MDMA increases glutamate release and reduces parvalbumin-positive GABAergic cells in the dorsal hippocampus of the rat: Role of cyclooxygenase

Journal of Neuroimmune Pharmacology

Volumn 8, Issue 1, 2013, Pages 58-65

  Anneken, John H ^a   Cunningham, Jacobi I ^b   Collins, Stuart A ^b   Yamamoto, Bryan K ^b   Gudelsky, Gary A ^a  

^a UNIVERSITY OF CINCINNATI   (United States)

^b MEDICAL COLLEGE OF OHIO   (United States)

Author keywords

Cyclooxygenase; GABA; Glutamate; MDMA

Indexed keywords

3,4 METHYLENEDIOXYMETHAMPHETAMINE; 4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMIC ACID; KETOPROFEN; NIMESULIDE; PARVALBUMIN; PIROXICAM; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; ENZYME INHIBITION; EXTRACELLULAR SPACE; GABAERGIC TRANSMISSION; HIPPOCAMPUS; INTERNEURON; MALE; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

ADRENERGIC UPTAKE INHIBITORS; ANIMALS; CELL COUNT; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYCLOOXYGENASE INHIBITORS; DENTATE GYRUS; DINOPROSTONE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERNEURONS; KETOPROFEN; MALE; MICRODIALYSIS; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; PARVALBUMINS; PRESYNAPTIC TERMINALS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RATS; RATS, SPRAGUE-DAWLEY; SEROTONIN;

EID: 84874651556     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-012-9420-x     Document Type: Article

References (48)

