Mitochondrial dysfunction and amyotrophic lateral sclerosis

Muscle and Nerve

Volumn 33, Issue 5, 2006, Pages 598-608

  Hervias, Isabel ^a   Beal, M Flint ^a   Manfredi, Giovanni ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Aggregation; Amyotrophic lateral sclerosis (ALS); Apoptosis; Mitochondria; Motor neuron disease; SOD1

Indexed keywords

ANTIOXIDANT; COPPER ZINC SUPEROXIDE DISMUTASE; MUTANT PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; AUTOPSY; BIOCHEMISTRY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG TARGETING; ENZYME LOCALIZATION; EVIDENCE BASED MEDICINE; HUMAN; MITOCHONDRION; MORPHOLOGY; MOTONEURON; MOTOR NEURON DISEASE; NERVE CELL NECROSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; REVIEW; TRANSGENIC MOUSE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; APOPTOSIS; CALCIUM; HUMANS; MITOCHONDRIAL DISEASES; MODELS, BIOLOGICAL; MUTATION; NEURONS; SUPEROXIDE DISMUTASE;

EID: 33646241740     PISSN: 0148639X     EISSN: 10974598     Source Type: Journal    
DOI: 10.1002/mus.20489     Document Type: Review

References (100)

1. Afifi AK, Aleu FP, Goodgold J, MacKay B. Ultrastructure of atrophic muscle in amyotrophic lateral sclerosis. Neurology 1966;16:475-481.
2. Agar J, Durham H. Relevance of oxidative injury in the pathogenesis of motor neuron diseases. Amyotroph Lateral Scler Other Motor Neuron Disord 2003;4:232-242.
3. Appel SH, Beers D, Siklos L, Engelhardt JI, Mosier DR. Calcium: the Darth Vader of ALS. Amyotroph Lateral Scler Other Motor Neuron Disord 2001;2(suppl 1):S47-54.
4. Atsumi T, Miyatake T. Morphometry of the degenerative process in the hypoglossal nerves in amyotrophic lateral sclerosis. Acta Neuropathol (Berl) 1987;73:25-31.
5. Beal MF. Mitochondrial dysfunction and oxidative damage in Alzheimer's and Parkinson's diseases and coenzyme Q10 as a potential treatment. J Bioenerg Biomembr 2004;36:381-386.
6. Beretta S, Sala G, Mattavelli L, Ceresa C, Casciati A, Ferri A, et al. Mitochondrial dysfunction due to mutant copper/zinc superoxide dismutase associated with amyotrophic lateral sclerosis is reversed by N-acetylcysteine. Neurobiol Dis 2003;13:213-221.
7. Bianchi K, Rimessi A, Prandini A, Szabadkai G, Rizzuto R. Calcium and mitochondria: mechanisms and functions of a troubled relationship. Biochim Biophys Acta 2004;1742:119-131.
8. Borchelt DR, Lee MK, Slunt HS, Guarnieri M, Xu ZS, Wong PC, et al. Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc Natl Acad Sci USA 1994;91:8292-8296.
9. Bordo D, Djinovic K, Bolognesi M. Conserved patterns in the Cu,Zn superoxide dismutase family. J Mol Biol 1994;238:366-386.
10. Borthwick GM, Johnson MA, Ince PG, Shaw PJ, Turnbull DM. Mitochondrial enzyme activity in amyotrophic lateral sclerosis: implications for the role of mitochondria in neuronal cell death. Ann Neurol 1999;46:787-790.
11. Bowling AC, Barkowski EE, McKenna-Yasek D, Sapp P, Horvitz HR, Beal MF, et al. Superoxide dismutase concentration and activity in familial amyotrophic lateral sclerosis. J Neurochem 1995;64:2366-2369.
12. 2+ concentration in transfected neuroblastoma SH-SY5Y cells. FEBS Lett 1997;414:365-368.
13. Carroll MC, Girouard JB, Ulloa JL, Subramaniam JR, Wong PC, Valentine JS, et al. Mechanisms for activating Cu- and Zn-containing superoxide dismutase in the absence of the CCS Cu chaperone. Proc Natl Acad Sci USA 2004;101:5964-5969.
14. Chacinska A, Pfanner N, Meisinger C. How mitochondria import hydrophilic and hydrophobic proteins. Trends Cell Biol 2002;12:299-303.
15. Clement AM, Nguyen MD, Roberts EA, Garcia ML, Boillee S, Rule M, et al. Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice. Science 2003;302:113-117.
