Combined antagonism of glutamate mGlu5 and adenosine A2A receptors interact to regulate alcohol-seeking in rats

International Journal of Neuropsychopharmacology

Volumn 11, Issue 2, 2008, Pages 229-241

  Adams, Cameron L ^a,b   Cowen, Michael S ^b,c   Short, Jennifer L ^a   Lawrence, Andrew J ^b,c  

^a MONASH UNIVERSITY   (Australia)

^b FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Adenosine A2A receptor; Alcohol; Glutamate mGlu5 receptor; Reinstatement; Self administration

Indexed keywords

3 [(2 METHYL 4 THIAZOLYL)ETHYNYL]PYRIDINE; 5 AMINO 2 (2 FURYL) 7 (2 PHENYLETHYL)PYRAZOLO[4,3 E][1,2,4]TRIAZOLO[1,5 C]PYRIMIDINE; 8 CYCLOPENTYL 1,3 DIPROPYLXANTHINE; ADENOSINE A2A RECEPTOR; METABOTROPIC RECEPTOR 5;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; INSTRUMENTAL CONDITIONING; LOCOMOTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; RAT;

ADENOSINE; ALCOHOL DRINKING; ANIMALS; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM DEPRESSANTS; CONDITIONING, OPERANT; CUES; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; EXTINCTION, PSYCHOLOGICAL; GLUTAMIC ACID; MODELS, ANIMAL; MOTOR ACTIVITY; PYRIDINES; PYRIMIDINES; RATS; RATS, INBRED STRAINS; REACTION TIME; RECEPTOR, ADENOSINE A1; RECEPTOR, ADENOSINE A2A; RECEPTORS, METABOTROPIC GLUTAMATE; SELF ADMINISTRATION; THIAZOLES; TIME FACTORS; TRIAZOLES; XANTHINES;

EID: 38949186761     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1017/S1461145707007845     Document Type: Article

References (87)

