Neuroprotective effects of the mitochondria-targeted antioxidant MitoQ in a model of inherited amyotrophic lateral sclerosis

Free Radical Biology and Medicine

Volumn 70, Issue , 2014, Pages 204-213

  Miquel, Ernesto ^a   Cassina, Adriana ^a   Martínez Palma, Laura ^a   Souza, José M ^a   Bolatto, Carmen ^a   Rodríguez Bottero, Sebastián ^a   Logan, Angela ^b   Smith, Robin A J ^c   Murphy, Michael P ^b   Barbeito, Luis ^d   Radi, Rafael ^a   Cassina, Patricia ^a  

^a DEPARTAMENTO DE BIOQUÍMICA   (Uruguay)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

^c UNIVERSITY OF OTAGO   (New Zealand)

^d INSTITUT PASTEUR DE MONTEVIDEO   (Uruguay)

Author keywords

Amyotrophic lateral sclerosis; Antioxidants; Free radicals; Mitochondria; MitoQ; Nitroxidative stress

Indexed keywords

ANTIOXIDANT; COPPER ZINC SUPEROXIDE DISMUTASE; MITOQ; UNCLASSIFIED DRUG; [10 4 (5 DIMETHOXY 2 METHYL 3,6 DIOXO 1,4 CYCLOHEXADIEN 1 YL)DECYL]TRIPHENYLPHOSPHONIUM METHANE SULFONATE; 10-(6'-UBIQUINONYL)DECYLTRIPHENYLPHOSPHONIUM BROMIDE; NEUROPROTECTIVE AGENT; ORGANOPHOSPHORUS COMPOUND; UBIQUINONE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; ASTROCYTOSIS; CELL COUNT; CONTROLLED STUDY; DISEASE COURSE; DRUG EFFECT; DRUG TARGETING; DRUG TISSUE LEVEL; FEMALE; FUNCTIONAL ASSESSMENT; GENETIC DISORDER; GRIP STRENGTH; HIGH RESOLUTION RESPIROMETRY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOTONEURON; MOTOR PERFORMANCE; MOUSE; MSOD1 MOUSE; NERVE DEGENERATION; NEUROMUSCULAR SYNAPSE; NEUROPATHOLOGY; NEUROPROTECTION; NITROXIDATIVE STRESS; NONHUMAN; OUTCOME ASSESSMENT; OXIDATIVE STRESS; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; RESPIROMETRY; SPINAL CORD; SURVIVAL RATE; ANALOGS AND DERIVATIVES; ANIMAL; DISEASE MODEL; DRUG EFFECTS; HUMAN; METABOLISM;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ANTIOXIDANTS; DISEASE MODELS, ANIMAL; HUMANS; MICE; MITOCHONDRIA; NEUROPROTECTIVE AGENTS; ORGANOPHOSPHORUS COMPOUNDS; OXIDATIVE STRESS; UBIQUINONE;

EID: 84897006654     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.02.019     Document Type: Article

References (59)

1. M.R. Turner, O. Hardiman, M. Benatar, B.R. Brooks, A. Chio, M. de Carvalho, P.G. Ince, C. Lin, R.G. Miller, H. Mitsumoto, G. Nicholson, J. Ravits, P.J. Shaw, M. Swash, K. Talbot, B.J. Traynor, L.H. Van den Berg, J.H. Veldink, S. Vucic, and M.C. Kiernan Controversies and priorities in amyotrophic lateral sclerosis Lancet Neurol. 12 2013 310 322
2. H. Kawamata, and G. Manfredi Mitochondrial dysfunction and intracellular calcium dysregulation in ALS Mech. Ageing Dev. 131 2010 517 526
3. A.G. Estevez, J.P. Crow, J.B. Sampson, C. Reiter, Y. Zhuang, G.J. Richardson, M.M. Tarpey, L. Barbeito, and J.S. Beckman Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase Science 286 1999 2498 2500
4. C. Raoul, A.G. Estevez, H. Nishimune, D.W. Cleveland, O. deLapeyriere, C.E. Henderson, G. Haase, and B. Pettmann Motoneuron death triggered by a specific pathway downstream of Fas: potentiation by ALS-linked SOD1 mutations Neuron 35 2002 1067 1083
5. P. Cassina, H. Peluffo, M. Pehar, L. Martinez-Palma, A. Ressia, J.S. Beckman, A.G. Estevez, and L. Barbeito Peroxynitrite triggers a phenotypic transformation in spinal cord astrocytes that induces motor neuron apoptosis J. Neurosci. Res. 67 2002 21 29
6. P. Cassina, M. Pehar, M.R. Vargas, R. Castellanos, A.G. Barbeito, A.G. Estevez, J.A. Thompson, J.S. Beckman, and L. Barbeito Astrocyte activation by fibroblast growth factor-1 and motor neuron apoptosis: implications for amyotrophic lateral sclerosis J. Neurochem. 93 2005 38 46
7. M. Pehar, P. Cassina, M.R. Vargas, R. Castellanos, L. Viera, J.S. Beckman, A.G. Estevez, and L. Barbeito Astrocytic production of nerve growth factor in motor neuron apoptosis: implications for amyotrophic lateral sclerosis J. Neurochem. 89 2004 464 473
8. R.W. Orrell, R.J. Lane, and M. Ross A systematic review of antioxidant treatment for amyotrophic lateral sclerosis/motor neuron disease Amyotrophic Lateral Scler. 9 2008 195 211
9. P. Kaufmann, J.L. Thompson, G. Levy, R. Buchsbaum, J. Shefner, L.S. Krivickas, J. Katz, Y. Rollins, R.J. Barohn, C.E. Jackson, E. Tiryaki, C. Lomen-Hoerth, C. Armon, R. Tandan, S.A. Rudnicki, K. Rezania, R. Sufit, A. Pestronk, S.P. Novella, T. Heiman-Patterson, E.J. Kasarskis, E.P. Pioro, J. Montes, R. Arbing, D. Vecchio, A. Barsdorf, H. Mitsumoto, and B. Levin Phase II trial of CoQ10 for ALS finds insufficient evidence to justify phase III Ann. Neurol. 66 2009 235 244
10. N. Atassi, E.M. Ratai, D.J. Greenblatt, D. Pulley, Y. Zhao, J. Bombardier, S. Wallace, J. Eckenrode, M. Cudkowicz, and A. Dibernardo A phase I, pharmacokinetic, dosage escalation study of creatine monohydrate in subjects with amyotrophic lateral sclerosis Amyotrophic Lateral Scler. 11 2010 508 513
11. R.A.J. Smith, R.C. Hartley, H.M. Cocheme, and M.P. Murphy Mitochondrial pharmacology Trends Pharmacol. Sci. 33 2012 341 352
12. R.A.J. Smith, R.C. Hartley, and M.P. Murphy Mitochondria-targeted small molecule therapeutics and probes Antioxid. Redox Signaling 15 2011 3021 3038
13. M.P. Murphy, and R.A.J. Smith Targeting antioxidants to mitochondria by conjugation to lipophilic cations Annu. Rev. Pharmacol. Toxicol. 47 2007 629 656
14. G.F. Kelso, C.M. Porteous, C.V. Coulter, G. Hughes, W.K. Porteous, E.C. Ledgerwood, R.A.J. Smith, and M.P. Murphy Selective targeting of a redox-active ubiquinone to mitochondria within cells: antioxidant and antiapoptotic properties J. Biol. Chem. 276 2001 4588 4596
