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Vertebrate reproductive science and technology
RESEARCH ARTICLE (Open Access)

Characterisation of bovine embryos following prolonged culture in embryonic stem cell medium containing leukaemia inhibitory factor

Misa Hosoe A B H , Tadashi Furusawa A , Ken-Go Hayashi B , Toru Takahashi C , Yutaka Hashiyada D E , Keiichiro Kizaki C , Kazuyoshi Hashizume C , Tomoyuki Tokunaga A , Shuichi Matsuyama F G and Ryosuke Sakumoto B
+ Author Affiliations
- Author Affiliations

A Institute of Agrobiological Sciences, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-8602, Japan.

B Institute of Livestock and Grassland Science, National Agriculture and Food Research Organization, Tsukuba, Ibaraki 305-0901, Japan.

C Department of Veterinary Medicine, Faculty of Agriculture, Iwate University, Iwate 020-8550, Japan.

D National Livestock Breeding Center, Nishigo, Fukushima 961-8511, Japan.

E Ishikawa Prefectural University, Nono, Ishikawa, 921-8836, Japan.

F Institute of Livestock and Grassland Science, National Agriculture and Food Reasarch Organization, Nasushiobara, Tochigi 329-2793, Japan.

G Nagoya University, Nagoya, Aichi 464-8601, Japan.

H Corresponding author. Email: hosoe@affrc.go.jp

Reproduction, Fertility and Development 31(6) 1157-1165 https://doi.org/10.1071/RD18343
Submitted: 25 August 2018  Accepted: 2 February 2019   Published: 29 April 2019

Journal Compilation © CSIRO 2019 Open Access CC BY-NC-ND

Abstract

In order to help elucidate the process of epiblast and trophoblast cell differentiation in bovine embryos in vitro, we attempted to develop a suitable culture medium to allow extended embryo culture. Day 7 bovine blastocysts developed in conventional medium were cultured further in embryonic stem cell medium with or without leukaemia inhibitory factor (LIF) until Day 23. At Day 14, the expression of octamer-binding transcription factor 3/4 (OCT3/4) and VIMENTIN was significantly higher in embryos cultured with than without LIF, but embryonic disc formation was not observed. Although expression of SRY (sex determining region Y)-box 17 (SOX17) mRNA was significantly lower in Day 14 embryos cultured with and without LIF than in in vivo embryos, hypoblast cells formed just inside the trophoblast cells of the in vitro-cultured embryos. On Day 23, expression of placental lactogen (PL) and prolactin-related protein 1 (PRP1) was not affected by LIF in in vitro-cultured embryos, levels of both genes were significantly lower in the in vitro than in vivo embryos. Similar to in vivo embryos, binucleate cell clusters seen in Day 23 in vitro-cultured embryos were composed of PL-negative and -positive cells. These results suggest that our culture system partially reproduced the differentiation process of trophoblast cells in vivo.

Additional keywords: binucleate cell, embryo differentiation, epiblast, trophoblast.


References

Alexopoulos, N. I., Vajta, G., Maddox-Hyttel, P., French, A. J., and Trounson, A. O. (2005). Stereomicroscopic and histological examination of bovine embryos following extended in vitro culture. Reprod. Fertil. Dev. 17, 799–808.
Stereomicroscopic and histological examination of bovine embryos following extended in vitro culture.Crossref | GoogleScholarGoogle Scholar | 16476207PubMed |

Berg, D. K., Smith, C. S., Pearton, D. J., Wells, D. N., Broadhurst, R., Donnison, M., and Pfeffer, P. L. (2011). Trophectoderm lineage determination in cattle. Dev. Cell 20, 244–255.
Trophectoderm lineage determination in cattle.Crossref | GoogleScholarGoogle Scholar | 21316591PubMed |

Blomberg, L., Hashizume, K., and Viebahn, C. (2008). Blastocyst elongation, trophoblastic differentiation, and embryonic pattern formation. Reproduction 135, 181–195.
Blastocyst elongation, trophoblastic differentiation, and embryonic pattern formation.Crossref | GoogleScholarGoogle Scholar | 18239048PubMed |

Brandão, D. O., Maddox-Hyttel, P., Løvendahl, P., Rumpf, R., Stringfellow, D., and Callesen, H. (2004). Post hatching development: a novel system for extended in vitro culture of bovine embryos. Biol. Reprod. 71, 2048–2055.
Post hatching development: a novel system for extended in vitro culture of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 15329327PubMed |

