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DNA methylation and lncRNA control asynchronous DNA replication at specific imprinted gene domains.

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Parental DNA methylation imprints and long non-coding RNA (lncRNA) Meg3 control asynchronous replication timing in imprinted domains. This epigenetic regulation overrides typical replication timing organization in mouse stem cells.

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Area of Science:

  • Epigenetics and Genomics
  • Mammalian Stem Cell Biology
  • Gene Regulation

Background:

  • While genome-wide replication timing (RT) patterns are established, some genes exhibit allelic replication asynchrony in stem cells due to stochastic events and genetic variations.
  • The role of epigenetic modifications, particularly DNA methylation imprints in mammalian imprinted domains, in controlling this asynchronous replication remains largely unexplored.

Purpose of the Study:

  • To investigate whether epigenetic modifications, specifically parental DNA methylation imprints, regulate asynchronous replication in mammalian imprinted domains.
  • To determine the influence of long non-coding RNAs (lncRNAs) and DNA methylation on replication timing and chromatin organization within these domains.

Main Methods:

  • Genome-wide and locus-specific assays were performed in mono-parental and hybrid mouse embryonic stem cells (ESCs).
  • Analysis included replication timing, DNA methylation patterns, 3D chromatin structure, and gene expression.
  • Generation of mutant mouse lines to assess the functional roles of specific genes and lncRNAs.

Main Results:

  • Pronounced, parent-of-origin-dependent replication timing asynchrony was observed at the Dlk1-Dio3 and Snrpn imprinted domains in mouse ESCs, which was lost upon neural differentiation.
  • Differential DNA methylation was identified as the mediator of asynchronous replication at the Dlk1-Dio3 domain.
  • The lncRNA Meg3 was found to control early replication on the maternal chromosome within the Dlk1-Dio3 domain; no link between replication timing and TAD organization was found.

Conclusions:

  • Parental DNA methylation imprints and lncRNA expression, exemplified by Meg3, are key regulators of replication timing asynchrony in imprinted domains.
  • These epigenetic factors can override established replication timing domain organization, demonstrating a novel layer of gene regulation.
  • The findings highlight the intricate interplay between epigenetics, lncRNA function, and DNA replication in controlling genome organization and gene expression.