15. R.A.J. Smith, and M.P. Murphy Animal and human studies with the mitochondria-targeted antioxidant MitoQ Ann. N. Y. Acad. Sci. 1201 2010 96 103
16. M.J. McManus, M.P. Murphy, and J.L. Franklin The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimerx's disease J. Neurosci. 31 2011 15703 15715
17. R.A.J. Smith, C.M. Porteous, C.V. Coulter, and M.P. Murphy Selective targeting of an antioxidant to mitochondria Eur. J. Biochem. 263 1999 709 716
18. A. Ghosh, K. Chandran, S.V. Kalivendi, J. Joseph, W.E. Antholine, C.J. Hillard, A. Kanthasamy, and B. Kalyanaraman Neuroprotection by a mitochondria-targeted drug in a Parkinsonx's disease model Free Radic. Biol. Med. 49 2010 1674 1684
19. M.E. Gurney, H. Pu, A.Y. Chiu, M.C. Dal Canto, C.Y. Polchow, D.D. Alexander, J. Caliendo, A. Hentati, Y.W. Kwon, and H.X. Deng et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation Science 264 1994 1772 1775
20. D.S. Howland, J. Liu, Y. She, B. Goad, N.J. Maragakis, B. Kim, J. Erickson, J. Kulik, L. DeVito, G. Psaltis, L.J. DeGennaro, D.W. Cleveland, and J.D. Rothstein Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS) Proc. Natl. Acad. Sci. USA 99 2002 1604 1609
21. A.M. Clement, M.D. Nguyen, E.A. Roberts, M.L. Garcia, S. Boillee, M. Rule, A.P. McMahon, W. Doucette, D. Siwek, R.J. Ferrante, R.H. Brown Jr, J.P. Julien, L.S. Goldstein, and D.W. Cleveland Wild-type nonneuronal cells extend survival of SOD1 mutant motor neurons in ALS mice Science 302 2003 113 117
22. H. Ilieva, M. Polymenidou, and D.W. Cleveland Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond J. Cell Biol. 187 2009 761 772
23. M. Pehar, M.R. Vargas, K.M. Robinson, P. Cassina, P.J. Diaz-Amarilla, T.M. Hagen, R. Radi, L. Barbeito, and J.S. Beckman Mitochondrial superoxide production and nuclear factor erythroid 2-related factor 2 activation in p75 neurotrophin receptor-induced motor neuron apoptosis J. Neurosci. 27 2007 7777 7785
24. P. Cassina, A. Cassina, M. Pehar, R. Castellanos, M. Gandelman, A. de Leon, K.M. Robinson, R.P. Mason, J.S. Beckman, L. Barbeito, and R. Radi Mitochondrial dysfunction in SOD1G93A-bearing astrocytes promotes motor neuron degeneration: prevention by mitochondrial-targeted antioxidants J. Neurosci. 28 2008 4115 4122
25. J.B. Levine, J. Kong, M. Nadler, and Z. Xu Astrocytes interact intimately with degenerating motor neurons in mouse amyotrophic lateral sclerosis (ALS) Glia 28 1999 215 224
26. M.F. Ross, T.A. Prime, I. Abakumova, A.M. James, C.M. Porteous, R.A.J. Smith, and M.P. Murphy Rapid and extensive uptake and activation of hydrophobic triphenylphosphonium cations within cells Biochem. J. 411 2008 633 645
27. S. Rodriguez-Cuenca, H.M. Cocheme, A. Logan, I. Abakumova, T.A. Prime, C. Rose, A. Vidal-Puig, A.C. Smith, D.C. Rubinsztein, I.M. Fearnley, B.A. Jones, S. Pope, S.J. Heales, B.Y. Lam, S.G. Neogi, I. McFarlane, A.M. James, R.A.J. Smith, and M.P. Murphy Consequences of long-term oral administration of the mitochondria-targeted antioxidant MitoQ to wild-type mice Free Radic. Biol. Med. 48 2010 161 172
28. Y. Li, H. Zhang, J.P. Fawcett, and I.G. Tucker Quantitation and metabolism of mitoquinone, a mitochondria-targeted antioxidant, in rat by liquid chromatography/tandem mass spectrometry Rapid Commun. Mass Spectrom. 21 2007 1958 1964
