Dissociation of the neurochemical and behavioral toxicology of MDMA ('ecstasy') by citalopram

Neuropsychopharmacology

Volumn 33, Issue 5, 2008, Pages 1192-1205

  Piper, Brian J ^a,c   Fraiman, Joseph B ^a   Owens, Cullen B ^a,d   Ali, Syed F ^b   Meyer, Jerrold S ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^c UNIVERSITY OF OREGON   (United States)

^d BOSTON UNIVERSITY   (United States)

Author keywords

Behavior; Citalopram; MDMA; Neurotoxicity; Rats; Serotonin transporter

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; 5 HYDROXYINDOLEACETIC ACID; CITALOPRAM; SEROTONIN; SEROTONIN TRANSPORTER;

AGGRESSION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BODY WEIGHT; BRAIN TISSUE; COGNITION; CONTROLLED STUDY; CORE TEMPERATURE; EJACULATION; EXPERIMENTAL TEST; EXPLORATORY BEHAVIOR; HYPERTHERMIA; MALE; MOTOR ACTIVITY; NEUROTOXICITY; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; RAT; SOCIAL INTERACTION; SPRAGUE DAWLEY RAT; WEIGHT REDUCTION;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; BODY TEMPERATURE; BODY WEIGHT; BRAIN CHEMISTRY; CITALOPRAM; DOSE-RESPONSE RELATIONSHIP, DRUG; EJACULATION; EXPLORATORY BEHAVIOR; HALLUCINOGENS; INTERPERSONAL RELATIONS; MALE; MAZE LEARNING; MOTOR ACTIVITY; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; NEUROTOXICITY SYNDROMES; RATS; RATS, SPRAGUE-DAWLEY; RECOGNITION (PSYCHOLOGY); SEROTONIN UPTAKE INHIBITORS; TIME FACTORS;

EID: 40549088916     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301491     Document Type: Article

References (79)

