Tolerance to 3,4-methylenedioxymethamphetamine in rats exposed to single high-dose binges

Neuroscience

Volumn 152, Issue 3, 2008, Pages 773-784

  Baumann, M H ^a   Clark, R D ^b   Franken, F H ^c   Rutter, J J ^d   Rothman, R B ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b Uniformed Services University of the Health Sciences and the Walter Reed National Military Medical Center   (United States)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d TRUMAN STATE UNIVERSITY   (United States)

Author keywords

5 HT; dopamine; ecstasy; microdialysis; neuroendocrine; transporter

Indexed keywords

3,4 METHYLENEDIOXYAMPHETAMINE; CORTICOSTERONE; MONOAMINE; PROLACTIN; SEROTONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR CHANGE; BLOOD SAMPLING; CONTROLLED STUDY; CORE TEMPERATURE; DIALYSATE; DOPAMINE RELEASE; DRUG EFFECT; DRUG TOLERANCE; FOREBRAIN; HORMONE RELEASE; HYPERTHERMIA; MALE; MICRODIALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN SECRETION; RAT;

ANIMALS; BODY TEMPERATURE; BRAIN; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; DRUG ADMINISTRATION SCHEDULE; DRUG TOLERANCE; EXTRACELLULAR FLUID; FEVER; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; INFUSIONS, INTRAVENOUS; INFUSIONS, PARENTERAL; MALE; MICRODIALYSIS; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN; SEROTONIN AGENTS; SYNAPTIC TRANSMISSION;

EID: 41049096536     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.01.007     Document Type: Article

References (69)

