Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-29T00:07:26.801Z Has data issue: false hasContentIssue false
  • English
  • Français

Developmental potential and kinetics of pig embryos with different cytoplasmic volume

Published online by Cambridge University Press:  15 November 2013

Juan Li ,
Rong Li ,
Klaus Villemoes ,
Ying Liu ,
Stig Purup  and
Henrik Callesen
Juan Li*
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, 210095, Jiangsu Province, Nanjing, Wei Gang No. 1, China. Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark.
Rong Li
Affiliation:
Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark.
Klaus Villemoes
Affiliation:
Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark.
Ying Liu
Affiliation:
Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark.
Stig Purup
Affiliation:
Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark.
Henrik Callesen
Affiliation:
Department of Animal Science, Aarhus University, DK-8830 Tjele, Denmark.
*
All correspondence to: Juan Li. College of Animal Science and Technology, Nanjing Agricultural University, 210095, Jiangsu Province, Nanjing, Wei Gang No. 1, China. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The effects of cytoplasmic volumes on development and developmental kinetics of in vitro produced porcine embryos were investigated. During hand-made cloning (HMC), selected cytoplasts were separated into two groups according to their size in relation to the initial oocyte: ~75% or ~50%. Following two fusion steps and activation (day 0), reconstructed embryos were cultured in vitro for 6 days. Cleavage rates on day 2 as well as blastocyst rates and cell numbers on day 6 were recorded. Results showed that embryo development was no different for ~50% versus ~75% cytoplasm at first fusion. This result was used in the following experiments, where the effect of varying cytoplasm volume in second fusion to obtain a final cytoplasm volume of ~75% to ~200% was tested. The results showed that the lowest quality was obtained when the final cytoplasm volume was ~75% and the highest quality at ~200% of the original oocyte. Similar results were observed in parthenogenetic (PA) embryos activated with different cytoplasmic volumes. A common pattern for the developmental kinetics of HMC and PA embryos was observed: the smaller group tended to have a longer time for the first two cell cycles, but subsequently a shorter time to form morula and blastocyst. In conclusion, the developmental kinetics of in vitro produced embryos was affected by the cytoplasm volume of the initial oocyte, and this further accounted for the developmental ability of the reconstructed embryos.

Keywords

Cell cycleIn vitro maturationPorcineSomatic cell nuclear transferTime-lapse
Type
Research Article
Information
Zygote , Volume 23 , Issue 2 , April 2015 , pp. 277 - 287
Copyright
Copyright © Cambridge University Press 2013 

