Synergistic Mechanisms of DNA Demethylation during Transition to Ground-State Pluripotency
Pluripotent stem cells (PSCs) occupy a spectrum of reversible molecular states ranging from a naive ground-state in 2i, to metastable embryonic stem cells (ESCs) in serum, to lineage-primed epiblast stem cells (EpiSCs). To investigate the role of DNA methylation (5mC) across distinct pluripotent sta...
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| Published in | Stem cell reports Vol. 1; no. 6; pp. 518 - 531 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
17.12.2013
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2213-6711 2213-6711 |
| DOI | 10.1016/j.stemcr.2013.11.010 |
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| Abstract | Pluripotent stem cells (PSCs) occupy a spectrum of reversible molecular states ranging from a naive ground-state in 2i, to metastable embryonic stem cells (ESCs) in serum, to lineage-primed epiblast stem cells (EpiSCs). To investigate the role of DNA methylation (5mC) across distinct pluripotent states, we mapped genome-wide 5mC and 5-hydroxymethycytosine (5hmC) in multiple PSCs. Ground-state ESCs exhibit an altered distribution of 5mC and 5hmC at regulatory elements and dramatically lower absolute levels relative to ESCs in serum. By contrast, EpiSCs exhibit increased promoter 5mC coupled with reduced 5hmC, which contributes to their developmental restriction. Switch to 2i triggers rapid onset of both the ground-state gene expression program and global DNA demethylation. Mechanistically, repression of de novo methylases by PRDM14 drives DNA demethylation at slow kinetics, whereas TET1/TET2-mediated 5hmC conversion enhances both the rate and extent of hypomethylation. These processes thus act synergistically during transition to ground-state pluripotency to promote a robust hypomethylated state.
[Display omitted]
•Distinct genome-wide 5mC and 5hmC profiles in diverse pluripotent stem cells•Poised enhancers and promoters are enriched in 5hmC in ESCs in serum, but not 2i•Prdm14 overexpression in serum ESCs promotes partial demethylation at slow kinetics•Mutations in Tet1/Tet2 partially block DNA hypomethylation in ground-state cells
Pluripotent stem cells (PSCs) can give rise to all embryonic lineages. Hackett, Surani, and colleagues analyzed the epigenetic landscape of PSCs in distinct but interchangeable pluripotent “states” and found they are associated with discrete 5mC and 5hmC profiles at regulatory elements and genome wide. Notably, ground-state PSCs are globally hypomethylated via the synergistic effects of PRDM14-dependent repression of Dnmt3 genes and TET-mediated 5hmC conversion. |
|---|---|
| AbstractList | Pluripotent stem cells (PSCs) occupy a spectrum of reversible molecular states ranging from a naive ground-state in 2i, to metastable embryonic stem cells (ESCs) in serum, to lineage-primed epiblast stem cells (EpiSCs). To investigate the role of DNA methylation (5mC) across distinct pluripotent states, we mapped genome-wide 5mC and 5-hydroxymethycytosine (5hmC) in multiple PSCs. Ground-state ESCs exhibit an altered distribution of 5mC and 5hmC at regulatory elements and dramatically lower absolute levels relative to ESCs in serum. By contrast, EpiSCs exhibit increased promoter 5mC coupled with reduced 5hmC, which contributes to their developmental restriction. Switch to 2i triggers rapid onset of both the ground-state gene expression program and global DNA demethylation. Mechanistically, repression of de novo methylases by PRDM14 drives DNA demethylation at slow kinetics, whereas TET1/TET2-mediated 5hmC conversion enhances both the rate and extent of hypomethylation. These processes thus act synergistically during transition to ground-state pluripotency to promote a robust hypomethylated state.
•
Distinct genome-wide 5mC and 5hmC profiles in diverse pluripotent stem cells
•
Poised enhancers and promoters are enriched in 5hmC in ESCs in serum, but not 2i
•
Prdm14
overexpression in serum ESCs promotes partial demethylation at slow kinetics
•
Mutations in
Tet1
/
Tet2
partially block DNA hypomethylation in ground-state cells
Pluripotent stem cells (PSCs) can give rise to all embryonic lineages. Hackett, Surani, and colleagues analyzed the epigenetic landscape of PSCs in distinct but interchangeable pluripotent “states” and found they are associated with discrete 5mC and 5hmC profiles at regulatory elements and genome wide. Notably, ground-state PSCs are globally hypomethylated via the synergistic effects of PRDM14-dependent repression of
Dnmt3
genes and TET-mediated 5hmC conversion. Pluripotent stem cells (PSCs) occupy a spectrum of reversible molecular states ranging from a naive ground-state in 2i, to metastable embryonic stem cells (ESCs) in serum, to lineage-primed epiblast stem cells (EpiSCs). To investigate the role of DNA methylation (5mC) across distinct pluripotent states, we mapped genome-wide 5mC and 5-hydroxymethycytosine (5hmC) in multiple PSCs. Ground-state ESCs exhibit an altered distribution of 5mC and 5hmC at regulatory elements and dramatically lower absolute levels relative to ESCs in serum. By contrast, EpiSCs exhibit increased promoter 5mC coupled with reduced 5hmC, which contributes to their developmental restriction. Switch to 2i triggers rapid onset of both the ground-state gene expression program and global DNA demethylation. Mechanistically, repression of de novo methylases by PRDM14 drives DNA demethylation at slow kinetics, whereas TET1/TET2-mediated 5hmC conversion enhances both the rate and extent of hypomethylation. These processes thus act synergistically during transition to ground-state pluripotency to promote a robust hypomethylated state.Pluripotent stem cells (PSCs) occupy a spectrum of reversible molecular states ranging from a naive ground-state in 2i, to metastable embryonic stem cells (ESCs) in serum, to lineage-primed epiblast stem cells (EpiSCs). To investigate the role of DNA methylation (5mC) across