Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity

Nature. 2007 Sep 13;449(7159):228-32. doi: 10.1038/nature06098. Epub 2007 Aug 29.

Abstract

A subset of neurons in the brain, known as 'glucose-excited' neurons, depolarize and increase their firing rate in response to increases in extracellular glucose. Similar to insulin secretion by pancreatic beta-cells, glucose excitation of neurons is driven by ATP-mediated closure of ATP-sensitive potassium (K(ATP)) channels. Although beta-cell-like glucose sensing in neurons is well established, its physiological relevance and contribution to disease states such as type 2 diabetes remain unknown. To address these issues, we disrupted glucose sensing in glucose-excited pro-opiomelanocortin (POMC) neurons via transgenic expression of a mutant Kir6.2 subunit (encoded by the Kcnj11 gene) that prevents ATP-mediated closure of K(ATP) channels. Here we show that this genetic manipulation impaired the whole-body response to a systemic glucose load, demonstrating a role for glucose sensing by POMC neurons in the overall physiological control of blood glucose. We also found that glucose sensing by POMC neurons became defective in obese mice on a high-fat diet, suggesting that loss of glucose sensing by neurons has a role in the development of type 2 diabetes. The mechanism for obesity-induced loss of glucose sensing in POMC neurons involves uncoupling protein 2 (UCP2), a mitochondrial protein that impairs glucose-stimulated ATP production. UCP2 negatively regulates glucose sensing in POMC neurons. We found that genetic deletion of Ucp2 prevents obesity-induced loss of glucose sensing, and that acute pharmacological inhibition of UCP2 reverses loss of glucose sensing. We conclude that obesity-induced, UCP2-mediated loss of glucose sensing in glucose-excited neurons might have a pathogenic role in the development of type 2 diabetes.

Publication types

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

MeSH terms

  • Adenosine Triphosphate / biosynthesis
  • Adenosine Triphosphate / metabolism
  • Animals
  • Diabetes Mellitus, Type 2 / metabolism
  • Diabetes Mellitus, Type 2 / physiopathology
  • Dietary Fats / administration & dosage
  • Dietary Fats / pharmacology
  • Glucose / metabolism*
  • Homeostasis*
  • Humans
  • Ion Channels / antagonists & inhibitors
  • Ion Channels / genetics
  • Ion Channels / metabolism
  • Iridoid Glycosides
  • Iridoids / pharmacology
  • Mice
  • Mice, Obese
  • Mice, Transgenic
  • Mitochondrial Proteins / antagonists & inhibitors
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / metabolism
  • Neurons / drug effects
  • Neurons / metabolism*
  • Neurons / pathology
  • Obesity / chemically induced
  • Obesity / metabolism
  • Obesity / physiopathology*
  • Potassium Channels, Inwardly Rectifying / genetics
  • Potassium Channels, Inwardly Rectifying / metabolism
  • Pro-Opiomelanocortin / metabolism*
  • Uncoupling Protein 2

Substances

  • Dietary Fats
  • Ion Channels
  • Iridoid Glycosides
  • Iridoids
  • Kir6.2 channel
  • Mitochondrial Proteins
  • Potassium Channels, Inwardly Rectifying
  • UCP2 protein, human
  • Ucp2 protein, mouse
  • Uncoupling Protein 2
  • Pro-Opiomelanocortin
  • Adenosine Triphosphate
  • genipin
  • Glucose