Neurodegeneration induced by complex I inhibition in a cellular model of familial amyotrophic lateral sclerosis

Brain Research Bulletin

Volumn 69, Issue 4, 2006, Pages 465-474

  Rizzardini, Milena ^a   Lupi, Monica ^a   Mangolini, Alessandra ^a   Babetto, Elisabetta ^a   Ubezio, Paolo ^a   Cantoni, Lavinia ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

Amyotrophic lateral sclerosis; Cu Zn superoxide dismutase; Mitochondrial membrane potential; Motor neuron(s); Oxidative stress; Rotenone

Indexed keywords

ADENOSINE TRIPHOSPHATE; MUTANT PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL POPULATION; CELL VIABILITY; CONTROLLED STUDY; DEPOLARIZATION; ELECTRON TRANSPORT; ENZYME INHIBITION; FLOW CYTOMETRY; HYPERPOLARIZATION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MOTONEURON; MOUSE; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT; WILD TYPE;

ADENOSINE TRIPHOSPHATE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL DEATH; CELL LINE; CELL SURVIVAL; ELECTRON TRANSPORT COMPLEX I; HUMANS; MEMBRANE POTENTIALS; MICE; MITOCHONDRIA; MOTOR NEURONS; MUTATION; OXIDATIVE STRESS; PESTICIDES; REACTIVE OXYGEN SPECIES; ROTENONE; SUPEROXIDE DISMUTASE; TRANSFECTION;

EID: 33646395389     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2006.02.013     Document Type: Article

References (55)

