Islet cells share promoter hypomethylation independently of expression, but exhibit cell-type-specific methylation in enhancers

Proc Natl Acad Sci U S A. 2017 Dec 19;114(51):13525-13530. doi: 10.1073/pnas.1713736114. Epub 2017 Dec 4.

Abstract

DNA methylation at promoters is an important determinant of gene expression. Earlier studies suggested that the insulin gene promoter is uniquely unmethylated in insulin-expressing pancreatic β-cells, providing a classic example of this paradigm. Here we show that islet cells expressing insulin, glucagon, or somatostatin share a lack of methylation at the promoters of the insulin and glucagon genes. This is achieved by rapid demethylation of the insulin and glucagon gene promoters during differentiation of Neurogenin3+ embryonic endocrine progenitors, regardless of the specific endocrine cell-type chosen. Similar methylation dynamics were observed in transgenic mice containing a human insulin promoter fragment, pointing to the responsible cis element. Whole-methylome comparison of human α- and β-cells revealed generality of the findings: genes active in one cell type and silent in the other tend to share demethylated promoters, while methylation differences between α- and β-cells are concentrated in enhancers. These findings suggest an epigenetic basis for the observed plastic identity of islet cell types, and have implications for β-cell reprogramming in diabetes and diagnosis of β-cell death using methylation patterns of circulating DNA.

Keywords: DNA methylation; development; epigenetic; islets; β-cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Differentiation
  • Cell Line
  • Cells, Cultured
  • DNA Methylation*
  • Enhancer Elements, Genetic*
  • Epigenesis, Genetic
  • Glucagon-Secreting Cells / cytology
  • Glucagon-Secreting Cells / metabolism*
  • Humans
  • Insulin-Secreting Cells / cytology
  • Insulin-Secreting Cells / metabolism*
  • Mice
  • Mice, Inbred ICR
  • Promoter Regions, Genetic*