Neurochemical evidence supporting dopamine D1–D2 receptor heteromers in the striatum of the long-tailed macaque: changes following dopaminergic manipulation

Brain Structure and Function

Volumn 222, Issue 4, 2017, Pages 1767-1784

  Rico, Alberto J ^a,b   Dopeso Reyes, Iria G ^a,b   Martínez Pinilla, Eva ^a,b   Sucunza, Diego ^a,b   Pignataro, Diego ^a,b   Roda, Elvira ^a,b   Marín Ramos, David ^a   Labandeira García, José L ^b,c   George, Susan R ^d   Franco, Rafael ^b,e   Lanciego, José L ^a,b  

^a UNIVERSITY OF NAVARRA   (Spain)

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

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Basal ganglia; Caudate nucleus; Dyskinesia; MPTP; Putamen

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; LEVODOPA; DOPAMINE;

ADULT; ARTICLE; CAUDATE NUCLEUS; CELL DENSITY; CONTROLLED STUDY; CORPUS STRIATUM; GOLGI COMPLEX; MACACA FASCICULARIS; MALE; NEUROCHEMISTRY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PUTAMEN; YOUNG ADULT; ANIMAL; METABOLISM; PARKINSONISM;

ANIMALS; CAUDATE NUCLEUS; CORPUS STRIATUM; DOPAMINE; MACACA FASCICULARIS; MALE; NUCLEUS ACCUMBENS; PARKINSONIAN DISORDERS; PUTAMEN; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2;

EID: 84986275908     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-016-1306-x     Document Type: Article

References (61)

