Journal of Neural Transmission

, Volume 114, Issue 1, pp 93–104 | Cite as

Receptor–receptor interactions involving adenosine A1 or dopamine D1 receptors and accessory proteins

  • R. Franco
  • C. Lluis
  • E. I. Canela
  • J. Mallol
  • L. Agnati
  • V. Casadó
  • F. Ciruela
  • S. Ferré
  • K. Fuxe
Article

Summary.

The molecular basis for the known intramembrane receptor–receptor interactions among heptahelical receptors (G protein coupled receptors, GPCR) was postulated to be heteromerization based on receptor subtype specific interactions between different types of homomers of GPCR. Adenosine and dopamine receptors in the basal ganglia have been fundamental to demonstrate the existence of receptor heteromers and the functional consequences of such molecular interactions. The heterodimer is only one type of heteromeric complex and the evidence is equally compatible with the existence of higher order heteromeric complexes, where also adapter proteins such as homer proteins and scaffolding proteins can exist, assisting in the process of linking the GPCR and ion channel receptors together in a receptor mosaic that may have special integrative value and may constitute the molecular basis for learning and memory. Heteromerization of D2 dopamine and A2A adenosine receptors is reviewed by Fuxe in another article in this special issue. Here, heteromerization between D1 dopamine and A1 adenosine receptors is reviewed. Heteromers formed by dopamine D1 and D2 receptors and by adenosine A1 and A2A receptors also occur in striatal cells and open new perspectives to understand why two receptors with apparently opposite effects are expressed in the same neuron and in the nerve terminals. The role of accessory proteins also capable of interacting with receptor–receptor heteromers in regulating the traffic and the molecular physiology of these receptors is also discussed. Overall, the knowledge of the reason why such complex networks of receptor–receptor and receptor–protein interactions occur in striatal cells is crucial to develop new strategies to combat neurological and neuropsychiatric diseases.

Keywords: Adenosine deaminase, hsc73, clustering parkinson, caveolin 

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References

  1. Agnati, L, Ferré, S, Lluis, C, Franco, R, Fuxe, K 2003Molecular mechanisms and therapeutical implications of intramembrane receptor–receptor interactions among heptahelical receptors with examples from the striato-pallidal GABA neuronsPharmacol Rev55509550PubMedCrossRefGoogle Scholar
  2. Bouvier, M 2001Oligomerization of G-protein-coupled transmitter receptorsNat Rev Neurosci2274286PubMedCrossRefGoogle Scholar
  3. Canals, M, Marcellino, M, Fanelli, F, Ciruela, F, de Benedetti, P, Goldberg, S, Fuxe, K, Agnati, LF, Woods, AS, Ferré, S, Lluis, C, Bouvier, M, Franco, R 2003Adenosine A2A-dopamine D2 receptor–receptor heteromerization. Qualitative and quantitative assessment by fluorescence and bioluminescence energy transferJ Biol Chem2784674146749PubMedCrossRefGoogle Scholar
  4. Ciruela, F, Casadó, V, Mallol, J, Canela, EI, Lluís, C, Franco, R 1995Immunological identification of A1 adenosine receptors in brain cortexJ Neurosci Res23818828CrossRefGoogle Scholar
