Transcription induces context-dependent remodeling of chromatin architecture during differentiation

PLoS Biol. 2023 Dec 4;21(12):e3002424. doi: 10.1371/journal.pbio.3002424. eCollection 2023 Dec.

Abstract

Metazoan chromosomes are organized into discrete spatial domains (TADs), believed to contribute to the regulation of transcriptional programs. Despite extensive correlation between domain organization and gene activity, a direct mechanistic link is unclear, with perturbation studies often showing little effect. To follow chromatin architecture changes during development, we used Capture Hi-C to interrogate the domains around key differentially expressed genes during mouse thymocyte maturation, uncovering specific remodeling events. Notably, one TAD boundary was broadened to accommodate RNA polymerase elongation past the border, and subdomains were formed around some activated genes without changes in CTCF binding. The ectopic induction of some genes was sufficient to recapitulate domain formation in embryonic stem cells, providing strong evidence that transcription can directly remodel chromatin structure. These results suggest that transcriptional processes drive complex chromosome folding patterns that can be important in certain genomic contexts.

MeSH terms

  • Animals
  • CCCTC-Binding Factor / genetics
  • Cell Differentiation / genetics
  • Chromatin Assembly and Disassembly
  • Chromatin* / genetics
  • Chromosomes* / metabolism
  • Genome
  • Mice
  • Transcription, Genetic

Substances

  • Chromatin
  • CCCTC-Binding Factor

Grants and funding

Work in the TS lab was supported by funds from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (Starting Grant 678624 - CHROMTOPOLOGY), the ATIP-Avenir program, and the grant ANR-10-LABX-0030-INRT, a French State fund managed by the Agence Nationale de la Recherche under the frame program Investissements d’Avenir ANR-10-IDEX-0002-02. YBZ was additionally supported by la Region Grand Est. Work in the DJ lab was supported by funding from Agence Nationale de la Recherche (ANR-18-CE12-0006-03; ANR-18-CE45-0022-01). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.