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Originally published In Press as doi:10.1074/jbc.M010498200 on February 13, 2001

J. Biol. Chem., Vol. 276, Issue 19, 16391-16398, May 11, 2001
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NADH Oxidase Activity of Mitochondrial Apoptosis-inducing Factor*

M. Dolores Miramarab, Paola Costantinicd, Luigi Ravagnance, Ligia M. Saraivaf, Delphine Haouzic, Greg Brothersg, Josef M. Penningerg, M. Luisa Peleatoah, Guido Kroemerchi, and Santos A. Susinch

From the a Departamento de Bioquímica y Biología Molecular y Celular. Universidad de Zaragoza, Plaza San Francisco s/n 50009 Zaragoza, Spain, c CNRS, UMR1599, Institut Gustave Roussy, 39 rue Camille Desmoulins, F-94805 Villejuif, France, the f Instituto de Tecnología Química y Biológica, Universidade Nova de Lisboa, rua da Quinta Grande, 6 Apartado 127, 2780 Oeiras, Portugal, and the g Amgen Institute and Ontario Cancer Institute, Department of Medical Biophysics and Immunology, University of Toronto, Toronto, Ontario M5G 2C1, Canada

Apoptosis-inducing factor (AIF) is a mitochondrial flavoprotein, which translocates to the nucleus during apoptosis and causes chromatin condensation and large scale DNA fragmentation. Here we report the biochemical characterization of AIF's redox activity. Natural AIF purified from mitochondria and recombinant AIF purified from bacteria (AIFDelta 1-120) exhibit NADH oxidase activity, whereas superoxide anion (O<UP><SUB>2</SUB><SUP>−</SUP></UP>) is formed. AIFDelta 1-120 is a monomer of 57 kDa containing 1 mol of noncovalently bound FAD/mol of protein. ApoAIFDelta 1-120, which lacks FAD, has no NADH oxidase activity. However, native AIFDelta 1-120, apoAIFDelta 1-120, and the reconstituted (FAD-containing) holoAIFDelta 1-120 protein exhibit a similar apoptosis-inducing potential when microinjected into the cytoplasm of intact cells. Inhibition of the redox function, by external addition of superoxide dismutase or covalent derivatization of FAD with diphenyleneiodonium, failed to affect the apoptogenic function of AIFDelta 1-120 assessed on purified nuclei in a cell-free system. Conversely, blockade of the apoptogenic function of AIFDelta 1-120 with the thiol reagent para- chloromercuriphenylsulfonic acid did not affect its NADH oxidase activity. Altogether, these data indicate that AIF has a marked oxidoreductase activity which can be dissociated from its apoptosis-inducing function.

* This work was supported by a special grant from the Ligue Nationale contre le Cancer, as well as by grants from Agence Nationale de Recherches sur le Sida, Fondation pour la Recherche Medicale, and the European Union QLG1-1999-00739 (to G. K.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

b Recipient of a short term fellowship from Caja de Ahorros de la Inmaculada.

d Recipient of a postdoctoral fellowship from the Fondation pour la Recherche Medicale.

e Recipient of a Ph.D. fellowship from the French Ministry of Science & Technology.

h These authors contributed equally to this work and share senior co-authorship.

i To whom correspondence should be addressed: CNRS, UMR 1599, Inst. Gustave Roussy, Pavillon de Recherche I, 39, rue Camille-Desmoulins, F-94805 Villejuif, France. Tel.: 33-1-42-11-60-46; Fax: 33-1-42-11-60-47; E-mail: kroemer@igr.fr.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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