Calpain plays a central role in 1-methyl-4-phenylpyridinium (MPP(+))-induced neurotoxicity in cerebellar granule neurons

Neurotoxicity Research

Volumn 19, Issue 3, 2011, Pages 374-388

  Harbison, Richard A ^a   Ryan, Kristen R ^b   Wilkins, Heather M ^a   Schroeder, Emily K ^c   Loucks, F Alexandra ^d   Bouchard, Ron J ^c   Linseman, Daniel A ^a,c,e  

^a UNIVERSITY OF DENVER   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Bcl 2; Calpain; Cerebellar granule neurons; MPP(+); Neurotoxicity; Oxidative stress

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; CALPAIN; CASPASE 3; CASPASE 7; CYCLIN E; DNA FRAGMENT; FODRIN; GLUTATHIONE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROCASPASE 3; PROCASPASE 9; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL CYCLE; CEREBELLAR GRANULE NEURON; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; MITOCHONDRION; NEUROTOXICITY; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN TARGETING; RAT;

1-METHYL-4-PHENYLPYRIDINIUM; AMINO ACID SEQUENCE; ANIMALS; CALPAIN; CELL LINE, TUMOR; CELLS, CULTURED; CEREBELLUM; CYTOPLASMIC GRANULES; HUMANS; MOLECULAR SEQUENCE DATA; NEURONS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 79951942418     PISSN: 10298428     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12640-010-9172-4     Document Type: Article

References (66)

1. D Alvira M Tajes E Verdaguer SG de Arriba C Allgaier C Matute R Trullas A Jiménez M Pallàs A Camins 2007 Inhibition of cyclin-dependent kinases is neuroprotective in 1-methyl-4-phenylpyridinium-induced apoptosis in neurons Neuroscience 146 350 365 1:CAS:528:DC%2BD2sXkslais7g%3D 10.1016/j.neuroscience.2007.01.042 17343987 (Pubitemid 46654625)
2. V Anantharam S Kaul C Song A Kanthasamy AG Kanthasamy 2007 Pharmacological inhibition of neuronal NADPH oxidase protects against 1-methyl-4-phenylpyridinium (MPP +)-induced oxidative stress and apoptosis in mesencephalic dopaminergic neuronal cells Neurotoxicology 28 988 997 1:CAS:528:DC%2BD2sXhtFehsr7F 10.1016/j.neuro.2007.08.008 17904225 (Pubitemid 47519806)
3. N Bizat JM Hermel S Humbert C Jacquard C Créminon C Escartin F Saudou S Krajewski P Hantraye E Brouillet 2003 In vivo calpain/caspase cross-talk during 3-nitropropionic acid-induced striatal degeneration: implication of a calpain-mediated cleavage of active caspase-3 J Biol Chem 278 43245 43253 1:CAS:528:DC%2BD3sXosFSku7w%3D 10.1074/jbc.M305057200 12917435 (Pubitemid 37345944)
4. K Blomgren C Zhu X Wang JO Karlsson AL Leverin BA Bahr C Mallard H Hagberg 2001 Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia J Biol Chem 276 10191 10198 1:CAS:528:DC%2BD3MXis1Oktrs%3D 10.1074/jbc.M007807200 11124942
5. J Bo BY Ming LZ Gang C Lei AL Jia 2005 Protection by puerarin against MPP+-induced neurotoxicity in PC12 cells mediated by inhibiting mitochondrial dysfunction and caspase-3-like activation Neurosci Res 53 183 188 1:CAS:528:DC%2BD2MXpslCht7w%3D 10.1016/j.neures.2005.06.014 16112764 (Pubitemid 41219535)
