The noradrenaline transporter as site of action for the anti-Parkinson drug amantadine

Neuropharmacology

Volumn 62, Issue 4, 2012, Pages 1708-1716

  Sommerauer, Christian ^a   Rebernik, Patrick ^a   Reither, Harald ^a   Nanoff, Christian ^b   Pifl, Christian ^a  

^a Medical University of Vienna   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

Amantadine; Carrier mediated release; NMDA receptor; Noradrenaline transporter; Parkinson's disease; Transport related currents

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; ALPHA 2 ADRENERGIC RECEPTOR; AMANTADINE; AMPHETAMINE; DOPAMINE TRANSPORTER; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NORADRENALIN TRANSPORTER;

ARTICLE; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; DRUG POTENCY; DRUG RECEPTOR BINDING; DRUG UPTAKE; HUMAN; HUMAN CELL; IC 50; NORADRENALIN UPTAKE; PARKINSON DISEASE; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION;

AMANTADINE; ANTIPARKINSON AGENTS; CELL LINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; HEK293 CELLS; HUMANS; N-METHYLASPARTATE; NOREPINEPHRINE PLASMA MEMBRANE TRANSPORT PROTEINS; RECEPTORS, ADRENERGIC, ALPHA-2;

EID: 84856480886     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.11.017     Document Type: Article

References (68)