  5. Ciruela, F, Saura, C, Canela, EI, Mallol, J, Lluís, C, Franco, R 1996Adenosine deaminase affects signaling by interacting with cell surface receptorsFEBS Lett380219223PubMedCrossRefGoogle Scholar
  6. Ciruela, F, Escriche, M, Burgueño, J, Angulo, E, Casadó, V, Soloviev, MM, Canela, EI, Mallol, J, Chan, W-Y, Lluis, C, Mcllhinney, RAJ, Franco, R 2001Metabotropic glutamate 1 alpha and adenosine A1 receptors assemble into functionally interacting complexesJ Biol Chem2761834518351PubMedCrossRefGoogle Scholar
  7. Ciruela, F, Burgueño, J, Casado, V, Canals, M, Marcellino, D, Goldberg, SR, Bader, M, Fuxe, K, Agnati, LF, Lluis, C, Franco, R, Ferre, S, Woods, AS 2004Combining mass spectrometry and pull-down techniques for the study of receptor heteromerization. Direct epitope-epitope electrostatic interactions between adenosine A2A and dopamine D2 receptorsAnal Chem7653545363PubMedCrossRefGoogle Scholar
  8. Ciruela, F, Casadó, V, Rodrigues, RJ, Luján, R, Burgueño, J, Canals, M, Borycz, J, Rebola, N, Goldberg, SR, Mallol, J, Cortés, A, Canela, EI, López-Giménez, JF, Milligan, G, Lluis, C, Cunha, RA, Ferré, S, Franco, R 2006Presynaptic control of striatal glutamatergic neurotransmission by adenosine A1-A2A receptor heteromersJ Neurosci2620802087PubMedCrossRefGoogle Scholar
  9. Escriche, M, Burgueño, J, Ciruela, F, Canela, EI, Mallol, J, Enrich, C, Lluis, C, Franco, R 2003Ligand-induced caveolae-mediated internalization of A1 adenosine receptors: morphological evidence of endosomal sorting and receptor recyclingExp Cell Res2857290PubMedCrossRefGoogle Scholar
  10. Ferré, S, Fuxe, K, von Euler, G, Johansson, B, Fredholm, BB 1992Adenosine-dopamine interactions in the brainNeuroscience51501512PubMedCrossRefGoogle Scholar
  11. Ferré, S, O’Connor, WT, Svenningsson, P, Björklund, L, Lindberg, J, Tinner, B, Strömberg, I, Golstein, M, Ögren, SO, Ungerstedt, U, Fredholm, B, Fuxe, K 1996Dopamine D1 receptor-mediated facilitation of GABAergic neurotransmission in the rat strioentopeduncular pathway and its modulation by adenosine A1 receptor-mediated mechanismsEur J Neurosci815451553PubMedCrossRefGoogle Scholar
  12. Ferré, S, Fredholm, BB, Morelli, M, Popoli, P, Fuxe, K 1997Adenosine-dopamine receptor–receptor interactions as an integrative mechanism in the basal gangliaTrends Neurosci20482487PubMedCrossRefGoogle Scholar
  13. Ferré, S, Torvinen, M, Antoniou, K, Irenius, E, Civelli, O, Arenas, E, Fredholm, BB, Fuxe, K 1998Adenosine A1 receptor-mediated modulation of dopamine D1 receptors in stably cotransfected fibroblast cellsJ Biol Chem27347184724PubMedCrossRefGoogle Scholar
  14. Ferré, S, Karcz-Kubicha, M, Hope, BT, Popoli, P, Burgueño, J, Gutiérrez, MA, Casadó, V, Fuxe, K, Goldberg, SR, Lluis, C, Franco, R, Ciruela, F 2002Synergistic interaction between adenosine A2A and glutamate mGlu5 receptors: Implications for striatal neuronal functionProc Natl Acad Sci USA991194011945PubMedCrossRefGoogle Scholar