1. Aguirre N, Ballaz S, Lasheras B, Del Rio J (1998). MDMA ('Ecstasy') enhances 5-HT1A receptor density and 8-OH-DPAT-induced hypothermia: blockade by drugs preventing 5-hydroxytryptamine depletion. Eur J Pharmacol 346: 181-188.
2. Ali SF, Newport GD, Holson RR, Slikker W, Bowyer JF (1994). Low environmental temperature or pharmacologic agents that produce hypothermia decrease methamphetamine neurotoxicity in mice. Brain Res 658: 33-38.
3. Ando RD, Benko A, Ferrington L, Kirilly E, Kelly PA, Bagdy G (2006). Partial lesion of the serotonergic system by a single dose of MDMA results in behavioural disinhibition and enhances acute MDMA-induced social behaviour on the social interaction test. Neuropharmacology 50: 884-896.
4. Battaglia G, Yeh SY, De Souza EB (1988). MDMA-induced neurotoxicity: parameters of degeneration and recovery of brain serotonin neurons. Pharmacol Biochem Behav 29: 269-274.
5. Benmansour S, Cecchi M, Morilak DA, Gerhardt GA, Javors MA, Gould GG et al (1999). Effects of chronic antidepressant treatments on serotonin transporter function, density, and mRNA level. J Neurosci 19: 10494-10501.
6. Bilsky EJ, Hubbell CL, Delconte JD, Reid LD (1991). MDMA produces a conditioned place preference and elicits ejaculation in male rats: a modulatory role for the endogenous opiates. Pharmacol Biochem Behav 40: 443-447.
7. Bronstein PM (1972). Repeated trials with the albino rat in the open field as a function of age and deprivation. J Comp Physiol Psychol 81: 84-93.
8. Cole JC, Sumnall HR (2003). The pre-clinical behavioural pharmacology of 3,4-methylenedioxymethamphetamine (MDMA). Neurosci Biobehav Rev 27: 199-217.
9. Commins DL, Vosmer G, Virus RM, Woolverton WL, Schuster CR, Seiden LS (1987). Biochemical and histological evidence that methylenedioxymethamphetamine (MDMA) is toxic to neurons in the rat brain. J Pharmacol Exp Ther 241: 338-345.
10. Cowan RL (2007). Neuroimaging research in human MDMA users: a review. Psychopharmacology 189: 539-556.
11. Curran HV, Rees H, Hoare T, Hoshi R, Bond A (2004). Empathy and aggression: two faces of ecstasy? A study of interpretative cognitive bias and mood change in ecstasy users. Psychopharmacology 173: 425-433.
12. de la Torre R, Farre M, Roset PN, Pizarro N, Abanades S, Segura M et al (2004). Human pharmacology of MDMA: pharmacokinetics, metabolism, and disposition. Ther Drug Monit 26: 137-144.
13. File SE, Hyde JR (1978). Can social interaction be used to measure anxiety? Br J Pharmacol 62: 19-24.
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 159: 437-444.
15. Frith CH, Chang LW, Lattin DL, Walls RC, Hamm J, Doblin R (1987). Toxicity of methylenedioxymethamphetamine (MDMA) in the dog and the rat. Fundam Appl Toxicol 9: 110-119.
16. García-Marquez C, Giralt M, Armario A (1987). Long-lasting effects of chronic chlorimipramine treatment of rats on exploratory activity on a hole-board, and on immobility in the forced swimming test. Eur J Pharmacol 142: 385-389.
17. Gerra G, Bassignana S, Zaimovic A, Moi G, Bussandri M, Caccavari R et al (2003). Hypothalamic-pituitary-adrenal axis responses to stress in subjects with 3,4-methylenedioxy-methamphetamine ('ecstasy') use history: correlation with dopamine receptor sensitivity. Psychiatry Res 120: 115-124.
18. Gerra G, Zaimovic A, Moi G, Giusti F, Gardini S, Delsignore R et al (2002). Effects of (±) 3,4-methylene-dioxymethamphetamine (ecstasy) on dopamine system function in humans. Behav Brain Res 134: 403-410.
19. Green AR, Mechan AO, Elliott JM, O'Shea E, Colodo MI (2003). The pharmacology and clinical pharmacology of 3,4-methylenedioxymethamphetamine (MDMA, 'ecstasy'). Pharmacol Rev 55: 463-508.
20. Green AR, O'Shea E, Colado MI (2004). A review of the mechanisms involved in the acute MDMA (ecstasy)-induced hyperthermic response. Eur J Pharmacol 500: 3-13.
21. 2C receptors. Br J Pharmacol 124: 1781-1787.
22. Gurtman CG, Morley KC, Li KM, Hunt GE, McGregor IS (2002). Increased anxiety in rats after 3,4-methylenedioxymethamphetamine: association with serotonin depletion. Eur J Pharmacol 446: 89-96.
23. Hemeryck A, Belpaire FM (2002). Selective serotonin reuptake inhibitors and cytochrome P-450 mediated drug-drug interactions: an update. Curr Drug Metab 3: 13-37.
24. Hirano K, Seki T, Sakai N, Kato Y, Hashimoto H, Uchida S et al (2005). Effects of continuous administration of paroxetine on ligand binding site and expression of serotonin transporter protein in mouse brain. Brain Res 1053: 154-161.
25. Ho YJ, Pawlak CR, Guo L, Schwarting RK (2004). Acute and long-term consequences of single MDMA administration in relation to individual anxiety levels in the rat. Behav Brain Res 149: 135-144.
