Persistent cleavage and nuclear translocation of apoptosis-inducing factor in motor neurons in the spinal cord of sporadic amyotrophic lateral sclerosis patients

Acta Neuropathologica

Volumn 118, Issue 6, 2009, Pages 755-762

  Shibata, Noriyuki ^a   Kakita, Akiyoshi ^b   Takahashi, Hitoshi ^b   Ihara, Yuetsu ^c   Nobukuni, Keigo ^c   Fujimura, Harutoshi ^d   Sakoda, Saburo ^e   Sasaki, Shoichi ^a   Yamamoto, Tomoko ^a   Kobayashi, Makio ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

^c Department of Internal Medicine   (Japan)

^d TONEYAMA NATIONAL HOSPITAL   (Japan)

^e OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Apoptosis inducing factor; Glutamate excitotoxicity; Motor neuron degeneration; Oxidative stress

Indexed keywords

APOPTOSIS INDUCING FACTOR; BETA ACTIN; CYTOPLASM PROTEIN; HISTONE H1; NUCLEAR PROTEIN;

ADULT; AGE DISTRIBUTION; AGED; AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; ASTROCYTE; AUTOPSY; CELL NUCLEUS; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE DURATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MORTALITY; MOTONEURON; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS;

ACTIVE TRANSPORT, CELL NUCLEUS; ADULT; AGED; AGED, 80 AND OVER; AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS INDUCING FACTOR; BLOTTING, WESTERN; CELL NUCLEUS; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; MOTOR NEURONS; PROTEIN TRANSPORT; SPINAL CORD;

EID: 71449087503     PISSN: 00016322     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00401-009-0580-6     Document Type: Article

References (59)

