Cyclic DNA remethylation following active demethylation at euchromatic regions in mouse embryonic stem cells

DNA methylation is an essential epigenetic mark that regulates normal mammalian embryonic development. DNA methylation profiles are not always static, especially during germline development. In zygotes, DNA is typically highly methylated but, during preimplantation, DNA methylation is erased globall...

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Published inChromosome research Vol. 29; no. 2; pp. 145 - 157
Main Authors Kubiura-Ichimaru, Musashi, Ito, Takamasa, Lefebvre, Louis, Tada, Masako
Format Journal Article
LanguageEnglish
Published Dordrecht Springer Netherlands 01.06.2021
Springer Nature B.V
Subjects
Animal Genetics and Genomics
Biomedical and Life Sciences
Cell Biology
Cell cycle
Chromatin
Chromosomes
Demethylation
Deoxyribonucleic acid
DNA
DNA methylation
DNA methyltransferase
Embryo cells
Embryogenesis
Enzymes
Epigenetics
Human Genetics
Immunofluorescence
Life Sciences
Original Article
Plant Genetics and Genomics
Stem cell transplantation
Stem cells
Zygotes
5hmC
DNA methylation
chromatin
cell cycle
mouse ESCs
immunofluorescence
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Abstract DNA methylation is an essential epigenetic mark that regulates normal mammalian embryonic development. DNA methylation profiles are not always static, especially during germline development. In zygotes, DNA is typically highly methylated but, during preimplantation, DNA methylation is erased globally. Then, at the start of post-implantation development in mouse embryos, DNA again becomes dramatically hypermethylated. Chromatin structure regulates the accessibility of DNA-modifying enzymes to target DNA. Beyond that, however, our understanding of the pathway by which chromatin regulation initiates changes in global DNA methylation during mouse embryonic development remains incomplete. To analyse the relationship between global regulation of DNA methylation and chromatin status, we examined 5-methylcytosine (5mC), modified by the DNA methyltransferase DNMT, and the oxidative derivative 5-hydroxymethylation (5hmC), converted from 5mC by TET-family enzymes, by means of immunofluorescence staining of mitotic chromosomes in mouse embryonic stem cells (ESCs). Our comparison of immunostaining patterns for those epigenetic modifications in wild-type, DNMT-deficient, and TET-deficient ESCs allowed us to visualise cell cycle-mediated DNA methylation changes, especially in euchromatic regions. Our findings suggest that DNA methylation patterns in undifferentiated mouse ESCs are stochastically balanced by the opposing effects of two activities: demethylation by TET and subsequent remethylation by DNMT.
AbstractList DNA methylation is an essential epigenetic mark that regulates normal mammalian embryonic development. DNA methylation profiles are not always static, especially during germline development. In zygotes, DNA is typically highly methylated but, during preimplantation, DNA methylation is erased globally. Then, at the start of post-implantation development in mouse embryos, DNA again becomes dramatically hypermethylated. Chromatin structure regulates the accessibility of DNA-modifying enzymes to target DNA. Beyond that, however, our understanding of the pathway by which chromatin regulation initiates changes in global DNA methylation during mouse embryonic development remains incomplete. To analyse the relationship between global regulation of DNA methylation and chromatin status, we examined 5-methylcytosine (5mC), modified by the DNA methyltransferase DNMT, and the oxidative derivative 5-hydroxymethylation (5hmC), converted from 5mC by TET-family enzymes, by means of immunofluorescence staining of mitotic chromosomes in mouse embryonic stem cells (ESCs). Our comparison of immunostaining patterns for those epigenetic modifications in wild-type, DNMT-deficient, and TET-deficient ESCs allowed us to visualise cell cycle-mediated DNA methylation changes, especially in euchromatic regions. Our findings suggest that DNA methylation patterns in undifferentiated mouse ESCs are stochastically balanced by the opposing effects of two activities: demethylation by TET and subsequent remethylation by DNMT.
Author Tada, Masako
Kubiura-Ichimaru, Musashi
Ito, Takamasa
Lefebvre, Louis
Author_xml – sequence: 1
  givenname: Musashi
  surname: Kubiura-Ichimaru
  fullname: Kubiura-Ichimaru, Musashi
  organization: Stem Cells & Reprogramming Laboratory, Department of Biology, Faculty of Science, Toho University
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  givenname: Louis
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  givenname: Masako
  orcidid: 0000-0003-3641-3520
  surname: Tada
  fullname: Tada, Masako
  email: masako.tada@sci.toho-u.ac.jp
  organization: Stem Cells & Reprogramming Laboratory, Department of Biology, Faculty of Science, Toho University
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Keywords 5hmC
DNA methylation
chromatin
cell cycle
mouse ESCs
immunofluorescence
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Snippet DNA methylation is an essential epigenetic mark that regulates normal mammalian embryonic development. DNA methylation profiles are not always static,...
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SubjectTerms Animal Genetics and Genomics
Biomedical and Life Sciences
Cell Biology
Cell cycle
Chromatin
Chromosomes
Demethylation
Deoxyribonucleic acid
DNA
DNA methylation
DNA methyltransferase
Embryo cells
Embryogenesis
Enzymes
Epigenetics
Human Genetics
Immunofluorescence
Life Sciences
Original Article
Plant Genetics and Genomics
Stem cell transplantation
Stem cells
Zygotes
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Title Cyclic DNA remethylation following active demethylation at euchromatic regions in mouse embryonic stem cells
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