3,4-methylenedioxymethamphetamine induces gene expression changes in rats related to serotonergic and dopaminergic systems, but not to neurotoxicity

Neurotoxicity Research

Volumn 25, Issue 2, 2014, Pages 161-169

  Cuyas, Elisabet ^a   Robledo, Patricia ^a,b   Pizarro, Nieves ^a   Farré, Magí ^a   Puerta, Elena ^c   Aguirre, Norberto ^c   De La Torre, Rafael ^a,b,d  

^a Barcelona Biomedical Research Park   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c UNIVERSITY OF NAVARRA   (Spain)

^d CIBEROBN   (Spain)

Author keywords

Dopamine; Ecstasy; MDMA; PCR; Serotonin; Serotonin transporter

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; ALPHA SYNUCLEIN; AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; GLIAL FIBRILLARY ACIDIC PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 70 1A; SEROTONIN; SEROTONIN TRANSPORTER; TRYPTOPHAN HYDROXYLASE 2; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; VESICULAR MONOAMINE TRANSPORTER 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN STEM; CONTROLLED STUDY; CORPUS STRIATUM; CYTOTOXICITY; DOPAMINERGIC SYSTEM; DRUG DOSE REGIMEN; GENE EXPRESSION; HIPPOCAMPUS; MALE; MAOB GENE; NEUROTOXICITY; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAT; SEROTONINERGIC SYSTEM; SLC18A2 GENE; SLC6A4 GENE; TPH2GENE;

RATTUS;

ANIMALS; BRAIN; DOPAMINE AGENTS; GENE EXPRESSION; MALE; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; RATS; RATS, WISTAR; SEROTONIN AGENTS;

EID: 84891864500     PISSN: 10298428     EISSN: 14763524     Source Type: Journal    
DOI: 10.1007/s12640-013-9416-1     Document Type: Article

References (57)

