The human G93A-superoxide dismutase-1 mutation, mitochondrial glutathione and apoptotic cell death

Neurochemical Research

Volumn 34, Issue 10, 2009, Pages 1847-1856

  Muyderman, H ^a   Hutson, P G ^a   Matusica, D ^a   Rogers, M L ^a   Rush, R A ^a  

^a FLINDERS UNIVERSITY   (Australia)

Author keywords

Amyotrophic lateral sclerosis; Motor neuron; NSC 34; Oxidative stress; Transgenic

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE;

AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; CELL DEATH; CELL SURVIVAL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; GENE; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HYPOTHESIS; MITOCHONDRION; MOTONEURON; MOTOR PERFORMANCE; NERVE CELL NECROSIS; NERVE DEGENERATION; NERVE FUNCTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW;

ALANINE; AMINO ACID SUBSTITUTION; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; APOPTOSIS; CELL DEATH; GLUTATHIONE; GLYCINE; HUMANS; MITOCHONDRIA; MOTOR NEURONS; OXIDATIVE STRESS; SUPEROXIDE DISMUTASE;

EID: 69049087653     PISSN: 03643190     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11064-009-9974-z     Document Type: Review

References (104)

1. S Boillee VC Vande DW Cleveland 2006 ALS: a disease of motor neurons and their nonneuronal neighbors Neuron 52 39 59 10.1016/j.neuron.2006.09.018
2. BR Brooks 1996 Clinical epidemiology of amyotrophic lateral sclerosis Neurol Clin 14 399 420 10.1016/S0733-8619(05)70264-4
3. V McGuire WT Longstreth Jr TD Koepsell G van Belle 1996 Incidence of amyotrophic lateral sclerosis in three counties in western Washington state Neurology 47 571 573
4. DW Mulder 1982 Clinical limits of amyotrophic lateral sclerosis Adv Neurol 36 15 22
5. DR Rosen T Siddique D Patterson DA Figlewicz P Sapp A Hentati D Donaldson J Goto JP O'Regan HX Deng 1993 Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis Nature 362 59 62 10.1038/362059a0
6. LI Bruijn TM Miller DW Cleveland 2004 Unraveling the mechanisms involved in motor neuron degeneration in ALS Annu Rev Neurosci 27 723 749 10.1146/annurev.neuro.27.070203.144244
7. M Gaudette M Hirano T Siddique 2000 Current status of SOD1 mutations in familial amyotrophic lateral sclerosis Amyotroph Lateral Scler Other Motor Neuron Disord 1 83 89 10.1080/14660820050515377
8. ME Gurney H Pu AY Chiu MC Dal Canto CY Polchow DD Alexander J Caliendo A Hentati YW Kwon HX Deng 1994 Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation Science 264 1772 1775 10.1126/science.8209258
9. M Nagai M Aoki I Miyoshi M Kato P Pasinelli N Kasai RH Brown Jr Y Itoyama 2001 Rats expressing human cytosolic copper-zinc superoxide dismutase transgenes with amyotrophic lateral sclerosis: associated mutations develop motor neuron disease J Neurosci 21 9246 9254
10. JP Julien J Kriz 2006 Transgenic mouse models of amyotrophic lateral sclerosis Biochim Biophys Acta 1762 1013 1024
11. AY Chiu P Zhai MC Dal Canto TM Peters YW Kwon SM Prattis ME Gurney 1995 Age-dependent penetrance of disease in a transgenic mouse model of familial amyotrophic lateral sclerosis Mol Cell Neurosci 6 349 362 10.1006/mcne.1995.1027
12. A Pramatarova J Laganiere J Roussel K Brisebois GA Rouleau 2001 Neuron-specific expression of mutant superoxide dismutase 1 in transgenic mice does not lead to motor impairment J Neurosci 21 3369 3374
13. D Jaarsma E Teuling ED Haasdijk CI De Zeeuw CC Hoogenraad 2008 Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice J Neurosci 28 2075 2088 10.1523/JNEUROSCI.5258-07.2008
14. M Nagai DB Re T Nagata A Chalazonitis TM Jessell H Wichterle S Przedborski 2007 Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons Nat Neurosci 10 615 622 10.1038/nn1876
