The cyclin-dependent kinase inhibitor, JNJ-7706621, improves in vitro developmental competence of porcine parthenogenetic activation and somatic cell nuclear transfer embryos
Qing Guo A , Long Jin A , Hai-Ying Zhu A , Xiao-Xu Xing A , Mei-Fu Xuan A , Qi-Rong Luo A , Guang-Lei Zhang A , Zhao-Bo Luo A , Jun-Xia Wang A , Xi-Jun Yin A B and Jin-Dan Kang A BA Jilin Provincial Key Laboratory of Transgenic Animal and Embryo Engineering, Yanbian University, Yanji, Jilin, 133002, China.
B Corresponding authors. Emails: yinxj33@msn.com; kangjindan@hotmail.com
Reproduction, Fertility and Development 30(7) 1002-1010 https://doi.org/10.1071/RD17194
Submitted: 22 May 2017 Accepted: 18 November 2017 Published: 5 January 2018
Abstract
In this study we examined the effects of JNJ-7706621, a cyclin-dependent kinase inhibitor, on the in vitro growth of pig embryos that had been produced either by parthenogenetic activation (PA) or somatic cell nuclear transfer (SCNT). A significantly higher percentage of PA embryos reached the blastocyst stage by Day 7 after exposure to 10 µM JNJ-7706621 for 4 h compared with embryos exposed to 5 µg mL−1 cytochalasin B for 4 h (P < 0.05). Similarly, the rate of Tyr15 phosphorylation of the complex of cyclin and p34cdc2 (CDK1) was significantly elevated in the JNJ-7706621-treated embryos compared with embryos exposed to cytochalasin B or non-treated controls (P < 0.05). In contrast, Thr161 phosphorylation of CDK1 was significantly lower in the JNJ-7706621-treated group compared with the cytochalasin B-treated as well as the non-treated group (P < 0.05). Similarly, the level of M-phase-promoting factor (MPF) in embryos was significantly lower in the JNJ-7706621-treated group compared with the cytochalasin B-treated and non-treated groups (P < 0.05). In addition, more SCNT embryos reached the blastocyst stage after treatment with JNJ-7706621 than following exposure to cytochalasin B (P < 0.05). In conclusion, these results reveal that exposure to 10 µM JNJ-7706621 for 4 h improves early development of PA and SCNT porcine embryos by suppressing the activity of CDK1 and a concomitant reduction in the level of MPF.
Additional keywords: blastocyst, CDK1, cytochalasin B, embryos, M-phase-promoting factor.
References
Barros, J., Grenho, L., Fontenente, S., Manuel, C. M., Nunes, O. C., Melo, L. F., Monteiro, F. J., and Ferraz, M. P. (2017). Staphylococcus aureus and Escherichia coli dual-species biofilms on nanohydroxyapatite loaded with CHX or ZnO nanoparticles. J. Biomed. Mater. Res. A 105, 491–497.| Staphylococcus aureus and Escherichia coli dual-species biofilms on nanohydroxyapatite loaded with CHX or ZnO nanoparticles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhslGgu7jP&md5=9f59c6273f85c5b6b7f699df7c7c308bCAS |
Cha, S. K., Kim, N. H., Lee, S. M., Baik, C. S., Lee, H. T., and 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, 441–446.
| Effect of cytochalasin B and cycloheximide on the activation rate, chromosome constituent and in vitro development of porcine oocytes following parthenogenetic stimulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnslyksLY%3D&md5=8a134626a05961c2d4d59401e07687ccCAS |
Cui, M. S., Liu, Z. X., Wang, X. L., Zhang, J., Yi, W. U., Han, G. C., and Zeng, S. M. (2011). Relationship between differential expression of Bax and Bcl-2 genes and developmental differences of porcine parthenotes cultured in PZM-3 and NCSU-23. J. Integr. Agric. 10, 1772–1780.
| 1:CAS:528:DC%2BC3MXhsVOltbrL&md5=c84ac2000d702e0472d7bb971b9ad245CAS |
Do, M., Jang, W. G., Hwang, J. H., Jang, H., Kim, E. J., Jeong, E. J., Shim, H., Hwang, S. S., Oh, K. B., and Byun, S. J. (2012). Inheritance of mitochondrial DNA in serially recloned pigs by somatic cell nuclear transfer (SCNT). Biochem. Biophys. Res. Commun. 424, 765–770.
| Inheritance of mitochondrial DNA in serially recloned pigs by somatic cell nuclear transfer (SCNT).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFeitLbE&md5=ac2212133bcd73605dd7b0d0c591905aCAS |
Emanuel, S., Rugg, C. A., Gruninger, R. H., Lin, R., Fuentes-Pesquera, A., Connolly, P. J., Wetter, S. K., Hollister, B., Kruger, W. W., and Napier, C. (2005). The in vitro and in vivo effects of JNJ-7706621: a dual inhibitor of cyclin-dependent kinases and aurora kinases. Cancer Res. 65, 9038.
