Differential modulation of thresholds for intracranial self-stimulation by mGlu5 positive and negative allosteric modulators: Implications for effects on drug self-administration

Frontiers in Pharmacology

Volumn 3 JAN, Issue , 2012, Pages

  Cleva, Richard M ^a   Watterson, Lucas R ^a   Johnson, Meagan A ^a   Olive, M Foster ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Allosteric modulator; Brain reward; Glutamate; Intracranial self stimulation; mGluR5

Indexed keywords

(4 FLUOROPHENYL) [3 [3 (4 FLUOROPHENYL) [1,2,4] OXADIAZOL 5 YL]PIPERIDIN 1 YL]METHANONE; 3 [(2 METHYL 4 THIAZOLYL)ETHYNYL]PYRIDINE; 3 CYANO N (1,3 DIPHENYL 1H PYRAZOL 5 YL)BENZAMIDE; ADX 47273; BACITRACIN; FENOBAM; LIDOCAINE; MELOXICAM; METABOTROPIC RECEPTOR 5; METABOTROPIC RECEPTOR ANTAGONIST; NEGATIVE ALLOSTERIC MODULATOR; NEOMYCIN; POLYMYXIN B; POSITIVE ALLOSTERIC MODULATOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CONTROLLED STUDY; DOSE RESPONSE; DRUG ABUSE; ELECTRODE; MALE; MEDIAL FOREBRAIN BUNDLE; NEUROMODULATION; NONHUMAN; PERCEPTIVE THRESHOLD; RAT; REWARD; SELF STIMULATION; WOUND;

EID: 84865984526     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2011.00093     Document Type: Article

References (50)