1. Agnati LF, Ferre S, Lluis C, Franco R, Fuxe K (2003). Molecular mechanisms and therapeutical implications of intramembrane receptor/receptor interactions among heptahelical receptors with examples from the striatopallidal GABA neurons. Pharmacological Reviews 55, 509-550.
2. 3H] Methoxymethyl-3-[(2-methyl-1,3-thiazol-4-yl)ethynyl]pyridine binding to metabotropic glutamate receptor subtype 5 in rodent brain : in vitro and in vivo characterization. Journal of Pharmacology and Experimental Therapeutics 303, 1044-1051.
3. Anton RF (2001). Pharmacologic approaches to the management of alcoholism. Journal of Clinical Psychiatry 62 (Suppl. 20), 11-17.
4. Aoki T, Narita M, Shibasaki M, Suzuki T (2004). Metabotropic glutamate receptor 5 localized in the limbic forebrain is critical for the development of morphine-induced rewarding effect in mice. European Journal of Neuroscience 20, 1633-1638.
5. Arolfo MP, Yao L, Gordon AS, Diamond I, Janak PH (2004). Ethanol operant self-administration in rats is regulated by adenosine A2 receptors. Alcoholism: Clinical and Experimental Research 28, 1308-1316.
6. Backstrom P, Bachteler D, Koch S, Hyytia P, Spanagel R (2004). mGluR5 antagonist MPEP reduces ethanol-seeking and relapse behavior. Neuropsychopharmacology 29, 921-928.
7. Backstrom P, Hyytia P (2004). Ionotropic glutamate receptor antagonists modulate cue-induced reinstatement of ethanol-seeking behavior. Alcoholism : Clinical and Experimental Research 28, 558-565.
8. Baldo BA, Koob GF, Markou A (1999). Role of adenosine A2 receptors in brain stimulation reward under baseline conditions and during cocaine withdrawal in rats. Journal of Neuroscience 19, 11017-11026.
9. Balschun D, Wetzel W (2002). Inhibition of mGluR5 blocks hippocampal LTP in vivo and spatial learning in rats. Pharmacology Biochemistry and Behavior 73, 375-380.
10. Batista LC, Prediger RD, Morato GS, Takahashi RN (2005). Blockade of adenosine and dopamine receptors inhibits the development of rapid tolerance to ethanol in mice. Psychopharmacology (Berlin) 181, 714-721.
11. Bradbury MJ, Campbell U, Giracello D, Chapman D, King C, Tehrani L, Cosford ND, Anderson J, Varney MA, Strack AM (2005). Metabotropic glutamate receptor mGlu5 is a mediator of appetite and energy balance in rats and mice. Journal of Pharmacology and Experimental Therapeutics 313, 395-402.
12. Brodkin J, Busse C, Sukoff SJ, Varney MA (2002). Anxiolytic-like activity of the mGluR5 antagonist MPEP: A comparison with diazepam and buspirone. Pharmacology Biochemistry and Behavior 73, 359-366.
13. Busse CS, Brodkin J, Tattersall D, Anderson JJ, Warren N, Tehrani L, Bristow LJ, Varney MA, Cosford ND (2004). The behavioral profile of the potent and selective mGlu5 receptor antagonist 3-[(2-methyl-1,3-thiazol-4-yl) ethynyl]pyridine (MTEP) in rodent models of anxiety. Neuropsychopharmacology 29, 1971-1979.
14. Choi D-S, Cascini M-G, Mailliard W, Young H, Paredes P, McMahon T, Diamond I, Bonci A, Messing RO (2004). The type 1 equilibrative nucleoside transporter regulates ethanol intoxication and preference. Nature Neuroscience 7, 855-861.
15. Ciruela F, Casado V, Rodrigues RJ, Lujan R, Burgueno J, Canals M, Borycz J, Rebola N, Goldberg SR, Mallol J, et al. (2006a). Presynaptic control of striatal glutamatergic neurotransmission by adenosine A1-A2A receptor heteromers. Journal of Neuroscience 26, 2080-2087.
16. Ciruela F, Ferre S, Casado V, Cortes A, Cunha RA, Lluis C, Franco R (2006b). Heterodimeric adenosine receptors : a device to regulate neurotransmitter release. Cellular and Molecular Life Sciences 63, 2427-2431.
17. Coccurello R, Breysse N, Amalric M (2004). Simultaneous blockade of adenosine A2A and metabotropic glutamate mGlu5 receptors increase their efficacy in reversing Parkinsonian deficits in rats. Neuropsychopharmacology 29, 1451-1461.
