Adenosine A 2A receptors and A 2A receptor heteromers as key players in striatal function

Frontiers in Neuroanatomy

Volumn , Issue JUN, 2011, Pages

  Ferré, Sergi ^a   Quiroz, César ^a   Orru, Marco ^a   Guitart, Xavier ^a   Navarro, Gemma ^b   Cortés, Antonio ^b   Casadó, Vicent ^b   Canela, Enric I ^b   Lluis, Carme ^b   Franco, Rafael ^b,c  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF NAVARRA   (Spain)

Author keywords

Adenosine A 2A receptor; Cannabinoid receptors; Dopamine receptors; Receptor heteromers; Striatum

Indexed keywords

4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; 5 AMINO 2 (2 FURYL) 7 (2 PHENYLETHYL)PYRAZOLO[4,3 E][1,2,4]TRIAZOLO[1,5 C]PYRIMIDINE; 5 AMINO 2 (2 FURYL) 7 [3 (4 METHOXYPHENYL)PROPYL]PYRAZOLO[4,3 E][1,2,4]TRIAZOLO[1,5 C]PYRIMIDINE; ADENOSINE A2A RECEPTOR; ADENOSINE A2A RECEPTOR AGONIST; ADENOSINE A2A RECEPTOR ANTAGONIST; ADENOSINE RECEPTOR BLOCKING AGENT; CALMODULIN; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR ANTAGONIST; ISTRADEFYLLINE; METABOTROPIC RECEPTOR 5; MSX 2; MSX 3; PRELADENANT; UNCLASSIFIED DRUG;

ACETYLCHOLINE RELEASE; ARTICLE; BINDING AFFINITY; BRAIN FUNCTION; DRUG DEPENDENCE; DRUG EFFICACY; DRUG MECHANISM; DRUG RECEPTOR BINDING; DYSKINESIA; HUMAN; INTRACELLULAR SIGNALING; LIGAND BINDING; NEUROMODULATION; NONHUMAN; OBSESSIVE COMPULSIVE DISORDER; PARKINSON DISEASE; PATHOGENESIS; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC POTENTIAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SYNTHESIS INHIBITION; PROTEIN TARGETING;

EID: 84857053943     PISSN: 16625129     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnana.2011.00036     Document Type: Article

References (53)