16. Dal Canto MC. Comparison of pathological alterations in ALS and a murine transgenic model: pathogenetic implications. Clin Neurosci 1995;3:332-337.
17. Dal Canto MC, Gurney ME. Development of central nervous system pathology in a murine transgenic model of human amyotrophic lateral sclerosis. Am J Pathol 1994;145:1271-1279.
18. Deng HX, Hentati A, Tainer JA, Iqbal Z, Cayabyab A, Hung WY, et al. Amyotrophic lateral sclerosis and structural defects in Cu,Zn superoxide dismutase. Science 1993;261:1047-1051.
19. DiMauro S. Mitochondrial diseases. Biochim Biophys Acta 2004;1658:80-88.
20. Esaki M, Kanamori T, Nishikawa S, Endo T. Two distinct mechanisms drive protein translocation across the mitochondrial outer membrane in the late step of the cytochrome b(2) import pathway. Proc Natl Acad Sci USA 1999;96:11770-11775.
21. Estevez AG, Crow JP, Sampson JB, Reiter C, Zhuang Y, Richardson GJ, et al. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science 1999;286:2498-2500.
22. Fahandejsaadi A, Leung E, Rahaii R, Bu J, Geula C. Calbindin-D28K, parvalbumin and calretinin in primate lower motor neurons. Neuroreport 2004;15:443-448.
23. Ferri A, Gabbianelli R, Casciati A, Celsi F, Rotilio G, Carri MT. Oxidative inactivation of calcineurin by Cu,Zn superoxide dismutase G93A, a mutant typical of familial amyotrophic lateral sclerosis. J Neurochem 2001;79:531-538.
24. Field LS, Furukawa Y, O'Halloran TV, Culotta VC. Factors controlling the uptake of yeast copper/zinc superoxide dismutase into mitochondria. J Biol Chem 2003;278:28052-28059.
25. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, Castellano-Sanchez A, et al. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 2004;185:232-240.
26. Folsch H, Guiard B, Neupert W, Stuart RA. Internal targeting signal of the BCS1 protein: a novel mechanism of import into mitochondria. EMBO J 1996;15:479-487.
27. Friedlander RM, Brown RH, Gagliardini V, Wang J, Yuan J. Inhibition of ICE slows ALS in mice. Nature 1997;388:31.
28. Gajewski CD, Lin MT, Cudkowicz ME, Beal MF, Manfredi G. Mitochondrial DNA from platelets of sporadic ALS patients restores normal respiratory functions in rho(0) cells. Exp Neurol 2003;179:229-235.
29. Ghadge GD, Lee JP, Bindokas VP, Jordan J, Ma L, Miller RJ, et al. Mutant superoxide dismutase-1-linked familial amyotrophic lateral sclerosis: molecular mechanisms of neuronal death and protection. J Neurosci 1997;17:8756-8766.
30. Gohil VM, Hayes P, Matsuyama S, Schagger H, Schlame M, Greenberg ML. Cardiolipin biosynthesis and mitochondrial respiratory chain function are interdependent. J Biol Chem 2004;279:42612-42618.
31. Gong YH, Parsadanian AS, Andreeva A, Snider WD, Elliott JL. Restricted expression of G86R Cu/Zn superoxide dismutase in astrocytes results in astrocytosis but does not cause motoneuron degeneration. J Neurosci 2000;20:660-665.
32. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004;305:626-629.
33. Guegan C, Vila M, Rosoklija G, Hays AP, Przedborski S. Recruitment of the mitochondrial-dependent apoptotic pathway in amyotrophic lateral sclerosis. J Neurosci 2001;21:6569-6576.
34. Higgins CM, Jung C, Ding H, Xu Z. Mutant Cu,Zn superoxide dismutase that causes motoneuron degeneration is present in mitochondria in the CNS. J Neurosci 2002;22: RC215.
35. Higgins CM, Jung C, Xu Z. ALS-associated mutant SOD1G93A causes mitochondrial vacuolation by expansion of the intermembrane space and by involvement of SOD1 aggregation and peroxisomes. BMC Neurosci 2003;4:16.
36. Hirano A, Nakano I, Kurland LT, Mulder DW, Holley PW, Saccomanno G. Fine structural study of neurofibrillary changes in a family with amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 1984;43:471-480.
37. Inoue H, Tsukita K, Iwasato T, Suzuki Y, Tomioka M, Tateno M, et al. The crucial role of caspase-9 in the disease progression of a transgenic ALS mouse model. EMBO J 2003;22:6665-6674.
