The Transcriptionally Permissive Chromatin State of Embryonic Stem Cells Is Acutely Tuned to Translational Output
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Abstract
A permissive chromatin environment coupled to hypertranscription drives the rapid proliferation of embryonic stem cells (ESCs) and peri-implantation embryos. We carried out a genome-wide screen to systematically dissect the regulation of the euchromatic state of ESCs. The results revealed that cellular growth pathways, most prominently translation, perpetuate the euchromatic state and hypertranscription of ESCs. Acute inhibition of translation rapidly depletes euchromatic marks in mouse ESCs and blastocysts, concurrent with delocalization of RNA polymerase II and reduction in nascent transcription. Translation inhibition promotes rewiring of chromatin accessibility, which decreases at a subset of active developmental enhancers and increases at histone genes and transposable elements. Proteome-scale analyses revealed that several euchromatin regulators are unstable proteins and continuously depend on a high translational output. We propose that this mechanistic interdependence of euchromatin, transcription, and translation sets the pace of proliferation at peri-implantation and may be employed by other stem/progenitor cells.
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Ribosomal DNA copy number is associated with body mass in humans and other mammals
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Self-citationGlobal translation during early development depends on the essential transcription factor PRDM10
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Self-citationTET activity safeguards pluripotency throughout embryonic dormancy
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A Mediator-dependent hypertranscriptional program governs neural stem cell fate decisions in vivoPreprint
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CHD1 is a synthetic lethal vulnerability in MYC-driven breast cancer
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Self-citationTranslation sustains productive Pol II elongation through maintenance of nuclear RNA surveillancePreprint
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RNAPII and XPC remodel the 3D genome for UV repairPreprint
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Nucleolus orchestrates oocyte maturation and early embryogenesis: Genetics and epigenetics
Cai, X., Tian, Y., Zhou, L., Guo, Y.-X., & Li, Q. (2026) · Genes & Diseases · doi:10.1016/j.gendis.2026.102467
TANGO6 coordinates transcription and translation through nucleocytoplasmic partitioning
Bigliani, G., Ballaré, C., Wojnacki, J., Androulaki, S., Guitart, T., Blanco, E., Foresti, O., Lujan, A., Ana, Y., Gebauer, F., et al. (2026) · Science Advances · doi:10.1126/sciadv.aef0902
- Authors
- Bulut-Karslioglu, A., Macrae, T. A., Oses-Prieto, J. A., Covarrubias, S., Percharde, M., Ku, G., Diaz, A., McManus, M. T., Burlingame, A. L., & Ramalho-Santos, M.
- Affiliations
- University of California, San Francisco (US)
- ORCID
- Venue
- Cell Stem Cell
- Publisher
- Elsevier BV
- Published
- 2018-03
- Volume
- 22
- Issue
- 3
- Pages
- 369-383.e8
- ISSN
- 1875-9777 (ISSN-L)
- 1934-5909
- PMC
- PMC5836508
- OpenAlex
- W2792650071
- Cited by
- 97
- References
- 87
- Citations by year
- 2026: 8 · 2025: 6 · 2024: 9 · 2023: 20 · 2022: 9 · 2021: 18 · 2020: 13 · 2019: 6 · 2018: 8
- FWCI
- 4.00
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell stem cell (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Shurl and Kay Curci Foundation (R01GM113014, 1F30HD093116, R 01GM123556)
- University of California, San Francisco
- National Institute of General Medical Sciences
- Diabetes Research Center (P30 DK063720)
- National Institutes of Health (5P30CA082103)
- Dr. Miriam and Sheldon G. Adelson Medical Research Foundation (U01MH105028)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- embryonic stem cells, euchromatin, chromatin accessibility, translation (biology), RNA polymerase II, nascent transcription, developmental enhancers, histone genes, transposable elements, protein stability, stem cell proliferation, peri-implantation embryo, blastocyst, genome-wide screen
- MeSH terms
- Animals, Blastocyst, Cell Differentiation, Chromatin, DNA Transposable Elements, Enhancer Elements, Genetic, Female, Male, Models, Biological, Nuclear Proteins, Transcription, Genetic, Protein Biosynthesis, Proto-Oncogene Proteins c-myc, Genome, Euchromatin, RNA Interference, Histone Code, Mice, Embryonic Stem Cells, Protein Stability, TOR Serine-Threonine Kinases
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