Nutrient regulation of the islet epigenome controls adaptive insulin secretion

J Clin Invest. 2023 Apr 17;133(8):e165208. doi: 10.1172/JCI165208.

Abstract

Adaptation of the islet β cell insulin-secretory response to changing insulin demand is critical for blood glucose homeostasis, yet the mechanisms underlying this adaptation are unknown. Here, we have shown that nutrient-stimulated histone acetylation plays a key role in adapting insulin secretion through regulation of genes involved in β cell nutrient sensing and metabolism. Nutrient regulation of the epigenome occurred at sites occupied by the chromatin-modifying enzyme lysine-specific demethylase 1 (Lsd1) in islets. β Cell-specific deletion of Lsd1 led to insulin hypersecretion, aberrant expression of nutrient-response genes, and histone hyperacetylation. Islets from mice adapted to chronically increased insulin demand exhibited shared epigenetic and transcriptional changes. Moreover, we found that genetic variants associated with type 2 diabetes were enriched at LSD1-bound sites in human islets, suggesting that interpretation of nutrient signals is genetically determined and clinically relevant. Overall, these studies revealed that adaptive insulin secretion involves Lsd1-mediated coupling of nutrient state to regulation of the islet epigenome.

Keywords: Diabetes; Endocrinology; Epigenetics; Islet cells; Metabolism.

Publication types

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

MeSH terms

  • Animals
  • Diabetes Mellitus, Type 2* / genetics
  • Diabetes Mellitus, Type 2* / metabolism
  • Epigenome
  • Glucose / metabolism
  • Histones / genetics
  • Histones / metabolism
  • Humans
  • Insulin / metabolism
  • Insulin Secretion / genetics
  • Insulin-Secreting Cells* / metabolism
  • Islets of Langerhans* / metabolism
  • Mice

Substances

  • Histones
  • Insulin
  • Glucose