The Effects of Ecstasy (MDMA) on Brain Serotonin Transporters Are Dependent on Age-of-First Exposure in Recreational Users and Animals

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Klomp, Anne ^a   den Hollander, Bjørnar ^a   de Bruin, Kora ^a   Booij, Jan ^a   Reneman, Liesbeth ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; IODINE 123; SEROTONIN TRANSPORTER;

ADOLESCENT; ADULT; AGE DISTRIBUTION; AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; FRONTAL CORTEX; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS; MALE; MESENCEPHALON; NEUROTOXICITY; NEUROTRANSMISSION; NEUROTROPISM; NONHUMAN; OCCIPITAL CORTEX; PERINATAL DRUG EXPOSURE; PREFRONTAL CORTEX; PROTEIN BINDING; RAT; SINGLE PHOTON EMISSION COMPUTER TOMOGRAPHY; TEMPORAL CORTEX;

ADOLESCENT; ADULT; ANIMALS; BRAIN; HUMANS; MALE; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; RATS; RATS, WISTAR; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; TOMOGRAPHY, EMISSION-COMPUTED, SINGLE-PHOTON; YOUNG ADULT;

ANIMALIA; RATTUS;

EID: 84868144675     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047524     Document Type: Article

References (53)

1. Gaspar P, Cases O, Maroteaux L, (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 4: 1002-1012.
2. Homberg JR, Schubert D, Gaspar P, (2010) New perspectives on the neurodevelopmental effects of SSRIs. Trends Pharmacol Sci 31: 60-65.
3. Whitaker-Azmitia PM, Druse M, Walker P, Lauder JM, (1996) Serotonin as a developmental signal. Behav Brain Res 73: 19-29.
4. Shemer AV, Azmitia EC, Whitaker-Azmitia PM, (1991) Dose-related effects of prenatal 5-methoxytryptamine (5-MT) on development of serotonin terminal density and behavior. Brain Res Dev Brain Res 59: 59-63.
5. Cabrera-Vera TM, Garcia F, Pinto W, Battaglia G, (1997) Effect of prenatal fluoxetine (Prozac) exposure on brain serotonin neurons in prepubescent and adult male rat offspring. J Pharmacol Exp Ther 280: 138-145.
6. Maciag D, Simpson KL, Coppinger D, Lu Y, Wang Y, et al. (2006) Neonatal antidepressant exposure has lasting effects on behavior and serotonin circuitry. Neuropsychopharmacology 31: 47-57.
7. Wegerer V, Moll GH, Bagli M, Rothenberger A, Ruther E, et al. (1999) Persistently increased density of serotonin transporters in the frontal cortex of rats treated with fluoxetine during early juvenile life. J Child Adolesc Psychopharmacol 9: 13-24.
8. Won L, Bubula N, Heller A, (2002) Fetal exposure to (+/-)-methylenedioxymethamphetamine in utero enhances the development and metabolism of serotonergic neurons in three-dimensional reaggregate tissue culture. Brain Res Dev Brain Res 137: 67-73.
9. Azmitia EC, Murphy RB, Whitaker-Azmitia PM, (1990) MDMA (ecstasy) effects on cultured serotonergic neurons: evidence for Ca2(+)-dependent toxicity linked to release. Brain Res 510: 97-103.
10. Ricaurte GA, Yuan J, McCann UD, (2000) (+/-)3,4-Methylenedioxymethamphetamine ('Ecstasy')-induced serotonin neurotoxicity: studies in animals. Neuropsychobiology 42: 5-10.
11. Reneman L, Booij J, de Bruin K, Reitsma JB, de Wolff FA, et al. (2001) Effects of dose, sex, and long-term abstention from use on toxic effects of MDMA (ecstasy) on brain serotonin neurons. Lancet 358: 1864-1869.
12. Broening HW, Bacon L, Slikker W Jr, (1994) Age modulates the long-term but not the acute effects of the serotonergic neurotoxicant 3,4-methylenedioxymethamphetamine. J Pharmacol Exp Ther 271: 285-293.
13. Meyer JS, Ali SF, (2002) Serotonergic neurotoxicity of MDMA (ecstasy) in the developing rat brain. Ann N Y Acad Sci 965: 373-380.
