Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T15:22:21.140Z Has data issue: false hasContentIssue false
  • English
  • Français

Ooplasm transfer and interspecies somatic cell nuclear transfer: heteroplasmy, pattern of mitochondrial migration and effect on embryo development

Published online by Cambridge University Press:  25 August 2010

Marina J. Sansinena ,
John Lynn ,
Kenneth R. Bondioli ,
Richard S. Denniston  and
Robert A. Godke
Marina J. Sansinena*
Affiliation:
Facultad de Ciencias Agrarias, Universidad Católica Argentina, Cap. Gral. R. Freire 183, CABA 1426, Argentina.
John Lynn
Affiliation:
Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
Kenneth R. Bondioli
Affiliation:
Embryo Biotechnology Laboratory, Reproductive Biology Center, Louisiana State University Agricultural Center, St. Gabriel, LA 70776, USA. Department of Animal Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
Richard S. Denniston
Affiliation:
Embryo Biotechnology Laboratory, Reproductive Biology Center, Louisiana State University Agricultural Center, St. Gabriel, LA 70776, USA. Department of Animal Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
Robert A. Godke
Affiliation:
Embryo Biotechnology Laboratory, Reproductive Biology Center, Louisiana State University Agricultural Center, St. Gabriel, LA 70776, USA. Department of Animal Sciences, Louisiana State University, Baton Rouge, LA 70803, USA.
*
All correspondence to: Marina Sansinena. Facultad de Ciencias Agrarias, Universidad Católica Argentina, Cap. Gral. R. Freire 183, CABA 1426, Argentina. Tel: +5411 4552 2711/2721. e-mail: msansinena@uca.edu.ar
Get access Rights & Permissions [Opens in a new window]

Summary

Although interspecies somatic cell nuclear transfer (iSCNT) has potential applications in the conservation of exotic species, an in vitro developmental block has been observed in embryos produced by this approach. It has been suggested that mitochondrial mismatch between donor cell and recipient oocyte could cause embryonic developmental arrest. A series of experiments was conducted to investigate the effect of mixed mitochondrial populations (heteroplasmy) on early development of iSCNT-derived cloned embryos. The effect of combining the techniques of ooplasm transfer (OT) and somatic cell nuclear transfer (SCNT) was examined by monitoring in vitro embryonic development; the presence and pattern of migration of foreign mitochondria after OT was analysed by MitoTracker staining. In addition, the effect of transferring caprine ooplasm (iOT) into the bovine enucleated oocytes used in iSCNT was analysed. There was no significant effect of the sequence of events (OT-SCNT or SCNT-OT) on the number of fused, cleaved, blastocyst or hatched blastocyst stage embryos. MitoTracker Green staining of donor oocytes used for OT confirmed the introduction of foreign mitochondria. The distribution pattern of transferred mitochondria most commonly remained in a distinct cluster after 12, 74 and 144 h of in vitro culture. When goat ooplasm was injected into bovine enucleated oocytes (iSCNT), there was a reduction (p < 0.05) in fusion (52 vs. 82%) and subsequent cleavage rates (55 vs. 78%). The procedure of iOT prior to iSCNT had no effect in overcoming the 8- to 16-cell in vitro developmental block, and only parthenogenetic cow and goat controls reached the blastocyst (36 and 32%) and hatched blastocyst (25 and 12%) stages, respectively. This study indicates that when foreign mitochondria are introduced at the time of OT, these organelles tend to remain as distinct clusters without relocation after a few mitotic divisions. Although the bovine cytoplast appears capable of supporting mitotic divisions after iOT-iSCNT, heteroplasmy or mitochondrial incompatibilities may affect nuclear-ooplasmic events occurring at the time of genomic activation.

Keywords

HeteroplasmyInterspeciesMitochondriaNuclear transferOoplasm transfer
Type
Research Article
Information
Zygote , Volume 19 , Issue 2 , May 2011 , pp. 147 - 156
Copyright
Copyright © Cambridge University Press 2010

