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Changes in the expression of pluripotency-associated genes during preimplantation and peri-implantation stages in bovine cloned and in vitro produced embryos

Published online by Cambridge University Press:  30 April 2010

Lleretny Rodríguez-Alvarez ,
José Cox ,
Heribelt Tovar ,
Ralf Einspanier  and
Fidel Ovidio Castro
Lleretny Rodríguez-Alvarez
Affiliation:
Department of Animal Science, Faculty of Veterinary Medicine, Universidad de Concepción, Avenida Vicente Méndez 595, Chillán, Chile.
José Cox
Affiliation:
Department of Animal Science, Faculty of Veterinary Medicine, Universidad de Concepción, Avenida Vicente Méndez 595, Chillán, Chile.
Heribelt Tovar
Affiliation:
Department of Animal Science, Faculty of Veterinary Medicine, Universidad de Concepción, Avenida Vicente Méndez 595, Chillán, Chile.
Ralf Einspanier
Affiliation:
Institute of Veterinary Biochemistry, Freie Universität Berlin, Oertzenweg 19b D-14163 Berlin, Germany.
Fidel Ovidio Castro*
Affiliation:
Department of Animal Science, Faculty of Veterinary Medicine, Universidad de Concepción, Avenida Vicente Méndez 595, Chillán, Chile.
*
All correspondence to: Fidel Ovidio Castro. Department of Animal Science, Faculty of Veterinary Medicine, Universidad de Concepción, Avenida Vicente Méndez 595, Chillán, Chile. Tel: +56 42 207524. Fax: +56 42 207212. e-mail: fidcastro@udec.cl
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Summary

In cattle, embryos elongate before implantation and after hatching. Changes in gene expression during this transition are not well studied. Especially important are variations in the expression of pluripotency-associated genes as a result of assisted reproductive biotechnologies, such as cloning and in vitro fertilization (IVF). We hypothesize that there will be a decline in the expression of key pluripotency-associated genes and an increase in the expression of IFN-τ in elongated embryos when compared with day-7 blastocysts. To test this we generated cloned and IVF bovine day-7 blastocyst and day-17 elongated embryos (day 0 = day of nucleus transfer or IVF). Gene expression in all embryos was assessed via RT-qPCR. OCT4 was overexpressed (p < 0.05) in the cloned blastocysts when compared with IVF. No differences in gene expression at this stage between cloned and IVF embryos were found for EOMES, NANOG and FGF4. At elongation EOMES, NANOG and FGF4 were upregulated in IVF embryos (p < 0.05). IFN-τ and OCT4 were expressed at similar levels. There were changes in the expression levels for all transcripts between blastogenesis and elongation. NANOG, IFN-τ and EOMES were overexpressed in all the elongated embryos (p < 0.05), FGF4 was underexpressed in both treatments. OCT4 dropped drastically in the cloned elongated embryos, but not in the IVF. Interestingly only adult donor cells (but not fetal) from which the cloned embryos originated also expressed high levels of OCT4. Our findings might help to understand the shift of gene expression during elongation and to identify key markers of embryonic development useful for embryo screening purposes.

Keywords

Bovine embryosGene expressionPeri-implantationPreimplantationPluripotency
Type
Research Article
Information
Zygote , Volume 18 , Issue 3 , August 2010 , pp. 269 - 279
Copyright
Copyright © Cambridge University Press 2010

