also rescued the 2-cell block of AKR embryos. Examinations of in vitro development of reconstructed embryos and of embryos from F1 females between AKR and C57BL strains clearly demonstrated that the AKR cytoplast caused the 2-cell block. In the backcrossed female progeny between (AKR × C57BL) F1 males and AKR females, about three-quarters of the embryos were of the 2-cell blocking phenotype and about one-quarter were of the non-blocking phenotype. These results suggest that two genes are responsible for the 2-cell block of AKR embryos.

Keywords

2-cell blockCo-cultureEmbryonic developmentGenetic factorPhosphate
Type
Research Article
Information
Zygote , Volume 14 , Issue 2 , May 2006 , pp. 169 - 179
Copyright
Copyright © Cambridge University Press 2006

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References

Abramczuk, J., Solter, D. & Koprowski, A. (1977). The beneficial effect of EDTA on development of mouse one-cell embryos in chemically defined medium. Dev. Biol. 61, 378–83.CrossRefGoogle ScholarPubMed
Aoki, F., Choi, T., Mori, M., Yamashita, M., Nagahama, Y. & Kohmoto, K. (1992). A deficiency in the mechanism for p34cdc2 protein kinase activation in mouse embryos arrested at the 2-cell stage. Dev. Biol. 154, 66–72.CrossRefGoogle Scholar
Baldacci, P.A., Richoux, V., Renard, J.P., Guenet, J.L. & Babinet, C. (1992). The locus Om, responsible for the DDK syndrome, maps close to Sigje on mouse chromosome 11. Mamm. Genome. 2, 100–5.CrossRefGoogle ScholarPubMed
Bavister, B.D. (1992). Co-culture for embryo development: is it really necessary? Hum. Reprod. 7, 1339–41.CrossRefGoogle ScholarPubMed
Carr, B.I., Huang, T.H., Itakura, K., Noel, M. & Marceau, N. (1989). TGFβ gene transcription in normal and neoplastic liver growth. J. Cell. Biochem. 39, 477–87.CrossRefGoogle Scholar
Cross, P.C. & Brinster, R.L. (1973). The sensitivity of one-cell mouse embryos to pyruvate and lactate. Exp. Cell. Res. 77, 57–62.CrossRefGoogle Scholar
Fissore, R.A., Jackson, K.V. & Kiessling, A.A. (1989). Mouse zygote development in culture medium without protein in the presence of ethylenediamine-tetraacetic acid. Biol. Reprod. 41, 835–41.CrossRefGoogle Scholar
Goddard, M.J. & Pratt, H.P. (1983). Control of events during early cleavage of the mouse embryo: an analysis of the ‘2-cell block’. J. Embryol. Exp. Morphol. 73, 111–33.Google ScholarPubMed
Haraguchi, S., Naito, K., Azuma, S., Sato, E., Nagahama, Y., Yamashita, M. & Toyoda, Y. (1996). Effects of phosphate on in vitro 2-cell block of AKR/N mouse embryos based on changes in cdc2 kinase activity and phosphorylation states. Biol. Reprod. 55, 598–603.CrossRefGoogle ScholarPubMed
Johnson, M.H. & Nasr-Esfahani, M.H. (1994). Radical solutions and cultural problem: could free oxygen radicals be responsible for the impaired development of preimplantation mammalian embryos in vitro? BioEssays 16, 31–8.CrossRefGoogle ScholarPubMed
King, R.W., Jackson, P.K. & Kirchner, M.W. (1994). Mitosis in transition. Cell 79, 563–71.CrossRefGoogle ScholarPubMed
Kwon, H.C., Yang, H.W., Hwang, K.J., Yoo, J.H., Kim, M.S., Lee, C.H., Ryu, H.S. & Oh, K.S. (1999). Effect of oxygen condition on the generation of reactive oxygen species and the development in mouse embryos cultured in vitro. J. Obstet. Gynaecol. 25, 359–66.CrossRefGoogle ScholarPubMed
Lee, D.R., Lee, J.E., Yoon, H.S., Roh, S.I. & Kim, M.K. (2001). Compaction in preimplantation mouse embryo is regulated by a cytoplasmic regulatory factor that alters between 1- and 2-cell stages in a concentration-dependent manner. J. Exp. Zool. 290, 61–71.CrossRefGoogle Scholar
Lew, D.J. & Kornbluth, S. (1996). Regulatory roles of cyclin dependent kinase phosphorylation in cell cycle control. Curr. Opin. Cell. Biol. 8, 795–804.CrossRefGoogle ScholarPubMed
Liu, L.P.S., Chan, S.T.H., Ho, P.C. & Yeung, W.S.B. (1995). Human oviductal cells produce high molecular weight factor(s) that improves the development of mouse embryo. Mol. Hum. Reprod. 10, 2781–6.CrossRefGoogle ScholarPubMed
Massague, J., Kelly, B. & Mottola, C. (1985). Stimulation by insulin-like growth factor is required for cellular transformation by type B transforming growth factor. J. Biol. Chem. 260, 4551–4.CrossRefGoogle Scholar