38. Jaarsma D, Rognoni F, van Duijn W, Verspaget HW, Haasdijk ED, Holstege JC. CuZn superoxide dismutase (SOD1) accumulates in vacuolated mitochondria in transgenic mice expressing amyotrophic lateral sclerosis-linked SOD1 mutations. Acta Neuropathol (Berl) 2001;102:293-305.
39. Jung C, Higgins CMJ, Xu Z. Mitochondrial electron transport chain complex dysfunction in a transgenic mouse model for amyotrophic lateral sclerosis. J Neurochem 2002;83:535-545.
40. Jung C, Rong Y, Doctrow S, Baudry M, Malfroy B, Xu Z. Synthetic superoxide dismutase/catalase mimetics reduce oxidative stress and prolong survival in a mouse amyotrophic lateral sclerosis model. Neurosci Lett 2001;304:157-160.
41. Kabashi E, Agar JN, Taylor DM, Minotti S, Durham HD. Focal dysfunction of the proteasome: a pathogenic factor in a mouse model of amyotrophic lateral sclerosis. J Neurochem 2004;89:1325-1335.
42. Kang SJ, Sanchez I, Jing N, Yuan J. Dissociation between neurodegeneration and caspase-11-mediated activation of caspase-1 and caspase-3 in a mouse model of amyotrophic lateral sclerosis. J Neurosci 2003;23:5455-5460.
43. Kirkinezos IG, Bacman SR, Hernandez D, Oca-Cossio J, Arias LJ, Perez-Pinzon MA, et al. Cytochrome c association with the inner mitochondrial membrane is impaired in the CNS of G93A-SOD1 mice. J Neurosci 2005;25:164-172.
44. Klivenyi P, Ferrante RJ, Matthews RT, Bogdanov MB, Klein AM, Andreassen OA, et al. Neuroprotective effects of creatine in a transgenic animal model of amyotrophic lateral sclerosis. Nat Med 1999;5:347-350.
45. Klug D, Rabani J, Fridovich I. A direct demonstration of the catalytic action of superoxide dismutase through the use of pulse radiolysis. J Biol Chem 1972;247:4839-4842.
46. Kong J, Xu Z. Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J Neurosci 1998;18:3241-3250.
47. Kostic V, Jackson-Lewis V, de Bilbao F, Dubois-Dauphin M, Przedborski S. Bcl-2: prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 1997;277:559-562.
48. Kruman II, Pedersen WA, Springer JE, Mattson MP. ALS-linked Cu/Zn-SOD mutation increases vulnerability of motor neurons to excitotoxicity by a mechanism involving increased oxidative stress and perturbed calcium homeostasis. Exp Neurol 1999;160:28-39.
49. Lariviere RC, Julien JP. Functions of intermediate filaments in neuronal development and disease. J Neurobiol 2004;58:131-148.
50. Li M, Ona VO, Guegan C, Chen M, Jackson-Lewis V, Andrews LJ, et al. Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science 2000;288:335-339.
51. Lino MM, Schneider C, Caroni P. Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J Neurosci 2002;22:4825-4832.
52. Liu J, Lillo C, Jonsson PA, Vande Velde C, Ward CM, Miller TM, et al. Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 2004;43:5-17.
53. Mattiazzi M, D'Aurelio M, Gajewski CD, Martushova K, Kiaei M, Beal MF, et al. Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J Biol Chem 2002;5:5.
54. Mena MA, Khan U, Togasaki DM, Sulzer D, Epstein CJ, Przedborski S. Effects of wild-type and mutated copper/zinc superoxide dismutase on neuronal survival and L-DOPA-induced toxicity in postnatal midbrain culture. J Neurochem 1997;69:21-33.
55. Menzies FM, Cookson MR, Taylor RW, Turnbull DM, Chrzanowska-Lightowlers ZM, et al. Mitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis. Brain 2002;125:1522-1533.
56. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, et al. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 2005;121:1059-1069.
57. Migheli A, Atzori C, Piva R, Tortarolo M, Girelli M, Schiffer D, et al. Lack of apoptosis in mice with ALS. Nat Med 1999;5:966-967.
58. Mulder DW, Kurland LT. Motor neuron disease: epidemiologic studies. Adv Exp Med Biol 1987;209:325-332.
59. Okado-Matsumoto A, Fridovich I. Amyotrophic lateral sclerosis: a proposed mechanism. Proc Natl Acad Sci USA 2002;99:9010-9014.