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

Al-Mashhadi, R.H., Sørensen, C.B., Kragh, P.M., Christoffersen, C., Mortensen, M.B., Tolbod, L.P., Thim, T., Du, Y., Li, J., Liu, Y., Moldt, B., Schmidt, M., Vajta, G., Larsen, T., Purup, S., Bolund, L., Nielsen, L.B., Callesen, H., Falk, E., Mikkelsen, J.G. & Bentzon, J.F. (2013). Familial hypercholesterolemia and atherosclerosis in cloned minipigs created by DNA transposition of a human PCSK9 gain-of-function mutant. Sci. Transl. Med. 5, 166ra1.Google Scholar
Boquest, A.C., Grupen, C.G., Harrison, S.J., McIlfatrick, S.M., Ashman, R.J., d’Apice, A. J. & Nottle, M.B. (2002). Production of cloned pigs from cultured fetal fibroblast cells. Biol. Reprod. 66, 1283–7.Google Scholar
Bordignon, V. & Smith, L.C. (1998). Telophase enucleation: an improved method to prepare recipient cytoplasts for use in bovine nuclear transfer. Mol. Reprod. Dev. 49, 29–36.Google Scholar
Cao, W., Brenner, C.A., Alikani, M., Cohen, J. & Warner, C.M. (1999). Search for a human homologue of the mouse Ped gene. Mol. Hum. Reprod. 5, 541–7.Google Scholar
Chen, X.Y., Li, Q.W., Zhang, S.S., Han, Z.S., Zhao, R., Wu, S.Y. & Huwang, J. (2007). Effects of ovarian cortex cell co-culture during in vitro maturation on porcine oocytes maturation fertilization and embryo development. Anim. Reprod. Sci. 99, 306–16.Google Scholar
Cui, L.B., Huang, X.Y. & Sun, F.Z. (2005). Nucleocytoplasmic ratio of fully grown germinal vesicle oocytes is essential for mouse meiotic chromosome segregation and alignment, spindle shape and early embryonic development. Hum. Reprod. 20, 2946–53.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
El Shourbagy, S.H., Spikings, E.C., Freitas, M. & St John, J.C. (2006). Mitochondria directly influence fertilization outcome in the pig. Reproduction 131, 233–45.Google Scholar
Evsikov, S.V., Morozova, L.M. & Solomko, A.P. (1990). The role of the nucleocytoplasmic ratio in development regulation of the early mouse embryo. Development 109, 323–8.Google Scholar
Fair, T., Gutierrez-Adan, A., Murphy, M., Rizos, D., Martin, F., Boland, M.P. & Callesen, H. (2004). Search for the bovine homolog of the murine Ped gene and characterization of its messenger RNA expression during bovine preimplantation development. Bio. Reprod. 70, 488–94.Google Scholar
Feng, Y.L. & Gordon, , J.W. (1997). Removal of cytoplasm from one-celled mouse embryos induces early blastocyst formation. J. Exp. Zool. 277, 345–52.Google Scholar
Fulka, J. Jr., First, N.L. & Moor, R.M. (1998). Nuclear and cytoplasmic determinants involved in the regulation of mammalian oocyte maturation. Mol. Hum. Reprod. 4, 41–9.Google Scholar
Hyun, S., Lee, G., Kim, D., Kim, H., Lee, S., Nam, D., Jeong, Y., S., Kim, Yeom, S., Kang, S., Han, J., Lee, B. & Hwang, W. (2003). Production of nuclear transfer-derived piglets using porcine fetal transfected with the enhanced green fluorescent protein. Biol. Reprod. 69, 1060–8.Google Scholar
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.Google Scholar
Kishigami, S. & Wakayama, T. (2007). Efficient strontium-induced activation of mouse oocytes in standard culture media by chelating calcium. J. Reprod. Dev. 53, 1207–15.Google Scholar
Kragh, P.M., Du, Y., Corydon, T.J., Purup, S., Bolund, L. & Vajta, G. (2005). Efficient in vitro production of porcine blastocysts by handmade cloning with a combined electrical and chemical activation. Theriogenology 64, 1536–45.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
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
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.Google Scholar
Li, Y., Liu, J., Dai, J., Xing, F., Fang, Z., Zhang, T., Shi, Z., Zhang, D. & Chen, X. (2010). Production of cloned miniature pigs by enucleation using the spindle view system. Reprod. Domest. Anim. 45, 608–13.Google Scholar
Liu, L. & Keefe, D.L. (2000). Cytoplasm mediates both development and oxidation-induced apoptotic cell death in mouse zygotes. Biol. Reprod. 62, 1828–34.Google Scholar
Liu, Y., Østrup, O., Li, J., Vajta, G., Kragh, P.M., Purup, S. & Callesen, H. (2011). Cell colony formation induced by Xenopus egg extract as a marker for improvement of cloned blastocyst formation in the pig. Cell Reprogram. 13, 521–6.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.Google Scholar