15. MR Vargas M Pehar PJ Diaz-Amarilla JS Beckman L Barbeito 2008 Transcriptional profile of primary astrocytes expressing ALS-linked mutant SOD1 J Neurosci Res 86 3515 3525 10.1002/jnr.21797
16. K Yamanaka SJ Chun S Boillee N Fujimori-Tonou H Yamashita DH Gutmann R Takahashi H Misawa DW Cleveland 2008 Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis Nat Neurosci 11 251 253 10.1038/nn2047
17. PN Monk PJ Shaw 2006 ALS: life and death in a bad neighborhood Nat Med 12 885 887 10.1038/nm0806-885
18. DR Borchelt 2006 Amyotrophic lateral sclerosis-are microglia killing motor neurons? N Engl J Med 355 1611 1613 10.1056/NEJMcibr064358
19. DW Cleveland JD Rothstein 2001 From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS Nat Rev Neurosci 2 806 819 10.1038/35097565
20. JS Beckman AG Estevez JP Crow L Barbeito 2001 Superoxide dismutase and the death of motoneurons in ALS Trends Neurosci 24 S15 S20 10.1016/S0166- 2236(00)01981-0
21. AG Reaume JL Elliott EK Hoffman NW Kowall RJ Ferrante DF Siwek HM Wilcox DG Flood MF Beal RH Brown Jr RW Scott WD Snider 1996 Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury Nat Genet 13 43 47 10.1038/ng0596-43
22. LI Bruijn MK Houseweart S Kato KL Anderson SD Anderson E Ohama AG Reaume RW Scott DW Cleveland 1998 Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1 Science 281 1851 1854 10.1126/science.281.5384.1851
23. P Pasinelli RH Brown 2006 Molecular biology of amyotrophic lateral sclerosis: insights from genetics Nat Rev Neurosci 7 710 723 10.1038/nrn1971
24. A Hirano H Donnenfeld S Sasaki I Nakano 1984 Fine structural observations of neurofilamentous changes in amyotrophic lateral sclerosis J Neuropathol Exp Neurol 43 461 470 10.1097/00005072-198409000-00001
25. BF Shaw JS Valentine 2007 How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein? Trends Biochem Sci 32 78 85 10.1016/j.tibs.2006.12.005
26. S Kato Y Saeki M Aoki M Nagai A Ishigaki Y Itoyama M Kato K Asayama A Awaya A Hirano E Ohama 2004 Histological evidence of redox system breakdown caused by superoxide dismutase 1 (SOD1) aggregation is common to SOD1-mutated motor neurons in humans and animal models Acta Neuropathol 107 149 158 10.1007/s00401-003-0791-1
27. AL Schwartz A Ciechanover 1999 The ubiquitin-proteasome pathway and pathogenesis of human diseases Annu Rev Med 50 57 74 10.1146/annurev.med.50.1.57
28. AL Strom J Gal P Shi EJ Kasarskis LJ Hayward H Zhu 2008 Retrograde axonal transport and motor neuron disease J Neurochem 106 495 505 10.1111/j.1471-4159. 2008.05393.x
29. F Zhang AL Strom K Fukada S Lee LJ Hayward H Zhu 2007 Interaction between familial amyotrophic lateral sclerosis (ALS)-linked SOD1 mutants and the dynein complex J Biol Chem 282 16691 16699 10.1074/jbc.M609743200
30. PJ Shaw 2005 Molecular and cellular pathways of neurodegeneration in motor neurone disease J Neurol Neurosurg Psychiatry 76 1046 1057 10.1136/jnnp.2004.048652
31. S Sathasivam PJ Shaw 2005 Apoptosis in amyotrophic lateral sclerosis-what is the evidence? Lancet Neurol 4 500 509 10.1016/S1474-4422(05)70142-3
32. H Nishitoh H Kadowaki A Nagai T Maruyama T Yokota H Fukutomi T Noguchi A Matsuzawa K Takeda H Ichijo 2008 ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1 Genes Dev 22 1451 1464 10.1101/gad.1640108
33. JA Johnston MJ Dalton ME Gurney RR Kopito 2000 Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis Proc Natl Acad Sci USA 97 12571 12576 10.1073/pnas.220417997
34. JP Crow JB Sampson Y Zhuang JA Thompson JS Beckman 1997 Decreased zinc affinity of amyotrophic lateral sclerosis-associated superoxide dismutase mutants leads to enhanced catalysis of tyrosine nitration by peroxynitrite J Neurochem 69 1936 1944