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

Barritt, J.A, Brenner, C.A, Malter, H.E. & Cohen, J. (2001). Mitochondria in human offspring derived from ooplasmic transplantation. Hum. Reprod. 16, 513–6.CrossRefGoogle ScholarPubMed
Bhuiyan, M.M., Suzuki, Y., Watanabe, H., Lee, E., Hirayama, H., Matsuoka, K., Fujise, Y., Ishikawa, H., Ohsumi, S. & Fukui, Y. (2010). Production of Sei whale (Balaenoptera borealis) clones embryos by inter- and intra-species somatic cell nuclear transfer. J. Reprod. Dev. 56, 131–9.CrossRefGoogle ScholarPubMed
Brenner, C.A., Barritt, J.A., Willadsen, S. & Cohen, J. (2000). Mitochondrial DNA heteroplasmy after human ooplasmic transplantation. Fertil. Steril. 74, 573–8.CrossRefGoogle ScholarPubMed
Bui, L.C., Vignon, X., Campion, E., Laloy, E., Lavergne, Y., Ty, L.V., Nguyen, B.X. & Renard, J.P. (2002). Use of interspecies nuclear transfer to study the early embryonic development and nuclear activities of the endangered species Pseudoryx nghetinhensis (saola). Theriogenology 57, 427 (abstr.).Google Scholar
Cibelli, J.B., Stice, S.L., Golueke, P.J., Kane, J.J., Jerry, J., Blackwell, C., Ponce de Leon, F.A. & Robl, J.M. (1998). Cloned transgenic calves produced from non-quiescent fetal fibroblasts. Science 280, 1256–8.CrossRefGoogle Scholar
Cibelli, J.B., Kiessling, A.A., Cunniff, K., Richards, C., Lanza, R.P. & West, M.D. (2001). Somatic cell nuclear transfer in humans: pronuclear and early embryonic development. J. Regen. Med. 2, 25–31.Google Scholar
Cohen, J., Scott, R., Schimmel, T., Levron, J. & Willadsen, S. (1997). Birth of an infant after transfer of anucleate donor oocyte cytoplasm into recipient eggs. Lancet 350, 186–7.CrossRefGoogle ScholarPubMed
Cohen, J., Scott, R., Alikani, M., Schimmel, T., Munné, S., Levron, J., Wu, L., Brenner, C., Warner, C. & Willadsen, S. (1998). Ooplasmic transfer in mature human oocytes. Mol. Hum. Reprod. 4, 269–80.CrossRefGoogle ScholarPubMed
Colman, A. (2000). Somatic cell nuclear transfer in mammals: progress and applications. Cloning 1, 185–200.CrossRefGoogle Scholar
Damiani, P., Wirtu, G., Miller, F., Cole, A., Pope, C., Godke, R.A. & Dresser, B.L. (2003). Development of giant eland (Taurotragus oryx) and bovine (Bos taurus) oocytes. Theriogenology 59, 390 (abstr.).Google Scholar
Dominko, T., Mitalipova, M., Haley, B., Beyhan, Z., Memili, E., McKusick, B. & First, N.L. (1999). Bovine oocyte cytoplasm supports development of embryos produced by nuclear transfer of somatic cell nuclei from various mammalian species. Biol. Reprod. 60, 1496–1502.CrossRefGoogle ScholarPubMed
Ebert, K.M., Liem, H. & Hecht, N.B. (1988). Mitochondrial DNA in the mouse preimplantation embryo. J. Reprod. Fertil. 82, 145–9.CrossRefGoogle ScholarPubMed
Enright, B.P., Taneja, M., Schreiber, D., Riesen, J., Tian, X.C., Fortune, J.E. & Yang, X. (2002). Reproductive characteristics of cloned heifers derived from adult somatic cells. Biol. Reprod. 66, 291–6.CrossRefGoogle ScholarPubMed
Ferreira, C.R., Burgstaller, J.P., Perecin, F., Garcia, J.M., Chiaratti, M.R., Méo, S.C., Muller, M., Smith, L.C., Meirelles, F.V. & Steinborn, R. (2010). Pronounced segregation of donor mitochondria introduced by bovine ooplasmic transfer to the germline. Biol. Reprod. 82, 563–71.CrossRefGoogle Scholar
Hill, J.R., Winger, Q.A., Long, C.R., Looney, C.R., Thompson, J.A. & Westhusin, M.E. (2000). Developmental rates of male bovine nuclear transfer embryos derived from adult and fetal cells. Biol. Reprod. 62, 1135–40.CrossRefGoogle Scholar
International Embryo Transfer Society (IETS) Manual. 3rd edn. Savoy, IL, USA: IETS.Google Scholar
