Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-12-01T04:36:18.362Z Has data issue: false hasContentIssue false
  • English
  • Français

MBD1 and MeCP2 expression in embryos and placentas from transgenic cloned goats

Published online by Cambridge University Press:  03 July 2017

Ruoxin Jia ,
Guomin Zhang ,
Yixuan Fan ,
Zhengrong Zhou ,
Yongjie Wan ,
Yanli Zhang ,
Ziyu Wang  and
Feng Wang
Ruoxin Jia
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory; Jiangsu Engineering Technology Research Center of Meat Sheep and Goat Industry, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, People's Republic of China Department of Animal Husbandry and Veterinary Science, Zhejiang Academy of Agricultural Sciences, Hangzhou, Zhejiang 310021, People's Republic of China
Guomin Zhang
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory; Jiangsu Engineering Technology Research Center of Meat Sheep and Goat Industry, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, People's Republic of China
Yixuan Fan
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory; Jiangsu Engineering Technology Research Center of Meat Sheep and Goat Industry, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, People's Republic of China
Zhengrong Zhou
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory; Jiangsu Engineering Technology Research Center of Meat Sheep and Goat Industry, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, People's Republic of China
Yongjie Wan
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory; Jiangsu Engineering Technology Research Center of Meat Sheep and Goat Industry, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, People's Republic of China
Yanli Zhang*
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory, College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing, Jiangsu 210095, People's Republic of China
Ziyu Wang
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory; Jiangsu Engineering Technology Research Center of Meat Sheep and Goat Industry, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, People's Republic of China
Feng Wang
Affiliation:
Jiangsu Livestock Embryo Engineering Laboratory; Jiangsu Engineering Technology Research Center of Meat Sheep and Goat Industry, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing, Jiangsu 210095, People's Republic of China
*
All correspondence to: Yanli Zhang. Jiangsu Livestock Embryo Engineering Laboratory, College of Animal Science and Technology, Nanjing Agricultural University, Weigang 1, Nanjing, Jiangsu 210095, People's Republic of China. Tel: +86 25 84395381; Fax: +86 25 84395314. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

DNA methylation is an important form of epigenetic regulation in mammalian development. Methyl-CpG-binding domain protein 1 (MBD1) and methyl-CpG-binding domain protein 2 (MeCP2) are two members of the MBD subfamily of proteins that bind methylated CpG to maintain the silencing effect of DNA methylation. Given their important roles in linking DNA methylation with gene silencing, this study characterized the coordinated mRNA expression and protein localization of MBD1 and MeCP2 in embryos and placentas and aimed to analysis the effects of MBD1 and MeCP2 on transgenic cloned goats. Our result showed that MBD1 expression of transgenic cloned embryo increased significantly at the 2–4-cell and 8–16-cell stages (P < 0.05), then decreased at the morula and blastocyst stages (P < 0.05); MeCP2 expression in transgenic cloned embryo was significant decreased at the 2–4-cell stage and increased at the 8–16-cell stage (P < 0.05). Placenta morphology analysis showed that the cotyledon number of deceased transgenic cloned group (DTCG) was significantly lower than that the normal goats (NG) and in the live transgenic cloned goats (LTCG) (P < 0.05). MBD1 and MeCP2 were clearly detectable in the placental trophoblastic binucleate cells by immunohistochemical staining. Moreover, MBD1 and MeCP2 expression in DTCG was significant higher than in the NG and the LTCG (P < 0.05). In summary, aberrant expression of methylation CpG binding proteins MBD1 and MeCP2 was detected in embryonic and placental development, which reflected abnormal transcription regulation and DNA methylation involved in MBD1 and MeCP2. These findings have implications in understanding the low efficiency of transgenic cloning.

Keywords

EmbryoGoatMBD1MeCP2Placenta
Type
Research Article
Information
Zygote , Volume 25 , Issue 4 , August 2017 , pp. 462 - 471
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.)