1. Aizman O, Brismar H, Uhlen P, Zettergren E, Levey AI, Forssberg H, Greengard P, Aperia A (2000) Anatomical and physiological evidence for D1 and D2 dopamine receptor colocalization in neostriatal neurons. Nat Neurosci 3:226–230
2. Aubert I, Ghorayeb I, Normand E, Bloch B (2000) Phenotypical characterization of the neurons expressing the D1 and D2 dopamine receptors in the monkey striatum. J Comp Neurol 418:22–32
3. Aubert I, Guigoni G, Hakansson K, Li Q, Dovero S, Barthe N, Bioulac BH, Gross CE, Fisone G, Bloch B, Bezard E (2005) Increased D1 dopamine receptor signaling in levodopa-induced dyskinesia. Ann Neurol 57:17–26
4. Beaulieu JM, Espinoza S, Gainetdinov RR (2015) Dopamine receptors – IUPHAR Review 13. Br J Pharmacol 172:1–23
5. Bertran-Gonzalez J, Bosch C, Maroteaux M, Matamales M, Hervé D, Valjent E, Girault JA (2008) Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci 28:5671–5685
6. Bertran-Gonzalez J, Hervé D, Girault JA, Valjent E (2010) What is the degree of segregation between striatonigral and striatopallidal projections. Front Neuroanat 4:136
7. Bonaventura J, Rico AJ, Moreno E, Sierra S, Sánchez M, Luquin N, Farré D, Müller CE, Martínez-Pinilla E, Cortés A, Mallol J, Armentero MT, Pinna A, Canela EI, Lluís C, McCormick PJ, Lanciego JL, Casadó V, Franco R (2014) L-DOPA-treatment in primates disrupts the expression of A(2A) adenosine-CB(1) cannabinoid-D(2) dopamine receptor heteromers in the caudate nucleus. Neuropharmacol 79:90–100
8. Borroto-Escuela DO, Romero-Fernandez W, Tarakanov AO, Gómez-Soler M, Corrales F, Marcellino D, Narvaez M, Frankowska M, Flajolet M, Heintz N, Agnati LF, Ciruela F, Fuxe K (2010) Characterization of the A2AR-D2R interface: focus on the role of the C-terminal tail and the transmembrane heclices. Biochem Biophys Res Commun 402:801–807
9. Borroto-Escuela DO, Tarakanov AO, Guidolin D, Ciruela F, Agnati LF, Fuxe K (2011) Moonlighting characteristics of G protein-coupled receptors: focus on receptor heteromers and relevance for neurodegeneration. IUBMB Life 63:463–472
10. Boundy VA, Luedtke RR, Artymyshyn RP, Filtz TM, Molinoff PB (1993) Development of polyclonal anti-D2 dopamine receptor antibodies using sequence-specific peptides. Mol Pharmacol 43:666–676
11. Deng Y-P, Leim W-L, Reiner A (2006) Differential perikaryal localization in rats of D1 and D2 dopamine receptors on striatal projection neuron types identified by retrograde labeling. J Chem Neuroanat 32:101–116
12. Ding S, Li L, Zhou F-M (2015) Nigral dopamine loss induces a global upregulation of presynaptic dopamine D1 receptor facilitation of the striatonigral GABAergic output. J Neurophysiol 113:1697–1711
13. Dziedzicka-Wasylewska M, Faron-Górecka A, Andrecka J, Polit A, Kúsmider M, Wasylewski Z (2006) Fluorescence studies reveal heterodimerization of dopamine D1 and D2 receptors in the plasma membrane. Biochemistry 31:2424–2432
14. Farré D, Muñoz A, Moreno E, Reyes-Resina I, Canet-Pons J, Dopeso-Reyes IG, Rico AJ, Lluís C, Mallol J, Navarro G, Canela EI, Cortés A, Labandeira-García JL, Casadó V, Lanciego JL, Franco R (2015) Stronger dopamine D1 receptor-mediated neurotransmission in dyskinesia. Mol Neurobiol 52:1408–1420
15. Ferrada C, Ferré S, Casadó V, Cortés A, Justinova Z, Barnes C, Canela EI, Goldberg SR, Leurs R, Lluís C, Franco R (2008) Interactions between histamine H3 and dopamine D2 receptors and the implications for striatal function. Neuropharmacol 55:190–197
16. Ferrada C, Moreno E, Casadó V, Bongers G, Cortés A, Mallol J, Canela EI, Leurs R, Ferré S, Lluís C, Franco R (2009) Marked changes in signal transduction upon heteromerization of dopamine D1 and histamine H3 receptors. Br J Pharmacol 157:64–75