14. Aguirre N, Barrionuevo M, Lasheras B, Del RJ, (1998) The role of dopaminergic systems in the perinatal sensitivity to 3, 4-methylenedioxymethamphetamine-induced neurotoxicity in rats. J Pharmacol Exp Ther 286: 1159-1165.
15. Lyles J, Cadet JL, (2003) Methylenedioxymethamphetamine (MDMA, Ecstasy) neurotoxicity: cellular and molecular mechanisms. Brain Res Brain Res Rev 42: 155-168.
16. Capela JP, Carmo H, Remiao F, Bastos ML, Meisel A, et al. (2009) Molecular and cellular mechanisms of ecstasy-induced neurotoxicity: an overview. Mol Neurobiol 39: 210-271.
17. Colado MI, O'Shea E, Granados R, Misra A, Murray TK, et al. (1997) A study of the neurotoxic effect of MDMA ('ecstasy') on 5-HT neurones in the brains of mothers and neonates following administration of the drug during pregnancy. Br J Pharmacol 121: 827-833.
18. Andersen SL, (2003) Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27: 3-18.
19. Brenhouse HC, Andersen SL, (2011) Developmental trajectories during adolescence in males and females: a cross-species understanding of underlying brain changes. Neurosci Biobehav Rev 35: 1687-1703.
20. Crews F, He J, Hodge C, (2007) Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 86: 189-199.
21. Olivier JD, Blom T, Arentsen T, Homberg JR, (2011) The age-dependent effects of selective serotonin reuptake inhibitors in humans and rodents: A review. Prog Neuropsychopharmacol Biol Psychiatry 35: 1400-1408.
22. Moll GH, Mehnert C, Wicker M, Bock N, Rothenberger A, et al. (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. Brain Res Dev Brain Res 119: 251-257.
23. Andersen SL, (2005) Stimulants and the developing brain. Trends Pharmacol Sci 26: 237-243.
24. Spear LP, (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24: 417-463.
25. Brunello N, Riva M, Volterra A, Racagni G, (1985) Age-related changes in 5HT uptake and [3H]imipramine binding sites in rat cerebral cortex. Eur J Pharmacol 110: 393-394.
26. Slotkin TA, McCook EC, Ritchie JC, Carroll BJ, Seidler FJ, (1997) Serotonin transporter expression in rat brain regions and blood platelets: aging and glucocorticoid effects. Biol Psychiatry 41: 172-183.
27. van Dyck CH, Malison RT, Seibyl JP, Laruelle M, Klumpp H, et al. (2000) Age-related decline in central serotonin transporter availability with [(123)I]beta-CIT SPECT. Neurobiol Aging 21: 497-501.
28. Dahlstrom M, Ahonen A, Ebeling H, Torniainen P, Heikkila J, et al. (2000) Elevated hypothalamic/midbrain serotonin (monoamine) transporter availability in depressive drug-naive children and adolescents. Mol Psychiatry 5: 514-522.
29. Andersson A, Sundman I, Marcusson J, (1992) Age stability of human brain 5-HT terminals studied with [3H]paroxetine binding. Gerontology 38: 127-132.
30. Arranz B, Eriksson A, Mellerup E, Plenge P, Marcusson J, (1993) Effect of aging in human cortical pre- and postsynaptic serotonin binding sites. Brain Res 620: 163-166.
31. Sowell ER, Delis D, Stiles J, Jernigan TL, (2001) Improved memory functioning and frontal lobe maturation between childhood and adolescence: a structural MRI study. J Int Neuropsychol Soc 7: 312-322.
32. Reneman L, Lavalaye J, Schmand B, de Wolff FA, van den Brink W, et al. (2001) Cortical serotonin transporter density and verbal memory in individuals who stopped using 3,4-methylenedioxymethamphetamine (MDMA or "ecstasy"): preliminary findings. Arch Gen Psychiatry 58: 901-906.
33. de Win MM, Habraken JB, Reneman L, van den Brink W, den Heeten GJ, et al. (2005) Validation of [(123)I]beta-CIT SPECT to assess serotonin transporters in vivo in humans: a double-blind, placebo-controlled, crossover study with the selective serotonin reuptake inhibitor citalopram. Neuropsychopharmacology 30: 996-1005.
