bESC from cloned embryos do not retain transcriptomic or epigenetic memory from somatic donor cells

in Reproduction
Authors:
M Navarro Instituto de Investigaciones Biotecnológicas ‘Dr Rodolfo Ugalde’, UNSAM-CONICET, Buenos Aires, Argentina
Department of Animal Science, University of California, Davis, California, USA

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M M Halstead Department of Animal Science, University of California, Davis, California, USA

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Gonzalo Rincon Zoetis, Inc., Kalamazoo, Michigan, USA

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A A Mutto Instituto de Investigaciones Biotecnológicas ‘Dr Rodolfo Ugalde’, UNSAM-CONICET, Buenos Aires, Argentina

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P J Ross Department of Animal Science, University of California, Davis, California, USA

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https://orcid.org/0000-0002-3972-3754

Correspondence should be addressed to P J Ross; Email: pross@ucdavis.edu
DOI:
https://doi.org/10.1530/REP-22-0063
Volume/Issue:
Volume 164: Issue 5
Page Range:
243–257
Article Type:
Research Article
Online Publication Date:
12 Oct 2022
Copyright:
© Society for Reproduction and Fertility 2022
Restricted access
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In brief

Epigenetic reprogramming after mammalian somatic cell nuclear transfer is often incomplete, resulting in low efficiency of cloning. However, gene expression and histone modification analysis indicated high similarities in transcriptome and epigenomes of bovine embryonic stem cells from in vitro fertilized and somatic cell nuclear transfer embryos.

Abstract

Embryonic stem cells (ESC) indefinitely maintain the pluripotent state of the blastocyst epiblast. Stem cells are invaluable for studying development and lineage commitment, and in livestock, they constitute a useful tool for genomic improvement and in vitro breeding programs. Although these cells have been recently derived from bovine blastocysts, a detailed characterization of their molecular state is lacking. Here, we apply cutting-edge technologies to analyze the transcriptomic and epigenomic landscape of bovine ESC (bESC) obtained from in vitro fertilized (IVF) and somatic cell nuclear transfer (SCNT) embryos. bESC were efficiently derived from SCNT and IVF embryos and expressed pluripotency markers while retaining genome stability. Transcriptome analysis revealed that only 46 genes were differentially expressed between IVF- and SCNT-derived bESC, which did not reflect significant deviation in cellular function. Interrogating histone 3 lysine 4 trimethylation, histone 3 lysine 9 trimethylation, and histone 3 lysine 27 trimethylation with cleavage under targets and tagmentation, we found that the epigenomes of both bESC groups were virtually indistinguishable. Minor epigenetic differences were randomly distributed throughout the genome and were not associated with differentially expressed or developmentally important genes. Finally, the categorization of genomic regions according to their combined histone mark signal demonstrated that all bESC shared the same epigenomic signatures, especially at gene promoters. Overall, we conclude that bESC derived from SCNT and IVF embryos are transcriptomically and epigenetically analogous, allowing for the production of an unlimited source of pluripotent cells from high genetic merit organisms without resorting to transgene-based techniques.

Supplementary Materials

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Print ISSN:
1470-1626
Online ISSN:
1741-7899

