L-DOPA-treatment in primates disrupts the expression of A2A adenosine-CB1 cannabinoid-D2 dopamine receptor heteromers in the caudate nucleus

Neuropharmacology

Volumn 79, Issue , 2014, Pages 90-100

  Bonaventura, Jordi ^a,b   Rico, Alberto J ^b,c   Moreno, Estefanía ^a,b   Sierra, Salvador ^b,c   Sánchez, Marta ^a,b   Luquin, Natasha ^b,c   Farré, Daniel ^a,b   Müller, Christa E ^d   Martínez Pinilla, Eva ^c   Cortés, Antoni ^a,b   Mallol, Josefa ^a,b   Armentero, Marie Therese ^e   Pinna, Annalisa ^f   Canela, Enric I ^a,b   Lluís, Carme ^a,b   McCormick, Peter J ^a,b   Lanciego, José L ^b,c   Casadó, Vicent ^a,b   Franco, Rafael ^a,c  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

^c UNIVERSITY OF NAVARRA   (Spain)

^d UNIVERSITY OF BONN   (Germany)

^e C MONDINO NATIONAL NEUROLOGICAL INSTITUTE   (Italy)

^f CNR   (Italy)

Author keywords

Caudate; Dopamine; l Dopa; Parkinson's disease; Putamen; Receptor heteromer; Striatum

Indexed keywords

ADENOSINE A2A RECEPTOR; BENSERAZIDE PLUS LEVODOPA; CANNABINOID 1 RECEPTOR; DOPAMINE; DOPAMINE 2 RECEPTOR; LEVODOPA; 1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ADENOSINE A2 RECEPTOR AGONIST; ADENOSINE A2 RECEPTOR ANTAGONIST; ANTIPARKINSON AGENT; DOPAMINE RECEPTOR BLOCKING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BRAIN REGION; CAUDATE NUCLEUS; CONTROLLED STUDY; CORPUS STRIATUM; DRUG EFFICACY; DRUG RECEPTOR BINDING; DRUG RESPONSE; DYSKINESIA; LIGAND BINDING; MALE; NEUROTRANSMISSION; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; MACACA FASCICULARIS; METABOLISM; PARKINSONIAN DISORDERS; PUTAMEN;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ADENOSINE A2 RECEPTOR AGONISTS; ADENOSINE A2 RECEPTOR ANTAGONISTS; ANIMALS; ANTIPARKINSON AGENTS; CAUDATE NUCLEUS; DOPAMINE; DOPAMINE ANTAGONISTS; LEVODOPA; MACACA FASCICULARIS; MALE; PARKINSONIAN DISORDERS; PUTAMEN; RECEPTOR, ADENOSINE A2A; RECEPTOR, CANNABINOID, CB1; RECEPTORS, DOPAMINE D2;

EID: 84890068169     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.10.036     Document Type: Article

References (70)

