Increased desensitization of dopamine D 2 receptor-mediated response in the ventral tegmental area in the absence of adenosine A 2A receptors

Neuroscience

Volumn 190, Issue , 2011, Pages 103-111

  Al Hasani, R ^a   Foster, J D ^a   Metaxas, A ^a   Ledent, C ^b   Hourani, S M O ^a   Kitchen, I ^a   Chen, Y ^a  

^a UNIVERSITY OF SURREY   (United Kingdom)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

A 2A receptor knockout mice; Adenosine A 2A receptor; D 2 receptor desensitization; Dopamine D 2 receptor; Dopamine neuron; Ventral tegmental area

Indexed keywords

2 [4 (2 CARBOXYETHYL)PHENETHYLAMINO]ADENOSINE 5' (N ETHYLCARBOXAMIDE); ADENOSINE A2A RECEPTOR; DOPAMINE; DOPAMINE 2 RECEPTOR; QUINPIROLE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC TRANSMISSION; INHIBITION KINETICS; KNOCKOUT MOUSE; MESENCEPHALON; MOUSE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; VENTRAL TEGMENTUM; WILD TYPE;

ANIMALS; DOPAMINE AGONISTS; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; MICE; MICE, KNOCKOUT; NEURONS; QUINPIROLE; RECEPTOR, ADENOSINE A2A; RECEPTORS, DOPAMINE D2; VENTRAL TEGMENTAL AREA;

EID: 80051592518     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.05.068     Document Type: Article

References (74)