  • Azuara V, Perry P, Sauer S, Spivakov M, Jørgensen HF, John RM, Gouti M, Casanova M, Warnes G & Merkenschlager M et al.2006 Chromatin signatures of pluripotent cell lines. Nature Cell Biology 8 532–538. (https://doi.org/10.1038/ncb1403)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bao X, Wu H, Zhu X, Guo X, Hutchins AP, Luo Z, Song H, Chen Y, Lai K & Yin M et al.2015 The p53-induced lincRNA-p21 derails somatic cell reprogramming by sustaining H3K9me3 and CpG methylation at pluripotency gene promoters. Cell Research 25 80–92. (https://doi.org/10.1038/cr.2014.165)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Bogliotti YS, Wu J, Vilarino M, Okamura D, Soto DA, Zhong C, Sakurai M, Sampaio RV, Suzuki K & Izpisua Belmonte JC et al.2018 Efficient derivation of stable primed pluripotent embryonic stem cells from bovine blastocysts. PNAS 115 2090–2095. (https://doi.org/10.1073/pnas.1716161115)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Brambrink T, Hochedlinger K, Bell G & Jaenisch R 2006 ES cells derived from cloned and fertilized blastocysts are transcriptionally and functionally indistinguishable. PNAS 103 933–938. (https://doi.org/10.1073/pnas.0510485103)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Byrne JA, Pedersen DA, Clepper LL, Nelson M, Sanger WG, Gokhale S, Wolf DP & Mitalipov SM 2007 Producing primate embryonic stem cells by somatic cell nuclear transfer. Nature 450 497–502. (https://doi.org/10.1038/nature06357)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Choi KH, Lee DK, Kim SW, Woo SH, Kim DY & Lee CK 2019 Chemically defined media can maintain pig pluripotency network in vitro. Stem Cell Reports 13 221–234. (https://doi.org/10.1016/j.stemcr.2019.05.028)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chung YG, Eum JH, Lee JE, Shim SH, Sepilian V, Hong SW, Lee Y, Treff NR, Choi YH & Kimbrel EA et al.2014 Human somatic cell nuclear transfer using adult cells. Cell Stem Cell 14 777–780. (https://doi.org/10.1016/j.stem.2014.03.015)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Chung YG, Matoba S, Liu Y, Eum JH, Lu F, Jiang W, Lee JE, Sepilian V, Cha KY & Lee DR et al.2015 Histone demethylase expression enhances human somatic cell nuclear transfer efficiency and promotes derivation of pluripotent stem cells. Cell Stem Cell 17 758–766. (https://doi.org/10.1016/j.stem.2015.10.001)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Constant F, Guillomot M, Heyman Y, Vignon X, Laigre P, Servely JL, Renard JP & Chavatte-Palmer P 2006 Large offspring or large placenta syndrome? Morphometric analysis of late gestation bovine placentomes from somatic nuclear transfer pregnancies complicated by hydrallantois. Biology of Reproduction 75 122–130. (https://doi.org/10.1095/biolreprod.106.051581)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Cowan CA, Atienza J, Melton DA & Eggan K 2005 Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science 309 1369–1373. (https://doi.org/10.1126/science.1116447)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Evans MJ & Kaufman MH 1981 Establishment in culture of pluripotential cells.pdf. Nature 292 154–156. (https://doi.org/10.1038/292154a0)