1. R.L. Albin, A.B. Young, and J.B. Penney The functional anatomy of basal ganglia disorders Trends Neurosci. 12 10 1989 366 375
2. G.E. Alexander, and M.D. Crutcher Functional architecture of basal ganglia circuits: neural substrates of parallel processing Trends Neurosci. 13 7 1990 266 271
3. M.T. Armentero, A. Pinna, S. Ferré, J.L. Lanciego, C.E. Muller, and R. Franco Past, present and future of A(2A) adenosine receptor antagonists in the therapy of Parkinson's disease Pharmacol. Ther. 132 3 2011 280 299
4. E. Bezard, S. Dovero, C. Prunier, P. Ravenscroft, S. Chalon, and D. Guilloteau 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 17 2001 6853 6861
5. B2 form functional heteromers in brain J. Biol. Chem. 287 25 2012 20851 20865
6. 2 receptor-receptor heteromerization: qualitative and quantitative assessment by fluorescence and bioluminescence energy transfer J. Biol. Chem. 278 47 2003 46741 46749
7. P. Carriba, G. Navarro, F. Ciruela, S. Ferré, V. Casadó, and L. Agnati Detection of heteromerization of more than two proteins by sequential BRET-FRET Nat. Methods 5 8 2008 727 733
8. V. Casadó, C. Canti, J. Mallol, E.I. Canela, C. Lluis, and R. Franco Solubilization of A1 adenosine receptor from pig brain: characterization and evidence of the role of the cell membrane on the coexistence of high- and low-affinity states J. Neurosci. Res. 26 4 1990 461 473
9. V. Casadó, A. Cortes, F. Ciruela, J. Mallol, S. Ferré, and C. Lluis Old and new ways to calculate the affinity of agonists and antagonists interacting with G-protein-coupled monomeric and dimeric receptors: the receptor-dimer cooperativity index Pharmacol. Ther. 116 3 2007 343 354
10. V. Casadó, C. Ferrada, J. Bonaventura, E. Gracia, J. Mallol, and E.I. Canela Useful pharmacological parameters for G-protein-coupled receptor homodimers obtained from competition experiments. Agonist-antagonist binding modulation Biochem. Pharmacol. 78 12 2009 1456 1463
11. M.A. Cenci L-DOPA-induced dyskinesia: cellular mechanisms and approaches to treatment Parkinsonism Relat. Disord. 13 Suppl. 3 2007 S263 S267
12. M.B. Dalrymple, K.D. Pfleger, and K.A. Eidne G protein-coupled receptor dimers: functional consequences, disease states and drug targets Pharmacol. Ther. 118 3 2008 359 371
13. R. de la Fuente-Fernandez, V. Sossi, Z. Huang, S. Furtado, J.Q. Lu, and D.B. Calne Levodopa-induced changes in synaptic dopamine levels increase with progression of Parkinson's disease: implications for dyskinesias Brain 127 Pt 12 2004 2747 2754
14. M.R. DeLong Primate models of movement disorders of basal ganglia origin Trends Neurosci. 13 7 1990 281 285
15. 2 receptors in rat striatal membranes Proc. Natl. Acad. Sci. U. S. A. 88 16 1991 7238 7241
16. 2 receptors in the neostriatum Brain Res. 594 1 1992 124 130
17. 2 receptor-receptor heteromers. Targets for neuro-psychiatric disorders Parkinsonism Relat. Disord. 10 5 2004 265 271
18. S. Ferré, F. Ciruela, A.S. Woods, C. Lluis, and R. Franco Functional relevance of neurotransmitter receptor heteromers in the central nervous system Trends Neurosci. 30 9 2007 440 446
19. S. Ferré, R. Baler, M. Bouvier, M.G. Caron, L.A. Devi, and T. Durroux Building a new conceptual framework for receptor heteromers Nat. Chem. Biol. 5 3 2009 131 134
20. S. Ferré, S.R. Goldberg, C. Lluis, and R. Franco Looking for the role of cannabinoid receptor heteromers in striatal function Neuropharmacology 56 Suppl. 1 2009 226 234
21. S. Ferré, C. Quiroz, M. Orru, X. Guitart, G. Navarro, and A. Cortés Adenosine A(2A) receptors and A(2A) receptor heteromers as key players in striatal function Front Neuroanat. 5 2011 36
22. S.H. Fox, A.E. Lang, and J.M. Brotchie Translation of nondopaminergic treatments for levodopa-induced dyskinesia from MPTP-lesioned nonhuman primates to phase IIa clinical studies: keys to success and roads to failure Mov. Disord. 21 10 2006 1578 1594