References

Beaujean, N., Hartshorne, G., Cavilla, J., Taylor, J., Gardner, J., Wilmut, I., Meehan, R. & Young, L. (2004). Non-conservation of mammalian preimplantation methylation dynamics. Curr. Biol. 14, R266–7.CrossRefGoogle ScholarPubMed
Bourc'His, D., Le Bourhis, D., Patin, D., Niveleau, A., Comizzoli, P., Renard, J.-P. & Viegas-Pequignot, E. (2001). Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos. Curr. Biol. 11, 1542–6.CrossRefGoogle ScholarPubMed
Chesné, P., Adenot, P.G., Viglietta, C., Baratte, M., Boulanger, L. & Renard, J.-P. (2002). Cloned rabbits produced by nuclear transfer from adult somatic cells. Nat. Biotechnol. 20, 366–9.CrossRefGoogle ScholarPubMed
Cho, J.-H., Kimura, H., Minami, T., Ohgane, J., Hattori, N., Tanaka, S. & Shiota, K. (2001). DNA methylation regulates placental lactogen I gene expression. Endocrinology 142, 3389–96.CrossRefGoogle ScholarPubMed
Cibelli, J.B., Campbell, K.H., Seidel, G.E., West, M.D. & Lanza, R.P. (2002). The health profile of cloned animals. Nat. Biotechnol. 20, 13–4.CrossRefGoogle ScholarPubMed
Cibelli, J.B., Stice, S.L., Golueke, P.J., Kane, J.J., Jerry, J., Blackwell, C., de Leon, F.A.P. & Robl, J.M. (1998). Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science 280, 1256–8.CrossRefGoogle ScholarPubMed
De Sousa, P.A., King, T., Harkness, L., Young, L.E., Walker, S.K. & Wilmut, I. (2001). Evaluation of gestational deficiencies in cloned sheep fetuses and placentae. Biol. Reprod. 65, 23–30.CrossRefGoogle ScholarPubMed
Dean, W., Santos, F., Stojkovic, M., Zakhartchenko, V., Walter, J., Wolf, E. & Reik, W. (2001). Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc. Natl. Acad. Sci. 98, 13734–8.CrossRefGoogle ScholarPubMed
Farin, P.W., Piedrahita, J.A. & Farin, C.E. (2006). Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology 65, 178– 91.CrossRefGoogle ScholarPubMed
Fuks, F., Hurd, P.J., Wolf, D., Nan, X., Bird, A.P. & Kouzarides, T. (2003). The methyl-CpG-binding protein MeCP2 links DNA methylation to histone methylation. J. Biol. Chem. 278, 4035–40.CrossRefGoogle ScholarPubMed
Gu, P., Le Menuet, D., Chung, A.C.-K. & Cooney, A.J. (2006). Differential recruitment of methylated CpG binding domains by the orphan receptor GCNF initiates the repression and silencing of Oct4 expression. Mol. Cell. Biol. 26, 9471–83.CrossRefGoogle ScholarPubMed
Igwebuike, U. (2009). A review of uterine structural modifications that influence conceptus implantation and development in sheep and goats. Anim. Reprod. Sci. 112, 1–7.CrossRefGoogle ScholarPubMed
Jaenisch, R. & Bird, A. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33, 245–54.CrossRefGoogle ScholarPubMed
Jia, R., Zhou, Z., Zhang, G., Wang, L., Fan, Y., Wan, Y., Zhang, Y., Wang, Z. & Wang, F. (2016). Analysis of imprinted messenger RNA expression in deceased transgenic cloned goats. Genet. Mol. Res. 15, doi: 10.4238/gmr.15017455.CrossRefGoogle ScholarPubMed
Kato, Y., Tani, T., Sotomaru, Y., Kurokawa, K., Kato, J.-Y., Doguchi, H., Yasue, H. & Tsunoda, Y. (1998). Eight calves cloned from somatic cells of a single adult. Science 282, 2095–8.CrossRefGoogle ScholarPubMed