18. Conn PJ, Pin JP (1997). Pharmacology and functions of metabotropic glutamate receptors. Annual Review of Pharmacology and Toxicology 37, 205-237.
19. Cosford ND, Tehrani L, Roppe J, Schweiger E, Smith ND, Anderson J, Bristow L, Brodkin J, Jiang X, McDonald I, et al. (2003). 3-[(2-Methyl-1,3-thiazol-4-yl)ethynyl]-pyridine: a potent and highly selective metabotropic glutamate subtype 5 receptor antagonist with anxiolytic activity. Journal of Medicinal Chemistry 46, 204-206.
20. Cowen MS, Adams C, Kraehenbuehl T, Vengeliene V, Lawrence AJ (2005a). The acute anti-craving effect of acamprosate in alcohol-preferring rats is associated with modulation of the mesolimbic dopamine system. Addiction Biology 10, 233-242.
21. Cowen MS, Djouma E, Lawrence AJ (2005b). The mGlu5 antagonist MTEP reduces ethanol self-administration in multiple strains of alcohol-preferring rats and regulates olfactory glutamatergic systems. Journal of Pharmacology and Experimental Therapeutics 315, 590-600.
22. Cowen MS, Krstew E, Lawrence AJ (2007). Assessing appetitive and consummatory phases of ethanol self-administration in C57BL/6J mice under operant conditions : regulation by mGlu5 receptor antagonism. Psychopharmacology 190, 21-29.
23. El Yacoubi M, Costentin J, Vaugeois JM (2003). Adenosine A2A receptors and depression. Neurology 61 (Suppl. 6), S82-87.
24. El Yacoubi M, Ledent C, Parmentier M, Bertorelli R, Ongini E, Costentin J, Vaugeois JM (2001a). Adenosine A2A receptor antagonists are potential antidepressants : evidence based on pharmacology and A2A receptor knockout mice. British Journal of Pharmacology 134, 68-77.
25. El Yacoubi M, Ledent C, Parmentier M, Daoust M, Costentin J, Vaugeois J (2001b). Absence of the adenosine A(2A) receptor or its chronic blockade decrease ethanol withdrawal-induced seizures in mice. Neuropharmacology 40, 424-432.
26. Ferre S, Karcz-Kubicha M, Hope BT, Popoli P, Burgueno J, Gutierrez MA, Casado V, Fuxe K, Goldberg SR, Lluis C, et al. (2002). Synergistic interaction between adenosine A2A and glutamate mGlu5 receptors : implications for striatal neuronal function. Proceedings of the National Academy of Sciences USA 99, 11940-11945.
27. Fredholm BB, Arslan G, Halldner L, Kull B, Schulte G, Wasserman W (2000). Structure and function of adenosine receptors and their genes. Naunyn-Schmiedeberg's Archives of Pharmacology 362, 364-374.
28. Garbutt JC, West SL, Carey TS, Lohr KN, Crews FT (1999). Pharmacological treatment of alcohol dependence: a review of the evidence. Journal of the American Medical Association 281, 1318-1325.
29. Hermans E, Challiss RA (2001). Structural, signalling and regulatory properties of the group I metabotropic glutamate receptors : prototypic family C G-protein-coupled receptors. Biochemistry Journal 359, 465-484.
30. Hodge CW, Miles MF, Sharko AC, Stevenson RA, Hillmann JR, Lepoutre V, Besheer J, Schroeder JP (2006). The mGluR5 antagonist MPEP selectively inhibits the onset and maintenance of ethanol self-administration in C57BL/6J mice. Psychopharmacology 183, 429-438.
31. Jin S, Johansson B, Fredholm BB (1993). Effects of adenosine A1 and A2 receptor activation on electrically evoked dopamine and acetylcholine release from rat striatal slices. Journal of Pharmacology and Experimental Therapeutics 267, 801-808.
32. Justinova Z, Ferre S, Segal PN, Antoniou K, Solinas M, Pappas LA, Highkin JL, Hockemeyer J, Munzar P, Goldberg SR (2003). Involvement of adenosine A1 and A2A receptors in the adenosinergic modulation of the discriminative-stimulus effects of cocaine and methamphetamine in rats. Journal of Pharmacology and Experimental Therapeutics 307, 977-986.
33. Kachroo A, Orlando LR, Grandy DK, Chen J-F, Young AB, Schwarzschild MA (2005). Interactions between metabotropic glutamate 5 and adenosine A2A receptors in normal and parkinsonian mice. Journal of Neuroscience 25, 10414-10419.
