Heteromerization of dopamine D2 receptors with dopamine D1 or D5 receptors generates intracellular calcium signaling by different mechanisms

Current Opinion in Pharmacology

Volumn 10, Issue 1, 2010, Pages 93-99

  Hasbi, Ahmed ^b   O'Dowd, Brian F ^a,b   George, Susan R ^a,b  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; DOPAMINE 5 RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; INOSITOL TRISPHOSPHATE 3 RECEPTOR; PHOSPHOLIPASE C; RECEPTOR; UNCLASSIFIED DRUG;

BRAIN REGION; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CALCIUM TRANSPORT; CAVEOLA; CELLULAR DISTRIBUTION; DRUG DEPENDENCE; EXTRACELLULAR CALCIUM; HETEROMERIZATION; NONHUMAN; PATHOPHYSIOLOGY; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; SCHIZOPHRENIA; SEQUENCE HOMOLOGY;

ANIMALS; BRAIN; CALCIUM; CALCIUM SIGNALING; DOPAMINE; HUMANS; PROTEIN MULTIMERIZATION; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D5;

EID: 72449157561     PISSN: 14714892     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coph.2009.09.011     Document Type: Review

References (64)

1. Missale C., Nash S.R., Robinson S.W., Jaber M., and Caron M.G. Dopamine receptors: from structure to function. Physiol Rev 78 (1998) 189-225
2. Neve K.A., Seamans J.K., and Trantham-Davidson H. Dopamine receptor signaling. J Recept Signal Transduct Res 24 (2004) 165-205
3. Pivonello R., Ferone D., Lombardi G., Colao A., Lamberts S.W., and Hofland L.J. Novel insights in dopamine receptor physiology. Eur J Endocrinol Suppl 1 (2007) S13-S21 [Erratum in: Eur J Endocrinol 157:543]
4. Greengard P., Allen P.B., and Nairn A.C. Beyond the dopamine receptor: the DARPP-32/protein phosphatase-1 cascade. Neuron 23 (1999) 435-447
5. Beaulieu J.M., Sotnikova T.D., Marion S., Lefkowitz R.J., Gainetdinov R.R., and Caron M.G. An Akt/beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 122 (2005) 261-273
6. Park S.K., Nguyen M.D., Fischer A., Luke M.P., Affar el B., Dieffenbach P.B., Tseng H.C., Shi Y., and Tsai L.H. Par-4 links dopamine signaling and depression. Cell 122 (2005) 275-287
7. George S.R., and O'Dowd B.F. A novel dopamine receptor signaling unit in brain: heterooligomers of D1 and D2 dopamine receptors. Sci World J 7 (2007) 58-63
8. Rashid A.J., O'Dowd B.F., Verma V., and George S.R. Neuronal Gq/11-coupled dopamine receptors: an uncharted role for dopamine. Trends Pharmacol Sci 28 (2007) 551-555
9. So C.H., Verma V., Alijaniaram M., Cheng R., Rashid A.J., O'Dowd B.F., and George S.R. 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 (2009) 843-854. In this article the authors show that activation of the D5 receptor can trigger a calcium response and by the FRET technique that D2 and D5 receptors form heterooligomers. The D2-D5 heteromerization led to an inhibition of the robust, D5R-mediated calcium increase. This attenuation was inhibited when both D2R and D5R were concomitantly activated.
10. Jin L.Q., Goswami S., Cai G., Zhen X., and Friedman E. SKF83959 selectively regulates phosphatidylinositol-linked D1 dopamine receptors in rat brain. J Neurochem 85 (2003) 378-386
11. Undie A.S., and Friedman E. Stimulation of a dopamine D1 receptor enhances inositol phosphates formation in rat brain. J Pharmacol Exp Ther 253 (1990) 987-992
12. Lezcano N., and Bergson C. D1/D5 dopamine receptors stimulate intracellular calcium release in primary cultures of neocortical and hippocampal neurons. J Neurophysiol 87 (2002) 2167-2175
13. 2+ signaling in striatal medium spiny neurons. J Biol Chem 279 (2004) 42082-42094
14. Lee S.P., So C.H., Rashid A.J., Varghese G., Cheng R., Lanca A.J., O'Dowd B.F., and George S.R. Dopamine D1 and D2 receptor co-activation generates a novel phospholipase C-mediated calcium signal. J Biol Chem 279 (2004) 35671-35678
