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J. Biol. Chem., Vol. 277, Issue 48, 46566-46575, November 29, 2002

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Role of Glutaredoxin in Metabolic Oxidative Stress
GLUTAREDOXIN AS A SENSOR OF OXIDATIVE STRESS MEDIATED BY H₂O₂^*

Jae J. Song, Juong G. Rhee^§, Mohan Suntharalingam^§, Susan A. Walsh^¶, Douglas R. Spitz^¶, and Yong J. Lee

From the  Department of Surgery and Cancer Institute, University of Pittsburgh, Pittsburgh, Pennsylvania 15232, the ^§ Department of Radiation Oncology, School of Medicine, University of Maryland, Baltimore, Maryland 21201, and the ^¶ Free Radical and Radiation Biology Program, Department of Radiation Oncology, The University of Iowa, Iowa City, Iowa 52242

Epitope-tagged glutaredoxin (GRX) was utilized to determine the role of GRX in oxidative stress-induced signaling and cytotoxicity in glucose-deprived human cancer cells (MCF-7/ADR and DU-145). GRX-overexpressing cells demonstrated resistance to glucose deprivation-induced cytotoxicity and decreased activation of c-Jun N-terminal kinase (JNK1). Deletion mutants showed the C-terminal portion of apoptosis signal-regulating kinase 1 (ASK1) bound GRX, and glucose deprivation disrupted binding. Treatment with L-buthionine-(S,R)-sulfoximine reduced glutathione content by 99% and prevented glucose deprivation-induced dissociation of GRX from ASK1. A thiol antioxidant, N-acetyl-L-cysteine, or overexpression of an H₂O₂ scavenger, catalase, inhibited glucose deprivation-induced dissociation of GRX from ASK1. GRX active site cysteine residues (Cys²² and Cys²⁵) were required for dissociation of GRX from ASK1 during glucose deprivation. Kinase assays revealed that SEK1 and JNK1 were regulated in an ASK1-dependent fashion during glucose deprivation. Overexpression of GRX or catalase inhibited activation of ASK1-SEK1-JNK1 signaling during glucose deprivation. These results demonstrate that GRX is a negative regulator of ASK1 and dissociation of GRX from ASK1 activates ASK1-SEK1-JNK1 signaling leading to cytotoxicity during glucose deprivation. These results support the hypothesis that the GRX-ASK1 interaction is redox sensitive and regulated in a glutathione-dependent fashion by H₂O₂.

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