Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death

doi:10.1084/jem.182.2.367

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Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death

N Zamzami, P Marchetti, M Castedo, D Decaudin, A Macho, T Hirsch, SA Susin, PX Petit, B Mignotte and G Kroemer
Centre National de la Recherche Scientifique, Unite Propre de Recherche 420, Villejuif, France.

Programmed cell death (PCD) is a physiological process commonly defined by alterations in nuclear morphology (apoptosis) and/or characteristic stepwise degradation of chromosomal DNA occurring before cytolysis. However, determined characteristics of PCD such as loss in mitochondrial reductase activity or cytolysis can be induced in enucleated cells, indicating cytoplasmic PCD control. Here we report a sequential disregulation of mitochondrial function that precedes cell shrinkage and nuclear fragmentation. A first cyclosporin A-inhibitable step of ongoing PCD is characterized by a reduction of mitochondrial transmembrane potential, as determined by specific fluorochromes (5,5',6,6'-tetrachloro-1,1',3,3'-tetraethylbenzimidazolcarbocyanine++ + iodide; 3,3'dihexyloxacarbocyanine iodide). Cytofluorometrically purified cells with reduced mitochondrial transmembrane potential are initially incapable of oxidizing hydroethidine (HE) into ethidium. Upon short-term in vitro culture, such cells acquire the capacity of HE oxidation, thus revealing a second step of PCD marked by mitochondrial generation of reactive oxygen species (ROS). This step can be selectively inhibited by rotenone and ruthenium red yet is not affected by cyclosporin A. Finally, cells reduce their volume, a step that is delayed by radical scavengers, indicating the implication of ROS in the apoptotic process. This sequence of alterations accompanying early PCD is found in very different models of apoptosis induction: glucocorticoid-induced death of lymphocytes, activation-induced PCD of T cell hybridomas, and tumor necrosis factor-induced death of U937 cells. Transfection with the antiapoptotic protooncogene Bcl-2 simultaneously inhibits mitochondrial alterations and apoptotic cell death triggered by steroids or ceramide. In vivo injection of fluorochromes such as 5,5',6,6'-tetrachloro-1,1',3,3'- tetraethylbenzimidazolcarbocyanine iodide; 3,3'dihexyloxacarbocyanine iodide; or HE allows for the detection of cells that are programmed for death but still lack nuclear DNA fragmentation. In particular, assessment of mitochondrial ROS generation provides an accurate picture of PCD-mediated lymphocyte depletion. In conclusion, alterations of mitochondrial function constitute an important feature of early PCD.
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Tonomura, N., McLaughlin, K., Grimm, L., Goldsby, R. A., Osborne, B. A. (2003). Glucocorticoid-Induced Apoptosis of Thymocytes: Requirement of Proteasome-Dependent Mitochondrial Activity. J. Immunol. 170: 2469-2478 [Abstract] [Full Text]
Cartee, L., Maggio, S. C., Smith, R., Sankala, H. M., Dent, P., Grant, S. (2003). Protein Kinase C-dependent Activation of the Tumor Necrosis Factor Receptor-mediated Extrinsic Cell Death Pathway Underlies Enhanced Apoptosis in Human Myeloid Leukemia Cells Exposed to Bryostatin 1 and Flavopiridol. Molecular Cancer Therapeutics 2: 83-93 [Abstract] [Full Text]
Gardai, S. J., Hoontrakoon, R., Goddard, C. D., Day, B. J., Chang, L. Y., Henson, P. M., Bratton, D. L. (2003). Oxidant-Mediated Mitochondrial Injury in Eosinophil Apoptosis: Enhancement by Glucocorticoids and Inhibition by Granulocyte-Macrophage Colony-Stimulating Factor. J. Immunol. 170: 556-566 [Abstract] [Full Text]