34. Reneman L, Booij J, Habraken JB, de Bruin K, Hatzidimitriou G, et al. (2002) Validity of [123I]beta-CIT SPECT in detecting MDMA-induced serotonergic neurotoxicity. Synapse 46: 199-205.
35. Scheffel U, Dannals RF, Cline EJ, Ricaurte GA, Carroll FI, et al. (1992) [123/125I]RTI-55, an in vivo label for the serotonin transporter. Synapse 11: 134-139.
36. Booij J, Tissingh G, Boer GJ, Speelman JD, Stoof JC, et al. (1997) [123I]FP-CIT SPECT shows a pronounced decline of striatal dopamine transporter labelling in early and advanced Parkinson's disease. J Neurol Neurosurg Psychiatry 62: 133-140.
37. Pirker W, Asenbaum S, Hauk M, Kandlhofer S, Tauscher J, et al. (2000) Imaging serotonin and dopamine transporters with 123I-beta-CIT SPECT: binding kinetics and effects of normal aging. J Nucl Med 41: 36-44.
38. Elfving B, Madsen J, Knudsen GM, (2007) Neuroimaging of the serotonin reuptake site requires high-affinity ligands. Synapse 61: 882-888.
39. Gould RW, Gage HD, Banks ML, Blaylock BL, Czoty PW, et al. (2011) Differential effects of cocaine and MDMA self-administration on cortical serotonin transporter availability in monkeys. Neuropharmacology 61: 245-251.
40. Reneman L, Booij J, Lavalaye J, de Bruin K, de Wolff FA, et al. (1999) Comparative in vivo study of iodine-123-labeled beta-CIT and nor-beta-CIT binding to serotonin transporters in rat brain. Synapse 34: 77-80.
41. Rijks LJ, Booij J, Doornbos T, Boer GJ, Ronken E, et al. (1996) In vitro and in vivo characterization of newly developed iodinated 1-[2-[bis(4-fluorophenyl)methoxy]ethyl]piperazine derivatives in rats: limited value as dopamine transporter SPECT ligands. Synapse 23: 201-207.
42. Boylan CB, Bennett-Clarke CA, Chiaia NL, Rhoades RW, (2000) Time course of expression and function of the serotonin transporter in the neonatal rat's primary somatosensory cortex. Somatosens Mot Res 17: 52-60.
43. Woolsey TA, Welker C, Schwartz RH, (1975) Comparative anatomical studies of the SmL face cortex with special reference to the occurrence of "barrels" in layer IV. J Comp Neurol 164: 79-94.
44. de Win MM, de Jeu RA, de Bruin K, Habraken JB, Reneman L, et al. (2004) Validity of in vivo [123I]beta-CIT SPECT in detecting MDMA-induced neurotoxicity in rats. Eur Neuropsychopharmacol 14: 185-189.
45. Battaglia G, Yeh SY, O'Hearn E, Molliver ME, Kuhar MJ, et al. (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.
46. Lew R, Sabol KE, Chou C, Vosmer GL, Richards J, et al. (1996) Methylenedioxymethamphetamine-induced serotonin deficits are followed by partial recovery over a 52-week period. Part II: Radioligand binding and autoradiography studies. J Pharmacol Exp Ther 276: 855-865.
47. 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.
48. 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.
49. Lauder JM, Krebs H, (1978) Serotonin as a differentiation signal in early neurogenesis. Dev Neurosci 1: 15-30.
50. Lauder JM, Wallace JA, Wilkie MB, DiNome A, Krebs H, (1983) Roles for serotonin in neurogenesis. Monogr Neural Sci 9: 3-10.
51. Lauder JM, Tamir H, Sadler TW, (1988) Serotonin and morphogenesis. I. Sites of serotonin uptake and-binding protein immunoreactivity in the midgestation mouse embryo. Development 102: 709-720.
52. Whitaker-Azmitia PM, Azmitia EC, (1989) Stimulation of astroglial serotonin receptors produces culture media which regulates growth of serotonergic neurons. Brain Research 497: 80-85.
53. Farde L, Halldin C, Muller L, Suhara T, Karlsson P, et al. (1994) PET study of [11C]beta-CIT binding to monoamine transporters in the monkey and human brain. Synapse 16: 93-103.