Skip to main content Accessibility help
×
Home

In vitro development of nuclear transfer embryos derived from porcine embryonic germ cells and their descendent neural precursor cells

  • Susa Shin (a1), Kwang Sung Ahn (a1), Seong-Jun Choi (a2), Soon Young Heo (a3) and Hosup Shim (a4) (a5)...

Summary

Undifferentiated stem cells may support a greater development of cloned embryos compared with differentiated cell types due to their ease of reprogramming during the nuclear transfer (NT) process. Hence, stem cells may be more suitable as nuclear donor cells for NT procedures than are somatic cells. Embryonic germ (EG) cells are undifferentiated stem cells that are isolated from cultured primordial germ cells (PGC) and can differentiate into several cell types. In this study, the in vitro development of NT embryos using porcine EG cells and their derivative neural precursor (NP) cells was investigated, thus eliminating any variation in genetic differences. The rates of fusion did not differ between NT embryos from EG and NP cells; however, the rate of cleavage in NT embryos derived from EG cells was significantly higher (p < 0.05) than that from NP cells (141/247 [57.1%] vs. 105/228 [46.1%]). Similarly, the rate of blastocyst development was significantly higher (P < 0.05) in NT using EG cells than the rate using NP cells (43/247 [17.4%] vs. 18/228 [7.9%]). The results obtained from the present study in pigs demonstrate a reduced capability for nuclear donor cells to be reprogrammed following the differentiation of porcine EG cells. Undifferentiated EG cells may be more amenable to reprogramming after reconstruction compared with differentiated somatic cells.

Copyright

Corresponding author

All correspondence to: Hosup Shim. Department of Nanobiomedical Science and WCU Center for Nanobiomedical Science, Dankook University, San 29 Anseo-dong, Dongnam-gu, Cheonan, Chungnam 330–714, Korea. Tel: +82 41 550 3865. Fax: +82 41 550 1149. e-mail: shim@dku.edu