1. Able JA, Gudelsky GA, Vorhees CV, Williams MT (2006) 3,4- Methylenedioxymethamphetamine in adult rats produces deficits in path integration and spatial reference memory. Biol Psychiatry 59(12):1219-1226
2. Adori C, Andó RD, Kovács GG, Bagdy G (2006) Damage of serotonergic axons and immunolocalization of Hsp27, Hsp72, and Hsp90 molecular chaperones after a single dose of MDMA administration in Dark Agouti rat: temporal, spatial, and cellular patterns. J Comp Neurol 497(2):251-269 (Pubitemid 43825430)
3. Aguirre N, Barrionuevo M, Ramírez MJ, Del Río J, Lasheras B (1999) Alpha-lipoic acid prevents 3,4-methylenedioxy-methamphetamine (MDMA)-induced neurotoxicity. Neuroreport 10(17):3675-3680
4. Alves E, Summavielle T, Alves CJ, Gomes-da-Silva J, Barata JC, Fernandes E, Bastos ML, Tavares MA, Carvalho F (2007) Monoamine oxidase-B mediates ecstasy-induced neurotoxic effects to adolescent rat brain mitochondria. J Neurosci 27(38):10203-10210 (Pubitemid 47450472)
5. Alves E, Binienda Z, Carvalho F, Alves CJ, Fernandes E, de Lourdes BM, Tavares MA, Summavielle T (2009) Acetyl-l-carnitine provides effective in vivo neuroprotection over 3,4-methylenedioximethamphetamine-induced mitochondrial neurotoxicity in the adolescent rat brain. Neuroscience 158(2):514-523
6. Baumann MH, Wang X, Rothman RB (2007) 3,4-Methylenedioxymethamphetamine (MDMA) neurotoxicity in rats: a reappraisal of past and present findings. Psychopharmacology 189(4):407-424 (Pubitemid 44791212)
7. Biezonski DK, Meyer JS (2010) Effects of 3,4- methylenedioxymethamphetamine (MDMA) on serotonin transporter and vesicular monoamine transporter 2 protein and gene expression in rats: implications for MDMA neurotoxicity. J Neurochem 112(4):951-962
8. Biezonski DK, Meyer JS (2011) The nature of 3,4- methylenedioxymethamphetamine (MDMA)-induced serotonergic dysfunction: evidence for and against the neurodegeneration hypothesis. Curr Neuropharmacol 9(1):84-90
9. Bonkale WL, Austin MC (2008) 3,4-Methylenedioxymethamphetamine induces differential regulation of tryptophan hydroxylase 2 protein and mRNA levels in the rat dorsal raphe nucleus. Neuroscience 155(1):270-276
10. Bonvento G, Lacombe P, MacKenzie ET, Fage D, Benavides J, Rouquier L, Scatton B (1991) Evidence for differing origins of the serotonergic innervations of major cerebral arteries and small pial vessels in the rat. J Neurochem 56(2):681-689 (Pubitemid 21902014)
11. Breier JM, Bankson MG, Yamamoto BK (2006) l-Tyrosine contributes to (+)-3,4-methylenedioxymethamphetamine-induced serotonin depletions. J Neurosci 26(1):290-299 (Pubitemid 43089542)
12. Capela JP, Carmo H, Remiao F, Bastos ML, Meisel A, Carvalho F (2009) Molecular and cellular mechanisms of ecstasy-induced neurotoxicity: an overview. Mol Neurobiol 39(3):210-271
13. Colado MI, O'Shea E, Green AR (2004) Acute and long-term effects of MDMA on cerebral dopamine biochemistry and function. Psychopharmacology 173(3-4):249-263 (Pubitemid 38703798)
14. 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(1):338-345 (Pubitemid 17119380)
15. Cuyàs E, Verdejo-García A, Fagundo AB, Khymenets O, Rodríguez J, Cuenca A, de Sola Llopis S, Langohr K, Peña-Casanova J, Torrens M, Martín-Santos R, Farré M, de la Torre R (2011) The influence of genetic and environmental factors among MDMA users in cognitive performance. PLoS ONE 6(11):e27206
16. de Sola Llopis S, Miguelez-Pan M, Peña-Casanova J, Poudevida S, Farré M, Pacifici R, Böhm P, Abanades S, VerdejoGarcía A, Langohr K, Zuccaro P, de la Torre R (2008) Cognitive performance in recreational ecstasy polydrug users: a two-year follow-up study. J Psychopharmacol 22(5):498-510
17. Di Iorio CR, Watkins TJ, Dietrich MS, Cao A, Blackford JU, Rogers B, Ansari MS, Baldwin RM, Li R, Kessler RM, Salomon RM, Benningfield M, Cowan RL (2012) Evidence for chronically altered serotonin function in the cerebral cortex of female 3,4-methylenedioxymethamphetamine polydrug users. Arch Gen Psychiatry 69:399-409
18. Fitzgerald JL, Reid JJ (1990) Effects of methylenedioxymethamphetamine on the release of monoamines from rat brain slices. Eur J Pharmacol 191(2):217-220
