Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-24T14:48:51.042Z Has data issue: false hasContentIssue false
  • English
  • Français

Elongation and gene expression in bovine cloned embryos transferred to temporary recipients

Published online by Cambridge University Press:  08 June 2009

Lleretny Rodríguez-Alvarez ,
José Cox ,
Felipe Navarrete ,
Cristián Valdés ,
Teresa Zamorano ,
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.
Felipe Navarrete
Affiliation:
Department of Animal Science, Faculty of Veterinary Medicine, Universidad de Concepción, Avenida Vicente Méndez 595, Chillán, Chile.
Cristián Valdés
Affiliation:
Department of Animal Science, Faculty of Veterinary Medicine, Universidad de Concepción, Avenida Vicente Méndez 595, Chillán, Chile.
Teresa Zamorano
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. 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: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Elongated embryos provide a unique source of information about trophoblastic differentiation, gene expression and maternal-embryonic interactions; however they are difficult and costly to obtain, especially elongated cloned embryos. One alternative is their production in heterologous temporary recipients such as sheep and goats. We aimed to produce elongated bovine cloned embryos using heterologous transfer to temporary recipients. Day-7 cloned cattle blastocysts were transferred to the uteri of ewes and goats and recovered as elongated structures at day 17. We evaluated elongation, length, presence of embryonic disc and expression of several important genes for embryonic development. We also produced homologous (cloned cattle embryos transferred into cattle uteri). Cloned bovine blastocysts were able to proceed with preimplantation development through elongation with high efficiency despite the species to which they were transferred. In qualitative and quantitative RT-PCR experiments we found differences in the pattern of gene expression among embryos recovered from different species. Sox2, Nanog and FGF-4 were markedly deregulated. No previous reports about the expression pattern of the studied genes had been published for elongated bovine cloned embryos produced in intermediate recipients, furthermore, the pattern of expression of Nanog, Oct4, Eomes, Cdx2, IFN-tau, Dicer, FGF-4 and Sox2 shown here are novel for elongated cloned bovine embryos created by hand-made cloning. Our data confirmed that sheep and goats can be used as temporary recipients. This model could serve as a basis for further research on gene expression and cellular changes during bovine peri-implantation development.

Keywords

BlastocystElongationGene expressionHand-made cloningPeri-implantation
Type
Research Article
Information
Zygote , Volume 17 , Issue 4 , November 2009 , pp. 353 - 365
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