  15. Ferré, S, Ciruela, F, Woods, AS, Canals, M, Burgueño, J, Marcellino, D, Karcz-Kubicha, M, Hope, BT, Morales, M, Popoli, P, Goldberg, SR, Fuxe, K, Lluis, C, Franco, R, Agnati, L 2003Glutamate mGlu5-adenosine A2A-dopamine D2 receptor interactions in the striatum. Implications for drug therapy in neuro-psychiatric disorders and drug abuseMed Chem – Central Nervous System Agents3126CrossRefGoogle Scholar
  16. Ferré, S, Ciruela, F, Canals, M, Marcellino, D, Burgueño, J, Casado, V, Hillion, J, Torvinen, M, Fanelli, F, Benedetti, Pd P, Goldberg, SR, Bouvier, M, Fuxe, K, Agnati, LF, Lluis, C, Franco, R, Woods, A 2004Adenosine A2A-dopamine D2 receptor–receptor heteromers. Targets for neuro-psychiatric disordersParkinsonism Relat Disord10265271PubMedCrossRefGoogle Scholar
  17. Franco, R, Casadó, V, Ciruela, F, Mallol, J, Lluis, C, Canela, EI 1996The cluster-arranged cooperative model: A model that accounts for the binding kinetics to A1 adenosine receptorsBiochemistry3530073015PubMedCrossRefGoogle Scholar
  18. Franco, R, Casadó, V, Ciruela, F, Saura, C, Mallol, J, Canela, EI, Lluis, C 1997Cell surface adenosine deaminase: much more than an ectoenzymeProg Neurobiol52283294PubMedCrossRefGoogle Scholar
  19. Franco, R, Valenzuela, A, Lluís, C, Blanco, R 1998Enzymatic and extraenzymatic role of ecto-adenosine deaminase in lymphocytesImmunol Rev1612742PubMedCrossRefGoogle Scholar
  20. Franco, R, Mallol, J, Casadó, V, Lluís, C, Canela, EI, Saura, C, Blanco, J, Ciruela, F 1999Ecto-adenosine deaminase: An ectoenzyme and a costimulatory protein acting on a variety of cell surface receptorsDrug Dev Res45261268CrossRefGoogle Scholar
  21. Franco, R, Ferré, S, Agnati, L, Torvinen, M, Ginés, S, Hillion, J, Casadó, V, Lledó, PM, Zoli, M, Lluís, C, Fuxe, K 2000Evidence for adenosine/dopamine receptor interactions: Indications for heteromerizationNeuropsychopharmacology235059CrossRefGoogle Scholar
  22. Franco, R, Ferré, S, Torvinen, M, Ginés, S, Hillion, J, Ciruela, F, Canela, EI, Mallol, J, Casadó, V, Lluis, C,  et al. 2001Adenosine/dopamine receptor–receptor interactions in the central nervous systemDrug Dev Res52296302CrossRefGoogle Scholar
  23. Franco, R, Canals, M, Marcellino, D, Ferre, S, Agnati, L, Mallol, J, Casado, V, Ciruela, F, Fuxe, K, Lluis, C, Canela, EI 2003Regulation of heptaspanning-membrane-receptor function by dimerization and clusteringTrends Biochem Sci28238243PubMedCrossRefGoogle Scholar
  24. Franco, R, Casado, V, Mallol, J, Ferre, S, Fuxe, K, Cortes, A, Ciruela, F, Lluis, C, Canela, EI 2005Dimer-based model for heptaspanning membrane receptorsTrends Biochem Sci30360366PubMedCrossRefGoogle Scholar
  25. Franco, R, Casadó, V, Mallol, J, Ferrada, C, Ferré, S, Fuxe, K, Cortés, A, Ciruela, F, Lluis, C, Canela, EI 2006The two-state dimer receptor model. A general model for receptor dimersMol Pharmacol6919051912PubMedCrossRefGoogle Scholar
  26. Fredholm, BB, Abbracchio, MP, Burnstock, G, Daly, JW, Harden, TK, Jacobson, KA, Leff, P, Williams, M 1994Nomenclature and classification of purinoceptorsPharmacol Rev46143156PubMedGoogle Scholar
  27. Fredholm, BB 1995Adenosine, adenosine receptors and the actions of caffeinePharmacol Toxicol7693101PubMedCrossRefGoogle Scholar
  28. Fredholm, BB, Irenius, E, Kull, B, Schulte, G 2001Comparison of the potency of adenosine as an agonist at human adenosine receptors expressed in Chinese hamster ovary cellsBiochem Pharmacol15443448CrossRefGoogle Scholar
