Dissociating the dual roles of apoptosis-inducing factor in maintaining mitochondrial structure and apoptosis

EMBO Journal

Volumn 25, Issue 17, 2006, Pages 4061-4073

  Cheung, Eric C C ^a   Joza, Nicholas ^b   Steenaart, Nancy A E ^c   McClellan, Kelly A ^a   Neuspiel, Margaret ^d   McNamara, Stephen ^a   MacLaurin, Jason G ^a   Rippstein, Peter ^d   Park, David S ^a   Shore, Gordon C ^e   McBride, Heidi M ^d   Penninger, Josef M ^b   Slack, Ruth S ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^c INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^d UNIVERSITY OF OTTAWA HEART INSTITUTE   (Canada)

^e MCGILL UNIVERSITY   (Canada)

Author keywords

Apoptosis; Apoptosis inducing factor (AIF); DNAdamage; Mitochondria; Neuron

Indexed keywords

APOPTOSIS INDUCING FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN MITOCHONDRION; BRAIN NERVE CELL; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; FEMALE; MITOCHONDRIAL RESPIRATION; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TELENCEPHALON; TRANSMISSION ELECTRON MICROSCOPY;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; APOPTOSIS INDUCING FACTOR; CELL SURVIVAL; CELLS, CULTURED; DNA DAMAGE; MEMBRANE POTENTIALS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; NEURONS; OXYGEN CONSUMPTION; PROSENCEPHALON; PROTEIN TRANSPORT;

EID: 33748341710     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601276     Document Type: Article

References (54)

