Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-28T01:11:36.546Z Has data issue: false hasContentIssue false
  • English
  • Français

Methylation characteristics and developmental potential of Guangxi Bama minipig (Sus scrofa domestica) cloned embryos from donor cells treated with trichostatin A and 5-aza-2′-deoxycytidine

Published online by Cambridge University Press:  22 February 2012

Shu-Fang Ning ,
Qing-Yang Li ,
Ming-Ming Liang ,
Xiao-Gan Yang ,
Hui-Yan Xu ,
Yang-Qing Lu ,
Sheng-Sheng Lu  and
Ke-Huan Lu
Shu-Fang Ning
Affiliation:
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Animal Reproduction Institute, Guangxi University, Nanning, Guangxi 530004, China.
Qing-Yang Li
Affiliation:
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Animal Reproduction Institute, Guangxi University, Nanning, Guangxi 530004, China.
Ming-Ming Liang
Affiliation:
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Animal Reproduction Institute, Guangxi University, Nanning, Guangxi 530004, China.
Xiao-Gan Yang
Affiliation:
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Animal Reproduction Institute, Guangxi University, Nanning, Guangxi 530004, China.
Hui-Yan Xu
Affiliation:
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Animal Reproduction Institute, Guangxi University, Nanning, Guangxi 530004, China.
Yang-Qing Lu
Affiliation:
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Animal Reproduction Institute, Guangxi University, Nanning, Guangxi 530004, China.
Sheng-Sheng Lu*
Affiliation:
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Animal Reproduction Institute, Guangxi University, Nanning, Guangxi 530004, China.
Ke-Huan Lu*
Affiliation:
State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Animal Reproduction Institute, Guangxi University, Nanning, Guangxi 530004, China.
*
All correspondence to: Sheng-Sheng Lu or Ke-Huan Lu. State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Animal Reproduction Institute, Guangxi University, Nanning, Guangxi 530004, China. Tel: +86 771 3270036; e-mail: shengshenglu@sina.com (S-S. Lu). Tel:/Fax: +86 771 3238064; e-mail: kehuanlu@163.com (K-H. Lu).
All correspondence to: Sheng-Sheng Lu or Ke-Huan Lu. State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Animal Reproduction Institute, Guangxi University, Nanning, Guangxi 530004, China. Tel: +86 771 3270036; e-mail: shengshenglu@sina.com (S-S. Lu). Tel:/Fax: +86 771 3238064; e-mail: kehuanlu@163.com (K-H. Lu).
Get access Rights & Permissions [Opens in a new window]

Summary

Reprogramming of DNA methylation in somatic cell nuclear transfer (SCNT) embryos is incomplete, and aberrant DNA methylation patterns are related to the inefficiency of SCNT. To facilitate nuclear reprogramming, this study investigated the effect of treating Guangxi Bama minipig donor cells with trichostatin A (TSA), 5-aza-2′-deoxycytine (5-aza-dC), or combination of TSA and 5-aza-dC prior to nuclear transfer. Analyses showed that there were no major changes in cell-cycle status among all groups. We monitored the transcription of DNMT1, DNMT3a, HDAC1 and IGF2 genes in donor cells. Transcription levels of HDAC1 were decreased significantly after treatment with a combination of TSA and 5-aza-dC, along with a significantly increased level of IGF2 (P < 0.05). Although treatment of donor cells with either TSA or 5-aza-dC alone resulted in non-significant effects in blastocyst formation rate and DNA methylation levels, a combination of TSA and 5-aza-dC significantly improved the development rates of minipig SCNT embryos to blastocyst (25.6% vs. 16.0%, P < 0.05). This change was accompanied by decreased levels of DNA methylation in somatic cells and blastocyst (P < 0.05). Thus in combination with TSA, lower concentrations of 5-aza-dC may produce a potent demethylating activity, and lead to the significantly enhanced blastocyst development percentage of Bama minipig SCNT embryos.

