MDMA causes a redistribution of serotonin transporter from the cell surface to the intracellular compartment by a mechanism independent of phospho-p38-mitogen activated protein kinase activation

Neuroscience

Volumn 168, Issue 1, 2010, Pages 82-95

  Kivell, B ^a   Day, D ^a   Bosch, P ^a   Schenk, S ^a   Miller, J ^a  

^a VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

Ecstasy; MDMA; P38 MAPK; SERT trafficking

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; ENZYME ANTIBODY; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; SEROTONIN; SEROTONIN TRANSPORTER;

ANIMAL TISSUE; ARTICLE; BIOTINYLATION; BRAIN TISSUE; CELL STRAIN HEK293; CELL SURFACE; CELL VACUOLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CORPUS STRIATUM; DORSAL RAPHE NUCLEUS; ENZYME ACTIVATION; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BRAIN; CELL LINE, TUMOR; CELL MEMBRANE; ENZYME ACTIVATION; MALE; MICE; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 77952889355     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.03.018     Document Type: Article

References (52)

1. Awtry T.L., Frank J.G., Werling L.L. In vitro regulation of serotonin transporter activity by protein kinase A and nicotinic acetylcholine receptors in the prefrontal cortex of rats. Synapse 2006, 59:342-349.
2. Banks M.L., Czoty P.W., Gage H.D., Bounds M.C., Garg P.K., Garg S., Nader M.A. Effects of cocaine and MDMA self-administration on serotonin transporter availability in monkeys. Neuropsychopharmacology 2008, 32:219-225.
3. Battaglia G., Yeh S.Y., O'Hearn E., Molliver M.E., Kuhar M.J., 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 1987, 242:911-916.
4. Baumann M., Wang X., Rothman R. 3,4-Methylenedioxymethamphetamine (MDMA) neurotoxicity in rats: a reappraisal of past and present findings. Psychopharmacology 2007, 189:407-424.
5. Bogen I.L., Haug K.H., Myhre O., Fonnum F. Short- and long-term effects of MDMA on synaptosomal and vesicular uptake of neurotransmitters in vitro and ex vivo. Neurochem Int 2003, 43:393-400.
6. Campbell N.G., Koprich J.B., Kanaan N.M., Lipton J.W. MDMA administration to pregnant Sprague-Dawley rats results in its passage to the fetal compartment. Neurotoxicol Teratol 2006, 28:459-465.
7. Capela J.P., Carmo H., Remiao F., Bastos M.L., Meisel A., Carvalho F. Molecular and cellular mechnaisms of ecstasy induced neurotoxicity: an overview. Mol Neurobiol 2009, 39:210-271.
8. Capela J.P., Fernandes E., Remião F., Bastos M.L., Meisel A., Carvalho F. Ecstasy induces apoptosis via 5-HT2A-receptor stimulation in cortical neurons. Neurotoxicology 2007, 28:868-875.
9. Capela J.P., Ruscher K., Lautenschlager M., Freyer D., Dirnagl U., Gaio A.R., Bastos M.L., Meisel A., Carvalho F. Ecstasy-induced cell death in cortical neuronal cultures is serotonin 2A-receptor-dependent and potentiated under hyperthermia. Neuroscience 2006, 139:1069-1081.
10. Chamba A., Holder M.J., Barnes N.M., Gordon J. Characterisation of the endogenous human peripheral serotonin transporter SLC6A4 reveals surface expression without N-glycosylation. J Neuroimmunol 2008, 204:75-84.
11. Chu N.T., Kumagai Y., DiStefano E.W., Cho A.K. Disposition of methylenedioxymethamphetamine and three metabolites in the brains of different rat strains and their possible roles in acute serotonin depletion. Biochem Pharmacol 1996, 51:789-796.
12. Commins D.L., Vosmer G., Virus R.M., Woolverton W.L., Schuster C.R., Seiden L.S. Biochemical and histological evidence that methylenedioxymethylamphetamine (MDMA) is toxic to neurons in the rat brain. J Pharmacol Exp Ther 1987, 241:338-345.
13. Galineau L., Belzung C., Kodas E., Bodard S., Guilloteau D., Chalon S. Prenatal 3,4-methylenedioxymethamphetamine (ecstasy) exposure induces long-term alterations in the dopaminergic and serotonergic functions in the rat. Dev Brain Res 2005, 154:165-176.
14. Goñi-Allo B., Puerta E., Mathúna B., Hervias I., Lasheras B., de la Torre R., Aguirre N. On the role of tyrosine and peripheral metabolism in 3,4-methylenedioxymethamphetamine-induced serotonin neurotoxicity in rats. Neuropharmacology 2008, 54:885-900.