60. Okado-Matsumoto A, Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat liver: Cu,Zn-SOD in mitochondria. J Biol Chem 2001;276:38388-38393.
61. Orrell R, de Belleroche J, Marklund S, Bowe F, Hallewell R. A novel SOD mutant and ALS. Nature 1995;374:504-505.
62. Pasinelli P, Belford ME, Lennon N, Bacskai BJ, Hyman BT, Trotti D, et al. Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron 2004;43:19-30.
63. Pasinelli P, Borchelt DR, Houseweart MK, Cleveland DW, Brown RH Jr. Caspase-1 is activated in neural cells and tissue with amyotrophic lateral sclerosis-associated mutations in copper-zinc superoxide dismutase. Proc Natl Acad Sci USA 1998;95:15763-15768.
64. Pasinelli P, Houseweart MK, Brown RH Jr, Cleveland DW. Caspase-1 and -3 are sequentially activated in motor neuron death in Cu,Zn superoxide dismutase-mediated familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 2000;97:13901-13906.
65. Przedborski S. Programmed cell death in amyotrophic lateral sclerosis: a mechanism of pathogenic and therapeutic importance. Neurologist 2004;10:1-7.
66. Rabizadeh S, Gralla EB, Borchelt DR, Gwinn R, Valentine JS, Sisodia S, et al. 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 1995;92:3024-3028.
67. Reaume AG, Elliott JL, Hoffman EK, Kowall NW, Ferrante RJ, Siwek DF, et al. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat Genet 1996;13:43-47.
68. Reynolds IJ. Mitochondrial membrane potential and the permeability transition in excitotoxicity. Ann NY Acad Sci 1999;893:33-41.
69. Roman GC. Neuroepidemiology of amyotrophic lateral sclerosis: clues to aetiology and pathogenesis. J Neurol Neurosurg Psychiatry 1996;61:131-137.
70. Rothstein JD. Excitotoxicity hypothesis. Neurology 1996;47(suppl):S19-25.
71. Sasaki S, Iwata M. Impairment of fast axonal transport in the proximal axons of anterior horn neurons in amyotrophic lateral sclerosis. Neurology 1996;47:535-540.
72. Schon EA, Grossman MH. Mitochondrial diseases: genetics. Biofactors 1998;7:191-195.
73. Siklos L, Engelhardt J, Harati Y, Smith RG, Joo F, Appel SH. Ultrastructural evidence for altered calcium in motor nerve terminals in amyotropic lateral sclerosis. Ann Neurol 1996;39:203-216.
74. Stan T, Brix J, Schneider-Mergener J, Pfanner N, Neupert W, Rapaport D. Mitochondrial protein import: recognition of internal import signals of BCS1 by the TOM complex. Mol Cell Biol 2003;23:2239-2250.
75. Sturtz LA, Diekert K, Jensen LT, Lill R, Culotta VC. A fraction of yeast Cu,Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria, a physiological role for sod1 in guarding against mitochondrial oxidative damage. J Biol Chem 2001;276:38084-38089.
76. Swerdlow RH, Parks JK, Cassarino DS, Trimmer PA, Miller SW, Maguire DJ, et al. Mitochondria in sporadic amyotrophic lateral sclerosis. Exp Neurol 1998;153:135-142.
77. Takeuchi H, Kobayashi Y, Ishigaki S, Doyu M, Sobue G. Mitochondrial localization of mutant superoxide dismutase 1 triggers caspase-dependent cell death in a cellular model of familial amyotrophic lateral sclerosis. J Biol Chem 2002;277:50966-50972.
78. Tateno M, Sadakata H, Tanaka M, Itohara S, Shin RM, Miura M, et al. Calcium-permeable AMPA receptors promote misfolding of mutant SOD1 protein and development of amyotrophic lateral sclerosis in a transgenic mouse model. Hum Mol Genet 2004;13:2183-2196.
79. Tummala H, Jung C, Tiwari A, Higgins CM, Hayward LJ, Xu Z. Inhibition of chaperone activity is a shared property of several Cu, Zn superoxide dismutase mutants that cause amyotrophic lateral sclerosis. J Biol Chem 2005;280:17725-17731.
80. Urushitani M, Kurisu J, Tsukita K, Takahashi R. Proteasomal inhibition by misfolded mutant superoxide dismutase 1 induces selective motor neuron death in familial amyotrophic lateral sclerosis. J Neurochem 2002;83:1030-1042.