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 (2), 279–90.CrossRefGoogle ScholarPubMed
Bavister, B.D. (2002). How animal embryo research led to the first documented human IVF. Reprod. Biomed. Online 4 (Suppl 1), 24–9.CrossRefGoogle Scholar
Bertolini, M., Beam, S.W., Shim, H., Bertolini, L.R., Moyer, A.L., Famula, TR. & Anderson, G.B. (2002). Growth, development and gene expression by in vivo and in vitro-produced day 7 and 16 embryos. Mol. Reprod. Dev. 63, 318–28.CrossRefGoogle ScholarPubMed
Betteridge, K.J. & Flechon, J.E. (1988). The anatomy and physiology of preattachment bovine embryos. Theriogenology 29, 155–87.CrossRefGoogle Scholar
Bondioli, K.J., Beiry, K.A., Hill, K.G., Jones, K.B. & De Mayo, F.J. (1991). Production of transgenic cattle by microinjection. In Transgenic Animals (eds First, N.L. & Haseltine, F.P.) pp. 265–73. Boston: Butterworth-Heinemann.Google Scholar
Brandao, D., Maddox-Hyttel, P., Løvendahl, P., Rumpf, R., Stringfellow, D. & Callesen, H. (2004). Post hatching development: a novel system for extended in vitro culture of bovine embryos. Biol. Reprod. 71, 2048–55.Google Scholar
Chang, M.C. (1952). Development of bovine blastocyst with a note on implantation. Anat. Rec. 113, 143–61.CrossRefGoogle ScholarPubMed
Cox, J.F. & Alfaro, V. (2007). In vitro fertilization and development of OPU derived goat and sheep oocytes. Reprod. Domest. Anim. 42, 83–7.Google Scholar
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. Develop. 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 × Zebu cross cattle as oocyte donors for in vitro embryo production and gene microinjection. Theriogenology. 42, 977–85.CrossRefGoogle ScholarPubMed
Degrelle, S.A., 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, 448–640.CrossRefGoogle ScholarPubMed
Ellington, J.E., Farrell, P.B., Simkin, M.E., Foote, R.H., Goldman, E.E. & McGrath, A.B. (1990). Development and survival after transfer of cow embryos cultured from 1–2-cells to morulae or blastocysts in rabbit oviducts or in a simple medium with bovine oviduct epithelial cells. J. Reprod. Fertil. 89, 293–9.Google Scholar
Eyestone, W.H., Leibfried-Rutledge, M.L., Northey, D.L., Gilligan, B.G. & First, N.L. (1987). Culture of one- and two-cell bovine embryos to the blastocyst stage in the ovine oviduct. Theriogenology. 28, 1–7.CrossRefGoogle Scholar
George, F., Daniaux, C., Genicot, G., Verhaeghe, B., Lambert, P. & Donnay, I. (2008). Set up of a serum-free culture system for bovine embryos: embryo development and quality before and after transient transfer. Theriogenology 69, 612–23.CrossRefGoogle ScholarPubMed
Greenstein, J.S., Murray, R.W. & Foley, R.C. (1958). Observations on the morphogenesis and histochemistry of the bovine preattachment placenta between 16 and 33 days of gestation. Anat. Rec. 132, 321–41.Google Scholar
Guillomot, M. (1995). Cellular interactions during implantation in domestic ruminants. J. Reprod. Fertil. Suppl. 49, 39–51.Google 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
Hoffert, K.A., Batchelder, C.A., Bertolini, M., Moyer, A.L., Famula, T.R., anderson, D.L. & Anderson, G.B. (2005). Measures of maternal–fetal interaction in day–30 bovine pregnancies derived from nuclear transfer. Cloning Stem Cells 7, 289–305.CrossRefGoogle ScholarPubMed
Hue, I., Degrelle, S.A., Campion, E. & Renard, J.P. (2007). Gene expression in elongating and gastrulating embryos from ruminants. Soc. Reprod. Fertil. Suppl. 64, 365–77.Google ScholarPubMed
Hue, I., Renard, J.P. & Viebahn, C. (2001). Brachyury is expressed in gastrulating bovine embryos well ahead of implantation. Dev. Genes. Evol. 211, 157–9.CrossRefGoogle ScholarPubMed
Kubisch, H.M., Larson, M.A. & Roberts, R.M. 1998. Relationship between age of blastocyst formation and interferon secretion by in vitro-derived bovine embryos. Mol. Reprod. Dev. 49, 254–60.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
López-Gatius, F. & Hunter, R.H. (2005). Spontaneous reduction of advanced twin embryos: its occurrence and clinical relevance in dairy cattle. Theriogenology. 63, 118–25.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
Morris, D.G., Diskin, M.G. & Sreenan, J.M. (2000). Protein synthesis and phosphorylation by elongating 13–15-day-old cattle blastocysts. Reprod. Fertil. Dev. 12, 39–44.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
Rexroad, C.E. Jr & Powell, A.M. (1999). The ovine uterus as a host for in vitro-produced bovine embryos. Theriogenology. 15, 351–64.CrossRefGoogle Scholar
Ribas, R.C., Taylor, J.E., McCorquodale, C., Maurício, A.C., Sousa, M. & Wilmut, I. (2006). Effect of zona pellucida removal on DNA methylation in early mouse embryos. Biol Reprod. 74, 307–13.CrossRefGoogle ScholarPubMed
Rizos, D., Pintado, B., de la Fuente, J., Lonergan, P. & Gutiérrez-Adán, A. (2007). Development and pattern of mRNA relative abundance of bovine embryos cultured in the isolated mouse oviduct in organ culture. Mol. Reprod. Dev. 74, 716–23.CrossRefGoogle ScholarPubMed
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, 470–4.CrossRefGoogle ScholarPubMed
Rodríguez, L.I., 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.Google Scholar
Sawai, K., Kageyama, S., Moriyasu, S., Hirayama, H., Minamihashi, A. & Onoe, S. (2007). Changes in the mRNA transcripts of insulin-like growth factor ligand, receptors and binding proteins in bovine blastocysts and elongated embryos derived from somatic cell nuclear transfer. J. Reprod. Dev. 53, 77–86.CrossRefGoogle ScholarPubMed
Sirard, M.A., Lambert, R.D., Ménard, D.P. & Bedoya, M. (1985). Pregnancies after in-vitro fertilization of cow follicular oocytes, their incubation in rabbit oviduct and their transfer to the cow uterus. J. Reprod. Fertil. 75, 551–6.Google Scholar
Talbot, N.C., Powell, A., Garrett, W., Edwards, J.L. & Rexroad, C. Jr. (2000). Ultrastructural and karyotypic examination of in vitro produced bovine embryos developed in the sheep uterus. Tissue Cell 32, 19–27.CrossRefGoogle ScholarPubMed
Tveden-Nyborg, P., Peura, T.T., Hartwich, K.M., Walker, S.K. & Maddox-Hyttel, P. (2005). Morphological characterization of pre- and peri-implantation in vitro cultured somatic cell nuclear transfer and in vivo derived ovine embryos. Reproduction 130, 681–94.CrossRefGoogle ScholarPubMed
Vajta, G., Peura, T.T., Holm, P., Paldi, A., Greve, T. & Trounson, A.O. (2000a). New method for culture of zona-included or zona-free embryos: the well of the well (WOW) system. Mol. Reprod. Dev. 55, 256–64.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Vajta, G., Hyttel, P. & Trounson, A.O. (2000b). Post-hatching development of in vitro produced bovine embryos on agar and collagen gels. Anim. Reprod. Sci. 60–61, 208–12.Google Scholar