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The development and expression of pluripotency genes in embryos derived from nuclear transfer and in vitro fertilization

Published online by Cambridge University Press:  26 April 2013

Li-Bing Ma ,
Xiao-Ying He ,
Feng-Mei Wang ,
Jun-Wei Cao  and
Teng Cheng
Li-Bing Ma*
Affiliation:
School of Mathematics, Physics and Biological Engineering, Inner Mongolia University of Science & Technology, Aerding Avenue No. 7, Baotou, Inner Mongolia Autonomous Region 014010, China. Institute of Bioengineering & Technology, Inner Mongolia University of Science & Technology, Baotou, Inner Mongolia, China.
Xiao-Ying He
Affiliation:
School of Mathematics, Physics and Biological Engineering, Inner Mongolia University of Science and Technology, Baotou, Inner Mongolia, China. Institute of Bioengineering & Technology, Inner Mongolia University of Science & Technology, Baotou, Inner Mongolia, China.
Feng-Mei Wang
Affiliation:
School of Farm and Garden Engineering, Baotou Light Industry Vocational Technical College, Baotou, Inner Mongolia, China.
Jun-Wei Cao
Affiliation:
College of Life Science, Inner Mongolia Agricultural University, Hohhot, Inner Mongolia, China.
Teng Cheng
Affiliation:
School of Mathematics, Physics and Biological Engineering, Inner Mongolia University of Science and Technology, Baotou, Inner Mongolia, China.
*
All correspondence to: Li-Bing Ma. School of Mathematics, Physics and Biological Engineering, Inner Mongolia University of Science & Technology, Aerding Avenue No. 7, Baotou, Inner Mongolia Autonomous Region 014010, China. Tel: +86 15848638996. Fax: +86 04725954358. e-mail address: [email protected]
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Summary

Somatic cell nuclear transfer can be used to produce embryonic stem (ES) cells, cloned animals, and can even increase the population size of endangered animals. However, the application of this technique is limited by the low developmental rate of cloned embryos, a situation that may result from abnormal expression of some zygotic genes. In this study, sheep–sheep intra-species cloned embryos, goat–sheep inter-species cloned embryos, or sheep in vitro fertilized embryos were constructed and cultured in vitro and the developmental ability and expression of three pluripotency genes, SSEA-1, Nanog and Oct4, were examined. The results showed firstly that the developmental ability of in vitro fertilized embryos was significantly higher than that of cloned embryos. In addition, the percentage of intra-species cloned embryos that developed to morula or blastocyst stages was also significantly higher than that of the inter-species cloned embryos. Secondly, all three types of embryos expressed SSEA-1 at the 8-cell and morula stages. At the 8-cell stage, a higher percentage of in vitro fertilized embryos expressed SSEA-1 than occurred for cloned embryos. However, at the morula stage, all detected embryos could express SSEA-1. Thirdly, the three types of embryos expressed Oct4 mRNA at the morula and blastocyst stages, and embryos at the blastocyst stage expressed Nanog mRNA. The rate of expression of Oct4 and Nanog mRNA at these developmental stages was higher in in vitro fertilized embryos than in cloned embryos. These results indicated that, during early development, the failure to reactivate some pluripotency genes maybe is a reason for the low cloning efficiency found with cloned embryos.

Keywords

Inter-speciesNanogOct4Somatic cell nuclear transferSSEA-1
Type
Research Article
Information
Zygote , Volume 22 , Issue 4 , November 2014 , pp. 540 - 548
Copyright
Copyright © Cambridge University Press 2013 

