MPTP-induced dopamine neuron degeneration and glia activation is potentiated in MDMA-pretreated mice

Movement Disorders

Volumn 28, Issue 14, 2013, Pages 1957-1965

  Costa, Giulia ^a   Frau, Lucia ^a   Wardas, Jadwiga ^c   Pinna, Annalisa ^b   Plumitallo, Antonio ^a   Morelli, Micaela ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b CNR   (Italy)

^c INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

Basal ganglia; CD11b; Glial fibrillary acidic protein; Neuroinflammation; Parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; 3,4 METHYLENEDIOXYMETHAMPHETAMINE; CD11B ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MACROGLIA; MALE; MICROGLIA; MOUSE; NERVE CELL DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; SUBSTANTIA NIGRA PARS COMPACTA;

BASAL GANGLIA; CD11B; GLIAL FIBRILLARY ACIDIC PROTEIN; NEUROINFLAMMATION; PARKINSON'S DISEASE;

ADRENERGIC UPTAKE INHIBITORS; ANIMALS; ANTIGENS, CD11B; BRAIN; CELL COUNT; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; DRUG SYNERGISM; GLIAL FIBRILLARY ACIDIC PROTEIN; MALE; MICE; MICE, INBRED C57BL; MPTP POISONING; N-METHYL-3,4-METHYLENEDIOXYAMPHETAMINE; NEUROGLIA; TIME FACTORS; TYROSINE 3-MONOOXYGENASE;

EID: 84889646696     PISSN: 08853185     EISSN: 15318257     Source Type: Journal    
DOI: 10.1002/mds.25646     Document Type: Article

References (55)

