Norepinephrine transporter inhibition with desipramine exacerbates L-DOPA-induced dyskinesia: Role for synaptic dopamine regulation in denervated nigrostriatal terminals

Molecular Pharmacology

Volumn 86, Issue 6, 2014, Pages 675-685

  Chotibut, Tanya ^a   Fields, Victoria ^a   Salvatore, Michael F ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DESIPRAMINE; DOPAMINE; LEVODOPA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NORADRENALIN; NORADRENALIN TRANSPORTER; OXIDOPAMINE; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SYNAPTOSOME; CONTROLLED STUDY; CORPUS STRIATUM; DENERVATION; DISEASE EXACERBATION; DISEASE MODEL; DISEASE SEVERITY; DOPAMINE UPTAKE; DYSKINESIA; ENZYME PHOSPHORYLATION; MALE; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PROTEIN EXPRESSION; RAT; RAT MODEL; REDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; DYSKINESIA, DRUG-INDUCED; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; SPRAGUE DAWLEY RAT; SUBSTANTIA NIGRA; SYNAPSE; TOXICITY;

ANIMALS; CORPUS STRIATUM; DENERVATION; DESIPRAMINE; DOPAMINE; DYSKINESIA, DRUG-INDUCED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; LEVODOPA; MALE; NOREPINEPHRINE PLASMA MEMBRANE TRANSPORT PROTEINS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; SYNAPSES;

EID: 84912059078     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.114.093302     Document Type: Article

References (85)

1. Aarsland D, Pahlhagen S, Ballard CG, Ehrt U, and Svenningsson P (2012) Depression in Parkinson disease-epidemiology, mechanisms and management. Nat Rev Neurol 8:35-47.
2. Ahlskog JE and Muenter MD (2001) Frequency of levodopa-related dyskinesias and motor fluctuations as estimated from the cumulative literature. Mov Disord 16: 448-458.
3. Ahn NG and Klinman JP (1989) Nature of rate-limiting steps in a compartmentalized enzyme system: quantitation of dopamine transport and hydroxylation rates in resealed chromaffin granule ghosts. J Biol Chem 264:12259-12265.
4. Arai R, Karasawa N, Geffard M, and Nagatsu I (1995) L-DOPA is converted to dopamine in serotonergic fibers of the striatum of the rat: a double-labeling immunofluorescence study. Neurosci Lett 195:195-198.
5. Arai A, Tomiyama M, Kannari K, Kimura T, Suzuki C, Watanabe M, Kawarabayashi T, Shen H, and Shoji M (2008) Reuptake of L-DOPA-derived extracellular DA in the striatum of a rodent model of Parkinson's disease via norepinephrine transporter. Synapse 62:632-635.
6. Aubert I, Guigoni C, Hakansson K, Li Q, Dovero S, Barthe N, Bioulac BH, Gross CE, Fisone G, and Bloch B, et al. (2005) Increased D1 dopamine receptor signaling in levodopa-induced dyskinesia. Ann Neurol 57:17-26.
7. Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, and Seitelberger F (1973) Brain dopamine and the syndromes of Parkinson and Huntington: clinical, morphological and neurochemical correlations. J Neurol Sci 20:415-455.
8. Berthet A, Porras G, Doudnikoff E, Stark H, Cador M, Bezard E, and Bloch B (2009) Pharmacological analysis demonstrates dramatic alteration of D1 dopamine receptor neuronal distribution in the rat analog of L-DOPA-induced dyskinesia. J Neurosci 29: 4829-4835.
9. Bezard E, Dovero S, Prunier C, Ravenscroft P, Chalon S, Guilloteau D, Crossman AR, Bioulac B, Brotchie JM, and Gross CE (2001) Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl- 4-phenyl-1,2,3,6-tetrahydropyridine-lesioned macaque model of Parkinson's disease. J Neurosci 21:6853-6861.
10. Bishop C, George JA, Buchta W, Goldenberg AA, Mohamed M, Dickinson SO, Eissa S, and Eskow Jaunarajs KL (2012) Serotonin transporter inhibition attenuates l-DOPA-induced dyskinesia without compromising l-DOPA efficacy in hemiparkinsonian rats. Eur J Neurosci 36:2839-2848.
11. Brichta L, Greengard P, and Flajolet M (2013) Advances in the pharmacological treatment of Parkinson's disease: targeting neurotransmitter systems. Trends Neurosci 36:543-554.
12. Burn DJ (2002) Beyond the iron mask: towards better recognition and treatment of depression associated with Parkinson's disease. Mov Disord 17:445-454.
