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J. Biol. Chem., Vol. 279, Issue 40, 41975-41984, October 1, 2004

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Peroxiredoxin III, a Mitochondrion-specific Peroxidase, Regulates Apoptotic Signaling by Mitochondria^*

Tong-Shin Chang, Chun-Seok Cho, Sunjoo Park, Shiqin Yu, Sang Won Kang, and Sue Goo Rhee¶

From the Laboratory of Cell Signaling, NHLBI, National Institutes of Health, Bethesda, Maryland 20892 and the Center for Cell Signaling Research, Division of Molecular Life Science, Ewha Womans University, 11-1 Daehyun-dong, Seodaemoon-gu, Seoul 120-750, Korea

Various proapoptotic stimuli increase the production of superoxide and H₂O₂ by mitochondria. Whereas superoxide impairs mitochondrial function and is removed by Mn²⁺-dependent superoxide dismutase, the role and metabolism of mitochondrial H₂O₂ during apoptosis have remained unclear. The effects on apoptotic signaling of depletion of peroxiredoxin (Prx) III, a mitochondrion-specific H₂O₂-scavenging enzyme, have now been investigated by RNA interference in HeLa cells. Depletion of Prx III resulted in increased intracellular levels of H₂O₂ and sensitized cells to induction of apoptosis by staurosporine or TNF-. The rates of mitochondrial membrane potential collapse, cytochrome c release, and caspase activation were increased in Prx III-depleted cells, and these effects were reversed by ectopic expression of Prx III or mitochondrion-targeted catalase. Depletion of Prx III also exacerbated damage to mitochondrial macromolecules induced by the proapoptotic stimuli. Our results suggest that Prx III is a critical regulator of the abundance of mitochondrial H₂O₂, which itself promotes apoptosis in cooperation with other mediators of apoptotic signaling.

Received for publication, July 8, 2004 , and in revised form, July 22, 2004.

^* This work was supported by the Functional Proteomics Center of the 21st Century Frontier Program and the SK Corporation (to S. P. and S. W. K.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^¶ To whom correspondence should be addressed: Bldg. 50, Room 3523, South Drive, MSC 8015, Bethesda, MD 20892. Tel.: 301-496-9646; Fax: 301-480-0357; E-mail: sgrhee{at}nih.gov.

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