Brinkhof, B., van Tol, H. T. A., Groot Koerkamp, M. J. A., Wubbolts, R. W., Haagsman, H. P., and Roelen, B. A. J. (2017). Characterization of bovine embryos cultured under conditions appropriate for sustaining human naïve pluripotency. PLoS One 12, e0172920.
Characterization of bovine embryos cultured under conditions appropriate for sustaining human naïve pluripotency.Crossref | GoogleScholarGoogle Scholar | 28241084PubMed |

Degrelle, S. A., Campion, E., Cabau, C., Piumi, F., Reinaud, P., Richard, C., Renard, J.-P., and Hue, I. (2005). Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Dev. Biol. 288, 448–460.
Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 16289134PubMed |

Ealy, A. D., and Yang, Q. E. (2009). Control of interferon-tau expression during early pregnancy in ruminants. Am. J. Reprod. Immunol. 61, 95–106.
Control of interferon-tau expression during early pregnancy in ruminants.Crossref | GoogleScholarGoogle Scholar | 19143673PubMed |

Eckert, J., and Niemann, H. (1998). mRNA expression of leukaemia inhibitory factor (LIF) and its receptor subunits glycoprotein 130 and LIF-receptor-beta in bovine embryos derived in vitro or in vivo. Mol. Hum. Reprod. 4, 957–965.
mRNA expression of leukaemia inhibitory factor (LIF) and its receptor subunits glycoprotein 130 and LIF-receptor-beta in bovine embryos derived in vitro or in vivo.Crossref | GoogleScholarGoogle Scholar | 9809677PubMed |

Fry, R. C., Batt, P. A., Fairclough, R. J., and Parr, R. A. (1992). Human leukemia inhibitory factor improves the viability of cultured ovine embryos. Biol. Reprod. 46, 470–474.
Human leukemia inhibitory factor improves the viability of cultured ovine embryos.Crossref | GoogleScholarGoogle Scholar | 1617019PubMed |

Fujii, T., Hirayama, H., Naito, A., Kashima, M., Sakai, H., Fukuda, S., Yoshino, H., Moriyasu, S., Kageyama, S., Sugimoto, Y., Matsuyama, S., Hayakawa, H., and Kimura, K. (2017). Production of calves by the transfer of cryopreserved bovine elongating conceptuses and possible application for preimplantation genomic selection. J. Reprod. Dev. 63, 497–504.
Production of calves by the transfer of cryopreserved bovine elongating conceptuses and possible application for preimplantation genomic selection.Crossref | GoogleScholarGoogle Scholar | 28781338PubMed |

Fukui, Y., and Matsuyama, K. (1994). Development of in vitro matured and fertilized bovine embryos cultured in media containing human leukemia inhibitory factor. Theriogenology 42, 663–673.
Development of in vitro matured and fertilized bovine embryos cultured in media containing human leukemia inhibitory factor.Crossref | GoogleScholarGoogle Scholar | 16727572PubMed |

Furusawa, T., Ohkoshi, K., Kimura, K., Matsuyama, S., Akagi, S., Kaneda, M., Ikeda, M., Hosoe, M., Kizaki, K., and Tokunaga, T. (2013). Characteristics of bovine inner cell mass-derived cell lines and their fate in chimeric conceptuses. Biol. Reprod. 89, 28.
Characteristics of bovine inner cell mass-derived cell lines and their fate in chimeric conceptuses.Crossref | GoogleScholarGoogle Scholar | 23782837PubMed |

Hambruch, N., Haeger, J.-D., Dilly, M., and Pfarrer, C. (2010). EGF stimulates proliferation in the bovine placental trophoblast cell line F3 via Ras and MAPK. Placenta 31, 67–74.
EGF stimulates proliferation in the bovine placental trophoblast cell line F3 via Ras and MAPK.Crossref | GoogleScholarGoogle Scholar | 19914712PubMed |

Han, Y. M., Lee, E. S., Mogoe, T., Lee, K. K., and Fukui, Y. (1995). Effect of human leukemia inhibitory factor on in vitro development of IVF-derived bovine morulae and blastocysts. Theriogenology 44, 507–516.
Effect of human leukemia inhibitory factor on in vitro development of IVF-derived bovine morulae and blastocysts.Crossref | GoogleScholarGoogle Scholar | 16727749PubMed |

Hosoe, M., and Shioya, Y. (1997). Distribution of cortical granules in bovine oocytes classified by cumulus complex. Zygote 5, 371–376.
Distribution of cortical granules in bovine oocytes classified by cumulus complex.Crossref | GoogleScholarGoogle Scholar | 9563685PubMed |

Maddox-Hyttel, P., Alexopoulos, N. I., Vajta, G., Lewis, I., Rogers, P., Cann, L., Callesen, H., Tveden-Nyborg, P., and Trounson, A. (2003). Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Reproduction 125, 607–623.
Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos.Crossref | GoogleScholarGoogle Scholar | 12683931PubMed |