13. Cai G, Zhen X, Uryu K, and Friedman E (2000) Activation of extracellular signalregulated protein kinases is associated with a sensitized locomotor response to D(2) dopamine receptor stimulation in unilateral 6-hydroxydopamine-lesioned rats. J Neurosci 20:1849-1857.
14. Calne DB and Sandler M (1970) L-Dopa and Parkinsonism. Nature 226:21-24.
15. Carboni E, Tanda GL, Frau R, and Di Chiara G (1990) Blockade of the noradrenaline carrier increases extracellular dopamine concentrations in the prefrontal cortex: evidence that dopamine is taken up in vivo by noradrenergic terminals. J Neurochem 55:1067-1070.
16. Carta M, Lindgren HS, Lundblad M, Stancampiano R, Fadda F, and Cenci MA (2006) Role of striatal L-DOPA in the production of dyskinesia in 6-hydroxydopamine lesioned rats. J Neurochem 96:1718-1727.
17. Carta M, Carlsson T, Kirik D, and Björklund A (2007) Dopamine released from 5-HT terminals is the cause of L-DOPA-induced dyskinesia in parkinsonian rats. Brain 130:1819-1833.
18. Cenci MA, Lee CS, and Björklund A (1998) L-DOPA-induced dyskinesia in the rat is associated with striatal overexpression of prodynorphin- and glutamic acid decarboxylase mRNA. Eur J Neurosci 10:2694-2706.
19. Cenci MA and Lundblad M (2006) Post- versus presynaptic plasticity in L-DOPAinduced dyskinesia. J Neurochem 99:381-392.
20. Cenci MA and Konradi C (2010) Maladaptive striatal plasticity in L-DOPA-induced dyskinesia. Prog Brain Res 183:209-233.
21. Chase TN (1998) Levodopa therapy: consequences of the nonphysiologic replacement of dopamine. Neurology 50:S17-S25.
22. Chotibut T, Apple DM, Jefferis R, and Salvatore MF (2012) Dopamine transporter loss in 6-OHDA Parkinson's model is unmet by parallel reduction in dopamine uptake. PLoS One 7:e52322.
23. Chotibut T, Davis RW, Arnold JC, Frenchek Z, Gurwara S, Bondada V, Geddes JW, and Salvatore MF (2014) Ceftriaxone increases glutamate uptake and reduces striatal tyrosine hydroxylase loss in 6-OHDA Parkinson's model. Mol Neurobiol 49:1282-1292.
24. Dekundy A, Lundblad M, Danysz W, and Cenci MA (2007) Modulation of L-DOPAinduced abnormal involuntary movements by clinically tested compounds: further validation of the rat dyskinesia model. Behav Brain Res 179:76-89.
25. de la Fuente-Fernández R, Sossi V, Huang Z, Furtado S, Lu JQ, Calne DB, Ruth TJ, and Stoessl AJ (2004) Levodopa-induced changes in synaptic dopamine levels increase with progression of Parkinson's disease: implications for dyskinesias. Brain 127:2747-2754.
26. Devos D, Krystkowiak P, Clement F, Dujardin K, Cottencin O, Waucquier N, Ajebbar K, Thielemans B, Kroumova M, and Duhamel A, et al. (2007) Improvement of gait by chronic, high doses of methylphenidate in patients with advanced Parkinson's disease. J Neurol Neurosurg Psychiatry 78:470-475.
27. Devoto P and Flore G (2006) On the origin of cortical dopamine: is it a co-transmitter in noradrenergic neurons? Curr Neuropharmacol 4:115-125.
28. Di Chiara G, Tanda GL, Frau R, and Carboni E (1992) Heterologous monoamine reuptake: lack of transmitter specificity of neuron-specific carriers. Neurochem Int 20:231S-235S.
29. Donaldson I, Dolphin A, Jenner P, Marsden CD, and Pycock C (1976) The roles of noradrenaline and dopamine in contraversive circling behaviour seen after unilateral electrolytic lesions of the locus coeruleus. Eur J Pharmacol 39:179-191.
30. Eskow KL, Gupta V, Alam S, Park JY, and Bishop C (2007) The partial 5-HT(1A) agonist buspirone reduces the expression and development of l-DOPA-induced dyskinesia in rats and improves l-DOPA efficacy. Pharmacol Biochem Behav 87:306-314.
31. Espay AJ, Dwivedi AK, Payne M, Gaines L, Vaughan JE, Maddux BN, Slevin JT, Gartner M, Sahay A, and Revilla FJ, et al. (2011) Methylphenidate for gait impairment in Parkinson disease: a randomized clinical trial. Neurology 76: 1256-1262.
