Fatty acid ethyl esters cause pancreatic calcium toxicity via inositol trisphosphate receptors and loss of ATP synthesis

Gastroenterology. 2006 Mar;130(3):781-93. doi: 10.1053/j.gastro.2005.12.031.

Abstract

Background & aims: Fatty acid ethyl esters are ethanol metabolites inducing sustained, toxic elevations of the acinar cytosolic free calcium ion concentration ([Ca(2+)](C)) implicated in pancreatitis. We sought to define the mechanisms of this elevation.

Methods: Isolated mouse pancreatic acinar cells were loaded with fluorescent dyes for confocal microscopy to measure [Ca(2+)](C) (Fluo 4, Fura Red), endoplasmic reticulum calcium ion concentration ([Ca(2+)](ER), Mg Fluo 4), mitochondrial membrane potential (TMRM), ADP:ATP ratio (Mg Green), and NADH autofluorescence in response to palmitoleic acid ethyl ester and palmitoleic acid (10-100 micromol/L). Whole-cell patch clamp was used to measure the calcium-activated chloride current and apply ethanol metabolites and/or ATP intracellularly.

Results: Intracellular delivery of ester induced oscillatory increases of [Ca(2+)](C) and calcium-activated currents, inhibited acutely by caffeine (20 mmol/L), but not atropine, indicating involvement of inositol trisphosphate receptor channels. The stronger effect of extracellular ester or acid caused depletion of [Ca(2+)](ER), not prevented by caffeine, but associated with depleted ATP, depleted NADH autofluorescence, and depolarized mitochondria, suggesting calcium-ATPase pump failure because of lack of ATP. Intracellular ATP abolished the sustained rise in [Ca(2+)](C), although oscillatory signals persisted that were prevented by caffeine. Inhibition of ester hydrolysis markedly reduced its calcium-releasing effect and consequent toxicity.

Conclusions: Fatty acid ethyl ester increases [Ca(2+)](C) through inositol trisphosphate receptors and, following hydrolysis, through calcium-ATPase pump failure from impaired mitochondrial ATP production. Lowering cellular fatty acid substrate concentrations may reduce cell injury in pancreatitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / biosynthesis*
  • Animals
  • Caffeine / pharmacology
  • Calcium / metabolism*
  • Calcium Channels / physiology*
  • Calcium Signaling
  • Calcium-Transporting ATPases / metabolism
  • Endoplasmic Reticulum / metabolism
  • Ethanol / metabolism*
  • Ethanol / toxicity
  • Fatty Acids / metabolism
  • Fatty Acids / toxicity*
  • Inositol 1,4,5-Trisphosphate Receptors
  • Mice
  • Mitochondria / metabolism
  • Pancreas / drug effects*
  • Pancreatitis, Alcoholic / metabolism
  • Pancreatitis, Alcoholic / prevention & control
  • Receptors, Cytoplasmic and Nuclear / physiology*

Substances

  • Calcium Channels
  • Fatty Acids
  • Inositol 1,4,5-Trisphosphate Receptors
  • Receptors, Cytoplasmic and Nuclear
  • Caffeine
  • Ethanol
  • Adenosine Triphosphate
  • Calcium-Transporting ATPases
  • Calcium