23. R. Franco, V. Casadó, J. Mallol, C. Ferrada, S. Ferré, and K. Fuxe The two-state dimer receptor model: a general model for receptor dimers Mol. Pharmacol. 69 6 2006 1905 1912
24. K. Fuxe, S. Ferré, S. Genedani, R. Franco, and L.F. Agnati Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function Physiol. Behav. 92 1-2 2007 210 217
25. M. Garcia-Arencibia, C. Garcia, and J. Fernandez-Ruiz Cannabinoids and Parkinson's disease CNS Neurol. Disord. Drug Targets 8 6 2009 432 439
26. S. Gines, J. Hillion, M. Torvinen, S. Le Crom, V. Casadó, and E.I. Canela Dopamine D1 and adenosine A1 receptors form functionally interacting heteromeric complexes Proc. Natl. Acad. Sci. U. S. A. 97 15 2000 8606 8611
27. C.G. Goetz, G.T. Stebbins, H.M. Shale, A.E. Lang, D.A. Chernik, and T.A. Chmura Utility of an objective dyskinesia rating scale for Parkinson's disease: inter- and intrarater reliability assessment Mov. Disord. 9 4 1994 390 394
28. S. Gonzalez, D. Moreno-Delgado, E. Moreno, K. Perez-Capote, R. Franco, and J. Mallol Circadian-related heteromerization of adrenergic and dopamine D(4) receptors modulates melatonin synthesis and release in the pineal gland PLoS Biol. 10 6 2012 e1001347
29. M.D. Gottwald, and M.J. Aminoff Therapies for dopaminergic-induced dyskinesias in Parkinson disease Ann. Neurol. 69 6 2011 919 927
30. E. Gracia, E. Moreno, A. Cortés, C. Lluís, J. Mallol, and P.J. McCormick Homodimerization of adenosine A1 receptors in brain cortex explains the biphasic effect of caffeine Neuropharmacology 71 2013 56 69
31. 2A adenosine receptors Nat. Neurosci. 13 8 2010 958 966
32. 2 receptors J. Biol. Chem. 277 20 2002 18091 18097
33. O. Hornykiewicz A brief history of levodopa J. Neurol. 257 Suppl. 2 2010 S249 S252
34. M.M. Iravani, and P. Jenner Mechanisms underlying the onset and expression of levodopa-induced dyskinesia and their pharmacological manipulation J. Neural Transm. 118 12 2011 1661 1690
35. W.C. Koller Levodopa in the treatment of Parkinson's disease Neurology 55 11 Suppl. 4 2000 S2 S7 discussion S8-12
36. A.V. Kravitz, B.S. Freeze, P.R. Parker, K. Kay, M.T. Thwin, and K. Deisseroth Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry Nature 466 7306 2010 622 626
37. A. Kumar, S. Mann, V. Sossi, T.J. Ruth, A.J. Stoessl, and M. Schulzer [11C]DTBZ-PET correlates of levodopa responses in asymmetric Parkinson's disease Brain 126 Pt 12 2003 2648 2655
38. R. Kurlan, M.H. Kim, and D.M. Gash Oral levodopa dose-response study in MPTP-induced hemiparkinsonian monkeys: assessment with a new rating scale for monkey parkinsonism Mov. Disord. 6 2 1991 111 118
39. J.L. Lanciego, M.C. Rodriguez-Oroz, F.J. Blesa, L. Alvarez-Erviti, J. Guridi, and P. Barroso-Chinea Lesion of the centromedian thalamic nucleus in MPTP-treated monkeys Mov. Disord. 23 5 2008 708 715
40. J.L. Lanciego, and A. Vazquez The basal ganglia and thalamus of the long-tailed macaque in stereotaxic coordinates. A template atlas based on coronal, sagittal and horizontal brain sections Brain Struct. Funct. 217 2 2012 613 666
41. J.W. Langston, H. Widner, C.G. Goetz, D. Brooks, S. Fahn, and T. Freeman Core assessment program for intracerebral transplantations (CAPIT) Mov. Disord. 7 1 1992 2 13
42. B1 receptor binding and activation of GTP-binding proteins in the basal ganglia of patients with Parkinson's syndrome and of MPTP-treated marmosets Eur. J. Neurosci. 14 11 2001 1827 1832
43. S.J. Lewis, M.A. Caldwell, and R.A. Barker Modern therapeutic approaches in Parkinson's disease Expert Rev. Mol. Med. 5 10 2003 1 20
44. 2 heteromers. A combined neurochemical and behavioral analysis Neuropharmacology 54 5 2008 815 823
45. A.T. Mattfeld, M.A. Gluck, and C.E. Stark Functional specialization within the striatum along both the dorsal/ventral and anterior/posterior axes during associative learning via reward and punishment Learn Mem. 18 11 2011 703 711
46. C. Mazzucchelli, C. Vantaggiato, A. Ciamei, S. Fasano, P. Pakhotin, and W. Krezel Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory Neuron 34 5 2002 807 820