26. Kankaanpaa A, Merinne E, Lillsunde P, Seppala T (1998). The acute effects of amphetamine derivatives on extracellular serotonin and dopamine levels in rat nucleus accumbens. Pharmacol Biochem Behav 59: 1003-1009.
27. Kirilly E, Benko A, Ferrington L, Ando RD, Kelly PA, Bagdy G (2005). Acute and long-term effects of a single dose of MDMA on aggression in Dark Agouti rats. Int J Neuropsychopharmacol 9: 63-76.
28. Krakowski M (2003). Violence and serotonin: influence of impulse control, affect regulation, and social functioning. J Neuropsychiatry Clin Neurosci 15: 294-305.
29. Leussis MP, Bolivar VJ (2006). Habituation in rodents: a review of behavior, neurobiology, and genetics. Neurosci Biobehav Rev 30: 1045-1064.
30. Makanjuola ROA, Hill G, Maben I, Dow RC, Ashcroft GW (1977). An automated method for studying exploratory and stereotyped behaviour in rats. Psychopharmacology 52: 271-277.
31. Malberg JE, Sabol KE, Seiden LS (1996). Co-administration of MDMA with drugs that protect against MDMA neurotoxicity produces different effects on body temperature in the rat. J Pharmacol Exp Ther 278: 258-267.
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: 99-102.
33. McCann UD, Ridenour A, Shaham Y, Ricaurte GA (1994). Serotonin neurotoxicity after (±)3,4-methylenedioxymethamphetamine (MDMA; 'Ecstasy'): a controlled study in humans. Neuropsychopharmacology 10: 129-138.
34. McCann UD, Ricaurte GA (2004). Amphetamine neurotoxicity: accomplishments and remaining challenges. Neurosci Biobehav Rev 27: 821-826.
35. McGregor IS, Clemens KJ, Van der Plasse G, Li KM, Hunt GE, Chen F et al (2003a). Increased anxiety 3 months after brief exposure to MDMA ('Ecstasy') in rats: association with altered 5-HT transporter and receptor density. Neuropsychopharmacology 28: 1472-1484.
36. McGregor IS, Gurtman CG, Morley KC, Clemens KJ, Blokland A, Li KM et al (2003b). Increased anxiety and 'depressive' symptoms months after MDMA ('ecstasy') in rats: drug-induced hyperthermia does not predict long-term outcomes. Psychopharmacology 168: 465-474.
37. Mechan AO, Moran PM, Elliott M, Young AJ, Joseph MH, Green R (2002). A study of the effect of a single neurotoxic dose of 3,4- methylenedioxymethamphetamine (MDMA; 'ecstasy') on the subsequent long-term behaviour of rats in the plus maze and open field. Psychopharmacology 159: 167-175.
38. Miczek KA, Fish EW, De Bold JF, De Almeida RM (2002). Social and neural determinants of aggressive behavior: pharmacotherapeutic targets at serotonin, dopamine and gamma-aminobutyric acid systems. Psychopharmacology 163: 434-458.
39. IA receptors. Eur J Pharmacol 193: 145-152.
40. Mogensen J, Wörtwein G, Plenge P, Mellerup ET (2003). Serotonin, locomotion, exploration, and place recall in the rat. Pharmacol Biochem Behav 75: 381-395.
41. Morley KC, Gallate JE, Hunt GE, Mallet PE, McGregor IS (2001). Increased anxiety and impaired memory in rats 3 months after administration of 3,4-methylenedioxymethamphetamine ('ecstasy'). Eur J Pharmacol 433: 91-99.
42. Morley KC, Li KM, Hunt GE, Mallet PE, McGregor IS (2004). Cannabinoids prevent the acute hyperthermia and partially protect against the 5-HT depleting effects of MDMA ('Ecstasy') in rats. Neuropharmacology 46: 954-965.
43. Morley KC, McGregor IS (2000). (±)-3,4- methylenedioxymethamphetamine (MDMA, 'Ecstasy') increases social interaction in rats. Eur J Pharmacol 408: 41-49.
44. National Research Council (1996). Guide for the Care and Use of Laboratory Animals. National Academy Press: Washington, DC.
45. O'Callaghan JP, Miller DB (1993). Quantification of reactive gliosis as an approach to neurotoxicity assessment. NIDA Res Monogr 136: 188-212.
46. 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.
47. Parrott AC (2001). Human psychopharmacology of ecstasy (MDMA): a review of 15 years of empirical research. Hum Psychopharmacol 16: 557-577.
48. Parrott AC (2002). Recreational Ecstasy/MDMA, the serotonin syndrome, and serotonergic neurotoxicity. Pharmacol Biochem Behav 71: 837-844.
49. Paulson PE, Camp DM, Robinson TE (1991). Time course of transient behavioral depression and persistent behavioral sensitization in relation to regional brain monoamine concentrations during amphetamine withdrawal in rats. Psychopharmacology 103: 480-492.
50. Piper BJ, Fraiman JS, 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.
51. Piper B, Kim P, Daniels L, Betts C, Biezonski D, Shinday N et al (2006). Repeated intermittent methylenedioxymethamphetamine (MDMA or 'ecstasy') exposure blocks the behavioral and neurotoxic, but not hyperthermic, actions of an MDMA binge in adult male rats. Soc Neurosci, abstract #478.12.