17. Fiorentini C, Busi C, Gorruso E, Gotti C, Spano P, Missale C (2008) Reciprocal regulation of dopamine D1 and D3 receptor function and trafficking by heterodimerization. Mol Pharmacol 74:59–69
18. Fiorentini C, Busi C, Spano P, Missale C (2010) Dimerization of dopamine D1 and D3 receptors in the regulation of striatal function. Curr Opin Pharmacol 10:87–92
19. Frederick A, Yano H, Trifilieff P, Vishwasrao HD, Biezonski D, Mészáros J, Urizar E, Sibley DR, Kellendonk C, Sonntag KC, Graham DL, Colbran RJ, Stanwood GD, Javitch JA (2015) Evidence against dopamine D1/D2 receptor heteromers. Mol Psychiatry 20:1373–1385
20. Fuenzalida J, Galaz P, Araya KA, Slater PG, Blanco EH, Campusano JM, Ciruela F, Gysling K (2014) Dopamine D1 and corticotrophin-releasing hormone type-2A receptors assemble into functionally interacting complexes in living cells. Br J Pharmacol 171:5650–5664
21. Gangarossa G, Espallergues J, Mailly P, De Bundel D, Kerchove d’Exaerde A, Hervé D, Girault JA, Valjent E, Krieger P (2013a) Spatial distribution of D1R- and D2R-expressing medium-sized spiny neurons differs along the rostro-caudal axis of the mouse dorsal striatum. Front Neural Circuits 7:124
22. Gangarossa G, Espallergues J, de Kerchove d’Exaerde A, El Mestikawy S, Gerfen CR, Hervé D, Girault JA, Valjent E (2013b) Distribution and compartmental organization of GABAergic medium-sized spiny neurons in the mouse nucleus accumbens. Front Neural Circuits 7:122
23. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, Monsma FJ, Sibley DR (1990) D1 and D2 dopamine receptor-regulated gene expression of striato-nigral and striato-pallidal neurons. Science 250:1429–1432
24. Ginés S, Hillion J, Torvinen M, Le Crom S, Casadó V, Canela EI, Rondin S, Lew JY, Watson S, Zoli M, Agnati LF, Verniera P, Lluís C, Ferré S, Fuxe K, Franco R (2000) Dopamine D1 and adenosine A1 receptors form functionally interacting heteromeric complexes. Proc Natl Acad Sci USA 97:8606–8611
25. González S, Rangel-Barajas C, Peper M, Lorenzo R, Moreno E, Ciruela F, Borcycz J, Ortiz J, Lluís C, Franco R, McCormick PJ, Volkow ND, Rubinstein M, Floran B, Ferré S (2012) Dopamine D4 receptor, but not the ADHD-associated D4.7 variant, forms functional heteromers with the dopamine D2S receptor in the brain. Mol Psychiatr 17:650–662
26. Guigoni C, Doudnikoff E, Li Q, Bloch B, Bezard E (2007) Altered D1 dopamine receptor trafficking in parkinsonian and dyskinetic non-human primates. Neurobiol Dis 26:452–463
27. Hasbi A, Fan T, Alijaniaram M, Nguyen T, Perreault ML, O’Dowd BF, George SR (2009) Calcium signaling cascade links dopamine D1–D2 receptor heteromer to striatal BDNF production and neuronal growth. Proc Natl Acad Sci USA 106:21377–21382
28. Hilion 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, Ibanez CF, Franco R, Ferré S, Fuxe K (2002) Coaggregation, cointernalization and codesensitization of adenosine A2A receptors and dopamine D2 receptors. J Biol Chem 277:18091–18097
29. Jiang H, Betancourt L, Smith RG (2006) Ghrelin amplifies dopamine signaling by cross talk involving formation of growth hormone secretagogue receptor/dopamine receptor subtype 1 heterodimers. Mol Endocrinol 20:1772–1785
30. Juhasz JR, Hasbi A, Rashid AJ, So CH, George SR, O’Dowd BF (2008) Mu-opioid receptor heterooligomer formation with dopamine D1 receptor as directly visualized in living cells. Eur J Pharmacol 581:235–243
31. Kurlan R, Kim MH, Gash DM (1991) Oral levodopa dose-response study in MPTP-induced hemiparkinsonian monkeys: assessment with a new rating scale for monkey parkinsonism. Mov Disord 6:111–118
32. Lanciego JL, Vázquez A (2012) 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 217:613–666