81. Vielhaber S, Kunz D, Winkler K, Wiedemann FR, Kirches E, Feistner H, et al. Mitochondrial DNA abnormalities in skeletal muscle of patients with sporadic amyotrophic lateral sclerosis. Brain 2000;123:1339-1348.
82. Vijayvergiya C, Beal MF, Buck J, Manfredi G. Mutant superoxide dismutase 1 forms aggregates in the brain mitochondrial matrix of amyotrophic lateral sclerosis mice. J Neurosci 2005;25:2463-2470.
83. Vukosavic S, Stefanis L, Jackson-Lewis V, Guegan C, Romero N, Chen C, et al. Delaying caspase activation by Bcl-2: a clue to disease retardation in a transgenic mouse model of amyotrophic lateral sclerosis. J Neurosci 2000;20:9119-9125.
84. Wang J, Xu G, Li H, Gonzales V, Fromholt D, Karch C, et al. Somatodendritic accumulation of misfolded SOD1-L126Z in motor neurons mediates degeneration: alpha B-crystallin modulates aggregation. Hum Mol Genet 2005;14:2335-2347.
85. Weisiger RA, Fridovich I. Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization. J Biol Chem 1973;248:4793-4796.
86. Wiedemann FR, Manfredi G, Mawrin C, Beal MF, Schon EA. Mitochondrial DNA and respiratory chain function in spinal cords of ALS patients. J Neurochem 2002;80:616-625.
87. Wiedemann FR, Winkler K, Kuznetsov AV, Bartels C, Vielhaber S, Feistner H, et al. Impairment of mitochondrial function in skeletal muscle of patients with amyotrophic lateral sclerosis. J Neurol Sci 1998;156:65-72.
88. Wiedemann N, Kozjak V, Prinz T, Ryan MT, Meisinger C, Pfanner N, et al. Biogenesis of yeast mitochondrial cytochrome c: a unique relationship to the TOM machinery. J Mol Biol 2003;327:465-474.
89. Wong PC, Pardo CA, Borchelt DR, Lee MK, Copeland NG, Jenkins N, et al. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 1995;14:1105-1116.
90. Wood JD, Beaujeux TP, Shaw PJ. Protein aggregation in motor neurone disorders. Neuropathol Appl Neurobiol 2003;29:529-545.
91. Wu AS, Kiaei M, Aguirre N, Crow JP, Calingasan NY, Browne SE, et al. Iron porphyrin treatment extends survival in a transgenic animal model of amyotrophic lateral sclerosis. J Neurochem 2003;85:142-150.
92. Xu Z. Mechanism and treatment of motoneuron degeneration in ALS: what have SOD1 mutants told us? Amyotroph Lateral Scler Other Motor Neuron Disord 2000;1:225-234.
93. Xu Z, Jung C, Higgins C, Levine J, Kong J. Mitochondrial degeneration in amyotrophic lateral sclerosis. J Bioenerg Biomembr 2004;36:395-399.
94. Zhu S, Stavrovskaya IG, Drozda M, Kim BY, Ona V, Li M, et al. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 2002;417:74-78.
95. Urushitani M, Kurisu J, Tateno M, Hatakeyama S, Nakayama K, Kato S, et al. CHIP promotes proteasomal degradation of familial ALS-linked mutant SOD1 by ubiquitinating Hsp/Hsc70. J Neurochem 2004;90:231-244.
96. Jaarsma D, Haasdijk ED, Grashorn JA, Hawkins R, van Duijn W, Verspaget HW, et al. Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol Dis 2000;7:623-643.
97. Shults CW, Oakes D, Kieburtz K, Beal MF, Haas R, Plumb S, et al. Effects of coenzyme Q10 in early Parkinson disease: evidence of slowing of the functional decline. Arch Neurol 2002;59:1541-1550.
98. Wootz H, Hansson I, Korhonen L, Napankangas U, Lindholm D. Caspase-12 cleavage and increased oxidative stress during motoneuron degeneration in transgenic mouse model of ALS. Biochem Biophys Res Commun 2004;322:281-286.
99. Rizzardini M, Lupi M, Bernasconi S, Mangolini A, Cantoni L. Mitochondrial dysfunction and death in motor neurons exposed to the glutathione-depleting agent ethacrynic acid. J Neurol Sci 2003;207:51-58.
100. Rizzardini M, Mangolini A, Lupi M, Ubezio P, Bendotti C, Cantoni L. Low levels of ALS-linked Cu/Zn superoxide dismutase increase the production of reactive oxygen species and cause mitochondrial damage and death in motor neuron-like cells. J Neurol Sci 2005;232:95-103.