15. Rashid A.J., So C.H., Kong M.M., Furtak T., El-Ghundi M., Cheng R., O'Dowd B.F., and George S.R. D1-D2 dopamine receptor heterooligomers with unique pharmacology are coupled to rapid activation of Gq/11 in the striatum. Proc Natl Acad Sci U S A 104 (2007) 654-659. In this article, authors showed the activation of a signaling complex in brain through the costimulation of D1R and D2R in the heteromeric D1-D2 receptor complex. They also identified the D1 agonist SKF 83959 as a specific agonist for the heteromer, functioning as a full agonist for the D1R and a partial agonist for a pertussis toxin-resistant D2R in the heteromer. The activation of the D1-D2 heteromer increased calcium through Gq, PLC, and IP3-R and led to increased levels of phospho-CaMKIIα in the nucleus accumbens, a mechanism by which dopamine may contribute to synaptic plasticity.
16. So C.H., Varghese G., Curley K.J., Kong M.M., Alijaniaram M., Ji X., Nguyen T., O'Dowd B.F., and George S.R. D1 and D2 dopamine receptors form heterooligomers and co-internalize after selective activation of either receptor. Mol Pharmacol 68 (2005) 568-578
17. Dziedzicka-Wasylewska M., Faron-Górecka A., Andrecka J., Polit A., Kuśmider M., and Wasylewski Z. Fluorescence studies reveal heterodimerization of dopamine D1 and D2 receptors in the plasma membrane. Biochemistry 45 (2006) 8751-8759
18. Lee D., Huang W., and Lim A.T. Dopamine induces a biphasic modulation of hypothalamic ANF neurons: a ligand concentration-dependent effect involving D5 and D2 receptor interaction. Mol Psychiatry 5 (2000) 39-48
19. O'Sullivan G.J., Kinsella A., Sibley D.R., Tighe O., Croke D.T., and Waddington J.L. Ethological resolution of behavioural topography and D1-like versus D2-like agonist responses in congenic D5 dopamine receptor mutants: identification of D5:D2-like interactions. Synapse 55 (2005) 201-211
20. Ostrom R.S., and Insel P.A. The evolving role of lipid rafts and caveolae in G protein-coupled receptor signaling: implications for molecular pharmacology. Br J Pharmacol 143 (2004) 235-245
21. Insel P.A., Head B.P., Patel H.H., Roth D.M., Bundey R.A., and Swaney J.S. Compartmentation of G-protein-coupled receptors and their signalling components in lipid rafts and caveolae. Biochem Soc Trans 33 (2005) 1131-1134
22. Chini B., and Parenti M. G-protein-coupled receptors, cholesterol and palmitoylation: facts about fats. J Mol Endocrinol 42 (2009) 371-379
23. Kong M.M., Hasbi A., Mattocks M., Fan T., O'Dowd B.F., and George S.R. Regulation of D1 dopamine receptor trafficking and signaling by caveolin-1. Mol Pharmacol 72 (2007) 1157-1170
24. Oh P., and Schnitzer J.E. Immunoisolation of caveolae with high affinity antibody binding to the oligomeric caveolin cage. Toward understanding the basis of purification. J Biol Chem 274 (1999) 23144-23154 [Erratum in: J Biol Chem 274:29582]
25. Patel H.H., Murray F., and Insel P.A. G-protein-coupled receptor-signaling components in membrane raft and caveolae microdomains. Handb Exp Pharmacol 186 (2008) 167-184
26. Lee K.W., Kim Y., Kim A.M., Helmin K., Nairn A.C., and Greengard P. Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. Proc Natl Acad Sci U S A 103 (2006) 3399-3404
27. Gong S., Zheng C., Doughty M.L., Losos K., Didkovsky N., Schambra U.B., Nowak N.J., Joyner A., Leblanc G., Hatten M.E., and Heintz N. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425 (2003) 917-925
28. Lobo M.K., Karsten S.L., Gray M., Geschwind D.H., and Yang X.W. FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains. Nat Neurosci 9 (2006) 443-452
29. Shuen J.A., Chen M., Gloss B., and Calakos N. Drd1a-tdTomato BAC transgenic mice for simultaneous visualization of medium spiny neurons in the direct and indirect pathways of the basal ganglia. J Neurosci 28 (2008) 2681-2685
