Adenosine a2a-d2 receptor-receptor interactions in putative heteromers in the regulation of the striato-pallidal gaba pathway: Possible relevance for parkinson’s disease and its treatment

Current Protein and Peptide Science

Volumn 15, Issue 7, 2014, Pages 673-680

  Beggiato, Sarah ^a,b   Antonelli, Tiziana ^a,b   Tomasini, Maria C ^a,b   Borelli, Andrea C ^a   Agnati, Luigi F ^a   Tanganelli, Sergio ^a,b   Fuxe, Kjell ^c   Ferraro, Luca ^a,b  

^a UNIVERSITY OF FERRARA   (Italy)

^b IRET Foundation   (Italy)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

A2A receptor antagonists; D2 receptor agonists; GABA and glutamate levels; Heteromeric receptor complexes; Microdialysis; Parkinson's disease; Receptor receptor interaction

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; ADENOSINE A2A RECEPTOR; ADENOSINE A2A RECEPTOR ANTAGONIST; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOPAMINE 2 RECEPTOR; DOPAMINE 2 RECEPTOR STIMULATING AGENT; G PROTEIN COUPLED RECEPTOR; GLUTAMIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; LEVODOPA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; QUINPIROLE; ADENOSINE A2 RECEPTOR ANTAGONIST; ANTIPARKINSON AGENT;

ARTICLE; BASAL GANGLION; CHROMATIN IMMUNOPRECIPITATION; COGNITIVE DEFECT; CORPUS STRIATUM; DYSKINESIA; ELECTROPHYSIOLOGICAL PROCEDURES; GLOBUS PALLIDUS; HYPOKINESIA; LOCOMOTION; MICRODIALYSIS; MOLECULAR INTERACTION; NERVE EXCITABILITY; NEUROMODULATION; NEUROTRANSMISSION; PARKINSON DISEASE; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; SUBSTANTIA NIGRA PARS COMPACTA; SUBSTANTIA NIGRA PARS RETICULATA; SUBTHALAMIC NUCLEUS; ANIMAL; CHEMISTRY; DRUG DEVELOPMENT; HUMAN; METABOLISM; MOLECULARLY TARGETED THERAPY; PROTEIN MULTIMERIZATION;

PARKINSONIA;

ADENOSINE A2 RECEPTOR ANTAGONISTS; ANIMALS; ANTIPARKINSON AGENTS; DRUG DISCOVERY; GAMMA-AMINOBUTYRIC ACID; HUMANS; MOLECULAR TARGETED THERAPY; PARKINSON DISEASE; PROTEIN MULTIMERIZATION; RECEPTOR, ADENOSINE A2A; RECEPTORS, DOPAMINE D2;

EID: 84925874225     PISSN: 13892037     EISSN: 18755550     Source Type: Journal    
DOI: 10.2174/1389203715666140901103205     Document Type: Article

References (72)