19. Fornai F, Lenzi P, Ferrucci M, Lazzeri G, di Poggio AB, Natale G, Busceti CL, Biagioni F, Giusiani M, Ruggieri S, Paparelli A (2005) Occurrence of neuronal inclusions combined with increased nigral expression of alpha-synuclein within dopaminergic neurons following treatment with amphetamine derivatives in mice. Brain Res Bull 65(5):405-413
20. Goni-Allo B, Mathuna O, Segura M, Puerta E, Lasheras B, de la Torre R, Aguirre N (2008) The relationship between core body temperature and 3,4-methylenedioxymethamphetamine metabolism in rats: implications for neurotoxicity. Psychopharmacology 197(2):263-278
21. 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(3):463-508 (Pubitemid 37013213)
22. 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(1):56-59 (Pubitemid 39078784)
23. Johnson MP, Hoffman AJ, Nichols DE (1986) Effects of the enantiomers ofMDA, MDMA and related analogues on [3H]serotonin and [3H]dopamine release from superfused rat brain slices. Eur J Pharmacol 132(2-3):269-276 (Pubitemid 17003469)
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(1):298-306 (Pubitemid 39287809)
25. Kindlundh-Hogberg AM, Svenningsson P, Schiöth HB (2006) Quantitative mapping shows that serotonin rather than dopamine receptor mRNA expressions are affected after repeated intermittent administration of MDMA in rat brain. Neuropharmacology 51(4):838-847 (Pubitemid 44286936)
26. Kirilly E, Molnar E, Balogh B, Kantor S, Hansson SR, Palkovits M, Bagdy G (2008) Decrease in REM latency and changes in sleep quality parallel serotonergic damage and recovery after MDMA: a longitudinal study over 180 days. Int J Neuropsychopharmacol 11(6):795-809
27. Kish SJ, Furukawa Y, Ang L, Vorce SP, Kalasinsky KS (2000) Striatal serotonin is depleted in brain of a human MDMA (Ecstasy) user. Neurology 55(2):294-296 (Pubitemid 30604635)
28. Kovacs GG, Ando RD, Adori C, Kirilly E, Benedek A, Palkovits M, Bagdy G (2007) Single dose of MDMA causes extensive decrement of serotoninergic fibre density without blockage of the fast axonal transport in Dark Agouti rat brain and spinal cord. Neuropathol Appl Neurobiol 33(2):193-203 (Pubitemid 46385713)
29. Li IH, Huang WS, Shiue CY, Huang YY, Liu RS, Chyueh SC, Hu SH, Shen LH, Liao MH, Liu JC, Ma KH (2010) Study on the neuroprotective effect of fluoxetine against MDMA-induced neurotoxicity on the serotonin transporter in rat brain using micro-PET. Neuroimage 49(2):1259-1270
30. Lindvall O, Björklund A, Moore RY, Stenevi U (1974) Mesencephalic dopamine neurons projecting to neocortex. Brain Res 81(2):325-331
31. Martín-Santos R, Torrens M, Poudevida S, Langohr K, Cuyàs E, Pacifici R, Farre M, Pichini S, de la Torre R (2010) 5-HTTLPR polymorphism, mood disorders and MDMA use in a 3-year follow-up study. Addict Biol 15(1):15-22
32. Mayerhofer A, Kovar KA, Schmidt WJ (2001) Changes in serotonin, dopamine and noradrenaline levels in striatum and nucleus accumbens after repeated administration of the abused drug MDMA in rats. Neurosci Lett 308(2):99-102 (Pubitemid 32703677)
33. McGregor IS, Gurtman CG, Morley KC, Clemens KJ, Blokland A, Li KM, Cornish JL, Hunt GE (2003) Increased anxiety and "depressive" symptoms months after MDMA ("ecstasy") in rats: drug-induced hyperthermia does not predict long-term outcomes. Psychopharmacology 168(4):465-474 (Pubitemid 36994030)
34. Mladenovic A, Perovic M, Tanic N, Petanceska S, Ruzdijic S, Kanazir S (2007) Dietary restriction modulates alpha-synuclein expression in the aging rat cortex and hippocampus. Synapse 61(9):790-794 (Pubitemid 47122753)
35. Monks TJ, Jones DC, Bai F, Lau SS (2004) The role of metabolism in 3,4-(+)-methylenedioxyamphetamine and 3,4-(+)-methylenedioxymethamphetamine (ecstasy) toxicity. Ther Drug Monit 26(2):132-136 (Pubitemid 38501206)
36. Nichols DE, Lloyd DH, Hoffman AJ, Nichols MB, Yim GK (1982) Effects of certain hallucinogenic amphetamine analogues on the release of [3H]serotonin from rat brain synaptosomes. J Med Chem 25(3):530-535 (Pubitemid 12051977)
37. O'Callaghan JP, Miller DB (1993) The interactions of MK-801 with the amphetamine analogues d-methamphetamine (d-METH), 3,4- methylenedioxymethamphetamine (ds-MDMA) or d-fenfluramine (d-FEN): neural damage and neural protection. Ann N Y Acad Sci 679:321-324 (Pubitemid 23202425)