1. C.H. Adler, M.B. Stern, G. Vernon, and H.I. Hurtig Amantadine in advanced Parkinson's disease: good use of an old drug J. Neurol 244 1997 336 337 (Pubitemid 27212250)
2. A. Bacq, L. Balasse, G. Biala, B. Guiard, A.M. Gardier, A. Schinkel, F. Louis, V. Vialou, M.P. Martres, C. Chevarin, M. Hamon, B. Giros, and S. Gautron Organic cation transporter 2 controls brain norepinephrine and serotonin clearance and antidepressant response Mol. Psychiatry 2011
3. E. Bezard, C. Brefel, F. Tison, H. Peyro-Saint-Paul, P. Ladure, O. Rascol, and C.E. Gross Effect of the alpha 2 adrenoreceptor antagonist, idazoxan, on motor disabilities in MPTP-treated monkey Prog. Neuropsychopharmacol. Biol. Psychiatry 23 1999 1237 1246 (Pubitemid 29524884)
4. E. Bofill-Cardona, O. Kudlacek, Q. Yang, H. Ahorn, M. Freissmuth, and C. Nanoff Binding of calmodulin to the D2-dopamine receptor reduces receptor signaling by arresting the G protein activation switch J. Biol. Chem. 275 2000 32672 32680
5. A.E. Busch, U. Karbach, D. Miska, V. Gorboulev, A. Akhoundova, C. Volk, P. Arndt, J.C. Ulzheimer, M.S. Sonders, C. Baumann, S. Waldegger, F. Lang, and H. Koepsell Human neurons express the polyspecific cation transporter hOCT2, which translocates monoamine neurotransmitters, amantadine, and memantine Mol. Pharmacol 54 1998 342 352 (Pubitemid 28368824)
6. H.S. Chen, J.W. Pellegrini, S.K. Aggarwal, S.Z. Lei, S. Warach, F.E. Jensen, and S.A. Lipton Open-channel block of N-methyl-D-aspartate (NMDA) responses by memantine: therapeutic advantage against NMDA receptor-mediated neurotoxicity J. Neurosci 12 1992 4427 4436
7. D.T. Connolly, M.B. Knight, N.K. Harakas, A.J. Wittwer, and J. Feder Determination of the number of endothelial cells in culture using an acid phosphatase assay Anal. Biochem 152 1986 136 140 (Pubitemid 16140445)
8. W. Danysz, C.G. Parsons, J. Kornhuber, W.J. Schmidt, and G. Quack Aminoadamantanes as NMDA receptor antagonists and antiparkinsonian agents-preclinical studies Neurosci. Biobehav. Rev 21 1997 455 468 (Pubitemid 27255850)
9. J.P. Dunn, J.G. Henkel, and G. Gianutsos Pharmacological activity of amantadine: effect of N-alkyl substitution J. Pharm. Pharmacol 38 1986 353 356 (Pubitemid 16102024)
10. M. Fantin, Y.P. Auberson, and M. Morari Differential effect of NR2A and NR2B subunit selective NMDA receptor antagonists on striato-pallidal neurons: relationship to motor response in the 6-hydroxydopamine model of parkinsonism J. Neurochem 106 2008 957 968
11. L.-O. Farnebo, K. Fuxe, M. Goldstein, B. Hamberger, and U. Ungerstedt Dopamine and noradrenaline releasing action of amantadine in the central and peripheral nervous system: a possible mode in Parkinson's disease Eur. J. Pharmacol. 16 1971 27 38
12. E.A. Fletcher, and P.H. Redfern The effect of amantadine on the uptake of dopamine and noradrenaline by rat brain homogenates J. Pharm. Pharmacol 22 1970 957 959
13. A. Galli, L.J. DeFelice, B.J. Duke, K.R. Moore, and R.D. Blakely Sodium-dependent norepinephrine-induced currents in norepinephrine-transporter- transfected HEK-293 cells blocked by cocaine and antidepressants J. Exp. Biol. 198 1995 2197 2212
14. B. Giros, S. el Mestikawy, N. Godinot, K. Zheng, H. Han, T. Yang-Feng, and M.G. Caron Cloning, pharmacological characterization, and chromosome assignment of the human dopamine transporter Mol. Pharmacol 42 1992 383 390 (Pubitemid 23024654)
15. U. Haacke, G. Sturm, V. Suwer, W. Wesemann, and G. Wildenhahn [The action of 1-aminoadamantane. Comparative studies with isolated nerve endings and thrombocytes on the release of serotonin and dopamine] Arzneimittelforschung 27 1977 1481 1483 (Pubitemid 8128461)
16. R.E. Heikkila, and G. Cohen Evaluation of amantadine as a releasing agent or uptake blocker for H 3 -dopamine in rat brain slices Eur. J. Pharmacol. 20 1972 156 160
17. W.F. Herblin Amantadine and catecholamine uptake Biochem. Pharmacol 21 1972 1993 1995
