Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-23T08:18:37.771Z Has data issue: false hasContentIssue false

Short-term treatment with 6-DMAP and demecolcine improves developmental competence of electrically or Thi/DTT-activated porcine parthenogenetic embryos

Published online by Cambridge University Press:  23 June 2010

Sol Ji Park
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, 151–742, Korea.
Ok Jae Koo
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, 151–742, Korea.
Dae Kee Kwon
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, 151–742, Korea.
Ma Ninia Limas Gomez
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, 151–742, Korea.
Jung Taek Kang
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, 151–742, Korea.
Mohammad Atikuzzaman
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, 151–742, Korea.
Su Jin Kim
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, 151–742, Korea.
Goo Jang
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul, 151–742, Korea.
Byeong Chun Lee*
Affiliation:
Department of Theriogenology and Biotechnology, College of Veterinary Medicine, Seoul National University, 599 Gwanak-ro, Gwanak-gu, Seoul, 151–742, Korea.
*
All correspondence to: Byeong Chun Lee. Department of Theriogenology and Biotechnology, College of Veterinary Medicine, Seoul National University, 599 Gwanak-ro, Gwanak-gu, Seoul, 151–742, Korea. Tel: +822 880 1269. Fax: +822 873 1269. e-mail: bclee@snu.ac.kr

Summary

Treatment with 6-dimethylaminopurine (6-DMAP) or demecolcine (DE) for several (at least 2) hours after artificial activation is known to improve in vitro development of porcine embryos. However, several reports have also shown that treatments with these chemicals induce apoptosis. The aim of this study was to find out whether short-term treatment with 6-DMAP and DE combined with electrical or thimerosal/dithiothreitol (Thi/DTT) activation had a beneficial effect on development of parthenogenetically activated porcine oocytes. We additionally treated embryos with 6-DMAP (2 mM) and/or DE (0.4 μg/ml) for a short time (40 min) after an electrical pulse (EP) or Thi/DTT. As a result, short-term treatment with 6-DMAP and DE successfully induced development of electrically or Thi/DTT-activated porcine parthenogenetic embryos with no significant difference in cleavage rate, blastocyst formation rate and total cell number compared with long-term treatment. To find optimal activation protocol, cleavage rate, blastocyst formation rate and total cell number were compared between EP and Thi/DTT treatments. Thi/DTT + 6-DMAP + DE showed significantly higher blastocyst formation rate (36.1 ± 3.5%) and total cell number (46.9 ± 1.0) than other groups (EP + 6-DMAP + DE, EP + Thi/DTT + 6-DMAP + DE: 23.3 ± 3.0%, 42.2 ± 1.1 and 17.2 ± 2.7%, 36.7 ± 1.5, respectively). In conclusion, this study demonstrates that short-term treatment with 6-DMAP and DE is as effective as the standard long-term treatment and Thi/DTT + 6-DMAP + DE exerts a synergistic effect.