1. Albizu, L., Cottet, M., Kralikova, M., Stoev, S., Seyer, R., Brabet, I., Roux, T., Bazin, H., Bourrier, E., Lamarque, L., Breton, C., Rives, M. L., Newman, A., Javitch, J., Trinquet, E., Manning, M., Pin, J. P., Mouillac, B., and Durroux, T. (2010). Time-resolved FRET between GPCR ligands reveals oligomers in native tissues. Nat. Chem. Biol. 6, 587-594.
2. Andersson, M., Usiello, A., Borgkvist, A., Pozzi, L., Dominguez, C., Fienberg, A. A., Svenningsson, P., Fredholm, B. B., Borrelli, E., Greengard, P., and Fisone, G. (2005). Cannabinoid action depends on phosphorylation of dopamineand cAMPregulated phosphoprotein of 32 kDa at the protein kinase A site in striatal projection neurons. J. Neurosci. 25, 8432-8438.
3. Azdad, K., Gall, D., Woods, A. S., Ledent, C., Ferré, S., and Schiffmann, S. N. (2009). Dopamine D2 and adenosine A2A receptors regulate NMDA-excitation in accumbens neurons through A2AD2 receptor heteromerization. Neuropsychopharmacology 34, 972-986.
4. Bofill-Cardona, E., Kudlacek, O., Yang, Q., Ahorn, H., Freissmuth, M., and Nanoff, C. (2000). Binding of calmodulin to the D2-dopamine receptor reduces receptor signaling by arresting the G protein activation switch. J. Biol. Chem. 275, 32672-32680.
5. Borroto-Escuela, D. O., Marcellino, D., Narvaez, M., Flajolet, M., Heintz, N., Agnati, L., Ciruela, F., and Fuxe, K. (2010a). 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. 394, 222-227.
6. 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., and Fuxe, K. (2010b). Characterization of the A2AR-D2R interface: focus on the role of the C-terminal tail and the transmembrane helices. Biochem. Biophys. Res. Commun. 402, 801-807.
7. Bouvier, M. (2001). Oligomerization of G-protein-coupled transmitter receptors. Nat. Rev. Neurosci. 2, 274-286.
8. Brooks, D. J., Papapetropoulos, S., Vandenhende, F., Tomic, D., He, P., Coppell, A., and O'Neill, G. (2010). An open-label, positron emission tomography study to assess adenosine A2A brain receptor occupancy of vipadenant (BIIB014) at steadystate levels in healthy male volunteers. Clin. Neuropharmacol. 33, 55-60.
9. Cabello, N., Gandia, J., Bertarelli, D. C., Watanabe, M., Lluis, C., Franco, R., Ferré, S., Lujan, R., and Ciruela, F. (2009). Metabotropic glutamate type 5, dopamine D2 and adenosine A2A receptors form higherorder oligomers in living cells. J. Neurochem. 109, 1497-1507.
10. Carriba, P., Navarro, G., Ciruela, F., Ferré, S., Casado, V., Agnati, L. F., Cortes, A., Mallol, J., Fuxe, K., Canela, E. I., Lluis, C., and Franco, R. (2008). Detection of heteromerization of more than two proteins by sequential BRET-FRET. Nat. Methods 5, 727-733.
11. Carriba, P., Ortiz, O., Patkar, K., Justinova, Z., Stroik, J., Themann, A., Müller, C., Woods, A. S., Hope, B. T., Ciruela, F., Casadó, V., Canela, E. I., Lluis, C., Goldberg, S. R., Moratalla, R., Franco, R., and Ferré, S. (2007). Striatal adenosine A2A and cannabinoid CB1 receptors form functional heteromeric complexes that mediate the motor effects of cannabinoids. Neuropsychopharmacology 32, 2249-2259.
12. Chen, J. F., Moratalla, R., Impagnatiello, F., Grandy, D. K., Cuellar, B., Rubinstein, M., Beilstein, M. A., Hackett, E., Fink, J. S., Low, M. J., Ongini, E., and Schwarzschild, M. A. (2001). The role of the D(2) dopamine receptor (D(2)R) in A(2A) adenosine receptor (A(2A)R)-mediated behavioral and cellular responses as revealed by A(2A) and D(2) receptor knockout mice. Proc. Natl. Acad. Sci. U.S.A. 98, 1970-1975.