Keywords

5-aza-2′-deoxycytineBama minipigDNA methylationSomatic cell nuclear transferTrichostatin A
Type
Research Article
Information
Zygote , Volume 21 , Issue 2 , May 2013 , pp. 178 - 186
Copyright
Copyright © Cambridge University Press 2012

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

Beaujean, N., Taylor, J., Gardner, J., Wilmut, I., Meehan, R. & Young, L. (2004). Effect of limited DNA methylation reprogramming in the normal sheep embryo on somatic cell nuclear transfer. Biol. Reprod. 71, 185–93.CrossRefGoogle ScholarPubMed
Bo, F., Di, L., Qing-Chang, F., Liang, R., Hong, M., Liang, W., Zhen-Hua, G. & Zhong-Qiu, L. (2010). Effect of trichostatin A on transfected donor cells and subsequent development of porcine cloned embryos. Zygote 19, 237–43.CrossRefGoogle ScholarPubMed
Bonk, A.J., Cheong, H.T., Li, R., Lai, L., Hao, Y., Liu, Z., Samuel, M., Fergason, E.A., Whitworth, K.M., Murphy, C.N., Antoniou, E. & Prather, R.S. (2007). Correlation of developmental differences of nuclear transfer embryos cells to the methylation profiles of nuclear transfer donor cells in swine. Epigenetics 2, 179–86.CrossRefGoogle Scholar
Bonk, A.J., Li, R., Lai, L., Hao, Y., Liu, Z., Samuel, M., Fergason, E.A., Whitworth, K.M., Murphy, C.N., Antoniou, E. & Prather, R.S. (2008). Aberrant DNA methylation in porcine in vitro-, parthenogenetic-, and somatic cell nuclear transfer-produced blastocysts. Mol. Reprod. Dev. 75, 250–64.CrossRefGoogle ScholarPubMed
Bosak, N., Fujisaki, S., Kiuchi, S., Hiraiwa, H. & Yasue, H. (2003). Assignment of DNA cytosine-5-methyltransferase 1 (DNMT1) gene to porcine chromosome 2q21–q22 by somatic cell and radiation hybrid panel mapping. Cytogenet. Genome Res. 101, 178.Google Scholar
Cervera, R.P., Marti-Gutierrez, N., Escorihuela, E., Moreno, R. & Stojkovic, M. (2009). Trichostatin A affects histone acetylation and gene expression in porcine somatic cell nucleus transfer embryos. Theriogenology 72, 1097–110.CrossRefGoogle ScholarPubMed
Chen, T., Zhang, Y.L., Jiang, Y., Liu, S.Z., Schatten, H., Chen, D.Y. & Sun, Q.Y. (2004). The DNA methylation events in normal and cloned rabbit embryos. FEBS Lett. 578, 69–72.CrossRefGoogle ScholarPubMed
Costa-Borges, N., Santalo, J. & Ibanez, E. (2010). Comparison between the effects of valproic acid and trichostatin A on the in vitro development, blastocyst quality, and full-term development of mouse somatic cell nuclear transfer embryos. Cell Reprogram. 12, 437–46.CrossRefGoogle ScholarPubMed
Couldrey, C. & Lee, R.S. (2010). DNA methylation patterns in tissues from mid-gestation bovine foetuses produced by somatic cell nuclear transfer show subtle abnormalities in nuclear reprogramming. BMC Dev. Biol. 10, 27.CrossRefGoogle ScholarPubMed
Ding, X., Wang, Y., Zhang, D., Wang, Y., Guo, Z. & Zhang, Y. (2008). Increased pre-implantation development of cloned bovine embryos treated with 5-aza-2′-deoxycytidine and trichostatin A. Theriogenology 70, 622–30.CrossRefGoogle ScholarPubMed