35. AG Estevez JP Crow JB Sampson C Reiter Y Zhuang GJ Richardson MM Tarpey L Barbeito JS Beckman 1999 Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase Science 286 2498 2500 10.1126/science.286.5449.2498
36. MB Yim JH Kang HS Yim HS Kwak PB Chock ER Stadtman 1996 A gain-of-function of an amyotrophic lateral sclerosis-associated Cu, Zn-superoxide dismutase mutant: an enhancement of free radical formation due to a decrease in Km for hydrogen peroxide Proc Natl Acad Sci USA 93 5709 5714 10.1073/pnas.93.12.5709
37. TL Williamson LB Corson L Huang A Burlingame J Liu LI Bruijn DW Cleveland 2000 Toxicity of ALS-linked SOD1 mutants Science 288 399 10.1126/science.288. 5465.399a
38. MM Harraz JJ Marden W Zhou Y Zhang A Williams VS Sharov K Nelson M Luo H Paulson C Schoneich JF Engelhardt 2008 SOD1 mutations disrupt redox-sensitive Rac regulation of NADPH oxidase in a familial ALS model J Clin Invest 118 659 670
39. M Polymenidou DW Cleveland 2008 Motor neuron disease: the curious ways of ALS Nature 454 284 285 10.1038/454284a
40. P Cassina A Cassina M Pehar R Castellanos M Gandelman A de Leon KM Robinson RP Mason JS Beckman L Barbeito R Radi 2008 Mitochondrial dysfunction in SOD1G93A-bearing astrocytes promotes motor neuron degeneration: prevention by mitochondrial-targeted antioxidants J Neurosci 28 4115 4122 10.1523/JNEUROSCI. 5308-07.2008
41. LG Bilsland N Nirmalananthan J Yip L Greensmith MR Duchen 2008 Expression of mutant SOD1 in astrocytes induces functional deficits in motoneuron mitochondria J Neurochem 107 1271 1283 10.1111/j.1471-4159.2008.05699.x
42. RU Pathak GP Davey 2008 Complex I and energy thresholds in the brain Biochim Biophys Acta 1777 777 782 10.1016/j.bbabio.2008.05.443
43. SE Browne AC Bowling MJ Baik M Gurney RH Brown Jr MF Beal 1998 Metabolic dysfunction in familial, but not sporadic, amyotrophic lateral sclerosis J Neurochem 71 281 287
44. FM Menzies MR Cookson RW Taylor DM Turnbull ZM Chrzanowska-Lightowlers L Dong DA Figlewicz PJ Shaw 2002 Mitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis Brain 125 1522 1533 10.1093/brain/awf167
45. IG Kirkinezos SR Bacman D Hernandez J Oca-Cossio LJ Arias MA Perez-Pinzon WG Bradley CT Moraes 2005 Cytochrome c association with the inner mitochondrial membrane is impaired in the CNS of G93A-SOD1 mice J Neurosci 25 164 172 10.1523/JNEUROSCI.3829-04.2005
46. AC Bowling JB Schulz RH Brown Jr MF Beal 1993 Superoxide dismutase activity, oxidative damage, and mitochondrial energy metabolism in familial and sporadic amyotrophic lateral sclerosis J Neurochem 61 2322 2325 10.1111/j.1471-4159.1993.tb07478.x
47. M Mattiazzi M D'Aurelio CD Gajewski K Martushova M Kiaei MF Beal G Manfredi 2002 Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice J Biol Chem 277 29626 29633 10.1074/jbc.M203065200
48. MT Carri A Ferri A Battistoni L Famhy R Gabbianelli F Poccia G Rotilio 1997 Expression of a Cu, Zn superoxide dismutase typical of familial amyotrophic lateral sclerosis induces mitochondrial alteration and increase of cytosolic Ca2+ concentration in transfected neuroblastoma SH-SY5Y cells FEBS Lett 414 365 368 10.1016/S0014-5793(97)01051-X
49. HD Durham J Roy L Dong DA Figlewicz 1997 Aggregation of mutant Cu/Zn superoxide dismutase proteins in a culture model of ALS J Neuropathol Exp Neurol 56 523 530 10.1097/00005072-199705000-00008
50. S Rabizadeh EB Gralla DR Borchelt R Gwinn JS Valentine S Sisodia P Wong M Lee H Hahn DE Bredesen 1995 Mutations associated with amyotrophic lateral sclerosis convert superoxide dismutase from an antiapoptotic gene to a proapoptotic gene: studies in yeast and neural cells Proc Natl Acad Sci USA 92 3024 3028 10.1073/pnas.92.7.3024