1. G Amadoro MT Ciotti M Costanzi V Cestari P Calissano N Canu 2006 NMDA receptor mediates tau-induced neurotoxicity by calpine and ERK/MAPK activation Proc Natl Acad Sci USA 103 2892 2897 10.1073/pnas.0511065103 1:CAS:528:DC%2BD28XksF2rtbY%3D 16477009 (Pubitemid 43306645)
2. T Arai M Hasegawa H Akiyama K Ikeda T Nonaka H Mori D Mann K Tsuchiya M Yoshida Y Hashizume T Oda 2006 TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis Biochem Biophys Res Commun 351 602 611 10.1016/j.bbrc.2006.10. 093 1:CAS:528:DC%2BD28Xht1SmsbbJ 17084815 (Pubitemid 44708852)
3. SC Barber RJ Mead PJ Shaw 2006 Oxidative stress in ALS: a mechanism of neurodegeneration and a therapeutic target Biochim Biophys Acta 1762 1051 1067 1:CAS:528:DC%2BD28Xht1CgsLnJ 16713195
4. E Bertrand E Brouillet I Caille C Bouillot GM Cole A Prochiantz, et al. 2001 A short cytoplasmic domain of the amyloid precursor protein induces apoptosis in vitro and in vivo Mol Cell Neurosci 18 503 511 10.1006/mcne.2001. 1030 1:CAS:528:DC%2BD3MXosFGgtrg%3D 11922141 (Pubitemid 34008390)
5. LI Bruijn TM Miller DW Cleveland 2004 Unraveling the mechanisms involved in motor neuron degeneration in ALS Annu Rev Neurosci 27 723 740 10.1146/annurev.neuro.27.070203.144244 1:CAS:528:DC%2BD2cXmslantbw%3D 15217349 (Pubitemid 39050419)
6. C Cande F Cecconi P Dessen G Kroemer 2002 Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J Cell Sci 115 4727 4734 10.1242/jcs.00210 1:CAS:528:DC%2BD3sXis1Kkuw%3D%3D 12432061 (Pubitemid 36054627)
7. C Cande N Vahsen I Kouranti E Schmitt E Daugas C Spahr, et al. 2004 AIF and cyclophilin A cooperate in apoptosis-associated chromatinolysis Oncogne 23 1514 1521 10.1038/sj.onc.1207279 1:CAS:528:DC%2BD2cXhsFOht7w%3D (Pubitemid 38406513)
8. CT Cao RS Clark W Pei W Yin F Zhang FY Sun, et al. 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 10.1097/01.WCB.0000087090.01171.E7 1:CAS:528: DC%2BD3sXnslaqsLc%3D 14526224
9. MT Carri A Ferri M Cozzolino L Calabrese G Rotilio 2003 Neurodegeneration in amyotrophic lateral sclerosis: the role of oxidative stress and altered homeostasis of metals Brain Res Bull 61 365 374 10.1016/S0361-9230(03)00179-5 1:CAS:528:DC%2BD3sXlvFygtbw%3D 12909279 (Pubitemid 36945467)
10. EC Cheung L Melanson-Drapeau SP Cregan JL Vanderluit KL Ferguson WC McIntosh, et al. 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 10.1523/JNEUROSCI.4261-04.2005 1:CAS:528:DC%2BD2MXhs1Kmur4%3D 15703386 (Pubitemid 40250708)
11. KJ Cho YH Chung C Shin DH Shin YS Kim ME Gurney, et al. 1999 Reactive strocytes express p53 in the spinal cord of transgenic mice expressing a human Cu/Zn mutation Neuro Report 10 3939 3943 1:CAS:528:DC%2BD3cXjsFyrsw%3D%3D
12. YH Chung KM Joo YJ Lee DH Shin CI Cha 2004 Reactive astrocytes express PARP in the central nervous system of SOD (G93A) transgenic mice Brain Res 1003 199 204 10.1016/j.brainres.2004.01.010 1:CAS:528:DC%2BD2cXhvFaitbg%3D 15019581 (Pubitemid 38317102)
13. JC Corona LB Tovar-y-Romo R Tapia 2007 Glutamate excitotoxicity and therapeutic targets for amyotrophic lateral sclerosis Expert Onin Ther Targets 11 1415 1428 10.1517/14728222.11.11.1415 1:CAS:528:DC%2BD2sXht1amsbnI (Pubitemid 350200478)
14. SP Cregan VI Dawson RS Slack 2004 Role of AIF in caspase-dependent and caspase-independent cell death Oncogene 23 2785 2796 10.1038/sj.onc.1207517 1:CAS:528:DC%2BD2cXivFKms7k%3D 15077142 (Pubitemid 38638842)