Mayer, J.F.J. & Fritz, H.I. (1974). The culture of preimplantation rat embryos and the production of allophenic rats. J. Reprod. Fertil. 39, 1–9.CrossRefGoogle ScholarPubMed
Minami, N., Utsumi, K. & Iritani, A. (1992). Effects of low molecular weight oviductal factors on the development of mouse one-cell embryos in vitro. J. Reprod. Fertil. 96, 735–45.CrossRefGoogle ScholarPubMed
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
Noda, Y., Matsumoto, H., Umaoka, Y., Tatsumi, K., Kishi, J. & Mori, T. (1991). Involvement of superoxide radicals in the mouse two-cell block. Mol. Reprod. Dev. 28, 356–60.CrossRefGoogle ScholarPubMed
Ohashi, A., Minami, N. & Imai, H. (2001). Nuclear accumulation of cyclin B1 in mouse two-cell embryos is controlled by the activation of cdc2. Biol. Reprod. 65, 1195–200.CrossRefGoogle ScholarPubMed
Ookata, K., Hisanaga, S., Okano, T., Tachibana, K. & Kishimoto, T. (1992). Relocation and distinct subcellular localization of p34cdc2-cyclin B complex at meiosis reinitiation in starfish oocytes. EMBO. J. 11, 1763–72.CrossRefGoogle ScholarPubMed
Petters, R.M., Johnson, B.H., Reed, M.L. & Archibong, A.E. (1990). Glucose, glutamine and inorganic phosphate in early development of the pig embryo in vitro. J. Reprod. Fertil. 89, 269–75.CrossRefGoogle ScholarPubMed
Pines, J. & Hunter, T. (1991). Human cyclin A and B1 are differentially located in the cell and undergo cell cycle-dependent nuclear transport. J. Cell. Biol. 115, 1–17.CrossRefGoogle ScholarPubMed
Pinyopummintr, T. & Bavister, B.D. (1991). In vitro-matured/in vitro-fertilized bovine oocytes can develop into morulae/blastocysts in chemically defined, protein-free culture medium. Biol. Reprod. 45, 736–42.CrossRefGoogle Scholar
Quinn, P., Barros, C. & Whittingham, D.G. (1982). Preservation of hamster oocytes to assay the fertilizing capacity of human spermatozoa. J. Reprod. Fertil. 66, 161–8.CrossRefGoogle ScholarPubMed
Renard, J.P., Baldacci, P., Richoux-Duranthon, V., Pourmin, S. & Babinet, C. (1994). A maternal factor affecting mouse blastocyst formation. Development 120, 797–802.CrossRefGoogle ScholarPubMed
Sapienza, C., Paquette, J., Pannunzio, P., Albrechtson, S. & Morgan, K. (1992). The polar-lethal Ovum mutant gene maps to the distal portion of mouse chromosome 11. Genetics 132, 241–6.CrossRefGoogle Scholar
Schini, S.A. & Bavister, B.D. (1988). Two-cell block to development of cultured hamster embryos is caused by phosphate and glucose. Biol. Reprod. 39, 1183–92.CrossRefGoogle ScholarPubMed
Seshagiri, P.B. & Bavister, B.D. (1991). Glucose and phosphate inhibit respiration and oxidative metabolism in cultured hamster eight-cell embryos: evidence for the ‘Crabtree effect’. Mol. Reprod. Dev. 30, 105–11.CrossRefGoogle ScholarPubMed
Smith, A.G. & Hooper, M.L. (1987). Buffalo rat liver cells produce a diffusible activity which inhibits the differentiation of murine embryonal carcinoma and embryonic stem cells. Dev. Biol. 121, 1–9.CrossRefGoogle ScholarPubMed
Suzuki, O., Asano, T., Yamamoto, Y., Takano, K. & Koura, M. (1996). Development in vitro of preimplantation embryos from 55 mouse strains. Reprod. Fertil. Dev. 8, 975–80.CrossRefGoogle ScholarPubMed
Toyoda, Y., Azuma, S., Itagaki, Y. & Takada, S. (1992). Strain difference in the development of preimplantation mouse embryos in a medium supplemented with superoxide dismutase or ethylenediamine tetraacetic acid. J. Mamm. Ova. Res. 9, 180–90.Google Scholar
Wakasugi, N. (1974). A genetically determined incompatibility system between spermatozoa and eggs leading to embryonic death in mice. J. Reprod. Fertil. 41, 85–94.CrossRefGoogle ScholarPubMed
Wakasugi, N., Tomita, T. & Kondo, K. (1967). Differences of fertility in reciprocal crosses between inbred strain of mice DDK, KK and NC. J. Reprod. Fertil. 13, 41–50.CrossRefGoogle ScholarPubMed
Whitten, W.K. (1971). Nutrient requirement for the culture of preimplantation mouse embryos in vitro. In Intrinsic and Extrinsic Factors in Early Mammalian Development (ed. G. Raspa), Advances in Bioscience vol. 6, pp. 129–41. New York: Pergamon Press.Google Scholar