Klisch, K., Wooding, F. & Jones, C. (2010). The glycosylation pattern of secretory granules in binucleate trophoblast cells is highly conserved in ruminants. Placenta 31, 11–7.CrossRefGoogle ScholarPubMed
Klose, R.J. & Bird, A.P. (2006). Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 31, 89–97.CrossRefGoogle ScholarPubMed
Konyalı, A., Tölü, C., Daş, G. & Savaş, T. (2007). Factors affecting placental traits and relationships of placental traits with neonatal behaviour in goat. Anim. Reprod. Sci. 97, 394–401.CrossRefGoogle ScholarPubMed
Li, E., Bestor, T.H. & Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915–26.CrossRefGoogle ScholarPubMed
Li, L., Chen, B.F. & Chan, W.Y. (2015). An epigenetic regulator: methyl-CpG-binding domain protein 1 (MBD1). Internatl. J. Mol. Sci. 16, 5125–40.CrossRefGoogle ScholarPubMed
Mayer, W., Niveleau, A., Walter, J., Fundele, R. & Haaf, T. (2000). Embryogenesis: demethylation of the zygotic paternal genome. Nature 403, 501–2.CrossRefGoogle Scholar
Meng, L., Jia, R.-X., Sun, Y.-Y., Wang, Z.-Y., Wan, Y.-J., Zhang, Y.-L., Zhong, B.-S. & Wang, F. (2014). Growth regulation, imprinting, and epigenetic transcription-related gene expression differs in lung of deceased transgenic cloned and normal goats. Theriogenology 81, 459–66.CrossRefGoogle ScholarPubMed
Nan, X., Tate, P., Li, E. & Bird, A. (1996). DNA methylation specifies chromosomal localization of MeCP2. Mol. Cell. Biol. 16, 414–21.CrossRefGoogle ScholarPubMed
Osgerby, J., Gadd, T. & Wathes, D. (2003). The effects of maternal nutrition and body condition on placental and foetal growth in the ewe. Placenta 24, 236–47.CrossRefGoogle ScholarPubMed
Oswald, J., Engemann, S., Lane, N., Mayer, W., Olek, A., Fundele, R., Dean, W., Reik, W. & Walter, J. (2000). Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10, 475–8.CrossRefGoogle ScholarPubMed
Penninga, L. & Longo, L. (1998). Ovine placentome morphology: effect of high altitude, long-term hypoxia. Placenta 19, 187–93.CrossRefGoogle ScholarPubMed
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 29, e45.CrossRefGoogle ScholarPubMed
Polejaeva, I.A., Chen, S.-H., Vaught, T.D., Page, R.L., Mullins, J., Ball, S., Dai, Y., Boone, J., Walker, S. & Ayares, D.L. (2000). Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407, 86–90.CrossRefGoogle ScholarPubMed
Ruddock-D'Cruz, N.T., Xue, J., Wilson, K.J., Heffernan, C., Prashadkumar, S., Cooney, M.A., Sanchez-Partida, L.G., French, A.J. & Holland, M.K. (2008). Dynamic changes in the localization of five members of the methyl binding domain (MBD) gene family during murine and bovine preimplantation embryo development. Mol. Reprod. Dev. 75, 48–59.CrossRefGoogle ScholarPubMed
Santos, F. & Dean, W. (2004). Epigenetic reprogramming during early development in mammals. Reproduction 127, 643–51.CrossRefGoogle ScholarPubMed
Shi, S.R., Key, M.E. & Kalra, K.L. (1991). Antigen retrieval in formalin-fixed, paraffin-embedded tissues: an enhancement method for immunohistochemical staining based on microwave oven heating of tissue sections. J. Histochem. Cytochem. 39, 741–8.CrossRefGoogle ScholarPubMed