Gouaze, V., Andrieu-Abadie, N., Cuvillier, O., Malagarie-Cazenave, S., Frisach, M.-F., Mirault, M.-E., Levade, T. (2002). Glutathione Peroxidase-1 Protects from CD95-induced Apoptosis. J. Biol. Chem. 277: 42867-42874 [Abstract] [Full Text]
Grayson, J. M., Harrington, L. E., Lanier, J. G., Wherry, E. J., Ahmed, R. (2002). Differential Sensitivity of Naive and Memory CD8+ T Cells to Apoptosis in Vivo. J. Immunol. 169: 3760-3770 [Abstract] [Full Text]
Gottlieb, E., Armour, S. M., Thompson, C. B. (2002). Mitochondrial respiratory control is lost during growth factor deprivation. Proc. Natl. Acad. Sci. USA 99: 12801-12806 [Abstract] [Full Text]
Regula, K. M., Ens, K., Kirshenbaum, L. A. (2002). Inducible Expression of BNIP3 Provokes Mitochondrial Defects and Hypoxia-Mediated Cell Death of Ventricular Myocytes. Circ. Res. 91: 226-231 [Abstract] [Full Text]
Page, T. J., O'Brien, S., Jefcoate, C. R., Czuprynski, C. J. (2002). 7,12-Dimethylbenz[a]anthracene Induces Apoptosis in Murine Pre-B Cells through a Caspase-8-Dependent Pathway. Mol. Pharmacol. 62: 313-319 [Abstract] [Full Text]
Siskind, L. J., Kolesnick, R. N., Colombini, M. (2002). Ceramide Channels Increase the Permeability of the Mitochondrial Outer Membrane to Small Proteins. J. Biol. Chem. 277: 26796-26803 [Abstract] [Full Text]
Baker, P. K., Pettitt, A. R., Slupsky, J. R., Chen, H. J., Glenn, M. A., Zuzel, M., Cawley, J. C. (2002). Response of hairy cells to IFN-alpha involves induction of apoptosis through autocrine TNF-alpha and protection by adhesion. Blood 100: 647-653 [Abstract] [Full Text]
ZHANG, Y., NAN, B., YU, J., SNABBOON, T., ANDRIANI, F., MARCELLI, M. (2002). From Castration-Induced Apoptosis of Prostatic Epithelium to the Use of Apoptotic Genes in the Treatment of Prostate Cancer. Ann. N. Y. Acad. Sci. 963: 191-203 [Abstract] [Full Text]
Cartee, L., Smith, R., Dai, Y., Rahmani, M., Rosato, R., Almenara, J., Dent, P., Grant, S. (2002). Synergistic Induction of Apoptosis in Human Myeloid Leukemia Cells by Phorbol 12-Myristate 13-Acetate and Flavopiridol Proceeds via Activation of Both the Intrinsic and Tumor Necrosis Factor-Mediated Extrinsic Cell Death Pathways. Mol. Pharmacol. 61: 1313-1321 [Abstract] [Full Text]
Mbebi, C., See, V., Mercken, L., Pradier, L., Muller, U., Loeffler, J.-P. (2002). Amyloid Precursor Protein Family-induced Neuronal Death Is Mediated by Impairment of the Neuroprotective Calcium/Calmodulin Protein Kinase IV-dependent Signaling Pathway. J. Biol. Chem. 277: 20979-20990 [Abstract] [Full Text]
Kondo, M., Shibata, T., Kumagai, T., Osawa, T., Shibata, N., Kobayashi, M., Sasaki, S., Iwata, M., Noguchi, N., Uchida, K. (2002). 15-Deoxy-Delta 12,14-prostaglandin J2: The endogenous electrophile that induces neuronal apoptosis. Proc. Natl. Acad. Sci. USA 99: 7367-7372 [Abstract] [Full Text]
Wang, Z., Wang, S., Dai, Y., Grant, S. (2002). Bryostatin 1 Increases 1-beta -D-Arabinofuranosylcytosine-Induced Cytochrome c Release and Apoptosis in Human Leukemia Cells Ectopically Expressing Bcl-xL. J. Pharmacol. Exp. Ther. 301: 568-577 [Abstract] [Full Text]
Plotkowski, M.-C., Povoa, H. C. C., Zahm, J.-M., Lizard, G., Pereira, G. M. B., Tournier, J.-M., Puchelle, E. (2002). Early Mitochondrial Dysfunction, Superoxide Anion Production, and DNA Degradation Are Associated with Non-Apoptotic Death of Human Airway Epithelial Cells Induced by Pseudomonas aeruginosa Exotoxin A. Am. J. Respir. Cell Mol. Bio. 26: 617-626 [Abstract] [Full Text]
Vilenchik, M., Raffo, A. J., Benimetskaya, L., Shames, D., Stein, C. A. (2002). Antisense RNA Down-Regulation of bcl-xL Expression in Prostate Cancer Cells Leads to Diminished Rates of Cellular Proliferation and Resistance to Cytotoxic Chemotherapeutic Agents. Cancer Res. 62: 2175-2183 [Abstract] [Full Text]