51. S Vukosavic L Stefanis V Jackson-Lewis C Guegan N Romero C Chen M Dubois-Dauphin S Przedborski 2000 Delaying caspase activation by Bcl-2: a clue to disease retardation in a transgenic mouse model of amyotrophic lateral sclerosis J Neurosci 20 9119 9125
52. V Kostic V Jackson-Lewis F de Bilbao M Dubois-Dauphin S Przedborski 1997 Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis Science 277 559 562 10.1126/science.277.5325.559
53. 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
54. CM Higgins C Jung Z Xu 2003 ALS-associated mutant SOD1G93A causes mitochondrial vacuolation by expansion of the intermembrane space and by involvement of SOD1 aggregation and peroxisomes BMC Neurosci 4 16 10.1186/1471-2202-4-16
55. P Pasinelli ME Belford N Lennon BJ Bacskai BT Hyman D Trotti RH Brown Jr 2004 Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria Neuron 43 19 30 10.1016/j.neuron.2004.06.021
56. S Sasaki M Iwata 2007 Mitochondrial alterations in the spinal cord of patients with sporadic amyotrophic lateral sclerosis J Neuropathol Exp Neurol 66 10 16 10.1097/nen.0b013e31802c396b
57. MJ Chung YL Suh 2002 Ultrastructural changes of mitochondria in the skeletal muscle of patients with amyotrophic lateral sclerosis Ultrastruct Pathol 26 3 7 10.1080/01913120252934260
58. A Echaniz-Laguna J Zoll F Ribera C Tranchant JM Warter J Lonsdorfer E Lampert 2002 Mitochondrial respiratory chain function in skeletal muscle of ALS patients Ann Neurol 52 623 627 10.1002/ana.10357
59. S Sasaki H Warita T Murakami K Abe M Iwata 2004 Ultrastructural study of mitochondria in the spinal cord of transgenic mice with a G93A mutant SOD1 gene Acta Neuropathol 107 461 474 10.1007/s00401-004-0837-z
60. J Kong Z Xu 1998 Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1 J Neurosci 18 3241 3250
61. C Bendotti N Calvaresi L Chiveri A Prelle M Moggio M Braga V Silani S De Biasi 2001 Early vacuolization and mitochondrial damage in motor neurons of FALS mice are not associated with apoptosis or with changes in cytochrome oxidase histochemical reactivity J Neurol Sci 191 25 33 10.1016/S0022-510X(01)00627-X
62. H Takeuchi Y Kobayashi S Ishigaki M Doyu G Sobue 2002 Mitochondrial localization of mutant superoxide dismutase 1 triggers caspase-dependent cell death in a cellular model of familial amyotrophic lateral sclerosis J Biol Chem 277 50966 50972 10.1074/jbc.M209356200
63. M Keep E Elmer KS Fong K Csiszar 2001 Intrathecal cyclosporin prolongs survival of late-stage ALS mice Brain Res 894 327 331 10.1016/S0006-8993(01) 02012-1
64. AB Knott G Perkins R Schwarzenbacher E Bossy-Wetzel 2008 Mitochondrial fragmentation in neurodegeneration Nat Rev Neurosci 9 505 518 10.1038/nrn2417
65. N Leclerc F Ribera J Zoll JM Warter P Poindron E Lampert J Borg 2001 Selective changes in mitochondria respiratory properties in oxidative or glycolytic muscle fibers isolated from G93AhumanSOD1 transgenic mice Neuromuscul Disord 11 722 727 10.1016/S0960-8966(01)00240-1
66. J Liu C Lillo PA Jonsson VC Vande CM Ward TM Miller JR Subramaniam JD Rothstein S Marklund PM Andersen T Brannstrom O Gredal PC Wong DS Williams DW Cleveland 2004 Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria Neuron 43 5 17 10.1016/j.neuron.2004.06.016
67. FR Wiedemann G Manfredi C Mawrin MF Beal EA Schon 2002 Mitochondrial DNA and respiratory chain function in spinal cords of ALS patients J Neurochem 80 616 625 10.1046/j.0022-3042.2001.00731.x
68. KN Anderson AC Potter LG Piccenna AK Quah KE Davies SS Cheema 2004 Isolation and culture of motor neurons from the newborn mouse spinal cord Brain Res Brain Res Protoc 12 132 136 10.1016/j.brainresprot.2003.10.001
