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Developmental potential of pig embryos reconstructed by use of sow versus pre-pubertal gilt oocytes after somatic cell nuclear transfer*

Published online by Cambridge University Press:  18 January 2013

Juan Li ,
Hanne Skovsgaard Pedersen ,
Rong Li ,
Janne Adamsen ,
Ying Liu ,
Mette Schmidt ,
Stig Purup  and
Henrik Callesen
Juan Li
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, 210095, Jiangsu Province, Nanjing, Wei Gang 1, China. Department of Animal Science, Aarhus University, Blichers Alle 20, DK-8830 Tjele, Denmark.
Hanne Skovsgaard Pedersen
Affiliation:
Department of Animal Science, Aarhus University, Blichers Alle 20, DK-8830 Tjele, Denmark.
Rong Li
Affiliation:
Department of Animal Science, Aarhus University, Blichers Alle 20, DK-8830 Tjele, Denmark.
Janne Adamsen
Affiliation:
Department of Animal Science, Aarhus University, Blichers Alle 20, DK-8830 Tjele, Denmark.
Ying Liu
Affiliation:
Department of Animal Science, Aarhus University, Blichers Alle 20, DK-8830 Tjele, Denmark.
Mette Schmidt
Affiliation:
Veterinary Reproduction and Obstetrics, Faculty of Health and Medical Sciences, University of Copenhagen, DK-1870 Frederiksberg C, Denmark.
Stig Purup
Affiliation:
Department of Animal Science, Aarhus University, Blichers Alle 20, DK-8830 Tjele, Denmark.
Henrik Callesen*
Affiliation:
Department of Animal Science, Aarhus University, Blichers Alle 20, DK-8830 Tjele, Denmark.
*
All correspondence to: Henrik Callesen. Department of Animal Science, Aarhus University, Blichers Alle 20, DK-8830 Tjele, Denmark. Tel: +45 8715 7989. Fax: +45 8715 4249. e-mail: Henrik.Callesen@agrsci.dk
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Summary

In this study, the developmental ability of cloned embryos using gilt versus sow oocytes was evaluated under the hypothesis that the efficiency of nuclear transfer using gilt oocytes was lower than that of sow oocytes, but that it could be optimized. Five experiments were performed with routine production of cloned embryos with sow oocytes serving as the control. Results showed that: Experiment 1: Blastocyst rates of cloned embryos with gilt oocytes was about half compared with control. Experiment 2: An extended maturation time of 48 h used for gilt oocytes resulted in lower blastocyst rates after cloning. Experiment 3: Development of cloned embryos with gilt oocytes was improved by co-culture with sow oocytes. Experiment 4: After maturation of gilt oocytes using follicular fluid from gilt instead of sow, the oocytes were sorted into large and small oocytes, and after cloning, blastocyst rates were higher using large gilt oocytes compared with small oocytes; however, the rate remained lower compared with control. Experiment 5: Six sow recipients received a total of 503 morulae and blastocysts cloned from gilt oocytes (four recipients) and 190 cloned from sow oocytes (two recipients). All recipients became pregnant and went to term, resulting in 26 (gilt oocytes) and six (sow oocytes) piglets. In conclusion, results confirmed that nuclear transfer efficiency was higher using sow versus gilt oocytes, but the use of gilt oocytes can be optimized by sorting after ooplasm size following maturation and by maturing gilt and sow oocytes together.

Keywords

Co-cultureCytoplasmHand-made cloningIn vitroPiglets
Type
Research Article
Information
Zygote , Volume 22 , Issue 3 , August 2014 , pp. 356 - 365
Copyright
Copyright © Cambridge University Press 2013 

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Footnotes

*

This work was carried out at the Department of Animal Science, Aarhus University, Denmark.