Eilertsen, K.J., Power, R.A., Harkins, L.L. & Misica, P. (2007). Targeting cellular memory to reprogram the epigenome, restore potential, and improve somatic cell nuclear transfer. Anim. Reprod. Sci. 98, 129–46.CrossRefGoogle ScholarPubMed
Enright, B.P., Jeong, B.S., Yang, X. & Tian, X.C. (2003). Epigenetic characteristics of bovine donor cells for nuclear transfer: levels of histone acetylation. Biol. Reprod. 69, 1525–30.CrossRefGoogle ScholarPubMed
Enright, B.P., Sung, L.Y., Chang, C.C., Yang, X. & Tian, X.C. (2005). Methylation and acetylation characteristics of cloned bovine embryos from donor cells treated with 5-aza-2′-deoxycytidine. Biol. Reprod. 72, 944–8.CrossRefGoogle Scholar
Gebert, C., Wrenzycki, C., Herrmann, D., Groger, D., Reinhardt, R., Hajkova, P., Lucas-Hahn, A., Carnwath, J., Lehrach, H. & Niemann, H. (2006). The bovine IGF2 gene is differentially methylated in oocyte and sperm DNA. Genomics 88, 222–9.CrossRefGoogle ScholarPubMed
Giraldo, A.M., Hylan, D.A., Ballard, C.B., Purpera, M.N., Vaught, T.D., Lynn, J.W., Godke, R.A. & Bondioli, K.R. (2008). Effect of epigenetic modifications of donor somatic cells on the subsequent chromatin remodeling of cloned bovine embryos. Biol. Reprod. 78, 832–40.CrossRefGoogle ScholarPubMed
Himaki, T., Yokomine, T.A., Sato, M., Takao, S., Miyoshi, K. & Yoshida, M. (2010). Effects of trichostatin A on in vitro development and transgene function in somatic cell nuclear transfer embryos derived from transgenic Clawn miniature pig cells. Anim Sci J. 81, 558–63.CrossRefGoogle ScholarPubMed
Jiang, L., Jobst, P., Lai, L., Samuel, M., Ayares, D., Prather, R.S. & Tian, X.C. (2007). Expression levels of growth-regulating imprinted genes in cloned piglets. Cloning Stem Cells 9, 97–106.CrossRefGoogle ScholarPubMed
Kang, Y.K., Lee, K.K. & Han, Y.M. (2003). Reprogramming DNA methylation in the preimplantation stage: peeping with Dolly's eyes. Curr. Opin. Cell Biol. 15, 290–5.CrossRefGoogle ScholarPubMed
Kishigami, S., Mizutani, E., Ohta, H., Hikichi, T., Thuan, N.V., Wakayama, S., Bui, H.T. & Wakayama, T. (2006). Significant improvement of mouse cloning technique by treatment with trichostatin A after somatic nuclear transfer. Biochem. Biophys. Res. Commun. 340, 183–9.CrossRefGoogle ScholarPubMed
Kishigami, S., Bui, H.T., Wakayama, S., Tokunaga, K., Van Thuan, N., Hikichi, T., Mizutani, E., Ohta, H., Suetsugu, R., Sata, T. & Wakayama, T. (2007). Successful mouse cloning of an outbred strain by trichostatin A treatment after somatic nuclear transfer. J. Reprod. Dev. 53, 165–70.CrossRefGoogle ScholarPubMed
Li, J., Liu, Y., Zhang, J.W., Wei, H. & Yang, L. (2006). Characterization of hepatic drug-metabolizing activities of Bama miniature pigs (Sus scrofa domestica): comparison with human enzyme analogs. Comp. Med. 56, 286–90.Google ScholarPubMed
Li, J., Svarcova, O., Villemoes, K., Kragh, P.M., Schmidt, M., Bogh, I.B., Zhang, Y., Du, Y., Lin, L., Purup, S., Xue, Q., Bolund, L., Yang, H., Maddox-Hyttel, P. & Vajta, G. (2008). High in vitro development after somatic cell nuclear transfer and trichostatin A treatment of reconstructed porcine embryos. Theriogenology 70, 800–8.CrossRefGoogle ScholarPubMed