Suemizu, H., Aiba, K., Yoshikawa, T., Sharov, A.A., Shimozawa, N., Tamaoki, N. & Ko, M.S. (2003). Expression profiling of placentomegaly associated with nuclear transplantation of mouse ES cells. Dev. Biol. 253, 36–53.CrossRefGoogle ScholarPubMed
Tate, P., Skarnes, W. & Bird, A. (1996). The methyl-CpG binding protein MeCP2 is essential for embryonic development in the mouse. Nat. Genet. 12, 205–8.CrossRefGoogle ScholarPubMed
Wade, P.A. (2001). Methyl CpG binding proteins: coupling chromatin architecture to gene regulation. Oncogene 20, 3166–73.CrossRefGoogle ScholarPubMed
Wakayama, T., Perry, A.C., Zuccotti, M., Johnson, K.R. & Yanagimachi, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394, 369–74.CrossRefGoogle ScholarPubMed
Wan, Y.J., Zhang, Y.L., Zhou, Z.R., Jia, R.X., Li, M., Song, H., Wang, Z.Y., Wang, L.Z., Zhang, G.M., You, J.H. & Wang, F. (2012). Efficiency of donor cell preparation and recipient oocyte source for production of transgenic cloned dairy goats harboring human lactoferrin. Theriogenology 78, 583–92.CrossRefGoogle ScholarPubMed
Ward, J., Wooding, F. & Fowden, A. (2002). The effects of cortisol on the binucleate cell population in the ovine placenta during late gestation. Placenta 23, 451–8.CrossRefGoogle ScholarPubMed
Watanabe, S. & Nagai, T. (2009). Death losses due to stillbirth, neonatal death and diseases in cloned cattle derived from somatic cell nuclear transfer and their progeny: a result of nationwide survey in Japan. Anim. Sci. J. 80, 233–8.CrossRefGoogle ScholarPubMed
Watanabe, S. & Nagai, T. (2011). Survival of embryos and calves derived from somatic cell nuclear transfer in cattle: a nationwide survey in Japan. Anim. Sci. J. 82, 360–5.CrossRefGoogle ScholarPubMed
Wells, D.N., Misica, P.M., Day, T. & Tervit, H.R. (1997). Production of cloned lambs from an established embryonic cell line: a comparison between in vivo-and in vitro-matured cytoplasts. Biol. Reprod. 57, 385–93.CrossRefGoogle ScholarPubMed
Wells, D.N., Misica, P.M. & Tervit, H.R. (1999). Production of cloned calves following nuclear transfer with cultured adult mural granulosa cells. Biol. Reprod. 60, 996–1005.CrossRefGoogle ScholarPubMed
Wilmut, I., Schnieke, A., McWhir, J., Kind, A. & Campbell, K. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–3. Reprinted in Nussbaum, M.C. & Sunstein, C.R. (1998). Clones and Clones: Facts and Fantasies about Human Cloning, pp. 21–8. New York & London: W.W. Norton.CrossRefGoogle ScholarPubMed
Wooding, F., Morgan, G., Monaghan, S., Hamon, M. & Heap, R. (1996). Functional specialization in the ruminant placenta: evidence for two populations of fetal binucleate cells of different selective synthetic capacity. Placenta 17, 75–86.CrossRefGoogle ScholarPubMed
Wrenzycki, C., Wells, D., Herrmann, D., Miller, A., Oliver, J., Tervit, R. & Niemann, H. (2001). Nuclear transfer protocol affects messenger RNA expression patterns in cloned bovine blastocysts. Biol. Reprod. 65, 309–17.CrossRefGoogle ScholarPubMed
Yang, X., Smith, S.L., Tian, X.C., Lewin, H.A., Renard, J.P. & Wakayama, T. (2007). Nuclear reprogramming of cloned embryos and its implications for therapeutic cloning. Nat. Genet. 39, 295–302.CrossRefGoogle ScholarPubMed