MafA-Controlled Nicotinic Receptor Expression Is Essential for Insulin Secretion and Is Impaired in Patients with Type 2 Diabetes

Cell Rep. 2016 Mar 1;14(8):1991-2002. doi: 10.1016/j.celrep.2016.02.002. Epub 2016 Feb 18.

Abstract

Monoamine and acetylcholine neurotransmitters from the autonomic nervous system (ANS) regulate insulin secretion in pancreatic islets. The molecular mechanisms controlling neurotransmitter signaling in islet β cells and their impact on diabetes development are only partially understood. Using a glucose-intolerant, MafA-deficient mouse model, we demonstrate that MAFA controls ANS-mediated insulin secretion by activating the transcription of nicotinic (ChrnB2 and ChrnB4) and adrenergic (Adra2A) receptor genes, which are integral parts of acetylcholine- and monoamine-signaling pathways. We show that acetylcholine-mediated insulin secretion requires nicotinic signaling and that nicotinic receptor expression is positively correlated with insulin secretion and glycemic control in human donor islets. Moreover, polymorphisms spanning MAFA-binding regions within the human CHRNB4 gene are associated with type 2 diabetes. Our data show that MAFA transcriptional activity is required for establishing β cell sensitivity to neurotransmitter signaling and identify nicotinic signaling as a modulator of insulin secretion impaired in type 2 diabetes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autonomic Nervous System / metabolism
  • Binding Sites
  • Diabetes Mellitus, Experimental / genetics*
  • Diabetes Mellitus, Experimental / metabolism
  • Diabetes Mellitus, Experimental / pathology
  • Diabetes Mellitus, Type 2 / genetics*
  • Diabetes Mellitus, Type 2 / metabolism
  • Diabetes Mellitus, Type 2 / pathology
  • Female
  • Gene Expression Regulation
  • Glucose Tolerance Test
  • Humans
  • Insulin / genetics
  • Insulin / metabolism
  • Insulin-Secreting Cells / metabolism*
  • Insulin-Secreting Cells / pathology
  • Maf Transcription Factors, Large / genetics*
  • Maf Transcription Factors, Large / metabolism
  • Mice
  • Mice, Knockout
  • Nerve Tissue Proteins / genetics*
  • Nerve Tissue Proteins / metabolism
  • Polymorphism, Genetic
  • Protein Binding
  • Receptors, Adrenergic, alpha-2 / genetics*
  • Receptors, Adrenergic, alpha-2 / metabolism
  • Receptors, Nicotinic / genetics*
  • Receptors, Nicotinic / metabolism
  • Signal Transduction
  • Transcription, Genetic

Substances

  • Adra2a protein, mouse
  • Chrnb4 protein, mouse
  • Insulin
  • Maf Transcription Factors, Large
  • Mafa protein, mouse
  • Nerve Tissue Proteins
  • Receptors, Adrenergic, alpha-2
  • Receptors, Nicotinic
  • nicotinic receptor beta2