  • Gao X, Nowak-Imialek M, Chen X, Chen D, Herrmann D, Ruan D, Chen ACH, Eckersley-Maslin MA, Ahmad S & Lee YL et al.2019 Establishment of porcine and human expanded potential stem cells. Nature Cell Biology 21 687–699. (https://doi.org/10.1038/s41556-019-0333-2)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gerri C, McCarthy A, Alanis-Lobato G, Demtschenko A, Bruneau A, Loubersac S, Fogarty NME, Hampshire D, Elder K & Snell P et al.2020 Initiation of a conserved trophectoderm program in human, cow and mouse embryos. Nature 587 443–447. (https://doi.org/10.1038/s41586-020-2759-x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Goszczynski DE, Cheng H, Demyda-Peyrás S, Medrano JF, Wu J & Ross PJ 2019 In vitro breeding: application of embryonic stem cells to animal production. Biology of Reproduction 100 885–895. (https://doi.org/10.1093/biolre/ioy256)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Gunne-Braden A, Sullivan A, Gharibi B, Sheriff RSM, Maity A, Wang YF, Edwards A, Jiang M, Howell M & Goldstone R et al.2020 GATA3 mediates a fast, irreversible commitment to BMP4-driven differentiation in human embryonic stem cells. Cell Stem Cell 26 693 .e9–706.e9. (https://doi.org/10.1016/j.stem.2020.03.005)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hawkins RD, Hon GC, Lee LK, Ngo Q, Lister R, Pelizzola M, Edsall LE, Kuan S, Luu Y & Klugman S et al.2010 Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 6 479–491. (https://doi.org/10.1016/j.stem.2010.03.018)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Hu MS, Januszyk M, Hong WX, Walmsley GG, Zielins ER, Atashroo DA, Maan ZN, McArdle A, Takanishi DM & Gurtner GC et al.2014 Gene expression in fetal murine keratinocytes and fibroblasts. Journal of Surgical Research 190 344–357. (https://doi.org/10.1016/j.jss.2014.02.030)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Huan Y, Wang H, Wu Z, Zhang J, Zhu J, Liu Z & He H 2015 Epigenetic modification of cloned embryos improves Nanog reprogramming in pigs. Cellular Reprogramming 17 191–198. (https://doi.org/10.1089/cell.2014.0103)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • International Stem Cell Initiative, Adewumi O, Aflatoonian B, Ahrlund-Richter L, Amit M, Andrews PW, Beighton G, Bello PA, Benvenisty N & Berry LS et al.2007 Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nature Biotechnology 25 803–816. (https://doi.org/10.1038/nbt1318)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ju JY, Park CY, Gupta MK, Uhm SJ, Paik EC, Ryoo ZY, Cho YH, Chung KS & Lee HT 2008 Establishment of stem cell lines from nuclear transferred and parthenogenetically activated mouse oocytes for therapeutic cloning. Fertility and Sterility 89 (Supplement) 1314–1323. (https://doi.org/10.1016/j.fertnstert.2006.11.203)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kaufman MH, Robertson EJ, Handyside AH & Evans MJ 1983 Establishment of pluripotential cell lines from haploid mouse embryos. Journal of Embryology and Experimental Morphology 73 249–261. (https://doi.org/10.1242/dev.73.1.249)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kaya-Okur HS, Wu SJ, Codomo CA, Pledger ES, Bryson TD, Henikoff JG, Ahmad K & Henikoff S 2019 CUT&Tag for efficient epigenomic profiling of small samples and single cells. Nature Communications 10 1930. (https://doi.org/10.1038/s41467-019-09982-5)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Kishigami S, Wakayama S, van Thuan N & Wakayama T 2006 Cloned mice and embryonic stem cell establishment from adult somatic cells. Human Cell 19 2–10. (https://doi.org/10.1111/j.1749-0774.2005.00001.x)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lin T, Chao C, Saito S, Mazur SJ, Murphy ME, Appella E & Xu Y 2005 p53 induces differentiation of mouse embryonic stem cells by suppressing Nanog expression. Nature Cell Biology 7 165–171. (https://doi.org/10.1038/ncb1211)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Lin G, Ouyang Q, Zhou X, Gu Y, Yuan D, Li W, Liu G, Liu T & Lu G 2007 A highly homozygous and parthenogenetic human embryonic stem cell line derived from a one-pronuclear oocyte following in vitro fertilization procedure. Cell Research 17 999–1007. (https://doi.org/10.1038/cr.2007.97)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Liu X, Wang Y, Gao Y, Su J, Zhang J, Xing X, Zhou C, Yao K, An Q & Zhang Y 2018 H3K9 demethylase KDM4E is an epigenetic regulator for bovine embryonic development and a defective factor for nuclear reprogramming. Development 145 dev158261. (https://doi.org/10.1242/dev.158261)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ma H, Morey R, O’Neil RC, He Y, Daughtry B, Schultz MD, Hariharan M, Nery JR, Castanon R & Sabatini K et al.2014 Abnormalities in human pluripotent cells due to reprogramming mechanisms. Nature 511 177–183. (https://doi.org/10.1038/nature13551)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ma PJ, Zhang H, Li R, Wang YS, Zhang Y & Hua S 2015 P53-mediated repression of the reprogramming in cloned bovine embryos through direct interaction with HDAC1 and indirect interaction with DNMT3A. Reproduction in Domestic Animals 50 400–409. (https://doi.org/10.1111/rda.12502)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Mai Q, Yu Y, Li T, Wang L, Chen MJ, Huang SZ, Zhou C & Zhou Q 2007 Derivation of human embryonic stem cell lines from parthenogenetic blastocysts. Cell Research 17 1008–1019. (https://doi.org/10.1038/cr.2007.102)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Martin GR 1981 Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. PNAS 78 7634–7638. (https://doi.org/10.1073/pnas.78.12.7634)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Matoba S & Zhang Y 2018 Somatic cell nuclear transfer reprogramming: mechanisms and applications. Cell Stem Cell 23 471–485. (https://doi.org/10.1016/j.stem.2018.06.018)