6. X Cao X Deng WS May 2003 Cleavage of Bax to p18 Bax accelerates stress-induced apoptosis, and a cathepsin-like protease may rapidly degrade p18 Bax Blood 102 2605 2614 1:CAS:528:DC%2BD3sXnslykurk%3D 10.1182/blood-2003-01- 0211 12816867 (Pubitemid 37193602)
7. M Chen H He S Zhan S Krajewski JC Reed RA Gottlieb 2001 Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion J Biol Chem 276 30724 30728 1:CAS:528:DC%2BD3MXmsVaqt70%3D 10.1074/jbc.M103701200 11404357
8. EH Cheng MC Wei S Weiler RA Flavell TW Mak T Lindsten SJ Korsmeyer 2001 BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis Mol Cell 8 705 711 1:CAS:528: DC%2BD3MXnslGmt7s%3D 10.1016/S1097-2765(01)00320-3 11583631 (Pubitemid 32946946)
9. YF Cheng GQ Zhu M Wang H Cheng A Zhou N Wang N Fang XC Wang XQ Xiao ZW Chen QL Li 2009 Involvement of ubiquitin proteasome system in protective mechanisms of puerarin to MPP(+)-elicited apoptosis Neurosci Res 63 52 58 1:CAS:528:DC%2BD1cXhsFahtbrF 10.1016/j.neures.2008.10.009 19022306
10. WS Choi EH Lee CW Chung YK Jung BK Jin SU Kim TH Oh TC Saido YJ Oh 2001 Cleavage of Bax is mediated by caspase-dependent or-independent calpain activation in dopaminergic neuronal cells: protective role of Bcl-2 J Neurochem 77 1531 1541 1:CAS:528:DC%2BD3MXkslWnurg%3D 10.1046/j.1471-4159.2001.00368.x 11413236 (Pubitemid 32574488)
11. WS Choi E Lee J Lim YJ Oh 2008 Calbindin-D28K prevents drug-induced dopaminergic neuronal death by inhibiting caspase and calpain activity Biochem Biophys Res Commun 371 127 131 1:CAS:528:DC%2BD1cXlvVWgsbo%3D 10.1016/j.bbrc.2008.04.020 18413141
12. CT Chu JH Zhu G Cao A Signore S Wang J Chen 2005 Apoptosis inducing factor mediates caspase-independent 1-methyl-4-phenylpyridinium toxicity in dopaminergic cells J Neurochem 94 1685 1695 1:CAS:528:DC%2BD2MXhtVaksbvL 10.1111/j.1471-4159.2005.03329.x 16156740 (Pubitemid 41324649)
13. BT Chua K Guo P Li 2000 Direct cleavage by the calcium-activated protease calpain can lead to inactivation of caspases J Biol Chem 275 5131 5135 1:CAS:528:DC%2BD3cXhsVymtrk%3D 10.1074/jbc.275.7.5131 10671558 (Pubitemid 30108915)
14. SR D'Mello C Galli T Ciotti P Calissano 1993 Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP Proc Natl Acad Sci USA 90 10989 10993 10.1073/pnas.90.23.10989 8248201 (Pubitemid 23354354)
15. WX Ding HM Ni D DiFrancesca DB Stolz XM Yin 2004 Bid-dependent generation of oxygen radicals promotes death receptor activation-induced apoptosis in murine hepatocytes Hepatology 40 403 413 1:CAS:528:DC%2BD2cXnsFygur8%3D 10.1002/hep.20310 15368445 (Pubitemid 39062858)
16. AF Domingues AR Esteves RH Swerdlow CR Oliveira SM Cardoso 2008 Calpain-mediated MPP+ toxicity in mitochondrial DNA depleted cells Neurotox Res 13 31 38 1:CAS:528:DC%2BD1cXntV2ns7k%3D 10.1007/BF03033365 18367438
17. YS Du RC Dodel KR Bales R Jemmerson E Hamilton-Byrd SM Paul 1997 Involvement of a caspase-3-like cysteine protease in 1-methyl-4-phenypyridinium- mediated apoptosis of cultured cerebellar granule neurons J Neurochem 69 1382 1388 1:CAS:528:DyaK2sXmsVCks78%3D 10.1046/j.1471-4159.1997.69041382.x 9326266 (Pubitemid 27406938)