Mateusen, B., Van Soom, A., Maes, D.G., Donnay, I., Duchateau, L. & Lequarre, A.S. (2005). Porcine embryo development and fragmentation and their relation to apoptotic markers: a cinematographic and confocal laser scanning microscopic study. Reproduction 129, 443–52.Google Scholar
Memili, E. & First, N.L. (2000). Zygotic and embryonic gene expression in cow: a review of timing and mechanisms of early gene expression as compared with other species. Zygote 8, 87–96.Google Scholar
Misica-Turner, P.M., Oback, F.C., Eichenlaub, M., Wells, D.N. & Oback, B. (2007). Aggregating embryonic but not somatic nuclear transfer embryos increases cloning efficiency in cattle. Biol. Reprod. 76, 268–78.Google Scholar
Moor, R.M., Dai, Y., Lee, C. & Fulka, J. Jr. (1998). Oocyte maturation and embryonic failure. Hum. Reprod. Update 4, 223–36.Google Scholar
Park, M.R., Cho, S.K., Park, J.Y., Lee, S.Y., Choi, Y.J., Kwon, D.N., Son, W.J., Seo, H.G. & Kim, J.H. (2004). Detection of rare Leydig cell hypoplasias in somatic cell cloned male piglets. Zygote 12, 305–13.Google Scholar
Pedersen, H.G., Schmidt, M., Sangild, P.T., Strøbech, L., Vajta, G., Callesen, H. & Greve, T. (2005). Clinical experience with embryos produced by handmade cloning: work in progress. Mol. Cell. Endocrinol. 234, 137–43.Google Scholar
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.Google Scholar
Polejaeva, I.A., Chen, S.H., Vaught, T.D., Page, R.L., Mullins, J., Ball, S., Dai, Y., Boone, J., Walker, S., Ayares, D.L., Colman, A. & Campbell, K.H. (2000). Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407, 86–90.Google Scholar
Pratt, S.L., Sherrer, E.S., Reeves, D.E., Stice, S.L. (2006). Factors influencing the commercialisation of cloning in the pork industry. Soc. Reprod. Fertil. Suppl. 62, 303–15.Google Scholar
Ribeiro, E.S., Gerger, R.P., Ohlweiler, L.U., Ortigari, I. Jr, Mezzalira, J.C., Forell, F., Bertolini, L.R., Rodriques, J.L., Ambrósio, C.E., Miglino, M.A., Mezzalira, A. & Bertolini, M. (2009). Developmental potential of bovine hand-made clone embryos reconstructed by aggregation or fusion with distinct cytoplasmic volumes. Cloning Stem Cells. 11, 377–86.Google Scholar
Saito, S. & Niemann, H. (1991). Effects of extracellular matrices and growth factors on the development of isolated porcine blastomeres. Biol. Reprod. 44, 927–36.Google Scholar
Schmidt, M., Kragh, P.M., Li, J., Du, Y., Lin, L., Liu, Y., Bøgh, 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
St John, J.C. (2002). Ooplasm donation in humans: the need to investigate the transmission of mitochondrial DNA following cytoplasmic transfer. Hum. Reprod. 17, 1954–8.Google Scholar
Tecirlioglu, R.T., Cooney, M.A., Lewis, I.M., Korfiatis, N.A., Hodgson, R., Ruddock, N.T., Vajta, G., Downie, S., Trounson, A.O., Holland, M.K. & French, A.J. (2005). Comparison of two approaches to nuclear transfer in bovine: hand-made cloning with modifications and the conventional nuclear transfer technique. Reprod. Fertil. Dev. 17, 573–85.Google Scholar
Terashita, Y., Sugimura, S., Kudo, Y., Amano, R., Hiradate, Y. & Sato, E. (2011). Improving the quality of miniature pig somatic cell nuclear transfer blastocysts: aggregation of SCNT embryos at the four-cell stage. Reprod. Domest. Anim. 46, 189–96.Google Scholar
Vajta, G., Lewis, I.M., Trounson, A.O., Purup, S., Maddox-Hyttel, P., Schmidt, M., Pedersen, H. G., Greve, T. & Callesen, H. (2003). Handmade somatic cell cloning in cattle: analysis of factors contributing to high efficiency in vitro. Biol. Reprod. 68, 571–8.Google Scholar
Van Blerkom, J., Sinclair, J. & Davis, P. (1998). Mitochondria transfer between oocytes: potential applications of mitochondrial donation and the issue of heteroplasmy. Hum. Reprod. 13, 2857–68.Google Scholar
Wakayama, S., Kishigami, S., Nguyen, V.T., Ohta, H., Hikichi, T., Mizutani, E., Bui, H.T., Miyake, M. & Wakayama, T. (2008). Effect of volume of oocyte cytoplasm on embryo development after parthenogenetic activation, intracytoplasmic sperm injection, or somatic cell nuclear transfer. Zygote 16, 211–22.Google Scholar
Warner, C.M., Cao, W. & Exley, G.E. (1998). Genetic regulation of egg and embryo survival. Human Reproduction 13, 178–90.Google Scholar
Westhusin, M.E., Collas, P., Marek, D., Sullivan, E., Stepp, P., Pryor, J. & Barnes, F. (1996). Reducing the amount of cytoplasm available for early embryonic development decreases the quality but not quantity of embryos produced by in vitro fertilization and nuclear transplantation. Theriogenology 46, 243–52.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.Google Scholar