13. Ciruela, F., Casado, V., Rodrigues, R. J., Luján, R., Burgueno, J., Canals, M., Borycz, J., Rebola, N., Goldberg, S. R., Mallol, J., Cortés, A., Canela, E. I., López-Giménez, J. F., Milligan, G., Lluis, C., Cunha, R. A., Ferré, S., and Franco, R. (2006). Presynaptic control of striatal glutamatergic neurotransmission by adenosine A1-A2A receptor heteromers. J. Neurosci. 26, 2080-2087.
14. DeLong, M. R., and Wichmann, T. (2007). Circuits and circuit disorders of the basal ganglia. Arch. Neurol. 64, 20-24.
15. Ferré, S., Baler, R., Bouvier, M., Caron, M. G., Devi, L. A., Durroux, T., Fuxe, K., George, S. R., Javitch, J. A., Lohse, M. J., Mackie, K., Milligan, G., Pfleger, K. D. G., Pin, J.-P., Volkow, N., Waldhoer, M., Woods, A. S., and Franco, R. (2009). Building a new conceptual framework for receptor heteromers. Nat. Chem. Biol. 5, 131-134.
16. Ferré, S., Ciruela, F., Woods, A. S., Lluis, C., and Franco, R. (2007). Functional relevance of neurotransmitter receptor heteromers in the central nervous system. Trends Neurosci. 30, 440-446.
17. Ferré, S., Karcz-Kubicha, M., Hope, B. T., Popoli, P., Burgueno, J., Casado, V., Fuxe, K., Lluis, C., Goldberg, S. R., Franco, R., and Ciruela, F. (2002). Synergistic interaction between adenosine A2A and glutamate mGlu5 receptors: implications for striatal neuronal function. Proc. Natl. Acad. Sci. U.S.A. 99, 11940-11945.
18. Ferré, S., Lluis, C., Justinova, Z., Quiroz, C., Orru, M., Navarro, G., Canela, E. I., Franco, R., and Goldberg, S. R. (2010). Adenosine-cannabinoid receptor interactions. Implications for striatal function. Br. J. Pharmacol. 160, 443-453.
19. Ferré, S., Quiroz, C., Woods, A. S., Cunha, R., Popoli, P., Ciruela, F., Lluis, C., Franco, R., Azdad, K., and Schiffmann, S. N. (2008). An update on adenosine A2A-dopamine D2 receptor interactions. Implications for the function of G proteincoupled receptors. Curr. Pharm. Des. 14, 1468-1474.
20. Ferré, S., von Euler, G., Johansson, B., Fredholm, B. B., and Fuxe, K. (1991). Stimulation of high affinity adenosine A-2 receptors decreases the affinity of dopamine D-2 receptors in rat striatal membranes. Proc. Natl. Acad. Sci. U.S.A. 88, 7238-7241.
21. Håkansson, K., Galdi, S., Hendrick, J., Snyder, G., Greengard, P., and Fisone, G. (2006). Regulation of phosphorylation of the GluR1 AMPA receptor by dopamine D2 receptors. J. Neurochem. 96, 482-488.
22. Hettinger, B. D., Lee, A., Linden, J., and Rosin, D. L. (1998). Ultrastructural localization of adenosine A2A receptors suggests multiple cellular sites for modulation of GABAergic neurons in rat striatum. J. Comp. Neurol. 431, 331-346.
23. Higley, M. J., and Sabatini, B. L. (2010). Competitive regulation of synaptic Ca2(influx by D2 dopamine and A2A adenosine receptors. Nat. Neurosci. 13, 958-966.
24. 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., Ferré, S., and Fuxe, K. (2002). Coaggregation, cointernalization and codesensitization of adenosine A2A receptors and dopamine D2 receptors. J. Biol. Chem. 277, 18091-18097.
25. James, S., and Richardson, P. J. (1993). The subcellular distribution of [3H]-CGS 21680 binding sites in the rat striatum: copurification with cholinergic nerve terminals. Neurochem. Int. 23, 115-122.
26. Jin, S., Johansson, B., and Fredholm, B. B. (1993). Effects of adenosine A1 and A2 receptor activation on electrically evoked dopamine and acetylcholine release from rat striatal slices. J. Pharmacol. Exp. Ther. 267, 801-808.
