Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-27T22:39:36.363Z Has data issue: false hasContentIssue false
  • English
  • Français

TRIM28 down-regulation on methylation imprints in bovine preimplantation embryos

Published online by Cambridge University Press:  23 January 2019

Xin Ma Open the ORCID record for Xin Ma [Opens in a new window] ,
Sheng Zhang ,
Meiling Zhang ,
Yiran Zhu ,
Panpan Ma ,
Shubao Yang ,
Liyan Su ,
Ziyi Li ,
Wenfa Lv  and
Weimin Luan
Xin Ma
Affiliation:
College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin, China
Sheng Zhang
Affiliation:
State & Local Joint Engineering Laboratory for Animal Models of Human Diseases, Academy of Translational Medicine, First Hospital, Jilin University, Changchun, Jilin, China
Meiling Zhang
Affiliation:
College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin, China
Yiran Zhu
Affiliation:
College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin, China
Panpan Ma
Affiliation:
College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin, China
Shubao Yang
Affiliation:
College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin, China
Liyan Su
Affiliation:
College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin, China
Ziyi Li
Affiliation:
State & Local Joint Engineering Laboratory for Animal Models of Human Diseases, Academy of Translational Medicine, First Hospital, Jilin University, Changchun, Jilin, China
Wenfa Lv
Affiliation:
College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin, China
Weimin Luan*
Affiliation:
College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin, China
*
*Author for correspondence: Weimin Luan. College of Animal Science and Technology, Jilin Agricultural University, Changchun, Jilin, China. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

TRIM28/KAP1/TIF1β was identified as a universal transcriptional co-repressor and is critical for regulating post-fertilization methylation reprogramming in preimplantation embryos. In this study, three siRNAs (si647, si742, and si1153) were designed to target the TRIM28 mRNA sequence. After transfection of the mixture of the three siRNA (siMix) into bovine fibroblast cells, the most effective one for TRIM28 knockdown was selected. By injecting RNAi directed against TRIM28 mRNA, we found that TRIM28 knockdown in oocytes had the most effect on the H19 gene, in which differentially methylated region (DMR) methylation was almost completely absent at the 2-cell stage (1.4%), while control embryos showed 74% methylation. In addition, global H3K9me3 levels at the 2-cell stage were significantly higher in the in vitro fertilization (IVF) group than in the TRIM28 knockdown group (P<0.05). We further show that TRIM28 is highly expressed during oocyte maturation and reaches peak levels at the 2-cell stage. In contrast, at this stage, TRIM28 expression in somatic cell nuclear transfer (SCNT) embryos decreased significantly (P<0.05), suggesting that Trim28 transcripts are lost during SCNT. TRIM28 is required for the maintenance of methylation imprints in bovine preimplantation embryos, and the loss of TRIM28 during SCNT may contribute to the unfaithful maintenance of imprints in cloned embryos.

Keywords

BovineImprinted geneMethylationSCNTTRIM28
Type
Research Article
Information
Zygote , Volume 26 , Issue 6 , December 2018 , pp. 449 - 456
Copyright
© Cambridge University Press 2019 

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.)

Footnotes

*

These authors contributed equally to this work.