69. W Camu CE Henderson 1992 Purification of embryonic rat motoneurons by panning on a monoclonal antibody to the low-affinity NGF receptor J Neurosci Methods 44 59 70 10.1016/0165-0270(92)90114-S
70. ML Read A Logan LW Seymour 2005 Barriers to gene delivery using synthetic vectors Adv Genet 53PA 19 46 10.1016/S0065-2660(05)53002-5
71. K Yang GL Clifton RL Hayes 1997 Gene therapy for central nervous system injury: the use of cationic liposomes: an invited review J Neurotrauma 14 281 297 10.1089/neu.1997.14.281
72. M Berry L Barrett L Seymour A Baird A Logan 2001 Gene therapy for central nervous system repair Curr Opin Mol Ther 3 338 349
73. NR Cashman HD Durham JK Blusztajn K Oda T Tabira IT Shaw S Dahrouge JP Antel 1992 Neuroblastoma x spinal cord (NSC) hybrid cell lines resemble developing motor neurons Dev Dyn 194 209 221
74. R Li S Thode J Zhou N Richard J Pardinas MS Rao DW Sah 2000 Motoneuron differentiation of immortalized human spinal cord cell lines J Neurosci Res 59 342 352 10.1002/(SICI)1097-4547(20000201)59:3<342::AID-JNR7>3.0. CO;2-Z
75. EF Salazar-Grueso S Kim H Kim 1991 Embryonic mouse spinal cord motor neuron hybrid cells Neuroreport 2 505 508 10.1097/00001756-199109000-00002
76. RG Smith ME Alexianu G Crawford O Nyormoi E Stefani SH Appel 1994 Cytotoxicity of immunoglobulins from amyotrophic lateral sclerosis patients on a hybrid motoneuron cell line Proc Natl Acad Sci USA 91 3393 3397 10.1073/pnas.91.8.3393
77. BP He W Wen MJ Strong 2002 Activated microglia (BV-2) facilitation of TNF-alpha-mediated motor neuron death in vitro J Neuroimmunol 128 31 38 10.1016/S0165-5728(02)00141-8
78. BJ Turner SS Murray LG Piccenna EC Lopes TJ Kilpatrick SS Cheema 2004 Effect of p75 neurotrophin receptor antagonist on disease progression in transgenic amyotrophic lateral sclerosis mice J Neurosci Res 78 193 199 10.1002/jnr.20256
79. S Usuki J Ren I Utsunomiya NR Cashman J Inokuchi T Miyatake 2001 GM2 ganglioside regulates the function of ciliary neurotrophic factor receptor in murine immortalized motor neuron-like cells (NSC-34) Neurochem Res 26 375 382 10.1023/A:1010999014657
80. CJ Eggett S Crosier P Manning MR Cookson FM Menzies CJ McNeil PJ Shaw 2000 Development and characterisation of a glutamate-sensitive motor neurone cell line J Neurochem 74 1895 1902 10.1046/j.1471-4159.2000.0741895.x
81. A Rembach BJ Turner S Bruce IK Cheah RL Scott EC Lopes CJ Zagami PM Beart NS Cheung SJ Langford SS Cheema 2004 Antisense peptide nucleic acid targeting GluR3 delays disease onset and progression in the SOD1 G93A mouse model of familial ALS J Neurosci Res 77 573 582 10.1002/jnr.20191
82. S Allen PR Heath J Kirby SB Wharton MR Cookson FM Menzies RE Banks PJ Shaw 2003 Analysis of the cytosolic proteome in a cell culture model of familial amyotrophic lateral sclerosis reveals alterations to the proteasome, antioxidant defenses, and nitric oxide synthetic pathways J Biol Chem 278 6371 6383 10.1074/jbc.M209915200
83. C Gomes AS Palma R Almeida M Regalla LF McCluskey JQ Trojanowski J Costa 2008 Establishment of a cell model of ALS disease: Golgi apparatus disruption occurs independently from apoptosis Biotechnol Lett 30 603 610 10.1007/s10529-007-9595-z
84. D Matusica MP Fenech ML Rogers RA Rush 2008 Characterization and use of the NSC-34 cell line for study of neurotrophin receptor trafficking J Neurosci Res 86 553 565 10.1002/jnr.21507
85. 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
86. AA Fatokun TW Stone RA Smith 2008 Oxidative stress in neurodegeneration and available means of protection Front Biosci 13 3288 3311 10.2741/2926