1. Adam-Vizi V. Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources. Antioxid. Redox Sign. 7 (2005) 1140-1149
2. Allen S., Heath P.R., Kirby J., Wharton S.B., Cookson M.R., Menzies F.M., Banks R.E., and Shaw P.J. 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 (2003) 6371-6383
3. Andreassen O.A., Dedeoglu A., Klivenyi P., Beal M.F., and Bush A.I. N-Acetyl-l-cysteine improves survival and preserves motor performance in an animal model of familial amyotrophic lateral sclerosis. NeuroReport 11 (2000) 2491-2493
4. Andreassen O.A., Ferrante R.J., Klivenyi P., Klein A.M., Dedeoglu A., Albers D.S., Kowall N.W., and Beal M.F. Transgenic ALS mice show increased vulnerability to the mitochondrial toxin MPTP and 3-nitropropionic acid. Exp. Neurol. 168 (2001) 356-363
5. Barrientos A., and Moraes C.T. Titrating the effect of mitochondrial complex I impairment in the cell physiology. J. Biol. Chem. 274 (1999) 16188-16197
6. Basma A.N., Heikkila R.E., Saporito M.S., Philbert M., Geller H.M., and Nicklas W.J. 1-Methyl-4-(2′-ethylphenyl)-1,2,3,6-tetrahydropyridine-induced toxicity in PC12 cells is enhanced by preventing glycolysis. J. Neurochem. 58 (1992) 1052-1059
7. Beal M.F. Mitochondria and the pathogenesis of ALS. Brain 123 (2000) 1291-1292
8. Beltran B., Mathur A., Duchen M.R., Erusalimsky J.D., and Moncada S. The effect of nitric oxide on cell respiration: a key in understanding its role in cell survival or death. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 14602-14607
9. Bendotti C., and Carrì M.T. Lessons from models of SOD1-linked familial ALS. Trends Mol. Med. 10 (2004) 393-400
10. Beretta S., Sala G., Mattavelli L., Ceresa C., Casciati A., Ferri A., Carrì M.T., and Ferrarese C. Mitochondrial dysfunction due to mutant copper/zinc superoxide dismutase associated with amyotrophic lateral sclerosis is reversed by N-acetylcysteine. Neurobiol. Dis. 13 (2003) 213-221
11. Brujin L.I., Miller T.M., and Cleveland D.W. Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27 (2004) 723-749
12. 2+ concentration in transfected neuroblastoma SH-SY5Y cells. FEBS Lett. 414 (1997) 365-368
13. Carrì M.T., Ferri A., Cozzolino M., Calabrese L., and Rotilio G. Neurodegeneration in amyotrophic lateral sclerosis: the role of oxidative stress and altered homeostasis of metals. Brain Res. Bull. 61 (2003) 365-374
14. Cashman N.R., Durham H.D., Blusztajn J.K., Oda K., Tabira T., Shaw I.T., Dahrouge S., and Antel J.P. Neuroblastoma × spinal cord (NSC) hybrid cell lines resemble developing motor neurons. Dev. Dyn. 194 (1992) 209-221
15. Cocco T., Sgobbo P., Clemente M., Lopriore B., Grattagliano I., Di Paola M., and Villani G. Tissue-specific changes of mitochondrial functions in aged rats: effect of a long-term dietary treatment with N-acetylcysteine. Free Radic. Biol. Med. 38 (2005) 796-805
16. Di Lisa F., and Bernardi P. Mitochondrial function as a determinant of recovery or death in cell response to injury. Mol. Cell. Biochem. 184 (1998) 379-391
17. Erecinska M., and Silver I.A. Ions and energy in mammalian brain. Prog. Neurobiol. 43 (1994) 37-71
18. Fukada K., Zhang F., Vien A., Cashman N.R., and Zhu H. Mitochondrial proteomic analysis of a cell line model of familial amyotrophic lateral sclerosis. Mol. Cell. Proteomics 3 (2004) 1211-1223
19. Greco M., Villani G., Mazzucchelli F., Bresolin N., Papa S., and Attardi G. Marked aging-related decline in efficiency of oxidative phosphorylation in human skin fibroblasts. FASEB J. 17 (2003) 1706-1708
20. Hakem R., Hakem A., Duncan G.S., Henderson J.T., Woo M., Soengas M.S., Elia A., de la Pompa J.L., Kagi D., Khoo W., Potter J., Yoshida R., Kaufman S.A., Lowe S.W., Penninger J.M., and Mak T.W. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94 (1998) 339-352
21. Halestrap A.P., and Brenner C. The adenine nucleotide translocator: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr. Med. Chem. 10 (2003) 1507-1525
22. Isenberg J.S., and Klaunig J.E. Role of the mitochondrial membrane permeability transition (MPT) in rotenone-induced apoptosis in liver cells. Toxicol. Sci. 53 (2000) 340-351
23. Kadenbach B. Intrinsic and extrinsic uncoupling of oxidative phosphorylation. Biochim. Biophys. Acta 1604 (2003) 77-94
24. Kane D.J., Sarafian T.A., Anton R., Hahn H., Gralla E.B., Valentine J.S., Ord T., and Bredesen D.E. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262 (1993) 1274-1277
25. Kroemer G., and Reed J.C. Mitochondrial control of cell death. Nat. Med. 6 (2000) 513-519
26. Kruman I.I., Pedersen W.A., Springer J.E., and Mattson M.P. ALS-linked Cu/Zn SOD mutations increase vulnerability of motor neurons to excitotoxicity by a mechanism involving increased oxidative stress and perturbed calcium homeostasis. Exp. Neurol. 160 (1999) 28-39
27. Kudin A.P., Bimpong-Buta N.Y.-B., Vielhaber S., Elger C.E., and Kunz W.S. Characterization of superoxide-producing sites in isolated brain mitochondria. J. Biol. Chem. 279 (2004) 4127-4135
28. Kweon G.R., Marks J.D., Krencik R., Leung E.H., Schumacker P.T., Hyland K., and Kang U.J. Distinct mechanisms of neurodegeneration induced by chronic complex I inhibition in dopaminergic and non-dopaminergic cells. J. Biol. Chem. 279 (2004) 51783-51792
29. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J.A., and Robinson J.P. Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 278 (2003) 8516-8525
30. Liu R., Li B., Flanagan S.W., Oberley L.W., Gozal D., and Qiu M. Increased mitochondrial antioxidative activity or decreased oxygen free radical propagation prevent mutant SOD1-mediated motor neuron cell death. J. Neurochem. 80 (2002) 488-500
31. 2+ and respiratory chain complex II inhibition. J. Neurochem. 90 (2004) 1025-1035
32. Menzies F.M., Cookson M.R., Taylor R.W., Turnbull D.M., Chrzanowska-Lightowlers Z.M.A., Dong L., Figlewicz D.A., and Shaw P.J. Mitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis. Brain 125 (2002) 1522-1533
33. Menzies F.M., Ince P.G., and Shaw P.J. Mitochondrial involvement in amyotrophic lateral sclerosis. Neurochem. Int. 40 (2002) 543-551
34. Molina-Jimenez M.F., Sanchez-Reus M.I., Andres D., Cascales M., and Benedi J. Neuroprotective effect of fratexin and myricetin against rotenone-induced apoptosis in neuroblastoma cells. Brain Res. 1009 (2004) 9-16
35. Moreno-Sanchez R., Bravo C., Vasquez C., Ayala G., Silveira L.H., and Martinez-Lanvin M. Inhibition and uncoupling of oxidative phosphorylation by nonsteroidal anti-inflammatoty drugs. Biochem. Pharmacol. 57 (1999) 743-752
36. Nagano S., Fuji Y., Yamamoto T., Taniyama M., Fukada K., Yanagihara T., and Sakosa S. The efficacy of trientine or ascorbate alone compared to that of the combined treatment with these two agents in familial amyotrophic lateral sclerosis model in mice. Exp. Neurol. 179 (2003) 176-180
37. Newmeyer D.D., and Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machinery of death. Cell 112 (2003) 481-490
38. Ojaimi J., Masters C.L., Opeskin K., McKelvie P., and Byrne E. Mitochondrial respiratory chain activity in the human brain as a function of age. Mech. Ageing Dev. 111 (1999) 39-47
39. Okado-Matsumoto A., and Fridovich I. Subcellular distribution of superoxide dismutases (SOD) in rat liver. Cu, Zn-SOD in mitochondria. J. Biol. Chem. 276 (2001) 38388-38393
40. Pasinelli P., Belford M.E., Lennon N., Bacskai B.J., Hyman B.T., Trotti D., and Brown Jr. R.H. Amyotrophic lateral sclerosis-associated SOD1 mutant proteins bind and aggregate with Bcl-2 in spinal cord mitochondria. Neuron 43 (2004) 19-30
41. Perl A., Gergely Jr. P., Nagy G., Koncz A., and Banki K. Mitochondrial hyperpolarization: a checkpoint of T-cell life, death and autoimmunity. Trends Immunol. 25 (2004) 360-367
42. Raimondi A., Mangolini A., Vanoni C., Conforti L., Francolini M., Rizzardini M., Bendotti C., Cantoni L., and Pietrini G. Molecular basis for motor neuron selective damage induced by mutated SOD1: distribution of the G93A mutant of SOD1 in mitochondria and mitochondrial structural alterations in motor neuron-like and in non-neuronal cellular models of ALS, Amyotrophic Lateral Scler. Other Mot. Neuron Disord. 4 Suppl. 1 (2003) 50
43. Rizzardini M., Mangolini A., Lupi M., Ubezio P., Bendotti C., and Cantoni L. Low levels of ALS-linked Cu/Zn superoxide dismutase increases the production of reactive oxygen species and causes mitochondrial damage and death in motor neuron-like cells. J. Neurol. Sci. 232 (2005) 95-103
44. Sathasivam S., and Shaw P.J. Apoptosis in amyotrophic lateral sclerosis-what is the evidence?. Lancet Neurol. 4 (2005) 500-509
45. Shimizu S., Eguchi Y., Kamiike W., Waguri S., Uchiyama Y., Matsuda H., and Tsujmoto Y. Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 13 (1996) 21-29
46. Simpson E.P., Yen A.A., and Appel S.H. Oxidative stress: a common denominator in the pathogenesis of amyotrophic lateral sclerosis. Curr. Opin. Rheumatol. 15 (2003) 730-736
47. 2 production by membrane potential and NAD(P)H redox state. J. Neurochem. 86 (2003) 1101-1107
48. Sturtz L.A., Diekert K., Jensen L.T., Lill R., and Culotta V.C. 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. 276 (2001) 38084-38089
49. Tada-Oikawa S., Hiraku Y., Kawanishi M., and Kawanishi S. Mechanism for generation of hydrogen peroxide and change of mitochondrial membrane potential during rotenone-induced apoptosis. Life Sci. 73 (2003) 3277-3288
50. Tai K.-K., and Truong D.D. Activation of adenosine triphosphate-sensitive potassium channels confers protection against rotenone-induced cell death: therapeutic implications for Parkinson's disease. J. Neurosci. Res. 69 (2002) 559-566
51. Vijayvergiya A., Beal M.F., Buck J., and Manfredi G. Mutant superoxide dismutase 1 forms aggregates in the brain mitochondrial matrix of amyotrophic lateral sclerosis mice. J. Neurosci. 25 (2005) 2463-2470
52. Wolvetang E.J., Johnson K.L., Krauer K., Ralph S.J., and Linnane A.W. Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett. 339 (1994) 40-44
53. Yan L.-Y., and Sohal R.S. Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc. Natl. Acad. Sci. U.S.A. 98 (1998) 12896-12901
54. Zanzami N., and Kroemer G. The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell. Biol. 2 (2001) 67-71
55. Zhang Y., Marcillat O., Giulivi C., Ernster L., and Davies K.J.A. The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J. Biol. Chem. 27 (1990) 16330-16336