Mitochondrial control of nuclear apoptosis

doi:10.1084/jem.183.4.1533

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Mitochondrial control of nuclear apoptosis

N Zamzami, SA Susin, P Marchetti, T Hirsch, I Gomez-Monterrey, M Castedo and G Kroemer
Centre National de la Recherche Scientifique (CNRS)-UPR420, Villejuif, France.

Anucleate cells can be induced to undergo programmed cell death (PCD), indicating the existence of a cytoplasmic PCD pathway that functions independently from the nucleus. Cytoplasmic structures including mitochondria have been shown to participate in the control of apoptotic nuclear disintegration. Before cells exhibit common signs of nuclear apoptosis (chromatin condensation and endonuclease-mediated DNA fragmentation), they undergo a reduction of the mitochondrial transmembrane potential (delta psi m) that may be due to the opening of mitochondrial permeability transition (PT) pores. Here, we present direct evidence indicating that mitochondrial PT constitutes a critical early event of the apoptotic process. In a cell-free system combining purified mitochondria and nuclei, mitochondria undergoing PT suffice to induce chromatin condensation and DNA fragmentation. Induction of PT by pharmacological agents augments the apoptosis-inducing potential of mitochondria. In contrast, prevention of PT by pharmacological agents impedes nuclear apoptosis, both in vitro and in vivo. Mitochondria from hepatocytes or lymphoid cells undergoing apoptosis, but not those from normal cells, induce disintegration of isolated Hela nuclei. A specific ligand of the mitochondrial adenine nucleotide translocator (ANT), bongkreik acid, inhibits PT and reduces apoptosis induction by mitochondria in a cell-free system. Moreover, it inhibits the induction of apoptosis in intact cells. Several pieces of evidence suggest that the proto-oncogene product Bcl-2 inhibits apoptosis by preventing mitochondrial PT. First, to inhibit nuclear apoptosis, Bcl-2 must be localized in mitochondrial but not nuclear membranes. Second, transfection-enforced hyperexpression of Bcl-2 directly abolishes the induction of mitochondrial PT in response to a protonophore, a pro- oxidant, as well as to the ANT ligand atractyloside, correlating with its apoptosis-inhibitory effect. In conclusion, mitochondrial PT appears to be a critical step of the apoptotic cascade.
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Van Remmen, H., Williams, M. D., Guo, Z., Estlack, L., Yang, H., Carlson, E. J., Epstein, C. J., Huang, T. T., Richardson, A. (2001). Knockout mice heterozygous for Sod2 show alterations in cardiac mitochondrial function and apoptosis. Am. J. Physiol. Heart Circ. Physiol. 281: H1422-H1432 [Abstract] [Full Text]
Phenix, B. N., Lum, J. J., Nie, Z., Sanchez-Dardon, J., Badley, A. D. (2001). Antiapoptotic mechanism of HIV protease inhibitors: preventing mitochondrial transmembrane potential loss. Blood 98: 1078-1085 [Abstract] [Full Text]
Le'Negrate, G., Ricci, V., Hofman, V., Mograbi, B., Hofman, P., Rossi, B. (2001). Epithelial Intestinal Cell Apoptosis Induced by Helicobacter pylori Depends on Expression of the cag Pathogenicity Island Phenotype. Infect. Immun. 69: 5001-5009 [Abstract] [Full Text]
Oubrahim, H., Stadtman, E. R., Chock, P. B. (2001). Mitochondria play no roles in Mn(II)-induced apoptosis in HeLa cells. Proc. Natl. Acad. Sci. USA 10.1073/pnas.181319898v1 [Abstract] [Full Text]