32. Fulceri F, Biagioni F, Ferrucci M, Lazzeri G, Bartalucci A, Galli V, Ruggieri S, Paparelli A, and Fornai F (2007) Abnormal involuntary movements (AIMs) following pulsatile dopaminergic stimulation: severe deterioration and morphological correlates following the loss of locus coeruleus neurons. Brain Res 1135:219-229.
33. Gomez-Mancilla B and Bédard PJ (1993) Effect of nondopaminergic drugs on L-dopainduced dyskinesias in MPTP-treated monkeys. Clin Neuropharmacol 16:418-427.
34. Gresch PJ, Sved AF, Zigmond MJ, and Finlay JM (1995) Local influence of endogenous norepinephrine on extracellular dopamine in rat medial prefrontal cortex. J Neurochem 65:111-116.
35. Guigoni C, Doudnikoff E, Li Q, Bloch B, and Bezard E (2007) Altered D(1) dopamine receptor trafficking in parkinsonian and dyskinetic non-human primates. Neurobiol Dis 26:452-463.
36. Hashimoto W, Kitayama S, Kumagai K, Morioka N, Morita K, and Dohi T (2005) Transport of dopamine and levodopa and their interaction in COS-7 cells heterologously expressing monoamine neurotransmitter transporters and in monoaminergic cell lines PC12 and SK-N-SH. Life Sci 76:1603-1612.
37. Hornykiewicz O and Kish SJ (1987) Biochemical pathophysiology of Parkinson's disease, in Advances in Neurology, Parkinson's Disease (Yahr M and Bergmann K eds) vol. 45, pp 19-34, Raven Press, New York.
38. Hyttel J (1994) Pharmacological characterization of selective serotonin reuptake inhibitors (SSRIs). Int Clin Psychopharmacol 9 (Suppl 1):19-26.
39. Jeannotte AM, McCarthy JG, Redei EE, and Sidhu A (2009) Desipramine modulation of alpha-, gamma-synuclein, and the norepinephrine transporter in an animal model of depression. Neuropsychopharmacology 34:987-998.
40. Kannari K, Yamato H, Shen H, Tomiyama M, Suda T, and Matsunaga M (2001) Activation of 5-HT(1A) but not 5-HT(1B) receptors attenuates an increase in extracellular dopamine derived from exogenously administered L-DOPA in the striatum with nigrostriatal denervation. J Neurochem 76:1346-1353.
41. Kitayama T, Song L, Morita K, Morioka N, and Dohi T (2006) Down-regulation of norepinephrine transporter function induced by chronic administration of desipramine linking to the alteration of sensitivity of local-anesthetics-induced convulsions and the counteraction by co-administration with local anesthetics. Brain Res 1096:97-103.
42. Konradi C, Westin JE, Carta M, Eaton ME, Kuter K, Dekundy A, Lundblad M, and Cenci MA (2004) Transcriptome analysis in a rat model of L-DOPA-induced dyskinesia. Neurobiol Dis 17:219-236.
43. Kubrusly RC, Ventura AL, de Melo Reis RA, Serra GC, Yamasaki EN, Gardino PF, de Mello MC, and de Mello FG (2007) Norepinephrine acts as D1-dopaminergic agonist in the embryonic avian retina: late expression of beta1-adrenergic receptor shifts norepinephrine specificity in the adult tissue. Neurochem Int 50:211-218.
44. Lindgren HS, Andersson DR, Lagerkvist S, Nissbrandt H, and Cenci MA (2010) L-DOPA-induced dopamine efflux in the striatum and the substantia nigra in a rat model of Parkinson's disease: temporal and quantitative relationship to the expression of dyskinesia. J Neurochem 112:1465-1476.
45. Lundblad M, Andersson M, Winkler C, Kirik D, Wierup N, and Cenci MA (2002) Pharmacological validation of behavioural measures of akinesia and dyskinesia in a rat model of Parkinson's disease. Eur J Neurosci 15:120-132.
46. Lundblad M, Picconi B, Lindgren H, and Cenci MA (2004) A model of L-DOPAinduced dyskinesia in 6-hydroxydopamine lesioned mice: relation to motor and cellular parameters of nigrostriatal function. Neurobiol Dis 16:110-123.
47. Madras BK, Fahey MA, Goulet M, Lin Z, Bendor J, Goodrich C, Meltzer PC, Elmaleh DR, Livni E, and Bonab AA, et al. (2006) Dopamine transporter (DAT) inhibitors alleviate specific parkinsonian deficits in monkeys: association with DAT occupancy in vivo. J Pharmacol Exp Ther 319:570-585.