27. Justinova, Z., Ferré, S., Redhi, G. H., Mascia, P., Stroik, J., Quarta, D., Yasar, S., Muller, C. E., Franco, R., and Goldberg, S. R. (2011). Reinforcing and neurochemical effects of cannabinoid CB1 receptor agonists, but not cocaine, are altered by an adenosine A2A receptor antagonist. Addict. Biol. 16, 405-415.
28. Kachroo, A., Orlando, L. R., Grandy, D. K., Chen, J. F., Young, A. B., and Schwarzschild, M. A. (2005). Interactions between metabotropic glutamate 5 and adenosine A2A receptors in normal and parkinsonian mice. J. Neurosci. 25, 10414-10419.
29. Kreitzer, A. C., and Malenka, R. C. (2007). Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445, 643-647.
30. Kull, B., Ferré, S., Arslan, G., Svenningsson, P., Fuxe, K., Owman, C., and Fredholm, B. B. (1999). Reciprocal interactions between adenosine A2A and dopamine D2 receptors in CHO cells co-transfected with the two receptors. Biochem. Pharmacol. 58, 1035-1045.
31. Lerner, T. N., Horne, E. A., Stella, N., and Kreitzer, A. C. (2010). Endocannabinoid signaling mediates psychomotor activation by adenosine A2A antagonists. J. Neurosci. 30, 2160-2164.
32. Martire, A., Tebano, M. T., Chiodi, V., Ferreira, S. G., Cunha, R. A., Köfalvi, A., and Popoli, P. (2011). Presynaptic adenosine A2A receptors control cannabinoid CB1 receptormediated inhibition of striatal glutamatergic neurotransmission. J. Neurochem. 116, 273-280.
33. Moresco, R. M., Todde, S., Belloli, S., Simonelli, P., Panzacchi, A., Rigamonti, M., Galli-Kienle, M., and Fazio, F. (2005). In vivo imaging of adenosine A2A receptors in rat and primate brain using [11C]SCH442416. Eur. J. Nucl. Med. Mol. Imaging 32, 405-413.
34. Navarro, G., Aymerich, M. S., Marcellino, D., Cortes, A., Casado, V., Mallol, J., Canela, E. I., Agnati, L. F., Woods, A. S., Fuxe, K., Lluis, C., Lanciego, J. L., Ferré, S., and Franco, R. (2009). Interactions between calmodulin, adenosine A2A and dopamine D2 receptors. J. Biol. Chem. 284, 28058-28068.
35. Navarro, G., Ferré, S., Cordomi, A., Moreno, E., Mallol, J., Casadó, V., Cortés, A., Hoffmann, H., Ortiz, J., Canela, E. I., Lluís, C., Pardo, L., Franco, R., and Woods, A. S. (2010). Interactions between intracellular domains as key determinants of the quaternary structure and function of receptor heteromers. J. Biol. Chem. 285, 27346-27359.
36. Nishi, A., Liu, F., Matsuyama, S., Hamada, M., Higashi, H., Nairn, A. C., and Greengard, P. (2003). Metabotropic mGlu5 receptors regulate adenosine A2A receptor signaling. Proc. Natl. Acad. Sci. U.S.A. 100, 1322-1327.
37. Obeso, J. A., Rodríguez-Oroz, M. C., Rodríguez, M., Arbizu, J., and Giménez-Amaya, J. M. (2002). The basal ganglia and disorders of movement: pathophysiological mechanisms. News Physiol. Sci. 17, 51-55.
38. Orru, M., Bakešová, J., Brugarolas, M., Quiroz, C., Beaumont, V., Goldberg, S. R, Lluís, C., Cortés, A., Franco, R., Casadó, V., Canela, E. I., and Ferré, S. (2011). Striatal preand postsynaptic profile of adenosine A(2A) receptor antagonists. PLoS ONE 6, e16088. doi: 10.1371/journal.pone.0016088
39. Popoli, P., Betto, P., Reggio, R., and Ricciarello, G. (1995). Adenosine A2A receptor stimulation enhances striatal extracellular glutamate levels in rats. Eur. J. Pharmacol. 287, 215-217.
40. Popoli, P., Pezzola, A., Torvinen, M., Reggio, R., Pintor, A., Scarchili, L., Fuxe, K., and Ferré, S. (2001). The selective mGlu5 receptor agonist CHPG inhibits quinpirole-induced turning in 6-hydroxydopamine-lesioned rats and modulates the binding characteristics of dopamine D2 receptors in the rat striatum: interactions with adenosine A2A receptors. Neuropsychopharmacology 25, 505-513.
