A novel high-throughput assay for islet respiration reveals uncoupling of rodent and human islets

PLoS One. 2012;7(5):e33023. doi: 10.1371/journal.pone.0033023. Epub 2012 May 14.

Abstract

Background: The pancreatic beta cell is unique in its response to nutrient by increased fuel oxidation. Recent studies have demonstrated that oxygen consumption rate (OCR) may be a valuable predictor of islet quality and long term nutrient responsiveness. To date, high-throughput and user-friendly assays for islet respiration are lacking. The aim of this study was to develop such an assay and to examine bioenergetic efficiency of rodent and human islets.

Methodology/principal findings: The XF24 respirometer platform was adapted to islets by the development of a 24-well plate specifically designed to confine islets. The islet plate generated data with low inter-well variability and enabled stable measurement of oxygen consumption for hours. The F1F0 ATP synthase blocker oligomycin was used to assess uncoupling while rotenone together with myxothiazol/antimycin was used to measure the level of non-mitochondrial respiration. The use of oligomycin in islets was validated by reversing its effect in the presence of the uncoupler FCCP. Respiratory leak averaged to 59% and 49% of basal OCR in islets from C57Bl6/J and FVB/N mice, respectively. In comparison, respiratory leak of INS-1 cells and C2C12 myotubes was measured to 38% and 23% respectively. Islets from a cohort of human donors showed a respiratory leak of 38%, significantly lower than mouse islets.

Conclusions/significance: The assay for islet respiration presented here provides a novel tool that can be used to study islet mitochondrial function in a relatively high-throughput manner. The data obtained in this study shows that rodent islets are less bioenergetically efficient than human islets as well as INS1 cells.

Publication types

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

MeSH terms

  • Adult
  • Animals
  • Carbonyl Cyanide p-Trifluoromethoxyphenylhydrazone / pharmacology
  • Cell Line
  • Cell Respiration / drug effects
  • Cell Respiration / physiology
  • Diabetes Mellitus, Type 2 / metabolism
  • Female
  • High-Throughput Screening Assays / methods
  • Humans
  • In Vitro Techniques
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / metabolism
  • Islets of Langerhans / drug effects
  • Islets of Langerhans / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Oligomycins / pharmacology
  • Oxygen Consumption / drug effects
  • Oxygen Consumption / physiology
  • Species Specificity
  • Uncoupling Agents / pharmacology
  • Young Adult

Substances

  • Oligomycins
  • Uncoupling Agents
  • Carbonyl Cyanide p-Trifluoromethoxyphenylhydrazone