Knowles, M.K., Guenza, M.G., Capaldi, R.A. & Marcus, A.H. (2002). Cytoskeletal-assisted dynamics of the mitochondrial reticulum in living cells. Proc. Natl. Acad. Sci. USA 23, 14772–7.CrossRefGoogle 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 an endangered species (Bos gaurus) using interspecies nuclear transfer. Cloning 2, 79–90.CrossRefGoogle ScholarPubMed
Lee, E., Bhuiyan, M.M., Watanabe, H., Matsuoka, K., Fujise, Y., Ishikawa, H. & Fukui, Y. (2009). Production of cloned Sei whale (Balaenoptera borealis) embryos by interspecies somatic cell nuclear transfer using enucleated pig oocytes. J. Vet. Sci. 10, 285–92.CrossRefGoogle ScholarPubMed
Levron, J., Willadsen, S., Bertoli, M. & Cohen, J. (1996). The development of mouse zygotes after fusion with synchronous and asynchronous cytoplasm. Hum. Reprod. 11, 1287–92.CrossRefGoogle ScholarPubMed
Li, G.P., Siedel, G.E. & Squires, E.L. (2002). Interspecies cloning using fresh, stored and dead equine and bovine somatic cells as donor nuclei and bovine cytoplasts. Theriogenology 57, 432 (abstr.).Google Scholar
Li, Y., Dai, Y., Du, W., Zhao, C., Wang, L., Wang, H., Liu, Y., Li, R. & Li, N. (2007). In vitro development of yak (Bos grunniens) embryos generated by interspecies nuclear transfer. Anim. Reprod. Sci. 101, 45–59.CrossRefGoogle ScholarPubMed
Loi, P., Ptak, G., Barboni, B., Fulka, J., Cappai, P. & Clinton, M. (2001). Genetic rescue of an endangered mammal by cross-species nuclear transfer using post-mortem somatic cells. Nature Biotech. 19, 962–4.CrossRefGoogle ScholarPubMed
Meirelles, F.V. & Smith, L.C. (1998). Mitochondrial genotype segregation during preimplantation development in mouse heteroplasmic embryos. Genetics 148, 877–83.CrossRefGoogle ScholarPubMed
Nagao, Y., Totsuka, Y., Atomi, Y., Kaneda, H., Lindahl, K.F., Imai, H. & Yonekawa, H. (1998a). Decreased physical performance of congenic mice with mismatch between the nuclear and the mitochondrial genome. Genes Genet. Syst. 73, 21–7.CrossRefGoogle ScholarPubMed
Nagao, Y., Totsuka, Y., Atomi, Y., Yonekawa, H. & Imai, H. (1998b). Effect of different type of mitochondrial DNA on preimplantation embryonic development in the mouse. J. Reprod. Dev. 44, 129–34.CrossRefGoogle Scholar
Nel-Themaat, L., Gómez, M.C., Pope, C.E., Lopez, M., Wirtu, G., Jenkins, J.A., Cole, A., Dresser, B.L., Bondioli, K.R. & Godke, R.A. (2008). Cloned embryos from semen. Part 2: intergeneric nuclear transfer of semen-derived eland (Taurotragus oryx) epithelial cells into bovine oocytes. Cloning Stem Cells 10, 161–72.CrossRefGoogle ScholarPubMed
Pikó, L. & Taylor, K.D. (1987). Amounts of mitochondrial DNA and abundance of some mitochondrial gene transcripts in early mouse embryos. Dev. Biol. 123, 364–74.CrossRefGoogle ScholarPubMed
Reggio, B.C., James, A.N., Green, H.L., Gavin, W.G., Behboodi, E., Echelard, Y. & Godke, R.A. (2001). Cloned transgenic offspring resulting from somatic cell nuclear transfer in the goat: oocytes derived from both follicle-stimulating hormone-stimulated and nonstimulated abattoir-derived ovaries. Biol. Reprod. 65, 1528–33.CrossRefGoogle ScholarPubMed
Rosenkrans, C.F., Zeng, G.Q., McNamara, G.T., Schoff, P.K. & First, N.L. (1993). Development of bovine embryos in vitro is affected by energy substrates. Biol. Reprod. 49, 459–62.CrossRefGoogle ScholarPubMed
Sansinena, M.J., Reggio, B.C., Denniston, R.S. & Godke, R.A. (2002). Nuclear transfer embryos from different equine cell lines as donor karyoplasts using the bovine oocyte as recipient cytoplast. Theriogenology 58, 775–7.Google Scholar
Sansinena, M.J., Taylor, S.A., Taylor, P.J., Denniston, R.S. & Godke, R.A. (2003a). Production of interspecies nuclear transfer embryos using male and female llama (Lama glama) cell lines. Theriogenology 59, 287 (abstr.).Google Scholar