1. Arnoult D, Gaume B, Karbowski M, Sharpe JC, Cecconi F, Youle RJ (2003) Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J 22: 4385-4399
2. Beltrán B, Mathur A, Duchen MR, Erusalimsky JD, Moncada S (2000) The effect of nitric oxide on cell respiration: a key to understanding its role in cell survival or death. Proc Natl Acad Sci 97: 14602-14607
3. Beltrán B, Quintero M, García-Zaragozá E, O'Connor E, Esplugues JV, Moncada S (2002) Inhibition of mitochondrial respiration by endogenous nitric oxide: a critical step in Fas signalling. Proc Natl Acad Sci 99: 8892-8897
4. Bernardi P, Azzone GF (1981) Cytochrome C as an electron shuttle between outer and inner mitochondrial membranes. J Biol Chem 256: 7187-7192
5. Cande C, Vahsen N, Kouranti I, Schmitt E, Daugas E, Spahr C, Luban J, Kroemer RT, Giordanetto F, Garrido C, Penninger JM, Kroemer G (2004) AIF and cyclophilin A cooperate in apoptosis-associated chromatinolysis. Oncogene 23: 1514-1521
6. Cao G, Clark RS, Pei W, Yin W, Zhang F, Sun FY, Graham SH, Chen J (2003) Translocation of apoptosis-inducing factor in vulnerable neurons after transient cerebral ischemia and in neuronal cultures after oxygen-glucose deprivation. J Cereb Blood Flow Metab 23: 1137-1150
7. Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA, Gruss P (1998) Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94: 727-737
8. Cheung EC, Melanson-Drapeau L, Cregan SP, Vanderluit JL, Ferguson KL, McIntosh WC, Park DS, Bennett SA, Slack RS (2005) Apoptosis-inducing factor is a key factor in neuronal cell death propagated by BAX-dependent and BAX-independent mechanisms. J Neurosci 25: 1324-1334
9. Colgan J, Asmal M, Luban J (2000) Isolation, characterization and targeted disruption of mouse ppia: cyclophilin A is not essential for mammalian cell viability. Genomics 68: 167-178
10. Cozzolino M, Ferraro E, Ferri A, Rigamonti D, Quondamatteo F, Ding H, Xu ZS, Ferrari F, Angelini DF, Rotilio G, Cattaneo E, Carri MT, Cecconi F (2004) Apoptosome inactivation rescues proneural and neural cells from neurodegeneration. Cell Death Differ 11: 1179-1191
11. Cregan SP, Dawson VL, Slack RS (2004) Role of AIF in caspasedependent and caspase-independent cell death. Oncogene 23: 2785-2796
12. Cregan SP, Fortin A, MacLaurin JG, Callaghan SM, Cecconi F, Yu SW, Dawson TM, Dawson VL, Park DS, Kroemer G, Slack RS (2002) Apoptosis-inducing factor is involved in the regulation of caspase-independent neuronal cell death. J Cell Biol 158: 507-517
13. Cregan SP, MacLaurin JG, Craig CG, Robertson GS, Nicholson DW, Park DS, Slack RS (1999) Bax-dependent caspase-3 activation is a key determinant in p53-induced apoptosis in neurons. J Neurosci 19: 7860-7869
14. D'Sa-Eipper C, Leonard JR, Putcha G, Zheng TS, Flavell RA, Rakic P, Kuida K, Roth KA (2001) DNA damage-induced neural precursor cell apoptosis requires p53 and caspase 9 but neither Bax nor caspase 3. Development 128: 137-146
15. Danial NN, Korsmeyer SJ (2004) Cell death: critical control points. Cell 116: 205-219
16. Daugas E, Susin SA, Zamzami N, Ferri KF, Irinopoulou T, Larochette N, Prevost MC, Leber B, Andrews D, Penninger J, Kroemer G (2000) Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J 14: 729-739
17. Di Lisa F, Bernardi P (1998) Mitochondrial function as a determinant of recovery or death in cell response to injury. Mol Cell Biochem 184: 379-391
18. Fannjiang Y, Kim CH, Huganir RL, Zou S, Lindsten T, Thompson CB, Mito T, Traystman RJ, Larsen T, Griffin DE, Mandir AS, Dawson TM, Dike S, Sappington AL, Kerr DA, Jonas EA, Kaczmarek LK, Hardwick JM (2003) BAK alters neuronal excitability and can switch from anti- to pro-death function during postnatal development. Dev Cell 4: 575-585
19. Ferguson KL, Vanderluit JL, Hebert JM, McIntosh WC, Tibbo E, MacLaurin JG, Park DS, Wallace VA, Vooijs M, McConnell SK, Slack RS (2002) Telencephalon-specific Rb knockouts reveal enhanced neurogenesis, survival and abnormal cortical development. EMBO J 21: 3337-3346
20. Fischer U, Huber J, Boelens WC, Mattaj IW, Luhrmann R (1995) The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell 82: 475-483
21. Flick MJ, Konieczny SF (2002) Identification of putative mammalian D-lactate dehydrogenase enzymes. Biochem Biophys Res Commun 295: 910-916
22. Fortin A, Cregan SP, MacLaurin JG, Kushwaha N, Hickman ES, Thompson CS, Hakim A, Albert PR, Cecconi F, Helin K, Park DS, Slack RS (2001) APAF1 is a key transcriptional target for p53 in the regulation of neuronal cell death. J Cell Biol 155: 207-216
23. Frey TG, Mannella CA (2000) The internal structure of mitochondria. Trends Biochem Sci 25: 319-324
24. Germain M, Mathai JP, McBride HM, Shore GC (2005) Endoplasmic reticulum BIK initiates DRP1-regulated remodeling of mitochondrial cristae during apoptosis. EMBO J 24: 1546-1556
25. Hebert JM, McConnell SK (2000) Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev Biol 222: 296-306
26. Hong SJ, Dawson TM, Dawson VL (2004) Nuclear and mitochondrial conversations in cell death: PARP-1 and AIF signaling. Trends Pharmacol Sci 25: 259-264