1. Ball K.T., Budreau D., and Rebec G.V. Acute effects of 3,4-methylenedioxymethamphetamine on striatal single-unit activity and behavior in freely moving rats: differential involvement of dopamine D(1) and D(2) receptors. Brain Res 994 (2003) 203-215
2. Bankson M.G., and Cunningham K.A. 3,4-Methylenedioxymethamphetamine (MDMA) as a unique model of serotonin receptor function and serotonin-dopamine interactions. J Pharmacol Exp Ther 297 (2001) 846-852
3. Battaglia G., Yeh S.Y., O'Hearn E., Molliver M.E., Kuhar M.J., and De Souza E.B. 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 (1987) 911-916
4. Baumann M.H., Ayestas M.A., and Rothman R.B. Functional consequences of central serotonin depletion produced by repeated fenfluramine administration in rats. J Neurosci 18 (1998) 9069-9077
5. Baumann M.H., Clark R.D., Budzynski A.G., Partilla J.S., Blough B.E., and Rothman R.B. N-substituted piperazines abused by humans mimic the molecular mechanism of 3,4-methylenedioxymethamphetamine (MDMA, or "ecstasy"). Neuropsychopharmacology 30 (2005) 550-560
6. Baumann M.H., Wang X., and Rothman R.B. 3,4-Methylenedioxymethamphetamine (MDMA) neurotoxicity in rats: a reappraisal of past and present findings. Psychopharmacology (Berl) 189 (2007) 407-424
7. Brennan K.A., and Schenk S. Initial deficit and recovery of function after MDMA preexposure in rats. Psychopharmacology (Berl) 184 (2006) 239-246
8. Broening H.W., Bowyer J.F., and Slikker Jr. W. Age-dependent sensitivity of rats to the long-term effects of the serotonergic neurotoxicant (+/-)-3,4-methylenedioxymethamphetamine (MDMA) correlates with the magnitude of the MDMA-induced thermal response. J Pharmacol Exp Ther 275 (1995) 325-333
9. Callaway C.W., and Geyer M.A. Tolerance and cross-tolerance to the activating effects of 3,4-methylenedioxymethamphetamine and a 5-hydroxytryptamine1B agonist. J Pharmacol Exp Ther 263 (1992) 318-326
10. Callaway C.W., Johnson M.P., Gold L.H., Nichols D.E., and Geyer M.A. Amphetamine derivatives induce locomotor hyperactivity by acting as indirect serotonin agonists. Psychopharmacology (Berl) 104 (1991) 293-301
11. Cami J., Farre M., Mas M., Roset P.N., Poudevida S., Mas A., San L., and de la Torre R. Human pharmacology of 3,4-methylenedioxymethamphetamine ("ecstasy"): psychomotor performance and subjective effects. J Clin Psychopharmacol 20 (2000) 455-466
12. Cole J.C., Bailey M., Sumnall H.R., Wagstaff G.F., and King L.A. The content of ecstasy tablets: implications for the study of their long-term effects. Addiction 97 (2002) 1531-1536
13. Commins D.L., Vosmer G., Virus R.M., Woolverton W.L., Schuster C.R., and Seiden L.S. Biochemical and histological evidence that methylenedioxymethylamphetamine (MDMA) is toxic to neurons in the rat brain. J Pharmacol Exp Ther 241 (1987) 338-345
14. Dafters R.I. Hyperthermia following MDMA administration in rats: effects of ambient temperature, water consumption, and chronic dosing. Physiol Behav 58 (1995) 877-882
15. de la Torre R., and Farre M. Neurotoxicity of MDMA (ecstasy): the limitations of scaling from animals to humans. Trends Pharmacol Sci 25 (2004) 505-508
16. Easton N., and Marsden C.A. Ecstasy: are animal data consistent between species and can they translate to humans?. J Psychopharmacol 20 (2006) 194-210
17. Fantegrossi W.E. Reinforcing effects of methylenedioxy amphetamine congeners in rhesus monkeys: are intravenous self-administration experiments relevant to MDMA neurotoxicity?. Psychopharmacology (Berl) 189 (2007) 471-482
18. Fantegrossi W.E., Woolverton W.L., Kilbourn M., Sherman P., Yuan J., Hatzidimitriou G., Ricaurte G.A., Woods J.H., and Winger G. Behavioral and neurochemical consequences of long-term intravenous self-administration of MDMA and its enantiomers by rhesus monkeys. Neuropsychopharmacology 29 (2004) 1270-1281
19. Farre M., de la Torre R., Mathuna B.O., Roset P.N., Peiro A.M., Torrens M., Ortuno J., Pujadas M., and Cami J. Repeated doses administration of MDMA in humans: pharmacological effects and pharmacokinetics. Psychopharmacology (Berl) 173 (2004) 364-375
20. Frederick D.L., Ali S.F., Slikker Jr. W., Gillam M.P., Allen R.R., and Paule M.G. Behavioral and neurochemical effects of chronic methylenedioxymethamphetamine (MDMA) treatment in rhesus monkeys. Neurotoxicol Teratol 17 (1995) 531-543
21. Frederick D.L., and Paule M.G. Effects of MDMA on complex brain function in laboratory animals. Neurosci Biobehav Rev 21 (1997) 67-78
22. Gartside S.E., McQuade R., and Sharp T. Effects of repeated administration of 3,4-methylenedioxymethamphetamine on 5-hydroxytryptamine neuronal activity and release in the rat brain in vivo. J Pharmacol Exp Ther 279 (1996) 277-283
23. Gerra G., Zaimovic A., Ferri M., Zambelli U., Timpano M., Neri E., Marzocchi G.F., Delsignore R., and Brambilla F. Long-lasting effects of (+/-)3,4-methylenedioxymethamphetamine (ecstasy) on serotonin system function in humans. Biol Psychiatry 47 (2000) 127-136
