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Dick W Zijlmans1, Irene Talon2, Sigrid Verhelst3

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Human naive pluripotent stem cells possess chromatin barriers, contrary to previous assumptions. Polycomb repressive complex 2 (PRC2) restricts trophoblast differentiation, revealing epigenetic restrictions in these cells.

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Area of Science:

  • Stem cell biology
  • Epigenetics
  • Developmental biology

Background:

  • Human naive pluripotent stem cells are believed to have unrestricted lineage potential due to a lack of chromatin-based barriers.
  • This assumption, however, has not been experimentally verified, leaving a gap in understanding their epigenetic regulation.

Purpose of the Study:

  • To investigate the chromatin landscape and epigenetic state of human naive and primed pluripotent stem cells.
  • To determine if chromatin-based lineage barriers exist in naive pluripotent stem cells and identify the underlying molecular mechanisms.

Main Methods:

  • Comparative analysis of the chromatin-associated proteome, histone modifications (including H3K27me3), and transcriptomes between naive and primed human pluripotent stem cells.
  • Functional assays involving Polycomb repressive complex 2 (PRC2) inhibition to assess its role in lineage restriction.
  • Analysis of human blastoids to evaluate the impact of PRC2 activity on trophoblast differentiation and development.

Main Results:

  • Integrated analysis revealed significant differences in chromatin modules between naive and primed stem cells.
  • A notable enrichment of Polycomb repressive complex 2 (PRC2)-associated H3K27me3 was identified in naive pluripotent stem cells, particularly at promoters of lineage-determining genes.
  • PRC2 activity was confirmed as a chromatin barrier restricting trophoblast lineage differentiation; its inhibition promoted trophoblast fate and blastoid cavity formation.

Conclusions:

  • Human naive pluripotent stem cells are not epigenetically unrestricted as previously thought.
  • Chromatin mechanisms, specifically PRC2-mediated H3K27 trimethylation, actively oppose the induction of alternative cell fates, such as trophoblast differentiation.
  • These findings redefine the epigenetic landscape of naive pluripotency and have implications for stem cell differentiation protocols and developmental studies.