  29. Fuxe, K, Ferré, S, Zoli, M, Agnati, L 1998Integrated events in central dopamine transmission as analyzed at multiple levels. Evidence for intramembrane adenosine A2A/dopamine D2 and adenosine A1/dopamine 1 receptor interactions in the basal gangliaBrain Res Rev26258273PubMedCrossRefGoogle Scholar
  30. Fuxe, K, Stromberg, I, Popoli, P, Rimondini-Giorgini, R, Torvinen, M, Ogren, SO, Franco, R, Agnati, LF, Ferre, S 2001Adenosine receptors and Parkinson’s disease. Relevance of antagonistic adenosine and dopamine receptor interactions in the striatumAdv Neurol86345353PubMedGoogle Scholar
  31. Fuxe K, Ferré S, Torvinen M, Hillion J, Stroömberg I, Franzen O, Ibañez C, Zoli M, Lluis C, Agnati LF et al. (2002) Heteromerization of adenosine and dopamine receptor subtypes. Relevance for neuronal integration in normal and pathological states. In: Nagatsu T, Nabeshima T, McCarty R, Goldstein DS (eds) Catecholamine Research: From molecular insights to Clinical Medicine, 9th Int. Catecholamine symposium, Kyoto, Japan 2001. Kluwer Academic/Plenum Publishers, New York, pp 199–205Google Scholar
  32. Fuxe, K, Agnati, LF, 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, Ferre, S 2003Receptor heteromerization in adenosine A2A receptor signaling: relevance for striatal function and Parkinson’s diseaseNeurology611923Google Scholar
  33. Genazzani, AA, L’Episcopo, MR, Casabona, G, Shinozaki, H, Nicoletti, F 1994(2S,1′R,2′R,3′R)-2-(2,3-dicarboxycyclopropyl) glycine positively modulates metabotropic glutamate receptors coupled to polyphosphoinositide hydrolysis in rat hippocampal slicesBrain Res6591016PubMedCrossRefGoogle Scholar
  34. George, SR, Lee, SP, Varghese, G, Zeman, PR, Seeman, P, Ng, GYK, O’Dowd,  1998A transmembrane domain-derived peptide inhibits D1 dopamine receptor function without affecting receptor oligomerizationJ Biol Chem2733024430248PubMedCrossRefGoogle Scholar
  35. Gerfen, CR 1992The neostriatal mosaic: multiple levels of compartmental organization in the basal gangliaAnnu Rev Neurosci15285320PubMedCrossRefGoogle Scholar
  36. Ginés, S, Hillion, J, Torvinen, M, Le Crom, S, Casado, V, Canela, EI, Rondin, S, Lew, JY, Watson, S, Zoli, M, Agnati, LF, Vernier, P, Lluis, C, Ferré, S, Fuxe, K, Franco, R 2000Dopamine D1 and adenosine A1 receptors form functionally interacting heteromeric complexesProc Natl Acad Sci USA9786068611PubMedCrossRefGoogle Scholar
  37. Ginés, S, Ciruela, F, Burgueño, J, Casadó, V, Canela, EI, Mallol, J, Lluís, C, Franco, R 2001Involvement of caveolin in ligand-induced recruitment and internalization of A1 adenosine receptors and adenosine deaminase in an epithelial cell lineMol Pharmacol5913141323PubMedGoogle Scholar
  38. Herrera, C, Casadó, V, Ciruela, F, Schofield, P, Mallol, J, Lluís, C, Franco, R 2001Adenosine A2B receptors behave as an alternative anchoring protein for cell surface adenosine deaminase in lymphocytes and cultured cellsMol Pharmacol59127134PubMedGoogle Scholar
