Striatal Glutamate Release in l-DOPA-Induced Dyskinetic Animals

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Nevalainen, Nina ^a   Lundblad, Martin ^b   Gerhardt, Greg A ^c   Strömberg, Ingrid ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; GLUTAMIC ACID; LEVODOPA; OXIDOPAMINE; SEROTONIN 1A RECEPTOR;

AMPEROMETRY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; DYSKINESIA; EVOKED RESPONSE; FEMALE; IN VIVO STUDY; NEUROSECRETION; NEUROTRANSMISSION; NONHUMAN; RAT; STRIATE CORTEX;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ANIMALS; ANTIPARKINSON AGENTS; BENSERAZIDE; CORPUS STRIATUM; DOPAMINE; DRUG COMBINATIONS; DYSKINESIA, DRUG-INDUCED; FEMALE; GLUTAMIC ACID; INJECTIONS, INTRAVENTRICULAR; LEVODOPA; POTASSIUM; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT1A; SEROTONIN RECEPTOR AGONISTS; SIGNAL TRANSDUCTION;

EID: 84873502457     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055706     Document Type: Article

References (77)

1. Ahlskog JE, Muenter MD, (2001) Frequency of levodopa-related dyskinesias and motor fluctuations as estimated from the cumulative literature. Mov Disord 16: 448-458.
2. Brotchie JM, (2005) Nondopaminergic mechanisms in levodopa-induced dyskinesia. Mov Disord 20: 919-931.
3. Arai R, Karasawa N, Geffard M, Nagatsu I, (1995) l-DOPA is converted to dopamine in serotonergic fibers of the striatum of the rat: a double-labeling immunofluorescence study. Neuroscience Letters 195: 195-198.
4. Peter D, Liu Y, Sternini C, de Giorgio R, Brecha N, et al. (1995) Differential expression of two vesicular monoamine transporters. J Neurosci 15: 6179-6188.
5. Yamada H, Aimi Y, Nagatsu I, Taki K, Kudo M, et al. (2007) Immunohistochemical detection of l-DOPA-derived dopamine within serotonergic fibers in the striatum and the substantia nigra pars reticulata in Parkinsonian model rats. Neuroscience Research 59: 1-7.
6. Hollister AS, Breese GR, Mueller RA, (1979) Role of monoamine neural systems in L-dihydroxyphenylalanine-stimulated activity. J Pharmacol Exp Ther 208: 37-43.
7. Arai R, Karasawa N, Nagatsu I, (1996) Aromatic L-amino acid decarboxylase is present in serotonergic fibers of the striatum of the rat. A double-labeling immunofluorescence study. Brain Res 706: 177-179.
8. Ng KY, Chase TN, Colburn RW, Kopin IJ, (1970) L-Dopa-induced release of cerebral monoamines. Science 170: 76-77.
9. Maeda T, Nagata K, Yoshida Y, Kannari K, (2005) Serotonergic hyperinnervation into the dopaminergic denervated striatum compensates for dopamine conversion from exogenously administered l-DOPA. Brain Res 1046: 230-233.
10. Carta M, Carlsson T, Kirik D, Bjorklund A, (2007) Dopamine released from 5-HT terminals is the cause of L-DOPA-induced dyskinesia in parkinsonian rats. Brain 130: 1819-1833.
11. Munoz A, Li Q, Gardoni F, Marcello E, Qin C, et al. (2008) Combined 5-HT1A and 5-HT1B receptor agonists for the treatment of L-DOPA-induced dyskinesia. Brain 131: 3380-3394.
12. Lundblad M, Af Bjerken S, Cenci MA, Pomerleau F, Gerhardt GA, et al. (2009) Chronic intermittent L-DOPA treatment induces changes in dopamine release. J Neurochem 108: 998-1008.
13. Nevalainen N, Af Bjerken S, Lundblad M, Gerhardt GA, Stromberg I, (2011) Dopamine release from serotonergic nerve fibers is reduced in L-DOPA-induced dyskinesia. J Neurochem 118: 12-23.
