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J. Biol. Chem., Vol. 280, Issue 33, 29403-29408, August 19, 2005

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Cardiolipin Is Essential for Organization of Complexes III and IV into a Supercomplex in Intact Yeast Mitochondria^*

Mei Zhang, Eugenia Mileykovskaya, and William Dowhan¶

From the Department of Biochemistry and Molecular Biology, University of Texas-Houston Medical School and Graduate School of Biomedical Sciences, Houston, Texas 77225

Digitonin extracts of mitochondria from cardiolipin-containing (wild type) and cardiolipin-lacking (crd1 mutant) Saccharomyces cerevisiae subjected to colorless native polyacrylamide gel electrophoresis in the presence of 0.003% digitonin displayed a supercomplex composed of homodimers of complexes III and IV in the former case but only the individual homodimers in the latter case. To avoid treatment with any detergent or dye, we compared organization of the respiratory chain in intact mitochondria from wild type and cardiolipin-lacking cells by using a functional analysis developed previously for the study of the organization of the respiratory chain of S. cerevisiae (Boumans, H., Grivell, L. A., and Berden, J. A. (1998) J. Biol. Chem. 273, 4872–4877). Dependence of the kinetics of NADH oxidation via complexes III, IV, and cytochrome c on the concentration of the complex III-specific inhibitor antimycin A was studied. A linear relationship between respiratory activity and saturation of complex III with antimycin A was obtained for wild type mitochondria consistent with single functional unit kinetics of the respiratory chain. Under the same conditions, cardiolipin-lacking mitochondria displayed a hyperbolic relationship indicating cytochrome c pool behavior. No release of cytochrome c from cardiolipin-lacking mitochondria or mitoplasts under our standard experimental conditions was detected. Identical cytochrome c pool behavior was observed for both wild type and cardiolipin-lacking mitochondria in the presence of a chaotropic agent, which disrupts the interaction between respiratory complexes. The results demonstrate that cardiolipin is essential for association of complexes III and IV into a supercomplex in intact yeast mitochondria.

Received for publication, May 5, 2005 , and in revised form, June 10, 2005.

^* This work was supported in part by National Institutes of Health Grant GM56389 (to W. D.). 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.

Present address: One Baylor Plaza, Dept. of Molecular and Cellular Biology, Baylor College of Medicine, Houston, TX 77030.

To whom correspondence may be addressed: P.O. Box 20708, Dept. of Biochemistry and Molecular Biology, University of Texas-Houston Medical School, Houston, TX 77225. Tel.: 713-500-6152; Fax: 713-500-0652; E-mail: Eugenia.Mileykovskaya{at}uth.tmc.edu. ¶ To whom correspondence may be addressed: P.O. Box 20708, Dept. of Biochemistry and Molecular Biology, University of Texas-Houston Medical School, Houston, TX, 77225. Tel.: 713-500-6051; Fax: 713-500-0652; E-mail: William.Dowhan{at}uth.tmc.edu.

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