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References

Amarnath, D., Li, X., Kato, Y. & Tsunoda, Y. (2007). Gene expression in individual bovine somatic cell cloned embryos at the 8-cell and blastocyst stages of preimplantation development. J. Reprod. Dev. 53, 1247–63.CrossRefGoogle ScholarPubMed
Arnold, D.R., Bordignon, V., Lefebvre, R., Murphy, B.D. & Smith, L.C. (2006). Somatic cell nuclear transfer alters peri-implantation trophoblast differentiation in bovine embryos. Reproduction 132, 279–90.CrossRefGoogle ScholarPubMed
Arnold, D.R., Fortier, A.L., Lefebvre, R., Miglino, M.A., Pfarrer, C. & Smith, L.C. (2008). Placental insufficiencies in cloned animals – a workshop report. Placenta 29 Suppl. AS108–S110.CrossRefGoogle ScholarPubMed
Bazer, F.W.Mediators of maternal recognition of pregnancy in mammals. (1992). Proc. Soc. Exp. Biol. Med. 199, 373–84.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Boiani, M., Eckardt, S., Leu, N.A., Scholer, H.R. & McLaughlin, K.J. (2003). Pluripotency deficit in clones overcome by clone-clone aggregation: epigenetic complementation? EMBO J. 22, 5304–12.CrossRefGoogle ScholarPubMed
Boiani, M., Eckardt, S., Scholer, H.R. & McLaughlin, K.J. (2002). Oct4 distribution and level in mouse clones: consequences for pluripotency. Genes. Dev. 16, 1209–19.CrossRefGoogle ScholarPubMed
Boiani, M., Gentile, L., Gambles, V.V., Cavaleri, F., Redi, C.A. & Scholer, H.R. (2005). Variable reprogramming of the pluripotent stem cell marker Oct4 in mouse clones: Distinct developmental potentials in different culture environments. Stem Cells 23, 1089–104.CrossRefGoogle ScholarPubMed
Bortvin, A., Eggan, K., Skaletsky, H., Akutsu, H., Berry, D.L., Yanagimachi, R., Page, D.C. & Jaenisch, R. (2003). Incomplete reactivation of Oct4-related genes in mouse embryos cloned from somatic nuclei. Development 130, 1673–80.CrossRefGoogle ScholarPubMed
Castro, F.O., Sharbati, S., Rodríguez-Alvarez, LL., Cox, J.F., Hulstichg, C. & Einspanier, R.E. (2010). MicroRNA expression profiling of elongated cloned and in vitro fertilized bovine embryos. Theriogenology 73, 71–85.CrossRefGoogle ScholarPubMed
Daniels, R., Hall, V. & Trounson, A.O. (2000). Analysis of gene transcription in bovine nuclear transfer embryos reconstructed with granulosa cell nuclei. Biol. Reprod. 63, 1034–40.CrossRefGoogle ScholarPubMed
Daniels, R., Hall, V.J., French, A.J., Korfiatis, N.A. & Trounson, A.O. (2001). Comparison of gene transcription in cloned bovine embryos produced by different nuclear transfer techniques. Mol. Reprod. Dev. 60, 281–8.CrossRefGoogle ScholarPubMed
De Armas, R., Solano, R., Riego, E., Pupo, C.A., Aguilar, A., Ramos, B., Aguirre, A., de la Fuente, J. & Castro, F.O. (1994). Use of F1 progeny of Holstein x Zebu cross cattle as oocyte donors for in vitro embryo production and gene microinjection. Theriogenology 42, 977–85.CrossRefGoogle Scholar
Degrelle, S., Campion, E., Cabau, C., Piumi, F., Reinaud, P., Richard, C., Renard, J-P. & Hue, I. (2005). Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Dev Biol. 288, 448–60.CrossRefGoogle ScholarPubMed
Garry, F.B., Adams, R., McCann, J.P. & Odde, K.G. (1996). Postnatal characteristics of calves produced by nuclear transfer cloning. Theriogenology 45, 141–152.CrossRefGoogle Scholar
Guillomot, M., Turbe, A., Hue, I. & Renard, J.P. (2004). Staging of ovine embryos and expression of the T-box genes Brachyury and Eomesodermin around gastrulation. Reproduction 127, 491–501.CrossRefGoogle ScholarPubMed
Hall, V.J., Ruddock, N.T. & French, A.J. (2005). Expression profiling of genes crucial for placental and preimplantation development in bovine in vivo, in vitro, and nuclear transfer blastocysts. Mol. Reprod. Dev. 72, 16–24.CrossRefGoogle ScholarPubMed
Hattori, N., Nishino, K., Ko, Y.G., Hattori, N., Ohgane, J., Tanaka, S. & Shiota, K. (2004). Epigenetic control of mouse Oct-4 gene expression in embryonic stem cells and trophoblast stem cells. J. Biol. Chem. 279, 17063–9.CrossRefGoogle ScholarPubMed