18. O Ekshyyan TY Aw 2004 Apoptosis: a key in neurodegenerative disorders Curr Neurovasc Res 1 355 371 1:CAS:528:DC%2BD2cXos1entb4%3D 10.2174/ 1567202043362018 16181084
19. G Gao QP Dou 2000 N-terminal cleavage of bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes bcl-2-independent cytochrome c release and apoptotic cell death J Cell Biochem 80 53 72 1:CAS:528: DC%2BD3cXot1Glsrw%3D 10.1002/1097-4644(20010101)80:1<53::AID-JCB60>3.0. CO;2-E 11029754
20. RA González-Polo A Mora N Clemente G Sabio F Centeno G Soler JM Fuentes 2001 Mechanisms of MPP(+) incorporation into cerebellar granule cells Brain Res Bull 56 119 123 10.1016/S0361-9230(01)00610-4 11704348 (Pubitemid 33026454)
21. RA González-Polo G Soler JC Alonso A Rodríguez- Martín JM Fuentes 2003 MPP(+) causes inhibition of cellular energy supply in cerebellar granule cells Neurotoxicology 24 219 225 10.1016/S0161-813X(02) 00164-X 12606294 (Pubitemid 36288101)
22. RA González-Polo G Soler A Alvarez I Fabregat JM Fuentes 2003 Vitamin E blocks early events induced by 1-methyl-4-phenylpyridinium (MPP +) in cerebellar granule cells J Neurochem 84 305 315 10.1046/j.1471-4159.2003.01520.x 12558993 (Pubitemid 36182272)
23. RA González-Polo G Soler JM Fuentes 2004 MPP+: mechanism for its toxicity in cerebellar granule cells Mol Neurobiol 30 253 264 10.1385/MN:30:3:253 15655251 (Pubitemid 41264549)
24. BS Han HS Hong WK Choi GJ Markelonis TH Oh YJ Oh 2003 Caspase-dependent and-independent cell death pathways in primary cultures of mesencephalic dopaminergic neurons after neurotoxin treatment J Neurosci 23 5069 5078 1:CAS:528:DC%2BD3sXltlent70%3D 12832530 (Pubitemid 36793234)
25. RM Harwell DC Porter C Danes K Keyomarsi 2000 Processing of cyclin E differs between normal and tumor breast cells Cancer Res 60 481 489 1:CAS:528:DC%2BD3cXhtVahtr4%3D 10667604 (Pubitemid 30070779)
26. T Itoh H Itoh D Pleasure 2003 Bcl-2-related protein family gene expression during oligodendroglial differentiation J Neurochem 85 1500 1512 1:CAS:528:DC%2BD3sXkslOktLk%3D 10.1046/j.1471-4159.2003.01795.x 12787069 (Pubitemid 36702562)
27. YM Janumyan CG Sansam A Chattopadhyay N Cheng EL Soucie LZ Penn D Andrews CM Knudson E Yang 2003 Bcl-xL/Bcl-2 coordinately regulates apoptosis, cell cycle arrest and cell cycle entry EMBO J 22 5459 5470 1:CAS:528: DC%2BD3sXot1Cruro%3D 10.1093/emboj/cdg533 14532118 (Pubitemid 37279955)
28. KL Jordan-Sciutto LM Malaiyandi R Bowser 2002 Altered distribution of cell cycle transcriptional regulators during Alzheimer disease J Neuropathol Exp Neurol 61 358 367 1:CAS:528:DC%2BD38XjtFSlur0%3D 11939591 (Pubitemid 34266787)
29. H Jourdi L Hamo T Oka A Seegan M Baudry 2009 BDNF mediates the neuroprotective effects of positive AMPA receptor modulators against MPP(+)-induced toxicity in cultured hippocampal and mesencephalic slices Neuropharmacology 56 876 885 1:CAS:528:DC%2BD1MXkt1Sitrs%3D 10.1016/j. neuropharm.2009.01.015 19371576
30. K Keyomarsi TW Herliczek 1997 The role of cyclin E in cell proliferation, development and cancer Prog Cell Cycle Res 3 171 191 1:CAS:528: DyaK1cXivFWqtrg%3D 9552414
31. K Keyomarsi AB Pardee 1993 Redundant cyclin overexpression and gene amplification in breast cancer cells Proc Natl Acad Sci USA 90 1112 1116 1:CAS:528:DyaK3sXhvVyqsrY%3D 10.1073/pnas.90.3.1112 8430082 (Pubitemid 23053961)
32. K Keyomarsi D Conte Jr W Toyofuku MP Fox 1995 Deregulation of cyclin E in breast cancer Oncogene 11 941 950 1:STN:280:DyaK2MvgsFylsg%3D%3D 7675453
33. NK Kim BH Choi X Huang BJ Snyder S Bukhari TH Kong H Park HC Park SR Park Y Ha 2009 Granulocyte-macrophage colony-stimulating factor promotes survival of dopaminergic neurons in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine- induced murine Parkinson's disease model Eur J Neurosci 29 891 900 10.1111/j.1460-9568.2009.06653.x 19245369
34. G Kroemer L Galluzi P Vandenabeele J Abrams ES Alneri EH Baehrecke MV Blagosklonny WS El-Deiry P Golstein DR Green M Hengartner RA Knight S Kumar SA Lipton W Malorni G Nuñez ME Peter J Tscopp J Yuan M Piacentini B Zhivotovsky G Melino 2009 Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009 Cell Death Differ 16 3 11 1:CAS:528:DC%2BD1cXhsV2it7%2FK 10.1038/cdd.2008.150 18846107
35. M Leist C Volbracht E Fava P Nicotera 1998 1-Methyl-4-phenylpyridinium induces autocrine excitotoxicity, protease activation, and neuronal apoptosis Mol Pharmacol 54 789 801 1:CAS:528:DyaK1cXntlOntLo%3D 9804614 (Pubitemid 28523171)
36. -/+ mice Free Radic Biol Med 36 542 554 1:CAS:528:DC%2BD2cXhsFWktLk%3D 10.1016/j.freeradbiomed.2003.11.029 14980699 (Pubitemid 38230173)
37. SJ Libertini BS Robinson NK Dhillon D Glick M George S Dandekar JP Gregg E Sawai M Mudryj 2005 Cyclin E both regulates and is regulated by calpain 2, a protease associated with metastatic breast cancer phenotype Cancer Res 65 10700 10708 1:CAS:528:DC%2BD2MXht1Gqu7fJ 10.1158/0008-5472.CAN-05-1666 16322214 (Pubitemid 41713337)
38. DA Linseman RA Phelps RJ Bouchard SS Le TA Laessig ML McClure KA Heidenreich 2002 Insulin-like growth factor-I blocks Bcl-2 interacting mediator of cell death (Bim) induction and intrinsic death signaling in cerebellar granule neurons J Neurosci 22 9287 9297 1:CAS:528:DC%2BD3sXmsVems7k%3D 12417654 (Pubitemid 35356172)
39. DA Linseman BD Butts TA Precht RA Phelps SS Le TA Laessig RJ Bouchard ML Florez-McClure KA Heidenreich 2004 Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis J Neurosci 24 9993 10002 1:CAS:528:DC%2BD2cXhtVWht7%2FK 10.1523/JNEUROSCI.2057-04. 2004 15525785 (Pubitemid 39463581)
40. FA Loucks SS Le AK Zimmermann KR Ryan H Barth K Aktories DA Linseman 2006 Rho family GTPase inhibition reveals opposing effects of mitogen-activated protein kinase kinase/extracellular signal-regulated kinase and Janus kinase/signal transducer and activator of transcription signaling cascades on neuronal survival J Neurochem 97 957 967 1:CAS:528:DC%2BD28XlsVOntr4%3D 10.1111/j.1471-4159.2006.03802.x 16686690
