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J. Biol. Chem., Vol. 275, Issue 22, 17064-17071, June 2, 2000

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Activation of Calpain I Converts Excitotoxic Neuron Death into a Caspase-independent Cell Death^*

Silke Lankiewicz, C. Marc Luetjens, Nguyen Truc Bui, Aaron J. Krohn, Monika Poppe, Greg M. Cole^§, Takaomi C. Saido^¶, and Jochen H. M. Prehn^**

From the  Interdisciplinary Center for Clinical Research (IZKF), Research Group "Apoptosis and Cell Death," the  Department of Pharmacology and Toxicology, Westphalian Wilhelms University, D-48149 Münster, Germany, ^§ GRECC, Sepulvda Veterans Affairs Medical Center, UCLA, Sepulvda, California 91343, and ^¶ RIKEN Brain Science Institute, Saitama 351-0198, Japan

Glutamate receptor overactivation contributes to neuron death after stroke, trauma, and epileptic seizures. Exposure of cultured rat hippocampal neurons to the selective glutamate receptor agonist N-methyl-D-aspartate (300 µM, 5 min) or to the apoptosis-inducing protein kinase inhibitor staurosporine (300 nM) induced a delayed neuron death. In both cases, neuron death was preceded by the mitochondrial release of the pro-apoptotic factor cytochrome c. Unlike staurosporine, the N-methyl-D-aspartate-induced release of cytochrome c did not lead to significant activation of caspase-3, the main caspase involved in the execution of neuronal apoptosis. In contrast, activation of the Ca²⁺-activated neutral protease calpain I was readily detectable after the exposure to N-methyl-D-aspartate. In a neuronal cell-free apoptosis system, calpain I prevented the ability of cytochrome c to activate the caspase cascade by inhibiting the processing of procaspase-3 and -9 into their active subunits. In the hippocampal neuron cultures, the inhibition of calpain activity restored caspase-3-like protease activity after an exposure to N-methyl-D-aspartate. Our data demonstrate the existence of signal transduction pathways that prevent the entry of cells into a caspase-dependent cell death program after the mitochondrial release of cytochrome c.

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