References

Hide All
Ahn, K.S., Won, J.Y., Heo, S.Y., Kang, J.H., Yang, H.S. & Shim, H. (2007). Transgenesis and nuclear transfer using porcine embryonic germ cells. Cloning Stem Cells 9, 461–8.
Baguisi, A., Behboodi, E., Melican, D.T., Pollock, J.S., Destrempes, M.M., Cammuso, C., Williams, J.L., Nims, S.D., Porter, C.A., Midura, P., Palacios, M.J., Ayres, S.L., Denniston, R.S., Hayes, M.L., Ziomek, C.A., Meade, H.M., Godke, R.A., Gavin, W.G., Overstrom, E.W. & Echelard, Y. (1999). Production of goats by somatic cell nuclear transfer. Nat. Biotechnol. 17, 456–61.
Bosch, P., Pratt, S.L. & Stice, S.L. (2006). Isolation, characterization, gene modification, and nuclear reprogramming of porcine mesenchymal stem cells. Biol. Reprod. 74, 4657.
Brevini, T.A., Antonini, S., Cillo, F., Crestan, M. & Gandolfi, F. (2007). Porcine embryonic stem cells: Facts, challenges and hopes. Theriogenology 68 Suppl. 1, S20613.
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 nonquiescent fetal fibroblasts. Science 280, 1256–8.
Colleoni, S., Donofrio, G., Lagutina, I., Duchi, R., Galli, C. & Lazzari, G. (2005). Establishment, differentiation, electroporation, viral transduction, and nuclear transfer of bovine and porcine mesenchymal stem cells. Cloning Stem Cells 7, 154–66.
Faast, R., Harrison, S.J., Beebe, L.F., McIlfatrick, S.M., Ashman, R.J. & Nottle, M.B. (2006). Use of adult mesenchymal stem cells isolated from bone marrow and blood for somatic cell nuclear transfer in pigs. Cloning Stem Cells 8, 166–73.
Galli, C., Duchi, R., Moor, R.M. & Lazzari, G. (1999). Mammalian leukocytes contain all the genetic information necessary for the development of a new individual. Cloning 1, 161–70.
Gottlieb, D.I. (2002). Large-scale sources of neural stem cells. Annu. Rev. Neurosci. 25, 381407.
Guan, K., Chang, H., Rolletschek, A. & Wobus, A.M. (2001). Embryonic stem cell-derived neurogenesis. Retinoic acid induction and lineage selection of neuronal cells. Cell Tissue Res. 305, 171–6.
Gurdon, J.B. (1962). The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J. Embryol. Exp. Morphol. 10, 622–40.
Han, Y.M., Kang, Y.K., Koo, D.B. & Lee, K.K. (2003). Nuclear reprogramming of cloned embryos produced in vitro. Theriogenology 59, 3344.
Hochedlinger, K. & Jaenisch, R. (2002). Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 415, 1035–8.
Jaenisch, R., Hochedlinger, K., Blelloch, R., Yamada, Y., Baldwin, K. & Eggan, K. (2004). Nuclear cloning, epigenetic reprogramming, and cellular differentiation. Cold Spring Harb. Symp. Quant. Biol. 69, 1927.
Jin, H.F., Kumar, B.M., Kim, J.G., Song, H.J., Jeong, Y.J., Cho, S.K., Balasubramanian, S., Choe, S.Y. & Rho, G.J. (2007). Enhanced development of porcine embryos cloned from bone marrow mesenchymal stem cells. Int. J. Dev. Biol. 51, 8590.
Kato, Y., Tani, T. & Tsunoda, Y. (2000). Cloning of calves from various somatic cell types of male and female adult, newborn and fetal cows. J. Reprod. Fertil. 120, 231–7.
Kues, W.A. & Niemann, H. (2004). The contribution of farm animals to human health. Trends Biotechnol. 22, 286–94.
Lendahl, U., Zimmerman, L.B. & McKay, R.D. (1990). CNS stem cells express a new class of intermediate filament protein. Cell. 60, 585–95.
Matsui, Y., Zsebo, K. & Hogan, B.L. (1992). Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70, 841–7.
Miyashita, N., Shiga, K., Yonai, M., Kaneyama, K., Kobayashi, S., Kojima, T., Goto, Y., Kishi, M., Aso, H., Suzuki, T., Sakaguchi, M. & Nagai, T. (2002). Remarkable differences in telomere lengths among cloned cattle derived from different cell types. Biol. Reprod. 66, 1649–55.
Ogura, A., Inoue, K., Ogonuki, N., Noguchi, A., Takano, K., Nagano, R., Suzuki, O., Lee, J., Ishino, F. & Matsuda, J. (2000). Production of male cloned mice from fresh, cultured, and cryopreserved immature Sertoli cells. Biol. Reprod. 62, 1579–84.
Onishi, A., Takeda, K., Komatsu, M., Akita, T. & Kojima, T. (1994). Production of chimeric pigs and the analysis of chimerism using mitochondrial deoxyribonucleic acid as a cell marker. Biol. Reprod. 51, 1069–75.
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.S. (2000). Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407, 8690.
Resnick, J.L., Bixter, L.S., Cheng, L. & Donovan, P.J. (1992). Long-term proliferation of mouse primordial germ cells in culture. Nature 359, 550–1.
Rideout, W.M. 3rd, Wakayama, T., Wutz, A., Eggan, K., Jackson-Grusby, L., Dausman, J., Yanagimachi, R. & Jaenisch, R. (2000). Generation of mice from wild-type and targeted ES cells by nuclear cloning. Nat. Genet. 24, 109–10.
Schwartz, P.H., Nethercott, H., Kirov, I.I., Ziaeian, B., Young, M.J. & Klassen, H. (2005). Expression of neurodevelopmental markers by cultured porcine neural precursor cells. Stem Cells 23, 1286–94.
Shim, H., Gutierrez-Adan, A., Chen, L.R., BonDurant, R.H., Behboodi, E. & Anderson, G.B. (1997). Isolation of pluripotent stem cells from cultured porcine primordial germ cells. Biol. Reprod. 57, 1089–95.
Wakayama, T., Rodriguez, I., Perry, A.C., Yanagimachi, R. & Mombaerts, P. (1999). Mice cloned from embryonic stem cells. Proc. Natl. Acad. Sci. USA 96, 14984–9.
Westphal, H. (2005). Restoring stemness. Differentiation 73, 447–51.
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J. & Campbell, K.H.S. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–3.
Yang, X., Smith, S.L., Tian, X.C., Lewin, H.A., Renard, J.P. & Wakayama, T. (2007) Nuclear reprogramming of cloned embryos and its implications for therapeutic cloning. Nat. Genet. 39, 295302.
Ying, Q.L., Stavridis, M., Griffiths, D., Li, M. & Smith, A. (2003). Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21, 183–6.
Zhang, S.C., Wernig, M., Duncan, I.D., Brustle, O. & Thomson, J.A. (2001). In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19, 1129–33.
Zhu, H., Craig, J.A., Dyce, P.W., Sunnen, N. & Li, J. (2004). Embryos derived from porcine skin-derived stem cells exhibit enhanced preimplantation development. Biol. Reprod. 71, 1890–7.

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed