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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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 S. A. Vorburger, A. Pataer, K. Yoshida, Y. Liu, X. Lu, S. G. Swisher, and K. K. Hunt The Mitochondrial Apoptosis-Inducing Factor Plays a Role in E2F-1-Induced Apoptosis in Human Colon Cancer Cells Ann. Surg. Oncol., April 1, 2003; 10(3): 314 - 322. [Abstract] [Full Text] [PDF]
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 Y. Takagi-Morishita, N. Yamada, A. Sugihara, T. Iwasaki, T. Tsujimura, and N. Terada Mouse Uterine Epithelial Apoptosis Is Associated with Expression of Mitochondrial Voltage-Dependent Anion Channels, Release of Cytochrome C from Mitochondria, and the Ratio of Bax to Bcl-2 or Bcl-X Biol Reprod, April 1, 2003; 68(4): 1178 - 1184. [Abstract] [Full Text] [PDF]
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G. D. Diaz, Q. Li, and R. H. Dashwood Caspase-8 and Apoptosis-inducing Factor Mediate a Cytochrome c-independent Pathway of Apoptosis in Human Colon Cancer Cells Induced by the Dietary Phytochemical Chlorophyllin Cancer Res., March 15, 2003; 63(6): 1254 - 1261. [Abstract] [Full Text] [PDF]
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C. Cande, F. Cecconi, P. Dessen, and G. Kroemer Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J. Cell Sci., March 14, 2003; 115(24): 4727 - 4734. [Abstract] [Full Text] [PDF]
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 H. Murahashi, H. Azuma, N. Zamzami, K.-j. Furuya, K. Ikebuchi, M. Yamaguchi, Y. Yamada, N. Sato, M. Fujihara, G. Kroemer, et al. Possible contribution of apoptosis-inducing factor (AIF) and reactive oxygen species (ROS) to UVB-induced caspase-independent cell death in the T cell line Jurkat J. Leukoc. Biol., March 1, 2003; 73(3): 399 - 406. [Abstract] [Full Text] [PDF]
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M. Alonso, C. Tamasdan, D. C. Miller, and E. W. Newcomb Flavopiridol Induces Apoptosis in Glioma Cell Lines Independent of Retinoblastoma and p53 Tumor Suppressor Pathway Alterations by a Caspase-independent Pathway Mol. Cancer Ther., February 1, 2003; 2(2): 139 - 150. [Abstract] [Full Text] [PDF]
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F. Morrish, C. Giedt, and D. Hockenbery c-MYC apoptotic function is mediated by NRF-1 target genes Genes & Dev., January 15, 2003; 17(2): 240 - 255. [Abstract] [Full Text] [PDF]
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 R. Riachy, B. Vandewalle, J. Kerr Conte, E. Moerman, P. Sacchetti, B. Lukowiak, V. Gmyr, T. Bouckenooghe, M. Dubois, and F. Pattou 1,25-Dihydroxyvitamin D3 Protects RINm5F and Human Islet Cells against Cytokine-Induced Apoptosis: Implication of the Antiapoptotic Protein A20 Endocrinology, December 1, 2002; 143(12): 4809 - 4819. [Abstract] [Full Text] [PDF]
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W. F. Davidson, C. Haudenschild, J. Kwon, and M. S. Williams T Cell Receptor Ligation Triggers Novel Nonapoptotic Cell Death Pathways That Are Fas-Independent or Fas-Dependent J. Immunol., December 1, 2002; 169(11): 6218 - 6230. [Abstract] [Full Text] [PDF]
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V. Mateo, E. J. Brown, G. Biron, M. Rubio, A. Fischer, F. L. Deist, and M. Sarfati Mechanisms of CD47-induced caspase-independent cell death in normal and leukemic cells: link between phosphatidylserine exposure and cytoskeleton organization Blood, September 26, 2002; 100(8): 2882 - 2890. [Abstract] [Full Text] [PDF]
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 M. G. Fernandez, L. Troiano, L. Moretti, M. Nasi, M. Pinti, S. Salvioli, J. Dobrucki, and A. Cossarizza Early Changes in Intramitochondrial Cardiolipin Distribution during Apoptosis Cell Growth Differ., September 1, 2002; 13(9): 449 - 455. [Abstract] [Full Text] [PDF]