Hernandez-Ledezma, J.J, Sikes, J.D, Murphy, C.N, Watson, A.J, Schultz, G.A. & Roberts, R.M. (1992). Expression of bovine trophoblast interferon in conceptuses derived by in vitro techniques. Biol. Reprod. 47, 374–80.CrossRefGoogle ScholarPubMed
Keefer, C.L., Pant, D., Blomberg, L. & Talbot, N.C. (2007). Challenges and prospects for the establishment of embryonic stem cell lines of domesticated ungulates. Anim. Reprod. Sci. 98, 147–68.CrossRefGoogle ScholarPubMed
Kimber, S.J., Sneddon, S.F., Bloor, D.J, El-Bareg, A.M., Hawkhead, J.A., Metcalfe, A.D., Houghton, F.D., Leese, H.J., Rutherford, A., Lieberman, B.A. & Brison, D.R. (2008). Expression of genes involved in early cell fate decisions in human embryos and their regulation by growth factors. Reproduction 135, 635–47.CrossRefGoogle ScholarPubMed
Kremenskoy, M., Kremenska, Y., Suzuki, M., Imai, K., Takahashi, S., Hashizume, K., Yagi, S. & Shiota, K. (2006). Epigenetic characterization of the CpG islands of bovine leptin and POU5F1 genes in cloned bovine fetuses. J. Reprod. Dev. 52, 277–85.CrossRefGoogle ScholarPubMed
Latham, K.E. & Sapienza, C. (2004). Developmental potential as a criterion for understanding and defining embryos. Conn. Law. Rev. 36, 1171–6.Google ScholarPubMed
Liedtke, S., Enczmann, J., Waclawczyk, S., Wernet, P. & Kögler, G. (2007). Oct4 and its pseudogenes confuse stem cell research. Cell. Stem Cell 11, 364–6.CrossRefGoogle Scholar
Long, J.E., Cai, X. & He, L.Q. (2007). Gene profiling of cattle blastocysts derived from nuclear transfer, in vitro fertilization and in vivo development based on cDNA library. Anim. Reprod. Sci. 100, 243–56.CrossRefGoogle ScholarPubMed
MacLean, J.A. II, Chakrabarty, A., Xie, S., Bixby, J.A., Roberts, R.M. & Green, J.A. (2003). Family of Kunitz proteins from trophoblast: expression of the trophoblast Kunitz domain proteins (TKDP) in cattle and sheep. Mol. Reprod. Dev. 65, 30–40.CrossRefGoogle ScholarPubMed
Maddox-Hyttel, P., Alexopoulos, N.I., Vajta, G., Lewis, I., Rogers, P., Cann, L., Callesen, H., Tveden-Nyborg, P. & Trounson, A. (2003). Immunohistochemical and ultrastructural characterization of the initial post-hatching development of bovine embryos. Reproduction 125, 607–23.CrossRefGoogle ScholarPubMed
Misica-Turner, P.M., Oback, F.C., Eichenlaub, M., Well, D.N. & Oback, B. (2006). Aggregating embryonic but not somatic nuclear transfer embryos increases cattle cloning efficiency. Biol. Reprod. 76, 268–78.CrossRefGoogle Scholar
Mizuno, N. & Kosaka, M. (2008). Novel variants of Oct-3 /4 gene expressed in mouse somatic cells. J. Biol. Chem. 283, 30997–40004.CrossRefGoogle ScholarPubMed
Peura, T.T. & Vajta, G. (2003). A comparison of established and new approaches in ovine and bovine nuclear transfer. Cloning Stem Cells 5, 257–77.CrossRefGoogle ScholarPubMed
Piedrahita, J.A., Mir, B., Dindot, S. & Walker, S. (2004). Somatic cell cloning: the ultimate form of nuclear reprogramming? J. Am. Soc. Nephrol. 15, 1140–4.CrossRefGoogle ScholarPubMed
Pochampally, R.R., Smith, J.R., Ylostalo, J. & Prockop, D.J. (2004). Serum deprivation of human marrow stromal cells (hMSCs) selects for a subpopulation of early progenitor cells with enhanced expression of OCT-4 and other embryonic genes. Blood 103, 1647–52.CrossRefGoogle ScholarPubMed
Ranilla, M.J., Gebbie, F.E., King, M.E., Carolan, C., Sinclair, K.D., Watt, R.G., Dolman, D.F., Beckers, J.F. & Robinson, J.J. (1998). The incidence of embryo and fetal loss following the transfer of in vitro-cultured sheep embryos. Theriogenology 49, 248.CrossRefGoogle Scholar
Robinson, R.S., Fray, M.D., Wathes, D.C., Lamming, G.E. & Mann, G.E. (2006). In vivo expression of interferon tau mRNA by the embryonic trophoblast and uterine concentrations of interferon tau protein during early pregnancy in the cow. Mol. Reprod. Dev. 73, 470–74.CrossRefGoogle ScholarPubMed
Rodríguez, L.L., Navarrete, F.I., Tovar, H., Cox, J.F. & Castro, F.O. (2008). High developmental potential in vitro and in vivo of cattle embryos cloned without micromanipulators. J. Assist. Reprod. Genet. 25, 13–6.CrossRefGoogle ScholarPubMed