24. Gerra G., Zaimovic A., Giucastro G., Maestri D., Monica C., Sartori R., Caccavari R., and Delsignore R. Serotonergic function after (+/-)3,4-methylene-dioxymethamphetamine ("ecstasy") in humans. Int Clin Psychopharmacol 13 (1998) 1-9
25. Giorgi F.S., Pizzanelli C., Ferrucci M., Lazzeri G., Faetti M., Giusiani M., Pontarelli F., Busceti C.L., Murri L., and Fornai F. Previous exposure to (+/-) 3,4-methylenedioxymethamphetamine produces long-lasting alteration in limbic brain excitability measured by electroencephalogram spectrum analysis, brain metabolism and seizure susceptibility. Neuroscience 136 (2005) 43-53
26. Glennon R.A., and Higgs R. Investigation of MDMA-related agents in rats trained to discriminate MDMA from saline. Pharmacol Biochem Behav 43 (1992) 759-763
27. Gold L.H., Koob G.F., and Geyer M.A. Stimulant and hallucinogenic behavioral profiles of 3,4-methylenedioxymethamphetamine and N-ethyl-3,4-methylenedioxyamphetamine in rats. J Pharmacol Exp Ther 247 (1988) 547-555
28. Goodwin A.K., Pynnonen D.M., and Baker L.E. Serotonergic-dopaminergic mediation of MDMA's discriminative stimulus effects in a three-choice discrimination. Pharmacol Biochem Behav 74 (2003) 987-995
29. Gough B., Imam S.Z., Blough B., Slikker Jr. W., and Ali S.F. Comparative effects of substituted amphetamines (PMA, MDMA, and METH) on monoamines in rat caudate: a microdialysis study. Ann N Y Acad Sci 965 (2002) 410-420
30. Green A.R., Mechan A.O., Elliott J.M., O'Shea E., and Colado M.I. The pharmacology and clinical pharmacology of 3,4-methylenedioxymethamphetamine (MDMA, "ecstasy"). Pharmacol Rev 55 (2003) 463-508
31. Gudelsky G.A., and Nash J.F. Carrier-mediated release of serotonin by 3,4-methylenedioxymethamphetamine: implications for serotonin-dopamine interactions. J Neurochem 66 (1996) 243-249
32. Hall F.S., Devries A.C., Fong G.W., Huang S., and Pert A. Effects of 5,7-dihydroxytryptamine depletion of tissue serotonin levels on extracellular serotonin in the striatum assessed with in vivo microdialysis: relationship to behavior. Synapse 33 (1999) 16-25
33. Harris D.S., Baggott M., Mendelson J.H., Mendelson J.E., and Jones R.T. Subjective and hormonal effects of 3,4-methylenedioxymethamphetamine (MDMA) in humans. Psychopharmacology (Berl) 162 (2002) 396-405
34. Ikemoto S., and Panksepp J. The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev 31 (1999) 6-41
35. Johanson C.E., Kilbey M., Gatchalian K., and Tancer M. Discriminative stimulus effects of 3,4-methylenedioxymethamphetamine (MDMA) in humans trained to discriminate among d-amphetamine, meta-chlorophenylpiperazine and placebo. Drug Alcohol Depend 81 (2006) 27-36
36. Kalivas P.W., Duffy P., and White S.R. MDMA elicits behavioral and neurochemical sensitization in rats. Neuropsychopharmacology 18 (1998) 469-479
37. Kankaanpaa A., Meririnne E., Lillsunde P., and Seppala T. The acute effects of amphetamine derivatives on extracellular serotonin and dopamine levels in rat nucleus accumbens. Pharmacol Biochem Behav 59 (1998) 1003-1009
38. Kirby L.G., Kreiss D.S., Singh A., and Lucki I. Effect of destruction of serotonin neurons on basal and fenfluramine-induced serotonin release in striatum. Synapse 20 (1995) 99-105
39. Levy A.D., Baumann M.H., and Van de Kar L.D. Monoaminergic regulation of neuroendocrine function and its modification by cocaine. Front Neuroendocrinol 15 (1994) 85-156
40. Lin J.H. Applications and limitations of interspecies scaling and in vitro extrapolation in pharmacokinetics. Drug Metab Dispos 26 (1998) 1202-1212
41. Marston H.M., Reid M.E., Lawrence J.A., Olverman H.J., and Butcher S.P. Behavioural analysis of the acute and chronic effects of MDMA treatment in the rat. Psychopharmacology (Berl) 144 (1999) 67-76
42. Mas M., Farre M., de la Torre R., Roset P.N., Ortuno J., Segura J., and Cami J. Cardiovascular and neuroendocrine effects and pharmacokinetics of 3,4-methylenedioxymethamphetamine in humans. J Pharmacol Exp Ther 290 (1999) 136-145
43. Matuszewich L., Filon M.E., Finn D.A., and Yamamoto B.K. Altered forebrain neurotransmitter responses to immobilization stress following 3,4-methylenedioxymethamphetamine. Neuroscience 110 (2002) 41-48
44. McCreary A.C., Bankson M.G., and Cunningham K.A. Pharmacological studies of the acute and chronic effects of (+)-3,4-methylenedioxymethamphetamine on locomotor activity: role of 5-hydroxytryptamine(1A) and 5-hydroxytryptamine(1B/1D) receptors. J Pharmacol Exp Ther 290 (1999) 965-973
45. Mechan A.O., Esteban B., O'Shea E., Elliott J.M., Colado M.I., and Green A.R. The pharmacology of the acute hyperthermic response that follows administration of 3,4-methylenedioxymethamphetamine (MDMA, "ecstasy") to rats. Br J Pharmacol 135 (2002) 170-180