distinct pluripotent states, we mapped genome-wide 5mC and 5-hydroxymethycytosine (5hmC) in multiple PSCs. Ground-state ESCs exhibit an altered distribution of 5mC and 5hmC at regulatory elements and dramatically lower absolute levels relative to ESCs in serum. By contrast, EpiSCs exhibit increased promoter 5mC coupled with reduced 5hmC, which contributes to their developmental restriction. Switch to 2i triggers rapid onset of both the ground-state gene expression program and global DNA demethylation. Mechanistically, repression of de novo methylases by PRDM14 drives DNA demethylation at slow kinetics, whereas TET1/TET2-mediated 5hmC conversion enhances both the rate and extent of hypomethylation. These processes thus act synergistically during transition to ground-state pluripotency to promote a robust hypomethylated state. Pluripotent stem cells (PSCs) occupy a spectrum of reversible molecular states ranging from a naive ground-state in 2i, to metastable embryonic stem cells (ESCs) in serum, to lineage-primed epiblast stem cells (EpiSCs). To investigate the role of DNA methylation (5mC) across distinct pluripotent states, we mapped genome-wide 5mC and 5-hydroxymethycytosine (5hmC) in multiple PSCs. Ground-state ESCs exhibit an altered distribution of 5mC and 5hmC at regulatory elements and dramatically lower absolute levels relative to ESCs in serum. By contrast, EpiSCs exhibit increased promoter 5mC coupled with reduced 5hmC, which contributes to their developmental restriction. Switch to 2i triggers rapid onset of both the ground-state gene expression program and global DNA demethylation. Mechanistically, repression of de novo methylases by PRDM14 drives DNA demethylation at slow kinetics, whereas TET1/TET2-mediated 5hmC conversion enhances both the rate and extent of hypomethylation. These processes thus act synergistically during transition to ground-state pluripotency to promote a robust hypomethylated state. [Display omitted] •Distinct genome-wide 5mC and 5hmC profiles in diverse pluripotent stem cells•Poised enhancers and promoters are enriched in 5hmC in ESCs in serum, but not 2i•Prdm14 overexpression in serum ESCs promotes partial demethylation at slow kinetics•Mutations in Tet1/Tet2 partially block DNA hypomethylation in ground-state cells Pluripotent stem cells (PSCs) can give rise to all embryonic lineages. Hackett, Surani, and colleagues analyzed the epigenetic landscape of PSCs in distinct but interchangeable pluripotent “states” and found they are associated with discrete 5mC and 5hmC profiles at regulatory elements and genome wide. Notably, ground-state PSCs are globally hypomethylated via the synergistic effects of PRDM14-dependent repression of Dnmt3 genes and TET-mediated 5hmC conversion. Pluripotent stem cells (PSCs) occupy a spectrum of reversible molecular states ranging from a naive ground-state in 2i, to metastable embryonic stem cells (ESCs) in serum, to lineage-primed epiblast stem cells (EpiSCs). To investigate the role of DNA methylation (5mC) across distinct pluripotent states, we mapped genome-wide 5mC and 5-hydroxymethycytosine (5hmC) in multiple PSCs. Ground-state ESCs exhibit an altered distribution of 5mC and 5hmC at regulatory elements and dramatically lower absolute levels relative to ESCs in serum. By contrast, EpiSCs exhibit increased promoter 5mC coupled with reduced 5hmC, which contributes to their developmental restriction. Switch to 2i triggers rapid onset of both the ground-state gene expression program and global DNA demethylation. Mechanistically, repression of de novo methylases by PRDM14 drives DNA demethylation at slow kinetics, whereas TET1/TET2-mediated 5hmC conversion enhances both the rate and extent of hypomethylation. These processes thus act synergistically during transition to ground-state pluripotency to promote a robust hypomethylated state. |
| Author | Hackett, Jamie A. Dietmann, Sabine Leitch, Harry G. Murakami, Kazuhiro Surani, M. Azim Down, Thomas A. |
| AuthorAffiliation | 1 Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK 2 Wellcome Trust/MRC Stem Cell Institute, University of Cambridge, Cambridge CB2 1QR, UK 3 Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, UK |
| AuthorAffiliation_xml | – name: 1 Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK – name: 3 Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge CB2 3EG, UK – name: 2 Wellcome Trust/MRC Stem Cell Institute, University of Cambridge, Cambridge CB2 1QR, UK |
| Author_xml | – sequence: 1 givenname: Jamie A. surname: Hackett fullname: Hackett, Jamie A. email: j.hackett@gurdon.cam.ac.uk organization: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK – sequence: 2 givenname: Sabine surname: Dietmann fullname: Dietmann, Sabine organization: Wellcome Trust/MRC Stem Cell Institute, University of Cambridge, Cambridge CB2 1QR, UK – sequence: 3 givenname: Kazuhiro surname: Murakami fullname: Murakami, Kazuhiro organization: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK – sequence: 4 givenname: Thomas A. surname: Down fullname: Down, Thomas A. organization: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK – sequence: 5 givenname: Harry G. surname: Leitch fullname: Leitch, Harry G. organization: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK – sequence: 6 givenname: M. Azim surname: Surani fullname: Surani, M. Azim email: a.surani@gurdon.cam.ac.uk organization: Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24371807$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Animals Cell Culture Techniques Cell Differentiation - genetics DNA Methylation DNA-Binding Proteins - genetics Embryonic Stem Cells Female Gene Knockout Techniques Genomic Imprinting Male Mice Pluripotent Stem Cells - cytology Proto-Oncogene Proteins - genetics |
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| Title | Synergistic Mechanisms of DNA Demethylation during Transition to Ground-State Pluripotency |
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