  39. Hillion, J, Canals, M, Torvinen, M, Casadó, V, Scott, R, Terasmaa, A, Hansson, A, Watson, S, Olah, ME, Mallol, J, Canela, EI, Zoli, M, Agnati, LF, Ibáñez, CF, Lluis, C, Franco, R, Ferré, S, Fuxe, SS 2002Coaggregation, cointernalization and codesensitization of adenosine A2A receptors and dopamine D2 receptorsJ Biol Chem2771809118097PubMedCrossRefGoogle Scholar
  40. Kameoka, J, Tanaka, T, Nojima, Y, Schlossman, SF, Morimoto, C 1993Direct association of adenosine deaminase with a T cell activation antigen, CD26Science261466469PubMedCrossRefGoogle Scholar
  41. Lee, SP, Xie, Z, Varghese, G, Nguyen, T, O’Dowd, BF, George, SR 2000Oligomerization of dopamine and serotonin receptorsNeuropsychopharmacology233240CrossRefGoogle Scholar
  42. Lee, SP, Rashid, AJ, Varghese, G, Cheng, R, Lança, AJ, O’Dowd, BF, George, SR 2004Dopamine D1 and D2 receptor coactivation generates a novel phospholipase C-mediated calcium signalJ Biol Chem2793567135678PubMedCrossRefGoogle Scholar
  43. Lefkowitz, RJ 2000The superfamily of heptahelical receptorsNat Cell Biol2E133E136PubMedCrossRefGoogle Scholar
  44. Lezcano, N, Mrzljak, L, Eubanks, S, Levenson, R, Goldman-Rakic, P, Bergson, C 2000Dual signaling regulated by calcyon, a D1 dopamine receptor interacting proteinScience28716601664PubMedCrossRefGoogle Scholar
  45. Lluis, C, Cordero, O, Franco, R 1998Ecto-adenosine deaminase may play a relevant role in the development of the immune systemImmunology Today19533534PubMedCrossRefGoogle Scholar
  46. Lopes, LV, Cunha, RA, Kull, B, Fredholm, BB, Ribeiro, JA 2002Adenosine A(2A) receptor facilitation of hippocampal synaptic transmission is dependent on tonic A(1) receptor inhibitionNeuroscience112319329PubMedCrossRefGoogle Scholar
  47. Lu, D, Yan, H, Othman, T, Turner, CP, Woolf, T, Rivkees, SA 2004Cytoskeletal protein 4.1G binds to the third intracellular loop of the A1 adenosine receptor and inhibits receptor actionBiochem J3775159PubMedCrossRefGoogle Scholar
  48. Martín, M, Huguet, J, Centelles, JJ, Franco, R 1995Expression of ecto-adenosine deaminase and CD26 in human T cells triggered by the TCR/CD3 complex. Possible role of adenosine deaminase as co-stimulatory moleculeJ Immunol15546304643PubMedGoogle Scholar
  49. Mc Donald, PH, Lefkowitz, RJ 2001Betaarrestins: new roles in regulating heptahelical receptors’ functionCell Signal13683689CrossRefGoogle Scholar
  50. Mirabet, M, Herrera, C, Cordero, OJ, Mallol, J, Lluis, C, Franco, R 1999Expression of A2B adenosine receptors in human lymphocytes: their role in T cell activationJ Cell Science112491502PubMedGoogle Scholar
  51. Mistry, R, Golding, N, Challiss, RA 1998Regulation of phosphoinositide turnover in neonatal rat cerebral cortex by group I- and II- selective metabotropic glutamate receptor agonistsBr J Pharmacol123581589PubMedCrossRefGoogle Scholar
  52. Ng, GY, George, SR, Zastawny, RL, Caron, M, Bouvier, M, Dennis, M, O’Dowd, BF 1993Human serotonin1B receptor expression in Sf9 cells: phosphorylation, palmitoylation, and adenylyl cyclase inhibitionBiochemistry321172711733PubMedCrossRefGoogle Scholar
  53. Ng, GY, O’Dowd, BF, Caron, M, Dennis, M, Brann, MR, George, SR 1994aPhosphorylation and palmitoylation of the human D2L dopamine receptor in Sf9 cellsJ Neurochem6315891595CrossRefGoogle Scholar
