Monoamine oxidase-B mediates ecstasy-induced neurotoxic effects to adolescent rat brain mitochondria

Journal of Neuroscience

Volumn 27, Issue 38, 2007, Pages 10203-10210

  Alves, Ema ^a,b   Summavielle, Teresa ^a,c   Alves, Cecília Juliana ^a   Gomes da Silva, Joana ^a,d   Barata, José Custódio ^e   Fernandes, Eduarda ^b   Bastos, Maria De Lourdes ^b   Tavares, Maria Amélia ^a,b   Carvalho, Félix ^b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c POLYTECHNIC INSTITUTE OF PORTO   (Portugal)

^d UNIVERSITY OF AVEIRO   (Portugal)

^e UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

3,4 methylenedioxymethamphetamine; Adolescent rat model; Brain mitochondria; Monoamine oxidase B; Neurotoxicity; Oxidative stress

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; CYTOCHROME C OXIDASE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SELEGILINE; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CONTROLLED STUDY; DRUG BRAIN LEVEL; DRUG INHIBITION; HYPERTHERMIA; LIPID PEROXIDATION; MALE; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN EXPRESSION; RAT; WESTERN BLOTTING; WISTAR RAT;

AGE FACTORS; ANIMALS; BRAIN; LIPID PEROXIDATION; MALE; MITOCHONDRIA; MONOAMINE OXIDASE; MONOAMINE OXIDASE INHIBITORS; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; NEUROTOXICITY SYNDROMES; RATS; RATS, WISTAR;

EID: 34548842751     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2645-07.2007     Document Type: Article

References (48)