References

Abeydeera, L.R., Wang, W.H., Cantley, T.C., Rieke, A. & Day, B.N. (1998a). Coculture with follicular shell pieces can enhance the developmental competence of pig oocytes after in vitro fertilization: relevance to intracellular glutathione. Biol. Reprod. 58, 213–8.CrossRefGoogle ScholarPubMed
Abeydeera, L.R., Wang, W.H., Cantley, T.C., Rieke, A., Prather, R.S. & Day, B.N. (1998b). Presence of epidermal growth factor during in vitro maturation of pig oocytes and embryo culture can modulate blastocyst development after in vitro fertilization. Mol. Reprod. Dev. 51, 395–401.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
Ahn, K.S., Kim, Y.J., Kim, M., Lee, B.H., Heo, S.Y., Kang, M.J., Kang, Y.K., Lee, J.W., Nho, W.G., Hwang, S.S., Woo, J.S., Park, J.K., Park, S.B. & Shim, H. (2011). Resurrection of an alpha-1,3-galactosyltransferase gene-targeted miniature pig by recloning using postmortem ear skin fibroblasts. Theriogenology 75, 933–9.Google Scholar
Bagg, M. A., Nottle, M. B., Grupen, C. G. & Armstrong, D. T. (2006). Effect of dibutyryl cAMP on the cAMP content, meiotic progression, and developmental potential of in vitro matured pre-pubertal and adult pig oocytes. Mol. Reprod. Dev. 73, 1326–32.Google Scholar
Byskov, A.G., Yding, A.C., Hossaini, A. & Guoliang, X. (1997). Cumulus cells of oocyte-cumulus complexes secrete a meiosis-activating substance when stimulated with FSH. Mol. Reprod. Dev. 46, 296–305.Google Scholar
Chen, T., Zhang, Y.L., Jiang, Y., Liu, J.H., Schatten, H., Chen, D.Y. & Sun, Q.Y. (2006). Interspecies nuclear transfer reveals that demethylation of specific repetitive sequences is determined by recipient ooplasm but not by donor intrinsic property in cloned embryos. Mol. Reprod. Dev. 73, 313–7.CrossRefGoogle Scholar
Cho, S.K., Hwang, K.C., Choi, Y.J., Bui, H.T., Nguyen, V.T., Park, C., Kim, J.H. & Kim, J.H. (2009). Production of transgenic pigs harboring the human erythropoietin (hEPO) gene using somatic cell nuclear transfer. J. Reprod. Dev. 55, 128–36.Google Scholar
Choi, Y.H., Takagi, M., Kamishita, H., Wijayagunawardane, M.P., Acosta, T.J., Miyazawa, K. & Sato, K. (1998). Developmental capacity of bovine oocytes matured in two kinds of follicular fluid and fertilized in vitro . Anim Reprod. Sci. 50, 27–33.CrossRefGoogle ScholarPubMed
Dostal, J. & Pavlok, A. (1996). Isolation and characterization of maturation inhibiting compound in bovine follicular fluid. Reprod. Nutr. Dev. 36, 681–90.Google Scholar
Du, Y., Kragh, P.M., Zhang, Y., Li, J., Schmidt, M., Bogh, I.B., Zhang, X., Purup, S., Jorgensen, A.L., Pedersen, A.M., Villemoes, K., Yang, H., Bolund, L. & Vajta, G. (2007). Piglets born from handmade cloning, an innovative cloning method without micromanipulation. Theriogenology 68, 1104–10.Google Scholar
Holker, M., Petersen, B., Hassel, P., Kues, W.A., Lemme, E., Lucas-Hahn, A. & Niemann, H. (2005). Duration of in vitro maturation of recipient oocytes affects blastocyst development of cloned porcine embryos. Cloning Stem Cells 7, 35–44.Google Scholar
Hong, J.Y., Yong, H.Y., Lee, B.C., Hwang, W.S., Lim, J.M. & Lee, E.S. (2004). Effects of amino acids on maturation, fertilization and embryo development of pig follicular oocytes in two IVM media. Theriogenology 62, 1473–82.CrossRefGoogle ScholarPubMed
Hoshino, Y., Uchida, M., Shimatsu, Y., Miyake, M., Nagao, Y., Minami, N., Yamada, M. & Imai, H. (2005). Developmental competence of somatic cell nuclear transfer embryos reconstructed from oocytes matured in vitro with follicle shells in miniature pig. Cloning Stem Cells 7, 17–26.CrossRefGoogle ScholarPubMed
Hyun, S.H., Lee, G.S., Kim, D.Y., Kim, H.S., Lee, S.H., Kim, S., Lee, E.S., Lim, J.M., Kang, S.K., Lee, B.C. & Hwang, W.S. (2003). Effect of maturation media and oocytes derived from sows or gilts on the development of cloned pig embryos. Theriogenology 59, 1641–9.Google Scholar