33. Le Moine C, Bloch B (1995) D1 and D2 dopamine receptor gene expression in the rat striatum: sensitive cRNA probes demonstrate prominent segregation of D1 and D2 mRNA in distinct neuronal populations of the dorsal and ventral striatum. J Comp Neurol 355:418–426
34. Lee SP, So CH, Rashid AJ, Varghese G, Cheng R, Lanca AJ, O’Dowd BF, George SR (2004) Dopamine D1 and D2 receptor Co-activation generates a novel phospholipase C-mediated calcium signal. J Biol Chem 279:35671–35678
35. Lukasiewicz S, Polit A, Kedracka-Krok S, Wedzony K, Mackowiak M, Dziedzicka-Wasylewska M (2010) Hetero-dimerization of serotonin 5-HT(2A) and dopamine D(2) receptors. Biochem Biophys Acta 1803:1347–1358
36. Lukasiewicz S, Faron-Górecka A, Kedracka-Krok S, Dziedzicka-Wasylewska M (2011) Effect of clozapine on the dimerization of serotonin 5HT(2A) receptor and its genetic variant 5-HT(2A)H425Y with dopamine D(2) receptor. Eur J Pharmacol 659:114–123
37. Marcellino D, Ferré S, Casadó V, Cortés A, Le Foll B, Mazzola C, Drago F, Saur O, Stark H, Soriano A, Barnes C, Goldberg SR, Lluís C, Fuxe K, Franco R (2008) Identification of dopamine D1-D3 receptor heteromers. Indications for a role of synergistic D1-D3 receptor interactions in the striatum. J Biol Chem 283:26016–26025
38. Martinez-Pinilla E, Reyes-Resina I, Oñatibia-Astibia A, Zamarbide M, Ricobaraza A, Navarro G, Moreno E, Dopeso-Reyes IG, Sierra S, Rico AJ, Roda E, Lanciego JL, Franco R (2014) CB1 and GPR55 receptors are co-expressed and form heteromers in rat and monkey striatum. Exp Neurol 261:44–52
39. Martinez-Pinilla E, Rodríguez-Pérez AI, Navarro G, Aguinaga D, Moreno E, Lanciego JL, Labandeira-García JL, Franco R (2015) Dopamine D2 and angiotensin II type 1 receptors form functional heteromers in rat striatum. Biochem Pharmacol 96:131–142
40. Moreno E, Vaz SH, Cai NS, Ferrada C, Quiroz C, Barodia SK, Kabbani N, Canela EI, McCormick PJ, Lluís C, Franco R, Ribeiro JA, Sebastiao AM, Moreno E, Hoffmann H, Gonzalez-Sepúlveda M, Navarro G, Casadó V, Cortés A, Mallol J, Vignes M, McCormick PJ, Canela EI, Lluís C, Moratalla R, Ferré S, Ortiz J, Franco R (2011a) Dopamine D1-histamine H3 receptor heteromers provide a selective link to MAPK signaling in GABAergic neurons of the direct striatal pathway. J Biol Chem 286:5846–5854
41. Moreno E, Vaz SH, Cai NS, Ferrada C, Quiroz C, Barodia SK, Kabbani N, Canela EI, McCormick PJ, Llluís C, Franco R, Ribeiro JA, Sebastiao AM, Ferré S (2011b) Dopamine-galanin receptor heteromers modulate cholinergic neurotransmission in the rat ventral hippocampus. J Neurosci 31:7412–7423
42. Navarro G, Carriba P, Gandía J, Ciruela F, Casadó V, Cortés A, Mallol J, Canela EI, Lluís C, Franco R (2008) Detection of heteromers formed by cannabinoid CB1, dopamine D2 and adenosine A2A G-protein-coupled receptors by combining biomolecular fluorescence complementation and bioluminescence energy transfer. Sci World J 8:1088–1097
43. Ng J, Rashid AJ, So CH, O’Dowd BF, George SR (2010) Activation of calcium/calmodulin-dependent protein kinase II alpha in the striatum by the heteromeric D1–D2 dopamine receptor complex. Neuroscience 165:535–541
44. O’Dowd BF, Ji X, Nguyen T, George SR (2012) Two aminoacids in each of D1 and D2 dopamine receptor cytoplasmic regions are involved in D1–D2 heteromer formation. Biochem Biophys Res Commun 417:23–28
45. Pei L, Li S, Wang M, Diwan M, Anisman H, Fletcher PJ, Nobrega JN, Liu F (2010) Uncoupling the dopamine D1–D2 receptor complex exerts antidepressant-like effects. Nat Med 16:1393–1395
46. Perreault ML, Hasbi A, O’Dowd BF, George SR (2011) The dopamine D1–D2 receptor heteromer in striatal medium spiny neurons: evidence for a third distinct neuronal pathway in basal ganglia. Front Neuroanat 5:31