References

Abrink, M, Ortiz, JA, Mark, C, Sanchez, C, Looman, C, Hellman, L, Chambon, P Losson, R (2001) Conserved interaction between distinct Kruppel-associated box domains and the transcriptional intermediary factor 1 beta. Proc Natl Acad Sci USA 98, 1422–1426.Google Scholar
Alexander, KA, Wang, X, Shibata, M, Clark, AG García-García, MJ (2015) TRIM28 controls genomic imprinting through distinct mechanisms during and after early genome-wide reprogramming. Cell Rep 13, 1194–1205.Google Scholar
Barlow, DP Bartolomei, MS (2014) Genomic imprinting in mammals. Cold Spring Harbor Perspec Biol 6, a018382.Google Scholar
Bartolomei, MS (2009) Genomic imprinting: employing and avoiding epigenetic processes. Genes Dev 23, 2124–2133.Google Scholar
Bunch, H, Zheng, X, Burkholder, A, Dillon, ST, Motola, S, Birrane, G, Ebmeier, CC, Levine, S, Fargo, D, Hu, G, Taatjes, DJ Calderwood, SK (2014) TRIM28 regulates RNA polymerase II promoter-proximal pausing and pause release. Nat Struct Mol Biol 21, 876–883.Google Scholar
Cammas, F, Mark, M, Dolle, P, Dierich, A, Chambon, P, Losson, R, (2000) Mice lacking the transcriptional corepressor TIF1beta are defective in early postimplantation development. Development 127, 2955–2963.Google Scholar
Chen, L, Chen, DT, Kurtyka, C, Rawal, B, Fulp, WJ, Haura, EB Cress, WD (2012) Tripartite motif containing 28 (Trim28) can regulate cell proliferation by bridging HDAC1/E2F interactions. J Biol Chem 287, 40106–40118.Google Scholar
Chikuma, S, Suita, N, Okazaki, IM, Shibayama, S Honjo, T (2012) TRIM28 prevents autoinflammatory T cell development in vivo. Nat Immunol 13, 596–603.Google Scholar
Ferguson-Smith, AC Surani, MA (2001) Imprinting and the epigenetic asymmetry between parental genomes. Science 293, 1086–1089.Google Scholar
Hamm, J, Tessanne, K, Murphy, CN Prather, RS (2014) Transcriptional regulators TRIM28, SETDB1, and TP53 are aberrantly expressed in porcine embryos produced by in vitro fertilization in comparison to in vivo- and somatic-cell nuclear transfer-derived embryos. Mol Reprod Dev 81, 552–566.Google Scholar
Ivanov, AV, Peng, H, Yurchenko, V, Yap, KL, Negorev, DG, Schultz, DC, Psulkowski, E, Fredericks, WJ, White, DE, Maul, GG, Sadofsky, MJ, Zhou, MM Rauscher, FR (2007) PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol Cell 28, 823–837.Google Scholar
Iyengar, S Farnham, PJ (2011) KAP1 protein: an enigmatic master regulator of the genome. J Biol Chem 286, 26267–26276.Google Scholar
Kono, T, Obata, Y, Wu, Q, Niwa, K, Ono, Y, Yamamoto, Y, Park, ES, Seo, JS Ogawa, H (2004) Birth of parthenogenetic mice that can develop to adulthood. Nature 428, 860–864.Google Scholar
Lee, DH, Goodarzi, AA, Adelmant, GO, Pan, Y, Jeggo, PA, Marto, JA Chowdhury, D (2012) Phosphoproteomic analysis reveals that PP4 dephosphorylates KAP-1 impacting the DNA damage response. EMBO J 31, 2403–2415.Google Scholar
Messerschmidt, DM, de Vries, W, Ito, M, Solter, D, Ferguson-Smith, A Knowles, BB (2012) Trim28 is required for epigenetic stability during mouse oocyte to embryo transition. Science 335, 1499–1502.Google Scholar
Miles, DC, de Vries, NA, Gisler, S, Lieftink, C, Akhtar, W, Gogola, E, Pawlitzky, I, Hulsman, D, Tanger, E, Koppens, M, Beijersbergen, RL van Lohuizen, M (2017) TRIM28 is an epigenetic barrier to induced pluripotent stem cell reprogramming. Stem Cells 35, 147–157.Google Scholar
O’Doherty, AM, O’Shea, LC Fair, T (2012) Bovine DNA methylation imprints are established in an oocyte size-specific manner, which are coordinated with the expression of the DNMT3 family proteins. Biol Reprod 86, 67.Google Scholar
Quenneville, S, Verde, G, Corsinotti, A, Kapopoulou, A, Jakobsson, J, Offner, S, Baglivo, I, Pedone, PV, Grimaldi, G, Riccio, A Trono, D (2011) In embryonic stem cells, ZFP57/KAP1 recognize a methylated hexanucleotide to affect chromatin and DNA methylation of imprinting control regions. Mol Cell 44, 361–372.Google Scholar
Schultz, DC, Friedman, JR Rauscher, FR (2001) Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2α subunit of NuRD. Genes Dev 15, 428–443.Google Scholar
Schultz, DC, Ayyanathan, K, Negorev, D, Maul, GG Rauscher, FR (2002) SETDB1: a novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev 16, 919–932.Google Scholar
Tao, Y, Yen, MR, Chitiashvili, T, Nakano, H, Kim, R, Hosohama, L, Yao, CT, Nakano, A,Tan, YC Clark, AT (2017) TRIM28-regulated transposon repression is required for human germline competency and not primed or naive human pluripotency. Stem Cell Reports 10, 243–256.Google Scholar
Wang, Z, ZhaoB, T, Zhang, P, Zhang, S, Guan, J, Ma, X, Yin, Y, Zhang, J, Tang, B Li, Z (2011) Histone deacetylase 1 down-regulation on developmental capability and histone acetylation in bovine oocytes and parthenogenetic embryos. Reprod Domest Anim 46, 1022–1028.Google Scholar
Wolf, D Goff, SP (2007) TRIM28 mediates primer binding site-targeted silencing of murine leukemia virus in embryonic cells. Cell 131, 46–57.Google Scholar
Zhang, S, Tang, B, Fan, C, Shi, L, Zhang, X, Sun, L Li, Z (2015) Effect of DNMT inhibitor on bovine parthenogenetic embryo development. Biochem Biophys Res Commun 466, 505–511.Google Scholar
Zhang, S, Wang, F, Fan, C, Tang, B, Zhang, X Li, Z (2016a) Dynamic changes of histone H3 lysine 9 following trimethylation in bovine oocytes and pre-implantation embryos. Biotechnol Lett 38, 395–402.Google Scholar
Zhang, S, Chen, X, Wang, F, An, X, Tang, B, Zhang, X, Sun, L Li, Z (2016b) Aberrant DNA methylation reprogramming in bovine SCNT preimplantation embryos. Sci Rep 6, 30345.Google Scholar
Zuo, X, Sheng, J, Lau, HT, McDonald, CM, Andrade, M, Cullen, DE, Bell, FT, Iacovino, M, Kyba, M, Xu, G Li, X (2012) Zinc finger protein ZFP57 requires its co-factor to recruit DNA methyltransferases and maintains DNA methylation imprint in embryonic stem cells via its transcriptional repression domain. J Biol Chem 287, 2107–2118.Google Scholar