1,504
Views
13
CrossRef citations to date
0
Altmetric
Research Paper

TET family regulates the embryonic pluripotency of porcine preimplantation embryos by maintaining the DNA methylation level of NANOG

, , , & ORCID Icon
Pages 1228-1242 | Received 14 Jan 2020, Accepted 16 Apr 2020, Published online: 13 May 2020

References

  • Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6–21.
  • Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33(Suppl):245–254.
  • Robertson KD, Wolffe AP. DNA methylation in health and disease. Nat Rev Genet. 2000;1(1):11–19.
  • Reik W. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature. 2007;447(7143):425–432.
  • Surani MA, Hayashi K, Hajkova P. Genetic and epigenetic regulators of pluripotency. Cell. 2007;128(4):747–762.
  • Dean W, Santos F, Stojkovic M, et al. Conservation of methylation reprogramming in mammalian development: aberrant reprogramming in cloned embryos. Proc Natl Acad Sci USA. 2001;98(24):13734–13738.
  • Zaitseva I, Zaitsev S, Alenina N, et al. Dynamics of DNA-demethylation in early mouse and rat embryos developed in vivo and in vitro. Mol Reprod Dev. 2007;74(10):1255–1261.
  • Park JS, Jeong YS, Shin ST, et al. Dynamic DNA methylation reprogramming: active demethylation and immediate remethylation in the male pronucleus of bovine zygotes. Dev Dyn. 2007;236(9):2523–2533.
  • Mayer W, Niveleau A, Walter J, et al. Demethylation of the zygotic paternal genome. Nature. 2000;403(6769):501–502.
  • Oswald J, Engemann S, Lane N, et al. Active demethylation of the paternal genome in the mouse zygote. Curr Biol. 2000;10(8):475–478.
  • Shen L, Inoue A, He J, et al. Tet3 and DNA replication mediate demethylation of both the maternal and paternal genomes in mouse zygotes. Cell Stem Cell. 2014;15(4):459–471.
  • Guo F, Li X, Liang D, et al. Active and passive demethylation of male and female pronuclear DNA in the mammalian zygote. Cell Stem Cell. 2014;15(4):447–459.
  • Santos F, Hendrich B, Reik W, et al. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol. 2002;241(1):172–182.
  • Santos F, Dean W. Epigenetic reprogramming during early development in mammals. Reproduction. 2004;127(6):643–651.
  • Tahiliani M, Koh KP, Shen Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science (New York, NY). 2009;324(5929):930–935.
  • Ito S, D’Alessio AC, Taranova OV, et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature. 2010;466(7310):1129–1133.
  • He YF, Li BZ, Li Z, et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science. 2011;333(6047):1303–1307.
  • Maiti A, Drohat AC. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J Biol Chem. 2011;286(41):35334–35338.
  • Gu TP, Guo F, Yang H, et al. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature. 2011;477(7366):606–610.
  • Iqbal K, Jin SG, Pfeifer GP, et al. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci USA. 2011;108(9):3642–3647.
  • Koh KP, Yabuuchi A, Rao S, et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell. 2011;8(2):200–213.
  • Dawlaty MM, Ganz K, Powell BE, et al. Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell. 2011;9(2):166–175.
  • Quivoron C, Couronne L, Della Valle V, et al. TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell. 2011;20(1):25–38.
  • Ko M, Bandukwala HS, An J, et al. Ten-Eleven-Translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice. Proc Natl Acad Sci USA. 2011;108(35):14566–14571.
  • Dawlaty MM, Breiling A, Le T, et al. Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev Cell. 2013;24(3):310–323.
  • Dawlaty MM, Breiling A, Le T, et al. Loss of tet enzymes compromises proper differentiation of embryonic stem cells. Dev Cell. 2014;29(1):102–111.
  • Kang YK, Koo DB, Park JS, et al. Typical demethylation events in cloned pig embryos. Clues on species-specific differences in epigenetic reprogramming of a cloned donor genome. J Biol Chem. 2001;276(43):39980–39984.
  • Archer GS, Dindot S, Friend TH, et al. Hierarchical phenotypic and epigenetic variation in cloned swine. Biol Reprod. 2003;69(2):430–436.
  • Huang Y, Chavez L, Chang X, et al. Distinct roles of the methylcytosine oxidases Tet1 and Tet2 in mouse embryonic stem cells. Proc Natl Acad Sci USA. 2014;111(4):1361–1366.