1. Costello S, Cockburn M, Bronstein J, Zhang X, Ritz B. Parkinson's disease and residential exposure to maneb and paraquat from agricultural applications in the central valley of California. Am J Epidemiol 2009;169:919-926.
2. Greenamyre JT, Hastings TG. Biomedicine. Parkinson's divergent causes, convergent mechanisms. Science 2004;304:1120-1122.
3. Kamel F, Tanner C, Umbach D, et al. Pesticide exposure and self-reported Parkinson's disease in the agricultural health study. Am J Epidemiol 2007;165:364-374.
4. Sulzer D. Multiple hit hypotheses for dopamine neuron loss in Parkinson's disease. Trends Neurosci 2007;30:244-250.
5. Parrott AC, Rodgers J, Buchanan T, Scholey AB, Heffernan T, Ling J. The reality of psychomotor problems, and the possibility of Parkinson's disorder, in some recreational ecstasy/MDMA users: a rejoinder to Sumnall et al. (2003). Psychopharmacology (Berl) 2004;171:231-233.
6. Christine CW, Garwood ER, Schrock LE, Austin DE, McCulloch CE. Parkinsonism in patients with a history of amphetamine exposure. Mov Disord 2010;25:228-231.
7. Callaghan RC, Cunningham JK, Sajeev G, Kish SJ. Incidence of Parkinson's disease among hospital patients with methamphetamine-use disorders. Mov Disord 2010;25:2333-2339.
8. Garwood ER, Bekele W, McCulloch CE, Christine CW. Amphetamine exposure is elevated in Parkinson's disease. Neurotoxicology 2006;27:1003-1006.
9. Brust JC. Substance abuse and movement disorders. Mov Disord 2010;25:2010-2020.
10. Callaghan RC, Cunningham JK, Sykes J, Kish SJ. Increased risk of Parkinson's disease in individuals hospitalized with conditions related to the use of methamphetamine or other amphetamine-type drugs. Drug Alcohol Depend 2012;120:35-40.
11. Rice D, Barone S Jr. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 2000;108(suppl 3):511-533.
12. Miller DB, O'Callaghan JP. Do early-life insults contribute to the late-life development of Parkinson and Alzheimer diseases? Metabolism 2008;57(suppl 2):S44-S49.
13. Green AR, Mechan AO, Elliott JM, O'Shea E, Colado MI. The pharmacology and clinical pharmacology of 3, 4-methylenedioxymethamphetamine (MDMA, "ecstasy"). Pharmacol Rev 2003;55:463-508.
14. Colado MI, O'Shea E, Granados R, Misra A, Murray TK, Green AR. 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 1997;121:827-833.
15. Sonsalla PK, Nicklas WJ, Heikkila RE. Role for excitatory amino acids in methamphetamine-induced nigrostriatal dopaminergic toxicity. Science 1989;243:398-400.
16. Baldwin HA, Colado MI, Murray TK, De Souza RJ, Green AR. Striatal dopamine release in vivo following neurotoxic doses of methamphetamine and effect of the neuroprotective drugs, chlormethiazole and dizocilpine. Br J Pharmacol 1993;108:590-596.
17. Granado N, O'Shea E, Bove J, Vila M, Colado MI, Moratalla R. Persistent MDMA-induced dopaminergic neurotoxicity in the striatum and substantia nigra of mice. J Neurochem 2008;107:1102-1112.
18. Granado N, Ares-Santos S, Oliva I, et al. Dopamine D2-receptor knockout mice are protected against dopaminergic neurotoxicity induced by methamphetamine or MDMA. Neurobiol Dis 2011;42:391-403.
19. Khairnar A, Plumitallo A, Frau L, Schintu N, Morelli M. Caffeine enhances astroglia and microglia reactivity induced by 3, 4-methylenedioxymethamphetamine ("ecstasy") in mouse brain. Neurotox Res 2010;17:435-439.
20. Frau L, Simola N, Plumitallo A, Morelli M. Microglial and astroglial activation by 3, 4-methylenedioxymethamphetamine (MDMA) in mice depends on S(+) enantiomer and is associated with an increase in body temperature and motility. J Neurochem 2013;124:69-78.
21. Kindlundh-Hogberg AM, Schioth HB, 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.
22. Fantegrossi WE, Godlewski T, Karabenick RL, et al. Pharmacological characterization of the effects of 3, 4-methylenedioxymethamphetamine ("ecstasy") and its enantiomers on lethality, core temperature, and locomotor activity in singly housed and crowded mice. Psychopharmacology (Berl) 2003;166:202-211.
23. Miller DB, O'Callaghan JP. The role of temperature, stress, and other factors in the neurotoxicity of the substituted amphetamines 3, 4-methylenedioxymethamphetamine and fenfluramine. Mol Neurobiol 1995;11:177-192.
24. Cadoni C, Solinas M, Pisanu A, Zernig G, Acquas E, Di Chiara G. Effect of 3, 4-methylendioxymethamphetamine (MDMA, "ecstasy") on dopamine transmission in the nucleus accumbens shell and core. Brain Res 2005;1055:143-148.
25. Acquas E, Pisanu A, Spiga S, Plumitallo A, Zernig G, Di Chiara G. Differential effects of intravenous R, S-(+/-)-3, 4-methylenedioxymethamphetamine (MDMA, ecstasy) and its S(+)- and R(-)-enantiomers on dopamine transmission and extracellular signal regulated kinase phosphorylation (pERK) in the rat nucleus accumbens shell and core. J Neurochem 2007;102:121-132.
26. Barcia C, Fernandez Barreiro A, Poza M, Herrero MT. Parkinson's disease and inflammatory changes. Neurotox Res 2003;5:411-418.