1. Silkis, I. The cortico-basal ganglia-thalamocortical circuit with synaptic plasticity. II. Mechanism of synergistic modulation of thalamic activity via the direct and indirect pathways through the basal ganglia. Biosystems, 2001, 59(1), 7-14.
2. Hauser, R.A. Future treatments for Parkinson's disease: surfing the PD pipeline. Int. J. Neurosci., 2011, 121, 53-62.
3. Fuxe, K.; Agnati, L.F.; Jacobsen, K.; Hillion, J.; Canals, M.; Torvinen, M.; Tinner-Staines, B.; Staines, W.; Rosin, D.; Terasmaa, A.; Popoli, P.; Leo, G.; Vergoni, V.; Lluis, C.; Ciruela, F.; Franco, R.; Ferré, S. Receptor heteromerization in adenosine A2A receptor signaling: relevance for striatal function and Parkinson's disease. Neurology, 2003, 61(11), S19-23.
4. Schwarzschild, M.A.; Agnati, L.; Fuxe, K.; Chen, J.F.; Morelli, M. Targeting adenosine A2A receptors in Parkinson's disease. Trends Neurosci., 2006, 29(11), 647-654.
5. Fuxe, K.; Marcellino, D.; Genedani, S.; Agnati, L. Adenosine A(2A) receptors, dopamine D(2) receptors and their interactions in Parkinson's disease. Mov. Disord., 2007, 22(14), 1990-2017.
6. Morelli, M.; Carta, A.R.; Jenner, P. Adenosine A2A receptors and Parkinson's disease. Handb. Exp. Pharmacol., 2009, 193, 589-615.
7. Jenner, P.; Mori, A.; Hauser, R.; Morelli, M.; Fredholm, B.B.; Chen, J.F. Adenosine, adenosine A2A antagonists, and Parkinson's disease. Parkinsonism Relat. Disord., 2009, 15(6), 406-413.
8. Shook, B.C.; Jackson, P.F. Adenosine A(2A) Receptor Antagonists and Parkinson's Disease. ACS Chem. Neurosci., 2011, 2(10), 555-567.
9. Szabó, N.; Kincses, Z.T.; Vécsei, L. Novel therapy in Parkinson's disease: adenosine A(2A) receptor antagonists. Expert Opin. Drug Metab. Toxicol., 2011, 7(4), 441-455.
10. Hickey, P.; Stacy, M. Adenosine A2A antagonists in Parkinson's disease: what's next? Curr. Neurol. Neurosci. Rep., 2012, 12(4), 376-385.
11. Fuxe, K. Dopamine receptor agonists in brain research and as therapeutic agents. Trends Neurosci., 1979, 2, 1-4.
12. Armentero, M.T.; Pinna, A.; Ferré, S.; Lanciego, J.L.; Müller, C.E.; Franco, R. Past, present and future of A(2A) adenosine receptor antagonists in the therapy of Parkinson's disease. Pharmacol. Ther., 2011, 132(3), 280-299.
13. Fuxe, K.; Ferré, S.; Canals, M.; Torvinen, M.; Terasmaa, A.; Marcellino, D.; Goldberg, S.R.; Staines, W.; Jacobsen, K.X.; Lluis, C.; Woods, A.S.; Agnati, L.F.; Franco, R. Adenosine A2A and dopamine D2 heteromeric receptor complexes and their function. J. Mol. Neurosci., 2005, 26(2-3), 209-220.
14. Agnati, L.F.; Baldelli, E.; Andreoli, N.; Woods, A.S.; Vellani, V.; Marcellino, D.; Guidolin, D.; Fuxe, K. On the key role played by altered protein conformation in Parkinson's disease. J. Neural Transm., 2008, 115(9), 1285-1299.
15. Fuxe, K.; Marcellino, D.; Borroto-Escuela, D.O.; Guescini, M.; Fernández-Dueñas, V.; Tanganelli, S.; Rivera, A.; Ciruela, F.; Agnati, L.F. Adenosine-dopamine interactions in the pathophysiology and treatment of CNS disorders. CNS Neurosci. Ther., 2010, 16(3), 18-42.
16. Ciruela, F.; Fernández-Dueñas, V.; Llorente, J.; Borroto-Escuela, D.; Cuffí, M.L.; Carbonell, L.; Sánchez, S.; Agnati, L.F.; Fuxe, K.; Tasca, C.I. G protein-coupled receptor oligomerization and brain integration: focus on adenosinergic transmission. Brain Res., 2012, 1476, 86-95.