15. C Culmsee C Zhu S Landshamer B Becattini E Wagner M Pellecchia, et al. 2005 Apoptosis-inducing factor triggered by poly(ADP-ribose) polymerase and Bid mediates neuronal cell death after oxygen-glucose deprivation and focal cerebral ischemia J Neurosci 25 10262 10272 10.1523/JNEUROSCI.2818-05.2005 1:CAS:528:DC%2BD2MXht1Wqt7%2FP 16267234 (Pubitemid 41636223)
16. N Ghoshal JF Smiley AJ DeMaggio MF Hoekstra EJ Cochran LI Binder, et al. 1999 A new molecular link between the fibrillar and granulovacuolar lesions of Alzheimer's disease Am J Pathol 155 1163 1172 1:CAS:528:DyaK1MXntFWmtrY%3D 10514399
17. A Giovanni E Keramaris EJ Morris ST Hou M O'Hare M Dyson, et al. 2000 E2F1 mediates death of β-amyloid-treated cortical neurons in a manner independent of p53 and dependent on Bax and caspase-3 J Biol Chem 275 11553 11560 10.1074/jbc.275.16.11553 1:CAS:528:DC%2BD3cXislyqur0%3D 10766769 (Pubitemid 30237711)
18. HC Ha 2004 Defective transcriptional factor activation for proinflammatory gene expression in poly(ADP-ribose) polymerase 1-deficient glia Proc Natl Acad Sci USA 101 5087 5092 10.1073/pnas.0306895101 1:CAS:528:DC%2BD2cXjsFCisbo%3D 15041747 (Pubitemid 38469207)
19. N Joza SA Susin E Daugas WI Stanford SK Cho CY Li, et al. 2001 Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death Nature 410 549 554 10.1038/35069004 1:CAS:528:DC%2BD3MXis1Grur4%3D 11279485 (Pubitemid 32267191)
20. SJ Kang S Wang H Hara EP Peterson S Namura S Amin-Hanjani, et al. 2000 Dual role of caspase-11 in mediating activation of caspase-1 and caspase-3 under pathological conditions J Cell Biol 149 613 622 10.1083/jcb.149.3.613 1:CAS:528:DC%2BD3cXivFKgu7w%3D 10791975 (Pubitemid 30252395)
21. SJ Kang I Sanchez N Jing J Yuan 2003 Dissociation between neurodegeneration and caspase-11-mediated activation of caspase-1 and caspase-3 in a mouse model of amyotrophic lateral sclerosis J Neurosci 23 5455 5460 1:CAS:528:DC%2BD3sXltl2qsrc%3D 12843244
22. M Kiaei K Kipiani J Chen NY Calingasan MF Beal 2005 Peroxisome proliferator-activated receptor-gamma agonist extends survival in transgenic mouse model of amyotrophic lateral sclerosis Exp Neurol 191 331 336 10.1016/j.expneurol.2004.10.007 1:CAS:528:DC%2BD2MXksFKisw%3D%3D 15649489 (Pubitemid 40092877)
23. SH Kim JS Henkel DR Beers IS Simpson JC Goodman JI Engelhardt, et al. 2003 PARP expression is increased in astrocytes but decreased in motor neurons in the spinal cord of sporadic ALS patients J Neuropathol Exp Neurol 62 88 103 1:CAS:528:DC%2BD3sXpsVKmsw%3D%3D 12528821
24. JA Klein CM Longo-Guess MP Rossmann KL Seburn RE Hurd WN Frankel, et al. 2002 The harlequin mouse mutation down-regulates apoptosis-inducing factor Nature 419 369 374 10.1038/nature01034
25. U Kolthur-Seetharam F Dantzer MW McBurney G de Murcia P Sassone-Corsi 2006 Control of AIF-mediated cell death by the functional interplay of SIRT1 and PARP-1 in response to DNA damage Cell Cycle 5 873 877 1:CAS:528: DC%2BD28XmvVGru7Y%3D 16628003
26. S Krantic N Mechawar S Reix R Quirion 2007 Apoptosis-inducing factor: a matter of neuron life and death Prog Neurobiol 81 179 196 10.1016/j.pneurobio. 2006.12.002 1:CAS:528:DC%2BD2sXitFOrsLo%3D 17267093 (Pubitemid 46282274)
27. Kusaka H, Hirano A (1999) Cytopathology of the motor neuron. In: Younger PA, Younger DS (eds) Motor disorders. Lippincott Williams & Wilkins, Philadelphia, pp 93-103
28. IC Lang-Rollin HJ Rideout M Noticewala L Stefanis 2003 Mechanisms of caspase-independent neuronal death: energy depletion and free radical generation J Neurosci 23 11015 11025 1:CAS:528:DC%2BD3sXpvV2gt7Y%3D 14657158