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F. Li, H. P. Mao, K. L. Ruchalski, Y. H. Wang, W. Choy, J. H. Schwartz, and S. C. Borkan Heat stress prevents mitochondrial injury in ATP-depleted renal epithelial cells Am J Physiol Cell Physiol, September 1, 2002; 283(3): C917 - C926. [Abstract] [Full Text] [PDF]
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A. Goerke, N. Sakai, E. Gutjahr, W. A. Schlapkohl, J. F. Mushinski, H. Haller, W. Kolch, N. Saito, and H. Mischak Induction of Apoptosis by Protein Kinase Cdelta Is Independent of Its Kinase Activity J. Biol. Chem., August 23, 2002; 277(35): 32054 - 32062. [Abstract] [Full Text] [PDF]
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 S. P. Cregan, A. Fortin, J. G. MacLaurin, S. M. Callaghan, F. Cecconi, S.-W. Yu, T. M. Dawson, V. L. Dawson, D. S. Park, G. Kroemer, et al. Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death J. Cell Biol., August 5, 2002; 158(3): 507 - 517. [Abstract] [Full Text] [PDF]
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M. Chen, D.-J. Won, S. Krajewski, and R. A. Gottlieb Calpain and Mitochondria in Ischemia/Reperfusion Injury J. Biol. Chem., August 2, 2002; 277(32): 29181 - 29186. [Abstract] [Full Text] [PDF]
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M. Wu, L.-G. Xu, X. Li, Z. Zhai, and H.-B. Shu AMID, an Apoptosis-inducing Factor-homologous Mitochondrion-associated Protein, Induces Caspase-independent Apoptosis J. Biol. Chem., July 5, 2002; 277(28): 25617 - 25623. [Abstract] [Full Text] [PDF]
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Y. Guo, S. M. Srinivasula, A. Druilhe, T. Fernandes-Alnemri, and E. S. Alnemri Caspase-2 Induces Apoptosis by Releasing Proapoptotic Proteins from Mitochondria J. Biol. Chem., April 12, 2002; 277(16): 13430 - 13437. [Abstract] [Full Text] [PDF]
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I. W. Jeffrey, M. Bushell, V. J. Tilleray, S. Morley, and M. J. Clemens Inhibition of Protein Synthesis in Apoptosis: Differential Requirements by the Tumor Necrosis Factor {alpha} Family and a DNA-damaging Agent for Caspases and the Double-stranded RNA-dependent Protein Kinase Cancer Res., April 1, 2002; 62(8): 2272 - 2280. [Abstract] [Full Text] [PDF]
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 H. Wakiyama, D. B. Cowan, Y. Toyoda, M. Federman, S. Levitsky, and J. D. McCully Selective opening of mitochondrial ATP-sensitive potassium channels during surgically induced myocardial ischemia decreases necrosis and apoptosis Eur. J. Cardiothorac. Surg., March 1, 2002; 21(3): 424 - 433. [Abstract] [Full Text] [PDF]
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H. Hentze, I. Schmitz, M. Latta, A. Krueger, P. H. Krammer, and A. Wendel Glutathione Dependence of Caspase-8 Activation at the Death-inducing Signaling Complex J. Biol. Chem., February 8, 2002; 277(7): 5588 - 5595. [Abstract] [Full Text] [PDF]
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M. Pollack and C. Leeuwenburgh Apoptosis and Aging: Role of the Mitochondria J. Gerontol. A Biol. Sci. Med. Sci., November 1, 2001; 56(11): B475 - 482. [Abstract] [Full Text] [PDF]
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M. Castedo, K. F. Ferri, J. Blanco, T. Roumier, N. Larochette, J. Barretina, A. Amendola, R. Nardacci, D. Metivier, J. A. Este, et al. Human Immunodeficiency Virus 1 Envelope Glycoprotein Complex-induced Apoptosis Involves Mammalian Target of Rapamycin/FKBP12-Rapamycin-associated Protein-mediated p53 Phosphorylation J. Exp. Med., October 15, 2001; 194(8): 1097 - 1110. [Abstract] [Full Text] [PDF]
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B. Cipriani, G. Borsellino, H. Knowles, D. Tramonti, F. Cavaliere, G. Bernardi, L. Battistini, and C. F. Brosnan Curcumin Inhibits Activation of V{gamma}9V{delta}2 T Cells by Phosphoantigens and Induces Apoptosis Involving Apoptosis-Inducing Factor and Large Scale DNA Fragmentation J. Immunol., September 15, 2001; 167(6): 3454 - 3462. [Abstract] [Full Text] [PDF]