41. Preston, Z., Lee, K., Widdowson, L., Freeman, T. C., Dixon, A. K., and Richardson, P. J. (2000). Adenosine receptor expression and function in rat striatal cholinergic interneurons. Br. J. Pharmacol. 130, 886-890.
42. Quiroz, C., Lujan, R., Uchigashima, M., Simoes, A. P., Lerner, T. N., Borycz, J., Kachroo, A., Canas, P. M., Orru, M., Schwarzschild, M. A., Rosin, D. L., Kreitzer, A. C., Cunha, R. A., Watanabe, M., and Ferré, S. (2009). Key modulatory role of presynaptic adenosine A2A receptors in cortical neurotransmission to the striatal direct pathway. ScientificWorldJournal 9, 1321-1344.
43. Rodrigues, R. J., Alfaro, T. M., Rebola, N., Oliveira, C. R., and Cunha R. A. (2005). Co-localization and functional interaction between adenosine A(2A) and metabotropic group 5 receptors in glutamatergic nerve terminals of the rat striatum. J. Neurochem. 92, 433-441.
44. Rosin, D. L., Robeva, A., Woodard, R. L., Guyenet, P. G., and Linden, J. (1998). Immunohistochemical localization of adenosine A2A receptors in the rat central nervous system. J. Comp. Neurol. 401, 163-186.
45. Schiffmann, S. N., Fisone, G., Moresco, R., Cunha, R., and Ferré, S. (2007). Adenosine A2A receptors and basal ganglia physiology. Prog. Neurobiol. 83, 277-292.
46. Shen, H. Y., Coelho, J. E., Ohtsuka, N., Canas, P. M., Day, Y. J., Huang, Q. Y., Rebola, N., Yu, L., Boison, D., Cunha, R. A., Linden, J., Tsien, J. Z., and Chen, J. F. (2008). A critical role of the adenosine A2A receptor in extrastriatal neurons in modulating psychomotor activity as revealed by opposite phenotypes of striatum and forebrain A2A receptor knock-outs. J. Neurosci. 28, 2970-2975.
47. Soria, G., Castañé, A., Ledent, C., Parmentier, M., Maldonado, R., and Valverde, O. (2004). Adenosine A2A receptors are involved in physical dependence and place conditioning induced by THC. Eur. J. Neurosci. 20, 2203-2213.
48. Tanganelli, S., Sandager-Nielsen, K., Ferraro, L., Antonelli, T., Kehr, J., Franco, R., Ferré, S., Agnati, L. F., Fuxe, K., and Scheel-Krüger, J. (2004). Striatal plasticity at the network level. Focus on adenosine A2A and D2 interactions in models of Parkinson's disease. Parkinsonism Relat. Disord. 10, 273-280.
49. Tebano, M. T., Martire, A., Chiodi, V., Pepponi, R., Ferrante, A., Domenici, M. R., Frank, C., Chen, J. F., Ledent, C., and Popoli, P. (2009). Adenosine A2A receptors enable the synaptic effects of cannabinoid CB1 receptors in the rodent striatum. J. Neurochem. 110, 1921-1930.
50. Tozzi, A., de Iure, A., Di Filippo, M., Tantucci, M., Costa, C., Borsini, F., Ghiglieri, V., Giampà, C., Fusco, F. R., Picconi, B., and Calabresi, P. (2011). The distinct role of medium spiny neurons and cholinergic interneurons in the D2/A2A receptor interaction in the striatum: implications for Parkinson's disease. J. Neurosci. 31, 1850-1862.
51. Woods, A. S., and Ferré, S. (2005). The amazing stability of the argininephosphate electrostatic interaction. J. Proteome Res. 4, 1397-1402.
52. Yao, L., Fan, P., Jiang, Z., Mailliard, W. S., Gordon, A. S., and Diamond, I. (2003). Addicting drugs utilize a synergistic molecular mechanism in common requiring adenosine and Gi-beta gamma dimers. Proc. Natl. Acad. Sci. U.S.A. 100, 14379-14384.
53. Zoli, M., Agnati, L. F., Hedlund, P. B., Li, X.-M., Ferré, S., and Fuxe, K. (1993). Receptor-receptor interactions as an integrative mechanism in nerve cells. Mol. Neurobiol. 7, 293-334.