Ikeda, K. & Takahashi, Y. (2001). Effects of maturational age of porcine oocytes on the induction of activation and development in vitro following somatic cell nuclear transfer. J. Vet. Med. Sci. 63, 1003–8.CrossRefGoogle ScholarPubMed
Ikeda, K. & Takahashi, Y. (2003). Comparison of maturational and developmental parameters of oocytes recovered from prepubertal and adult pigs. Reprod. Fertil. Dev. 15, 215–21.CrossRefGoogle ScholarPubMed
Jakobsen, J.E., Li, J., Kragh, P.M., Moldt, B., Lin, L., Liu, Y., Schmidt, M., Winther, K.D., Schyth, B.D., Holm, I.E., Vajta, G., Bolund, L., Callesen, H., Jørgensen, A.L., Nielsen, A.L & Mikkelsen, J.G. (2011). Pig transgenesis by Sleeping Beauty DNA transposition. Transgenic Res. 20, 533–45.Google Scholar
Kidson, A., Schoevers, E., Langendijk, P., Verheijden, J., Colenbrander, B. & Bevers, M. (2003). The effect of oviductal epithelial cell co-culture during in vitro maturation on sow oocyte morphology, fertilization and embryo development. Theriogenology 59, 1889–903.CrossRefGoogle ScholarPubMed
Kikuchi, K., Nagai, T., Ding, J., Yamauchi, N., Noguchi, J. & Izaike, Y. (1999). Cytoplasmic maturation for activation of pig follicular oocytes cultured and arrested at metaphase I. J. Reprod. Fertil. 116, 143–56.Google Scholar
Kikuchi, K., Naito, K., Noguchi, J., Kaneko, H. & Tojo, H. (2002). Maturation/M-phase promoting factor regulates aging of porcine oocytes matured in vitro . Cloning Stem Cells 4, 211–22.CrossRefGoogle ScholarPubMed
Koo, D.B., Kang, Y.K., Choi, Y.H., Park, J.S., Kim, H.N., Oh, K.B., Son, D.S., Park, H., Lee, K.K. & Han, Y.M. (2002). Aberrant allocations of inner cell mass and trophectoderm cells in bovine nuclear transfer blastocysts. Biol. Reprod. 67, 487–92.Google Scholar
Kragh, P.M., Vajta, G., Corydon, T.J., Purup, S., Bolund, L. & Callesen, H. (2004). Production of transgenic porcine blastocysts by hand-made cloning. Reprod. Fertil. Dev. 16, 315–8.Google Scholar
Kragh, P.M., Nielsen, A.L., Li, J., Du, Y., Lin, L., Schmidt, M., Bogh, I.B., Holm, I.E., Jakobsen, J.E., Johansen, M.G., Purup, S., Bolund, L., Vajta, G. & Jorgensen, A.L. (2009). Hemizygous minipigs produced by random gene insertion and handmade cloning express the Alzheimer's disease-causing dominant mutation APPsw. Transgenic Res. 18, 545–58.Google Scholar
Kuhholzer, B., Hawley, R.J., Lai, L., Kolber-Simonds, D. & Prather, R.S. (2001). Clonal lines of transgenic fibroblast cells derived from the same fetus result in different development when used for nuclear transfer in pigs. Biol. Reprod. 64, 1695–8.Google Scholar
Kurome, M., Ishikawa, T., Tomii, R., Ueno, S., Shimada, A., Yazawa, H. & Nagashima, H. (2008). Production of transgenic and non-transgenic clones in miniature pigs by somatic cell nuclear transfer. J. Reprod. Dev. 54, 156–63.Google Scholar
Lee, G.S., Kim, H.S., Hyun, S.H., Lee, S.H., Jeon, H.Y., Nam, D.H., Jeong, Y.W., Kim, S., Kim, J.H., Han, J.Y., Ahn, C., Kang, S.K., Lee, B.C. & Hwang, W.S. (2005). Production of transgenic cloned piglets from genetically transformed fetal fibroblasts selected by green fluorescent protein. Theriogenology 63, 973–91.Google Scholar
Li, J., Du, Y., Zhang, Y.H., Kragh, P.M., Purup, S., Bolund, L., Yang, H., Xue, Q.Z. & Vajta, G. (2006). Chemically assisted handmade enucleation of porcine oocytes. Cloning Stem Cells 8, 241–50.Google Scholar
Li, J., Villemoes, K., Zhang, Y., Du, Y., Kragh, P.M., Purup, S., Xue, Q., Pedersen, A.M., Jorgensen, A.L., Jakobsen, J.E., Bolund, L., Yang, H. & Vajta, G. (2009). Efficiency of two enucleation methods connected to handmade cloning to produce transgenic porcine embryos. Reprod. Domest. Anim. 44, 122–7.CrossRefGoogle ScholarPubMed
