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Analysis of Cyclin E1 Functions in Porcine Preimplantation Embryonic Development by Fluorescence Microscopy

Published online by Cambridge University Press:  06 February 2017

Jing Guo ,
Kyung-Tae Shin  and
Xiang-Shun Cui
Jing Guo
Affiliation:
Department of Animal Sciences, Chungbuk National University, Chungbuk, Cheongju 361-763, Republic of Korea
Kyung-Tae Shin
Affiliation:
Department of Animal Sciences, Chungbuk National University, Chungbuk, Cheongju 361-763, Republic of Korea
Xiang-Shun Cui*
Affiliation:
Department of Animal Sciences, Chungbuk National University, Chungbuk, Cheongju 361-763, Republic of Korea
*
*Corresponding author. [email protected]
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Abstract

Cyclin E1 (CCNE1) is a core component of cell cycle regulation that drives the transition into the S phase. CCNE1 plays critical roles in cell cycle, cell proliferation, and cellular functions. However, the function of CCNE1 in early embryonic development is limited. In the present study, the function and expression of Ccne1 in porcine early parthenotes were examined. Immunostaining experiments showed that CCNE1 localized in the nucleus, starting at the four-cell stage. Knockdown of Ccne1 by double-stranded RNA resulted in the failure of blastocyst formation and induced blastocyst apoptosis. Ccne1 depletion increased expression of the pro-apoptotic gene Bax, and decreased the expression of Oct4 and the rate of inner cell mass (ICM)/trophectoderm formation. The results indicated that CCNE1 affects blastocyst formation by inducing cell apoptosis and ICM formation during porcine embryonic development.

Keywords

Cyclin E1embryonic developmentapoptosispluripotencypigmicroRNA
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 23 , Issue 1 , February 2017 , pp. 69 - 76
Copyright
© Microscopy Society of America 2017 