48. Mantovani M, Dooley DJ, Weyerbrock A, Jackisch R, and Feuerstein TJ (2009) Differential inhibitory effects of drugs acting at the noradrenaline and 5-hydroxytryptamine transporters in rat and human neocortical synaptosomes. Br J Pharmacol 158:1848-1856.
49. Marsden CD (1994) Problems with long-term levodopa therapy for Parkinson's disease. Clin Neuropharmacol 17 (Suppl 2):S32-S44.
50. Masana M, Santana N, Artigas F, and Bortolozzi A (2012) Dopamine neurotransmission and atypical antipsychotics in prefrontal cortex: a critical review. Curr Top Med Chem 12:2357-2374.
51. Meissner W, Ravenscroft P, Reese R, Harnack D, Morgenstern R, Kupsch A, Klitgaard H, Bioulac B, Gross CE, and Bezard E, et al. (2006) Increased slow oscillatory activity in substantia nigra pars reticulata triggers abnormal involuntary movements in the 6-OHDA-lesioned rat in the presence of excessive extracellular striatal dopamine. Neurobiol Dis 22:586-598.
52. Miller DW and Abercrombie ED (1999) Role of high-affinity dopamine uptake and impulse activity in the appearance of extracellular dopamine in striatum after administration of exogenous L-DOPA: studies in intact and 6-hydroxydopaminetreated rats. J Neurochem 72:1516-1522.
53. Mones RJ, Elizan TS, and Siegel GJ (1971) Analysis of L-dopa induced dyskinesias in 51 patients with Parkinsonism. J Neurol Neurosurg Psychiatry 34:668-673.
54. Morón JA, Brockington A, Wise RA, Rocha BA, and Hope BT (2002) Dopamine uptake through the norepinephrine transporter in brain regions with low levels of the dopamine transporter: evidence from knock-out mouse lines. J Neurosci 22:389-395.
55. Murugaiah KD and Ukponmwan OE (2003) Functional reactivity of central cholinergic systems following desipramine treatments and sleep deprivation. Naunyn Schmiedebergs Arch Pharmacol 368:294-300.
56. Navailles S, Milan L, Khalki H, Di Giovanni G, Lagière M, and De Deurwaerdère P (2014) Noradrenergic terminals regulate L-DOPA-derived dopamine extracellular levels in a region-dependent manner in Parkinsonian rats. CNS Neurosci Ther 20: 671-678.
57. Olanow CW and Koller WC; American Academy of Neurology (1998) An algorithm (decision tree) for the management of Parkinson's disease: treatment guidelines. Neurology 50(Suppl 3):S1-S57.
58. Pan D, Gatley SJ, Dewey SL, Chen R, Alexoff DA, Ding Y-S, and Fowler JS (1994) Binding of bromine-substituted analogs of methylphenidate to monoamine transporters. Eur J Pharmacol 264:177-182.
59. Pavese N, Evans AH, Tai YF, Hotton G, Brooks DJ, Lees AJ, and Piccini P (2006) Clinical correlates of levodopa-induced dopamine release in Parkinson disease: a PET study. Neurology 67:1612-1617.
60. Pavón N, Martín AB, Mendialdua A, and Moratalla R (2006) ERK phosphorylation and FosB expression are associated with L-DOPA-induced dyskinesia in hemiparkinsonian mice. Biol Psychiatry 59:64-74.
61. Paxinos G and Watson C (1998) Rat Brain in Stereotaxic Coordinates, 4th ed, Academic Press, Waltham, MA.
62. Perez XA, Parameswaran N, Huang LZ, O'Leary KT, and Quik M (2008) Pre-synaptic dopaminergic compensation after moderate nigrostriatal damage in non-human primates. J Neurochem 105:1861-1872.
63. Picconi B, Centonze D, Hakansson K, Bernardi G, Greengard P, Fisone G, Cenci MA, and Calabresi P (2003) Loss of bidirectional striatal synaptic plasticity in L-DOPAinduced dyskinesia. Nat Neurosci 6:501-506.
64. Quik M and Wonnacott S (2011) α6β2∗ and α4β2∗ nicotinic acetylcholine receptors as drug targets for Parkinson's disease. Pharmacol Rev 63:938-966.
65. Rommelfanger KS, Edwards GL, Freeman KG, Liles LC, Miller GW, and Weinshenker D (2007) Norepinephrine loss produces more profound motor deficits than MPTP treatment in mice. Proc Natl Acad Sci USA 104:13804-13809.
