Glucose-Sensitive CFTR Suppresses Glucagon Secretion by Potentiating KATP Channels in Pancreatic Islet α Cells

Endocrinology. 2017 Oct 1;158(10):3188-3199. doi: 10.1210/en.2017-00282.

Abstract

The secretion of glucagon by islet α cells is normally suppressed by high blood glucose, but this suppressibility is impaired in patients with diabetes or cystic fibrosis (CF), a disease caused by mutations in the gene encoding CF transmembrane conductance regulator (CFTR), a cyclic adenosine monophosphate-activated Cl- channel. However, precisely how glucose regulates glucagon release remains controversial. Here we report that elevated glucagon secretion, together with increased glucose-induced membrane depolarization and Ca2+ response, is found in CFTR mutant (DF508) mice/islets compared with the wild-type. Overexpression of CFTR in AlphaTC1-9 cells results in membrane hyperpolarization and reduced glucagon release, which can be reversed by CFTR inhibition. CFTR is found to potentiate the adenosine triphosphate-sensitive K+ (KATP) channel because membrane depolarization and whole-cell currents sensitive to KATP blockers are significantly greater in wild-type/CFTR-overexpressed α cells compared with that in DF508/non-overexpressed cells. KATP knockdown also reverses the suppressive effect of CFTR overexpression on glucagon secretion. The results reveal that by potentiating KATP channels, CFTR acts as a glucose-sensing negative regulator of glucagon secretion in α cells, a defect of which may contribute to glucose intolerance in CF and other types of diabetes.

MeSH terms

  • Animals
  • Calcium / analysis
  • Cell Line
  • Chlorides / metabolism
  • Cystic Fibrosis / complications
  • Cystic Fibrosis / genetics
  • Cystic Fibrosis Transmembrane Conductance Regulator / antagonists & inhibitors*
  • Cystic Fibrosis Transmembrane Conductance Regulator / genetics
  • Cystic Fibrosis Transmembrane Conductance Regulator / physiology*
  • Gene Expression
  • Gene Knockdown Techniques
  • Glucagon / antagonists & inhibitors
  • Glucagon / blood
  • Glucagon / metabolism*
  • Glucagon-Secreting Cells / metabolism*
  • Glucagon-Secreting Cells / physiology
  • Glucose / pharmacology*
  • Glucose Intolerance / complications
  • KATP Channels / physiology*
  • Mice
  • Mice, Mutant Strains
  • Mutation

Substances

  • Chlorides
  • KATP Channels
  • Cystic Fibrosis Transmembrane Conductance Regulator
  • Glucagon
  • Glucose
  • Calcium