Morgan, G., Wooding, F. B. P., Beckers, J. F., and Friesen, H. G. (1989). An immunological cryo-ultrastructural study of a sequential appearance of proteins in placental binucleate cells in early pregnancy in the cow. J. Reprod. Fertil. 86, 745–752.
An immunological cryo-ultrastructural study of a sequential appearance of proteins in placental binucleate cells in early pregnancy in the cow.Crossref | GoogleScholarGoogle Scholar | 2760899PubMed |

Nachtigall, M. J., Kliman, H. J., Feinberg, R. F., Olive, D. L., Engin, O., and Arici, A. (1996). The effect of leukemia inhibitory factor (LIF) on trophoblast differentiation: a potential role in human implantation. J. Clin. Endocrinol. Metab. 81, 801–806.
The effect of leukemia inhibitory factor (LIF) on trophoblast differentiation: a potential role in human implantation.Crossref | GoogleScholarGoogle Scholar | 8636307PubMed |

Nakano, H., Takahashi, T., Imai, K., and Hashizume, K. (2001). Expression of placental lactogen and cytokeratin in bovine placental binucleate cells in culture. Cell Tissue Res. 303, 263–270.
Expression of placental lactogen and cytokeratin in bovine placental binucleate cells in culture.Crossref | GoogleScholarGoogle Scholar | 11291772PubMed |

Nakano, H., Shimada, A., Imai, K., Takezawa, T., Takahashi, T., and Hashizume, K. (2002). Bovine trophoblastic cell differentiation on collagen substrata: formation of binucleate cells expressing placental lactogen. Cell Tissue Res. 307, 225–235.
Bovine trophoblastic cell differentiation on collagen substrata: formation of binucleate cells expressing placental lactogen.Crossref | GoogleScholarGoogle Scholar | 11845329PubMed |

Nedambale, T. L., Du, F., Yang, X., and Tian, X. C. (2006). Higher survival rate of vitrified and thawed in vitro produced bovine blastocysts following culture in defined medium supplemented with β-mercaptoethanol. Anim. Reprod. Sci. 93, 61–75.
Higher survival rate of vitrified and thawed in vitro produced bovine blastocysts following culture in defined medium supplemented with β-mercaptoethanol.Crossref | GoogleScholarGoogle Scholar | 16099115PubMed |

Neira, J. A., Tainturier, D., Peña, M. A., and Martal, J. (2010). Effect of the association of IGF-I, IGF-II, bFGF, TGF-β1, GM-CSF, and LIF on the development of bovine embryos produced in vitro. Theriogenology 73, 595–604.
Effect of the association of IGF-I, IGF-II, bFGF, TGF-β1, GM-CSF, and LIF on the development of bovine embryos produced in vitro.Crossref | GoogleScholarGoogle Scholar | 20035987PubMed |

Oshima, K., Watanabe, H., Yoshihara, K., Kojima, T., Dochi, O., Takenouchi, N., Fukushima, M., and Komatsu, M. (2003). Gene expression of leukemia inhibitory factor (LIF) and macrophage colony stimulating factor (M-CSF) in bovine endometrium during early pregnancy. Theriogenology 60, 1217–1226.
Gene expression of leukemia inhibitory factor (LIF) and macrophage colony stimulating factor (M-CSF) in bovine endometrium during early pregnancy.Crossref | GoogleScholarGoogle Scholar | 14511776PubMed |

Reinhart, K. C., Dubey, R. K., Mummery, C. L., van Rooijen, M., Keller, P. J., and Marinella, R. (1998). Synthesis and regulation of leukaemia inhibitory factor in cultured bovine oviduct cells by hormones. Mol. Hum. Reprod. 4, 301–308.
Synthesis and regulation of leukaemia inhibitory factor in cultured bovine oviduct cells by hormones.Crossref | GoogleScholarGoogle Scholar | 9570277PubMed |

Rizos, D., Lonergan, P., Boland, M. P., Arroyo-García, R., Pintado, B., de la Fuente, J., and Gutiérrez-Adán, A. (2002). Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality. Biol. Reprod. 66, 589–595.
Analysis of differential messenger RNA expression between bovine blastocysts produced in different culture systems: implications for blastocyst quality.Crossref | GoogleScholarGoogle Scholar | 11870062PubMed |

Sakurai, T., Sakamoto, A., Muroi, Y., Bai, H., Nagaoka, K., Tamura, K., Takahashi, T., Hashizume, K., Sakatani, M., Takahashi, M., Godkin, J. D., and Imakawa, K. (2009). Induction of endogenous interferon tau gene transcription by CDX2 and high acetylation in bovine nontrophoblast cells. Biol. Reprod. 80, 1223–1231.
Induction of endogenous interferon tau gene transcription by CDX2 and high acetylation in bovine nontrophoblast cells.Crossref | GoogleScholarGoogle Scholar | 19211809PubMed |

