Antioxidant effects of JM-20 on rat brain mitochondria and synaptosomes: Mitoprotection against Ca2+-induced mitochondrial impairment

Brain Research Bulletin

Volumn 109, Issue , 2014, Pages 68-76

  Nuñez Figueredo, Yanier ^a   Pardo Andreu, Gilberto L ^b   Ramírez Sánchez, Jeney ^a   Delgado Hernández, René ^a   Ochoa Rodríguez, Estael ^c   Verdecia Reyes, Yamila ^c   Naal, Zeki ^d   Muller, Alexandre Pastoris ^e   Portela, Luis Valmor ^e   Souza, Diogo O ^e  

^a CENTRO DE INVESTIGACIÓN Y DESARROLLO DE MEDICAMENTOS CIDEM   (Cuba)

^b INSTITUTO DE FARMACIA Y ALIMENTOS   (Cuba)

^c UNIVERSITY OF HAVANA   (Cuba)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

^e FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Antioxidant; Brain ischemia; JM 20; Mitochondria; Neuroprotector; Synaptosomes

Indexed keywords

3 ETHOXYCARBONYL 2 METHYL 4 (2 NITROPHENYL) 4,11 DIHYDRO 1H PYRIDO[2,3 B][1,5]BENZODIAZEPINE; ANTIMYCIN A1; ANTIOXIDANT; CALCIUM; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; CYTOCHROME C; GLUCOSE; GLUTAMIC ACID; HYDROGEN PEROXIDE; MALIC ACID; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NEUROPROTECTIVE AGENT; OXYGEN; POTASSIUM; ROTENONE; SODIUM; SUCCINIC ACID; SUPEROXIDE; UNCLASSIFIED DRUG; 3-ETHOXYCARBONYL-2-METHYL-4-(2-NITROPHENYL)-4,11-DIHYDRO-1H-PYRIDO(2,3-B)(1,5)BENZODIAZEPINE; ADENOSINE TRIPHOSPHATE; BENZODIAZEPINE DERIVATIVE; CATALASE; ENZYME INHIBITOR; NICOTINIC ACID; OLIGOMYCIN; REACTIVE OXYGEN METABOLITE;

ANIMAL CELL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BRAIN MITOCHONDRION; BRAIN SYNAPTOSOME; CALCIUM TRANSPORT; CELL DEATH; CELL RESPIRATION; CEREBROVASCULAR ACCIDENT; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG STRUCTURE; ELECTROCHEMICAL ANALYSIS; IC50; MALE; MEMBRANE POTENTIAL; NONHUMAN; PROTEIN SECRETION; RAT; ANALOGS AND DERIVATIVES; ANIMAL; DOSE RESPONSE; DRUG EFFECTS; FOREBRAIN; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; SYNAPTOSOME; ULTRASTRUCTURE; WISTAR RAT;

ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIOXIDANTS; BENZODIAZEPINES; CALCIUM; CATALASE; CYTOCHROMES C; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NIACIN; OLIGOMYCINS; OXYGEN; PROSENCEPHALON; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; SUPEROXIDES; SYNAPTOSOMES;

EID: 84908332192     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2014.10.001     Document Type: Article

References (40)

