Insulin protects pancreatic acinar cells from palmitoleic acid-induced cellular injury

J Biol Chem. 2014 Aug 22;289(34):23582-95. doi: 10.1074/jbc.M114.589440. Epub 2014 Jul 3.

Abstract

Acute pancreatitis is a serious and sometimes fatal inflammatory disease where the pancreas digests itself. The non-oxidative ethanol metabolites palmitoleic acid (POA) and POA-ethylester (POAEE) are reported to induce pancreatitis caused by impaired mitochondrial metabolism, cytosolic Ca(2+) ([Ca(2+)]i) overload and necrosis of pancreatic acinar cells. Metabolism and [Ca(2+)]i are linked critically by the ATP-driven plasma membrane Ca(2+)-ATPase (PMCA) important for maintaining low resting [Ca(2+)]i. The aim of the current study was to test the protective effects of insulin on cellular injury induced by the pancreatitis-inducing agents, ethanol, POA, and POAEE. Rat pancreatic acinar cells were isolated by collagenase digestion and [Ca(2+)]i was measured by fura-2 imaging. An in situ [Ca(2+)]i clearance assay was used to assess PMCA activity. Magnesium green (MgGreen) and a luciferase-based ATP kit were used to assess cellular ATP depletion. Ethanol (100 mM) and POAEE (100 μM) induced a small but irreversible Ca(2+) overload response but had no significant effect on PMCA activity. POA (50-100 μM) induced a robust Ca(2+) overload, ATP depletion, inhibited PMCA activity, and consequently induced necrosis. Insulin pretreatment (100 nm for 30 min) prevented the POA-induced Ca(2+) overload, ATP depletion, inhibition of the PMCA, and necrosis. Moreover, the insulin-mediated protection of the POA-induced Ca(2+) overload was partially prevented by the phosphoinositide-3-kinase (PI3K) inhibitor, LY294002. These data provide the first evidence that insulin directly protects pancreatic acinar cell injury induced by bona fide pancreatitis-inducing agents, such as POA. This may have important therapeutic implications for the treatment of pancreatitis.

Keywords: Calcium; Calcium ATPase; Calcium Transport; Insulin; PMCA; Pancreas; Pancreatitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Calcium / metabolism
  • Cell Death
  • Chromones / pharmacology
  • Ethanol / administration & dosage
  • Ethanol / metabolism
  • Fatty Acids / metabolism
  • Fatty Acids, Monounsaturated / pharmacology*
  • Fluorescence
  • Insulin / physiology*
  • Morpholines / pharmacology
  • Pancreas / cytology
  • Pancreas / drug effects*
  • Plasma Membrane Calcium-Transporting ATPases / metabolism
  • Rats
  • Rats, Sprague-Dawley

Substances

  • Chromones
  • Fatty Acids
  • Fatty Acids, Monounsaturated
  • Insulin
  • Morpholines
  • palmitoleic acid
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • Ethanol
  • Adenosine Triphosphate
  • Plasma Membrane Calcium-Transporting ATPases
  • Calcium