Beta-cell uncoupling protein 2 regulates reactive oxygen species production, which influences both insulin and glucagon secretion

Diabetes. 2011 Nov;60(11):2710-9. doi: 10.2337/db11-0132. Epub 2011 Oct 7.

Abstract

Objective: The role of uncoupling protein 2 (UCP2) in pancreatic β-cells is highly debated, partly because of the broad tissue distribution of UCP2 and thus limitations of whole-body UCP2 knockout mouse models. To investigate the function of UCP2 in the β-cell, β-cell-specific UCP2 knockout mice (UCP2BKO) were generated and characterized.

Research design and methods: UCP2BKO mice were generated by crossing loxUCP2 mice with mice expressing rat insulin promoter-driven Cre recombinase. Several in vitro and in vivo parameters were measured, including respiration rate, mitochondrial membrane potential, islet ATP content, reactive oxygen species (ROS) levels, glucose-stimulated insulin secretion (GSIS), glucagon secretion, glucose and insulin tolerance, and plasma hormone levels.

Results: UCP2BKO β-cells displayed mildly increased glucose-induced mitochondrial membrane hyperpolarization but unchanged rates of uncoupled respiration and islet ATP content. UCP2BKO islets had elevated intracellular ROS levels that associated with enhanced GSIS. Surprisingly, UCP2BKO mice were glucose-intolerant, showing greater α-cell area, higher islet glucagon content, and aberrant ROS-dependent glucagon secretion under high glucose conditions.

Conclusions: Using a novel β-cell-specific UCP2KO mouse model, we have shed light on UCP2 function in primary β-cells. UCP2 does not behave as a classical metabolic uncoupler in the β-cell, but has a more prominent role in the regulation of intracellular ROS levels that contribute to GSIS amplification. In addition, β-cell UCP2 contributes to the regulation of intraislet ROS signals that mediate changes in α-cell morphology and glucagon secretion.

Publication types

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

MeSH terms

  • Animals
  • Genes, Reporter
  • Glucagon / metabolism*
  • Glucagon-Secreting Cells / metabolism*
  • Glucagon-Secreting Cells / pathology
  • Glucose Intolerance / genetics
  • Glucose Intolerance / metabolism
  • Glucose Intolerance / pathology
  • Humans
  • Hyperglycemia / metabolism
  • Insulin / genetics
  • Insulin / metabolism*
  • Insulin Secretion
  • Insulin-Secreting Cells / metabolism*
  • Insulin-Secreting Cells / pathology
  • Ion Channels / genetics
  • Ion Channels / physiology*
  • Islets of Langerhans / metabolism
  • Islets of Langerhans / pathology
  • Male
  • Membrane Potential, Mitochondrial
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mitochondrial Proteins / genetics
  • Mitochondrial Proteins / physiology*
  • Organ Specificity
  • Promoter Regions, Genetic
  • Rats
  • Reactive Oxygen Species / metabolism*
  • Tissue Culture Techniques
  • Uncoupling Protein 2

Substances

  • Insulin
  • Ion Channels
  • Mitochondrial Proteins
  • Reactive Oxygen Species
  • UCP2 protein, human
  • Ucp2 protein, mouse
  • Ucp2 protein, rat
  • Uncoupling Protein 2
  • Glucagon