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 Signal. 2005, 7:1140-1149.
2. Allen C.L., Bayraktutan U. Oxidative stress and its role in the pathogenesis of ischaemic stroke. Int. J. Stroke 2009, 4:461-470.
3. Chan P.H. Mitochondrial dysfunction and oxidative stress as determinants of cell death/survival in stroke. Ann. N.Y. Acad. Sci. 2005, 1042:203-209.
4. Chen H., Yoshioka H., Kim G.S., Jung J.E., Okami N., Sakata H., Maier C.M., Narasimhan P., Goeders C.E., Chan P.H. Oxidative stress in ischemic brain damage: mechanisms of cell death and potential molecular targets for neuroprotection. Antioxid. Redox Signal. 2011, 14:1505-1517.
5. 3+/ascorbate-stimulated lipid peroxidation in rat brain slices. Gen. Pharmacol. 1998, 31:385-391.
6. Drago I., Pizzo P., Pozzan T. After half a century mitochondrial calcium in- and efflux machineries reveal themselves. EMBO J. 2011, 30:4119-4125.
7. Figueredo Y.N., Rodríguez E.O., Reyes Y.V., Domínguez C.C., Parra A.L., Sánchez J.R., Hernández R.D., Verdecia M.P., Pardo Andreu G.L. Characterization of the anxiolytic and sedative profile of JM-20, a novel hybrid molecule with putative neuroprotective activity. Neurol. Res. 2013, 35:804-812.
8. Fiskum G. Mitochondrial participation in ischemic and traumatic neural cell death. J. Neurotrauma 2000, 17:843-855.
9. Fiskum G., Murphy A.N., Beal M.F. Mitochondria in neurodegeneration: acute ischemia and chronic neurodegenerative diseases. J. Cereb. Blood flow Metab. 1999, 19:351-369.
10. Han D., Williams E., Cadenas E. Mitochondrial respiratory chain dependent generation of superoxide anion and its release into the intermembrane space. Biochem. J. 2001, 353(Pt 2):411-416.
11. Hill M.D., Martin R.H., Mikulis D., Wong J.H., Silver F.L., Terbrugge K.G., Milot G., Clark W.M., Macdonald R.L., Kelly M.E., et al. Safety and efficacy of NA-1 in patients with iatrogenic stroke after endovascular aneurysm repair (ENACT): a phase 2, randomised, double-blind, placebocontrolled trial. Lancet Neurol. 2012, 11:942-950.
12. Hirsch T., Susin S.A., Marzo I., Marchetti P., Zamzami N., Kroemer G. Mitochondrial permeability transition in apoptosis and necrosis. Cell Biol. Toxicol. 1998, 14:141-145.
13. Kilbride S.M., Gluchowska S.A., Telford J.E., O' Sullivan C., Davey G.P. High-level inhibition of mitochondrial complexes III and IV is required to increase glutamate release from the nerve terminal. Mol. Neurodegen. 2011, 6:53.
14. Kruglov A.G., Subbotina K.B., Saris N.E.L. Redox-cycling compounds can cause de permeabilization of mitochondrial membranes by mechanisms other than ROS production. Free Rad. Biol. Med. 2008, 44:646-656.
15. Lau A., Tymianski M. Glutamate receptors, neurotoxicity and neurodegeneration. Pflügers Arch.: Eur. J. Physiol. 2010, 460:525-542.
16. Lemasters J.J., Hackenbrock C.R. Continuous measurement and rapid kinetics of ATP synthesis in rat liver mitochondria, mitoplasts and inner membrane vesicles determined by firefly-luciferase luminescence. Eur. J. Biochem. 1976, 67:1-10.
17. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91:479-489.
18. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
19. Liu Y., Fiskum G., Schubert D. Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 2002, 80:780-787.
20. Manzanero S., Santro T., Arumugam T.V. Neuronal oxidative stress in acute ischemic stroke: sources and contribution to cell injury. Neurochem. Int. 2013, 62:712-718.
21. Mazat J.P., Rossignol R., Malgat M., Rocher C., Faustin B., Letellier T. What do mitochondrial diseases teach us about normal mitochondrial functions. . .that we already knew: threshold expression of mitochondrial defects. Biochim. Biophys. Acta 2001, 1504:20-30.
