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* Centre National de la Recherche Scientifique, UPR420, F-94801 Villejuif, France;
Assistance Publique-Hôpitaux de Paris, Service de Néphrologie B, Hôpital Tenon, F-75020, France;
Unité d’Oncologie Virale, Institut Pasteur, F-75724 Paris cedex 15, France;
§ McMaster University Medical Centre and
|| Department of Biochemistry, McMaster University, Hamilton, Ontario, L8N 3Z5, Canada;
** Laboratoire d’Anatomopathologie et INSERM U430, Hôpital Broussais, F-75014 Paris, France; and
The Amgen Institute and Ontario Cancer Institute, Department of Medical Biophysics and Immunology, University of Toronto, Toronto, Ontario M5G 2C1, Canada
1Correspondence: 19 rue Guy Môquet, B.P. 8, F-94801 Villejuif, France. E-mail: kroemer{at}infobiogen.fr
Apoptosis inducing factor (AIF) is a novel apoptotic effector protein that induces chromatin condensation and large-scale (~50 kbp) DNA fragmentation when added to purified nuclei in vitro. Confocal and electron microscopy reveal that, in normal cells, AIF is strictly confined to mitochondria and thus colocalizes with heat shock protein 60 (hsp60). On induction of apoptosis by staurosporin, c-Myc, etoposide, or ceramide, AIF (but not hsp60) translocates to the nucleus. This suggests that only the outer mitochondrial membrane (which retains AIF in the intermembrane space) but not the inner membrane (which retains hsp60 in the matrix) becomes protein permeable. The mitochondrio-nuclear redistribution of AIF is prevented by a Bcl-2 protein specifically targeted to mitochondrial membranes. The pan-caspase inhibitor Z-VAD.fmk does not prevent the staurosporin-induced translocation of AIF, although it does inhibit oligonucleosomal DNA fragmentation and arrests chromatin condensation at an early stage. ATP depletion is sufficient to cause AIF translocation to the nucleus, and this phenomenon is accelerated by the apoptosis inducer staurosporin. However, in conditions in which both glycolytic and respiratory ATP generation is inhibited, cells fail to manifest any sign of chromatin condensation and advanced DNA fragmentation, thus manifesting a ‘necrotic’ phenotype. Both in the presence of Z-VAD.fmk and in conditions of ATP depletion, AIF translocation correlates with the appearance of large-scale DNA fragmentation. Altogether, these data are compatible with the hypothesis that AIF is a caspase-independent mitochondrial death effector responsible for partial chromatinolysis.—Daugas, E., Susin, S. A., Zamzami, N., Ferri, K., Irinopoulou, T., Larochette, N., Prévost, M.-C., Leber, B., Andrews, D., Penninger, J., Kroemer, G. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis.
Key Words: antioncogene • mitochondrial transmembrane potential • oncogene • permeability transition • programmed cell death
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