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Published online 16 April 2001. doi:10.1083/jcb.153.2.319
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© The Rockefeller University Press, 0021-9525/2001//319 $5.00
The Journal of Cell Biology, Volume 153, Number 2, , 2001 319-328

Original Article

Cytochrome C Maintains Mitochondrial Transmembrane Potential and Atp Generation after Outer Mitochondrial Membrane Permeabilization during the Apoptotic Process



Nigel J. Waterhousea, Joshua C. Goldsteina, Oliver von Ahsena, Martin Schulera, Donald D. Newmeyera, and Douglas R. Greena

a Division of Cellular Immunology, La Jolla Institute for Allergy and Immunology, San Diego, California 92121
La Jolla Institute for Allergy and Immunology, 10355 Science Center Dr., San Diego, CA 92121.(858) 558-3526(858) 558-3500

DGreen5240{at}aol.com

During apoptosis, cytochrome c is released into the cytosol as the outer membrane of mitochondria becomes permeable, and this acts to trigger caspase activation. The consequences of this release for mitochondrial metabolism are unclear. Using single-cell analysis, we found that when caspase activity is inhibited, mitochondrial outer membrane permeabilization causes a rapid depolarization of mitochondrial transmembrane potential, which recovers to original levels over the next 30–60 min and is then maintained. After outer membrane permeabilization, mitochondria can use cytoplasmic cytochrome c to maintain mitochondrial transmembrane potential and ATP production. Furthermore, both cytochrome c release and apoptosis proceed normally in cells in which mitochondria have been uncoupled. These studies demonstrate that cytochrome c release does not affect the integrity of the mitochondrial inner membrane and that, in the absence of caspase activation, mitochondrial functions can be maintained after the release of cytochrome c.

Key Words: apoptosis • mitochondria • membrane potential • caspases • ATP

© 2001 The Rockefeller University Press

The online version of this article contains supplemental material.

Oliver von Ahsen's current address is ZMBH, University of Heidelberg, Im Neuenheimer Feld 282, 69120 Heidelberg, Germany.

Abbreviations used in this paper: Apaf, apoptotic protease activating factor; CCCP, carbonyl cyanide m-chlorophenylhydrazone; Cc-GFP-HeLa, HeLa cells stably expressing GFP-tagged cytochrome c; CLAMI, cell lysis and mitochondria intact; DNP, dinitrophenol, {Delta}{Psi}m, mitochondrial transmembrane potential; FCCP, carbonyl cyanide p-(trifluoromethoxy) phenylhydrazone; GFP, green fluorescent protein; MIB, mitochondria isolation buffer; tBid, truncated Bid; TMRE, tetramethylrhodamine ethyl ester; zVADfmk, N-benzoylcarbonyl-Val-Ala-Asp-fluoromethylketone.


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