22. Nagai T., Sakai M., Inoue R., Inoue H., Suzuki N. Antioxidative activities of some commercially honeys, royal jelly, and propolis. Food Chem. 2001, 75:237-240.
23. Niizuma K., Endo H., Chan P.H. Oxidative stress and mitochondrial dysfunction as determinants of ischemic neuronal death and survival. J. Neurochem. 2009, 109(Suppl 1):133-138.
24. Nuñez-Figueredo Y., Ramírez-Sánchez J., Hansel G., Nicoloso-Simões E., Merino N., Valdes O., Delgado-Hernández R., Lagarto-Parra A., Ochoa-Rodríguez E., Verdecia-Reyes Y., Salbego C., et al. A novel multi-target ligand (JM-20) protects mitochondrial integrity, inhibits brain excitatory amino acids release and reduces cerebral ischemia injury in vitro and in vivo. Neuropharmacoly 2014, 85:517-527.
25. Nuñez-Figueredo Y., Ramírez-Sánchez J., Delgado-Hernández R., Porto-Verdecia M., Ochoa-Rodríguez E., Verdecia-Reyes Y., Marin-Prida J., González-Durruthy M., Uyemura S.A., Rodrigues F.P., et al. JM-20, a novel benzodiazepine-dihydropyridine hybrid molecule, protects mitochondria and prevents ischemic insult-mediated neural cell death in vitro. Eur. J. Pharmacol. 2014, 726:57-65.
26. Núñez-Vergara L.J., Ortiz M.E., Bollo S., Squella J.A. Electrochemical generation and reactivity of free radical redox intermediates from ortho-and meta-nitro substituted 1,4-dihydropyridines. Chem.-Biol. Interact. 1997, 106:1-14.
27. Perluigi M., Swomley A.M., Butterfield D.A. Redox proteomics and the dynamic molecular landscape of the aging brain. Ageing Res. Rev. 2013, 13C:75-89.
28. 2+ concentrations associated with glutamate excitotoxicity in cultured rat brain neurons. Neurosci. Lett. 1993, 162:149-152.
29. Rossignol R., Malgat M., Mazat J.P., Letellier T. Threshold effect and tissue specificity. Implication for mitochondrial cytopathies. J. Biol. Chem. 1999, 274:33426-33432.
30. Saito A., Castilho R.F. Inhibitory effects of adenine nucleotides on brain mitochondrial permeability transition. Neurochem. Res. 2010, 35:1667-1674.
31. Sarnowska A., Berȩsewicz M., Zabłocka B., Domańska-Janik K. Diazepam neuroprotection in excitotoxic and oxidative stress involves a mitochondrial mechanism additional to the GABAAR and hypothermic effects. Neurochem. Int. 2009, 55:164-173.
32. Sims N.R. Rapid isolation of metabolically active mitochondria from rat brain and subregions using Percoll density gradient centrifugation. J. Neurochem. 1990, 55:698-707.
33. Sims N.R., Anderson M.F. Isolation of mitochondria from rat brain using Percoll density gradient centrifugation. Nat. Protoc. 2008, 3:1228-1239.
34. Sims N.R., Blass J.P. Expression of classical mitochondrial respiratory responses in homogenates of rat forebrain. J. Neurochem. 1986, 47:496-505.
35. Sullivan P.G., Rabchevsky A.G., Waldmeier P.C., Springer J.E. Mitochondrial permeability transition in CNS trauma: cause or effect of neuronal cell death?. J. Neurosci. Res. 2005, 79:231-239.
36. Taya K., Watanabe Y., Kobayashi H., Fujiwara M. Nimodipine improves the disruption of spatial cognition induced by cerebral ischemia. Physiol. Behav. 2000, 70:19-25.
37. Tretter L., Liktor B., Adam-Vizi V. Dual effect of pyruvate in isolated nerve terminals: generation of reactive oxygen species and protection of aconitase. Neurochem. Res. 2005, 30:1331-1338.
38. Wang Y., Qin Z.H. Molecular and cellular mechanisms of excitotoxic neuronal death. Apoptosis 2010, 15:1382-1402.
39. Yáñez C., López-Alarcón C., Camargo C., Valenzuela V., Squella A., Núñez-Vergara L.J. Structural effects on the reactivity 1,4-dihydropyridines with alkylperoxyl radicals and ABTS radical cation. Bioorg. Med. Chem. 2004, 12:2459-2468.
40. Zanotti A., Azzone G.F. Safranine as membrane potential probe in rat liver mitochondria. Arch. Biochem. Biophys. 1980, 201:255-265.