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References

Armstrong, L., Lako, M., Dean, W. & Stojkovic, M. (2006). Epigenetic modification is central to genome reprogramming in somatic cell nuclear transfer. Stem Cells 24, 805–14.Google Scholar
Aston, K.I., Li, G.P., Hicks, B.A., Sessions, B.R., Davis, A.P., Rickords, L.F., Stevens, J.R. & White, K.L. (2010). Abnormal levels of transcript abundance of developmentally important genes in various stages of preimplantation bovine somatic cell nuclear transfer embryos. Cell Reprogram 12, 23–32.CrossRefGoogle ScholarPubMed
Beaujean, N., Taylor, J., Gardner, J., Wilmut, I., Meehan, R. & Young, L. (2004). Effect of limited DNA methylation reprogramming in the normal sheep embryo on somatic cell nuclear transfer. Biol. Reprod. 71, 185–93.Google Scholar
Beyhan, Z., Forsberg, E.J., Eilertsen, K.J., Kent-First, M. & First, N.L. (2007). Gene expression in bovine nuclear transfer embryos in relation to donor cell efficiency in producing live offspring. Mol. Reprod. Dev. 74, 18–27.Google Scholar
Boiani, M., Eckardt, S., Schöler, H.R. & McLaughlin, K.J. (2002). Oct4 distribution and level in mouse clones: consequences for pluripotency. Genes Dev. 16, 1209–19.Google Scholar
Borowczyk, E., Caton, J.S., Redmer, D.A., Bilski, J.J., Weigl, R.M., Vonnahme, K.A., Borowicz, P.P., Kirsch, J.D., Kraft, K.C., Reynolds, L.P. & Grazul-Bilska, A.T. (2006). Effects of plane of nutrition on in vitro fertilization and early embryonic development in sheep. J. Anim. Sci. 84, 1593–9.CrossRefGoogle ScholarPubMed
Brambrink, T., Foreman, R., Welstead, G.G., Lengner, C.J., Wernig, M., Suh, H. & Jaenisch, R. (2008). Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell 2, 151–9.Google Scholar
Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S. & Smith, A. (2003). Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113, 643–55.CrossRefGoogle ScholarPubMed
Chen, Y., He, Z.X., Liu, A., Wang, K., Mao, W.W., Chu, J.X., Lu, Y., Fang, Z.F., Shi, Y.T., Yang, Q.Z., Chen, da Y., Wang, M.K., Li, J.S., Huang, S.L., Kong, X.Y., Shi, Y.Z., Wang, Z.Q., Xia, J.H., Long, Z.G., Xue, Z.G., Ding, W.X. & Sheng, H.Z. (2003). Embryonic stem cells generated by nuclear transfer of human somatic nuclei into rabbit oocytes. Cell Res. 13, 251–63.Google Scholar
Chung, Y., Bishop, C.E., Treff, N.R., Walker, S.J., Sandler, V.M., Becker, S., Klimanskaya, I., Wun, W.S., Dunn, R., Hall, R.M., Su, J., Lu, S.J., Maserati, M., Choi, Y.H., Scott, R., Atala, A., Dittman, R. & Lanza, R. (2009). Reprogramming of human somatic cells using human and animal oocytes. Cloning Stem Cells 11, 213–23.Google Scholar
Dattena, M., Chessa, B., Lacerenza, D., Accardo, C., Pilichi, S., Mara, L., Chessa, F., Vincenti, L. & Cappai, P. (2006). Isolation, culture, and characterization of embryonic cell lines from vitrified sheep blastocysts. Mol. Reprod. Dev. 73, 31–9.Google Scholar
Ferrer, F., Garcia, C., Villar, J. & Arias, M. (1995). Ultrastructural study of the early development of the sheep embryo. Anat. Histol. Embryol. 24, 191–6.Google Scholar
Fulka, J. Jr & Fulka, H. (2007). Somatic cell nuclear transfer (SCNT) in mammals: the cytoplast and its reprogramming activities. Adv. Exp. Med. Biol. 591, 93–102.Google Scholar
He, S., Pant, D., Schiffmacher, A., Bischoff, S., Melican, D., Gavin, W. & Keefer, C. (2006). Developmental expression of pluripotency determining factors in caprine embryos: novel pattern of NANOG protein localization in the nucleolus. Mol. Reprod. Dev. 73, 1512–22.CrossRefGoogle ScholarPubMed