34. Kalivas PW, McFarland K (2003). Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology (Berlin) 168, 44-56.
35. Kaplan GB, Bharmal NH, Leite-Morris KA, Adams WR (1999). Role of adenosine A1 and A2A receptors in the alcohol withdrawal syndrome. Alcohol 19, 157-162.
36. Kenny PJ, Boutrel B, Gasparini F, Koob GF, Markou A (2005). Metabotropic glutamate 5 receptor blockade may attenuate cocaine self-administration by decreasing brain reward function in rats. Psychopharmacology 179, 247-254.
37. Klodzinska A, Tatarczynska E, Chojnacka-Wojcik E, Nowak G, Cosford ND, Pilc A (2004). Anxiolytic-like effects of MTEP, a potent and selective mGlu5 receptor agonist does not involve GABA(A) signaling. Neuropharmacology 47, 342-350.
38. Kniazeff J, Bessis AS, Maurel D, Ansanay H, Prezeau L, Pin JP (2004). Closed state of both binding domains of homodimeric mGlu receptors is required for full activity. Nature Structural and Molecular Biology 11, 706-713.
39. Kranzler HR, Van Kirk J (2001). Efficacy of naltrexone and acamprosate for alcoholism treatment: a meta-analysis. Alcoholism : Clinical and Experimental Research 25, 1335-1341.
40. Kull B, Ferre S, Arslan G, Svenningsson P, Fuxe K, Owman C, Fredholm BB (1999). Reciprocal interactions between adenosine A2A and dopamine D2 receptors in Chinese hamster ovary cells co-transfected with the two receptors. Biochemical Pharmacology 58, 1035-1045.
41. Lawrence AJ, Cowen MS, Yang HJ, Chen F, Oldfield B (2006). The orexin system regulates alcohol-seeking in rats. British Journal of Pharmacology 148, 752-759.
42. Ledent C, Vaugeois JM, Schiffmann SN, Pedrazzini T, El Yacoubi M, Vanderhaeghen JJ, Costentin J, Heath JK, Vassart G, Parmentier M (1997). Aggressiveness, hypoalgesia and high blood pressure in mice lacking the adenosine A2A receptor. Nature 388, 674-678.
43. Li X, Need AB, Baez M, Witkin JM (2006). Metabotropic glutamate 5 receptor antagonism is associated with antidepressant-like effects in mice. Journal of Pharmacology and Experimental Therapeutics 319, 254-259.
44. Liang JH, Chen F, Krstew E, Cowen MS, Carroll FY, Crawford D, Beart PM, Lawrence AJ (2006). The GABA(B) receptor allosteric modulator CGP7930, like baclofen, reduces operant self-administration of ethanol in alcohol-preferring rats. Neuropharmacology 50, 632-639.
45. Lu YM, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM, Roder JC (1997). Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 longterm potentiation (LTP) but normal CA3 LTP. Journal of Neuroscience 17, 5196-5205.
46. McBride WJ, Li TK (1998). Animal models of alcoholism: neurobiology of high alcohol-drinking behavior in rodents. Critical Reviews in Neurobiology 12, 339-369.
47. Mcgeehan AJ, Olive MF (2003). The anti-relapse compound acamprosate inhibits the development of a conditioned place preference to ethanol and cocaine but not morphine. British Journal of Pharmacology 138, 9-12.
48. McKinzie DL, Nowak KL, Yorger L, McBride WJ, Murphy JM, Lumeng L, Li TK (1998). The alcohol deprivation effect in the alcohol-preferring P rat under free-drinking and operant access conditions. Alcoholism: Clinical and Experimental Research 22, 1170-1176.
49. McPherson CS, Lawrence AJ (2006). Exposure to amphetamine in rats during periadolescence establishes behavioural and extrastriatal neural sensitization in adulthood. International Journal of Neuropsychopharmacology 9, 377-392.
50. Meng ZH, Anwer J, Dar MS (1997). The striatal adenosinergic modulation of ethanol-induced motor incoordination in rats : possible role of chloride flux. Brain Research 776, 235-245.
51. Miller CA, Marshall JF (2005). Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory. Neuron 47, 873-884.
