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Effect of donor cell age on development of ovine nuclear transfer embryos in vitro

Published online by Cambridge University Press:  25 June 2010

B. Heidari
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran. Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Canada.
A. Shirazi*
Affiliation:
Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, 52 Campus Drive, Saskatoon SK S7N 5B4, Canada. Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran.
P. Tajic
Affiliation:
Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran.
E. Ahmadi
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran.
H. Nazari
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran.
N. Shams-Esfandabadi
Affiliation:
Research Institute of Animal Embryo Technology, Shahrekord University, Shahrekord, Iran.
H. Ghasemzadeh-Nava
Affiliation:
Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran.
*
All correspondence to: Abolfazl Shirazi. Department of Veterinary Biomedical Sciences, Western College of Veterinary Medicine, University of Saskatchewan, 52 Campus Drive, Saskatoon SK S7N 5B4, Canada. Tel: +1 306 966 4317. Fax: +1 306 966 7376. e-mail: shiraziabbas@ yahoo.com; a.shirazi@avicenna.ac.ir

Summary

The effects of the age of cell donor animal on in vitro development of ovine nuclear transfer (NT) embryos were investigated. Somatic donor cells were obtained from two different sources: (1) adult cells (adult fibroblast cells; AFC and adult cumulus cells; ACC); and (2) fetal fibroblasts (40-day-old; FFC-40 and 65-day-old; FFC-65). The fibroblast cell lines were used for NT procedures within 4–13 subpassages. While the cumulus cells were used as non-cultured (fresh) cells. The in vitro matured abattoir-derived oocytes were considered as recipients. No differences in the rates of fusion (75.7, 77.7, 76.3 and 86.7%) and cleavage (80.1, 84.3, 77.8 and 74%) were detected among couplets reconstructed with FFC-40, FFC-65, AFC and ACC, respectively. Blastocyst formation rate of those oocytes reconstructed with FFC-40 was higher (18%; p < 0.001) than those reconstructed with FFC-65 (13%) and AFC (10.9) and comparable with those reconstructed with ACC (17.5%). When the effect of passage number was analysed within groups (FFC-40, FFC-65 and AFC) there were no significant differences in fusion, cleavage and blastocyst rates between reconstructed oocytes. The present study demonstrates that the fetal and adult fibroblasts as well as fresh cumulus cells are comparable in their ability to attain cell fusion and embryonic cleavage. Moreover, the blastocyst formation rate is influenced by the age of the donor animal and the fresh cumulus cells have similar remodelling potential to that of fetal fibroblasts in term of blastocyst formation rate.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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References