Rodriguez-Alvarez, LL., Cox, J.F., Navarrete, F., Valdés, C., Zamorano, T., Einspanier, R.E. & Castro, F.O. (2009). Elongation and gene expression in bovine cloned embryos transferred to temporary recipients. Zygote 8, 1–13.Google Scholar
Sarta, S., Schneider, Y-J. & Agathos, S.N. (2009). Ear mesenchymal stem cells: An efficient adult multipotent cell population fit for rapid and scalable expansion. J. Biotechnol. 139, 291–99.CrossRefGoogle Scholar
Tai, M.H., Chang, C.C., Kiupel, M., Webster, J.D., Olson, L.K. & Trosko, J.E. (2005). Oct4 expression in adult human stem cells: evidence in support of the stem cell theory of carcinogenesis. Carcinogenesis 26, 495–502.CrossRefGoogle ScholarPubMed
Takeda, J., Seino, S. & Bell, G.I. (1992). Human Oct3 gene family: cDNA sequences, alternative splicing, gene organization, chromosomal location, and expression at low levels in adult tissues. Nucleic Acids Res. 11, 4613–20.CrossRefGoogle Scholar
Telford, N.A., Watson, A.J. & Schultz, G.A. (1990). Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol. Reprod. Dev. 26, 90–100.CrossRefGoogle ScholarPubMed
Thompson, J.G., Sherman, A.N., Allen, N.W., McGowan, L.T. & Tervit, H.R. (1998). Total protein content and protein synthesis within pre-elongation stage bovine embryos. Mol. Reprod. Dev. 50, 139–45.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Tomikawa, J., Fukatsu, K., Tanaka, S. & Shiota, K. (2006). DNA methylation-dependent epigenetic regulation of dimethylarginine dimethylaminohydrolase 2 gene in trophoblast cell lineage. J. Biol. Chem. 28, 12163–9.CrossRefGoogle Scholar
Tondreau, T., Meuleman, N., Delforge, A., Dejeneffe, M., Leroy, R., Massy, M., Mortier, C., Bron, D. & Lagneaux, L. (2005). Mesenchymal stem cells derived from CD133-positive cells in mobilized peripheral blood and cord blood: proliferation, Oct4 expression, and plasticity. Stem Cells 23, 1105–12.CrossRefGoogle ScholarPubMed
Ushizawa, K., Herath, C.B., Kaneyama, K., Shiojima, S., Hirasawa, A., Takahashi, T., Imai, K., Ochiai, K., Tokunaga, T., Tsunoda, Y., Tsujimoto, G. & Hashizume, K. (2004). cDNA microarray analysis of bovine embryo gene expression profiles during the pre-implantation period. Reprod. Biol. Endocrinol. 2, 77.CrossRefGoogle ScholarPubMed
Vajta, G., Peura, T.T., Holm, P., Páldi, A., Greve, T., Trounson, A.O. & Callesen, H. (2000). New method for culture of zona-included or zonafree embryos: the well-of-the-well (WOW) system. Mol. Reprod. Dev. 55, 256–64.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Viebahn, C. (1999). The anterior margin of the mammalian gastrula: comparative and phylogenetic aspects of its role in axis formation and head induction. Curr. Top. Dev. Biol. 46, 63–103.CrossRefGoogle ScholarPubMed
Walker, S.K., Hartwich, K.M. & Seamark, R.F. (1996). The production of unusually large offspring following embryo manipulation: concepts and changes. Theriogenology 45, 111–20.CrossRefGoogle Scholar
Wrenzycki, C., Wells, D., Herrmann, D., Miller, A., Oliver, J., Tervit, R. & Niemann, H. (2001). Nuclear transfer protocol affects messenger RNA expression patterns in cloned bovine blastocysts. Biol. Reprod. 65, 309–17.CrossRefGoogle ScholarPubMed
Yadav, P.S., Kues, W.A., Herrmann, D., Carnwath, J.W. & Niemann, H. (2005). Bovine ICM derived cells express the Oct4 ortholog. Mol. Reprod. Dev. 72, 182–90.CrossRefGoogle ScholarPubMed
Zangrossi, S., Marabese, M., Broggini, M., Giordano, R., D'Erasmo, M., Montelatici, E., Intini, D., Neri, A., Pesce, M., Rebulla, P. & Lazzari, L. (2007). Oct-4 expression in adult human differentiated cells challenges its role as a pure stem cell marker. Stem Cells 25, 1675–80.CrossRefGoogle ScholarPubMed
Zhan, S., Kubota, C., Yang, L., Zhang, Y., Page, R. & O'Neill, M. (2004). Genomic imprinting of H19 in naturally reproduced and cloned cattle. Biol. Reprod. 71, 1540–44.CrossRefGoogle Scholar
Zhou, W., Xiang, T., Walker, S., Farrar, V., Hwang, E., Findeisen, B., Sadeghieh, S., Arenivas, F., von Abruzzese, R. & Polejaeva, I. (2008). Global gene expression analysis of bovine blastocysts produced by multiple methods. Mol. Reprod. Dev. 75, 744–58.CrossRefGoogle ScholarPubMed