Sansinena, M.J., Taylor, S.A., Taylor, P.J., Denniston, R.S. & Godke, R.A. (2003b). Production of nuclear transfer llama (Lama glama) embryos from in vitro matured llama oocytes. Cloning Stem Cells 5, 191–8.CrossRefGoogle ScholarPubMed
Sansinena, M.J., Hylan, D., Hebert, K., Denniston, R.S. & Godke, R.A. (2005). Banteng (Bos javanicus) embryos and pregnancies produced by interspecies nuclear transfer. Theriogenology 63, 1081–91.CrossRefGoogle ScholarPubMed
Sansinena, M.J., Owiny, D., Denniston, R.S., Salamone, D. & Barry, D. (2007). Initiation of pregnancies in South Africa Riverine rabbit (Bunolagus monticularis) by interspecies nuclear transfer using adipose-derived somatic cells. Reprod. Fert. Dev. 20, 106–7 (abstr.).CrossRefGoogle Scholar
Savage, A.F., Maull, J., Tian, X.C., Taneja, M., Jatz, L., Darre., M. & Yang, X. (2003). Behavioral observations of adolescent Holstein heifers cloned from adult somatic cells. Theriogenology 60, 1097–10.CrossRefGoogle ScholarPubMed
Shiga, K., Fujita, T., Hirose, K., Sasae, Y. & Nagai, T. (1999). Production of calves by transfer of nuclei from cultured somatic cells obtained from Japanese black bulls. Theriogenology 52, 527–35.CrossRefGoogle ScholarPubMed
Song, J., Hua, S., Song, K. & Zhang, Y. (2007). Culture, characteristics and chromosome complement of Siberian tiger fibroblasts for nuclear transfer. In Vitro Cell. Dev. Biol. Anim. 43, 203–9.CrossRefGoogle ScholarPubMed
Song, B.S., Lee, S.H., Kim, S.U., Kim, J.S., Park, J.S., Kim, C.H., Han, Y.M., Lee, K.K., Lee, D.S. & Koo, D.B. (2009). Nucleogenesis and embryonic genome activation are defective in interspecies cloned embryos between bovine ooplasm and rhesus monkey somatic cell. BMC Dev. Biol. 9, 44.CrossRefGoogle Scholar
Tao, Y., Liu, J., Zhang, Y., Zhang, M., Fang, J., Han, W., Zhang, Z., Liu, Y., Ding, J. & Zhang, X. (2009). Fibroblast cell line establishment, cryopreservation and interspecies embryos reconstruction in red panda (Ailurus fulgens). Zygote 17, 117–24.CrossRefGoogle ScholarPubMed
Tecirlioglu, R.T., Guo, J. & Trounson, A.O. (2006). Interspecies somatic cell nuclear transfer and preliminary data for horse-cow/mouse iSCNT. Stem Cell Review 2, 277–87.CrossRefGoogle ScholarPubMed
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
Ty, L.V., Hanh, N.V., Uoc, N.T., Duc, N.H., Thanh, N.T., Bui, L.C., Huu, Q.X. & Nguyen, B.X. (2003). Preliminary results of cell cryobanking and embryo production of black bear (Ursus thibetanus) by interspecies somatic cell nuclear transfer. Theriogenology 59, 290 (abstr.).Google Scholar
Wells, D.N., Misica, P.M. & Tervit, H.R. (1999). Production of cloned claves following nuclear transfer with cultured adult mural granulosa cells. Biol. Reprod. 60, 996–1005.CrossRefGoogle Scholar
White, K.L., Bunch, T.D., Mitalipov, S. & Reed, W.A. (1999). Establishment of pregnancy after the transfer of nuclear transfer embryos produced from the fusion of argali (Ovis ammon) nuclei into domestic sheep (Ovis aries) enucleated oocytes. Cloning 1, 47–54.CrossRefGoogle ScholarPubMed
Williams, J.B., Shin, T., Liu, L., Flores-Foxworth, G., Romano, J., Blue-McClendon, A., Kraemer, D. & Westhusin, M.E. (2006). Cloning of exotic/endangered species: desert Bighorn sheep. Methods Mol. Biol. 348, 169–82.CrossRefGoogle ScholarPubMed
Wilmut, I. & Campbell, K.H. (1998). Embryonic and somatic cell cloning. Reprod. Fertil. Dev. 10, 639–43.CrossRefGoogle ScholarPubMed
Yoon, J.T., Choi, E.J., Han, K.Y., Shim, H. & Roh, S. (2001). In vitro development of embryos produced by nuclear transfer of porcine somatic cell nuclei into bovine oocytes using three different culture systems. Theriogenology 55, 298 (abstr.).Google Scholar