46. Nash Jr. J.F., Meltzer H.Y., and Gudelsky G.A. Elevation of serum prolactin and corticosterone concentrations in the rat after the administration of 3,4-methylenedioxymethamphetamine. J Pharmacol Exp Ther 245 (1988) 873-879
47. Nash Jr. J.F., Meltzer H.Y., and Gudelsky G.A. Neuroendocrinological effects of MDMA in the rat. In: Peroutka S.J. (Ed). Ecstasy: The clinical, pharmacological and neurotoxicological effects of the drug MDMA (1990), Kluwer Academic, Boston 225-239
48. O'Shea E., Granados R., Esteban B., Colado M.I., and Green A.R. The relationship between the degree of neurodegeneration of rat brain 5-HT nerve terminals and the dose and frequency of administration of MDMA ("ecstasy"). Neuropharmacology 37 (1998) 919-926
49. Parrott A.C. Chronic tolerance to recreational MDMA (3,4-methylenedioxymethamphetamine) or ecstasy. J Psychopharmacol 19 (2005) 71-83
50. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (2005), Elsevier, New York
51. Piper B.J., Vu H.L., Safain M.G., Oliver A.J., and Meyer J.S. Repeated adolescent 3,4-methylenedioxymethamphetamine (MDMA) exposure in rats attenuates the effects of a subsequent challenge with MDMA or a 5-hydroxytryptamine(1A) receptor agonist. J Pharmacol Exp Ther 317 (2006) 838-849
52. Poland R.E., Lutchmansingh P., McCracken J.T., Zhao J.P., Brammer G.L., Grob C.S., Boone K.B., and Pechnick R.N. Abnormal ACTH and prolactin responses to fenfluramine in rats exposed to single and multiple doses of MDMA. Psychopharmacology (Berl) 131 (1997) 411-419
53. Ricaurte G.A., Yuan J., and McCann U.D. (+/-)3,4-Methylenedioxymethamphetamine ("ecstasy")-induced serotonin neurotoxicity: studies in animals. Neuropsychobiology 42 (2000) 5-10
54. Rothman R.B., and Baumann M.H. Therapeutic and adverse actions of serotonin transporter substrates. Pharmacol Ther 95 (2002) 73-88
55. Schechter M.D. Serotonergic-dopaminergic mediation of 3,4-methylenedioxymethamphetamine (MDMA, "ecstasy"). Pharmacol Biochem Behav 31 (1988) 817-824
56. Schechter M.D. Effect of MDMA neurotoxicity upon its conditioned place preference and discrimination. Pharmacol Biochem Behav 38 (1991) 539-544
57. Schifano F., Corkery J., Deluca P., Oyefeso A., and Ghodse A.H. Ecstasy (MDMA, MDA, MDEA, MBDB) consumption, seizures, related offences, prices, dosage levels and deaths in the UK (1994-2003). J Psychopharmacol 20 (2006) 456-463
58. Series H.G., Cowen P.J., and Sharp T. p-Chloroamphetamine (PCA), 3,4-methylenedioxy-methamphetamine (MDMA) and d-fenfluramine pretreatment attenuates d-fenfluramine-evoked release of 5-HT in vivo. Psychopharmacology (Berl) 116 (1994) 508-514
59. Shankaran M., and Gudelsky G.A. A neurotoxic regimen of MDMA suppresses behavioral, thermal and neurochemical responses to subsequent MDMA administration. Psychopharmacology (Berl) 147 (1999) 66-72
60. Slikker Jr. W., Holson R.R., Ali S.F., Kolta M.G., Paule M.G., Scallet A.C., McMillan D.E., Bailey J.R., Hong J.S., and Scalzo F.M. Behavioral and neurochemical effects of orally administered MDMA in the rodent and nonhuman primate. Neurotoxicology 10 (1989) 529-542
61. Spanos L.J., and Yamamoto B.K. Acute and subchronic effects of methylenedioxymethamphetamine [(+/-)MDMA] on locomotion and serotonin syndrome behavior in the rat. Pharmacol Biochem Behav 32 (1989) 835-840
62. Stone D.M., Merchant K.M., Hanson G.R., and Gibb J.W. Immediate and long-term effects of 3,4-methylenedioxymethamphetamine on serotonin pathways in brain of rat. Neuropharmacology 26 (1987) 1677-1683
63. Verheyden S.L., Henry J.A., and Curran H.V. Acute, sub-acute and long-term subjective consequences of "ecstasy" (MDMA) consumption in 430 regular users. Hum Psychopharmacol 18 (2003) 507-517
64. Verkes R.J., Gijsman H.J., Pieters M.S., Schoemaker R.C., de Visser S., Kuijpers M., Pennings E.J., de Bruin D., Van de Wijngaart G., Van Gerven J.M., and Cohen A.F. Cognitive performance and serotonergic function in users of ecstasy. Psychopharmacology (Berl) 153 (2001) 196-202
65. Virden T.B., and Baker L.E. Disruption of the discriminative stimulus effects of S(+)-3,4-methylenedioxymethamphetamine (MDMA) by (+/-)-MDMA neurotoxicity: protection by fluoxetine. Behav Pharmacol 10 (1999) 195-204
66. Wang X., Baumann M.H., and Rothman R.B. Restoration of 3,4-methylenedioxymethamphetamine-induced 5-HT depletion by the administration of L-5-hydroxytryptophan. Neuroscience 148 (2007) 212-220
67. Wang X., Baumann M.H., Xu H., Morales M., and Rothman R.B. (+/-)-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 (2005) 1002-1012
68. White S.R., Obradovic T., Imel K.M., and Wheaton M.J. The effects of methylenedioxymethamphetamine (MDMA, "ecstasy") on monoaminergic neurotransmission in the central nervous system. Prog Neurobiol 49 (1996) 455-479
69. Zacny J.P., Virus R.M., and Woolverton W.L. Tolerance and cross-tolerance to 3,4-methylenedioxymethamphetamine (MDMA), methamphetamine and methylenedioxyamphetamine. Pharmacol Biochem Behav 35 (1990) 637-642