29. CL Liu BK Siesjo BR Hu 2004 Pathogenesis of hippocampal neuronal death after hypoxia-ischemia changes during brain development Neuroscience 127 113 123 10.1016/j.neuroscience.2004.03.062 1:CAS:528:DC%2BD2cXlt1ags7s%3D 15219674 (Pubitemid 38829157)
30. LJ Martin 1999 Neuronal death in amyotrophic lateral sclerosis is apoptosis: possible contribution of a programmed cell death mechanism J Neuropathol Exp Neurol 58 459 471 10.1097/00005072-199905000-00005 1:STN:280:DyaK1M3mtVaktQ%3D%3D 10331434
31. LJ Martin 2000 p53 is abnormally elevated and active in the CNS of patients with amyotrophic lateral sclerosis Neurobiol Dis 7 613 622 10.1006/nbdi.2000.0314 1:CAS:528:DC%2BD3cXoslSms7w%3D 11114260 (Pubitemid 32044286)
32. FM Menzies PG Ince PJ Shaw 2002 Mitochondrial involvement in amyotrophic lateral sclerosis Neurochem Int 40 543 551 10.1016/S0197-0186(01)00125-5 1:CAS:528:DC%2BD38XhtFyktbw%3D 11850111 (Pubitemid 34159155)
33. A Migheli C Atzori R Piva M Tortarolo M Girelli D Schiffer, et al. 1999 Lack of apoptosis in mice with ALS Nat Med 5 966 967 10.1038/12381 1:CAS:528:DyaK1MXlslGktLw%3D 10470053 (Pubitemid 29439556)
34. MD Miramar P Costantini L Ravagnan LM Saraiva D Haouzi G Brothers, et al. 2001 NADH oxidase activity of mitochondrial apoptosis-inducing factor J Biol Chem 276 16391 16398 10.1074/jbc.M010498200 1:CAS:528:DC%2BD3MXjvFaku78%3D 11278689
35. M Neumann DM Sampathu LK Kwong AC Truax MC Micsenyi TT Chou, et al. 2006 Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis Science 314 130 133 10.1126/science.1134108 1:CAS:528:DC%2BD28XhtVCiurrL 17023659 (Pubitemid 44547757)
36. C Neusch M Bähr C Schneider-Gold 2007 Glia cells in amyotrophic lateral sclerosis: new clues to understanding an old disease? Muscle Nerve 35 712 724 10.1002/mus.20768 1:CAS:528:DC%2BD2sXntFaitbs%3D 17373702 (Pubitemid 46835112)
37. YK Oh KS Shin SJ Kang 2006 AIF translocates to the nucleus in the spinal motor neurons in a mouse model of ALS Neurosci Lett 406 205 210 10.1016/j.neulet.2006.07.044 1:CAS:528:DC%2BD28XpsVOms70%3D 16916579 (Pubitemid 44311370)
38. H Otera S Ohsakaya Z Nagaura N Ishihara K Mihara 2005 Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space EMBO J 24 1375 1386 10.1038/sj.emboj.7600614 1:CAS:528:DC%2BD2MXjslGlt7Y%3D 15775970 (Pubitemid 40593058)
39. BM Polster G Basanez A Etxebarria JM Hardwick DG Nicholls 2005 Calpine I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria J Biol Chem 280 6447 6454 10.1074/jbc.M413269200 1:CAS:528:DC%2BD2MXhsV2qs78%3D 15590628 (Pubitemid 40341192)
40. S Reix N Mechawar SA Susin R Quirion S Krantic 2007 Expression of cortical and hippocampal apoptosis-inducing factor (AIF) in aging and Alzheimer's disease Neurobiol Aging 28 351 356 10.1016/j.neurobiolaging.2006.01. 003 1:CAS:528:DC%2BD2sXhtlantrY%3D 16504343 (Pubitemid 46177383)
41. CV Sapan RL Lundblad NC Price 1999 Colorimetric protein assay techniques Biotechnol Appl Biochem 29 99 108 1:CAS:528:DyaK1MXisFWntbk%3D 10075906
42. SA Sargsyan PN Monk PJ Shaw 2005 Microglia as potential contributors to motor neuron injury in amyotrophic lateral sclerosis Glia 51 241 253 10.1002/glia.20210 15846792 (Pubitemid 41532100)
43. 2 in cortical neurons J Neurochem 106 45 55 10.1111/j.1471-4159.2008.05347.x 1:CAS:528: DC%2BD1cXot1Ohurs%3D 18346200 (Pubitemid 351840199)
44. N Shibata A Hirano T Yamamoto Y Kato M Kobayashi 2000 Superoxide dismutase-1 mutation-related neurotoxicity in familial amyotrophic lateral sclerosis Amyotroph Lateral Scler 1 143 161 10.1080/14660820050515151 1:CAS:528:DC%2BD3cXmtVWqtbY%3D