15. Green A.R., O'Shea E., Colado M. A review of the mechanisms involved in the acute. MDMA (ecstasy)-induced hyperthermic response. Eur J Pharmacol 2004, 500:3-13.
16. Green A.R., Mechan A.O., Elliott J.M., O'Shea E., Colado M.I. The pharmacology and clinical pharmacology of 3,4-methylenedioxymethamphetamine (MDMA, "ecstasy"). Pharmacol Rev 2003, 55:463-508.
17. Green A.R., Gabrielsson J., Marsden C.A., Fone K.C. MDMA: on the translation from rodent to human dosing. Psychopharmacology (Berl) 2009, 204:375-378.
18. Gudelsky G.A., Yamamoto B.K. Actions of 3,4-methylenedioxymethamphetamine (MDMA) on cerebral dopaminergic, serotonergic and cholinergic neurons. Pharmacol Biochem Behav 2008, 90:198-207.
19. Jayanthi L.D., Ramamoorthy S. Regulation of monoamine transporters: influence of psychostimulants and therapeutic antidepressants. AAPS J 2005, 7:E728-E738.
20. Jayanthi L.D., Samuvel D.J., Blakely R.D., Ramamoorthy S. Evidence for biphasic effects of protein kinase C on serotonin transporter function, endocytosis, and phosphorylation. Mol Pharmacol 2005, 67:2077-2087.
21. Jensen K.F., Olin J., Haykal-Coates N., O'Callaghan J., Miller D.B., de Olmos J.S. Mapping toxicant-induced nervous system damage with a cupric silver stain: a quantitative analysis of neural degeneration induced by 3, 4-methylenedioxymethamphetamine. NIDA Res Monogr 1993, 136:133-149.
22. Kindlundh-Högberg A.M.S., Schiöth H.B., Svenningsson P. Repeated intermittent MDMA binges reduce DAT density in mice and SERT density in rats in reward regions of the adolescent brain. Neurotoxicology 2007, 28:1158-1169.
23. Kittler K., Lau T., Schloss P. Antagonists and substrates differentially regulate serotonin transporter cell surface expression in serotonergic neurons. Eur J Pharmacol 2010, 629:63-67.
24. Lau T., Horschitz S., Bartsch D., Schloss P. Monitoring mouse serotonin transporter internalization in stem cell-derived serotonergic neurons by confocal laser scanning microscopy. Neurochem Int 2009, 54:271-276.
25. Lew R., Sabol K.E., Chou C., Vosmer G.L., Richards J., Seiden L.S. 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 1996, 276:855-865.
26. Li L.B., Chen N., Ramamoorthy S., Chi L., Cui X.N., Wang L.C., Reith M.E.A. The role of N-glycosylation in function and surface trafficking of the human dopamine transporter. J Biol Chem 2004, 279:21012-21020.
27. McCann U.D., Szabo Z., Scheffel U., Dannals R.F., Ricaurte G.A. Positron emission tomographic evidence of toxic effect of MDMA ("Ecstasy") on brain serotonin neurons in human beings. Lancet 1998, 352:1433-1437.
28. McCann U.D., Szabo Z., Seckin E., Rosenblatt P., Matthews W.B., Ravert H.T., Dannals R.F., Ricaurte G.A. Quantitative PET studies of the serotonin transporter in MDMA users and controls using [11C]McN5652 and [11C]DASB. Neuropsychopharmacology 2005, 30:1741-1750.
29. McCann U.D., Ricaurte G.A., Molliver M.E. "Ecstasy" and serotonin neurotoxicity: new findings raise more questions. Arch Gen Psychiatry 2001, 58:901-906.
30. McLane M.W., Hatzidimitriou G., Yuan J., McCann U., Ricaurte G. Heating induces aggregation and decreases detection of serotonin transporter protein on western blots. Synapse 2007, 61:875-876.
31. Morón J.A., Zakharova I., Ferrer J.V., Merrill G.A., Hope B., Lafer E.M., Lin Z.C., Wang J.B., Javitch J.A., Galli A., Shippenberg T.S. Mitogen-activated protein kinase regulates dopamine transporter surface expression and dopamine transport capacity. J Neurosci 2003, 23(24):8480-8488.
32. O'Callaghan J.P., Miller D.B. Quantification of reactive gliosis as an approach to neurotoxicity assessment. NIDA Res Monogr 1993, 136:188-212.
33. Pifl C., Nagy G., Berenyi S., Kattinger A., Reither H., Antus S. Pharmacological characterization of ecstasy synthesis byproducts with recombinant human monoamine transporters. J Pharmacol Exp Ther 2005, 314:346-354.