  • Matoba S, Liu Y, Lu F, Iwabuchi KA, Shen L, Inoue A & Zhang Y 2014 Embryonic development following somatic cell nuclear transfer impeded by persisting histone methylation. Cell 159 884–895. (https://doi.org/10.1016/j.cell.2014.09.055)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Matoba S, Wang H, Jiang L, Lu F, Iwabuchi KA, Wu X, Inoue K, Yang L, Press W & Lee JT et al.2018 Loss of H3K27me3 imprinting in somatic cell nuclear transfer embryos disrupts post-implantation development. Cell Stem Cell 23 343 .e5–354.e5. (https://doi.org/10.1016/j.stem.2018.06.008)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Min B, Cho S, Park JS, Lee YG, Kim N & Kang YK 2015 Transcriptomic features of bovine blastocysts derived by somatic cell nuclear transfer. G3 5 2527–2538. (https://doi.org/10.1534/g3.115.020016)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Munsie MJ, Michalska AE, O’Brien CM, Trounson AO, Pera MF & Mountford PS 2000 Isolation of pluripotent embryonic stem cells from reprogrammed adult mouse somatic cell nuclei. Current Biology 10 989–992. (https://doi.org/10.1016/s0960-9822(0000648-5)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Navarro M, Soto DA, Pinzon CA, Wu J & Ross PJ 2019 Livestock pluripotency is finally captured in vitro. Reproduction, Fertility, and Development 32 11–39. (https://doi.org/10.1071/RD19272)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Nishibuchi G & Déjardin J 2017 The molecular basis of the organization of repetitive DNA-containing constitutive heterochromatin in mammals. Chromosome Research 25 77–87. (https://doi.org/10.1007/s10577-016-9547-3)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Noggle S, Fung HL, Gore A, Martinez H, Satriani KC, Prosser R, Oum K, Paull D, Druckenmiller S & Freeby M et al.2011 Human oocytes reprogram somatic cells to a pluripotent state. Nature 478 70–75. (https://doi.org/10.1038/nature10397)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Peters AHFM, Kubicek S, Mechtler K, O’Sullivan RJ, Derijck AAHA, Perez-Burgos L, Kohlmaier A, Opravil S, Tachibana M & Shinkai Y et al.2003 Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Molecular Cell 12 1577–1589. (https://doi.org/10.1016/s1097-2765(0300477-5)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Qin H, Yu T, Qing T, Liu Y, Zhao Y, Cai J, Li J, Song Z, Qu X & Zhou P et al.2007 Regulation of apoptosis and differentiation by p53 in human embryonic stem cells. Journal of Biological Chemistry 282 5842–5852. (https://doi.org/10.1074/jbc.M610464200)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Revazova ES, Turovets NA, Kochetkova OD, Kindarova LB, Kuzmichev LN, Janus JD & Pryzhkova MV 2007 Patient-specific stem cell lines derived from human parthenogenetic blastocysts. Cloning and Stem Cells 9 432–449. (https://doi.org/10.1089/clo.2007.0033)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rideout WM, Hochedlinger K, Kyba M, Daley GQ & Jaenisch R 2002 Correction of a genetic defect by nuclear transplantation and combined cell and gene therapy. Cell 109 17–27. (https://doi.org/10.1016/s0092-8674(0200681-5)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Roadmap Epigenomics Consortium, Kundaje A, Meuleman W, Ernst J, Bilenky M, Yen A, Heravi-Moussavi A, Kheradpour P, Zhang Z & Wang J et al.2015 Integrative analysis of 111 reference human epigenomes. Nature 518 317–330. (https://doi.org/10.1038/nature14248)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Robertson EJ, Evans MJ & Kaufman MH 1983 X-chromosome instability in pluripotential stem cell lines derived from parthenogenetic embryos. Journal of Embryology and Experimental Morphology 74 297–309. (https://doi.org/10.1242/dev.74.1.297)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Rodriguez-Osorio N, Urrego R, Cibelli JB, Eilertsen K & Memili E 2012 Reprogramming mammalian somatic cells. Theriogenology 78 1869–1886. (https://doi.org/10.1016/j.theriogenology.2012.05.030)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Ross PJ & Cibelli JB 2010 Bovine somatic cell nuclear transfer. Methods in Molecular Biology 636 155–177. (https://doi.org/10.1007/978-1-60761-691-7_10)