27. Irvine RA, Adachi N, Shibata DK, Cassell GD, Yu K, Karanjawala ZE, Hsieh CL, Lieber MR (2005) Generation and characterization of endonuclease G null mice. Mol Cell Biol 25: 294-302
28. Joza N, Oudit GY, Brown D, Benit P, Kassiri Z, Vahsen N, Benoit L, Patel MM, Nowikovsky K, Vassault A, Backx PH, Wada T, Kroemer G, Rustin P, Penninger JM (2005) Muscle-specific loss of apoptosis-inducing factor leads to mitochondrial dysfunction, skeletal muscle atrophy, and dilated cardiomyopathy. Mol Cell Biol 25: 10261-10272
29. King MP, Attardi G (1989) Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science 246: 500-503
30. Klein JA, Longo-Guess CM, Rossmann MP, Seburn KL, Hurd RE, Frankel WN, Bronson RT, Ackerman SL (2002) The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 419: 367-374
31. Lang-Rollin IC, Rideout HJ, Noticewala M, Stefanis L (2003) Mechanisms of caspase-independent neuronal death: energy depletion and free radical generation. J Neurosci 23: 11015-11025
32. Li K, Li Y, Shelton JM, Richardson JA, Spencer E, Chen ZJ, Wang X, Williams RS (2000) Cytochrome c deficiency causes embryonic lethality and attenuates stress-induced apoptosis. Cell 101: 389-399
33. Lipton SA, Bossy-Wetzel E (2002) Dueling activities of AIF in cell death versus survival: DNA binding and redox activity. Cell 111: 147-150
34. Mannella CA (2006) The relevance of mitochondrial membrane topology to mitochondrial function. Biochim Biophys Acta 1762: 140-147
35. Mattson MP, Klapper W (2001) Emerging roles for telomerase in neuronal development and apoptosis. J Neurosci Res 63: 1-9
36. Narasimhaiah R, Tuchman A, Lin SL, Naegele JR (2005) Oxidative damage and defective DNA repair is linked to apoptosis of migrating neurons and progenitors during cerebral cortex development in Ku70-deficient mice. Cereb Cortex 15: 696-707
37. Neuspiel M, Zunino R, Gangaraju S, Rippstein P, McBride H (2005) Activated mitofusin 2 signals mitochondrial fusion, interferes with Bax activation, and reduces susceptibility to radical induced depolarization. J Biol Chem 280: 25060-25070
38. Otera H, Ohsakaya S, Nagaura Z, Ishihara N, Mihara K (2005) Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space. EMBO J 24: 1375-1386
39. Parrish JZ, Xue D (2003) Functional genomic analysis of apoptotic DNA degradation in C. elegans. Mol Cell 11: 987-996
40. Peachman KK, Lyles DS, Bass DA (2001) Mitochondria in eosinophils: functional role in apoptosis but not respiration. Proc Natl Acad Sci 98: 1717-1722
41. Plesnila N, Zhu C, Culmsee C, Groger M, Moskowitz MA, Blomgren K (2004) Nuclear translocation of apoptosis-inducing factor after focal cerebral ischemia. J Cereb Blood Flow Metab 24: 458-466
42. Rego AC, Vesce S, Nicholls DG (2001) The mechanism of mitochondrial membrane potential retention following release of cytochrome c in apoptotic GT1-7 neural cells. Cell Death Diff 8: 995-1003
43. Rojo EE, Guiard B, Neupert W, Stuart RA (1998) Sorting of D-lactate dehydrogenase to the inner membrane of mitochondria. Analysis of topogenic signal and energetic requirements. J Biol Chem 273: 8040-8047
44. Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannella CA, Korsmeyer SJ (2002) A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome C during apoptosis. Dev Cell 2: 55-67
45. Skulachev VP (2006) Bioenergetics aspects of apoptosis, necrosis and mitoptosis. Apoptosis 11: 473-485
46. Steenaart NA, Shore GC (1997) Alteration of a mitochondrial outer membrane signal anchor sequence that permits its insertion into the inner membrane. Contribution of hydrophobic residues. J Biol Chem 272: 12057-12061
47. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosisinducing factor. Nature 397: 441-446
48. Tsatmali M, Walcott EC, Crossin KL (2005) Newborn neurons acquire high levels of reactive oxygen species and increased mitochondrial proteins upon differentiation from progenitors. Brain Res 1040: 137-150
49. Vahsen N, Cande C, Briere JJ, Benit P, Joza N, Larochette N, Mastroberardino PG, Pequignot MO, Casares N, Lazar V, Feraud O, Debili N, Wissing S, Engelhardt S, Madeo F, Piacentini M, Penninger JM, Schagger H, Rustin P, Kroemer G (2004) AIF deficiency compromises oxidative phosphorylation. EMBO J 23: 4679-4689
50. Wang H, Yu SW, Koh DW, Lew J, Coombs C, Bowers W, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2004) Apoptosis-inducing factor substitutes for caspase executioners in NMDA-triggered excitotoxic neuronal death. J Neurosci 24: 10963-10973
51. Wang X, Yang C, Chai J, Shi Y, Xue D (2002) Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science 298: 1587-1592
52. Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM, Dawson VL (2002) Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science 297: 259-263
53. Yuan J, Lipinski M, Degterev A (2003) Diversity in the mechanisms of neuronal cell death. Neuron 40: 401-413
54. Zhang X, Chen J, Graham SH, Du L, Kochanek PM, Draviam R, Guo F, Nathaniel PD, Szabo C, Watkins SC, Clark RS (2002) Intranuclear localization of apoptosis-inducing factor (AIF) and large scale DNA fragmentation after traumatic brain injury in rats and in neuronal cultures exposed to peroxynitrite. J Neurochem 82: 181-191