34. Prasad H.C., Zhu C.B., McCauley J.L., Samuvel D.J., Ramamoorthy S., Shelton R.C., Hewlett W.A., Sutcliffe J.S., Blakely R.D. Human serotonin transporter variants display altered sensitivity to protein kinase G and p38 mitogen-activated protein kinase. Proc Natl Acad Sci U S A 2005, 102:11545-11550.
35. Quan Y., Galli A., Ramamoorthy S., Risso S., DeFelice L.J., Blakely R.D. Protein kinase C activation regulates human serotonin transporters in HEK-293 cells via altered cell surface expression. J Neurosci 1997, 17:45-57.
36. Ramamoorthy S., Samuvel D.J., Buck E.R., Rudnick G., Jayanthi L.D. Phosphorylation of threonine residue 276 is required for acute regulation of serotonin transporter by cyclic GMP. J Biol Chem 2007, 282:11639-11647.
37. Reneman L., de Win M.M., van den Brink W., Booij J., den Heeten G.J. Neuroimaging findings with MDMA/ecstasy: technical aspects, conceptual issues and future prospects. J Psychopharmacol 2006, 20:164-175.
38. Rothman R.B., Jayanthi S., Wang X., Dersch C.M., Cadet J.L., Prisinzano T., Rice K.C., Baumann M.H. High-dose fenfluramine administration decreases serotonin transporter binding, but not serotonin transporter protein levels, in rat forebrain. Synapse 2003, 50:233-239.
39. Rouse J., Cohen P., Trigon S., Morange M., Alonso-Llamazares A., Zamanillo D., Hunt T., Nebreda A.R. A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell 1994, 78:1027-1037.
40. Samuvel D.J., Jayanthi L.D., Bhat N.R., Ramamoorthy S. A role for p38 mitogen-activated protein kinase in the regulation of the serotonin transporter: evidence for distinct cellular mechanisms involved in transporter surface expression. J Neurosci 2005, 25:29-41.
41. Schenk S., Hely L., Lake B., Daniela E., Gittings D., Mash D.C. MDMA self-administration in rats: acquisition, progressive ratio responding and serotonin transporter binding. Eur J Neurosci 2007, 26:3229-3236.
42. Schmued L., Slikker W., Clausing P., Bowyer J. d-Fenfluramine produces neuronal degeneration in localized regions of the cortex, thalamus, and cerebellum of the rat. Toxicol Sci 1999, 48:100-106.
43. Schmued L.C. Demonstration and localization of neuronal degeneration in the rat forebrain following a single exposure to MDMA. Brain Res 2003, 974:127-133.
44. Steiner J.A., Carneiro A.M., Blakely R.D. Going with the flow: trafficking-dependent and -independent regulation of serotonin transport. Traffic 2008, 9:1393-1402.
45. Sveen M.L., Knudsen G.M., Aznar S. No effect of MDMA (ecstasy) on cell death and 5-HT2A receptor density in organotypic rat hippocampal cultures. Neurosci Lett 2004, 362:6-9.
46. Upreti V.V., Eddington N.D. Fluoxetine pretreatment effects pharmacokinetics of 3,4-Methylenedioxymethamphetamine (MDMA, ecstasy) in rat. J Pharm Sci 2007, 97(4):1593-1605.
47. Walker T.M., Davenport-Jones J.E., Fox R.M., Atterwill C.K. The neurotoxic effects of methylenedioxymethamphetamine (MDMA) and its metabolites on rat brain spheroids in culture. Cell Biol Toxicol 1999, 15:137-142.
48. Wang X., Baumann M.H., Xu H., Rothman R.B. 3,4-methylenedioxymethamphetamine (MDMA) administration to rats decreases brain tissue serotonin but not serotonin transporter protein and glial fibrillary acidic protein. Synapse 2004, 53:240-248.
49. Wang X., Baumann M.H., Dersch C.M., Rothman R.B. Restoration of 3,4-methylenedioxymethamphetamine-induced 5-HT depletion by the administration of L-5-hydroxytryptophan. Neuroscience 2007, 148:212-220.
50. Wang X., Baumann M.H., Xu H., Morales M., 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 2005, 314:1002-1012.
51. Williams M.T., Schaefer T.L., Ehrman L.A., Able J.A., Gudelsky G.A., Sah R., Vorhees C.V. 3,4-Methylenedioxymethamphetamine administration on postnatal day 11 in rats increases pituitary-adrenal output and reduces striatal and hippocampal serotonin without altering SERT activity. Brain Res 2005, 1039:97-107.
52. Xie T., Tong L., McLane M.W., Hatzidimitriou G., Yuan J., McCann U., Ricaurte G. Loss of serotonin transporter protein after MDMA and other ring-substituted amphetamines. Neuropsychopharmacology 2006, 31:2639-2651.