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S. Ura, N. Masuyama, J. D. Graves, and Y. Gotoh Caspase cleavage of MST1 promotes nuclear translocation and chromatin condensation PNAS, August 17, 2001; (2001) 181161698. [Abstract] [Full Text] [PDF]
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J. Pardo, P. Perez-Galan, S. Gamen, I. Marzo, I. Monleon, A. A. Kaspar, S. A. Susin, G. Kroemer, A. M. Krensky, J. Naval, et al. A Role of the Mitochondrial Apoptosis-Inducing Factor in Granulysin-Induced Apoptosis J. Immunol., August 1, 2001; 167(3): 1222 - 1229. [Abstract] [Full Text] [PDF]
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 T. Hisatomi, T. Sakamoto, T. Murata, I. Yamanaka, Y. Oshima, Y. Hata, T. Ishibashi, H. Inomata, S. A. Susin, and G. Kroemer Relocalization of Apoptosis-Inducing Factor in Photoreceptor Apoptosis Induced by Retinal Detachment in Vivo Am. J. Pathol., April 1, 2001; 158(4): 1271 - 1278. [Abstract] [Full Text] [PDF]
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K. D. Kim, Y.-K. Choe, I. S. Choe, and J.-S. Lim Inhibition of glucocorticoid-mediated, caspase-independent dendritic cell death by CD40 activation J. Leukoc. Biol., March 1, 2001; 69(3): 426 - 434. [Abstract] [Full Text]
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M. LOEFFLER, E. DAUGAS, S. A. SUSIN, N. ZAMZAMI, D. METIVIER, A.-L. NIEMINEN, G. BROTHERS, J. M. PENNINGER, and G. KROEMER Dominant cell death induction by extramitochondrially targeted apoptosis-inducing factor FASEB J, March 1, 2001; 15(3): 758 - 767. [Abstract] [Full Text] [PDF]
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E. Ahlbom, V. Gogvadze, M. Chen, G. Celsi, and S. Ceccatelli Prenatal exposure to high levels of glucocorticoids increases the susceptibility of cerebellar granule cells to oxidative stress-induced cell death PNAS, December 8, 2000; (2000) 260501697. [Abstract] [Full Text]
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K. F. Ferri, E. Jacotot, J. Blanco, J. A. Este, N. Zamzami, S. A. Susin, Z. Xie, G. Brothers, J. C. Reed, J. M. Penninger, et al. Apoptosis Control in Syncytia Induced by the HIV Type 1-Envelope Glycoprotein Complex: Role of Mitochondria and Caspases J. Exp. Med., October 9, 2000; 192(8): 1081 - 1092. [Abstract] [Full Text] [PDF]
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 G. Zhou and B. Roizman Wild-Type Herpes Simplex Virus 1 Blocks Programmed Cell Death and Release of Cytochrome c but Not the Translocation of Mitochondrial Apoptosis-Inducing Factor to the Nuclei of Human Embryonic Lung Fibroblasts J. Virol., October 1, 2000; 74(19): 9048 - 9053. [Abstract] [Full Text]
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S. A. Susin, E. Daugas, L. Ravagnan, K. Samejima, N. Zamzami, M. Loeffler, P. Costantini, K. F. Ferri, T. Irinopoulou, M.-C. Prevost, et al. Two Distinct Pathways Leading to Nuclear Apoptosis J. Exp. Med., August 21, 2000; 192(4): 571 - 580. [Abstract] [Full Text] [PDF]
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M. Suter, C. Reme, C. Grimm, A. Wenzel, M. Jaattela, P. Esser, N. Kociok, M. Leist, and C. Richter Age-related Macular Degeneration. THE LIPOFUSCIN COMPONENT N-RETINYL-N-RETINYLIDENE ETHANOLAMINE DETACHES PROAPOPTOTIC PROTEINS FROM MITOCHONDRIA AND INDUCES APOPTOSIS IN MAMMALIAN RETINAL PIGMENT EPITHELIAL CELLS J. Biol. Chem., December 8, 2000; 275(50): 39625 - 39630. [Abstract] [Full Text] [PDF]
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M. D. Miramar, P. Costantini, L. Ravagnan, L. M. Saraiva, D. Haouzi, G. Brothers, J. M. Penninger, M. L. Peleato, G. Kroemer, and S. A. Susin NADH Oxidase Activity of Mitochondrial Apoptosis-inducing Factor J. Biol. Chem., May 4, 2001; 276(19): 16391 - 16398. [Abstract] [Full Text] [PDF]
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