14. Hornykiewicz O, (1975) Brain monoamines and Parkinsonism. Psychopharmacol Bull 11: 34-35.
15. Kish SJ, Tong J, Hornykiewicz O, Rajput A, Chang LJ, et al. (2008) Preferential loss of serotonin markers in caudate versus putamen in Parkinson's disease. Brain 131: 120-131.
16. Jenner P, Sheehy M, Marsden CD, (1983) Noradrenaline and 5-hydroxytryptamine modulation of brain dopamine function: implications for the treatment of Parkinson's disease. Br J Clin Pharmacol 15 Suppl 2: 277S-289S.
17. Navailles S, Bioulac B, Gross C, De Deurwaerdere P, (2011) Chronic L-DOPA therapy alters central serotonergic function and L-DOPA-induced dopamine release in a region-dependent manner in a rat model of Parkinson's disease. Neurobiol Dis 41: 585-590.
18. Robelet S, Melon C, Guillet B, Salin P, Kerkerian-Le Goff L, (2004) Chronic L-DOPA treatment increases extracellular glutamate levels and GLT1 expression in the basal ganglia in a rat model of Parkinson's disease. Eur J Neurosci 20: 1255-1266.
19. Chase TN, Oh JD, (2000) Striatal dopamine- and glutamate-mediated dysregulation in experimental parkinsonism. Trends Neurosci 23: S86-91.
20. Oh JD, Russell DS, Vaughan CL, Chase TN, (1998) Enhanced tyrosine phosphorylation of striatal NMDA receptor subunits: effect of dopaminergic denervation and L-DOPA administration. Brain Res 813: 150-159.
21. Ahmed I, Bose SK, Pavese N, Ramlackhansingh A, Turkheimer F, et al. (2011) Glutamate NMDA receptor dysregulation in Parkinson's disease with dyskinesias. Brain 134: 979-986.
22. Silverdale MA, Kobylecki C, Hallett PJ, Li Q, Dunah AW, et al. (2010) Synaptic recruitment of AMPA glutamate receptor subunits in levodopa-induced dyskinesia in the MPTP-lesioned nonhuman primate. Synapse 64: 177-180.
23. Calon F, Rajput AH, Hornykiewicz O, Bedard PJ, Di Paolo T, (2003) Levodopa-induced motor complications are associated with alterations of glutamate receptors in Parkinson's disease. Neurobiol Dis 14: 404-416.
24. Darmopil S, Martin AB, De Diego IR, Ares S, Moratalla R, (2009) Genetic inactivation of dopamine D1 but not D2 receptors inhibits L-DOPA-induced dyskinesia and histone activation. Biol Psychiatry 66: 603-613.
25. Santini E, Valjent E, Usiello A, Carta M, Borgkvist A, et al. (2007) Critical involvement of cAMP/DARPP-32 and extracellular signal-regulated protein kinase signaling in L-DOPA-induced dyskinesia. J Neurosci 27: 6995-7005.
26. Westin JE, Vercammen L, Strome EM, Konradi C, Cenci MA, (2007) Spatiotemporal pattern of striatal ERK1/2 phosphorylation in a rat model of L-DOPA-induced dyskinesia and the role of dopamine D1 receptors. Biol Psychiatry 62: 800-810.
27. Aubert I, Guigoni C, Hakansson K, Li Q, Dovero S, et al. (2005) Increased D1 dopamine receptor signaling in levodopa-induced dyskinesia. Ann Neurol 57: 17-26.
28. Mela F, Marti M, Bido S, Cenci MA, Morari M, (2012) In vivo evidence for a differential contribution of striatal and nigral D1 and D2 receptors to L-DOPA induced dyskinesia and the accompanying surge of nigral amino acid levels. Neurobiol Dis 45: 573-582.
