Glucose Sensing by Skeletal Myocytes Couples Nutrient Signaling to Systemic Homeostasis

Mol Cell. 2017 May 4;66(3):332-344.e4. doi: 10.1016/j.molcel.2017.04.007.

Abstract

Skeletal muscle is a major site of postprandial glucose disposal. Inadequate insulin action in skeletal myocytes contributes to hyperglycemia in diabetes. Although glucose is known to stimulate insulin secretion by β cells, whether it directly engages nutrient signaling pathways in skeletal muscle to maintain systemic glucose homeostasis remains largely unexplored. Here we identified the Baf60c-Deptor-AKT pathway as a target of muscle glucose sensing that augments insulin action in skeletal myocytes. Genetic activation of this pathway improved postprandial glucose disposal in mice, whereas its muscle-specific ablation impaired insulin action and led to postprandial glucose intolerance. Mechanistically, glucose triggers KATP channel-dependent calcium signaling, which promotes HDAC5 phosphorylation and nuclear exclusion, leading to Baf60c induction and insulin-independent AKT activation. This pathway is engaged by the anti-diabetic sulfonylurea drugs to exert their full glucose-lowering effects. These findings uncover an unexpected mechanism of glucose sensing in skeletal myocytes that contributes to homeostasis and therapeutic action.

Keywords: Baf60c; Deptor; SWI/SNF; chromatin remodeling; diabetes; epigenetic; glucose sensing; insulin resistance; skeletal muscle; sulfonylurea.

MeSH terms

  • Animals
  • Blood Glucose / drug effects
  • Blood Glucose / metabolism*
  • Cell Line
  • Chromosomal Proteins, Non-Histone / genetics
  • Chromosomal Proteins, Non-Histone / metabolism
  • Energy Metabolism* / drug effects
  • Enzyme Activation
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism
  • Homeostasis
  • Humans
  • Hypoglycemic Agents / pharmacology
  • Insulin / blood
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • KATP Channels / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle Fibers, Skeletal / drug effects
  • Muscle Fibers, Skeletal / metabolism*
  • Muscle Proteins / genetics
  • Muscle Proteins / metabolism
  • Postprandial Period
  • Proto-Oncogene Proteins c-akt / metabolism
  • Signal Transduction* / drug effects
  • Sulfonylurea Compounds / pharmacology
  • Time Factors
  • Tissue Culture Techniques

Substances

  • Blood Glucose
  • Chromosomal Proteins, Non-Histone
  • Hypoglycemic Agents
  • Insulin
  • Intracellular Signaling Peptides and Proteins
  • KATP Channels
  • Muscle Proteins
  • Smarcd3 protein, mouse
  • Sulfonylurea Compounds
  • deptor protein, mouse
  • Proto-Oncogene Proteins c-akt
  • Hdac5 protein, mouse
  • Histone Deacetylases