52. Murphy JM, Stewart RB, Bell RL, Badia-Elder NE, Carr LG, McBride WJ, Lumeng L, Li T-K (2002). Phenotypic and genotypic characterization of the Indiana University rat lines selectively bred for high and low alcohol preference. Behavior Genetics 32, 363-388.
53. Naassila M, Ledent C, Daoust M (2002). Low ethanol sensitivity and increased ethanol consumption in mice lacking adenosine A2A receptors. Journal of Neuroscience 22, 10487-10493.
54. Nagel J, Schladebach H, Koch M, Schwienbacher I, Muller CE, Hauber W (2003). Effects of an adenosine A2A receptor blockade in the nucleus accumbens on locomotion, feeding, and prepulse inhibition in rats. Synapse 49, 279-286.
55. National Institute on Alcohol Abuse and Alcoholism (2004). Alcholism, Getting the Facts. Bethesda, MD: National Institute of Health.
56. Nishi A, Liu F, Matsuyama S, Hamada M, Higashi H, Nairn AC, Greengard P (2003). Metabotropic mGlu5 receptors regulate adenosine A2A receptor signaling. Proceedings of the National Academy of Sciences USA 100, 1322-1327.
57. Olive MF, McGeehan AJ, Kinder JR, McMahon T, Hodge CW, Janak PH, Messing RO (2005). The mGluR5 antagonist 6-methyl-2-(phenylethynyl)pyridine decreases ethanol consumption via a protein kinase C epsilon-dependent mechanism. Molecular Pharmacology 67, 349-355.
58. Ongini E, Fredholm BB (1996). Pharmacology of adenosine A2A receptors. Trends in Pharmacological Sciences 17, 364-372.
59. 3H]MethoxyPyEP, an mGluR5 selective radioligand. Life Sciences 73, 371-379.
60. Paterson NE, Semenova S, Gasparini F, Markou A (2003). The mGluR5 antagonist MPEP decreased nicotine self-administration in rats and mice. Psychopharmacology (Berlin) 167, 257-264.
61. Pilc A, Klodzinska A, Branski P, Nowak G, Palucha A, Szewczyk B, Tatarczynska E, Chojnacka-Wojcik E, Wieronska JM (2002). Multiple MPEP administrations evoke anxiolytic- and antidepressant-like effects in rats. Neuropharmacology 43, 181-187.
62. Quiroz C, Gomes C, Pak AC, Ribeiro JA, Goldberg SR, Hope BT, Ferre S (2006). Blockade of adenosine A2A receptors prevents protein phosphorylation in the striatum induced by cortical stimulation. Journal of Neuroscience 26, 10808-10812.
63. Rodd-Henricks ZA, McKinzie DL, Murphy JM, McBride WJ, Lumeng L, Li TK (2000). The expression of an alcohol deprivation effect in the high-alcohol-drinking replicate rat lines is dependent on repeated deprivations. Alcoholism : Clinical and Experimental Research 24, 747-753.
64. Rodrigues RJ, Alfaro TM, Rebola N, Oliveira CR, Cunha RA (2005). Co-localization and functional interaction between adenosine A and metabotropic group 5 receptors in glutamatergic nerve terminals of the rat striatum. Journal of Neurochemistry 92, 433-441.
65. Rosin DL, Robeva A, Woodard RL, Guyenet PG, Linden J (1998). Immunohistochemical localization of adenosine A2A receptors in the rat central nervous system. Journal of Comparative Neurology 401, 163-186.
66. Samson HH, Files FJ, Denning C, Marvin S (1998). Comparison of alcohol-preferring and nonpreferring selectively bred rat lines. Alcoholism: Clinical and Experimental Research 22, 2133-2146.
67. Samson HH, Pfeffer AO, Tolliver GA (1988). Oral ethanol self-administration in rats : models of alcohol-seeking behavior. Alcoholism : Clinical and Experimental Research 12, 591-598.
68. Sanchis-Segura C, Borchardt T, Vengeliene V, Zghoul T, Bachteler D, Gass P, Sprengel R, Spanagel R (2006). Involvement of the AMPA receptor GluR-C subunit in alcohol-seeking behavior and relapse. Journal of Neuroscience 26, 1231-1238.
69. Schroeder JP, Overstreet DH, Hodge CW (2005). The mGluR5 antagonist MPEP decreases operant ethanol self-administration during maintenance and after repeated alcohol deprivations in alcohol-preferring (P) rats. Psychopharmacology (Berlin) 179, 262-270.
70. Shigemoto R, Nomura S, Ohishi H, Sugihara H, Nakanishi S, Mizuno N (1993). Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neuroscience Letters 163, 53-57.
