Hostname: page-component-78c5997874-mlc7c Total loading time: 0 Render date: 2024-11-16T15:10:45.411Z Has data issue: false hasContentIssue false
  • English
  • Français

Parthenogenetic activation and somatic cell nuclear transfer of porcine oocytes activated by an electric pulse and AZD5438 treatment

Published online by Cambridge University Press:  17 July 2017

Xiao-Chen Li ,
Qing Guo ,
Hai-Ying Zhu ,
Long Jin ,
Yu-Chen Zhang ,
Guang-Lei Zhang ,
Xiao-Xu Xing ,
Mei-Fu Xuan ,
Qi-Rong Luo  and
Zhao-Bo Luo
...Show all authors
Xiao-Chen Li
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Qing Guo
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Hai-Ying Zhu
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Long Jin
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Yu-Chen Zhang
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Guang-Lei Zhang
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Xiao-Xu Xing
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Mei-Fu Xuan
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Qi-Rong Luo
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Zhao-Bo Luo
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Jun-Xia Wang
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Cheng-Du Cui
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Wen-Xue Li
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Zheng-Yun Cui
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Xi-Jun Yin*
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
Jin-Dan Kang*
Affiliation:
Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
*
All correspondence to: Jin-Dan Kang or Xi-Jun Yin. Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China. Tel: +86 0433 2435623. Fax: +86 0433 2435622. E-mail: [email protected] or [email protected]
All correspondence to: Jin-Dan Kang or Xi-Jun Yin. Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China. Tel: +86 0433 2435623. Fax: +86 0433 2435622. E-mail: [email protected] or [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

We examined the in vitro developmental competence of parthenogenetic activation (PA) oocytes activated by an electric pulse (EP) and treated with various concentrations of AZD5438 for 4 h. Treatment with 10 µM AZD5438 for 4 h significantly improved the blastocyst formation rate of PA oocytes in comparison with 0, 20, or 50 µM AZD5438 treatment (46.4% vs. 34.5%, 32.3%, and 24.0%, respectively; P < 0.05). The blastocyst formation rate was higher in the group treated with AZD5438 for 4 h than in the groups treated with AZD5438 for 2 or 6 h (42.8% vs. 38.6% and 37.2%, respectively; P > 0.05). Furthermore, 66.67% of blastocysts derived from these AZD5438-treated PA oocytes had a diploid karyotype. The blastocyst formation rate of PA and somatic cell nuclear transfer (SCNT) embryos was similar between oocytes activated by an EP and treated with 2 mM 6-dimethylaminopurine for 4 h and those activated by an EP and treated with 10 µM AZD5438 for 4 h (11.11% vs. 13.40%, P > 0.05). In addition, the level of maturation-promoting factor (MPF) was significantly decreased in oocytes activated by an EP and treated with 10 µM AZD5438 for 4 h. Finally, the mRNA expression levels of apoptosis-related genes (Bax and Bcl-2) and pluripotency-related genes (Oct4, Nanog, and Sox2) were checked by RT-PCR; however, there were no differences between the AZD5438-treated and non-treated control groups. Our results demonstrate that porcine oocyte activation via an EP in combination with AZD5438 treatment can lead to a high blastocyst formation rate in PA and SCNT experiments.

Keywords

AZD5438Cyclin-dependent kinase inhibitorMPFPASCNT
Type
Research Article
Information
Zygote , Volume 25 , Issue 4 , August 2017 , pp. 453 - 461
Copyright
Copyright © Cambridge University Press 2017 

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.)

Footnotes

3

These authors contributed equally to this study.