47. M. Mishina, K. Ishiwata, M. Naganawa, Y. Kimura, S. Kitamura, and M. Suzuki Adenosine A(2A) receptors measured with [C]TMSX PET in the striata of Parkinson's disease patients PLoS One 6 2 2011 e17338
48. 2A receptors in parkinsonian motor impairment and l-DOPA-induced motor complications Prog. Neurobiol. 83 5 2007 293 309
49. 2A receptors: a new strategy for basal ganglia disorders Recent Pat. CNS Drug Discov. 2 1 2007 1 21
50. G. Navarro, S. Ferré, A. Cordomi, E. Moreno, J. Mallol, and V. Casadó Interactions between intracellular domains as key determinants of the quaternary structure and function of receptor heteromers J. Biol. Chem. 285 35 2010 27346 27359
51. J.A. Obeso, M.C. Rodriguez-Oroz, M. Rodriguez, J.L. Lanciego, J. Artieda, and N. Gonzalo Pathophysiology of the basal ganglia in Parkinson's disease Trends Neurosci. 23 10 Suppl. 2000 S8 19
52. J.A. Obeso, M.C. Rodriguez-Oroz, B. Benitez-Temino, F.J. Blesa, J. Guridi, and C. Marin Functional organization of the basal ganglia: therapeutic implications for Parkinson's disease Mov. Disord. 23 Suppl. 3 2008 S548 S559
53. J.M. Orgado, J. Fernandez-Ruiz, and J. Romero The endocannabinoid system in neuropathological states Int. Rev. Psychiatry 21 2 2009 172 180
54. M. Orru, J. Bakešová, M. Brugarolas, C. Quiroz, V. Beaumont, S.R. Goldberg, C. Lluís, A. Cortés, R. Franco, V. Casadó, E.I. Canela, and S. Ferré Striatal pre- and postsynaptic profile of adenosine A(2A) receptor antagonists PLoS One 6 1 2011 Jan 11
55. J.P. Pin, R. Neubig, M. Bouvier, L. Devi, M. Filizola, and J.A. Javitch International Union of Basic and Clinical Pharmacology. LXVII. Recommendations for the recognition and nomenclature of G protein-coupled receptor heteromultimers Pharmacol. Rev. 59 1 2007 5 13
56. 2A adenosine receptors positively modulates turning behaviour and c-Fos expression induced by D1 agonists in dopamine-denervated rats Eur. J. Neurosci. 8 6 1996 1176 1181
57. 2A receptor antagonists for Parkinson's disease Expert Opin. Investig. Drugs 18 11 2009 1619 1631
58. A. Pisani, F. Fezza, S. Galati, N. Battista, S. Napolitano, and A. Finazzi-Agro High endogenous cannabinoid levels in the cerebrospinal fluid of untreated Parkinson's disease patients Ann. Neurol. 57 5 2005 777 779
59. A.E. Pollack, and J.S. Fink Synergistic interaction between an adenosine antagonist and a D1 dopamine agonist on rotational behavior and striatal c-Fos induction in 6-hydroxydopamine-lesioned rats Brain Res. 743 1-2 1996 124 130
60. O. Rascol, A. Lozano, M. Stern, and W. Poewe Milestones in Parkinson's disease therapeutics Mov. Disord. 26 6 2011 1072 1082
61. A.J. Rico, P. Barroso-Chinea, L. Conte-Perales, E. Roda, V. Gomez-Bautista, and M. Gendive A direct projection from the subthalamic nucleus to the ventral thalamus in monkeys Neurobiol. Dis. 39 3 2010 381 392
62. B1 receptor mRNA levels in the caudate-putamen Life Sci. 66 6 2000 485 494
63. 2A receptors in the rat central nervous system J. Comp. Neurol. 401 2 1998 163 186
64. O. Sagredo, M. Garcia-Arencibia, E. de Lago, S. Finetti, A. Decio, and J. Fernandez-Ruiz Cannabinoids and neuroprotection in basal ganglia disorders Mol. Neurobiol. 36 1 2007 82 91
65. 2A receptors and basal ganglia physiology Prog. Neurobiol. 83 5 2007 277 292
66. 2A receptors in Parkinson's disease Trends Neurosci. 29 11 2006 647 654
67. O. Soderberg, K.J. Leuchowius, M. Gullberg, M. Jarvius, I. Weibrecht, and L.G. Larsson Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay Methods 45 3 2008 227 232
68. 3 heteromeric complexes Mol. Pharmacol. 67 2 2005 400 407
69. 2A receptor complexes in the striatum Biotechniques 51 2 2011 111 118
70. A.R. Troiano, R. de la Fuente-Fernandez, V. Sossi, M. Schulzer, E. Mak, and T.J. Ruth PET demonstrates reduced dopamine transporter expression in PD with dyskinesias Neurology 72 14 2009 1211 1216