1. Adell A., Artigas F. The somatodendritic release of dopamine in the ventral tegmental area and its regulation by afferent transmitter systems. Neurosci Biobehav Rev 2004, 28:415-431.
2. Azdad K., Gall D., Woods A.S., Ledent C., Ferre S., Schiffmann S.N. Dopamine D2 and adenosine A2A receptors regulate NMDA-mediated excitation in accumbens neurons through A2A-D2 receptor heteromerization. Neuropsychopharmacology 2009, 34:972-986.
3. Bailey A., Davis L., Lesscher H.M., Kelly M.D., Ledent C., Hourani S.M., Kitchen I. Enhanced morphine withdrawal and micro-opioid receptor G-protein coupling in A2A adenosine receptor knockout mice. J Neurochem 2004, 88:827-834.
4. Bailey A., Weber D., Zimmer A., Zimmer A.M., Hourani S.M., Kitchen I. Quantitative autoradiography of adenosine receptors and NBTI-sensitive adenosine transporters in the brains of mice deficient in the preproenkephalin gene. Brain Res 2004, 1025:1-9.
5. Bailey A., Gianotti R., Ho A., Kreek M.J. Downregulation of kappa-opioid receptors in basolateral amygdala and septum of rats withdrawn for 14 days from an escalating dose binge cocaine administration paradigm. Synapse 2007, 61:820-826.
6. Bartlett S.E., Enquist J., Hopf F.W., Lee J.H., Gladher F., Kharazia V., Waldhoer M., Mailliard W.S., Armstrong R., Bonci A., Whistler J.L. Dopamine responsiveness is regulated by targeted sorting of D2 receptors. Proc Natl Acad Sci U S A 2005, 102:11521-11526.
7. Beckstead M.J., Grandy D.K., Wickman K., Williams J.T. Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 2004, 42:939-946.
8. Beckstead M.J., Williams J.T. Long-term depression of a dopamine IPSC. J Neurosci 2007, 27:2074-2080.
9. Bernardini G.L., Gu X., German D.C. Nucleus A10 dopaminergic neurons in inbred mouse strains: firing rate and autoreceptor sensitivity are independent of the number of cells in the nucleus. Brain Res Bull 1991, 27:163-168.
10. Bonci A., Malenka R.C. Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area. J Neurosci 1999, 19:3723-3730.
11. Bouthenet M.L., Martres M.P., Sales N., Schwartz J.C. A detailed mapping of dopamine D-2 receptors in rat central nervous system by autoradiography with [125I]iodosulpride. Neuroscience 1987, 20:117-155.
12. Bowery B., Rothwell L.A., Seabrook G.R. Comparison between the pharmacology of dopamine receptors mediating the inhibition of cell firing in rat brain slices through the substantia nigra pars compacta and ventral tegmental area. Br J Pharmacol 1994, 112:873-880.
13. Boyer S.B., Clancy S.M., Terunuma M., Revilla-Sanchez R., Thomas S.M., Moss S.J., Slesinger P.A. Direct interaction of GABAB receptors with M2 muscarinic receptors enhances muscarinic signaling. J Neurosci 2009, 29:15796-15809.
14. Brown M.T., Henny P., Bolam J.P., Magill P.J. Activity of neurochemically heterogeneous dopaminergic neurons in the substantia nigra during spontaneous and driven changes in brain state. J Neurosci 2009, 29:2915-2925.
15. Bunney B.S., Walters J.R., Roth R.H., Aghajanian G.K. Dopaminergic neurons: effect of antipsychotic drugs and amphetamine on single cell activity. J Pharmacol Exp Ther 1973, 185:560-571.
16. Carta A., Casu S., Salaris S. Invited review: Current state of genetic improvement in dairy sheep. J Dairy Sci 2009, 92:5814-5833.
17. Castane A., Soria G., Ledent C., Maldonado R., Valverde O. Attenuation of nicotine-induced rewarding effects in A2A knockout mice. Neuropharmacology 2006, 51:631-640.
18. Centonze D., Usiello A., Gubellini P., Pisani A., Borrelli E., Bernardi G., Calabresi P. Dopamine D2 receptor-mediated inhibition of dopaminergic neurons in mice lacking D2L receptors. Neuropsychopharmacology 2002, 27:723-726.
19. Chen J.F., Beilstein M., Xu Y.H., Turner T.J., Moratalla R., Standaert D.G., Aloyo V.J., Fink J.S., Schwarzschild M.A. Selective attenuation of psychostimulant-induced behavioral responses in mice lacking A(2a) adenosine receptors. Neuroscience 2000, 97:195-204.
20. 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., Schwarzschild M.A. 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 2001, 98:1970-1975.
21. Chen J.F., Qin Z.H., Szele F., Bai G., Weiss B. Neuronal localization and modulation of the D2 dopamine receptor mRNA in brain of normal mice and mice lesioned with 6-hydroxydopamine. Neuropharmacology 1991, 30:927-941.
22. Chen Y., Phillips K., Minton G., Sher E. GABA(B) receptor modulators potentiate baclofen-induced depression of dopamine neuron activity in the rat ventral tegmental area. Br J Pharmacol 2005, 144:926-932.