Baguisi, A., Behboodi, E., Melican, D.T., Pollock, J.S., Desrempes, 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.CrossRefGoogle ScholarPubMed
Campbell, K.H.S., McWhir, J., Ritchie, W.A. & Wilmut, I. (1996), Sheep cloned by nuclear transfer from a cultured cell line. Nature 380, 6466.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Enright, B.P., Jeong, B.S., Yang, X. & Tian, X.C. (2003). Epigenetic characteristics of bovine donor cells for nuclear transfer levels of histone acetylation. Biol. Reprod. 69, 1525–30.CrossRefGoogle ScholarPubMed
Forsberg, E.J., Strelchenko, N.S., Augenstein, M.L., Betthauser, J.M., Childs, L.A., Eilertsen, K.J., Enos, J.M., Forsythe, T.M., Golueke, P.J., Koppang, R.W., Lange, G., Lesmeister, T.L., Mallon, K.S., Mell, G.D., Misica, P.M., Pace, M.M., Pfister-Genskow, M., Voelker, G.R., Watt, S.R. & Bishop, M.D. (2002). Production of cloned cattle from in vitro systems. Biol. Reprod. 67, 327–33.CrossRefGoogle ScholarPubMed
Freshney, I.R. (1994). Culture of Animal Cells, 3rd edn, pp. 310348. New York: Wiley-Liss, Inc.Google Scholar
Hill, J.R., Winger, Q.A., Long, C.R., Looney, C.R., Thompson, J.A. & Westhusin, M.E. (2000). Development rates of male bovine nuclear transfer embryos derived from adult and fetal cells. Biol. Reprod. 62, 1135–40.CrossRefGoogle ScholarPubMed
Kasinathan, P., Knott, J.G., Moreira, P.N., Burnside, A.S., Jerry, D.J. & Robl, J.M. (2001). Effect of fibroblast donor cell age and cell cycle on development of bovine nuclear transfer embryos in vitro. Biol. Reprod. 64, 1487–93.CrossRefGoogle ScholarPubMed
Kato, Y., Tetsuya, T., Sotomaru, Y., Kurokawa, K., Kato, J., Doguchi, H., Yasue, H. & Tsunoda, Y. (1998). Eight calves cloned from somatic cells of a single adult. Science 282, 2095–8.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Keefer, C.L., Baldassarre, H., Keyston, R., Wang, B., Bhatia, B., Bilodeau, A.S., Zhou, J.F., Leduc, M., Downey, B.R., Lazaris, A. & Karatzas, C.N. (2001). Generation of dwarf goat (Capra hircus) clones following nuclear transfer with transfected and nontransfected fetal fibroblasts and in vitro-matured oocytes. Biol. Reprod. 64, 849–56.CrossRefGoogle ScholarPubMed
Kubota, C., Yamakuchi, H., Todoroki, J., Mizoshita, K., Tabara, N., Barber, M. & Yang, X. (2000). Six cloned calves produced from adult fibroblast cells after long-term culture. Proc. Natl. Acad. Sci. USA 97, 990–5.CrossRefGoogle ScholarPubMed
Kuhholzer, B., Tao, T., Machaty, Z. & Hawley, R.J. (2000). Greenstein JL, Day BN. Production of transgenic porcine blastocysts by nuclear transfer. Mol. Reprod. Dev. 56, 145–8.3.0.CO;2-8>CrossRefGoogle ScholarPubMed
Lai, L., Tao, T., Machaty, Z., Kuhholzer, B., Sun, Q.Y., Park, K.W., Day, B.N. & Prather, R.S. (2001). Feasibility of producing porcine nuclear transfer embryos by using G2/M-stage fetal fibroblasts as donors. Biol. Reprod. 65, 1558–64.CrossRefGoogle ScholarPubMed
Lanza, R.P., Cibelli, J.B., Blackwell, C., Cristofalo, V., Francis, M.K., Baerlocher, G.M., Mak, J., Schertzer, M., Chavez, E.A., Sawyer, N., Lansdorp, P.M. & West, M.D. (2000). Extension of cell life-span and telomere length in animals cloned from senescent somatic cells. Science 288, 665–9.CrossRefGoogle ScholarPubMed
Ledda, S., Bogliolo, L., Leoni, G., Calvia, P. & Naitana, S. (1996). Influence of vasoactive intestinal peptide (VIP), atrial natriuretic peptide (ANP) and insulin-like growth factor-I (IGF-I) on in vitro maturation of prepubertal and adult sheep oocytes. Zygote 4, 343–8.CrossRefGoogle ScholarPubMed
Ledda, S., Bogliolo, L., Calvia, P., Leoni, G. & Naitana, S. (1997). Meiotic progression and developmental competence of oocytes collected from juvenile and adult ewes. J. Reprod. Fert. 109, 73–8.CrossRefGoogle ScholarPubMed
Lee, J.W., Wu, S.C., Tian, X.C., Barber, M., Hoagland, T., Riesen, J., Lee, K.H., Tu, C.F., Cheng, W.T.K. & Yang, X. (2003). Production of cloned pigs by whole-cell intracytoplasmic microinjection. Biol. Reprod. 69, 9951001.CrossRefGoogle ScholarPubMed