  • Rouhani F, Kumasaka N, de Brito MC, Bradley A, Vallier L & Gaffney D 2014 Genetic background drives transcriptional variation in human induced pluripotent stem cells. PLoS Genetics 10 e1004432. (https://doi.org/10.1371/journal.pgen.1004432)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Soto DA, Navarro M, Zheng C, Halstead MM, Zhou C, Guiltinan C, Wu J & Ross PJ 2021 Simplification of culture conditions and feeder-free expansion of bovine embryonic stem cells. Scientific Reports 11 11045. (https://doi.org/10.1038/s41598-021-90422-0)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Sparman M, Dighe V, Sritanaudomchai H, Ma H, Ramsey C, Pedersen D, Clepper L, Nighot P, Wolf D & Hennebold J et al.2009 Epigenetic reprogramming by somatic cell nuclear transfer in primates. Stem Cells 27 1255–1264. (https://doi.org/10.1002/stem.60)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tachibana M, Amato P, Sparman M, Gutierrez NM, Tippner-Hedges R, Ma H, Kang E, Fulati A, Lee HS & Sritanaudomchai H et al.2013 Human embryonic stem cells derived by somatic cell nuclear transfer. Cell 153 1228–1238. (https://doi.org/10.1016/j.cell.2013.05.006)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tada M, Tada T, Lefebvre L, Barton SC & Surani MA 1997 Embryonic germ cells induce epigenetic reprogramming of somatic nucleus in hybrid cells. EMBO Journal 16 6510–6520. (https://doi.org/10.1093/emboj/16.21.6510)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tada M, Takahama Y, Abe K, Nakatsuji N & Tada T 2001 Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Current Biology 11 1553–1558. (https://doi.org/10.1016/s0960-9822(0100459-6)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tada M, Morizane A, Kimura H, Kawasaki H, Ainscough JFX, Sasai Y, Nakatsuji N & Tada T 2003 Pluripotency of reprogrammed somatic genomes in embryonic stem hybrid cells. Developmental Dynamics 227 504–510. (https://doi.org/10.1002/dvdy.10337)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Taranger CK, Noer A, Sørensen AL, Håkelien AM, Boquest AC & Collas P 2005 Induction of dedifferentiation, genomewide transcriptional programming, and epigenetic reprogramming by extracts of carcinoma and embryonic stem cells. Molecular Biology of the Cell 16 5719–5735. (https://doi.org/10.1091/mbc.e05-06-0572)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Thomson JA, Kalishman J, Golos TG, Durning M, Harris CP, Becker RA & Hearn JP 1995 Isolation of a primate embryonic stem cell line. PNAS 9 2 7844–7848.

