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J Biol Chem, Vol. 274, Issue 39, 27905-27913, September 24, 1999

Hydrogen Peroxide Alters Mitochondrial Activation and Insulin Secretion in Pancreatic Beta Cells

Pierre MaechlerDagger , Lan Jornot§, and Claes B. WollheimDagger

From the Dagger  Division of Clinical Biochemistry and the § Respiratory Division, Department of Internal Medicine, University Medical Center, CH-1211 Geneva, Switzerland

The effects of a transient exposure to hydrogen peroxide (10 min at 200 µM H2O2) on pancreatic beta cell signal transduction and insulin secretion have been evaluated. In rat islets, insulin secretion evoked by glucose (16.7 mM) or by the mitochondrial substrate methyl succinate (5 mM) was markedly blunted following exposure to H2O2. In contrast, the secretory response induced by plasma membrane depolarization (20 mM KCl) was not significantly affected. Similar results were obtained in insulinoma INS-1 cells using glucose (12.8 mM) as secretagogue. After H2O2 treatment, glucose no longer depolarized the membrane potential (Delta Psi ) of INS-1 cells or increased cytosolic Ca2+. Both Delta Psi and Ca2+ responses were still observed with 30 mM KCl despite an elevated baseline of cytosolic Ca2+ appearing ~10 min after exposure to H2O2. The mitochondrial Delta Psi of INS-1 cells was depolarized by H2O2 abolishing the hyperpolarizing action of glucose. These Delta Psi changes correlated with altered mitochondrial morphology; the latter was not preserved by the overexpression of the antiapoptotic protein Bcl-2. Mitochondrial Ca2+ was increased following exposure to H2O2 up to the micromolar range. No further augmentation occurred after glucose addition, which normally raises this parameter. Nevertheless, KCl was still efficient in enhancing mitochondrial Ca2+. Cytosolic ATP was markedly reduced by H2O2 treatment, probably explaining the decreased endoplasmic reticulum Ca2+. Taken together, these data point to the mitochondria as primary targets for H2O2 damage, which will eventually interrupt the transduction of signals normally coupling glucose metabolism to insulin secretion.

Copyright © 1999 by The American Society for Biochemistry and Molecular Biology, Inc.
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