18. T.J. Huber, D.E. Dietrich, and H.M. Emrich Possible use of amantadine in depression Pharmacopsychiatry 32 1999 47 55 (Pubitemid 29197549)
19. J. Jankovic Atomoxetine for freezing of gait in Parkinson disease J. Neurol. Sci. 284 2009 177 178
20. J. Kornhuber, J. Bormann, M. Hubers, K. Rusche, and P. Riederer Effects of the 1-amino-adamantanes at the MK-801-binding site of the NMDA-receptor-gated ion channel: a human postmortem brain study Eur. J. Pharmacol 206 1991 297 300
21. J. Kornhuber, G. Quack, W. Danysz, K. Jellinger, W. Danielczyk, W. Gsell, and P. Riederer Therapeutic brain concentration of the NMDA receptor antagonist amantadine Neuropharmacology 34 1995 713 721
22. C.M. Kosinski, D.G. Standaert, T.J. Counihan, C.R. Scherzer, J.A. Kerner, L.P. Daggett, G. Velicelebi, J.B. Penney, A.B. Young, and G.B. Landwehrmeyer Expression of N-methyl-D-aspartate receptor subunit mRNAs in the human brain: striatum and globus pallidus J.Comp Neurol. 390 1998 63 74 (Pubitemid 28083646)
23. R. Kuczenski, and D.S. Segal Locomotor effects of acute and repeated threshold doses of amphetamine and methylphenidate: relative roles of dopamine and norepinephrine J. Pharmacol. Exp. Ther 296 2001 876 883 (Pubitemid 32187360)
24. O. Kudlacek, M. Waldhoer, M.U. Kassack, P. Nickel, J.I. Salmi, M. Freissmuth, and C. Nanoff Biased inhibition by a suramin analogue of A1-adenosine receptor/G protein coupling in fused receptor/G protein tandems: the A1-adenosine receptor is predominantly coupled to Goalpha in human brain Naunyn Schmiedebergs Arch. Pharmacol. 365 2002 8 16 (Pubitemid 34045234)
25. K.D. Kuppenbender, D.G. Standaert, T.J. Feuerstein, J.B. Penney Jr., A.B. Young, and G.B. Landwehrmeyer Expression of NMDA receptor subunit mRNAs in neurochemically identified projection and interneurons in the human striatum J. Comp Neurol. 419 2000 407 421 (Pubitemid 30185983)
26. L. Laitinen Desipramine in treatment of Parkinson's disease. A placebo-controlled study Acta Neurol. Scand 45 1969 109 113
27. E.L. Lane, S. Cheetham, and P. Jenner Dopamine uptake inhibitor-induced rotation in 6-hydroxydopamine-lesioned rats involves both D1 and D2 receptors but is modulated through 5-hydroxytryptamine and noradrenaline receptors J. Pharmacol. Exp. Ther 312 2005 1124 1131 (Pubitemid 40293772)
28. F. Lechin, B. van der Dijs, B. Parde-Maldonado, J.E. Rivera, S. Baez, and M.E. Lechin Effects of amantadine on circulating neurotransmitters in healthy subjects J. Neural. Transm 117 2010 293 299
29. A. Lupp, C.H. Lucking, R. Koch, R. Jackisch, and T.J. Feuerstein Inhibitory effects of the antiparkinsonian drugs memantine and amantadine on N-methyl-D-aspartate-evoked acetylcholine release in the rabbit caudate nucleus in vitro J. Pharmacol. Exp. Ther 263 1992 717 724
30. H.S. Lustig, K.V. Ahern, and D.A. Greenberg Antiparkinsonian drugs and in vitro excitotoxicity Brain Res. 597 1992 148 150
31. B.K. Madras, M.A. Fahey, M. Goulet, Z. Lin, J. Bendor, C. Goodrich, P.C. Meltzer, D.R. Elmaleh, E. Livni, A.A. Bonab, and A.J. Fischman Dopamine transporter (DAT) inhibitors alleviate specific parkinsonian deficits in monkeys: association with DAT occupancy in vivo J. Pharmacol. Exp. Ther 319 2006 570 585
32. L. Marsh, K. Biglan, M. Gerstenhaber, and J.R. Williams Atomoxetine for the treatment of executive dysfunction in Parkinson's disease: a pilot open-label study Mov. Disord 24 2009 277 282
33. M. Merello, M.I. Nouzeilles, A. Cammarota, and R. Leiguarda Effect of memantine (NMDA antagonist) on Parkinson's disease: a double-blind crossover randomized study Clin. Neuropharmacol 22 1999 273 276 (Pubitemid 29506396)
34. E. Miller, and H.A. Nieburg Amphetamines, valuable adjunct in treatment of Parkinsonism N.Y. State J. Med 73 1973 2657 2661