  • Thomson JA, ItsKovitz-Eldor J, Shapiro SS, Waknitz MA, Swierhiel JJ, Marshall VS & Jones JM 1998 Embryonic stem cell lines derived from human blastocysts. Science 282 1145–1147. (https://doi.org/10.1126/science.282.5391.1145)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Tian XC, Kubota C, Enright B & Yang X 2003 Cloning animals by somatic cell nuclear transfer-biological factors. Reproductive Biology and Endocrinology 1 98. (https://doi.org/10.1186/1477-7827-1-98)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Vilarino M, Alba Soto D, Soledad Bogliotti Y, Yu L, Zhang Y, Wang C, Paulson E, Zhong C, Jin M & Carlos Izpisua Belmonte J et al.2020 Derivation of sheep embryonic stem cells under optimized conditions. Reproduction 160 761–772. (https://doi.org/10.1530/REP-19-0606)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Voigt P, Tee WW & Reinberg D 2013 A double take on bivalent promoters. Genes and Development 27 1318–1338. (https://doi.org/10.1101/gad.219626.113)

  • Wakayama T, Tabar V, Rodriguez I, Perry ACF, Studer L & Mombaerts P 2001 Differentiation of embryonic stem cell lines generated from adult somatic cells by nuclear transfer. Science 292 740–743. (https://doi.org/10.1126/science.1059399)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Wakayama S, Jakt ML, Suzuki M, Araki R, Hikichi T, Kishigami S, Ohta H, Van Thuan N, Mizutani E & Sakaide Y et al.2006 Equivalency of nuclear transfer-derived embryonic stem cells to those derived from fertilized mouse blastocysts. Stem Cells 24 2023–2033. (https://doi.org/10.1634/stemcells.2005-0537)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Xiao L, Ma L, Wang Z, Yu Y, Lye SJ, Shan Y & Wei Y 2020 Deciphering a distinct regulatory network of TEAD4, CDX2 and GATA3 in humans for trophoblast transition from embryonic stem cells. Biochimica et Biophysica Acta: Molecular Cell Research 1867 118736. (https://doi.org/10.1016/j.bbamcr.2020.118736)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Xie B, Zhang H, Wei R, Li Q, Weng X, Kong Q & Liu Z 2016 Histone H3 lysine 27 trimethylation acts as an epigenetic barrier in porcine nuclear reprogramming. Reproduction 151 9–16. (https://doi.org/10.1530/REP-15-0338)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhang S, Chen X, Wang F, An X, Tang B, Zhang X, Sun L & Li Z 2016 Aberrant DNA methylation reprogramming in bovine SCNT preimplantation embryos. Scientific Reports 6 30345. (https://doi.org/10.1038/srep30345)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhang Z, Zhai Y, Ma X, Zhang S, An X, Yu H & Li Z 2018 Down-regulation of H3K4me3 by MM-102 facilitates epigenetic reprogramming of porcine somatic cell nuclear transfer embryos. Cellular Physiology and Biochemistry 45 1529–1540. (https://doi.org/10.1159/000487579)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhao MT, Chen H, Liu Q, Shao NY, Sayed N, Wo HT, Zhang JZ, Ong SG, Liu C & Kim Y et al.2017 Molecular and functional resemblance of differentiated cells derived from isogenic human iPSCs and SCNT-derived ESCs. PNAS 114 E11111–E11120. (https://doi.org/10.1073/pnas.1708991114)

    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhou C, Wang Y, Zhang J, Su J, An Q, Liu X, Zhang M, Wang Y, Liu J & Zhang Y 2019 H3K27me3 is an epigenetic barrier while KDM6A overexpression improves nuclear reprogramming efficiency. FASEB Journal 33 4638–4652. (https://doi.org/10.1096/fj.201801887R)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

  • Zhou C, Zhang J, Zhang M, Wang D, Ma Y, Wang Y, Wang Y, Huang Y & Zhang Y 2020 Transcriptional memory inherited from donor cells is a developmental defect of bovine cloned embryos. FASEB Journal 34 1637–1651. (https://doi.org/10.1096/fj.201900578RR)

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation