Cited by 206Epigenetics and DNA MethylationGenetic Syndromes and ImprintingGenomics and Chromatin Dynamics

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Epigenetic restriction of extraembryonic lineages mirrors the somatic transition to cancer

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Smith, Zachary D., Shi, Jiantao, Gu, Hongcang, Donaghey, Julie, Clement, Kendell, Cacchiarelli, Davide, Gnirke, Andreas, Michor, Franziska, Meissner, Alexander·2017·Nature

DOI 10.1038/nature23891PMC PMC5789792

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Abstract

In mammals, the canonical somatic DNA methylation landscape is established upon specification of the embryo proper and subsequently disrupted within many cancer types. However, the underlying mechanisms that direct this genome-scale transformation remain elusive, with no clear model for its systematic acquisition or potential developmental utility. Here, we analysed global remethylation from the mouse preimplantation embryo into the early epiblast and extraembryonic ectoderm. We show that these two states acquire highly divergent genomic distributions with substantial disruption of bimodal, CpG density-dependent methylation in the placental progenitor. The extraembryonic epigenome includes specific de novo methylation at hundreds of embryonically protected CpG island promoters, particularly those that are associated with key developmental regulators and are orthologously methylated across most human cancer types. Our data suggest that the evolutionary innovation of extraembryonic tissues may have required co-option of DNA methylation-based suppression as an alternative to regulation by Polycomb-group proteins, which coordinate embryonic germ-layer formation in response to extraembryonic cues. Moreover, we establish that this decision is made deterministically, downstream of promiscuously used-and frequently oncogenic-signalling pathways, via a novel combination of epigenetic cofactors. Methylation of developmental gene promoters during tumorigenesis may therefore reflect the misappropriation of an innate trajectory and the spontaneous reacquisition of a latent, developmentally encoded epigenetic landscape.

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Additional file 5 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
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Additional file 2 of Association of expression of epigenetic molecular factors with DNA methylation and sensitivity to chemotherapeutic agents in cancer cell lines
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Additional file 4 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558393
Additional file 6 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558399
Additional file 2 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558387
Additional file 21 of Association of expression of epigenetic molecular factors with DNA methylation and sensitivity to chemotherapeutic agents in cancer cell lines
Vural, S., Palmisano, A., Reinhold, W. C., Pommier, Y., Teicher, B. A., & Krushkal, J. (2021) · Figshare · doi:10.6084/m9.figshare.14176024
Additional file 1 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558384
Additional file 2 of Single-cell multi-omics profiling links dynamic DNA methylation to cell fate decisions during mouse early organogenesis
Clark, S. J., Argelaguet, R., Lohoff, T., Krueger, F., Drage, D., Göttgens, B., Marioni, J. C., Nichols, J., & Reik, W. (2022) · Figshare · doi:10.6084/m9.figshare.21211318
Additional file 12 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558417
Additional file 3 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558390
Additional file 9 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558408
Additional file 11 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558414
Additional file 1 of Association of expression of epigenetic molecular factors with DNA methylation and sensitivity to chemotherapeutic agents in cancer cell lines
Vural, S., Palmisano, A., Reinhold, W. C., Pommier, Y., Teicher, B. A., & Krushkal, J. (2021) · Figshare · doi:10.6084/m9.figshare.14176018
Additional file 8 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558405
Additional file 16 of Association of expression of epigenetic molecular factors with DNA methylation and sensitivity to chemotherapeutic agents in cancer cell lines
Vural, S., Palmisano, A., Reinhold, W. C., Pommier, Y., Teicher, B. A., & Krushkal, J. (2021) · Figshare · doi:10.6084/m9.figshare.14176006
Additional file 20 of Association of expression of epigenetic molecular factors with DNA methylation and sensitivity to chemotherapeutic agents in cancer cell lines
Vural, S., Palmisano, A., Reinhold, W. C., Pommier, Y., Teicher, B. A., & Krushkal, J. (2021) · Figshare · doi:10.6084/m9.figshare.14176021
Additional file 7 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558402
Additional file 10 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558411
Additional file 19 of Association of expression of epigenetic molecular factors with DNA methylation and sensitivity to chemotherapeutic agents in cancer cell lines
Vural, S., Palmisano, A., Reinhold, W. C., Pommier, Y., Teicher, B. A., & Krushkal, J. (2021) · Figshare · doi:10.6084/m9.figshare.14176015
Additional file 13 of DNA methylation in human gastric epithelial cells defines regional identity without restricting lineage plasticity
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2024) · Figshare · doi:10.6084/m9.figshare.26558420
Lamin A/C directs nucleosome-scale chromatin remodeling to define early lineage segregation in mammalsPreprint
Sherrard, A., Zhong, L., Hoppe, C., Gopinath, S. K., Youlten, S. E., Boswell, C. W., Cross, S., Sievers, F. E., Ardestani, G., Sakkas, D., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.01.696913
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Authors: Smith, Z. D., Shi, J., Gu, H., Donaghey, J., Clement, K., Cacchiarelli, D., Gnirke, A., Michor, F., & Meissner, A.
Affiliations: Broad Institute (US)
Harvard University (US)
Corresponding author: Meissner, Alexander
ORCID: Smith, Zachary D.
Shi, Jiantao
Gu, Hongcang
Clement, Kendell
Cacchiarelli, Davide
Gnirke, Andreas
Meissner, Alexander
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2017-09-20
Volume: 549
Issue: 7673
Pages: 543-547
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature23891
PMC: PMC5789792
OpenAlex: W2754109996
Cited by: 201
References: 67
Citations by year: 2026: 13 · 2025: 17 · 2024: 20 · 2023: 20 · 2022: 29 · 2021: 37 · 2020: 26 · 2019: 25 · 2018: 11 · 2017: 3
FWCI: 7.26
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
RePEc: Research Papers in Economics (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders: New York Stem Cell Foundation (P01GM099117, R01DA036898)
Starr Foundation (R01DA036898)
Israel Science Foundation
Max-Planck-Gesellschaft
National Institutes of Health (5rm1hg006193-10, NIH U54CA193461)
National Institute on Drug Abuse (R01DA036898)
National Human Genome Research Institute (RM1‐HG006193, P50HG006193)
National Cancer Institute (U54CA193461)
National Institute of General Medical Sciences (P01GM099117)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD078679)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords: DNA methylation, extraembryonic ectoderm, epiblast, preimplantation embryo, de novo methylation, CpG island promoters, developmental regulators, cancer epigenetics, Polycomb group proteins, mouse embryo development, carcinogenesis
MeSH terms: Animals, Blastocyst, Ectoderm, Female, Germ Layers, Humans, Male, Neoplasms, Placenta, Pregnancy, Promoter Regions, Genetic, Gene Expression Regulation, Neoplastic, Gene Expression Regulation, Developmental, CpG Islands, Cell Lineage, DNA Methylation, Epigenesis, Genetic, Mice

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Epigenetic restriction of extraembryonic lineages mirrors the somatic transition to cancer

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