29. Y. Li, J.P. Fawcett, H. Zhang, and I.G. Tucker Transport and metabolism of MitoQ10, a mitochondria-targeted antioxidant, in Caco-2 cell monolayers J. Pharm. Pharmacol. 59 2007 503 511
30. E. Gnaiger Mitochondrial Pathways and Respiratory Control 2007 Oroboros MiPNet Publications Innsbruck
31. E. Miquel, A. Cassina, L. Martinez-Palma, C. Bolatto, E. Trias, M. Gandelman, R. Radi, L. Barbeito, and P. Cassina Modulation of astrocytic mitochondrial function by dichloroacetate improves survival and motor performance in inherited amyotrophic lateral sclerosis PLoS One 7 2012 e34776
32. C. Brito, M. Naviliat, A.C. Tiscornia, F. Vuillier, G. Gualco, G. Dighiero, R. Radi, and A.M. Cayota Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death J. Immunol. 162 1999 3356 3366
33. D.A. Drechsel, A.G. Estevez, L. Barbeito, and J.S. Beckman Nitric oxide-mediated oxidative damage and the progressive demise of motor neurons in ALS Neurotox. Res. 22 2012 251 264
34. M.R. Vargas, M. Pehar, P. Cassina, L. Martinez-Palma, J.A. Thompson, J.S. Beckman, and L. Barbeito Fibroblast growth factor-1 induces heme oxygenase-1 via nuclear factor erythroid 2-related factor 2 (Nrf2) in spinal cord astrocytes: consequences for motor neuron survival J. Biol. Chem. 280 2005 25571 25579
35. L.R. Fischer, D.G. Culver, P. Tennant, A.A. Davis, M. Wang, A. Castellano-Sanchez, J. Khan, M.A. Polak, and J.D. Glass Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man Exp. Neurol. 185 2004 232 240
36. R. Liu, B. Li, S.W. Flanagan, L.W. Oberley, D. Gozal, and M. Qiu Increased mitochondrial antioxidative activity or decreased oxygen free radical propagation prevent mutant SOD1-mediated motor neuron cell death and increase amyotrophic lateral sclerosis-like transgenic mouse survival J. Neurochem. 80 2002 488 500
37. E. Linares, L.V. Seixas, J.N. Dos Prazeres, F.V. Ladd, A.A. Ladd, A.A. Coppi, and O. Augusto Tempol moderately extends survival in a hSOD1(G93A) ALS rat model by inhibiting neuronal cell loss, oxidative damage and levels of non-native hSOD1(G93A) forms PLoS One 8 2013 e55868
38. J.P. Crow, N.Y. Calingasan, J. Chen, J.L. Hill, and M.F. Beal Manganese porphyrin given at symptom onset markedly extends survival of ALS mice Ann. Neurol. 58 2005 258 265
39. A.S. Wu, M. Kiaei, N. Aguirre, J.P. Crow, N.Y. Calingasan, S.E. Browne, and M.F. Beal Iron porphyrin treatment extends survival in a transgenic animal model of amyotrophic lateral sclerosis J. Neurochem. 85 2003 142 150
40. M.F. Beal Mitochondria take center stage in aging and neurodegeneration Ann. Neurol. 58 2005 495 505
41. R. Radi, A. Cassina, and R. Hodara Nitric oxide and peroxynitrite interactions with mitochondria Biol. Chem. 383 2002 401 409
42. A.J. Kowaltowski, and A.E. Vercesi Mitochondrial damage induced by conditions of oxidative stress Free Radic. Biol. Med. 26 1999 463 471
43. J.P. Bolaños, M.A. Moro, I. Lizasoain, and A. Almeida Mitochondria and reactive oxygen and nitrogen species in neurological disorders and stroke: therapeutic implications Adv. Drug Delivery Rev. 61 2009 1299 1315
44. M.R. Vargas, M. Pehar, P. Cassina, J.S. Beckman, and L. Barbeito Increased glutathione biosynthesis by Nrf2 activation in astrocytes prevents p75NTR-dependent motor neuron apoptosis J. Neurochem. 97 2006 687 696