17. Ferraro, L.; Beggiato, S.; Tomasini, M.C.; Fuxe, K.; Antonelli, T.; Tanganelli, S. A(2A)/D(2) receptor heteromerization in a model of Parkinson's disease. Focus on striatal aminoacidergic signaling. Brain Res., 2012, 1476, 96-107.
18. Svenningsson, P.; Lindskog, M.; Ledent, C.; Parmentier, M.; Greengard, P.; Fredholm, B.B.; Fisone, G. Regulation of the phosphorylation of the dopamine- and cAMP-regulated phosphoprotein of 32 kDa in vivo by dopamine D1, dopamine D2, and adenosine A2A receptors. Proc. Natl. Acad. Sci. U.S.A., 2000, 97(4), 1856-1860.
19. Gerfen, C.R. Synaptic organization of the striatum. J. Electron. Microsc. Tech., 1988, 10(3), 265-281.
20. Parent, A.; Hazrati, L.N. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Brain Res. Rev., 1995, 20(1), 91-127.
21. Kulisevsky, J.; Poyurovsky, M. Adenosine A2A-receptor antagonism and pathophysiology of Parkinson's disease and drug-induced movement disorders. Eur. Neurol., 2012, 67(1), 4-11.
22. Hersch, S.M.; Ciliax, B.J.; Gutekunst, C.A.; Rees, H.D.; Heilman, C.J.; Yung, K..; Bolam, J.P.; Ince, E.; Yi, H.; Levey, A.I. Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents. J. Neurosci., 1995, 15, 5222-5237.
23. Yung, K.K.; Bolam, J.P.; Smith, A.D.; Hersch, S.M.; Ciliax, B.J.; Levey, A.I. Immunocytochemical localization of D1 and D2 dopamine receptors in the basal ganglia of the rat: light and electron microscopy. Neuroscience, 1995, 65(3), 709-730.
24. Obeso, J.A.; Rodríguez-Oroz, M.C.; Rodríguez, M.; Lanciego, J.L.; Artieda, J.; Gonzalo, N.; Olanow, C.W. Pathophysiology of the basal ganglia in Parkinson's disease. Trends Neurosci., 2000, 23, S8-19.
25. Obeso, J.A.; Rodríguez-Oroz, M.C.; Benitez-Temino, B.; Blesa, F.J.; Guridi, J.; Marin, C.; Rodriguez, M. Functional organization of the basal ganglia: therapeutic implications for Parkinson's disease. Mov. Disord., 2008, 23, S548-559.
26. Kawaguchi, Y.; Wilson, C.J.; Emson, P.C. Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin. J. Neurosci., 1990, 10(10), 3421-338.
27. Surmeier, D.J.; Mercer, J.N.; Chan, C.S. Autonomous pacemakers in the basal ganglia: who needs excitatory synapses anyway? Curr. Opin. Neurobiol., 2005, 15(3), 312-318.
28. Gatev, P.; Darbin, O.; Wichmann, T. Oscillations in the basal ganglia under normal conditions and in movement disorders. Mov. Disord., 2006, 21(10), 1566-1577.
29. Smith, Y.; Villalba, R. Striatal and extrastriatal dopamine in the basal ganglia: an overview of its anatomical organization in normal and Parkinsonian brains. Mov. Disord., 2008, 23, S534-547.
30. Fredholm, B.B. Purinoceptors in the nervous system. Pharmacol. Toxicol., 1995, 76(4), 228-239.
31. Fuxe, K.; Ferré, S.; Zoli, M.; Agnati, L.F. Integrated events in central dopamine transmission as analyzed at multiple levels. Evidence for intramembrane adenosine A2A/dopamine D2 and adenosine A1/dopamine D1 receptor interactions in the basal ganglia. Brain Res. Brain Res. Rev., 1998, 26(2-3), 258-2573.
32. Schiffmann, S.N.; Dassesse, D.; d'Alcantara, P.; Ledent, C.; Swillens, S.; Zoli, M. A2A receptor and striatal cellular functions: regulation of gene expression, currents, and synaptic transmission. Neurology, 2003, 61, S24-29.
