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Influence of oocyte selection, activation with a zinc chelator and inhibition of histone deacetylases on cloned porcine embryo and chemically activated oocytes development

Published online by Cambridge University Press:  14 April 2020

Felipe L. Ongaratto Open the ORCID record for Felipe L. Ongaratto [Opens in a new window] ,
Paula Rodriguez-Villamil ,
Marcelo Bertolini  and
Daniel F. Carlson
Felipe L. Ongaratto*
Affiliation:
Recombinetics Inc., Saint Paul, Minnesota, USA
Paula Rodriguez-Villamil
Affiliation:
Recombinetics Inc., Saint Paul, Minnesota, USA
Marcelo Bertolini
Affiliation:
Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
Daniel F. Carlson
Affiliation:
Recombinetics Inc., Saint Paul, Minnesota, USA
*
Author for correspondence: Felipe L. Ongaratto. Recombinetics Inc., 1246 University Ave W, Saint Paul, MN55104, USA. Tel: +1 612 727 2000. E-mail: felipe.ongaratto@recombinetics.com
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Summary

The aim of this study was to evaluate the effects of alternative protocols to improve oocyte selection, embryo activation and genomic reprogramming on in vitro development of porcine embryos cloned by somatic cell nuclear transfer (SCNT). In Experiment 1, in vitro-matured oocytes were selected by exposure to a hyperosmotic sucrose solution prior to micromanipulation. In Experiment 2, an alternative chemical activation protocol using a zinc chelator as an adjuvant (ionomycin + N,N,N′,N′-tetrakis(2-pyridylmethyl)ethylenediamine (TPEN) + N-6-dimethylaminopurine (6-DMAP)) was compared with a standard protocol (ionomycin + 6-DMAP) for the activation of porcine oocytes or SCNT embryos. In Experiment 3, presumptive cloned zygotes were incubated after chemical activation in a histone deacetylase inhibitor (Scriptaid) for 15 h, with the evaluation of embryo yield and total cell number in day 7 blastocysts. In Experiment 1, cleavage rates tended to be higher in sucrose-treated oocytes than controls (123/199, 61.8% vs. 119/222, 53.6%, respectively); however, blastocyst rates were similar between groups. In Experiment 2, cleavage rates were higher in zygotes treated with TPEN than controls but no difference in blastocyst rates between groups occurred. For Experiment 3, the exposure to Scriptaid did not improve embryo development after cloning. Nevertheless, the total number of cells was higher in cloned zygotes treated with Scriptaid than SCNT controls. In conclusion, oocyte selection by sucrose as well as treatments with zinc chelator and an inhibitor of histone deacetylases did not significantly improve blastocyst yield in cloned and parthenotes. However, the histone deacetylases inhibitor produced a significant improvement in the blastocyst quality.

Keywords

ActivationHDACiPorcine embryosSCNTScriptaidTPEN
Type
Research Article
Information
Zygote , Volume 28 , Issue 4 , August 2020 , pp. 286 - 290
Copyright
© Cambridge University Press 2020