Hong, S.G., Oh, H.J., Park, J.E., Kim, M.J., Kim, G.A., Koo, O.J., Jang, G. & Lee, B.C. (2012). Production of transgenic canine embryos using interspecies somatic cell nuclear transfer. Zygote 20, 67–72.CrossRefGoogle ScholarPubMed
Hosseini, S.M., Hajian, M., Forouzanfar, M., Moulavi, F., Abedi, P., Asgari, V., Tanhaei, S., Abbasi, H., Jafarpour, F., Ostadhosseini, S., Karamali, F., Karbaliaie, K., Baharvand, H. & Nasr-Esfahani, M.H. (2012). Enucleated ovine oocyte supports human somatic cells reprogramming back to the embryonic stage. Cell Reprogram 14, 155–63.Google Scholar
Hua, S., Zhang, Y., Song, K., Song, J., Zhang, Z., Zhang, L., Zhang, C., Cao, J. & Ma, L. (2008). Development of bovine–ovine interspecies cloned embryos and mitochondria segregation in blastomeres during preimplantation. Anim. Reprod. Sci. 105, 245–57.Google Scholar
Kühholzer, B., Baguisi, A. & Overström, E.W. (2000). Long-term culture and characterization of goat primordial germ cells. Theriogenology 53, 1071–9.Google Scholar
Kurosaka, S., Eckardt, S. & McLaughlin, K.J. (2004). Pluripotent lineage definition in bovine embryos by Oct4 transcript localization. Biol. Reprod. 71, 1578–82.Google Scholar
Lanza, R.P., Cibelli, J.B., Diaz, F., Moraes, C.T., Farin, P.W., Farin, C.E., Hammer, C.J., West, M.D. & Damiani, P. (2000). Cloning of endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning 2, 79–90.Google Scholar
Lee, E., Kim, J.H., Park, S.M., Jeong, Y.I., Lee, J.Y., Park, S.W., Choi, J., Kim, H.S., Jeong, Y.W., Kim, S., Hyun, S.H. & Hwang, W.S. (2008). The analysis of chromatin remodeling and the staining for DNA methylation and histone acetylation do not provide definitive indicators of the developmental ability of inter-species cloned embryos. Anim. Reprod. Sci. 105, 438–50.Google Scholar
Li, X., Kato, Y. & Tsunoda, Y. (2005). Comparative analysis of development-related gene expression in mouse preimplantation embryos with different developmental potential. Mol. Reprod. Dev. 72, 152–60.Google Scholar
Li, Y., Dai, Y., Du, W., Zhao, C., Wang, H., Wang, L., Li, R., Liu, Y., Wan, R. & Li, N. (2006). Cloned endangered species takin (Budorcas taxicolor) by inter-species nuclear transfer and comparison of the blastocyst development with yak (Bos grunniens) and bovine. Mol. Reprod. Dev. 73, 189–95.Google Scholar
Loh, Y.H., Wu, Q., Chew, J.L., Vega, V.B., Zhang, W., Chen, X., Bourque, G., George, J., Leong, B., Liu, J., Wong, K.Y., Sung, K.W., Lee, C.W., Zhao, X.D., Chiu, K.P., Lipovich, L., Kuznetsov, V.A., Robson, P., Stanton, L.W., Wei, C.L., Ruan, Y., Lim, B. & Ng, H.H. (2006). The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 38, 431–40.Google Scholar
Loi, P., Ptak, G., Barboni, B., Fulka, J. Jr, Cappai, P. & Clinton, M. (2001). Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nat. Biotechnol. 19, 962–4.Google Scholar
Lorthongpanich, C., Laowtammathron, C., Chan, A.W., Ketudat-Cairns, M. & Parnpai, R. (2008). Development of interspecies cloned monkey embryos reconstructed with bovine enucleated oocytes. J. Reprod. Dev. 54, 306–13.Google Scholar
Ma, L.B., Yang, L., Hua, S., Cao, J.W., Li, J.X. & Zhang, Y. (2008a). Development in vitro and mitochondrial fate of interspecies cloned embryos. Reprod. Domest. Anim. 43, 279–85.CrossRefGoogle ScholarPubMed
Ma, L.B., Yang, L., Zhang, Y., Cao, J.W., Hua, S. & Li, J.X. (2008b). Quantitative analysis of mitochondrial RNA in goat–sheep cloned embryos. Mol. Reprod. Dev. 75, 33–9.Google Scholar
Murakami, M., Otoi, T., Wongsrikeao, P., Agung, B., Sambuu, R. & Suzuki, T. (2005). Development of interspecies cloned embryos in yak and dog. Cloning Stem Cells 7, 77–81.Google Scholar