References

Arias, M.E., Sánchez, R. & Felmer, R. (2016). Effect of anisomycin, a protein synthesis inhibitor, on the in vitro developmental potential, ploidy and embryo quality of bovine ICSI embryos. Zygote 24, 724–32.CrossRefGoogle ScholarPubMed
Bos-Mikich, A., Bressan, F.F., Ruggeri, R.R., Watanabe, Y. & Meirelles, F.V. (2016). Parthenogenesis and human assisted reproduction. Stem Cells Int. 2016, 1970843.Google Scholar
Byth, K.F., Thomas, A., Hughes, G., Forder, C., McGregor, A., Geh, C., Oakes, S., Green, C., Walker, M., Newcombe, N., Green, S., Growcott, J., Barker, A. & Wilkinson, R.W. (2009). AZD5438, a potent oral inhibitor of cyclin-dependent kinases 1, 2, and 9, leads to pharmacodynamic changes and potent antitumor effects in human tumour xenografts. Mol. Cancer Ther. 8, 1856–66.CrossRefGoogle Scholar
Camidge, D.R., Pemberton, M., Growcott, J., Amakye, D., Wilson, D., Swaisland, H., Forder, C., Wilkinson, R., Byth, K. & Hughes, A. (2007a). Phase I pharmacodynamic study of the effects of the cyclin-dependent kinase-inhibitor AZD5438 on cell cycle markers within the buccal mucosa, plucked scalp hairs and peripheral blood mononucleocytes of healthy male volunteers. Cancer Chemother. Pharmacol. 60, 479–88.CrossRefGoogle ScholarPubMed
Camidge, D.R., Smethurst, D., Growcott, J., Barrass, N.C., Foster, J.R., Febbraro, S., Swaisland, H. & Hughes, A. (2007b). A first-in-man phase I tolerability and pharmacokinetic study of the cyclin-dependent kinase-inhibitor AZD5438 in healthy male volunteers. Cancer Chemother. Pharmacol. 60, 391–8.Google Scholar
Cha, S.K., Kim, N.H., Lee, S.M., Baik, C.S., Lee, H.T. & Chung, K.S. (1997). Effect of cytochalasin B and cycloheximide on the activation rate, chromosome constituent and in vitro development of porcine oocytes following parthenogenetic stimulation. Reprod. Fertil. Dev. 9, 441–6.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
Diao, Y.F., Naruse, K., Li, X.X., Han, R.X., Kim, D.K., Lin, T. & Jin, D.I. (2013). Effects of 5-aza-2´-deoxyctidine on the development of porcine parthenogenetic and nuclear transfer embryos. Nat. Sci. 5, 31–37.Google Scholar
Dinnyés, A., Hirao, Y. & Nagai, T. (2000). Parthenogenetic activation of porcine oocytes by electric pulse and/or butyrolactone I treatment. Cloning 1, 209–16.Google Scholar
Fukui, Y., Sawai, K., Furudate, M., Sato, N., Iwazumi, Y. & Ohsaki, K. (1992). Parthenogenetic development of bovine oocytes treated with ethanol and cytochalasin B after in vitro maturation. Mol. Reprod. Dev. 33, 357–62.Google Scholar
Hashimoto, N. & Kishimoto, T. (1988). Regulation of meiotic metaphase by a cytoplasmic maturation promoting factor during mouse oocytes maturation. Dev. Biol. 126, 242–52.CrossRefGoogle Scholar
Lee, H.S., Kim, K.H., Kim, E.Y., Lee, S.Y., Ko, J.J. & Lee, K.A. (2016). Obox4-silencing-activated STAT3 and MPF/MAPK signaling accelerate nuclear membrane breakdown in mouse oocytes. Reproduction 151, 369–78.Google Scholar
Lee, J., Park, J.I., Yun, J.I., Lee, Y., Yong, H., Lee, S.T., Park, C.K., Hyun, S.H., Lee, G.S. & Lee, E. (2015). Rapamycin treatment during in vitro maturation of oocytes improves embryonic development after parthenogenesis and somatic cell nuclear transfer in pigs. J. Vet. Sci. 16, 373–80.Google Scholar
Lee, J.W., Tian, X.C. & Yang, X. (2004). Optimization of parthenogenetic activation protocol in porcine. Mol. Reprod. Dev. 68, 51–7.CrossRefGoogle ScholarPubMed
Li, S., Kang, J.D., Jin, J.X., Hong, Y., Zhu, H.Y., Jin, L., Gao, Q.S., Yan, C.G., Cui, C.D., Li, W.X. & Yin, X.J. (2014). Effect of demecolcine-assisted enucleation on the MPF level and cyclin B1 distribution in porcine oocytes. PLoS One 9, e91483.CrossRefGoogle ScholarPubMed