23. Dalrymple M.B., Pfleger K.D., Eidne K.A. G protein-coupled receptor dimers: functional consequences, disease states and drug targets. Pharmacol Ther 2008, 118:359-371.
24. Dassesse D., Massie A., Ferrari R., Ledent C., Parmentier M., Arckens L., Zoli M., Schiffmann S.N. Functional striatal hypodopaminergic activity in mice lacking adenosine A(2A) receptors. J Neurochem 2001, 78:183-198.
25. de Filippi G., Mogg A.J., Phillips K.G., Zwart R., Sher E., Chen Y. The subtype-selective nicotinic acetylcholine receptor positive allosteric potentiator 2087101 differentially facilitates neurotransmission in the brain. Eur J Pharmacol 2010, 643:218-224.
26. Di Chiara G. The role of dopamine in drug abuse viewed from the perspective of its role in motivation. Drug Alcohol Depend 1995, 38:95-137.
27. Ferre S. Adenosine-dopamine interactions in the ventral striatum-implications for the treatment of schizophrenia. Psychopharmacology 1997, 133:107-120.
28. Ferre S., Quiroz C., Woods A.S., Cunha R., Popoli P., Ciruela F., Lluis C., Franco R., Azdad K., Schiffmann S.N. An update on adenosine A2A-dopamine D2 receptor interactions: implications for the function of G protein-coupled receptors. Curr Pharm Des 2008, 14:1468-1474.
29. Ferre 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, 88:7238-7241.
30. Filip M., Frankowska M., Zaniewska M., Przegalinski E., Muller C.E., Agnati L., Franco R., Roberts D.C., Fuxe K. Involvement of adenosine A2A and dopamine receptors in the locomotor and sensitizing effects of cocaine. Brain Res 2006, 1077:67-80.
31. Ford C.P., Gantz S.C., Phillips P.E., Williams J.T. Control of extracellular dopamine at dendrite and axon terminals. J Neurosci 2010, 30:6975-6983.
32. Fredholm B.B., Chen J.F., Masino S.A., Vaugeois J.M. Actions of adenosine at its receptors in the CNS: insights from knockouts and drugs. Annu Rev Pharmacol Toxicol 2005, 45:385-412.
33. Fredholm B.B., Ijzerman A.P., Jacobson K.A., Linden J., Muller C.E. International Union of Basic and Clinical Pharmacology. LXXXI. Nomenclature and classification of adenosine receptors-an update. Pharmacol Rev 2011, 63:1-34.
34. Grace A.A., Bunney B.S. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 1984, 4:2877-2890.
35. Grace A.A., Bunney B.S. Induction of depolarization block in midbrain dopamine neurons by repeated administration of haloperidol: analysis using in vivo intracellular recording. J Pharmacol Exp Ther 1986, 238:1092-1100.
36. Grace A.A., Onn S.P. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 1989, 9:3463-3481.
37. Hanyaloglu A.C., von Zastrow M. Regulation of GPCRs by endocytic membrane trafficking and its potential implications. Annu Rev Pharmacol Toxicol 2008, 48:537-568.
38. 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., Ferre S., Fuxe K. Coaggregation, cointernalization, and codesensitization of adenosine A2A receptors and dopamine D2 receptors. Chem 2002, 277:18091-18097.
39. Javitch J.A., Strittmatter S.M., Snyder S.H. Differential visualization of dopamine and norepinephrine uptake sites in rat brain using [3H] mazindol autoradiography. J Neurosci 1985, 5:1513-1521.
40. Johnson S.W., North R.A. Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 1992, 450:455-468.
41. Kalivas P.W., Churchill L., Klitenick M.A. GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area. Neuroscience 1993, 57:1047-1060.
42. Kitchen I., Slowe S.J., Matthes H.W., Kieffer B. Quantitative autoradiographic mapping of mu-, delta- and kappa-opioid receptors in knockout mice lacking the mu-opioid receptor gene. Brain Res 1997, 778:73-88.
43. Knapp C.M., Foye M.M., Cottam N., Ciraulo D.A., Kornetsky C. Adenosine agonists CGS 21680 and NECA inhibit the initiation of cocaine self-administration. Pharmacol Biochem Behav 2001, 68:797-803.
44. Kull B., Ferre 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, 58:1035-1045.
45. Ledent C., Vaugeois J.M., Schiffmann S.N., Pedrazzini T., El Yacoubi M., Vanderhaeghen J.J., Costentin J., Heath J.K., Vassart G., Parmentier M. Aggressiveness, hypoalgesia and high blood pressure in mice lacking the adenosine A(2a) receptor. Nature 1997, 388:674-678.
46. Lena I., Matthes H., Kieffer B., Kitchen I. Quantitative autoradiography of dopamine receptors in the brains of micro-opioid receptor knockout mice. Neurosci Lett 2004, 356:220-224.
47. Lu X.Y., Churchill L., Kalivas P.W. Expression of D1 receptor mRNA in projections from the forebrain to the ventral tegmental area. Synapse 1997, 25:205-214.