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 59:1219-1226
2. Anneken JH, Gudelsky GA (2012) MDMA produces a delayed and sustained increase in the extracellular concentration of glutamate in the rat hippocampus. Neuropharmacology 63(6):1022-1027
3. Armstrong BD, Noguchi KK (2004) The neurotoxic effects of 3,4-methylenedioxymethamphetamine (MDMA) and methamphetamine on serotonin, dopamine, and GABA-ergic terminals: an in-vitro autoradiographic study in rats. Neurotoxicology 25:905-914
4. Asanuma M, Tsuji T, Miyazaki I, Miyoshi K, Ogawa N (2003) Methamphetamine-induced neurotoxicity in mouse brain is attenuated by ketoprofen, a non-steroidal anti-inflammatory drug. Neurosci Lett 352:13-16
5. Asi SS, Farhadi HM, Naghdi N, Choopani S, Samzadeh-Kermani A, Mehdizadeh M (2011) Non-acute effects of different doses of 3,4- methylenedioxymethamphetamine on spatial memory in the morris water maze in Sprague-Dawley male rats. Neural Regen Res 6:1715
6. Asi SS, Farhadi HM, Mousavizadeh K, Samadikuchaksaraei A, Soleimani M, Jameie SB, Joghataei MT, Samzadeh-Kermani A, Hashemi-Nasl H, Mehdizadeh, M (2012) Evaluation of Bcl-2 Family Gene Expression in Hippocampus of 3,4-methylenedioxymethamphetamine Treated Rats. Cell J Vol 13, No 4, Winter 2012
7. Bezzi P, Carmignoto G, Pasti L, Vesce S, Rossi D, Rizzini BL, Pozzan T, Volterra A (1998) Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391:281-285
8. Burgess AP, Venables L, Jones H, Edwards R, Parrott AC (2011) Event related potential (ERP) evidence for selective impairment of verbal recollection in abstinent recreational methylenedioxymethamphetamine ("ecstasy")/ polydrug users. Psychopharmacol (Berl) 216:545-556
9. Candelario-Jalil E, Gonzalez-Falcon A, Garcia-Cabrera M, Leon OS, Fiebich BL (2004) Wide therapeutic time window for nimesulide neuroprotection in a model of transient focal cerebral ischemia in the rat. Brain Res 1007:98-108
10. Capela JP, Fernandes E, Remiao F, Bastos ML, Meisel A, Carvalho F (2007) Ecstasy induces apoptosis via 5-HT(2A)-receptor stimulation in cortical neurons. Neurotoxicology 28:868-875
11. Capela JP, da Costa Araujo S, Costa VM, Ruscher K, Fernandes E, Bastos MD, Dirnagl U, Meisel A, Carvalho F (2012) The neurotoxicity of hallucinogenic amphetamines in primary cultures of hippocampal neurons. Neurotoxicology. doi: 10.1016/j.neuro.2012.09.005
12. Cunningham JI, Raudensky J, Tonkiss J, Yamamoto BK (2009) MDMA pretreatment leads to mild chronic unpredictable stress-induced impairments in spatial learning. Behav Neurosci 123:1076-1084
13. Czeh B, Simon M, van der Hart MG, Schmelting B, Hesselink MB, Fuchs E (2005) Chronic stress decreases the number of parvalbumin-immunoreactive interneurons in the hippocampus: Prevention by treatment with a substance P receptor (NK1) antagonist. Neuropsychopharmacology 30:67-79
14. de Sola Llopis S, Miguelez-Pan M, Pena-Casanova J, Poudevida S, Farre M, Pacifici R, Bohm P, Abanades S, Verdejo Garcia 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 22:498-510
15. Donzanti BA, Yamamoto BK (1988) An improved and rapid HPLC-EC method for the isocratic separation of amino acid neurotransmitters from brain tissue and microdialysis perfusates. Life Sci 43:913-922
16. Farfel GM, Seiden LS (1995) Role of hypothermia in the mechanism of protection against serotonergic toxicity. I. experiments using 3,4-methylenedioxymethamphetamine, dizocilpine, CGS 19755 and NBQX. J Pharmacol Exp Ther 272:860-867
17. Garcia MC, Kim HY (1997) Mobilization of arachidonate and docosahexaenoate by stimulation of the 5-HT2A receptor in rat C6 glioma cells. Brain Res 768:43-48
18. 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 55:463-508
19. Gudelsky GA, Yamamoto BK (2003) Neuropharmacology and neurotoxicity of 3,4-methylenedioxymethamphetamine. Methods Mol Med 79:55-73
20. Gundersen HJ, Jensen EB, Kieu K, Nielsen J (1999) The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193:199-211
21. Jacobsen LK, Mencl WE, Pugh KR, Skudlarski P, Krystal JH (2004) Preliminary evidence of hippocampal dysfunction in adolescent MDMA ("ecstasy") users: Possible relationship to neurotoxic effects. Psychopharmacol (Berl) 173:383-390
22. Kay C, Harper DN, Hunt M (2011) The effects of binge MDMA on acquisition and reversal learning in a radial-arm maze task. Neurobiol Learn Mem 95:473-483
23. Kelley KA, Ho L, Winger D, Freire-Moar J, Borelli CB, Aisen PS, Pasinetti GM (1999) Potentiation of excitotoxicity in transgenic mice overexpressing neuronal cyclooxygenase-2. Am J Pathol 155:995-1004
24. Kermanian F, Mehdizadeh M, Soleimani M, Ebrahimzadeh Bideskan AR, Asadi-Shekaari M, Kheradmand H, Haghir H (2012) The role of adenosine receptor agonist and antagonist on hippocampal MDMA detrimental effects; a structural and behavioral study. Metab Brain Dis