Liang, S., Zhao, M.H., Choi, J.W., Kim, N.H. & Cui, X.S. (2015). Scriptaid treatment decreases DNA methyltransferase 1 expression by induction of micriRNA-125 expression in porcine somatic cell nuclear transfer embryos. PLoS One 10, e0134567.Google Scholar
Liu, L., Ju, J.C. & Yang, X. (1998). Parthenogenetic development and protein patterns of newly matured bovine oocytes following chemical activation. Mol. Reprod. Dev. 49, 298–307.3.0.CO;2-T>CrossRefGoogle Scholar
Masui, Y. (1991). The role of cytostatic factor (CSF) in the control of oocyte cell cycle – a summary of 20 years study. Dev. Growth Differ. 33, 543–51.CrossRefGoogle Scholar
Masui, Y. & Markert, C.L. (1971). Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 177, 129–45.Google Scholar
Mayes, M.A., Stogsdill, P.L. & Prather, R.S. (1995). Parthenogenic activation of pig oocytes by protein kinase inhibition. Biol. Reprod. 53, 270–5.Google Scholar
McGrath, J. & Solter, D. (1984). Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37, 179–83.Google Scholar
Nussbaum, D.J. & Prather, R.S. (1995). Differential effects of protein synthesis inhibitors on porcine oocyte activation. Mol. Reprod. Dev. 41, 70–5.Google Scholar
Presicce, G.A. & Yang, X. (1994). Parthenogenetic development of bovine oocytes matured in vitro for 24 hr and activated by ethanol and cycloheximide. Mol. Reprod. Dev. 38, 380–5.Google Scholar
Raghavan, P., Tumati, V., Yu, L., Chan, N., Tomimatsu, N., Burma, S., Bristow, R.G. & Saha, D. (2012). AZD5438, an inhibitor of Cdk1, 2, and 9, enhances the radiosensitivity of non-small cell lung carcinoma cells. Int. J. Radiat. Oncol. Biol. Phys. 84, e507–14.Google Scholar
Saikhun, J., Kitiyanant, N., Songtaveesin, C., Pavasuthipaisit, K. & Kitiyanant, Y. (2004). Development of swamp buffalo (Bubalus bubalis) embryos after parthenogenetic activation and nuclear transfer using serum fed or starved fetal fibroblasts. Reprod. Nutr. Dev. 44, 65–78.Google Scholar
Sommer, C.A., Stadtfeld, M., Murphy, G.J., Hochedlinger, K., Kotton, D.N. & Mostoslavsky, G. (2009). Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 27, 543–9.Google Scholar
Surani, M.A. & Barton, S.C. (1983). Development of gynogenetic eggs in the mouse: implications for parthenogenetic embryos. Science 222, 1034–6.Google Scholar
Van De Velde, A., Liu, L., Bols, P.E., Ysebaert, M.T. & Yang, X. (1999). Cell allocation and chromosomal complement of parthenogenetic and IVF bovine embryos. Mol. Reprod. Dev. 54, 57–62.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Wang, H.Y., Luo, Y.B., Lin, Z.L., Lee, I.W., Kwon, J., Cui, X.S. & Kim, N.H. (2015). Effect of ATM and HDAC inhibition on etoposide-induced DNA damage in porcine early preimplantation embryos. PLoS One 10, e0142561.CrossRefGoogle ScholarPubMed
Whitworth, K.M., Li, R.F., Spate, L.D., Wax, D.M., Rieke, A., Whyte, J.J., Manandhar, G., Sutovsky, M., Green, J.A., Sutovsky, P. & Prather, R. (2009). Method of oocyte activation affects cloning efficiency in pigs. Mol. Reprod. Dev. 76, 490–500.Google Scholar
Yang, M.Y. & Rajamahendran, R. (2002). Expression of Bcl-2 and BAX proteins in relation to quality of bovine oocytes and embryos produced in vitro . Anim. Reprod. Sci. 70, 159–69.Google Scholar
Yin, X.J., Tani, T., Yonemura, I., Kawakami, M., Miyamoto, K., Hasegawa, R., Kato, Y. & Tsunoda, Y. (2002). Production of cloned pigs from adult somatic cells by chemically assisted removal of maternal chromosomes. Biol. Reprod. 67, 442–6.Google Scholar
Zhang, D.X., Park, W.J., Sun, S.C., Xu, Y.N., Li, Y.H., Cui, X.S. & Kim, N.H. (2011). Regulation of maternal gene expression by MEK/MAPK and MPF signaling in porcine oocytes during in vitro meiotic maturation. J. Reprod. Dev. 57, 49–56.Google Scholar
Zhao, M.H., Kim, N.H. & Cui, X.S. (2016). GlutaMAX prolongs the shelf life of the culture medium for porcine parthenotes. Theriogenology 85, 368–375.Google Scholar