27. Hirsch EC, Vyas S, Hunot S. Neuroinflammation in Parkinson's disease. Parkinsonism Relat Disord 2012;18(suppl 1):S210-S212.
28. Taylor JM, Main BS, Crack PJ. Neuroinflammation and oxidative stress: co-conspirators in the pathology of Parkinson's disease. Neurochem Int 2013;62:803-819.
29. Halliday GM, Stevens CH. Glia: initiators and progressors of pathology in Parkinson's disease. Mov Disord 2011;26:6-17.
30. Barcia C, Ros CM, Annese V, et al. IFN-γ signaling, with the synergistic contribution of TNF-α, mediates cell specific microglial and astroglial activation in experimental models of Parkinson's disease [serial online]. Cell Death Dis 2011;2:e142.
31. Kerschensteiner M, Meinl E, Hohlfeld R. Neuro-immune crosstalk in CNS diseases. Neuroscience 2009;158:1122-1132.
32. Phani S, Loike JD, Przedborski S. Neurodegeneration and inflammation in Parkinson's disease. Parkinsonism Relat Disord 2012;18(suppl 1):S207-S209.
33. Langston JW, Ballard P, Tetrud JW, Irwin I. Chronic parkinsonism in humans due to a product of meperidine-analog synthesis. Science 1983;219:979-980.
34. Jansen KL. Ecstasy (MDMA) dependence. Drug Alcohol Depend 1999;53:121-124.
35. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates, 3rd ed. San Diego, CA: Academic Press; 2008.
36. Sterio DC. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 1984;134:127-136.
37. Frau L, Borsini F, Wardas J, Khairnar AS, Schintu N, Morelli M. Neuroprotective and anti-inflammatory effects of the adenosine A(2A) receptor antagonist ST1535 in a MPTP mouse model of Parkinson's disease. Synapse 2011;65:181-188.
38. Delle Donne KT, Sonsalla PK. Protection against methamphetamine-induced neurotoxicity to neostriatal dopaminergic neurons by adenosine receptor activation. J Pharmacol Exp Ther 1994;271:1320-1326.
39. Sonsalla PK, Jochnowitz ND, Zeevalk GD, Oostveen JA, Hall ED. Treatment of mice with methamphetamine produces cell loss in the substantia nigra. Brain Res 1996;738:172-175.
40. Obeso JA, Rodriguez-Oroz MC, Goetz CG, et al. Missing pieces in the Parkinson's disease puzzle. Nat Med 2010;16:653-661.
41. Easton N, Marsden CA. Ecstasy: are animal data consistent between species and can they translate to humans? J Psychopharmacol 2006;20:194-210.
42. Chipana C, Garcia-Rates S, Camarasa J, Pubill D, Escubedo E. Different oxidative profile and nicotinic receptor interaction of amphetamine and 3, 4-methylenedioxy-methamphetamine. Neurochem Int 2008;52:401-410.
43. Darvesh AS, Yamamoto BK, Gudelsky GA. Evidence for the involvement of nitric oxide in 3, 4-methylenedioxymethamphetamine-induced serotonin depletion in the rat brain. J Pharmacol Exp Ther 2005;312:694-701.
44. Jayanthi S, Ladenheim B, Andrews AM, Cadet JL. Overexpression of human copper/zinc superoxide dismutase in transgenic mice attenuates oxidative stress caused by methylenedioxymethamphetamine (ecstasy). Neuroscience 1999;91:1379-1387.
45. Lotharius J, O'Malley KL. The parkinsonism-inducing drug 1-methyl-4-phenylpyridinium triggers intracellular dopamine oxidation. A novel mechanism of toxicity. J Biol Chem 2000;275:38581-38588.
46. O'Mathúna B, Farré M, Rostami-Hodjegan A, et al. The consequences of 3, 4-methylenedioxymethamphetamine induced CYP2D6 inhibition in humans. J Clin Psychopharmacol 2008;28:523-529.
47. Mann A, Tyndale RF. Cytochrome P450 2D6 enzyme neuroprotects against 1-methyl-4-phenylpyridinium toxicity in SH-SY5Y neuronal cells. Eur J Neurosci 2010;31:1185-1193.
48. Sisk CL, Zehr JL. Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol 2005;26:163-174.
49. Goffin D, Ali AB, Rampersaud N, et al. Dopamine-dependent tuning of striatal inhibitory synaptogenesis. J Neurosci 2010;30:2935-2950.
50. Fasano C, Poirier A, DesGroseillers L, Trudeau LE. Chronic activation of the D2 dopamine autoreceptor inhibits synaptogenesis in mesencephalic dopaminergic neurons in vitro. Eur J Neurosci 2008;28:1480-1490.
51. Rao A, Richards TL, Simmons D, Zahniser NR, Sorkin A. Epitope-tagged dopamine transporter knock-in mice reveal rapid endocytic trafficking and filopodia targeting of the transporter in dopaminergic axons. FASEB J 2012;26:1921-1933.
52. Gao HM, Zhang F, Zhou H, Kam W, Wilson B, Hong JS. Neuroinflammation and α-synuclein dysfunction potentiate each other, driving chronic progression of neurodegeneration in a mouse model of Parkinson's disease. Environ Health Perspect 2011;119:807-814.
53. O'Callaghan JP, Sriram K. Glial fibrillary acidic protein and related glial proteins as biomarkers of neurotoxicity. Expert Opin Drug Saf 2005;4:433-442.
54. Zhang L, Shirayama Y, Shimizu E, Iyo M, Hashimoto K. Protective effects of minocycline on 3, 4-methylenedioxymethamphetamine-induced neurotoxicity in serotonergic and dopaminergic neurons of mouse brain. Eur J Pharmacol 2006;544:1-9.
55. Thomas DM, Dowgiert J, Geddes TJ, Francescutti-Verbeem D, Liu X, Kuhn DM. Microglial activation is a pharmacologically specific marker for the neurotoxic amphetamines. Neurosci Lett 2004;367:349-354.