Liu, H.B., Lv, P.R., Yang, X.G., Qin, X.E., Pi, D.Y., Lu, Y.Q., Lu, K.H., Lu, S.S. & Li, D.S. (2009). Fibroblasts from the new-born male testicle of Guangxi Bama mini-pig (Sus scrofa) can support nuclear transferred embryo development in vitro. Zygote 17, 147–56.CrossRefGoogle ScholarPubMed
Liu, H.B., Lv, P.R., He, R.G., Yang, X.G., Qin, X.E., Pan, T.B., Huang, G.Y., Huang, M.R., Lu, Y.Q., Lu, S.S., Li, D.S. & Lu, K.H. (2010). Cloned Guangxi Bama minipig (Sus scrofa) and its offspring have normal reproductive performance. Cell Reprogram. 12, 543–50.CrossRefGoogle ScholarPubMed
Livak, K.J. & Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCT Method. Methods 25, 402–8.CrossRefGoogle Scholar
Martinez-Diaz, M.A., Che, L., Albornoz, M., Seneda, M.M., Collis, D., Coutinho, A.R., El-Beirouthi, N., Laurin, D., Zhao, X. & Bordignon, V. (2010). Pre- and postimplantation development of swine-cloned embryos derived from fibroblasts and bone marrow cells after inhibition of histone deacetylases. Cell Reprogram. 12, 85–94.CrossRefGoogle ScholarPubMed
Meng, Q., Polgar, Z., Liu, J. & Dinnyes, A. (2009). Live birth of somatic cell-cloned rabbits following trichostatin A treatment and cotransfer of parthenogenetic embryos. Cloning Stem Cells 11, 203–8.CrossRefGoogle ScholarPubMed
Mohana Kumar, B., Jin, H.F., Kim, J.G., Song, H.J., Hong, Y., Balasubramanian, S., Choe, S.Y. & Rho, G.J. (2006). DNA methylation levels in porcine fetal fibroblasts induced by an inhibitor of methylation, 5-azacytidine. Cell Tissue Res. 325, 445–54.CrossRefGoogle ScholarPubMed
Mohana Kumar, B., Song, H.J., Cho, S.K., Balasubramanian, S., Choe, S.Y. & Rho, G.J. (2007). Effect of histone acetylation modification with sodium butyrate, a histone deacetylase inhibitor, on cell cycle, apoptosis, ploidy and gene expression in porcine fetal fibroblasts. J. Reprod. Dev. 53, 903–13.CrossRefGoogle ScholarPubMed
Murko, C., Lagger, S., Steiner, M., Seiser, C., Schoefer, C. & Pusch, O. (2010). Expression of class I histone deacetylases during chick and mouse development. Int. J. Dev. Biol. 54, 1527–37.CrossRefGoogle ScholarPubMed
Niemann, H., Carnwath, J.W., Herrmann, D., Wieczorek, G., Lemme, E., Lucas-Hahn, A. & Olek, S. (2010). DNA methylation patterns reflect epigenetic reprogramming in bovine embryos. Cell Reprogram. 12, 33–42.CrossRefGoogle ScholarPubMed
Ohgane, J., Wakayama, T., Senda, S., Yamazaki, Y., Inoue, K., Ogura, A., Marh, J., Tanaka, S., Yanagimachi, R. & Shiota, K. (2004). The Sall3 locus is an epigenetic hotspot of aberrant DNA methylation associated with placentomegaly of cloned mice. Genes Cells 9, 253–60.CrossRefGoogle ScholarPubMed
Okano, M., Bell, D.W., Haber, D.A. & Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247–57.CrossRefGoogle Scholar
Pradhan, S. & Esteve, P.O. (2003). Mammalian DNA (cytosine-5) methyltransferases and their expression. Clin. Immunol. 109, 6–16.CrossRefGoogle ScholarPubMed