30. Bertran-Gonzalez J., Bosch C., Maroteaux M., Matamales M., Hervé D., Valjent E., and Girault J.A. Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci 28 (2008) 5671-5685. The authors used transgenic mice, in which EGFP expression was driven by D1R or D2R promoters in BAC (bacterial artificial chromosome) constructs. They confirmed the expression of D1R in striatonigral and D2R in striatopallidal neurons, with colocalization of D1 and D2R in up to 17% of neurons. D2R was also shown to be expressed in cholinergic interneurons, whereas no expression of either promoter was detected in GABAergic interneurons. They also demonstrated that cocaine and haloperidol used selective mechanisms to exert their short-term and long-term effects by specifically activating signaling pathways in the two segregated populations of striatal output neurons.
31. Matamales M., Bertran-Gonzalez J., Salomon L., Degos B., Deniau J.M., Valjent E., Hervé D., and Girault J.A. Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in BAC transgenic mice. PLoS One 4 (2009) e4770. The authors used bacterial artificial chromosome (BAC) transgenic mice expressing EGFP driven by D1R or D2R promoters and performed a quantitative analysis of striatal neurons in the drd1a-EGFP and drd2-EGFP mice. They showed that nuclear labeling was a simple method for identifying MSNs, and they confirmed that D1R and D2R were largely expressed in two populations of striatal neurons, however with an expression of both types of receptors, D1R and D2R in 5%, 6%, and 17%, in the dorsal striatum, core, and shell, respectively.
32. Aizman O., Brismar H., Uhlén P., Zettergren E., Levey A.I., Forssberg H., Greengard P., and Aperia A. Anatomical and physiological evidence for D1 and D2 dopamine receptor colocalization in neostriatal neurons. Nat Neurosci 3 (2000) 226-230
33. Shetreat M.E., Lin L., Wong A.C., and Rayport S. Visualization of D1 dopamine receptors on living nucleus accumbens neurons and their colocalization with D2 receptors. J Neurochem 66 (1996) 1475-1482
34. Wong A.C., Shetreat M.E., Clarke J.O., and Rayport S. D1- and D2-like dopamine receptors are colocalized on the presynaptic varicosities of striatal and nucleus accumbens neurons in vitro. Neuroscience 89 (1999) 221-233
35. 2+ signaling mechanism, which changed during the postnatal period.
36. Levey A.I., Hersch S.M., Rye D.B., Sunahara R.K., Niznik H.B., Kitt C.A., Price D.L., Maggio R., Brann M.R., Ciliax B.J., et al. Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. Proc Nat Acad Sci U S A 90 (1993) 8861-8865
37. Deng Y.P., Lei W.L., and Reiner A. Differential perikaryal localization in rats of D1 and D2 dopamine receptors on striatal projection neuron types identified by retrograde labeling. J Chem Neuroanat 32 (2006) 101-116
38. Hersch S.M., Ciliax B.J., Gutekunst C.A., Rees H.D., Heilman C.J., Yung K.K., Bolam J.P., Ince E., Yi H., and 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 15 (1995) 5222-5237
39. Capper-Loup C., Canales J.J., Kadaba N., and Graybiel A.M. Concurrent activation of dopamine D1 and D2 receptors is required to evoke neural and behavioral phenotypes of cocaine sensitization. J Neurosci 22 (2002) 6218-6227
40. Harsing Jr. L.G., and Zigmond M.J. Influence of dopamine on GABA release in striatum: evidence for D1-D2 interactions and non-synaptic influences. Neuroscience 77 (1997) 419-429
41. Hasbi A, Fan T, Alijaniaram M, Nguyen T, Perreault ML, O'Dowd BF, George SR: Calcium signaling cascade links dopamine D1-D2 receptor heteromer to striatal BDNF production and neuronal growth. Proc. Natl. Acad. Sci. In press. doi:10.1073_pnas.0903676106.
42. Berlanga M.L., Simpson T.K., and Alcantara A.A. Dopamine D5 receptor localization on cholinergic neurons of the rat forebrain and diencephalon: a potential neuroanatomical substrate involved in mediating dopaminergic influences on acetylcholine release. J Comp Neurol 492 (2005) 34-49
43. Bergson C., Mrzljak L., Smiley J.F., Pappy M., Levenson R., and Goldman-Rakic P.S. Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain. J Neurosci 15 (1995) 7821-7836