Type
Research Article
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

Akagi, S., Adachi, N., Matsukawa, K., Kubo, M. & Takahashi, S. (2003). Developmental potential of bovine nuclear transfer embryos and postnatal survival rate of cloned calves produced by two different timings of fusion and activation. Mol. Reprod. Dev. 66, 264–72.CrossRefGoogle ScholarPubMed
Alexander, B., Coppola, G., Di Berardino, D., Rho, G.J., St John, E., Betts, D.H. & King, W.A. (2006). The effect of 6-dimethylaminopurine (6-DMAP) and cycloheximide (CHX) on the development and chromosomal complement of sheep parthenogenetic and nuclear transfer embryos. Mol. Reprod. Dev. 73, 2030.CrossRefGoogle ScholarPubMed
Betthauser, J., Forsberg, E., Augenstein, M., Childs, L., Eilertsen, K., Enos, J., Forsythe, T., Golueke, P., Jurgella, G., Koppang, R., Lesmeister, T., Mallon, K., Mell, G., Misica, P., Pace, M., Pfister-Genskow, M., Strelchenko, N., Voelker, G., Watt, S., Thompson, S. & Bishop, M. (2000). Production of cloned pigs from in vitro systems. Nat. Biotechnol. 18, 1055–9.CrossRefGoogle ScholarPubMed
Campbell, K.H., Fisher, P., Chen, W.C., Choi, I., Kelly, R.D., Lee, J.H. & Xhu, J. (2007). Somatic cell nuclear transfer, past, present and future perspectives. Theriogenology 68 (Suppl. 1), S214–31.CrossRefGoogle ScholarPubMed
Collas, P., Fissore, R., Robl, J.M., Sullivan, E.J. & Barnes, F.L. (1993). Electrically induced calcium elevation, activation, and parthenogenetic development of bovine oocytes. Mol. Reprod. Dev. 34, 212–23.CrossRefGoogle ScholarPubMed
De La Fuente, R. & King, W.A. (1998). Developmental consequences of karyokinesis without cytokinesis during the first mitotic cell cycle of bovine parthenotes. Biol. Reprod. 58, 952–62.CrossRefGoogle ScholarPubMed
De Sousa, P.A., Dobrinsky, J.R., Zhu, J., Archibald, A.L., Ainslie, A., Bosma, W., Bowering, J., Bracken, J., Ferrier, P.M., Fletcher, J., Gasparrini, B., Harkness, L., Johnston, P., Ritchie, M., Ritchie, W.A., Travers, A., Albertini, D., Dinnyes, A., King, T.J. & Wilmut, I. (2002). Somatic cell nuclear transfer in the pig, control of pronuclear formation and integration with improved methods for activation and maintenance of pregnancy. Biol. Reprod. 66, 642–50.CrossRefGoogle ScholarPubMed
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, 3544.CrossRefGoogle ScholarPubMed
Ibanez, E., Albertini, D.F. & Overstrom, E.W. (2003). Demecolcine-induced oocyte enucleation for somatic cell cloning: coordination between cell-cycle egress, kinetics of cortical cytoskeletal interactions, and second polar body extrusion. Biol. Reprod. 68, 1249–58.CrossRefGoogle ScholarPubMed
Im, G.S., Seo, J.S., Hwang, I.S., Kim, D.H., Kim, S.W., Yang, B.C., Yang, B.S., Lai, L. & Prather, R.S. (2006). Development and apoptosis of pre-implantation porcine nuclear transfer embryos activated with different combination of chemicals. Mol. Reprod. Dev. 73, 1094–101.CrossRefGoogle ScholarPubMed
Inoue, K., Noda, S., Ogonuki, N., Miki, H., Inoue, S., Katayama, K., Mekada, K., Miyoshi, H. & Ogura, A. (2007). Differential developmental ability of embryos cloned from tissue-specific stem cells. Stem Cells 25, 1279–85.CrossRefGoogle ScholarPubMed
Jiang, J.Y., Mizuno, S., Mizutani, E., Sasada, H. & Sato, E. (2002). Parthenogenetic activation and subsequent development of rat oocytes in vitro. Mol. Reprod. Dev. 61, 120–5.CrossRefGoogle ScholarPubMed
Katoh, M., Araki, A., Ogura, T. & Valdivia, R.P. (2004). 6-Dimethylaminopurine (6-DMAP), which is used to produce most cloned animals, is mutagenic in Salmonella typhimurium TA1535. Mutat. Res. 560, 199201.CrossRefGoogle ScholarPubMed
Koo, O. J., Park, H. J., Kwon, D.K., Kang, J.T., Jang, G. & Lee, B.C. (2009). Effect of recipient breed on delivery rate of cloned miniature pig. Zygote 17, 203–7.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
Lee, S.H., Kim, D.Y., Nam, D.H., Hyun, S.H., Lee, G.S., Kim, H.S., Lee, C.K., Kang, S.K., Lee, B.C. & Hwang, W.S. (2004). Role of messenger RNA expression of platelet activating factor and its receptor in porcine in vitro-fertilized and cloned embryo development. Biol. Reprod. 71, 919–25.CrossRefGoogle ScholarPubMed
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