47. Perreault ML, Fan T, Alijaniaram M, O’Dowd BF, George SR (2012) Dopamine D1–D2 receptor heteromer in dual phenotype GABA/glutamate-coexpressing striatal medium spiny neurons: regulation of BDNF, GAD67 and VGLUT1/2. PLoS ONE 7:e33348
48. Perrreault ML, Hasbi A, Alijaniaram M, Fan T, Varghese G, Fletcher PJ, Seeman P, O’Dowd BF, George SR (2010) The dopamine D1–D2 receptor heteromer localizes in dynorphin/enkephalin neurons: increased high affinity state following amphetamine and in schizophrenia. J Biol Chem 285:36625–36634
49. Pinna A, Bonaventura J, Farré D, Sánchez M, Simola N, Mallol J, Lluís C, Costa G, Baqi Y, Müller CE, Cortés A, McCormick PJ, Canela EI, Martínez-Pinilla E, Lanciego JL, Casadó V, Armentero MT, Franco R (2014) L-DOPA disrupts adenosine A(2A)-cannabinoid CB(1)-dopamine D(2) receptor heteromer cross-talk in the striatum of hemiparkinsonian rats: biochemical and behavioral studies. Exp Neurol 253:180–191
50. Przybyla JA, Watts VJ (2009) Ligand-induced regulation and localization of cannabinoid CB1 and dopamine D2L receptor heterodimers. J Pharmacol Exp Ther 332:710–719
51. Rashid AJ, So CH, Kong MM, Furtak T, El-Ghundi M, Cheng R, O’Dowd BF, George SR (2007) D1–D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc Natl Acad Sci USA 104:654–659
52. Scarselli M, Novi F, Schallmach E, Lin R, Baragli A, Colzi A, Griffon N, Corsini GU, Sokoloff P, Levenson R, Vogel Z, Maggio R (2001) D2/D3 dopamine receptor heterodimers exhibit unique functional properties. J Biol Chem 276:30308–30314
53. Schellenkens H, van Oeffelen WE, Dinan TG, Cryan JF (2013) Promiscuous dimerization of the growth hormone secretatogue receptor (GHS-R1a) attenuates ghrelin-mediated signaling. J Biol Chem 288:181–191
54. Shen J, Zhang L, Song WL, Meng T, Wang X, Chen L, Feng LY, Xu YC, Shen JK (2013) Design, synthesis and biological evaluation of bivalent ligands against A(1)-D(1) receptor heteromers. Acta Pharmacol Sin 34:441–452
55. Sierra S, Luquin N, Rico AJ, Gómez-Bautista V, Roda E, Dopeso-Reyes IG, Vázquez A, Martínez-Pinilla E, Labandeira-García JL, Franco R, Lanciego JL (2015) Detection of cannabinoid receptors CB1 and CB2 within basal ganglia output neurons in macaques: changes following experimental parkinsonism. Brain Struct Funct 220:2721–2738
56. So CH, Varghese C, Curley KJ, Kong MM, Alijaniaram M, Ji X, Nguyen T, O’Dowd BF, George SR (2005) D1 and D2 dopamine receptors form heterooligomers and cointernalize after selective activation of either receptor. Mol Pharmacol 68:568–578
57. So CH, Verma V, Alijaniaram M, Cheng R, Rashid AJ, O’Dowd BF, George SR (2009) Calcium signaling by dopamine D5 receptor and D5-D2 receptor hetero-oligomers occurs by a mechanism distinct from that for dopamine D1–D2 receptor hetero-oligomers. Mol Pharmacol 75:843–854
58. Söderberg O, Leuchowius KJ, Gullberg M, Jarvius M, Weibrecht I, Larsson LG, Landegren U (2008) Characterizing proteins and their interaction in cells and tissues using the in situ proximity ligation assay. Methods 45:227–232
59. Trifilieff P, Rives ML, Urizar E, Piskorowski RA, Vishwasrao HD, Castrillon J, Schmauss C, Slattman M, Gulberg M, Javitch JA (2011) Detection of antigen interactions ex vivo by proximity ligation assay: endogenous dopamine D2-adenosine A2A receptor interactions in the striatum. Biotechniques 51:111–118
60. Verma V, Hasbi A, O’Dowd BF, George SR (2010) Dopamine D1–D2 receptor heteromer-mediated calcium release is desensitized by D1 receptor occupancy with or without signal activation: dual functional regulation by G protein-coupled receptor kinase 2. J Biol Chem 285:35092–35103
61. Wang H, Pickel VM (2002) Dopamine D2 receptors are present in prefrontal cortical afferents and their targets in patches of the rat caudate-putamen nucleus. J Comp Neurol 442:392–404