41. FA Loucks EK Schroeder AE Zommer S Hilger NA Kelsey RJ Bouchard C Blackstone JL Brewster DA Linseman 2009 Caspases indirectly regulate cleavage of the mitochondrial fusion GTPase OPA1 in neurons undergoing apoptosis Brain Res 1250 63 74 1:CAS:528:DC%2BD1MXkt1WisA%3D%3D 10.1016/j.brainres.2008.10.081 19046944
42. A Mandic K Viktorsson L Strandberg T Heiden J Hansson S Linder MC Shoshan 2002 Calpain-mediated Bid cleavage and calpain-independent Bak modulation: two separate pathways in cisplatin-induced apoptosis Mol Cell Biol 22 3003 3013 1:CAS:528:DC%2BD38XivFylsbo%3D 10.1128/MCB.22.9.3003-3013.2002 11940658 (Pubitemid 34437459)
43. SJ Martin DR Green TG Cotter 1994 Dicing with death: dissecting the components of the apoptosis machinery Trends Biochem Sci 19 26 30 1:STN:280:DyaK2c7ovV2hug%3D%3D 10.1016/0968-0004(94)90170-8 8140617 (Pubitemid 24028728)
44. KM McGinnis ME Gnegy YH Park N Mukerjee KK Wang 1999 Procaspase-3 and poly(ADP)ribose polymerase (PARP) are calpain substrates Biochem Biophys Res Commun 263 94 99 1:CAS:528:DyaK1MXlvVWquro%3D 10.1006/bbrc.1999.1315 10486259 (Pubitemid 29443645)
45. R Nath KJ Raser D Stafford I Hajimohammadreza A Posner H Allen RV Talanian P Yuen RB Gilbertsen KK Wang 1996 Non-erythroid alpha-spectrin breakdown by calpain and interleukin 1 beta-converting-enzyme-like protease(s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis Biochem J 319 Pt 3 683 690 1:CAS:528:DyaK28Xnt1Gmt7o%3D 8920967 (Pubitemid 26386177)
46. RW Neumar YA Xu H Gada RP Guttmann R Siman 2003 Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis J Biol Chem 278 14162 14167 1:CAS:528:DC%2BD3sXjtVShsrw%3D 10.1074/jbc.M212255200 12576481 (Pubitemid 36799963)
47. MA O'Brien RA Moravec TL Riss 2001 Poly (ADP-ribose) polymerase cleavage monitored in situ in apoptotic cells Biotechniques 30 886 891 11314271 (Pubitemid 32319834)
48. M Okouchi O Ekshyyan M Maracine TY Aw 2007 Neuronal apoptosis in neurodegeneration Antioxid Redox Signal 9 1059 1096 1:CAS:528: DC%2BD2sXot1Wktrc%3D 10.1089/ars.2007.1511 17571960 (Pubitemid 47080820)
49. LL Rubin CL Gatchalian G Rimon SF Brooks 1994 The molecular mechanisms of neuronal apoptosis Curr Opin Neurobiol 4 696 702 1:CAS:528:DyaK2MXhvFGjtL8%3D 10.1016/0959-4388(94)90012-4 7849526 (Pubitemid 24325312)
50. ME Saez R Ramirez-Lorca FJ Moron A Ruiz 2006 The therapeutic potential of the calpain family: new aspects Drug Discov Today 11 917 923 1:CAS:528:DC%2BD28XpvFSis74%3D 10.1016/j.drudis.2006.08.009 16997142 (Pubitemid 44425428)
51. T Shang AV Uihlein J Van Asten B Kalyanaraman CJ Hillard 2003 1-Methyl-4-phenylpyridinium accumulates in cerebellar granule neurons via organic cation transporter 3 J Neurochem 85 358 367 1:CAS:528: DC%2BD3sXjtlylsr0%3D 10.1046/j.1471-4159.2003.01686.x 12675912 (Pubitemid 36438331)
52. AA Starkov BM Polster G Fiskum 2002 Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax J Neurochem 83 220 228 1:CAS:528:DC%2BD38XnvVGgtro%3D 10.1046/j.1471-4159.2002.01153.x 12358746
53. P Tompa P Buzder-Lantos A Tantos A Farkas A Szilágyi Z Bánóczi F Hudecz P Friedrich 2004 On the sequential determinants of calpain cleavage J Biol Chem 279 20775 20785 1:CAS:528:DC%2BD2cXjvV2ns7s%3D 10.1074/jbc.M313873200 14988399 (Pubitemid 38656474)