Liu, L., Dai, Y. & Moor, R. M. (1997). Role of secreted proteins and gonadotrophins in promoting full maturation of porcine oocytes in vitro . Mol. Reprod. Dev. 47, 191–9.Google Scholar
Luo, Y., Li, J., Liu, Y., Lin, L., Du, Y., Li, S., Yang, H., Vajta, G., Callesen, H., Bolund, L., Sørensen, C.B. (2011). High efficiency of BRCA1 knockout using rAAV-mediated gene targeting: developing a pig model for breast cancer. Transgenic Res. 20, 975–88.CrossRefGoogle ScholarPubMed
Makarevich, A.V., Sirotkin, A.V. & Genieser, H.G. (2004). Action of protein kinase A regulators on secretory activity of porcine granulosa cells in vitro . Anim. Reprod. Sci. 81, 125–36.CrossRefGoogle ScholarPubMed
Miyoshi, K., Rzucidlo, S.J., Pratt, S.L. & Stice, S.L. (2002). Utility of rapidly matured oocytes as recipients for production of cloned embryos from somatic cells in the pig. Biol. Reprod. 67, 540–5.Google Scholar
Miyoshi, K., Rzucidlo, S.J., Pratt, S.L. & Stice, S.L. (2003). Improvements in cloning efficiencies may be possible by increasing uniformity in recipient oocytes and donor cells. Biol. Reprod. 68, 1079–86.Google Scholar
Nottle, M.B., Beebe, L.F., Harrison, S.J., McIlfatrick, S.M., Ashman, R.J., O'Connell, P.J., Salvaris, E.J., Fisicaro, N., Pommey, S., Cowan, P.J. & d'Apice, A.J. (2007). Production of homozygous alpha-1,3-galactosyltransferase knockout pigs by breeding and somatic cell nuclear transfer. Xenotransplantation. 14, 339–44.CrossRefGoogle ScholarPubMed
Park, K.W., Choi, K.M., Hong, S.P., Han, G.S., Yoo, J.Y., Jin, D.I., Seol, J.G. & Park, C.S. (2008). Production of transgenic recloned piglets harboring the human granulocyte-macrophage colony stimulating factor (hGM-CSF) gene from porcine fetal fibroblasts by nuclear transfer. Theriogenology 70, 1431–8.CrossRefGoogle ScholarPubMed
Peura, T.T., Lewis, I.M. & Trounson, A.O. (1998). The effect of recipient oocyte volume on nuclear transfer in cattle. Mol. Reprod. Dev. 50, 185–91.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Schmidt, M., Kragh, P.M., Li, J., Du, Y., Lin, L., Liu, Y., Bogh, I.B., Winther, K.D., Vajta, G. & Callesen, H. (2010). Pregnancies and piglets from large white sow recipients after two transfer methods of cloned and transgenic embryos of different pig breeds. Theriogenology 74, 1233–40.Google Scholar
Sommer, J.R., Estrada, J.L., Collins, E.B., Bedell, M., Alexander, C.A., Yang, Z., Hughes, G., Mir, B., Gilger, B.C., Grob, S., Wei, X., Piedrahita, J.A., Shaw, P.X., Petters, R.M. & Zhang, K. (2011). Production of ELOVL4 transgenic pigs: a large animal model for Stargardt-like macular degeneration. Br. J. Ophthalmol. 95, 1749–54.Google Scholar
Song, K. & Lee, E. (2007). Modification of maturation condition improves oocyte maturation and in vitro development of somatic cell nuclear transfer pig embryos. J. Vet. Sci. 8, 81–7.Google Scholar
Tao, T., Machaty, Z., Boquest, A.C., day, B.N. & Prather, R.S. (1999). Development of pig embryos reconstructed by microinjection of cultured fetal fibroblast cells into in vitro matured oocytes. Anim Reprod. Sci. 56, 133–41.Google Scholar
Vajta, G., Peura, T.T., Holm, P., Paldi, A., Greve, T., Trounson, A.O. & Callesen, H. (2000). New method for culture of zona-included or zona-free embryos: the Well of the Well (WOW) system. Mol. Reprod. Dev. 55, 256–64.Google Scholar
Wiesak, T., Hunter, M.G. & Foxcroft, G.R. (1990). Differences in follicular morphology, steroidogenesis and oocyte maturation in naturally cyclic and PMSG/hCG-treated prepubertal gilts. J. Reprod. Fertil. 89, 633–41.Google Scholar
Yoshioka, K., Suzuki, C., Tanaka, A., Anas, I.M. & Iwamura, S. (2002). Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol. Reprod. 66, 112–9.CrossRefGoogle Scholar