| The in vitro and in vivo effects of JNJ-7706621: a dual inhibitor of cyclin-dependent kinases and aurora kinases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKiu7vM&md5=d47ac2c2855b2cc1a1bb90d1a889c165CAS |
Fukui, Y., Sawai, K., Furudate, M., Sato, N., Iwazumi, Y., and Ohsaki, K. (1992). Parthenogenetic development of bovine oocytes treated with ethanol and cytochalasin B after in vitro maturation. Mol. Reprod. Dev. 33, 357–362.
| Parthenogenetic development of bovine oocytes treated with ethanol and cytochalasin B after in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlsVSqug%3D%3D&md5=0f4dbfc45695c0335b1f6d7e9e16be35CAS |
Funahashi, H., Cantley, T. C., and Day, B. N. (1997). Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization. Biol. Reprod. 57, 49–53.
| Synchronization of meiosis in porcine oocytes by exposure to dibutyryl cyclic adenosine monophosphate improves developmental competence following in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXktFCntb0%3D&md5=29ae05e3072dd1632c6e97bf8e67dd0dCAS |
Guo, Q., Zhu, H. Y., Jin, L., Gao, Q. S., Kang, J. D., Cui, C. D., and Yin, X. J. (2015). Production of cloned Wuzhishan miniature pigs and application for alloxan toxicity test. Anim. Biotechnol. 26, 292–297.
| Production of cloned Wuzhishan miniature pigs and application for alloxan toxicity test.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1Sgt73K&md5=1de4e7c8deb161d0e3275531e0b9471eCAS |
Guo, Q., Jin, L., Zhu, H. Y., Li, X. C., Zhang, Y. C., Xing, X. X., Zhang, G. L., Xuan, M. F., Luo, Q. R., and Luo, Z. B. (2017). CDK inhibitor SU9516 induces tetraploid blastocyst formation from parthenogenetically activated porcine embryos. Biotechnol. Lett. 39, 951–957.
| CDK inhibitor SU9516 induces tetraploid blastocyst formation from parthenogenetically activated porcine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXks12lsb4%3D&md5=f08681d69f1c6636c4fd3e2bc3e8aa73CAS |
Hégarat, N., Rata, S., and Hochegger, H. (2016). Bistability of mitotic entry and exit switches during open mitosis in mammalian cells. BioEssays 38, 627.
| Bistability of mitotic entry and exit switches during open mitosis in mammalian cells.Crossref | GoogleScholarGoogle Scholar |
Hunter, T. (1995). Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80, 225–236.
| Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtlGnsrs%3D&md5=ee343ef233d8f7d2447042734e7683aeCAS |
Jin, L., Zhu, H. Y., Guo, Q., Li, X. C., Zhang, Y. C., Zhang, G. L., Xing, X. X., Xuan, M. F., Luo, Q. R., and Yin, X. J. (2016). PCI-24781 can improve in vitro and in vivo developmental capacity of pig somatic cell nuclear transfer embryos. Biotechnol. Lett. 38, 1433–1441.
| PCI-24781 can improve in vitro and in vivo developmental capacity of pig somatic cell nuclear transfer embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XpsVOntbo%3D&md5=c805c7ba8d49270528f4467c47c783a1CAS |
Kim, Y. J., Ahn, K. S., Kim, M., Kim, M. J., Park, S. M., Ryu, J., Ahn, J. S., Heo, S. Y., Kang, J. H., and Choi, Y. J. (2014). Targeted disruption of Ataxia-telangiectasia mutated gene in miniature pigs by somatic cell nuclear transfer. Biochem. Biophys. Res. Commun. 452, 901–905.
| Targeted disruption of Ataxia-telangiectasia mutated gene in miniature pigs by somatic cell nuclear transfer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFWgu77I&md5=a1d61595ab9dbc52397790a2212b3c0dCAS |
Kubiak, J. Z., Weber, M., De, P. H., Winston, N. J., and Maro, B. (1993). The metaphase II arrest in mouse oocytes is controlled through microtubule-dependent destruction of cyclin B in the presence of CSF. EMBO J. 12, 3773–3778.
| 1:CAS:528:DyaK3sXmtVSlsrk%3D&md5=7fe5243d0bf56452617ecb5e0f34f110CAS |
Li, S., Kang, J. D., Jin, J. X., Hong, Y., Zhu, H. Y., Jin, L., Gao, Q. S., Yan, C. G., Cui, C. D., and Li, W. X. (2014). Effect of demecolcine-assisted enucleation on the MPF level and cyclin B1 distribution in porcine oocytes. PLoS One 9, e91483.
| Effect of demecolcine-assisted enucleation on the MPF level and cyclin B1 distribution in porcine oocytes.Crossref | GoogleScholarGoogle Scholar |
Masui, Y. (1991). The role of “Cytostatic Factor (CSF)” in the control of oocyte cell cycles: a summary of 20 years of study. Dev. Growth Differ. 33, 543–551.
| The role of “Cytostatic Factor (CSF)” in the control of oocyte cell cycles: a summary of 20 years of study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XhsVynu7s%3D&md5=17f09fd9ab85ed2acc417749e0472e43CAS |
Masui, Y., and Markert, C. L. (1971). Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J. Exp. Zool. 177, 129–145.