Primeau, M., Gagnon, J. & Momparler, R.L. (2003). Synergistic antineoplastic action of DNA methylation inhibitor 5-aza-2′-deoxycytidine and histone deacetylase inhibitor depsipeptide on human breast carcinoma cells. Int. J. Cancer 103, 177–84.CrossRefGoogle ScholarPubMed
Sambucetti, L.C., Fischer, D.D., Zabludoff, S., Kwon, P.O., Chamberlin, H., Trogani, N., Xu, H. & Cohen, D. (1999). Histone deacetylase inhibition selectively alters the activity and expression of cell cycle proteins leading to specific chromatin acetylation and antiproliferative effects. J. Biol. Chem. 274, 34940–7.CrossRefGoogle ScholarPubMed
Shaker, S., Bernstein, M., Momparler, L.F. & Momparler, R.L. (2003). Preclinical evaluation of antineoplastic activity of inhibitors of DNA methylation (5-aza-2′-deoxycytidine) and histone deacetylation (trichostatin A, depsipeptide) in combination against myeloid leukemic cells. Leuk. Res. 27, 437–44.CrossRefGoogle ScholarPubMed
Simonsson, S. & Gurdon, J. (2004). DNA demethylation is necessary for the epigenetic reprogramming of somatic cell nuclei. Nat. Cell Biol. 6, 984–90.CrossRefGoogle ScholarPubMed
Tsuji, Y., Kato, Y. & Tsunoda, Y. (2009). The developmental potential of mouse somatic cell nuclear-transferred oocytes treated with trichostatin A and 5-aza-2′-deoxycytidine. Zygote 17, 109–15.CrossRefGoogle Scholar
Wang, Y., Su, J., Wang, L., Xu, W., Quan, F., Liu, J. & Zhang, Y. (2011a). The effects of 5-Aza-2′-deoxycytidine and trichostatin A on gene expression and DNA methylation status in cloned bovine blastocysts. Cell Reprogram. 13, 297–306.CrossRefGoogle ScholarPubMed
Wang, Y.S., Xiong, X.R., An, Z.X., Wang, L.J., Liu, J., Quan, F.S., Hua, S. & Zhang, Y. (2011b). Production of cloned calves by combination treatment of both donor cells and early cloned embryos with 5-aza-2′-deoxycytidine and trichostatin A. Theriogenology 75, 819–25.CrossRefGoogle ScholarPubMed
Wee, G., Shim, J.J., Koo, D.B., Chae, J.I., Lee, K.K. & Han, Y.M. (2007). Epigenetic alteration of the donor cells does not recapitulate the reprogramming of DNA methylation in cloned embryos. Reproduction 134, 781–7.CrossRefGoogle Scholar
Wrenzycki, C., Herrmann, D., Gebert, C., Carnwath, J.W. & Niemann, H. (2006). Gene expression and methylation patterns in cloned embryos. Methods Mol. Biol. 348, 285–304.CrossRefGoogle ScholarPubMed
Wu, X., Li, Y., Li, G.P., Yang, D., Yue, Y., Wang, L., Li, K., Xin, P., Bou, S. & Yu, H. (2008). Trichostatin A improved epigenetic modifications of transfected cells but did not improve subsequent cloned embryo development. Anim. Biotechnol. 19, 211–24.CrossRefGoogle Scholar
Yamagata, K. (2008). Capturing epigenetic dynamics during pre-implantation development using live cell imaging. J. Biochem. 143, 279–86.CrossRefGoogle ScholarPubMed
Zhang, Y., Li, J., Villemoes, K., Pedersen, A.M., Purup, S. & Vajta, G. (2007). An epigenetic modifier results in improved in vitro blastocyst production after somatic cell nuclear transfer. Cloning Stem Cells 9, 357–63.CrossRefGoogle ScholarPubMed
Zhao, J., Hao, Y., Ross, J.W., Spate, L.D., Walters, E.M., Samuel, M.S., Rieke, A., Murphy, C.N. & Prather, R.S. (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