The Permeability Transition Pore Complex: A Target for Apoptosis Regulation by Caspases and Bcl-2-related Proteins

doi:10.1084/jem.187.8.1261

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J. Exp. Med., Volume 187, Number 8, April 20, 1998 1261-1271

The Permeability Transition Pore Complex: A Target for Apoptosis Regulation by Caspases and Bcl-2-related Proteins

By Isabel Marzo,^* Catherine Brenner,^* Naoufal Zamzami,^* Santos A. Susin,^* Gisela Beutner, Dieter Brdiczka, René Rémy,^§ Zhi-Hua Xie, John C. Reed, and Guido Kroemer^*

From the ^* Centre National de la Recherche Scientifique, Unité Propre de Recherche 420, F-94801 Villejuif, France; the Faculty of Biology, University of Konstanz, D-78434 Konstanz, Germany; the ^§ Centre National de la Recherche Scientifique, Université de Paris 11, F-91405 Orsay, France; and The Burnham Institute, La Jolla, California 92037

Early in programmed cell death (apoptosis), mitochondrial membrane permeability increases. This is at least in part due toopening of the permeability transition (PT) pore, a multiproteincomplex built up at the contact site between the inner and theouter mitochondrial membranes. The PT pore has been previouslyimplicated in clinically relevant massive cell death induced bytoxins, anoxia, reactive oxygen species, and calcium overload.Here we show that PT pore complexes reconstituted in liposomesexhibit a functional behavior comparable with that of the naturalPT pore present in intact mitochondria. The PT pore complex isregulated by thiol-reactive agents, calcium, cyclophilin D ligands(cyclosporin A and a nonimmunosuppressive cyclosporin A derivative),ligands of the adenine nucleotide translocator, apoptosis-relatedendoproteases (caspases), and Bcl-2-like proteins. Although calcium,prooxidants, and several recombinant caspases (caspases 1, 2,3, 4, and 6) enhance the permeability of PT pore-containing liposomes,recombinant Bcl-2 or Bcl-X_L augment the resistance of the reconstitutedPT pore complex to pore opening. Mutated Bcl-2 proteins that havelost their cytoprotective potential also lose their PT modulatorycapacity. In conclusion, the PT pore complex may constitute acrossroad of apoptosis regulation by caspases and members of theBcl-2 family.

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