  • Williams K, Christensen J, Helin K. DNA methylation: TET proteins-guardians of CpG islands? EMBO Rep. 2011;13(1):28–35.
  • Yamagata K, Yamazaki T, Miki H, et al. Centromeric DNA hypomethylation as an epigenetic signature discriminates between germ and somatic cell lineages. Dev Biol. 2007;312(1):419–426.
  • Pastor WA, Pape UJ, Huang Y, et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature. 2011;473(7347):394–397.
  • Ficz G, Branco MR, Seisenberger S, et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature. 2011;473(7347):398–402.
  • Wu H, D’Alessio AC, Ito S, et al. Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature. 2011;473(7347):389–393.
  • Freudenberg JM, Ghosh S, Lackford BL, et al. Acute depletion of Tet1-dependent 5-hydroxymethylcytosine levels impairs LIF/Stat3 signaling and results in loss of embryonic stem cell identity. Nucleic Acids Res. 2012;40(8):3364–3377.
  • Williams K, Christensen J, Pedersen MT, et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature. 2011;473(7347):343–348.
  • Kang J, Lienhard M, Pastor WA, et al. Simultaneous deletion of the methylcytosine oxidases Tet1 and Tet3 increases transcriptome variability in early embryogenesis. Proc Natl Acad Sci USA. 2015;112(31):E4236–45.
  • Shi FT, Kim H, Lu W, et al. Ten-eleven translocation 1 (Tet1) is regulated by O-linked N-acetylglucosamine transferase (Ogt) for target gene repression in mouse embryonic stem cells. J Biol Chem. 2013;288(29):20776–20784.
  • Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci. 2006;31(2):89–97.
  • Lu F, Liu Y, Jiang L, et al. Role of Tet proteins in enhancer activity and telomere elongation. Genes Dev. 2014;28(19):2103–2119.
  • Lee K, Hamm J, Whitworth K, et al. Dynamics of TET family expression in porcine preimplantation embryos is related to zygotic genome activation and required for the maintenance of NANOG. Dev Biol. 2014;386(1):86–95.
  • Prasad P, Mittal SA, Chongtham J, et al. Hypoxia-mediated epigenetic regulation of stemness in brain tumor cells. Stem Cells. 2017;35(6):1468–1478.
  • Festuccia N, Osorno R, Halbritter F, et al. Esrrb is a direct Nanog target gene that can substitute for Nanog function in pluripotent cells. Cell Stem Cell. 2012;11(4):477–490.
  • Kuijk EW, Du Puy L, Van Tol HT, et al. Differences in early lineage segregation between mammals. Dev Dyn. 2008;237(4):918–927.
  • Hall VJ, Christensen J, Gao Y, et al. Porcine pluripotency cell signaling develops from the inner cell mass to the epiblast during early development. Dev Dyn. 2009;238(8):2014–2024.
  • Du Puy L, Lopes SM, Haagsman HP, et al. Analysis of co-expression of OCT4, NANOG and SOX2 in pluripotent cells of the porcine embryo, in vivo and in vitro. Theriogenology. 2011;75(3):513–526.
  • Lei S, Ryu J, Wen K, et al. Increased and prolonged human norovirus infection in RAG2/IL2RG deficient gnotobiotic pigs with severe combined immunodeficiency. Sci Rep. 2016;6:25222.
  • Yugo DM, Heffron CL, Ryu J, et al. Infection dynamics of hepatitis E virus in wild-type and immunoglobulin heavy chain knockout JH (-/-) gnotobiotic piglets. J Virol. 2018;92(21). DOI:10.1128/JVI.01208-18.
  • Whitworth KM, Lee K, Benne JA, et al. Use of the CRISPR/Cas9 system to produce genetically engineered pigs from in vitro-derived oocytes and embryos. Biol Reprod. 2014;91(3):78.
  • Santos F, Hyslop L, Stojkovic P, et al. Evaluation of epigenetic marks in human embryos derived from IVF and ICSI. Hum Reprod. 2010;25(9):2387–2395.
  • Deshmukh RS, Ostrup O, Ostrup E, et al. DNA methylation in porcine preimplantation embryos developed in vivo and produced by in vitro fertilization, parthenogenetic activation and somatic cell nuclear transfer. Epigenetics. 2011;6(2):177–187.
  • Fulka J, Fulka H, Slavik T, et al. DNA methylation pattern in pig in vivo produced embryos. Histochem Cell Biol. 2006;126(2):213–217.
  • Braude P, Bolton V, Moore S. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature. 1988;332(6163):459–461.
  • Prather RS. Nuclear control of early embryonic development in domestic pigs. J Reprod Fertil Suppl. 1993;48:17–29.
  • Yoshioka K, Suzuki C, Tanaka A, et al. Birth of piglets derived from porcine zygotes cultured in a chemically defined medium. Biol Reprod. 2002;66(1):112–119.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.