1. Agostinelli E, Arancia G, Vedova LD, Belli F, Marra M, Salvi M, Toninello A (2004) The biological functions of polyamine oxidation products by amine oxidases: perspectives of clinical applications. Amino Acids 27:347-358.
2. Aguirre N, Galbete JL, Lasheras B, Del Rio J (1995) Methylenedioxymethamphetamine induces opposite changes in central pre- and postsynaptic 5-HT1A receptors in rats. Eur J Pharmacol 281:101-105.
3. Arai R, Karasawa N, Kurokawa K, Kanai H, Horiike K, Ito A (2002) Differential subcellular location of mitochondria in rat serotonergic neurons depends on the presence and the absence of monoamine oxidase type B. Neuroscience 114:825-835.
4. Battaglia G, Yeh SY, O'Hearn E, Molliver ME, Kuhar MJ, De Souza EB (1987) 3,4-Methylenedioxymethamphetamine and 3,4-methylenedioxyamphetamine destroy serotonin terminals in rat brain: quantification of neurodegeneration by measurement of [3H]paroxetine-labeled serotonin uptake sites. J Pharmacol Exp Ther 242:911-916.
5. Battaglia G, Sharkey J, Kuhar MJ, de Souza EB (1991) Neuroanatomic specificity and time course of alterations in rat brain serotonergic pathways induced by MDMA (3,4-methylenedioxymethamphetamine): assessment using quantitative autoradiography. Synapse 8:249-260.
6. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302-310.
7. Capela JP, Ruscher K, Lautenschlager M, Freyer D, Dirnagl U, Gaio AR, Bastos ML, Meisel A, Carvalho F (2006a) Ecstasy-induced cell death in cortical neuronal cultures is serotonin 2A-receptor-dependent and potentiated under hyperthermia. Neuroscience 139:1069-1081.
8. Capela JP, Meisel A, Abreu AR, Branco PS, Ferreira LM, Lobo AM, Remiao F, Bastos ML, Carvalho F (2006b) Neurotoxicity of ecstasy metabolites in rat cortical neurons, and influence of hyperthermia. J Pharmacol Exp Ther 316:53-61.
9. Carvalho M, Carvalho F, Pereira ML, Pires-das-Neves R, Bastos ML (2002) Effect of 3,4-methylenedioxymethamphetamine ("ecstacy") on body temperature and liver antioxidant status in mice. Influence of ambient temperature. Arch Toxicol 76:166-172.
10. Commins DL, Vosmer G, Virus RM, Woolverton WL, Schuster CR, Seiden LS (1987) Biochemical and histological evidence that methylenedioxymethylamphetamine (MDMA) is toxic to neurons in the rat brain. J Pharmacol Exp Ther 241:338-345.
11. Falk EM, Cook VJ, Nichols DE, Sprague JE (2002) An antisense oligonucleotide targeted at MAO-B attenuates rat striatal serotonergic neurotoxicity induced by MDMA. Pharmacol Biochem Behav 72:617-622.
12. Ferger B, van Amsterdam C, Seyfried C, Kuschinsky K (1998) Effects of alpha-phenyl-tert-butylnitrone and selegiline on hydroxyl free radicals in rat striatum produced by local application of glutamate. J Neurochem 70:276-280.
13. Finnegan KT, Ricaurte GA, Ritchie LD, Irwin I, Peroutka SJ, Langston JW (1988) Orally administered MDMA causes a long-term depletion of serotonin in rat brain. Brain Res 447:141-144.
14. Fone KC, Beckett SR, Topham IA, Swettenham J, Ball M, Maddocks L (2002) Long-term changes in social interaction and reward following repeated MDMA administration to adolescent rats without accompanying serotonergic neurotoxicity. Psychopharmacology (Berl) 159:437-444.
15. Fornai F, Giorgi FS, Gesi M, Chen K, Alessri MG, Shih JC (2001) Biochemical effects of the monoamine neurotoxins DSP-4 and MDMA in specific brain regions of MAO-B-deficient mice. Synapse 39:213-221.
16. Fowler CJ, Tipton KF (1982) Deamination of 5-hydroxytryptamine by both forms of monoamine oxidase in the rat brain. J Neurochem 38:733-736.
17. Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751-766.
18. Green AR, Cross AJ, Goodwin GM (1995) Rev of the pharmacology and clinical pharmacology of 3,4-methylenedioxymethamphetamine (MDMA or "ecstasy"). Psychopharmacology (Berl) 119:247-260.
19. Green AR, Mechan AO, Elliott JM, O'Shea E, Colado MI (2003) The pharmacology and clinical pharmacology of 3,4-methylenedioxymethamphetamine (MDMA, "ecstasy"). Pharmacol Rev 55:463-508.
20. Green AR, O'Shea E, Saadat KS, Elliott JM, Colado MI (2005) Studies on the effect of MDMA ("ecstasy") on the body temperature of rats housed at different ambient room temperatures. Br J Pharmacol 146:306-312.
21. Gudelsky GA, Yamamoto BK (2003) Neuropharmacology and neurotoxicity of 3,4-methylenedioxymethamphetamine. Methods Mol Med 79:55-73.
22. Hatzidimitriou G, McCann UD, Ricaurte GA (1999) Altered serotonin innervation patterns in the forebrain of monkeys treated with (+/-)3,4-methylenedioxymethamphetamine seven years previously: factors influencing abnormal recovery. J Neurosci 19:5096-5107.
23. Hrometz SL, Brown AW, Nichols DE, Sprague JE (2004) 3,4- Methylenedioxymethamphetamine (MDMA, ecstasy)-mediated production of hydrogen peroxide in an in vitro model: the role of dopamine, the serotonin-reuptake transporter, and monoamine oxidase-B. Neurosci Lett 367:56-59.