Loi, P., Ledda, S., Fulka, J. Jr., Cappai, P. & Moor, R.M. (1998). Development of parthenogenetic and cloned ovine embryos: effect of activation protocols. Biol. Reprod. 58, 1177–87.CrossRefGoogle ScholarPubMed
Machaty, Z., Wang, W.H., Day, B.N. & Prather, R.S. (1997). Complete activation of porcine oocytes induced by the sulfhydryl reagent, thimerosal. Biol. Reprod. 57, 1123–7.CrossRefGoogle ScholarPubMed
Meo, S.C., Yamazaki, W., Ferreira, C.R., Perecin, F., Saraiva, N.Z., Leal, C.L. & Garcia, J.M. (2007). Parthenogenetic activation of bovine oocytes using single and combined strontium, ionomycin and 6-dimethylaminopurine treatments. Zygote 15, 295306.CrossRefGoogle ScholarPubMed
Miyazaki, S., Shirakawa, H., Nakada, K., Honda, Y., Yuzaki, M., Nakade, S. & Mikoshiba, K. (1992). Antibody to the inositol trisphosphate receptor blocks thimerosal-enhanced Ca2+-induced Ca2+ release and Ca2+ oscillations in hamster eggs. FEBS Lett. 309, 180–4.CrossRefGoogle Scholar
Nanassy, L., Lee, K., Javor, A. & Machaty, Z. (2007). Changes in MPF and MAPK activities in porcine oocytes activated by different methods. Theriogenology. 68, 146–52.CrossRefGoogle ScholarPubMed
Onishi, A., Iwamoto, M., Akita, T., Mikawa, S., Takeda, K., Awata, T., Hanada, H. & Perry, A.C. (2000). Pig cloning by microinjection of fetal fibroblast nuclei. Science. 289, 1188–90.CrossRefGoogle ScholarPubMed
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, 8690.CrossRefGoogle ScholarPubMed
Russell, D.F., Ibanez, E., Albertini, D.F. & Overstrom, E.W. (2005). Activated bovine cytoplasts prepared by demecolcine-induced enucleation support development of nuclear transfer embryos in vitro. Mol. Reprod. Dev. 72, 161–70.CrossRefGoogle ScholarPubMed
Saraiva, N.Z., Perecin, F., Meo, S.C., Ferreira, C.R., Tetzner, T.A. & Garcia, J.M. (2009). Demecolcine effects on microtubule kinetics and on chemically assisted enucleation of bovine oocytes. Cloning Stem Cells 11, 141–52.CrossRefGoogle ScholarPubMed
Solter, D. (2000). Mammalian cloning: advances and limitations. Nat. Rev. Genet. 1, 199207.CrossRefGoogle ScholarPubMed
Sugimura, S., Kawahara, M., Wakai, T., Yamanaka, K., Sasada, H. & Sato, E. (2008). Effect of cytochalasins B and D on the developmental competence of somatic cell nuclear transfer embryos in miniature pigs. Zygote. 16, 153–9.CrossRefGoogle Scholar
Swann, K. (1992). Different triggers for calcium oscillations in mouse eggs involve a ryanodine-sensitive calcium store. Biochem. J. 287 (Pt 1), 7984.CrossRefGoogle ScholarPubMed
Swann, K. & Ozil, J.P. (1994). Dynamics of the calcium signal that triggers mammalian egg activation. Int. Rev. Cytol. 152, 183222.CrossRefGoogle ScholarPubMed
Szollosi, M.S., Kubiak, J.Z., Debey, P., de Pennart, H., Szollosi, D. & Maro, B. (1993). Inhibition of protein kinases by 6-dimethylaminopurine accelerates the transition to interphase in activated mouse oocytes. J. Cell. Sci. 104 (Pt 3), 861–72.CrossRefGoogle ScholarPubMed
Tian, X.C., Kubota, C., Enright, B. & Yang, X. (2003). Cloning animals by somatic cell nuclear transfer—biological factors. Reprod. Biol. Endocrinol. 1, 98.CrossRefGoogle ScholarPubMed
Tian, J.H., Wu, Z.H., Liu, L., Cai, Y., Zeng, S.M., Zhu, S.E., Liu, G.S., Li, Y. & Wu, C.X. (2006). Effects of oocyte activation and sperm preparation on the development of porcine embryos derived from in vitro-matured oocytes and intracytoplasmic sperm injection. Theriogenology 66, 439–48.CrossRefGoogle ScholarPubMed
Varga, E., Pataki, R., Lorincz, Z., Koltai, J. & Papp, A.B. (2008). Parthenogenetic development of in vitro matured porcine oocytes treated with chemical agents. Anim. Reprod. Sci. 105, 226–33.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
Wakayama, T., Perry, A.C., Zuccotti, M., Johnson, K.R. & Yanagimachi, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394, 369–74.CrossRefGoogle ScholarPubMed
Wang, W.H., Abeydeera, L.R., Prather, R.S. & Day, B.N. (1998). Functional analysis of activation of porcine oocytes by spermatozoa, calcium ionophore, and electrical pulse. Mol. Reprod. Dev. 51, 346–53.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Yang, X.Y., Zhao, J.G., Li, H.W., Li, H., Liu, H.F., Huang, S.Z. & Zeng, Y.T. (2005). Improving in vitro development of cloned bovine embryos with hybrid (Holstein-Chinese Yellow) recipient oocytes recovered by ovum pick up. Theriogenology 64, 1263–72.CrossRefGoogle ScholarPubMed