33. Schiffmann, S.N.; Fisone, G.; Moresco, R.; Cunha, R.A.; Ferré, S. Adenosine A2A receptors and basal ganglia physiology. Prog. Neurobiol., 2007, 83(5), 277-292.
34. Tozzi, A.; de Iure, A.; Di Filippo, M.; Tantucci, M.; Costa, C.; Borsini, F.; Ghiglieri, V.; Giampà, C.; Fusco, F.R.; Picconi, B.; Calabresi, P. The distinct role of medium spiny neurons and cholinergic interneurons in the D_/A_A receptor interaction in the striatum: implications for Parkinson's disease. J. Neurosci., 2011, 31(5), 1850-1862.
35. Mayfield, R.D.; Suzuki, F.; Zahniser, N.R. Adenosine A2a receptor modulation of electrically evoked endogenous GABA release from slices of rat globus pallidus. J. Neurochem., 1993, 60(6), 2334-2337.
36. Fredholm, B.B.; Cunha, R.A.; Svenningsson, P. Pharmacology of adenosine A2A receptors and therapeutic applications. Curr. Top. Med. Chem., 2003, 3(4), 413-426.
37. Shindou, T.; Mori, A.; Kase, H.; Ichimura, M. Adenosine A(2A) receptor enhances GABA(A)-mediated IPSCs in the rat globus pallidus. J. Physiol., 2001, 532, 423-434.
38. Shindou, T.; Nonaka, H.; Richardson, P.J.; Mori, A.; Kase, H.; Ichimura, M. Presynaptic adenosine A2A receptors enhance GABAergic synaptic transmission via a cyclic AMP dependent mechanism in the rat globus pallidus. Br. J. Pharmacol., 2002, 136(2), 296-302.
39. Shindou, T.; Richardson, P.J.; Mori, A.; Kase, H.; Ichimura, M. Adenosine modulates the striatal GABAergic inputs to the globus pallidus via adenosine A2A receptors in rats. Neurosci. Lett., 2003, 352(3), 167-170.
40. Fuxe, K.; Agnati, L.F. Receptor-receptor interactions in the central nervous system. A new integrative mechanism in synapses. Med. Res. Rev., 1985, 5(4), 441-482.
41. Canals, M.; Marcellino, D.; Fanelli, F.; Ciruela, F.; de Benedetti, P.; Goldberg, S.R.; Neve, K.; Fuxe, K.; Agnati, L.F.; Woods, A.S; Ferré, S.; Lluis, C.; Bouvier, M.; Franco, R. Adenosine A2Adopamine D2 receptor-receptor heteromerization: qualitative and quantitative assessment by fluorescence and bioluminescence energy transfer. J. Biol. Chem., 2003, 278(47), 46741-46749.
42. Milligan, G.; Bouvier, M. Methods to monitor the quaternary structure of G protein-coupled receptors. FEBS J., 2005, 272(12), 2914-2925.
43. Trifilieff, P.; Rives, M.L.; Urizar, E.; Piskorowski, R.A.; Vishwasrao, H.D.; Castrillon, J.; Schmauss, C.; Slättman, M.; Gullberg, M.; Javitch, J.A. Detection of antigen interactions ex vivo by proximity ligation assay: endogenous dopamine D2-adenosine A2A receptor complexes in the striatum. Biotechniques, 2011, 51(2), 111-118.
44. Borroto-Escuela, D.O.; Romero-Fernandez, W.; Garriga, P.; Ciruela, F.; Narvaez, M.; Tarakanov, A.O.; Palkovits, M.; Agnati, L.F.; Fuxe, K. G protein-coupled receptor heterodimerization in the brain. Methods Enzymol., 2013, 521, 281-294.
45. Ciruela, F.; Burgueño, J.; Casadó, V.; Canals, M.; Marcellino, D.; Goldberg, S.R.; Bader, M.; Fuxe, K.; Agnati, L.F.; Lluis, C.; Franco, R.; Ferré, S.; Woods, A.S. Combining mass spectrometry and pull-down techniques for the study of receptor heteromerization. Direct epitope-epitope electrostatic interactions between adenosine A2A and dopamine D2 receptors. Anal. Chem., 2004, 76(18), 5354-5363.