Sakurai, T., Bai, H., Konno, T., Ideta, A., Aoyagi, Y., Godkin, J. D., and Imakawa, K. (2010). Function of a transcription factor CDX2 beyond its trophectoderm lineage specification. Endocrinology 151, 5873–5881.
Function of a transcription factor CDX2 beyond its trophectoderm lineage specification.Crossref | GoogleScholarGoogle Scholar | 20962045PubMed |

Schiffmacher, A. T., and Keefer, C. L. (2013). CDX2 regulates multiple trophoblast genes in bovine trophectoderm CT-1 cells. Mol. Reprod. Dev. 80, 826–839.
CDX2 regulates multiple trophoblast genes in bovine trophectoderm CT-1 cells.Crossref | GoogleScholarGoogle Scholar | 23836438PubMed |

Shimada, A., Nakano, H., Takahashi, T., Imai, K., and Hashizume, K. (2001). Isolation and characterization of a bovine blastocyst-derived trophoblastic cell line, BT-1: development of a culture system in the absence of feeder cell. Placenta 22, 652–662.
Isolation and characterization of a bovine blastocyst-derived trophoblastic cell line, BT-1: development of a culture system in the absence of feeder cell.Crossref | GoogleScholarGoogle Scholar | 11504534PubMed |

Smith, A. G., Heath, J. K., Donaldson, D. D., Wong, G. G., Moreau, J., Stahl, M., and Rogers, D. (1988). Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 336, 688–690.
Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides.Crossref | GoogleScholarGoogle Scholar | 3143917PubMed |

Stewart, C. L., Kaspar, P., Brunet, L. J., Bhatt, H., Gadi, I., Köntgen, F., and Abbondanzo, S. J. (1992). Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76–79.
Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor.Crossref | GoogleScholarGoogle Scholar | 1522892PubMed |

Suzuki, Y., Koshi, K., Imai, K., Takahashi, T., Kizaki, K., and Hashizume, K. (2011). Bone morphogenetic protein 4 accelerates the establishment of bovine trophoblastic cell lines. Reproduction 142, 733–743.
Bone morphogenetic protein 4 accelerates the establishment of bovine trophoblastic cell lines.Crossref | GoogleScholarGoogle Scholar | 21862694PubMed |

Talbot, N. C., Caperna, T. J., Edwards, J. L., Garrett, W., Wells, K. D., and Ealy, A. D. (2000). Bovine blastocyst-derived trophectoderm and endoderm cell cultures: interferon tau and transferrin expression as respective in vitro markers. Biol. Reprod. 62, 235–247.
Bovine blastocyst-derived trophectoderm and endoderm cell cultures: interferon tau and transferrin expression as respective in vitro markers.Crossref | GoogleScholarGoogle Scholar | 10642558PubMed |

Talbot, N. C., Powell, A. M., Ocón, O. M., Caperna, T. J., Camp, M., Garrett, W. M., and Ealy, A. D. (2008). Comparison of the interferon-tau expression from primary trophectoderm outgrowths derived from IVP, NT, and parthenogenote bovine blastocysts. Mol. Reprod. Dev. 75, 299–308.
Comparison of the interferon-tau expression from primary trophectoderm outgrowths derived from IVP, NT, and parthenogenote bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 17721989PubMed |

Ushizawa, K., Takahashi, T., Kaneyama, K., Tokunaga, T., Tsunoda, Y., and Hashizume, K. (2005). Gene expression profiles of bovine trophoblastic cell line (BT-1) analyzed by a custom cDNA microarray. J. Reprod. Dev. 51, 211–220.
Gene expression profiles of bovine trophoblastic cell line (BT-1) analyzed by a custom cDNA microarray.Crossref | GoogleScholarGoogle Scholar | 15613779PubMed |

Vajta, G., Alexopoulos, N. I., and Callesen, H. (2004). Rapid growth and elongation of bovine blastocysts in vitro in a three-dimensional gel system. Theriogenology 62, 1253–1263.
Rapid growth and elongation of bovine blastocysts in vitro in a three-dimensional gel system.Crossref | GoogleScholarGoogle Scholar | 15325552PubMed |

Vejlsted, M., Du, Y., Vajta, G., and Maddox-Hyttel, P. (2006). Post-hatching development of the porcine and bovine embryo – defining criteria for expected development in vivo and in vitro. Theriogenology 65, 153–165.
Post-hatching development of the porcine and bovine embryo – defining criteria for expected development in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar | 16257443PubMed |