29. Rylander D, Iderberg H, Li Q, Dekundy A, Zhang J, et al. (2010) A mGluR5 antagonist under clinical development improves L-DOPA-induced dyskinesia in parkinsonian rats and monkeys. Neurobiol Dis 39: 352-361.
30. Papa SM, Chase TN, (1996) Levodopa-induced dyskinesias improved by a glutamate antagonist in Parkinsonian monkeys. Ann Neurol 39: 574-578.
31. Kobylecki C, Cenci MA, Crossman AR, Ravenscroft P, (2010) Calcium-permeable AMPA receptors are involved in the induction and expression of l-DOPA-induced dyskinesia in Parkinson's disease. J Neurochem 114: 499-511.
32. Konitsiotis S, Blanchet PJ, Verhagen L, Lamers E, Chase TN, (2000) AMPA receptor blockade improves levodopa-induced dyskinesia in MPTP monkeys. Neurology 54: 1589-1595.
33. Hadj Tahar A, Gregoire L, Darre A, Belanger N, Meltzer L, et al. (2004) Effect of a selective glutamate antagonist on L-dopa-induced dyskinesias in drug-naive parkinsonian monkeys. Neurobiol Dis 15: 171-176.
34. Blanchet PJ, Konitsiotis S, Chase TN, (1998) Amantadine reduces levodopa-induced dyskinesias in parkinsonian monkeys. Mov Disord 13: 798-802.
35. Mela F, Marti M, Dekundy A, Danysz W, Morari M, et al. (2007) Antagonism of metabotropic glutamate receptor type 5 attenuates l-DOPA-induced dyskinesia and its molecular and neurochemical correlates in a rat model of Parkinson's disease. J Neurochem 101: 483-497.
36. Bibbiani F, Oh JD, Kielaite A, Collins MA, Smith C, et al. (2005) Combined blockade of AMPA and NMDA glutamate receptors reduces levodopa-induced motor complications in animal models of PD. Exp Neurol 196: 422-429.
37. Verhagen Metman L, Del Dotto P, van den Munckhof P, Fang J, Mouradian MM, et al. (1998) Amantadine as treatment for dyskinesias and motor fluctuations in Parkinson's disease. Neurology 50: 1323-1326.
38. Luginger E, Wenning GK, Bosch S, Poewe W, (2000) Beneficial effects of amantadine on L-dopa-induced dyskinesias in Parkinson's disease. Mov Disord 15: 873-878.
39. DeFelipe J, Arellano JI, Gomez A, Azmitia EC, Munoz A, (2001) Pyramidal cell axons show a local specialization for GABA and 5-HT inputs in monkey and human cerebral cortex. J Comp Neurol 433: 148-155.
40. Antonelli T, Fuxe K, Tomasini MC, Bartoszyk GD, Seyfried CA, et al. (2005) Effects of sarizotan on the corticostriatal glutamate pathways. Synapse 58: 193-199.
41. Mignon LJ, Wolf WA, (2005) 8-hydroxy-2-(di-n-propylamino)tetralin reduces striatal glutamate in an animal model of Parkinson's disease. Neuroreport 16: 699-703.
42. Bamford NS, Zhang H, Schmitz Y, Wu NP, Cepeda C, et al. (2004) Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron 42: 653-663.
43. Ungerstedt U, Arbuthnott GW, (1970) Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain research 24: 485-493.
44. Hudson JL, van Horne CG, Stromberg I, Brock S, Clayton J, et al. (1993) Correlation of apomorphine- and amphetamine-induced turning with nigrostriatal dopamine content in unilateral 6-hydroxydopamine lesioned rats. Brain Res 626: 167-174.
45. Cenci MA, Lundblad M (2007) Ratings of L-DOPA-induced dyskinesia in the unilateral 6-OHDA lesion model of Parkinson's disease in rats and mice. Curr Protoc Neurosci Chapter 9: Unit 9 25.
46. Hascup KN, Rutherford EC, Quintero JE, Day BK, Nickell JR, et al. (2007) Second-by-Second Measures of L-Glutamate and Other Neurotransmitters Using Enzyme-Based Microelectrode Arrays. In: Michael AC, Borland LM, editors. Electrochemical Methods for Neuroscience. Boca Raton (FL).