46. Woods, A.; Dickerson, K.; Heath, R.; Hong, S.P.; Momcilovic, M.; Johnstone, S.R.; Carlson, M.; Carling, D. Ca2+/calmodulindependent protein kinase kinase-beta acts upstream of AMPactivated protein kinase in mammalian cells. Cell Metab., 2005, 2(1), 21-33.
47. Borroto-Escuela, D.O.; Marcellino, D.; Narvaez, M.; Flajolet, M.; Heintz, N.; Agnati, L.; Ciruela, F.; Fuxe, K.; A serine point mutation in the adenosine A2AR C-terminal tail reduces receptor heteromerization and allosteric modulation of the dopamine D2R. Biochem. Biophys. Res. Commun., 2010, 394(1), 222-227.
48. Borroto-Escuela, D.O.; Romero-Fernandez, W.; Tarakanov, A.O.; Gómez-Soler, M.; Corrales, F.; Marcellino, D.; Narvaez, M.; Frankowska, M.; Flajolet, M.; Heintz, N.; Agnati, L.F.; Ciruela, F.; Fuxe, K. Characterization of the A2AR-D2R interface: focus on the role of the C-terminal tail and the transmembrane helices. Biochem. Biophys. Res. Commun., 2010, 402(4), 801-807.
49. Fernández-Dueñas, V.; Gómez-Soler, M.; Jacobson, K.A.; Kumar, S.T.; Fuxe, K.; Borroto-Escuela, D.O.; Ciruela, F. Molecular determinants of A2AR-D2R allosterism: role of the intracellular loop 3 of the D2R. J. Neurochem., 2012, 123(3), 373-384.
50. Ferré, S.; von Euler, G.; Johansson, B.; Fredholm, B.B.; Fuxe, K. Stimulation of high-affinity adenosine A2 receptors decreases the affinity of dopamine D2 receptors in rat striatal membranes. Proc. Natl. Acad. Sci. U.S.A., 1991, 88(16), 7238-7241.
51. Ferré, S.; Snaprud, P.; Fuxe K. Opposing actions of an adenosine A2 receptor agonist and a GTP analogue on the regulation of dopamine D2 receptors in rat neostriatal membranes. Eur. J. Pharmacol., 1993, 244(3), 311-315.
52. Hillion, J.; Canals, M.; Torvinen, M.; Casado, V.; Scott, R.; Terasmaa, A.; Hansson, A.; Watson, S.; Olah, M.E.; Mallol, J.; Canela, E.I.; Zoli, M.; Agnati, L.F.; Ibanez, C.F.; Lluis, C.; Franco, R.; Ferrè, S.; Fuxe, K. Coaggregation, cointernalization, and codesensitization of adenosine A2A receptors and dopamine D2 receptors. J. Biol. Chem., 2002, 277(20), 18091-18097.
53. Kull, B.; Ferré, S.; Arslan, G.; Svenningsson, P.; Fuxe, K.; Owman, C.; Fredholm, B.B. Reciprocal interactions between adenosine A2A and dopamine D2 receptors in Chinese hamster ovary cells co-transfected with the two receptors. Biochem. Pharmacol., 1999, 58(6), 1035-1045.
54. Azdad, K.; Gall, D.; Woods, A.S.; Ledent, C.; Ferré, S.; Schiffmann, S.N. Dopamine D2 and adenosine A2A receptors regulate NMDA-mediated excitation in accumbens neurons through A2A-D2 receptor heteromerization. Neuropsychopharmacology, 2009, 34(4), 972-986.
55. Fuxe, K.; Marcellino, D.; Leo, G.; Agnati, L.F. Molecular integration via allosteric interactions in receptor heteromers. A working hypothesis. Curr. Opin. Pharmacol., 2010, 10(1), 14-22.
56. Higley, M.J.; Sabatini, B.L. Competitive regulation of synaptic Ca++ influx by D2 dopamine and A2A adenosine receptors. Nat. Neurosci., 2010, 13(8), 958-966.
57. Strömberg, I.; Popoli, P.; Müller, C.E.; Ferré, S.; Fuxe, K. Electrophysiological and behavioural evidence for an antagonistic modulatory role of adenosine A2A receptors in dopamine D2 receptor regulation in the rat dopamine-denervated striatum. Eur. J. Neurosci., 2000, 12(11), 4033-4037.
