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Long-range phasing of dynamic, tissue-specific and allele-specific regulatory elements.

Sofia Battaglia1,2,3, Kevin Dong2, Jingyi Wu1,2,3

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Summary

Targeted nanopore sequencing reveals gene regulatory element interactions and phasing on long DNA molecules. This method uncovers primate-specific features at the H19/IGF2 locus, including a mechanism overriding imprinting in human cells.

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Area of Science:

  • Genomics
  • Epigenetics
  • Molecular Biology

Background:

  • Epigenomic maps use chromatin state to identify gene regulatory elements.
  • Short-read sequencing has limitations in distinguishing alleles, evaluating element interdependence, and capturing single-molecule dynamics.

Purpose of the Study:

  • To apply targeted nanopore sequencing for profiling chromatin accessibility and DNA methylation on long DNA molecules (~100 kb).
  • To investigate gene regulatory element relationships and phasing across developmental, immune, and imprinting loci.

Main Methods:

  • Targeted nanopore sequencing of contiguous ~100-kb DNA molecules.
  • Profiling chromatin accessibility and DNA methylation using exogenous GpC methylation.
  • Analysis of regulatory element phasing and dynamics in immune loci and the H19/IGF2 locus.

Main Results:

  • Detection of promoters, enhancers, insulators, and transcription factor footprints on single molecules.
  • Inference of dynamic element relationships in immune loci and ordering of remodeling events during T cell stimulation.
  • Phasing of sequence and regulatory elements at the H19/IGF2 locus, revealing primate-specific features like a stabilizing segmental duplication and a noncanonical enhancer driving biallelic IGF2 expression.

Conclusions:

  • Targeted nanopore sequencing provides a powerful strategy for phasing gene regulatory landscapes.
  • A novel mechanism overriding IGF2 imprinting in human cells was identified, involving primate-specific genomic features.