47. Burmeister JJ, Moxon K, Gerhardt GA, (2000) Ceramic-based multisite microelectrodes for electrochemical recordings. Anal Chem 72: 187-192.
48. Burmeister JJ, Pomerleau F, Palmer M, Day BK, Huettl P, et al. (2002) Improved ceramic-based multisite microelectrode for rapid measurements of L-glutamate in the CNS. J Neurosci Methods 119: 163-171.
49. Burmeister JJ, Gerhardt GA, (2001) Self-referencing ceramic-based multisite microelectrodes for the detection and elimination of interferences from the measurement of L-glutamate and other analytes. Anal Chem 73: 1037-1042.
50. Day BK, Pomerleau F, Burmeister JJ, Huettl P, Gerhardt GA, (2006) Microelectrode array studies of basal and potassium-evoked release of L-glutamate in the anesthetized rat brain. J Neurochem 96: 1626-1635.
51. Jonkers N, Sarre S, Ebinger G, Michotte Y, (2002) MK801 suppresses the L-DOPA-induced increase of glutamate in striatum of hemi-Parkinson rats. Brain Res 926: 149-155.
52. Lindefors N, Ungerstedt U, (1990) Bilateral regulation of glutamate tissue and extracellular levels in caudate-putamen by midbrain dopamine neurons. Neurosci Lett 115: 248-252.
53. Holmer HK, Keyghobadi M, Moore C, Meshul CK, (2005) l-dopa-induced reversal in striatal glutamate following partial depletion of nigrostriatal dopamine with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neuroscience 136: 333-341.
54. Bianchi L, Galeffi F, Bolam JP, Della Corte L, (2003) The effect of 6-hydroxydopamine lesions on the release of amino acids in the direct and indirect pathways of the basal ganglia: a dual microdialysis probe analysis. Eur J Neurosci 18: 856-868.
55. Bido S, Marti M, Morari M, (2011) Amantadine attenuates levodopa-induced dyskinesia in mice and rats preventing the accompanying rise in nigral GABA levels. J Neurochem 118: 1043-1055.
56. Corsi C, Pinna A, Gianfriddo M, Melani A, Morelli M, et al. (2003) Adenosine A2A receptor antagonism increases striatal glutamate outflow in dopamine-denervated rats. Eur J Pharmacol 464: 33-38.
57. Meshul CK, Emre N, Nakamura CM, Allen C, Donohue MK, et al. (1999) Time-dependent changes in striatal glutamate synapses following a 6-hydroxydopamine lesion. Neuroscience 88: 1-16.
58. Dupre KB, Ostock CY, Eskow Jaunarajs KL, Button T, Savage LM, et al. (2011) Local modulation of striatal glutamate efflux by serotonin 1A receptor stimulation in dyskinetic, hemiparkinsonian rats. Exp Neurol 229: 288-299.
59. McGeorge AJ, Faull RL, (1987) The organization and collateralization of corticostriate neurones in the motor and sensory cortex of the rat brain. Brain Res 423: 318-324.
60. Fisher RS, Shiota C, Levine MS, Hull CD, Buchwald NA, (1984) Interhemispheric organization of corticocaudate projections in the cat: a retrograde double-labelling study. Neurosci Lett 48: 369-373.
61. Jones EG, Coulter JD, Burton H, Porter R, (1977) Cells of origin and terminal distribution of corticostriatal fibers arising in the sensory-motor cortex of monkeys. J Comp Neurol 173: 53-80.
62. Wilson CJ, (1987) Morphology and synaptic connections of crossed corticostriatal neurons in the rat. J Comp Neurol 263: 567-580.
63. Breit S, Martin A, Lessmann L, Cerkez D, Gasser T, et al. (2008) Bilateral changes in neuronal activity of the basal ganglia in the unilateral 6-hydroxydopamine rat model. J Neurosci Res 86: 1388-1396.