58. Fuxe, K.; Marcellino, D.; Rivera, A.; Diaz-Cabiale, Z.; Filip, M.; Gago, B.; Roberts, D.C.; Langel, U.; Genedani, S.; Ferraro, L.; de la Calle, A.; Narvaez, J.; Tanganelli, S.; Woods, A.; Agnati, L.F. Receptor-receptor interactions within receptor mosaics. Impact on neuropsychopharmacology. Brain. Res. Rev., 2008, 58(2), 415-452.
59. Ferré, S.; O'Connor, W.T.; Fuxe, K.; Ungerstedt, U. The striopallidal neuron: a main locus for adenosine-dopamine interactions in the brain. J. Neurosci., 1993, 13(12), 5402-5406.
60. Tanganelli, S.; Sandager Nielsen, K.; Ferraro, L.; Antonelli, T.; Kehr, J.; Franco, R.; Ferré, S.; Agnati, L.F.; Fuxe, K.; Scheel- Krüger, J. Striatal plasticity at the network level. Focus on adenosine A2A and D2 interactions in models of Parkinson's Disease. Parkinsonism Relat. Disord., 2004, 10(5), 273-280.
61. Ferré, S.; Rubio, A.; Fuxe, K. Stimulation of adenosine A2 receptors induces catalepsy. Neurosci. Lett., 1991, 130(2), 162-164.
62. Mandhane, S.N.; Chopde, C.T.; Ghosh, A.K. Adenosine A2 receptors modulate haloperidol-induced catalepsy in rats. Eur. J. Pharmacol., 1997, 328(2-3), 135-141.
63. Fuxe, K.; Ungerstedt, U. Action of caffeine and theophyllamine on supersensitive dopamine receptors: considerable enhancement of receptor response to treatment with DOPA and dopamine receptor agonists. Med. Biol., 1974, 52(1), 48-54.
64. Hettinger, B.D.; Lee, A.; Linden, J.; Rosin, D.L. Ultrastructural localization of adenosine A2A receptors suggests multiple cellular sites for modulation of GABAergic neurons in rat striatum. J. Comp. Neurol., 2001, 431(3), 331-346.
65. Popoli, P.; Betto, P.; Reggio, R.; Ricciarello, G. Adenosine A2A receptor stimulation enhances striatal extracellular glutamate levels in rats. Eur. J. Pharmacol., 1995, 287(2), 215-217.
66. Antonelli, T.; Fuxe, K.; Agnati, L.; Mazzoni, E.; Tanganelli, S.; Tomasini, M.C.; Ferraro, L. Experimental studies and theoretical aspects on A2A/D2 receptor interactions in a model of Parkinson's disease. Relevance for L-dopa induced dyskinesias. J. Neurol. Sci., 2006, 248(1-2), 16-22.
67. Ferré, S.; Fuxe, K. Dopamine denervation leads to an increase in the intramembrane interaction between adenosine A2 and dopamine D2 receptors in the neostriatum. Brain Res., 1992, 594(1), 124-130.
68. Vortherms, T.A.; Watts, V.J. Sensitization of neuronal A2A adenosine receptors after persistent D2 dopamine receptor activation. J. Pharmacol. Exp. Ther., 2004, 308(1), 221-227.
69. Chase, T.N.; Bibbiani, F.; Bara-Jimenez, W.; Dimitrova, T.; Oh- Lee, J.D. Translating A2A antagonist KW6002 from animal models to parkinsonian patients. Neurology, 2003, 61(11), S107-111.
70. Koga, K.; Kurokawa, M.; Ochi, M.; Nakamura, J.; Kuwana, Y. Adenosine A(2A) receptor antagonists KF17837 and KW-6002 potentiate rotation induced by dopaminergic drugs in hemi- Parkinsonian rats. Eur. J. Pharmacol., 2000, 408(3), 249-255.
71. Morelli, M.; Blandini, F.; Simola, N.; Hauser, R.A. A(2A) Receptor Antagonism and Dyskinesia in Parkinson's Disease. Parkinsons Dis., 2012, 2012:489853.
72. Borroto-Escuela, D.O.; Tarakanov, A.O.; Guidolin, D.; Ciruela, F.; Agnati, L.F.; Fuxe, K. Moonlighting characteristics of G proteincoupled receptors: focus on receptor heteromers and relevance for neurodegeneration. IUBMB Life, 2011, 63(7), 463-472.