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References

Aguiar, LH, Ticiani, E, Rodriguez-Villamil, P, Ongaratto, FL, Lazzarotto, CR, Rodrigues, JL, Bertolini, LR and Bertolini, M (2017) Probability, odds and random chance: the difficult task of modulating the epigenetic profile of cloned embryos. Anim Reprod 14, 102–23.CrossRefGoogle Scholar
Bang, JI, Yoo, JG, Park, MR, Shin, TS, Cho, BW, Lee, HG, Kim, BW, Kang, TY, Kong, IK, Kim, JH and Cho, SK (2013) The effects of artificial activation timing on the development of SCNT-derived embryos and newborn piglets. Reprod Biol 13, 127–32.CrossRefGoogle ScholarPubMed
Bannister, AJ and Kouzarides, T (2011) Regulation of chromatin by histone modifications. Cell Res 21, 381–95.CrossRefGoogle ScholarPubMed
Callensen, H, Liu, Y, Pedersen, HS, Li, R and Schmidt, M (2014) Increasing efficiency in production of cloned piglets. Cell Reprogram 16, 407–10.CrossRefGoogle Scholar
Cao, Z, Sui, L, Li, Y, Ji, S, Zhang, X and Zhang, Y (2012) Effects of chemically defined medium on early development of porcine embryos derived from parthenogenetic activation and cloning. Zygote 20, 229–36.CrossRefGoogle ScholarPubMed
Cibelli, JB, Campbell, KH, Seidel, GE, West, MD and Lanza, RP (2002) The health profile of cloned animals. Nat Biotechnol 20, 13–14.CrossRefGoogle ScholarPubMed
Dang-Nguyen, TQ, Nguyen, HT, Somfai, T, Wells, D, Men, NT, Viet-Linh, N, Noguchi, J, Kaneko, H, Kikuchi, K and Nagai, T (2018) Sucrose assists selection of high-quality oocytes in pigs. Anim Sci J 89, 880–7.CrossRefGoogle ScholarPubMed
Ducibella, T and Fissore, R (2008) The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev Biol 315, 257–79.CrossRefGoogle ScholarPubMed
Ferrer-Buitrago, M, Bonte, D, De Sutter, P, Leybaert, L and Heindryckx, B (2018) Single Ca2+ transients vs oscillatory Ca2+ signaling for assisted oocyte activation: limitations and benefits. Reproduction 155, 105–19.CrossRefGoogle ScholarPubMed
Iwasaki, W, Yamanaka, K, Sugiyama, D, Teshima, Y, Briones-Nagata, MP, Maeki, M, Yamashita, K, Takahashi, M and Miyazaki, M (2018) Simple separation of good quality bovine oocytes using a microfluidic device. Sci Rep 8, 14273.CrossRefGoogle ScholarPubMed
Kato, Y, Tani, T, Sotomaru, Y, Kurokawa, K, Kato, JY, Doguchi, H, Yasue, H and Tsunoda, Y (1998) Eight calves cloned from somatic cells of a single adult. Science 282, 2095–8.CrossRefGoogle ScholarPubMed
Keefer, CL (2015) Artificial cloning of domestic animals. Proc Natl Acad Sci USA 112, 8874–8.CrossRefGoogle ScholarPubMed
Kempisty, B, Piotrowska, H, Rybska, M, Woźna, M, Antosik, P, Bukowska, D, Zawierucha, P, Ciesiółka, S, Jaśkowski, JM, Nowicki, M and Brüssow, KP (2015) Expression of INHβA and INHβB proteins in porcine oocytes cultured in vitro is dependent on the follicle size. Zygote 23, 205–11.CrossRefGoogle ScholarPubMed
Kishigami, S, Mizutani, E, Ohta, H, Hikichi, T, Van Thuan, N, Wakayama, S, Bui, HT and Wakayama, T (2006) Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem Biophys Res Commum 340, 183–9.CrossRefGoogle ScholarPubMed
Lee, BC, Kim, MK, Jang, G, Oh, HJ, Yuda, F, Kim, HJ, Shamim, MH, Kim, JJ, Kang, SK, Schatten, G and Hwang, WS (2005) Dogs cloned from adult somatic cells. Nature 436, 641.CrossRefGoogle ScholarPubMed
Lee, J, Lee, Y, Park, B, Elahi, F, Jeon, Y, Hyun, SH and Lee, E (2014) Developmental competence of IVM pig oocytes after SCNT in relation to the shrinkage pattern induced by hyperosmotic treatment. Theriogenology 81, 974–81.CrossRefGoogle ScholarPubMed
Lee, K, Davis, A, Zhang, L, Ryu, J, Spate, LD, Park, KW, Samuel, MS, Walters, EM, Murphy, CN, Machaty, Z and Prather, RS (2015) Pig oocyte activation using a Zn2+ chelator, TPEN. Theriogenology 84, 1024–32.CrossRefGoogle Scholar
Li, XC, Guo, Q, Zhu, HY, Jin, L, Zhang, YC, Zhang, GL, Xing, XX, Xuan, MF, Luo, QR, Luo, ZB and Wang, JX (2017) Parthenogenetic activation and somatic cell nuclear transfer of porcine oocytes activated by an electric pulse and AZD5438 treatment. Zygote 25, 453–61.CrossRefGoogle ScholarPubMed