35. H. Monyer, R. Sprengel, R. Schoepfer, A. Herb, M. Higuchi, H. Lomeli, N. Burnashev, B. Sakmann, and P.H. Seeburg Heteromeric NMDA receptors: molecular and functional distinction of subtypes Science 256 1992 1217 1221
36. H. Narabayashi, T. Kondo, F. Yokochi, and T. Nagatsu Clinical effects of L-threo-3,4-dihydroxyphenylserine in cases of parkinsonism and pure akinesia Adv. Neurol 45 1987 593 602
37. S.O. Ögren, T. Archer, and C. Johansson Evidence for a selective brain noradrenergic involvement in the locomotor stimulant effects of amphetamine in the rat Neurosci. Lett. 43 1983 327 331 (Pubitemid 14154792)
38. B. Ossola, N. Schendzielorz, S.H. Chen, G.S. Bird, R.K. Tuominen, P.T. Mannisto, and J.S. Hong Amantadine protects dopamine neurons by a dual action: reducing activation of microglia and inducing expression of GNDF in astroglia Neuropharmacology 61 2011 574 582
39. H.J. Otton, M.A. Lawson, M.A. Pannozzo, C.H. Davies, and D.J. Wyllie Quantification of the Mg(2+)-induced potency shift of amantadine and memantine voltage-dependent block in human recombinant GluN1/GluN2A NMDARs Neuropharmacology 60 2011 388 396
40. F.A. Paczkowski, L.J. Bryan-Lluka, P. Porzgen, M. Bruss, and H. Bonisch Comparison of the pharmacological properties of cloned rat, human, and bovine norepinephrine transporters J. Pharmacol. Exp. Ther 290 1999 761 767 (Pubitemid 29344573)
41. R. Papeschi Amantadine may stimulate dopamine and noradrenaline receptors Neuropharmacology 13 1974 77 83
42. J.D. Parkes, D.M. Calver, K.J. Zilkha, and R.P. Knill-Jones Controlled trial of amantadine hydrochloride in Parkinson's disease Lancet 1 1970 259 262
43. J.D. Parkes, D. Tarsy, C.D. Marsden, K.T. Bovill, J.A. Phipps, P. Rose, and P. Asselman Amphetamines in the treatment of Parkinson's disease J. Neurol. Neurosurg. Psychiatry 38 1975 232 237
44. C.G. Parsons, W. Danysz, A. Bartmann, P. Spielmanns, T. Frankiewicz, M. Hesselink, B. Eilbacher, and G. Quack Amino-alkyl-cyclohexanes are novel uncompetitive NMDA receptor antagonists with strong voltage-dependency and fast blocking kinetics: in vitro and in vivo characterization Neuropharmacology 38 1999 85 108 (Pubitemid 29073529)
45. C.G. Parsons, V.A. Panchenko, V.O. Pinchenko, A.Y. Tsyndrenko, and O.A. Krishtal Comparative patch-clamp studies with freshly dissociated rat hippocampal and striatal neurons on the NMDA receptor antagonistic effects of amantadine and memantine Eur. J. Neurosci 8 1996 446 454 (Pubitemid 26090749)
46. C.G. Parsons, G. Quack, I. Bresink, L. Baran, E. Przegalinski, W. Kostowski, P. Krzascik, S. Hartmann, and W. Danysz Comparison of the potency, kinetics and voltage-dependency of a series of uncompetitive NMDA receptor antagonists in vitro with anticonvulsive and motor impairment activity in vivo Neuropharmacology 34 1995 1239 1258
47. C. Pifl, O. Hornykiewicz, B. Giros, and M.G. Caron Catecholamine transporters and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine neurotoxicity: studies comparing the cloned human noradrenaline and human dopamine transporter J. Pharmacol. Exp. Ther 277 1996 1437 1443
48. C. Pifl, M. Khorchide, A. Kattinger, H. Reither, J. Hardy, and O. Hornykiewicz Alpha-Synuclein selectively increases manganese-induced viability loss in SK-N-MC neuroblastoma cells expressing the human dopamine transporter Neurosci. Lett. 354 2004 34 37 (Pubitemid 38041094)
49. 2+ modulates currents generated by the dopamine transporter: parallel effects on amphetamine-induced charge transfer and release Neuropharmacology 46 2004 223 231 (Pubitemid 37532830)
50. E. Pita, and N. Perez Ultrastructural evidence of amantadine and amphetamine noradrenaline releasing action Experientia 33 1977 72 74 (Pubitemid 8028501)
51. G. Quack, M. Hesselink, W. Danysz, and R. Spanagel Microdialysis studies with amantadine and memantine on pharmacokinetics and effects on dopamine turnover J. Neural Transm. Suppl. 46 1995 97 105 (Pubitemid 26043225)