44. Ciliax B.J., Nash N., Heilman C., Sunahara R., Hartney A., Tiberi M., Rye D.B., Caron M.G., Niznik H.B., and Levey A.I. Dopamine D(5) receptor immunolocalization in rat and monkey brain. Synapse 2 (2000) 125-145
45. Rappaport M.S., Sealfon S.C., Prikhozhan A., Huntley G.W., and Morrison J.H. Heterogeneous distribution of D1, D2 and D5 receptor mRNAs in monkey striatum. Brain Res 616 (1993) 242-250
46. 2+ currents in rat neostriatal cholinergic interneurons through a membrane-delimited, protein kinase C-insensitive pathway. J Neurophysiol 77 (1997) 1003-1015
47. Alcantara A.A., Chen V., Herring B.H., Mendenhall J.M., and Berlanga M.L. Localization of dopamine D2 receptors on cholinergic interneurons of the dorsal striatum and nucleus accumbens of the rat. Brain Res 986 (2003) 22-29
48. Nicola S.M., Surmeier D.J., and Malenka R.C. Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23 (2000) 185-215
49. Wang Z., Kai L., Day M., Ronesi J., Yin H.H., Ding J., Tkatch T., Lovinger D.M., and Surmeier D.J. Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50 (2006) 443-452
50. Yao W.-D., Spealman R.D., and Zhang J. Dopaminergic signaling in dendritic spines. Biochem Pharmacol 75 (2008) 2055-2069. This is an excellent review, which presents an overview of dopaminergic system signaling and details the dopaminergic signaling in dendritic spines.
51. Sajikumar S., and Frey J.U. Resetting of 'synaptic tags' is time- and activity-dependent in rat hippocampal CA1 in vitro. Neuroscience 129 (2004) 503-507
52. Seamans J.K., and Yang C.R. The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74 (2004) 1-58
53. Calabresi P., Picconi B., Tozzi A., and Di Filippo M. Dopamine mediated regulation of corticostriatal synaptic plasticity. Trends Neurosci 30 (2007) 211-219
54. Friedman E., Jin L.Q., Cai G.P., Hollon T.R., Drago J., Sibley D.R., and Wang H.Y. D1-like dopaminergic activation of phosphoinositide hydrolysis is independent of D1A dopamine receptors: evidence from D1A knockout mice. Mol Pharmacol 51 (1997) 6-11
55. Montague D.M., Striplin C.D., Overcash J.S., Drago J., Lawler C.P., and Mailman R.B. Quantification of D1B(D5) receptors in dopamine D1A receptor-deficient mice. Synapse 39 (2001) 319-322
56. Lowetha J.A., Bakerb L.K., Guptaab T., Guillorya A.M., and Vezina P. Inhibition of CaMKII in the nucleus accumbens shell decreases enhanced amphetamine intake in sensitized rats. Neurosci Lett 444 (2008) 157-160
57. 2+/calmodulin-dependent protein kinase II pathway in the impairment of latent learning in a model of schizophrenia induced by phencyclidine. Mol Pharmacol 71 (2007) 1598-1609
58. Rushlow W.J., Seah C., Sutton L.P., Bjelica A., and Rajakumar N. Antipsychotics affect multiple calcium calmodulin dependent proteins. Neuroscience 161 (2009) 877-886
59. 2+ channels and CaMKII. They concluded that CaMKII may represent an essential link between shell dopaminergic and glutamatergic signaling and may be an important element in the neuronal plasticity involved in cocaine craving and relapse.
60. Seeman P., Niznik H.B., Guan H.C., Booth G., and Ulpian C. Link between D1 and D2 dopamine receptors is reduced in schizophrenia and Huntington diseased brain. Proc Natl Acad Sci U S A 86 (1989) 10156-10160
61. Lidow M.S. Calcium signaling dysfunction in schizophrenia: a unifying approach. Brain Res Brain Res Rev 43 (2003) 70-84
62. Centonze D., Grande C., Usiello A., Gubellini P., Erbs E., Martin A.B., Pisani A., Toqnazzi N., Bernardi G., Moratalla R., et al. Receptor subtypes involved in the presynaptic and postsynaptic actions of dopamine on striatal interneurons. J Neurosci 23 (2003) 6245-6254
63. Otani S., Daniel H., Roisin M.P., and Crepel F. Dopaminergic modulation of long-term synaptic plasticity in rat prefrontal neurons. Cereb Cortex 13 (2003) 1251-1256
64. Kreitzer A.C., and Malenka R.C. Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson's disease models. Nature 445 (2007) 643-647