87. R Dringen 2000 Metabolism and functions of glutathione in brain Prog Neurobiol 62 649 671 10.1016/S0301-0082(99)00060-X
88. D Sheehan G Meade VM Foley CA Dowd 2001 Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily Biochem J 360 1 16 10.1042/0264-6021: 3600001
89. D Giustarini R Rossi A Milzani R Colombo I Dalle-Donne 2004 S-glutathionylation: from redox regulation of protein functions to human diseases J Cell Mol Med 8 201 212 10.1111/j.1582-4934.2004.tb00275.x
90. MD Shelton PB Chock JJ Mieyal 2005 Glutaredoxin: role in reversible protein s-glutathionylation and regulation of redox signal transduction and protein translocation Antioxid Redox Signal 7 348 366 10.1089/ars.2005.7.348
91. JC Fernandez-Checa N Kaplowitz C Garcia-Ruiz A Colell 1998 Mitochondrial glutathione: importance and transport Semin Liver Dis 18 389 401 10.1055/s-2007-1007172
92. OW Griffith A Meister 1985 Origin and turnover of mitochondrial glutathione Proc Natl Acad Sci USA 82 4668 4672 10.1073/pnas.82.14.4668
93. A Meister 1995 Mitochondrial changes associated with glutathione deficiency Biochim Biophys Acta 1271 35 42
94. C Garcia-Ruiz A Morales A Ballesta J Rodes N Kaplowitz JC Fernandez-Checa 1994 Effect of chronic ethanol feeding on glutathione and functional integrity of mitochondria in periportal and perivenous rat hepatocytes J Clin Invest 94 193 201 10.1172/JCI117306
95. MJ Meredith DJ Reed 1983 Depletion in vitro of mitochondrial glutathione in rat hepatocytes and enhancement of lipid peroxidation by adriamycin and 1, 3-bis(2-chloroethyl)-1-nitrosourea (BCNU) Biochem Pharmacol 32 1383 1388 10.1016/0006-2952(83)90451-3
96. H Muyderman M Nilsson NR Sims 2004 Highly selective and prolonged depletion of mitochondrial glutathione in astrocytes markedly increases sensitivity to peroxynitrite J Neurosci 24 8019 8028 10.1523/JNEUROSCI.1103-04. 2004
97. U Wullner J Seyfried P Groscurth S Beinroth S Winter M Gleichmann M Heneka P Loschmann JB Schulz M Weller T Klockgether 1999 Glutathione depletion and neuronal cell death: the role of reactive oxygen intermediates and mitochondrial function Brain Res 826 53 62 10.1016/S0006-8993(99)01228-7
98. H Muyderman AL Wadey M Nilsson NR Sims 2007 Mitochondrial glutathione protects against cell death induced by oxidative and nitrative stress in astrocytes J Neurochem 102 1369 1382 10.1111/j.1471-4159.2007.04641.x
99. NR Sims M Nilsson H Muyderman 2004 Mitochondrial glutathione: a modulator of brain cell death J Bioenerg Biomembr 36 329 333 10.1023/B:JOBB.0000041763. 63958.e7
100. A Colell C Garcia-Ruiz M Miranda E Ardite M Mari A Morales F Corrales N Kaplowitz JC Fernandez-Checa 1998 Selective glutathione depletion of mitochondria by ethanol sensitizes hepatocytes to tumor necrosis factor Gastroenterology 115 1541 1551 10.1016/S0016-5085(98)70034-4
101. MF Anderson NR Sims 2002 The effects of focal ischemia and reperfusion on the glutathione content of mitochondria from rat brain subregions J Neurochem 81 541 549 10.1046/j.1471-4159.2002.00836.x
102. M Rizzardini M Lupi S Bernasconi A Mangolini L Cantoni 2003 Mitochondrial dysfunction and death in motor neurons exposed to the glutathione-depleting agent ethacrynic acid J Neurol Sci 207 51 58 10.1016/S0022-510X(02)00357-X
103. Ballatori N, Krance SM, Marchan R, Hammond CL (2008) Plasma membrane glutathione transporters and their roles in cell physiology and pathophysiology. Mol Aspects Med (Aug):26, (Epub ahead of print)
104. TP Akerboom H Sies 1981 Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples Methods Enzymol 77 373 382 10.1016/S0076-6879(81)77050-2