| 1:STN:280:DyaE3M3ptFOitA%3D%3D&md5=8e04db2e8bcda13bcf98c07d24dd7026CAS |
Presicce, G. A., and Yang, X. (1994). Nuclear dynamics of parthenogenesis of bovine oocytes matured in vitro for 20 and 40 hours and activated with combined ethanol and cycloheximide treatment. Mol. Reprod. Dev. 37, 61–68.
| Nuclear dynamics of parthenogenesis of bovine oocytes matured in vitro for 20 and 40 hours and activated with combined ethanol and cycloheximide treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhvVyhu7w%3D&md5=86e23cc9e5f185009730b8c5a23cdec2CAS |
Seamon, J. A., Rugg, C. A., Emanuel, S., Calcagno, A. M., Ambudkar, S. V., Middleton, S. A., Butler, J., Borowski, V., and Greenberger, L. M. (2006). Role of the ABCG2 drug transporter in the resistance and oral bioavailability of a potent cyclin-dependent kinase/Aurora kinase inhibitor. Mol. Cancer Ther. 5, 2459.
| Role of the ABCG2 drug transporter in the resistance and oral bioavailability of a potent cyclin-dependent kinase/Aurora kinase inhibitor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOmtbbE&md5=f48c6a0f64724b8da02c8cc0d38c5d7fCAS |
Sommer, C. A., Stadtfeld, M., Murphy, G. J., Hochedlinger, K., Kotton, D. N., and Mostoslavsky, G. (2009). Induced pluripotent stem cell generation using a single lentiviral stem cell cassette. Stem Cells 27, 543–549.
| Induced pluripotent stem cell generation using a single lentiviral stem cell cassette.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvVKgtbY%3D&md5=c1a28fe358151619ca36831e007be3c2CAS |
Szöllösi, M. S., Kubiak, J. Z., Debey, P., De, P. H., Szöllösi, D., and Maro, B. (1993). Inhibition of protein kinases by 6-dimethylaminopurine accelerates the transition to interphase in activated mouse oocytes. J. Cell Sci. 104, 861–872.
Tao, L., Yang, M., Wang, X., Zhang, Z., Wu, Z., Tian, J., An, L., and Wang, S. (2016). Efficient biallelic mutation in porcine parthenotes using a CRISPR-Cas9 system. Biochem. Biophys. Res. Commun. 476, 225.
| Efficient biallelic mutation in porcine parthenotes using a CRISPR-Cas9 system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XptVWrs74%3D&md5=a9225f8a64bed1d6b1e688055899de02CAS |
Tiwari, M., and Chaube, S. K. (2017). Maturation-promoting factor destabilization mediates human chorionic gonadotropin-induced meiotic resumption in rat oocytes. Dev. Growth Differ. 59, 603–614.
| Maturation-promoting factor destabilization mediates human chorionic gonadotropin-induced meiotic resumption in rat oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXhsFWqurjI&md5=b71a370238a88dd27ba57da1d938a3beCAS |
Van De Velde, A., Liu, L., Bols, P. E., Ysebaert, M. T., and Yang, X. (1999). Cell allocation and chromosomal complement of parthenogenetic and IVF bovine embryos. Mol. Reprod. Dev. 54, 57–62.
| Cell allocation and chromosomal complement of parthenogenetic and IVF bovine embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkvFanur4%3D&md5=933c3aa2e2396818cf4d50eaed8cdb29CAS |
Wang, H. Y., Luo, Y. B., Lin, Z. L., Lee, I. W., Kwon, J., Cui, X. S., and Kim, N. H. (2015). Effect of ATM and HDAC inhibition on etoposide-induced DNA damage in porcine early preimplantation embryos. PLoS One 10, e0142561.
| Effect of ATM and HDAC inhibition on etoposide-induced DNA damage in porcine early preimplantation embryos.Crossref | GoogleScholarGoogle Scholar |
Whitaker, M. (1996). Control of meiotic arrest. Rev. Reprod. 1, 127.
| Control of meiotic arrest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksVymu7w%3D&md5=0aacd659520e034a7d1b800527d7f796CAS |
Yang, X., Presicce, G. A., Moraghan, L., Jiang, S. E., and Foote, R. H. (1994). Synergistic effect of ethanol and cycloheximide on activation of freshly matured bovine oocytes. Theriogenology 41, 395.
| Synergistic effect of ethanol and cycloheximide on activation of freshly matured bovine oocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktlWqu7o%3D&md5=cd4d085a574c1c5553a187d88d12f0a5CAS |
Yin, X. J., Tani, T., Yonemura, I., Kawakami, M., Miyamoto, K., Hasegawa, R., Kato, Y., and Tsunoda, Y. (2002). Production of cloned pigs from adult somatic cells by chemically assisted removal of maternal chromosomes. Biol. Reprod. 67, 442.
| Production of cloned pigs from adult somatic cells by chemically assisted removal of maternal chromosomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsFKqtrc%3D&md5=f0090009bfacb3b3ffca003f23b0177aCAS |