24. Jones DC, Lau SS, Monks TJ (2004) Thioether metabolites of 3,4-methylenedioxyamphetamine and 3,4-methylenedioxymethamphetamine inhibit human serotonin transporter (hSERT) function and simultaneously stimulate dopamine uptake into hSERT-expressing SK-N-MC cells. J Pharmacol Exp Ther 311:298-306.
25. Koenig J, Lazarus C, Jeltsch H, Ben Hamida S, Riegert C, Kelche C, Jones BC, Cassel JC (2005) MDMA (ecstasy) effects in pubescent rats: males are more sensitive than females. Pharmacol Biochem Behav 81:635-644.
26. Kort WJ, Hekking-Weijma JM, TenKate MT, Sorm V, VanStrik R (1998) A microchip implant system as a method to determine body temperature of terminally ill rats and mice. Lab Anim 32:260-269.
27. Leonardi ET, Azmitia EC (1994) MDMA (ecstasy) inhibition of MAO type A and type B: comparisons with fenfluramine and fluoxetine (Prozac). Neuropsychopharmacology 10:231-238.
28. Malberg JE, Seiden LS (1998) Small changes in ambient temperature cause large changes in 3,4-methylenedioxymethamphetamine (MDMA)-induced serotonin neurotoxicity and core body temperature in the rat. J Neurosci 18:5086-5094.
29. Mathai JC, Sitaramam V (1994) Stretch sensitivity of transmembrane mobility of hydrogen peroxide through voids in the bilayer. Role of cardiolipin. J Biol Chem 269:17784-17793.
30. Moll GH, Mehnert C, Wicker M, Bock N, Rothenberger A, Ruther E, Huether G (2000) Age-associated changes in the densities of presynaptic monoamine transporters in different regions of the rat brain from early juvenile life to late adulthood. Dev Brain Res 119:251-257.
31. Montoya AG, Sorrentino R, Lukas SE, Price BH (2002) Long-term neuropsychiatric consequences of "ecstasy" (MDMA): a review. Harv Rev Psychiatry 10:212-220.
32. Muralikrishnan D, Samantaray S, Mohanakumar KP (2003) D-deprenyl protects nigrostriatal neurons against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine- induced dopaminergic neurotoxicity. Synapse 50:7-13.
33. O'Hearn E, Battaglia G, De Souza EB, Kuhar MJ, Molliver ME (1988) Methylenedioxyamphetamine (MDA) and methylenedioxymethamphetamine (MDMA) cause selective ablation of serotonergic axon terminals in forebrain: immunocytochemical evidence for neurotoxicity. J Neurosci 8:2788-2803.
34. Piper BJ, Fraiman JB, Meyer JS (2005) Repeated MDMA ("ecstasy") exposure in adolescent male rats alters temperature regulation, spontaneous motor activity, attention, and serotonin transporter binding. Dev Psychobiol 47:145-157.
35. Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol 233:357-363.
36. Ricaurte GA, Forno LS, Wilson MA, DeLanney LE, Irwin I, Molliver ME, Langston JW (1988) (+/-)3,4-Methylenedioxymethamphetamine selectively damages central serotonergic neurons in nonhuman primates. JAMA 260:51-55.
37. Rohn TT, Hinds TR, Vincenzi FF (1993) Ion transport ATPases as targets for free radical damage. Protection by an aminosteroid of the Ca2+ pump ATPase and Na+/K+ pump ATPase of human red blood cell membranes. Biochem Pharmacol 46:525-534.
38. Rosenthal RE, Hamud F, Fiskum G, Varghese PJ Sharpe S (1987) Cerebral ischemia and reperfusion: prevention of brain mitochondrial injury by lidoflazine. J Cereb Blood Flow Metab 7:752-758.
39. Schmidt CJ (1987) Neurotoxicity of the psychedelic amphetamine, methylenedioxymethamphetamine. J Pharmacol Exp Ther 240:1-7.
40. Sharma SK, Carlson EC, Ebadi M (2003) Neuroprotective actions of Selegiline in inhibiting 1-methyl, 4-phenyl, pyridinium ion (MPP+)-induced apoptosis in SK-N-SH neurons. J Neurocytol 32:329-343.
41. Shigenaga MK, Hagen TM, Ames BN (1994) Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci USA 91:10771-10778.
42. Shih JC, Grimsby J, Chen K (1999) Molecular biology of monoamine oxidase A and B: their role in the degradation of serotonin. In: Serotoninergic neurons and 5-HT receptors in the SNC (Gothert HB, ed), pp 655-670. Berlin: Springer.
43. Sprague JE, Nichols DE (1995) The monoamine oxidase-B inhibitor L-deprenyl protects against 3,4-methylenedioxymethamphetamine-induced lipid peroxidation and long-term serotonergic deficits. J Pharmacol Exp Ther 273:667-673.
44. Sprague JE, Everman SL, Nichols DE (1998) An integrated hypothesis for the serotonergic axonal loss induced by 3,4-methylenedioxymethamphetamine. Neurotoxicology 19:427-441.
45. Stone DM, Stahl DC, Hanson GR, Gibb JW (1986) The effects of 3,4-methylenedioxymethamphetamine (MDMA) and 3,4-methylenedioxyamphetamine (MDA) on monoaminergic systems in the rat brain. Eur J Pharmacol 128:41-48.
46. Suliman HB, Carraway MS, Velsor LW, Day BJ, Ghio AJ, Piantadosi CA (2002) Rapid mtDNA deletion by oxidants in rat liver mitochondria after hemin exposure. Free Radic Biol Med 32:246-256.
47. Suliman HB, Carraway MS, Piantadosi CA (2003) Postlipopolysaccharide oxidative damage of mitochondrial DNA. Am J Respir Crit Care Med 167:570-579.
48. Sulzer D, Sonders MS, Poulsen NW, Galli A (2005) Mechanisms of neurotransmitter release by amphetamines: a review. Prog Neurobiol 75:406-433.