71. Short JL, Drago J, Lawrence AJ (2006). Comparison of ethanol preference and neurochemical measures of mesolimbic dopamine and adenosine systems across different strains of mice. Alcoholism : Clinical and Experimental Research 30, 606-620.
72. Sihver W, Bier D, Holschbach MH, Schulze A, Wutz W, Olsson RA, Coenen HH (2004). Binding of tritiated and radioiodinated ZM241,385 to brain A2A adenosine receptors. Nuclear Medicine & Biology 31, 173-177.
73. Soria G, Castane A, Ledent C, Parmentier M, Maldonado R, Valverde O (2006). The lack of A2A adenosine receptors diminishes the reinforcing efficacy of cocaine. Neuropsychopharmacology 31, 978-987.
74. Spanagel R, Pendyala G, Abarca C, Zghoul T, Sanchis-Segura C, Magnone MC, Lascorz J, Depner M, Holzberg D, Soyka M, et al. (2005). The clock gene Per2 influences the glutamatergic system and modulates alcohol consumption. Nature Medicine 11, 35-42.
75. Spooren WP, Vassout A, Neijt HC, Kuhn R, Gasparini F, Roux S, Porsolt RD, Gentsch C (2000). Anxiolytic-like effects of the prototypical metabotropic glutamate receptor 5 antagonist 2-methyl-6-(phenylethynyl)pyridine in rodents. Journal of Pharmacology and Experimental Therapeutics 295, 1267-1275.
76. Swift RM (1999). Drug therapy for alcohol dependence. New England Journal of Medicine 340, 1482-1490.
77. Tallaksen-Greene SJ, Kaatz KW, Romano C, Albin RL (1998). Localization of mGluR1a-like immunoreactivity and mGluR5-like immunoreactivity in identified populations of striatal neurons. Brain Research 780, 210-217.
78. Tatarczynska E, Klodzinska A, Chojnacka-Wojcik E, Palucha A, Gasparini F, Kuhn R, Pilc A (2001). Potential anxiolytic- and antidepressant-like effects of MPEP, a potent, selective and systemically active mGlu5 receptor antagonist. British Journal of Pharmacology 132, 1423-1430.
79. Tessari M, Pilla M, Andreoli M, Hutcheson DM, Heidbreder CA (2004). Antagonism at metabotropic glutamate 5 receptors inhibits nicotine- and cocaine-taking behaviours and prevents nicotine-triggered relapse to nicotine-seeking. European Journal of Pharmacology 499, 121-133.
80. Vanderschuren LJ, Di Ciano P, Everitt BJ (2005). Involvement of the dorsal striatum in cue-controlled cocaine seeking. Journal of Neuroscience 25, 8665-8670.
81. Varty GB, Grilli M, Forlani A, Fredduzzi S, Grzelak ME, Guthrie DH, Hodgson RA, Lu SX, Nicolussi E, Pond AJ, et al. (2005). The antinociceptive and anxiolytic-like effects of the metabotropic glutamate receptor 5 (mGluR5) antagonists, MPEP and MTEP, and the mGluR1 antagonist, LY456236, in rodents : a comparison of efficacy and side-effect profiles. Psychopharmacology (Berlin) 179, 207-217.
82. Vengeliene V, Bachteler D, Danysz W, Spanagel R (2005). The role of the NMDA receptor in alcohol relapse : a pharmacological mapping study using the alcohol deprivation effect. Neuropharmacology 48, 822-829.
83. Waller MB, McBride WJ, Lumeng L, Li TK (1983). Initial sensitivity and acute tolerance to ethanol in the P and NP lines of rats.. Pharmacology Biochemistry and Behavior 19, 683-686.
84. WHO (2001). A Summary of Global Status Report on Alcohol. Geneva: World Health Organization.
85. Yaar R, Jones MR, Chen JF, Ravid K (2005). Animal models for the study of adenosine receptor function. Journal of Cellular Physiology 202, 9-20.
86. Yabuuchi K, Kuroiwa M, Shuto T, Sotogaku N, Snyder GL, Higashi H, Tanaka M, Greengard P, Nishi A (2006). Role of adenosine A1 receptors in the modulation of dopamine D1 and adenosine A2A receptor signaling in the neostriatum. Neuroscience 141, 19-25.
87. Yao L, McFarland K, Fan P, Jiang Z, Ueda T, Diamond I (2006). Adenosine A2a blockade prevents synergy between mu-opiate and cannabinoid CB1 receptors and eliminates heroin-seeking behavior in addicted rats. Proceedings of the National Academy of Sciences USA 103, 7877-7882.