45. M. Nagai, D.B. Re, T. Nagata, A. Chalazonitis, T.M. Jessell, H. Wichterle, and S. Przedborski Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons Nat. Neurosci. 10 2007 615 622
46. F.P. Di Giorgio, M.A. Carrasco, M.C. Siao, T. Maniatis, and K. Eggan Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model Nat. Neurosci. 10 2007 608 614
47. H.M. Cocheme, G.F. Kelso, A.M. James, M.F. Ross, J. Trnka, T. Mahendiran, J. Asin-Cayuela, F.H. Blaikie, A.R. Manas, C.M. Porteous, V.J. Adlam, R.A.J. Smith, and M.P. Murphy Mitochondrial targeting of quinones: therapeutic implications Mitochondrion 7 Suppl 2007 S94 102
48. L. Dupuis, and J.P. Loeffler Neuromuscular junction destruction during amyotrophic lateral sclerosis: insights from transgenic models Curr. Opin. Pharmacol. 9 2009 341 346
49. M. Suzuki, C. Tork, B. Shelley, J. McHugh, K. Wallace, S.M. Klein, M.J. Lindstrom, and C.N. Svendsen Sexual dimorphism in disease onset and progression of a rat model of ALS Amyotrophic Lateral Scler. 8 2007 20 25
50. I.G. Kirkinezos, D. Hernandez, W.G. Bradley, and C.T. Moraes Regular exercise is beneficial to a mouse model of amyotrophic lateral sclerosis Ann. Neurol. 53 2003 804 807
51. M.E. Cudkowicz, K.A. Pastusza, P.C. Sapp, R.K. Mathews, J. Leahy, P. Pasinelli, J.W. Francis, D. Jiang, J.K. Andersen, and R.H. Brown Jr. Survival in transgenic ALS mice does not vary with CNS glutathione peroxidase activity Neurology 59 2002 729 734
52. D.J. Mahoney, C. Rodriguez, M. Devries, N. Yasuda, and M.A. Tarnopolsky Effects of high-intensity endurance exercise training in the G93A mouse model of amyotrophic lateral sclerosis Muscle Nerve 29 2004 656 662
53. C.J. Alves, L.P. de Santana, A.J. dos Santos, G.P. de Oliveira, T. Duobles, J.M. Scorisa, R.S. Martins, J.R. Maximino, and G. Chadi Early motor and electrophysiological changes in transgenic mouse model of amyotrophic lateral sclerosis and gender differences on clinical outcome Brain Res. 1394 2011 90 104
54. C.I. Choi, Y.D. Lee, B.J. Gwag, S.I. Cho, S.S. Kim, and H. Suh-Kim Effects of estrogen on lifespan and motor functions in female hSOD1 G93A transgenic mice J. Neurol. Sci. 268 2008 40 47
55. S. Scott, J.E. Kranz, J. Cole, J.M. Lincecum, K. Thompson, N. Kelly, A. Bostrom, J. Theodoss, B.M. Al-Nakhala, F.G. Vieira, J. Ramasubbu, and J.A. Heywood Design, power, and interpretation of studies in the standard murine model of ALS Amyotrophic Lateral Scler. 9 2008 4 15
56. G. Giordano, L. Tait, C.E. Furlong, T.B. Cole, T.J. Kavanagh, and L.G. Costa Gender differences in brain susceptibility to oxidative stress are mediated by levels of paraoxonase-2 expression Free Radic. Biol. Med. 58C 2013 98 108
57. R. Li, R. Strykowski, M. Meyer, P. Mulcrone, D. Krakora, and M. Suzuki Male-specific differences in proliferation, neurogenesis, and sensitivity to oxidative stress in neural progenitor cells derived from a rat model of ALS PLoS One 7 2012 e48581
58. S. Petri, M. Kiaei, K. Kipiani, J. Chen, N.Y. Calingasan, J.P. Crow, and M.F. Beal Additive neuroprotective effects of a histone deacetylase inhibitor and a catalytic antioxidant in a transgenic mouse model of amyotrophic lateral sclerosis Neurobiol. Dis. 22 2006 40 49
59. E.A. Schon, and S. Przedborski Mitochondria: the next (neurode)generation Neuron 70 2011 1033 1053