66. Sabeti J, Gerhardt GA, and Zahniser NR (2002) Acute cocaine differentially alters accumbens and striatal dopamine clearance in low and high cocaine locomotor responders: behavioral and electrochemical recordings in freely moving rats. J Pharmacol Exp Ther 302:1201-1211.
67. Salvatore MF (2014) ser31 Tyrosine hydroxylase phosphorylation parallels differences in dopamine recovery in nigrostriatal pathway following 6-OHDA lesion. J Neurochem 129:548-558.
68. Salvatore MF, Apparsundaram S, and Gerhardt GA (2003) Decreased plasma membrane expression of striatal dopamine transporter in aging. Neurobiol Aging 24:1147-1154.
69. Salvatore MF, Pruett BS, Spann SL, and Dempsey C (2009) Aging reveals a role for nigral tyrosine hydroxylase ser31 phosphorylation in locomotor activity generation. PLoS One 4:e8466.
70. Salvatore MF, Pruett BS, Dempsey C, and Fields V (2012) Comprehensive profiling of dopamine regulation in substantia nigra and ventral tegmental area. J Vis Exp DOI: 10.3791/4171 [published ahead of print].
71. Santini E, Valjent E, Usiello A, Carta M, Borgkvist A, Girault JA, Hervé D, Greengard P, and Fisone G (2007) Critical involvement of cAMP/DARPP-32 and extracellular signal-regulated protein kinase signaling in L-DOPA-induced dyskinesia. J Neurosci 27:6995-7005.
72. Sarre S, Yuan H, Jonkers N, Van Hemelrijck A, Ebinger G, and Michotte Y (2004) In vivo characterization of somatodendritic dopamine release in the substantia nigra of 6-hydroxydopamine-lesioned rats. J Neurochem 90:29-39.
73. Shin E, Rogers JT, Devoto P, Björklund A, and Carta M (2014) Noradrenaline neuron degeneration contributes to motor impairments and development of L-DOPAinduced dyskinesia in a rat model of Parkinson's disease. Exp Neurol 257:25-38.
74. Siderowf A and Stern M (2003) Update on Parkinson disease. Ann Intern Med 138: 651-658.
75. Snyder GL, Keller RW, Jr, and Zigmond MJ (1990) Dopamine efflux from striatal slices after intracerebral 6-hydroxydopamine: evidence for compensatory hyperactivity of residual terminals. J Pharmacol Exp Ther 253:867-876.
76. Steiger MJ and Quinn NP (1995) Levodopa-based therapy, in Therapy of Parkinson's Disease (Koller WC and Paulson G eds), 2nd ed, pp 105-143, Marcel-Dekker, New York.
77. Takeda H, Inazu M, and Matsumiya T (2002) Astroglial dopamine transport is mediated by norepinephrine transporter. Naunyn Schmiedebergs Arch Pharmacol 366:620-623.
78. Tanaka H, Kannari K, Maeda T, Tomiyama M, Suda T, and Matsunaga M (1999) Role of serotonergic neurons in L-DOPA-derived extracellular dopamine in the striatum of 6-OHDA-lesioned rats. Neuroreport 10:631-634.
79. Tanda G, Pontieri FE, Frau R, and Di Chiara G (1997) Contribution of blockade of the noradrenaline carrier to the increase of extracellular dopamine in the rat prefrontal cortex by amphetamine and cocaine. Eur J Neurosci 9:2077-2085.
80. Teismann P and Schulz JB (2004) Cellular pathology of Parkinson's disease: astrocytes, microglia and inflammation. Cell Tissue Res 318:149-161.
81. Ungerstedt U and Arbuthnott GW (1970) Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res 24:485-493.
82. Wayment HK, Schenk JO, and Sorg BA (2001) Characterization of extracellular dopamine clearance in the medial prefrontal cortex: role of monoamine uptake and monoamine oxidase inhibition. J Neurosci 21:35-44.
83. Westin JE, Vercammen L, Strome EM, Konradi C, and Cenci MA (2007) Spatiotemporal pattern of striatal ERK1/2 phosphorylation in a rat model of L-DOPAinduced dyskinesia and the role of dopamine D1 receptors. Biol Psychiatry 62: 800-810.
84. Yamamoto BK and Novotney S (1998) Regulation of extracellular dopamine by the norepinephrine transporter. J Neurochem 71:274-280.
85. Zhen X, Torres C, Cai G, and Friedman E (2002) Inhibition of protein tyrosine/ mitogen-activated protein kinase phosphatase activity is associated with D2 dopamine receptor supersensitivity in a rat model of Parkinson's disease. Mol Pharmacol 62:1356-1363.