Niemann, H., Tian, X.C., King, W.A. & Lee, R.S. (2008). Epigenetic reprogramming in embryonic and foetal development upon somatic cell nuclear transfer cloning. Reproduction 135, 151–63.CrossRefGoogle ScholarPubMed
Park, P.J., Colletti, E., Ozturk, F., Wood, J.A., Tellez, J., Almeida-Porada, G. & Porada, C. (2009). Factors determining the risk of inadvertent retroviral transduction of male germ cells after in utero gene transfer in sheep. Hum. Gene Ther. 20, 201–15.Google Scholar
Pivko, J., Grafenau, P. & Kopecný, V. (1995). Nuclear fine structure and transcription in early goat embryos. Theriogenology 44, 661–71.Google Scholar
Solter, D. & Knowles, B.B. (1978). Monoclonal antibody defining a stage-specific mouse embryonic antigen (SSEA-1). Proc. Natl. Acad. Sci. USA 75, 5565–9.Google Scholar
Srirattana, K., Imsoonthornruksa, S., Laowtammathron, C., Sangmalee, A., Tunwattana, W., Thongprapai, T., Chaimongkol, C., Ketudat-Cairns, M. & Parnpai, R. (2012). Full-term development of gaur–bovine interspecies somatic cell nuclear transfer embryos: effect of trichostatin A treatment. Cell Reprogram 14, 248–57.Google Scholar
Stadtfeld, M., Maherali, N., Breault, D.T. & Hochedlinger, K. (2008). Defining molecular cornerstones during fibroblast to iPS cell reprogramming in mouse. Cell Stem Cell 2, 230–40.Google Scholar
Sugawara, A., Sugimura, S., Hoshino, Y. & Sato, E. (2009). Development and spindle formation in rat somatic cell nuclear transfer (SCNT) embryos in vitro using porcine recipient oocytes. Zygote 17, 195–202.Google Scholar
Takahashi, K. & Yamanaka, S. (2006). Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663–76.Google Scholar
Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K. & Yamanaka, S. (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861–72.Google Scholar
Vassilieva, S., Guan, K., Pich, U. & Wobus, A.M. (2000). Establishment of SSEA-1- and Oct-4-expressing rat embryonic stem-like cell lines and effects of cytokines of the IL-6 family on clonal growth. Exp. Cell Res. 258, 361–73.CrossRefGoogle ScholarPubMed
Wakayama, T., Tabar, V., Rodriguez, I., Perry, A.C., Studer, L. & Mombaerts, P. (2001). Differentiation of embryonic stem cell lines generated from adult somatic cells by nuclear transfer. Science 292, 740–3.Google Scholar
Wang, K., Out, H.H., Chen, Y., Lee, Y., Latham, K. & Cibelli, J.B. (2011). Reprogrammed transcriptome in rhesus–bovine interspecies somatic cell nuclear transfer embryos. PLoS One 6, e22197.Google Scholar
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J. & Campbell, K.H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–3.Google Scholar
Wilmut, I., Beaujean, N., de Sousa, P.A., Dinnyes, A., King, T.J., Paterson, L.A., Wells, D.N. & Young, L.E. (2002). Somatic cell nuclear transfer. Nature 419, 583–6.Google Scholar
Xing, X., Magnani, L., Lee, K., Wang, C., Cabot, R.A. & Machaty, Z. (2009). Gene expression and development of early pig embryos produced by serial nuclear transfer. Mol. Reprod. Dev. 76, 555–63.Google Scholar
Yan, L., Lei, L., Yang, C., Gao, Z., Lei, A., Ma, X. & Dou, Z. (2008). Improved isolation and culture of embryonic germ cells from Guanzhong dairy goat. Sheng Wu Gong Cheng Xue Bao 24, 1670–6.Google Scholar
Yu, J., Vodyanik, M.A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J.L., Tian, S., Nie, J., Jonsdottir, G.A., Ruotti, V., Stewart, R., Slukvin, I.I. & Thomson, J.A. (2007). Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917–20.Google Scholar
Zhao, Z.J., Ouyang, Y.C., Nan, C.L., Lei, Z.L., Song, X.F., Sun, Q.Y. & Chen, D.Y. (2006). Rabbit oocyte cytoplasm supports development of nuclear transfer embryos derived from the somatic cells of the camel and tibetan antelope. J. Reprod. Fertil. 52, 449–59.Google Scholar