Pallis, M., Grundy, M., Turzanski, J., Kofler, R., Russell, N. (2001). Mitochondrial membrane sensitivity to depolarization in acute myeloblastic leukemia is associated with spontaneous in vitro apoptosis, wild-type TP53, and vicinal thiol/disulfide status. Blood 98: 405-413 [Abstract] [Full Text]
Nakao, Y., Otani, H., Yamamura, T., Hattori, R., Osako, M., Imamura, H. (2001). Insulin-like growth factor 1 prevents neuronal cell death and paraplegia in the rabbit model of spinal cord ischemia. J. Thorac. Cardiovasc. Surg. 122: 136-143 [Abstract] [Full Text]
Motoori, S., Majima, H. J., Ebara, M., Kato, H., Hirai, F., Kakinuma, S., Yamaguchi, C., Ozawa, T., Nagano, T., Tsujii, H., Saisho, H. (2001). Overexpression of Mitochondrial Manganese Superoxide Dismutase Protects against Radiation-induced Cell Death in the Human Hepatocellular Carcinoma Cell Line HLE. Cancer Res. 61: 5382-5388 [Abstract] [Full Text]
Poppe, M., Reimertz, C., Du{beta}mann, H., Krohn, A. J., Luetjens, C. M., Bockelmann, D., Nieminen, A.-L., Kogel, D., Prehn, J. H. M. (2001). Dissipation of Potassium and Proton Gradients Inhibits Mitochondrial Hyperpolarization and Cytochrome c Release during Neural Apoptosis. J. Neurosci. 21: 4551-4563 [Abstract] [Full Text]
Kaspar, A. A., Okada, S., Kumar, J., Poulain, F. R., Drouvalakis, K. A., Kelekar, A., Hanson, D. A., Kluck, R. M., Hitoshi, Y., Johnson, D. E., Froelich, C. J., Thompson, C. B., Newmeyer, D. D., Anel, A., Clayberger, C., Krensky, A. M. (2001). A Distinct Pathway of Cell-Mediated Apoptosis Initiated by Granulysin. J. Immunol. 167: 350-356 [Abstract] [Full Text]
Leach, J. K., Van Tuyle, G., Lin, P.-S., Schmidt-Ullrich, R., Mikkelsen, R. B. (2001). Ionizing Radiation-induced, Mitochondria-dependent Generation of Reactive Oxygen/Nitrogen. Cancer Res. 61: 3894-3901 [Abstract] [Full Text]
Sciacco, M., Fagiolari, G., Lamperti, C., Messina, S., Bazzi, P., Napoli, L., Chiveri, L., Prelle, A., Comi, G.P., Bresolin, N., Scarlato, G., Moggio, M. (2001). Lack of apoptosis in mitochondrial encephalomyopathies. Neurology 56: 1070-1074 [Abstract] [Full Text]
Northington, F. J., Ferriero, D. M., Flock, D. L., Martin, L. J. (2001). Delayed Neurodegeneration in Neonatal Rat Thalamus after Hypoxia-Ischemia Is Apoptosis. J. Neurosci. 21: 1931-1938 [Abstract] [Full Text]
LOEFFLER, M., DAUGAS, E., SUSIN, S. A., ZAMZAMI, N., METIVIER, D., NIEMINEN, A.-L., BROTHERS, G., PENNINGER, J. M., KROEMER, G. (2001). Dominant cell death induction by extramitochondrially targeted apoptosis-inducing factor. FASEB J. 15: 758-767 [Abstract] [Full Text]
Tafani, M., Minchenko, D. A., Serroni, A., Farber, J. L. (2001). Induction of the Mitochondrial Permeability Transition Mediates the Killing of HeLa Cells by Staurosporine. Cancer Res. 61: 2459-2466 [Abstract] [Full Text]
Vayssier-Taussat, M., Camilli, T., Aron, Y., Meplan, C., Hainaut, P., Polla, B. S., Weksler, B. (2001). Effects of tobacco smoke and benzo[a]pyrene on human endothelial cell and monocyte stress responses. Am. J. Physiol. Heart Circ. Physiol. 280: H1293-H1300 [Abstract] [Full Text]
Fernandez, A., Udagawa, T., Schwesinger, C., Beecken, W.-D., Achilles-Gerte, E., McDonnell, T. J., D'Amato, R. J. (2001). Angiogenic Potential of Prostate Carcinoma Cells Overexpressing bcl-2. JNCI J Natl Cancer Inst 93: 208-213 [Abstract] [Full Text]