  54. Ng, GY, Mouillac, B, George, SR, Caron, M, Dennis, M, Bouvier, M, O’Dowd, BF 1994bDesensitization, phosphorylation and palmitoylation of the human dopamine D1 receptorEur J Pharmacol267719CrossRefGoogle Scholar
  55. Ng, GY, O’Dowd, BF, Lee, SP, Chung, HT, Brann, S, Seeman, P, George, SR 1996Dopamine D2 receptor dimers and receptor-blocking peptidesBiochim Biophys Res Commun227200204CrossRefGoogle Scholar
  56. Ogata, T, Nakamura, Y, Tsuji, K, Shibata, T, Kataoka, K, Schubert, P 1994Adenosine enhances intracellular Ca2+ mobilization in conjunction with metabotropic glutamate receptor activation by t-ACPD in cultured hippocampal astrocytesNeurosci Lett17058PubMedCrossRefGoogle Scholar
  57. O’Kane, EM, Stone, TW 1998Interaction between adenosine A1 and A2 receptor-mediated responses in the rat hippocampus in vitroEur J Pharmacol3621725PubMedCrossRefGoogle Scholar
  58. Pacheco, R, Martinez-Navio, JM, Lejeune, M, Climent, N, Oliva, H, Gatell, JM, Gallart, T, Mallol, J, Lluis, C, Franco, R 2005CD26, adenosine deaminase, and adenosine receptors mediate costimulatory signals in the immunological synapseProc Natl Acad Sci USA10295839588PubMedCrossRefGoogle Scholar
  59. Parent, A, Hazrati, LN 1995Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loopBrain Res Brain Res Rev2091127PubMedCrossRefGoogle Scholar
  60. Quarta, D, Borycz, J, Solinas, M, Patkar, K, Hockemeyer, J, Ciruela, F, Lluis, C, Franco, R, Woods, AS, Goldberg, SR, Ferré, S 2004aAdenosine receptor-mediated modulation of dopamine release in the nucleus accumbens depends on glutamate neurotransmission and N-methyl-D-aspartate receptor stimulationJ Neurochem91873880CrossRefGoogle Scholar
  61. Quarta, D, Ferré, S, Solinas, M, You, Z-B, Hockemeyer, J, Popoli, P, Goldberg, SR 2004bOpposite modulatory roles for adenosine A1 and A2A receptors on glutamate and dopamine release in the shell of the nucleus accumbens. Effects of chronic caffeine exposureJ Neurochem8811511158CrossRefGoogle Scholar
  62. Rivkees, SA, Price, SL, Zhou, FC 1995Immunohistochemical detection of A1 adenosine receptors in rat brain with emphasis in localization in the hippocampal formation, cerebral cortex, cerebellum, and basal gangliaBrain Res677193203PubMedCrossRefGoogle Scholar
  63. Rocheville, M, Lange, DC, Kumar, U, Patel, SC, Patel, RC, Patel, YC 2000aReceptors for dopamine and somatostatin: formation of hetero-oligomers with enhanced functional activityScience288154157CrossRefGoogle Scholar
  64. Rocheville, M, Lange, DC, Kumar, U, Sasi, R, Patel, RC, Patel, YC 2000bSubtypes of the somatostatin receptor assemble as functional homo- and heterodimersJ Biol Chem27578627869CrossRefGoogle Scholar
  65. Ruiz, MA, Escriche, M, Lluis, C, Franco, R, Martin, M, Andres, A, Ros, M 2000Adenosine A1 receptor in cultured neurons from rat cerebral cortex: colocalization with adenosine deaminaseJ Neurochem75656664PubMedCrossRefGoogle Scholar
  66. Salim, ,  et al. 2000Activation of adenosine A1 and A2A receptors modulates dopamine D2 receptor-induced responses in stably transfected human neuroblastoma cellsJ Neurochem74432439PubMedCrossRefGoogle Scholar
  67. Sarrió, S, Casado, V, Escriche, M, Ciruela, F, Mallol, J, Canela, EI, Lluis, C, Franco, R 2000The heat shock cognate protein hsc73 assembles with A(1) adenosine receptors to form functional modules in the cell membraneMol Cell Biol2051645174PubMedCrossRefGoogle Scholar