Liang, S, Zhao, MH, Choi, JW, Kim, NH and Cui, XS (2015) Scriptaid treatment decreases DNA methyltransferase 1 expression by induction of microRNA-152 expression in porcine somatic cell nuclear transfer embryos. PLoS One 10, e0134567.CrossRefGoogle ScholarPubMed
Lin, T, Lee, JE, Shin, HY, Oqani, RK and Jin, DI (2015) Factors influencing the efficiency of in vitro embryo production in the pig. Reprod Dev Biol 39, 29–36.CrossRefGoogle Scholar
Liu, S, Cui, K, Li, HL, Sun, JM, Lu, XR, Shen, KY, Liu, QY and Shi, DS (2015) Comparison of chemical, electrical, and combined activation methods for in vitro matured porcine oocytes. In Vitro Cell Dev Biol Anim 51, 103–12.CrossRefGoogle ScholarPubMed
Macedo, MP, Glanzner, WG, Rissi, VB, Gutierrez, K, Currin, L, Baldassarre, H and Bordignon, V (2019) A fast and reliable protocol for activation of porcine oocytes. Theriogenology 123, 22–9.CrossRefGoogle ScholarPubMed
Meerschaut, FV, Nikiforaki, D, Heindryckx, B and De Sutter, P (2014) Assisted oocyte activation following ICSI fertilization failure. Reprod Biomed Online 28, 560–71.CrossRefGoogle Scholar
Polejaeva, IA, Chen, SH, Vaught, TD, Page, RL, Mullins, J, Ball, S, Dai, Y, Boone, J, Walker, S, Ayares, DL and Colman, A (2000) Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407, 86.CrossRefGoogle ScholarPubMed
Shin, T, Kraemer, D, Pryor, J, Liu, L, Rugila, J, Howe, L, Buck, S, Murphy, K, Lyons, L and Westhusin, M (2002) Cell biology: a cat cloned by nuclear transplantation. Nature 415, 859.CrossRefGoogle Scholar
Siriboon, C, Li, TS, Yu, CW, Chern, JW and Ju, JC (2018) Novel histone deacetylase inhibitors and embryo aggregation enhance cloned embryo development and ES cell derivation in pigs. PLoS One, 13, 0204588.CrossRefGoogle ScholarPubMed
Solter, D (2000) Mammalian cloning: advances and limitations. Nat Rev Genet 1, 199.CrossRefGoogle ScholarPubMed
Tosti, E, Boni, R and Cuomo, A (2002) Fertilization and activation currents in bovine oocytes. Reproduction 124, 835–46.CrossRefGoogle ScholarPubMed
Wakayama, T, Perry, AC, Zuccotti, M, Johnson, KR and Yanagimachi, R (1998) Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394, 369.CrossRefGoogle ScholarPubMed
Wang, MK, Liu, JL, Li, GP, Lian, L and Chen, DY (2001) Sucrose pretreatment for enucleation: An efficient and non‐damage method for removing the spindle of the mouse MII oocyte. Mol Reprod Dev 58, 432–6.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
Whitworth, KM, Zhao, J, Spate, LD, Li, R and Prather, RS (2011) Scriptaid corrects gene expression of a few aberrantly reprogrammed transcripts in nuclear transfer pig blastocyst stage embryos. Cell Reprogram 13, 191–204.CrossRefGoogle ScholarPubMed
Wilmut, I, Schnieke, AE, McWhir, J, Kind, AJ and Campbell, KH (1997) Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810.CrossRefGoogle ScholarPubMed
Xu, W, Li, Z, Yu, B, He, X, Shi, J, Zhou, R, Liu, D and Wu, Z (2013) Effects of DNMT1 and HDAC inhibitors on gene-specific methylation reprogramming during porcine somatic cell nuclear transfer. PLoS One 8, e64705.CrossRefGoogle ScholarPubMed
Yang, X, Smith, SL, Tian, XC, Lewin, HA, Renard, JP and Wakayama, T (2007) Nuclear reprogramming of cloned embryos and its implications for therapeutic cloning. Nat Genet 39, 295.CrossRefGoogle ScholarPubMed
Zhao, J, Hao, Y, Ross, JW, Spate, LD, Walters, EM, Samuel, MS, Rieke, A, Murphy, CN and Prather, RS (2010) Histone deacetylase inhibitors improve in vitro and in vivo developmental competence of somatic cell nuclear transfer porcine embryos. Cell Reprogram 12, 75–83.CrossRefGoogle ScholarPubMed
Zhao, MH, Kim, NH and Cui, XS (2014) Zinc depletion activates porcine metaphase II oocytes independently of the protein kinase C pathway. In Vitro Cell Dev Biol Anim 50, 945–51.CrossRefGoogle ScholarPubMed
Zhou, Q, Renard, JP, Le Friec, G, Brochard, V, Beaujean, N, Cherifi, Y, Fraichard, A and Cozzi, J (2003) Generation of fertile cloned rats by regulating oocyte activation. Science 302, 1179.CrossRefGoogle ScholarPubMed