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References

Adjaye, J., Huntriss, J., Herwig, R., BenKahla, A., Brink, T.C., Wierling, C., Hultschig, C., Groth, D., Yaspo, M.L. & Picton, H.M. (2005). Primary differentiation in the human blastocyst: comparative molecular portraits of inner cell mass and trophectoderm cells. Stem Cells 23(10), 1514–1525.Google Scholar
Aleem, E., Kiyokawa, H. & Kaldis, P. (2005). Cdc2–cyclin E complexes regulate the G1/S phase transition. Nat Cell Biol 7(8), 831–836.Google Scholar
Bartek, J., Lukas, C. & Lukas, J. (2004). Checking on DNA damage in S phase. Nat Rev Mol Cell Biol 5(10), 792–804.CrossRefGoogle ScholarPubMed
Bavister, B.D., Leibfried, M.L. & Lieberman, G. (1983). Development of preimplantation embryos of the golden hamster in a defined culture medium. Biol Reprod 28(1), 235–247.Google Scholar
Becker, K.A., Ghule, P.N., Therrien, J.A., Lian, J.B., Stein, J.L., Van Wijnen, A.J. & Stein, G.S. (2006). Self‐renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase. J Cell Physiol 209(3), 883–893.CrossRefGoogle ScholarPubMed
Bertoli, C., Skotheim, J.M. & de Bruin, R.A. (2013). Control of cell cycle transcription during G1 and S phases. Nat Rev Mol Cell Biol 14(8), 518–528.Google Scholar
Biedermann, B., Wright, J., Senften, M., Kalchhauser, I., Sarathy, G., Lee, M.-H. & Ciosk, R. (2009). Translational repression of cyclin E prevents precocious mitosis and embryonic gene activation during C. elegans meiosis. Dev Cell 17(3), 355–364.Google Scholar
Caldon, C.E. & Musgrove, E.A. (2010). Distinct and redundant functions of cyclin E1 and cyclin E2 in development and cancer. Cell Div 5(1), 1.Google Scholar
De Paepe, C., Krivega, M., Cauffman, G., Geens, M. & Van de Velde, H. (2014). Totipotency and lineage segregation in the human embryo. Mol Human Reprod 20(7), 599–618.CrossRefGoogle ScholarPubMed
Gardner, D.K., Lane, M., Stevens, J., Schlenker, T. & Schoolcraft, W.B. (2000). Blastocyst score affects implantation and pregnancy outcome: towards a single blastocyst transfer. Fertil Steril 73(6), 1155–1158.Google Scholar
Geng, Y., Yu, Q., Sicinska, E., Das, M., Schneider, J.E., Bhattacharya, S., Rideout, W.M., Bronson, R.T., Gardner, H. & Sicinski, P. (2003). Cyclin E ablation in the mouse. Cell 114(4), 431–443.Google Scholar
Geng, Y., Yu, Q., Whoriskey, W., Dick, F., Tsai, K.Y., Ford, H.L., Biswas, D.K., Pardee, A.B., Amati, B. & Jacks, T. (2001). Expression of cyclins E1 and E2 during mouse development and in neoplasia. Proc Natl Acad Sci 98(23), 13138–13143.Google Scholar
Gotoh, T., Shigemoto, N. & Kishimoto, T. (2007). Cyclin E2 is required for embryogenesis in Xenopus laevis. Dev Biol 310(2), 341–347.CrossRefGoogle ScholarPubMed
Guo, J., Zhao, M.-H., Liang, S., Choi, J.-W., Kim, N.-H. & Cui, X.-S. (2016). Liver receptor homolog 1 influences blastocyst hatching in pigs. J Reprod Dev 62(3), 297–303.CrossRefGoogle ScholarPubMed
Hui, W., Yuntao, L., Lun, L., WenSheng, L., ChaoFeng, L., HaiYong, H. & Yueyang, B. (2013). MicroRNA-195 inhibits the proliferation of human glioma cells by directly targeting cyclin D1 and cyclin E1. PLoS One 8(1), e54932.Google Scholar
Kiessling, A.A., Bletsa, R., Desmarais, B., Mara, C., Kallianidis, K. & Loutradis, D. (2010). Genome-wide microarray evidence that 8-cell human blastomeres over-express cell cycle drivers and under-express checkpoints. J Assist Reprod Genet 27(6), 265–276.CrossRefGoogle ScholarPubMed
Krivega, M., Geens, M., Heindryckx, B., Santos-Ribeiro, S., Tournaye, H. & Van de Velde, H. (2015). Cyclin E1 plays a key role in balancing between totipotency and differentiation in human embryonic cells.. Mol Human Reprod 21(12), 942–956.Google Scholar
Lim, S. & Kaldis, P. (2013). Cdks, cyclins and CKIs: roles beyond cell cycle regulation. Development 140(15), 3079–3093.CrossRefGoogle ScholarPubMed
Lu, X., Liu, J. & Legerski, R.J. (2009). Cyclin E is stabilized in response to replication fork barriers leading to prolonged S phase arrest. J Biol Chem 284(51), 35325–35337.Google Scholar
Möröy, T. & Geisen, C. (2004). Cyclin E. Int J Biochem Cell Biol 36(8), 1424–1439.Google Scholar
Nasr-Esfahani, M.H., Aitken, J.R. & Johnson, M.H. (1990). Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109(2), 501–507.Google Scholar
O’connor, P. (1996). Mammalian G1 and G2 phase checkpoints. Cancer Surv 29, 151–182.Google Scholar
Ohtsubo, M., Theodoras, A.M., Schumacher, J., Roberts, J.M. & Pagano, M. (1995). Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol Cell Biol 15(5), 2612–2624.Google Scholar
Parisi, T., Beck, A.R., Rougier, N., McNeil, T., Lucian, L., Werb, Z. & Amati, B. (2003). Cyclins E1 and E2 are required for endoreplication in placental trophoblast giant cells. EMBO J 22(18), 4794–4803.CrossRefGoogle ScholarPubMed
Sakurai, N., Fujii, T., Hashizume, T. & Sawai, K. (2013). Effects of downregulating oct-4 transcript by RNA interference on early development of porcine embryos. J Reprod Dev 59(4), 353–360.CrossRefGoogle ScholarPubMed
Siu, K.T., Rosner, M.R. & Minella, A.C. (2012). An integrated view of cyclin E function and regulation. Cell Cycle 11(1), 57–64.Google Scholar
Stead, E., White, J., Faast, R., Conn, S., Goldstone, S., Rathjen, J., Dhingra, U., Rathjen, P., Walker, D. & Dalton, S. (2002). Pluripotent cell division cycles are driven by ectopic Cdk2, cyclin A/E and E2F activities. Oncogene 21(54), 8320–8333.Google Scholar
Wang, H., Luo, Y., Lin, Z., 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(11), e0142561.Google Scholar
Wang, J., Xu, G., Shen, F. & Kang, Y. (2014). Mir-132 targeting cyclin E1 suppresses cell proliferation in osteosarcoma cells. Tumor Biol 35(5), 4859–4865.CrossRefGoogle ScholarPubMed
Wang, Z.-W., Ma, X.-S., Ma, J.-Y., Luo, Y.-B., Lin, F., Wang, Z.-B., Fan, H.-Y., Schatten, H. & Sun, Q.-Y. (2013). Laser microbeam-induced DNA damage inhibits cell division in fertilized eggs and early embryos. Cell Cycle 12(20), 3336–3344.CrossRefGoogle ScholarPubMed
Yamanaka, K.-I., Sugimura, S., Wakai, T., Kawahara, M. & Sato, E. (2009). Difference in sensitivity to culture condition between in vitro fertilized and somatic cell nuclear transfer embryos in pigs. J Reprod Dev 55(3), 299–304.CrossRefGoogle ScholarPubMed
Yang, H.W., Hwang, K.J., Kwon, H.C., Kim, H.S., Choi, K.W. & Oh, K.S. (1998). Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum Reprod 13(4), 998–1002.CrossRefGoogle ScholarPubMed