25. Kerner JA, Standaert DG, Penney JB Jr, Young AB, Landwehrmeyer GB (1997) Expression of group one metabotropic glutamate receptor subunit mRNAs in neurochemically identified neurons in the rat neostriatum, neocortex, and hippocampus. Brain Res Mol Brain Res 48:259-269
26. Lister JP, Tonkiss J, Blatt GJ, Kemper TL, DeBassio WA, Galler JR, Rosene DL (2006) Asymmetry of neuron numbers in the hippocampal formation of prenatally malnourished and normally nourished rats: a stereological investigation. Hippocampus 16:946-958
27. Mackowiak M, Chocyk A, Sanak M, Czyrak A, Fijal K, Wedzony K (2002) DOI, an agonist of 5-HT2A/2C serotonin receptor, alters the expression of cyclooxygenase-2 in the rat parietal cortex. J Physiol Pharmacol 53:395-407
28. Meller R, Harrison PJ, Elliott JM, Sharp T (2002) In vitro evidence that 5-hydroxytryptamine increases efflux of glial glutamate via 5-HT(2A) receptor activation. J Neurosci Res 67:399-405
29. Meyer JS, Grande M, Johnson K, Ali SF (2004) Neurotoxic effects of MDMA ("ecstasy") administration to neonatal rats. Int J Dev Neurosci 22:261-271
30. Moga DE, Janssen WG, Vissavajjhala P, Czelusniak SM, Moran TM, Hof PR, Morrison JH (2003) Glutamate receptor subunit 3 (GluR3) immunoreactivity delineates a subpopulation of parvalbumin-containing interneurons in the rat hippocampus. J Comp Neurol 462:15-28
31. Morris AM, Churchwell JC, Kesner RP, Gilbert PE (2012) Selective lesions of the dentate gyrus produce disruptions in place learning for adjacent spatial locations. Neurobiol Learn Mem 97:326-331
32. Muller GJ, Moller A, Johansen FF (2001) Stereological cell counts of GABAergic neurons in rat dentate hilus following transient cerebral ischemia. Exp Brain Res 141:380-388
33. Okada K, Okaichi H (2009) Functional differentiation and cooperation among the hippocampal subregions in rats to effect spatial memory processes. Behav Brain Res 200:181-191
34. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, 4th edn. Academic, San Diego
35. Perrine SA, Ghoddoussi F, Michaels MS, Hyde EM, Kuhn DM, Galloway MP (2010) MDMA administration decreases serotonin but not N-acetylaspartate in the rat brain. Neurotoxicology 31:654-661
36. Raj V, Liang HC, Woodward ND, Bauernfeind AL, Lee J, Dietrich MS, Park S, Cowan RL (2010) MDMA (ecstasy) use is associated with reduced BOLD signal change during semantic recognition in abstinent human polydrug users: a preliminary fMRI study. J Psychopharmacol 24:187-201
37. Riezzo I, Cerretani D, Fiore C, Bello S, Centini F, D'Errico S, Fiaschi AI, Giorgi G, Neri M, Pomara C, Turillazzi E, Fineschi V (2010) Enzymatic-nonenzymatic cellular antioxidant defense systems response and immunohistochemical detection of MDMA, VMAT2, HSP70, and apoptosis as biomarkers for MDMA (ecstasy) neurotoxicity. J Neurosci Res 88:905-916
38. Sang N, Yun Y, Yao GY, Li HY, Guo L, Li GK (2011) SO(2)-induced neurotoxicity is mediated by cyclooxygenases-2-derived prostaglandin E(2) and its downstream signaling pathway in rat hippocampal neurons. Toxicol Sci 124:400-413
39. Sanon N, Carmant L, Emond M, Congar P, Lacaille JC (2005) Short-term effects of kainic acid on CA1 hippocampal interneurons differentially vulnerable to excitotoxicity. Epilepsia 46:837-848
40. Sanzgiri RP, Araque A, Haydon PG (1999) Prostaglandin E(2) stimulates glutamate receptor-dependent astrocyte neuromodulation in cultured hippocampal cells. J Neurobiol 41:221-229
41. Schmued LC (2003) Demonstration and localization of neuronal degeneration in the rat forebrain following a single exposure to MDMA. Brain Res 974:127-133
42. Shankaran M, Yamamoto BK, Gudelsky GA (2001) Ascorbic acid prevents 3,4-methylenedioxymethamphetamine (MDMA)-induced hydroxyl radical formation and the behavioral and neurochemical consequences of the depletion of brain 5-HT. Synapse 40:55-64
43. Skelton MR, Williams MT, Vorhees CV (2006) Treatment with MDMA from P11-20 disrupts spatial learning and path integration learning in adolescent rats but only spatial learning in older rats. Psychopharmacol (Berl) 189:307-318
44. Terao A, Matsumura H, Saito M (1998) Interleukin-1 induces slow-wave sleep at the prostaglandin D2-sensitive sleep-promoting zone in the rat brain. J Neurosci 18:6599-6607
45. Wang X, Zhu SP, Kuang WH, Li J, Sun X, Huang MS, Sun XL (2009) Neuron apoptosis induced by 3,4-methylenedioxy methamphetamine and expression of apoptosis-related factors in rat brain. Sichuan Da Xue Xue Bao Yi Xue Ban 40(1000-2):1037
46. Warren MW, Larner SF, Kobeissy FH, Brezing CA, Jeung JA, Hayes RL, Gold MS, Wang KK (2007) Calpain and caspase proteolytic markers co-localize with rat cortical neurons after exposure to methamphetamine and MDMA. Acta Neuropathol 114:277-286
47. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497
48. 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 31:2639-2651