  68. Saura, C, Ciruela, F, Casadó, V, Canela, EI, Mallol, J, Lluís, C, Franco, R 1996Adenosine deaminase interacts with A1 adenosine receptors in pig brain cortical membranesJ Neurochem6616751682PubMedCrossRefGoogle Scholar
  69. Saura, C, Mallol, J, Canela, EI, Lluís, C, Franco, R 1998Adenosine deaminase and A1 adenosine receptors internalize together following agonist-induced receptor desensitizationJ Biol Chem2711761017617CrossRefGoogle Scholar
  70. Schiffmann, SN, Jacobs, O, Vanderhaeghen, J-J 1991Striatal restricted adenosine A2 receptor (RDC8) is expressed by enkephalin but not by substance P neurons: an in situ hybridization histochemistry studyJ Neurochem5710621067PubMedCrossRefGoogle Scholar
  71. Schoepp, DD, Salhoff, CR, Wright, RA, Johnson, BG, Burnett, JP, Mayne, NG, Belagaje, R, Wu, S, Monn, JA 1996The novel metabotropic glutamate receptor agonist 2R,4R-APDC potentiates stimulation of phosphoinositide hydrolysis in the rat hippocampus by 3,5-dihydroxyphenylglycine: evidence for a synergistic interaction between group 1 and group 2 receptorsNeuropharmacology3516611672PubMedCrossRefGoogle Scholar
  72. So, CH, Varghese, G, Curley, KJ, Kong, MMC, Alijaniaram, M, Ji, X, Nguyen, T, O’Dowd, BF, George, SR 2005D1 and D2 dopamine receptors form heterooligomeres and cointernalize after selective activation of either receptorMol Pharmacol68568578PubMedGoogle Scholar
  73. Toda, S, Alguacil, LF, Kalivas, PW 2003Repeated cocaine adminsitration changes the function and subcellular distribution of adenosine A1 receptor in rat nucleus accumbensJ Neurochem8714781484PubMedCrossRefGoogle Scholar
  74. Toms, NJ, Roberts, PJ 1999Group 1 mGlu receptors elevate [Ca2+]i in rat cultured cortical type 2 astrocytes: [Ca2+]i synergy with adenosine A1 receptorsNeuropharmacology3815111517PubMedCrossRefGoogle Scholar
  75. Torvinen, M, Ginés, S, Hillion, J, Latini, S, Canals, M, Ciruela, F, Bordoni, F, Staines, W, Pedata, F, Agnati, LF, Lluis, C, Franco, R, Ferre, S, Fuxe, K 2002Interactions among adenosine deaminase, adenosine A1 receptors and dopamine D1 receptors in stably cotransfected fibroblast cells and neuronsNeuroscience113709719PubMedCrossRefGoogle Scholar
  76. Yoshioka, K, Sayito, O, Nakata, H 2001Heteromeric association creates a P2Y-like adenosine receptorPNAS9876177622PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • R. Franco
    • 1
  • C. Lluis
    • 1
  • E. I. Canela
    • 1
  • J. Mallol
    • 1
  • L. Agnati
    • 2
  • V. Casadó
    • 1
  • F. Ciruela
    • 1
  • S. Ferré
    • 3
  • K. Fuxe
    • 4
  1. 1.Molecular Neurobiology Unit, Department of Biochemistry and Molecular Biology, IDIBAPS (Institut d’Investigacions Biomèdiques August Pi i Sunyer)Universitat de BarcelonaBarcelonaSpain
  2. 2.Department of Biomedical SciencesUniversity of ModenaModenaItaly
  3. 3.Intramural Research Program, NIH, Department of Health and Human ServicesNational Institute on Drug AbuseBaltimoreUSA
  4. 4.Department of NeuroscienceKarolinska InstitutetStockholmSweden

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