54. SQ Wales JM Laing L Chen L Aurelian 2008 ICP10PK inhibits calpain-dependent release of apoptosis-inducing factor and programmed cell death in response to the toxin MPP+ Gene Ther 15 1397 1409 1:CAS:528: DC%2BD1cXht1Siu7zP 10.1038/gt.2008.88 18496573
55. +-induced cytotoxicity Neurosci Res 51 129 138 1:CAS:528:DC%2BD2MXosVOjtw%3D%3D 10.1016/j.neures.2004.10.001 15681030 (Pubitemid 40164948)
56. XD Wang JL Rosales A Magliocco R Gnanakumar KY Lee 2003 Cyclin E in breast tumors is cleaved into its low molecular weight forms by calpain Oncogene 22 769 774 1:CAS:528:DC%2BD3sXoslOksw%3D%3D 10.1038/sj.onc.1206166 12569370 (Pubitemid 36269291)
57. MC Wei WX Zong EH Cheng T Lindsten V Panoutsakopoulou AJ Ross KA Roth GR MacGregor CB Thompson SJ Korsmeyer 2001 Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death Science 292 727 730 1:CAS:528:DC%2BD3MXjt1eltr0%3D 10.1126/science.1059108 11326099 (Pubitemid 32385543)
58. J Wesierska-Gadek M Gueorguieva J Wojciechowski S Tudzarova-Trajkovska 2004 In vivo activated caspase-3 cleaves PARP-1 in rat liver after administration of the hepatocarcinogen N-nitrosomomorpholine (NNM) generating the 85 kDa fragment J Cell Biochem 93 774 787 1:CAS:528:DC%2BD2cXpvVCgur8%3D 10.1002/jcb.20181 15660421 (Pubitemid 44264173)
59. SN Willis JM Adams 2005 Life in the balance: how BH3-only proteins induce apoptosis Curr Opin Cell Biol 17 617 625 1:CAS:528:DC%2BD2MXhtFyksL%2FO 10.1016/j.ceb.2005.10.001 16243507 (Pubitemid 41540411)
60. DE Wood EW Newcomb 2000 Cleavage of Bax enhances its cell death function Exp Cell Res 256 375 382 1:CAS:528:DC%2BD3cXisFelu70%3D 10.1006/excr.2000.4859 10772810 (Pubitemid 30244196)
61. Y Yang DS Geldmacher K Herrup 2001 DNA replication precedes neuronal cell death in Alzheimer's disease J Neurosci 21 2661 2668 1:CAS:528: DC%2BD3MXjtVWku7s%3D 11306619 (Pubitemid 32298208)
62. Y Yang EJ Mufson K Herrup 2003 Neuronal cell death is preceded by cell cycle events at all stages of Alzheimer's disease J Neurosci 23 2557 2563 1:CAS:528:DC%2BD3sXjtFCnsbg%3D 12684440 (Pubitemid 36418589)
63. Yang L, Zhao K, Calingasan NY, Luo G, Szeto HH, Beal F (2009) Mitochondria targeted peptides protect against 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine neurotoxicity. Antioxid Redox Signal. Epub 2009 Feb 9
64. M Zatz A Starling 2005 Calpains and disease N Engl J Med 352 2413 2423 1:CAS:528:DC%2BD2MXltVCjtr4%3D 10.1056/NEJMra043361 15944426 (Pubitemid 40958438)
65. Z Zhang SF Larner MC Liu W Zheng RL Hayes KKW Wang 2009 Multiple alphaII-spectrin breakdown products distinguish calpain and caspase dominated necrotic and apoptotic cell death pathways Apoptosis 14 1289 1298 1:CAS:528:DC%2BD1MXht1artb%2FL 10.1007/s10495-009-0405-z 19771521
66. AK Zimmermann FA Loucks EK Schroeder RJ Bouchard KL Tyler DA Linseman 2007 Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria J Biol Chem 282 29296 29304 1:CAS:528:DC%2BD2sXhtV2ntbjK 10.1074/jbc.M702853200 17690097 (Pubitemid 350043369)