48. Margolis E.B., Coker A.R., Driscoll J.R., Lemaitre A.I., Fields H.L. Reliability in the identification of midbrain dopamine neurons. PLoS One 2010, 5:e15222.
49. Margolis E.B., Lock H., Hjelmstad G.O., Fields H.L. The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons?. J Physiol 2006, 577:907-924.
50. Mercuri N.B., Saiardi A., Bonci A., Picetti R., Calabresi P., Bernardi G., Borrelli E. Loss of autoreceptor function in dopaminergic neurons from dopamine D2 receptor deficient mice. Neuroscience 1997, 79:323-327.
51. Moore H., Todd C.L., Grace A.A. Striatal extracellular dopamine levels in rats with haloperidol-induced depolarization block of substantia nigra dopamine neurons. J Neurosci 1998, 18:5068-5077.
52. Nimitvilai S., Brodie M.S. Reversal of prolonged dopamine inhibition of dopaminergic neurons of the ventral tegmental area. J Pharmacol Exp Ther 2010, 333:555-563.
53. Overton P.G., Clark D. Burst firing in midbrain dopaminergic neurons. Brain Res Brain Res Rev 1997, 25:312-334.
54. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 2001, Academic Press, San Diego, CA. 2nd edition.
55. Pierce R.C., Kumaresan V. The mesolimbic dopamine system: the final common pathway for the reinforcing effect of drugs of abuse?. Neurosci Biobehav Rev 2006, 30:215-238.
56. Rimondini R., Ferre S., Ogren S.O., Fuxe K. Adenosine A2A agonists: a potential new type of atypical antipsychotic. Neuropsychopharmacology 1997, 17:82-91.
57. Rosin D.L., Hettinger B.D., Lee A., Linden J. Anatomy of adenosine A2A receptors in brain: morphological substrates for integration of striatal function. Neurology 2003, 61:S12-S18.
58. Rosin D.L., Robeva A., Woodard R.L., Guyenet P.G., Linden J. Immunohistochemical localization of adenosine A2A receptors in the rat central nervous system. J Comp Neurol 1998, 401:163-186.
59. Schiffmann S.N., Fisone G., Moresco R., Cunha R.A., Ferre S. Adenosine A2A receptors and basal ganglia physiology. Prog Neurobiol 2007, 83:277-292.
60. Schultz W. Getting formal with dopamine and reward. Neuron 2002, 36:241-263.
61. Schwarzschild M.A., Agnati L., Fuxe K., Chen J.F., Morelli M. Targeting adenosine A2A receptors in Parkinson's disease. Trends Neurosci 2006, 29:647-654.
62. Sebastiao A.M., Ribeiro J.A. Adenosine A2 receptor-mediated excitatory actions on the nervous system. Prog Neurobiol 1996, 48:167-189.
63. 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., Chen J.F. 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 2008, 28:2970-2975.
64. Shimazoe T., Yoshimatsu A., Kawashimo A., Watanabe S. Roles of adenosine A(1) and A(2A) receptors in the expression and development of methamphetamine-induced sensitization. Eur J Pharmacol 2000, 388:249-254.
65. Short J.L., Ledent C., Borrelli E., Drago J., Lawrence A.J. Genetic interdependence of adenosine and dopamine receptors: evidence from receptor knockout mice. Neuroscience 2006, 139:661-670.
66. Sibley D.R., Monsma F.J., Shen Y. Molecular neurobiology of dopaminergic receptors. Int Rev Neurobiol 1993, 35:391-415.
67. Soria D.R., Castane A., Ledent C., Parmentier M., Maldonado R., Valverde O. The lack of A2A adenosine receptors diminishes the reinforcing efficacy of cocaine. Neuropsychopharmacology 2006, 31:978-987.
68. Svenningsson P., Le Moine C., Fisone G., Fredholm B.B. Distribution, biochemistry and function of striatal adenosine A2A receptors. Prog Neurobiol 1999, 59:355-396.
69. Torvinen M., Torri C., Tombesi A., Marcellino D., Watson S., Lluis C., Franco R., Fuxe K., Agnati L.F. Trafficking of adenosine A2A and dopamine D2 receptors. J Mol Neurosci 2005, 25:191-200.
70. Vidi P.A., Chemel B.R., Hu C.D., Watts V.J. Ligand-Dependant Oligomerization of Dopamine D2 and Adenosine A2A Receptors in Living Neuronal Cells. Mol Pharmacol 2008, 74:544-551.
71. Wamsley J.K., Gehlert D.R., Filloux F.M., Dawson T.M. Comparison of the distribution of D-1 and D-2 dopamine receptors in the rat brain. J Chem Neuroanat 1989, 2:119-137.
72. Werner P., Hussy N., Buell G., Jones K.A., North R.A. D2, D3, and D4 dopamine receptors couple to G protein-regulated potassium channels in Xenopus oocytes. Mol Pharmacol 1996, 49:656-661.
73. White F.J., Wang R.Y. A10 dopamine neurons: role of autoreceptors in determining firing rate and sensitivity to dopamine agonists. Life Sci 1984, 34:1161-1170.
74. Wise R.A. Neurobiology of addiction. Curr Opin Neurobiol 1996, 6:243-251.