45. N Shibata M Kawaguchi-Niida T Yamamoto S Toi A Hirano M Kobayashi 2008 Effects of the PPARγ activator pioglitazone on p38 MAP kinase and IκBα in the spinal cord of a transgenic mouse model of amyotrophic lateral sclerosis Neuropathology 28 387 398 10.1111/j.1440-1789.2008.00890.x 18312546 (Pubitemid 351798977)
46. C Stadelmann TL Deckwerth A Srinivasan C Bancher W Bruck K Jellinger, et al. 1999 Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease. Evidence for apoptotic cell death Am J Pathol 155 1459 1466 1:CAS:528:DyaK1MXnvVKisrc%3D 10550301
47. P Stambolsky L Weisz I Shats Y Klein N Goldfinger M Oren, et al. 2006 Regulation of AIF expression by p53 Cell Death Differ 13 2140 2149 10.1038/sj.cdd.4401965 1:CAS:528:DC%2BD28XhtF2nsrfN 16729031 (Pubitemid 44742697)
48. R Strosznajder R Gadamski M Walski 2005 Inhibition of poly(ADP-ribose) polymerase activity protects hippocampal cells against morphological and ultrastructural alteration evoked by ischemia-reperfusion injury Folia Neuropathol 43 156 165 1:CAS:528:DC%2BD2MXht1WjtrjF 16245211
49. SA Susin HK Lorenzo N Zamzami I Marzo BE Snow GM Brothers, et al. 1999 Molecular characterization of mitochondrial apoptosis-inducing factor Nature 397 441 446 10.1038/17135 1:CAS:528:DyaK1MXhtFOhu78%3D 9989411
50. NA Sutedja JH Veldink K Fischer H Kromhout D Heederik MH Huisman, et al. 2008 Exposure to chemicals and metals and risk of amyotrophic lateral sclerosis: a systematic review Amyotroph Lateral Scler 8 1 20
51. B Tomik D Adamek P Pierzchalski S Banares A Duda D Paryka, et al. 2005 Does apoptosis occur in amyotrophic lateral sclerosis? TUNEL experience from human amyotrophic lateral sclerosis (ALS) tissues Folia Neuropathol 43 75 80 16012908
52. M Tortarolo P Veglianese N Calvaresi A Botturi C Rossi A Giorgini, et al. 2003 Persistent activation of p38 mitogen-activated protein kinase in a mouse model of familial amyotrophic lateral sclerosis correlates with disease progression Mol Cell Neurosci 23 180 192 10.1016/S1044-7431(03)00022-8 1:CAS:528:DC%2BD3sXksF2htrg%3D 12812752 (Pubitemid 36703155)
53. van den Bosch, Van Damme P, Bogaert E, Robberecht W (2006) The role of excitotoxicity in the pathogenesis of amyotrophic lateral sclerosis. Biochim Biophys Acta 1762:1068-1082
54. SJ van Wijk GJ Hageman 2005 Poly(ADP-ribosse) polymerase-1 mediated caspase-independent cell death after ischemia/reperfusion Free Radic Biol Med 39 81 90 15925280
55. M Yamazaki E Esumi I Nakano 2005 Is motor neuron cell death in amyotrophic lateral sclerosis apoptosis? Neuropathology 25 381 387 10.1111/j.1440-1789.2005.00648.x 16382789
56. SW Yu H Wang TM Dawson VL Dawson 2003 Poly(ADP-ribose) polymerase-1 and apoptosis-inducing factor in neurotoxicity Neurobiol Dis 14 303 317 10.1016/j.nbd.2003.08.008 1:CAS:528:DC%2BD3sXpvVWks7Y%3D 14678748 (Pubitemid 37543510)
57. VJ Yuste RS Moubarak C Delettre M Bras P Sancho N Robert, et al. 2005 Cysteine protease inhibition prevents mitochondrial apoptosis-inducing factor (AIF) release Cell Death Differ 12 1445 1448 10.1038/sj.cdd.4401687 1:CAS:528:DC%2BD2MXhtV2kt73P 15933737 (Pubitemid 41521936)
58. X Zhang J Chen SH Graham L Du PM Kochaneck R Draviam, et al. 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 10.1046/j.1471-4159.2002.00975.x 1:CAS:528:DC%2BD38XlsV2jtrs%3D 12091479 (Pubitemid 34755263)
59. C Zhu X Wang L Qui C Peeters-Scholte H Hagberg K Blomgren 2004 Nitrosylation precedes caspase-3 activation and translocation of apoptosis-inducing factor in neonatal rat cerebral hypoxia-ischaemia J Neurochem 90 462 471 10.1111/j.1471-4159.2004.02500.x 1:CAS:528:DC%2BD2cXmtVyrt7g%3D 15228602 (Pubitemid 38938231)