52. Piper BJ, Meyer JS (2004). Memory deficit and reduced anxiety in young adult rats given repeated intermittent MDMA treatment during the periadolescent period. Pharmacol Biochem Behav 79: 723-731.
53. 1A receptor agonist. J Pharmacol Exp Ther 317: 838-849.
54. Prutt L, Belzung C (2003). The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463: 3-33.
55. Renfrew JW (1996). Aggression and its Causes: A Biopsychosocial Approach. Oxford University Press: New York.
56. Ricaurte GA, Martello AL, Katz JL, Martello MB (1992). Lasting effects of (±)-3,4-methylenedioxymethamphetamine (MDMA) on central serotonergic neurons in nonhuman primates: neurochemical observations. J Pharmacol Exp Ther 261: 616-622.
57. Rosen RC, Lane RM, Menza M (1999). Effects of SSRIs on sexual function: a critical review. J Clin Psychopharmacol 19: 67-85.
58. Sánchez C, Bergqvist PBF, Brennum LT, Gupta S, Hogg S, Larsen A et al (2003). Escitalopram, the S-(+)-enantiomer of citalopram, is a selective serotonin reuptake inhibitor with potent effects in animal models predictive of antidepressant and anxiolytic activities. Psychopharmacology 167: 353-362.
59. 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: 46-57.
60. Sara SJ, Dyon-Laurent C, Hervé A (1995). Novelty seeking behavior in the rat is dependent upon the integrity of the noradrenergic system. Cogn Brain Res 2: 181-187.
61. Schmidt CJ (1987). Neurotoxicity of the psychedelic amphetamine, methylenedioxymethamphetamine. J Pharmacol Exp Ther 240: 1-7.
62. Schmued LC (2003). Demonstration and localization of neuronal degeneration in the rat forebrain following a single exposure to MDMA. Brain Res 974: 127-133.
63. Schmued LC, Hopkins KJ (2000). Fluoro-Jade: novel fluorochromes for detecting toxicant-induced neuronal degeneration. Toxicol Pathol 28: 91-99.
64. Shumaker RC (1986). PKCALC: a BASIC interactive computer program for statistical and pharmacokinetic analysis of data. Drug Metab Rev 17: 331-348.
65. Sprague JE, Preston AS, Leifheit M, Woodside B (2003). Hippocampal serotonergic damage induced by MDMA (ecstasy): effects on spatial learning. Physiol Behav 79: 281-287.
66. Sumnall HR, O'Shea E, Marsden CA, Cole JC (2004). The effects of MDMA pretreatment on the behavioural effects of other drugs of abuse in the rat elevated plus-maze test. Pharmacol Biochem Behav 77: 805-814.
67. Thompson MR, Li KM, Clemens KJ, Gurtman CG, Hunt GE, Cornish JL et al (2004). Chronic fluoxetine treatment partly attenuates the long-term anxiety and depressive symptoms induced by MDMA ('Ecstasy') in rats. Neuropsychopharmacology 29: 694-704.
68. Timár J, Gyarmati S, Szabo A, Furst S (2003). Behavioural changes in rats treated with a neurotoxic dose regimen of dextrorotatory amphetamine derivatives. Behav Pharmacol 14: 199-206.
69. Traub SJ, Hoffman RS, Nelson LS (2002). The 'ecstasy' hangover: hyponatremia due to 3,4-methylenedioxymethamphetamine. J Urban Health 79: 549-555.
70. Verheyden SL, Hadfield J, Calin T, Curran HV (2002). Sub-acute effects of MDMA (+/-3,4-methylenedioxymethamphetamine, 'ecstasy') on mood: evidence of gender differences. Psychopharmacology 161: 23-31.
71. Wallace TL, Gudelsky GA, Vorhees CV (2001). Alterations in diurnal and nocturnal locomotor activity in rats treated with monoamine-depleting regimen of methamphetamine or 3,4-methylenedioxymethamphetamine. Psychopharmacology 153: 321-326.
72. 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: 1002-1012.
73. 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: 240-248.
74. White W, Feldon J, White IM (2004). Development of acute withdrawal during periodic administration of amphetamine in rats. Pharmacol Biochem Behav 79: 55-63.
75. White W, White IM (2006). An activity indicator of acute withdrawal depends on amphetamine dose in rats. Physiol Behav 87: 368-376.
76. Wilson MA, Mamounas LA, Fasman KH, Axt KJ, Molliver ME (1993). Reactions of 5-HT neurons to drugs of abuse: neurotoxicity and plasticity. NIDA Res Monogr 136: 155-178.
77. 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. Mol Brain Res 25: 34-40.
78. Xie T, Tong L, McLane MW, Hatzidimitriou G, Yuan J, McCann U et al (2006). Loss of serotonin transporter protein after MDMA and other ring-substituted amphetamines. Neuropsychopharmacology 31: 2639-2651.
79. Yonezawa A, Yoshizumi M, Ebiko M, Iwanaga T, Kimura Y, Sakurada S (2005). Evidence for an involvement of peripheral serotonin in p-chloroamphetamine-induced ejaculation of rats. Pharmacol Biochem Behav 82: 744-750.