Majerus, V., Lequarrè, A.S., Ferguson, E.M., Kaidi, S., Massip, A., Dessy, F. & Donnay, I. (2000). Characterization of embryos derived from calf oocytes: kinetics of cleavage, cell allocation to inner cell mass and trophectoderm and lipid metabolism. Mol. Reprod. Dev. 57, 346–52.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Ng, S.C., Chen, N., Yip, W.Y., Liow, S.L., Tong, G.Q., Martelli, B., Tan, L.G. & Martelli, P. (2004). The first cell cycle after transfer of somatic cell nuclei in a non-human primate. Development 131, 2475–84.CrossRefGoogle Scholar
O'Brien, J.K., Dwarte, D., Ryan, J.P., Maxwell, W.M.C. & Evans, G. (1996). Developmental capacity, energy metabolism and ultrastructure of mature oocytes from prepubertal and adult sheep. Reprod. Fert. Dev. 8, 1029–37.CrossRefGoogle ScholarPubMed
Park, K.W., Lai, L., Cheong, H.T., Im, G.S., Sun, Q.Y., Wu, G., Day, B.N. & Prather, R.S. (2001). Developmental potential of porcine nuclear transfer embryos derived from transgenic fetal fibroblasts infected with the gene for the green fluorescent protein: comparison of different fusion/activation conditions. Biol. Reprod. 65, 1681–5.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
Renard, J.P. (1999). Chromatin remodeling and potential for full term development of cloned embryos. In: Proceedings of Transgenic Animal Research Conference, p. 15. Aug, Tahoe City, CA, USA.Google Scholar
Rideout, W.M., Eggan, K. & Jaenisch, R. (2001). Nuclear cloning and epigenetic reprogramming of the genome. Science 293, 1093–8.CrossRefGoogle ScholarPubMed
Roh, S., Shim, H., Hwang, W. & Yoon, J. (2000). In vitro development of green fluorescent protein (GFP) transgenic bovine embryos after nuclear transfer using different cell cycles and passages of fetal fibroblasts. Reprod. Fertil. Dev. 12, 16.CrossRefGoogle ScholarPubMed
Schnieke, A.E., Kind, A.J., Ritchie, W.A., Mycock, K., Scott, A.R., Ritchie, M., Wilmut, I., Colman, A. & Campbell, K.H. (1997). Human factor IX transgenic sheep production by transfer of nuclei from transfected fetal fibroblasts. Science 278, 2130–3.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
Tian, X.C., Kubota, C., Enright, B. & Yang, X. (2003). Cloning animals by somatic cell nuclear transfer–biological factors. Reprod. Biol. Endocrinol. 13, 98.CrossRefGoogle Scholar
Vignon, X., Lebourhis, D., Chesne, P., Marchal, J., Heyman, Y. & Renard, J.P. (1999). Development of bovine nuclear transfer embryos reconstituted with quiescent and proliferative skin fibroblasts. Theriogenology 51, 216.CrossRefGoogle Scholar
Wakayama, T., Rodriguez, I., Perry, A.C.F., Yanagimachi, R. & Mombaerts, P. (1999). Mice cloned from embryonic stem cells. Proc. Natl. Acad. Sci. USA 96, 14984–9.CrossRefGoogle ScholarPubMed
Wakayama, T. & Yanagimachi, R. (2001). Mouse cloning with nucleus donor cells of different age and type. Mol. Reprod. Dev. 58, 376–83.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Walker, S.K., Hartwich, K.M. & Seamark, R.F. (1996). The production of unusually large offspring following embryo manipulation: concepts and challenges. Theriogenology 45, 111–20.CrossRefGoogle Scholar
Wells, D.N., Misica, P.M., McMillan, W.H. & Tervit, H.R. (1998). Production of cloned bovine fetuses following nuclear transfer using cells from a fetal fibroblast cell line. Theriogenology 49, 330.CrossRefGoogle Scholar
Wells, D.N., Misica, P.M. & Tervit, H.R. (1999). Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biol, Reprod. 60, 9961005.CrossRefGoogle ScholarPubMed
Westhusin, M.E., Long, C.R., Shin, T., Hill, J.R., Looney, C.R., Pryor, J.H. & Piedrahita, J.A. (2001). Cloning to reproduce desired genotypes. Theriogenology 55, 3549.CrossRefGoogle ScholarPubMed
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, K.L. & Campbell, K.H.S. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–3.CrossRefGoogle ScholarPubMed