64. Del Dotto P, Pavese N, Gambaccini G, Bernardini S, Metman LV, et al. (2001) Intravenous amantadine improves levadopa-induced dyskinesias: an acute double-blind placebo-controlled study. Mov Disord 16: 515-520.
65. Lundblad M, Andersson M, Winkler C, Kirik D, Wierup N, et al. (2002) Pharmacological validation of behavioural measures of akinesia and dyskinesia in a rat model of Parkinson's disease. Eur J Neurosci 15: 120-132.
66. Paquette MA, Anderson AM, Lewis JR, Meshul CK, Johnson SW, et al. (2010) MK-801 inhibits L-DOPA-induced abnormal involuntary movements only at doses that worsen parkinsonism. Neuropharmacol 58: 1002-1008.
67. Morin N, Gregoire L, Gomez-Mancilla B, Gasparini F, Di Paolo T, (2010) Effect of the metabotropic glutamate receptor type 5 antagonists MPEP and MTEP in parkinsonian monkeys. Neuropharmacol 58: 981-986.
68. Arai A, Kannari K, Shen H, Maeda T, Suda T, et al. (2003) Amantadine increases L-DOPA-derived extracellular dopamine in the striatum of 6-hydroxydopamine-lesioned rats. Brain Res 972: 229-234.
69. King JM, Muthian G, Mackey V, Smith M, Charlton C, (2011) L-Dihydroxyphenylalanine modulates the steady-state expression of mouse striatal tyrosine hydroxylase, aromatic L-amino acid decarboxylase, dopamine and its metabolites in an MPTP mouse model of Parkinson's disease. Life Sci 89: 638-643.
70. Iravani MM, Tayarani-Binazir K, Chu WB, Jackson MJ, Jenner P, (2006) In 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primates, the selective 5-hydroxytryptamine 1a agonist (R)-(+)-8-OHDPAT inhibits levodopa-induced dyskinesia but only with\ increased motor disability. J Pharmacol Exp Ther 319: 1225-1234.
71. Goodwin GM, De Souza RJ, Green AR, Heal DJ, (1987) The pharmacology of the behavioural and hypothermic responses of rats to 8-hydroxy-2-(di-n-propylamino)tetralin (8-OH-DPAT). Psychopharmacology (Berl) 91: 506-511.
72. Yamada J, Sugimoto Y, Horisaka K, (1988) The behavioural effects of 8-hydroxy-2-(di-n-propylamino)tetralin (8-OH-DPAT) in mice. Eur J Pharmacol 154: 299-304.
73. Ostock CY, Dupre KB, Jaunarajs KL, Walters H, George J, et al. (2011) Role of the primary motor cortex in L-Dopa-induced dyskinesia and its modulation by 5-HT1A receptor stimulation. Neuropharmacol 61: 753-760.
74. Nahimi A, Holtzermann M, Landau AM, Simonsen M, Jakobsen S, et al. (2012) Serotonergic modulation of receptor occupancy in rats treated with L-DOPA after unilateral 6-OHDA lesioning. J Neurochem 120: 806-817.
75. Sprouse JS, Aghajanian GK, (1987) Electrophysiological responses of serotoninergic dorsal raphe neurons to 5-HT1A and 5-HT1B agonists. Synapse 1: 3-9.
76. Dupre KB, Eskow KL, Steiniger A, Klioueva A, Negron GE, et al. (2008) Effects of coincident 5-HT1A receptor stimulation and NMDA receptor antagonism on L-DOPA-induced dyskinesia and rotational behaviors in the hemi-parkinsonian rat. Psychopharmacology 199: 99-108.
77. Fiorentini C, Rizzetti MC, Busi C, Bontempi S, Collo G, et al. (2006) Loss of synaptic D1 dopamine/N-methyl-D-aspartate glutamate receptor complexes in L-DOPA-induced dyskinesia in the rat. Mol Pharmacol 69: 805-812.