52. A.H. Rajput, A. Rajput, A.E. Lang, R. Kumar, R.J. Uitti, and N. Galvez-Jimenez New use for an old drug: amantadine benefits levodopa-induced dyskinesia Mov Disord. 13 1998 851 (Pubitemid 28429991)
53. O. Rascol, I. Arnulf, P.H. Peyro-Saint, C. Brefel-Courbon, M. Vidailhet, C. Thalamas, A.M. Bonnet, S. Descombes, B. Bejjani, N. Fabre, J.L. Montastruc, and Y. Agid Idazoxan, an alpha-2 antagonist, and L-DOPA-induced dyskinesias in patients with Parkinson's disease Mov Disord. 16 2001 708 713 (Pubitemid 36040852)
54. K.S. Rommelfanger, and D. Weinshenker Norepinephrine: the redheaded stepchild of Parkinson's disease Biochem. Pharmacol. 74 2007 177 190 (Pubitemid 46890808)
55. R.B. Rothman, M.H. Baumann, C.M. Dersch, D.V. Romero, K.C. Rice, F.I. Carroll, and J.S. Partilla Amphetamine-type central nervous system stimulants release norepinephrine more potently than they release dopamine and serotonin Synapse 39 2001 32 41
56. E. Ruzicka, H. Streitova, R. Jech, P. Kanovsky, J. Roth, I. Rektorova, P. Mecir, H. Hortova, M. Bares, B. Hejdukova, and I. Rektor Amantadine infusion in treatment of motor fluctuations and dyskinesias in Parkinson's disease J. Neural Transm. 107 2000 1297 1306
57. J.M. Savola, M. Hill, M. Engstrom, H. Merivuori, S. Wurster, S.G. McGuire, S.H. Fox, A.R. Crossman, and J.M. Brotchie Fipamezole (JP-1730) is a potent alpha2 adrenergic receptor antagonist that reduces levodopa-induced dyskinesia in the MPTP-lesioned primate model of Parkinson's disease Mov Disord. 18 2003 872 883 (Pubitemid 37021161)
58. H. Sawada, T. Oeda, S. Kuno, M. Nomoto, K. Yamamoto, M. Yamamoto, K. Hisanaga, and T. Kawamura Amantadine for dyskinesias in Parkinson's disease: a randomized controlled trial PLoS One 5 2010 e15298
59. B. Scatton, A. Cheramy, M.J. Besson, and J. Glowinski Increased synthesis and release of dopamine in the striatum of the rat after amantadine treatment Eur. J. Pharmacol. 13 1970 131 133
60. R.S. Schwab, A.C. England Jr., D.C. Poskanzer, and R.R. Young Amantadine in the treatment of Parkinson's disease JAMA 208 1969 1168 1170
61. H.H. Sitte, S. Huck, H. Reither, S. Boehm, E.A. Singer, and C. Pifl Carrier-mediated release, transport rates, and charge transfer induced by amphetamine, tyramine, and dopamine in mammalian cells transfected with the human dopamine transporter J. Neurochem 71 1998 1289 1297 (Pubitemid 28390284)
62. P. Solomon, R.S. Mitchell, and M. Prinzmetal The use of benzedrie sulfate in postencephalitic Parkinson's disease J. Am. Med. Assoc. 108 1937 1765 1770
63. T. Takahashi, H. Yamashita, Y.X. Zhang, and S. Nakamura Inhibitory effect of MK-801 on amantadine-induced dopamine release in the rat striatum Brain Res. Bull. 41 1996 363 367 (Pubitemid 26427629)
64. A. Thomas, D. Iacono, A.L. Luciano, K. Armellino, I.A. Di, and M. Onofrj Duration of amantadine benefit on dyskinesia of severe Parkinson's disease J. Neurol. Neurosurg. Psychiatry 75 2004 141 143 (Pubitemid 38091285)
65. J.E. Thornburg, and K.E. Moore Dopamine and norepinephrine uptake by rat brain synaptosomes: relative inhibitory potencies of 1- and d-amphetamine and amantadine Res. Commun. Chem. Pathol. Pharmacol. 5 1973 81 89
66. H. Tohgi, T. Abe, and S. Takahashi The effects of L-threo-3,4- dihydroxyphenylserine on the total norepinephrine and dopamine concentrations in the cerebrospinal fluid and freezing gait in parkinsonian patients J. Neural Transm. Park Dis. Dement. Sect 5 1993 27 34 (Pubitemid 23038787)
67. R.J. Uitti, A.H. Rajput, J.E. Ahlskog, K.P. Offord, D.R. Schroeder, M.M. Ho, M. Prasad, A. Rajput, and P. Basran Amantadine treatment is an independent predictor of improved survival in Parkinson's disease Neurology 46 1996 1551 1556 (Pubitemid 26185770)
68. M.L. Verhagen, D.P. Del, M.P. van den, J. Fang, M.M. Mouradia, and T.N. Chase Amantadine as treatment for dyskinesias and motor fluctuations in Parkinson's disease Neurology 50 1998 1323 1326 (Pubitemid 28240346)