38. O'Loinsigh ED, Boland G, Kelly JP, O'Boyle KM (2001) Behavioural, hyperthermic and neurotoxic effects of 3,4-methylenedioxymethamphetamine analogues in the Wistar rat. Prog Neuropsychopharmacol Biol Psychiatry 25(3):621-638 (Pubitemid 32391542)
39. Pubill D, Canudas AM, Pallàs M, Camins A, Camarasa J, Escubedo E (2003) Different glial response to methamphetamine- and methylenedioxymethamphetamine-induced neurotoxicity. Naunyn Schmiedebergs Arch Pharmacol 367(5):490-499 (Pubitemid 36718300)
40. Puerta E, Aguirre N (2011) Methylenedioxymethamphetamine (MDMA, 'Ecstasy'): neurodegeneration versus neuromodulation. Pharmaceuticals 4:992-1018
41. Purves D (2004) Neurotransmitters, receptors, and their effects. In: Purves D (ed) Neuroscience. Sinauer Associates, Sunderland, pp 129-165
42. Reneman L, Endert E, de Bruin K, Lavalaye J, Feenstra MG, de Wolff FA, Booij J (2002) The acute and chronic effects of MDMA ("ecstasy") on cortical 5-HT2A receptors in rat and human brain. Neuropsychopharmacology 26:387-396 (Pubitemid 34159216)
43. 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(1):51-55
44. Ricaurte GA, Yuan J, McCann UD (2000) (±)3,4- Methylenedioxymethamphetamine ('Ecstasy')-induced serotonin neurotoxicity: studies in animals. Neuropsychobiology 42(1):5-10 (Pubitemid 30436310)
45. Sanchez V, Camarero J, Esteban B, Peter MJ, Green AR, Colado MI (2001) The mechanisms involved in the long-lasting neuroprotective effect of fluoxetine against MDMA ('ecstasy')-induced degeneration of 5-HT nerve endings in rat brain. Br J Pharmacol 134(1):46-57 (Pubitemid 32835467)
46. Schmidt CJ, Taylor VL (1987) Depression of rat brain tryptophan hydroxylase activity following the acute administration of methylenedioxymethamphetamine. Biochem Pharmacol 36(23):4095-4102 (Pubitemid 18010965)
47. Shankaran M, Yamamoto BK, Gudelsky GA (1999) Mazindol attenuates the 3,4-methylenedioxymethamphetamine-induced formation of hydroxyl radicals and long-term depletion of serotonin in the striatum. J Neurochem 72:2516-2522 (Pubitemid 29242203)
48. Sharma HS, Ali SF (2008) Acute administration of 3,4- methylenedioxymethamphetamine induces profound hyperthermia, blood-brain barrier disruption, brain edema formation, and cell injury. Ann N Y Acad Sci 1139:242-258
49. Sprague JE, Everman SL, Nichols DE (1998) An integrated hypothesis for the serotonergic axonal loss induced by 3,4-methylenedioxymethamphetamine. Neurotoxicology 19(3):427-441
50. Stone DM, Johnson M, Hanson GR, Gibb JW (1988) Role of endogenous dopamine in the central serotonergic deficits induced by 3,4- methylenedioxymethamphetamine. J Pharmacol Exp Ther 247:79-87
51. Stone DM, Johnson M, Hanson GR, Gibb JW (1989) Acute inactivation of tryptophan hydroxylase by amphetamine analogs involves the oxidation of sulfhydryl sites. Eur J Pharmacol 172(7):93-97 (Pubitemid 19230188)
52. Wang X, Baumann MH, Xu H, Rothman RB (2004) 3,4- Methylenedioxymethamphetamine (MDMA) administration to rats decreases brain tissue serotonin but not serotonin transporter protein and glial fibrillary acidic protein. Synapse 53(4):240-248 (Pubitemid 39045543)
53. Wang X, Baumann MH, Xu H, Morales M, Rothman RB (2005) (±)-3,4-Methylenedioxymethamphetamine administration to rats does not decrease levels of the serotonin transporter protein or alter its distribution between endosomes and the plasma membrane. J Pharmacol Exp Ther 314(5):1002-1012 (Pubitemid 41205963)
54. Wersinger C, Sidhu A (2009) Partial regulation of serotonin transporter function by gamma-synuclein. Neurosci Lett 453(3):157-161
55. Wersinger C, Rusnak M, Sidhu A (2006) Modulation of the trafficking of the human serotonin transporter by human alpha-synuclein. Eur J Neurosci 24(1):55-64 (Pubitemid 44050666)
56. Wotherspoon G, Savery D, Priestley JV, Rattray M (1994) Repeated administration of MDMA down-regulates preprocholecystokinin mRNA expression but not tyrosine hydroxylase mRNA expression in neurones of the rat substantia nigra. Brain Res Mol Brain Res 25(1-2):34-40 (Pubitemid 24223260)
57. Xie T, Tong L, McLane MW, Hatzidimitriou G, Yuan J, McCann U, Ricaurte G (2006) Loss of serotonin transporter protein after MDMA and other ring-substituted amphetamines. Neuropsychopharmacology 31(12):2639-2651 Erratum in: Neuropsychopharmacology. 2008 Feb;33(3):712-713 (Pubitemid 44764161)