1. Adams, C. L., Cowen, M. S., Short, J. L., and Lawrence, A. J. (2008). Combined antagonism of glutamate mGlu5 and adenosine A2A receptors interact to regulate alcohol-seeking in rats. Int. J. Neuropsychopharmacol. 11, 229-241.
2. Besheer, J., Grondin, J. J., Cannady, R., Sharko, A. C., Faccidomo, S., and Hodge, C. W. (2010). Metabotropic glutamate receptor 5 activity in the nucleus accumbens is required for the maintenance of ethanol self-administration in a rat genetic model of high alcohol intake. Biol. Psychiatry 67, 812-822.
3. Berry-Kravis, E. M., Hessl, D., Coffey, S., Hervey, C., Schneider, A., Yuhas, J., Hutchison, J., Snape, M., Tranfaglia, M., Nguyen, D. V., and Hagerman, R. (2009). A pilot open-label singledose trial of fenobam in adults with fragile X syndrome. J. Med. Genet. 46, 266-271.
4. Bird, M. K., Kirchhoff, J., Djouma, E., and Lawrence, A. J. (2008). Metabotropic glutamate 5 receptors regulate sensitivity to ethanol in mice. Int. J. Neuropsychopharmacol. 11, 765-774.
5. Bird, M. K., and Lawrence, A. J. (2009a). Group I metabotropic glutamate receptors: involvement in drugseeking and drug-induced plasticity. Curr. Mol. Pharmacol. 2, 83-94.
6. Bird, M. K., and Lawrence,A. J. (2009b). The promiscuous mGlu5 receptor a range of partners for therapeutic possibilities? Trends Pharmacol. Sci. 30, 617-623.
7. Chiamulera, C., Epping-Jordan, M. P., Zocchi, A., Marcon, C., Cottiny, C., Tacconi, S., Corsi, M., Orzi, F., and Conquet, F. (2001). Reinforcing and locomotor stimulant effects of cocaine are absent in mGluR5 null mutant mice. Nat. Neurosci. 4, 873-874.
8. Cleva, R. M., Hicks, M. P., Gass, J. T., Wischerath, K. C., Plasters, E. T., Widholm, J. J., and Olive, M. F. (2011). mGluR5 positive allosteric modulation enhances extinction learning following cocaine selfadministration. Behav. Neurosci. 125, 10-19.
9. Cleva, R. M., and Olive, M. F. (in press). Metabotropic glutamate receptors and drug addiction. Wiley Interdiscip. Rev. Membr. Transp. Signal.
10. Cosford, N. D., Tehrani, L., Roppe, J., Schwieger, E., Smith, N. D., Anderson, J., Bristow, L., Brodkin, J., Jiang, X., Mcdonald, I., Rao, S., Washburn, M., and Varney, M. A. (2003). 3-[(2-Methyl-1,3-thiazol-4yl)ethynyl]-pyridine: a potent and highly selective metabotropic glutamate subtype 5 receptor antagonist with anxiolytic activity. J. Med. Chem. 46, 204-206.
11. Cowen, M. S., Djouma, E., and Lawrence, A. J. (2005). The metabotropic glutamate 5 receptor antagonist 3-[(2-methyl-1,3-thiazol-4-yl)ethynyl)-pyridine reduces ethanol self-administration in multiple strains of alcohol-preferring rats and regulates olfactory glutamatergic systems. J. Pharmacol. Exp. Ther. 315, 590-600.
12. Cowen, M. S., Krstew, E., and Lawrence, A. J. (2007). Assessing appetitive and consummatory phases of ethanol self-administration in C57BL/6J mice under operant conditions: regulation by mGlu5 receptor antagonism. Psychopharmacology (Berl.) 190, 21-29.
13. Cozzoli, D. K., Goulding, S. P., Zhang, P. W., Xiao, B., Hu, J. H., Ary, A. W., Obara, I., Rahn, A., AbouZiab, H., Tyrrel, B., Marini, C., Yoneyama, N., Metten, P., Snelling, C., Dehoff, M. H., Crabbe, J. C., Finn, D. A., Klugmann, M., Worley, P. F., and Szumlinski, K. K. (2009). Binge drinking upregulates accumbens mGluR5-Homer2-PI3K signaling: functional implications for alcoholism. J. Neurosci. 29, 8655-8668.
14. Friedmann, C. T. H., Davis, L. J., Ciccone, P. E., and Rubin, R. T. (1980). Phase II double-blind controlled study of a new anxiolytic, fenobam (McN-3377) vs. placebo. Curr. Ther. Res. 27, 144-151.
15. Gass, J. T., and Olive, M. F. (2009a). Positive allosteric modulation of mGluR5 receptors facilitates extinction of a cocaine contextual memory. Biol. Psychiatry 65, 717-720.
16. Gass, J. T., and Olive, M. F. (2009b). Role of protein kinase C epsilon (PKCε) in the reduction of ethanol reinforcement due to mGluR5 antagonism in the nucleus accumbens shell. Psychopharmacology (Berl.) 204, 587-597.
17. Gass, J. T., Osborne, M. P., Watson, N. L., Brown, J. L., and Olive, M. F. (2009). mGluR5 antagonism attenuates methamphetamine rein forcement and prevents reinstatement of methamphetamine-seeking behavior in rats. Neuropsychophar macology 34, 820-833.
18. Goldberg, M. E., Salama, A. I., Patel, J. B., and Malick, J. B. (1983). Novel non-benzodiazepine anxiolytics. Neuropharmacology 22, 1499-1504.
19. Gormley, S., and Rompre, P. P. (2011). Blockade of mGLUR5 receptors differentially alters amphetamineinduced enhancement of locomotor activity and of brain stimulation reward. J. Psychopharmacol. 25, 393-401.
20. Hao, Y., Martin-Fardon, R., and Weiss, F. (2010). Behavioral and functional evidence of metabotropic glutamate receptor 2/3 and metabotropic glutamate receptor 5 dysregulation in cocaine-escalated rats: factor in the transition to dependence. Biol. Psychiatry 68, 240-248.
21. Harrison, A. A., Gasparini, F., and Markou, A. (2002). Nicotine potentiation of brain stimulation reward reversed by DHβE and SCH 23390, but not by eticlopride, LY 314582 or MPEP in rats. Psychopharmacology (Berl.) 160, 56-66.
22. Heidbreder, C. A., Bianchi, M., Lacroix, L. P., Faedo, S., Perdona, E., Remelli, R., Cavanni, P., and Crespi, F. (2003). Evidence that the metabotropic glutamate receptor 5 antagonist MPEP may act as an inhibitor of the norepinephrine transporter in vitro and in vivo. Synapse 50, 269-276.
23. Itil, T. M., Seaman, P. A., Huque, M., Mukhopadhyay, S., Blasucci, D., Tat, K., and Ciccone, P. E. (1978). The clinical and quantitative EEG effects and plasma levels of fenobam (McN-3377) in subjects with anxiety: an open rising dose tolerance and efficacy study. Curr. Ther. Res. 24, 708-724.
24. Kenny, P. J., Boutrel, B., Gasparini, F., Koob, G. F., and Markou, A. (2005). Metabotropic glutamate 5 receptor blockade may attenuate cocaine self-administration by decreasing brain reward function in rats. Psychopharmacology (Berl.) 179, 247-254.
25. Kenny, P. J., Gasparini, F., and Markou, A. (2003). Group II metabotropic and alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA)/kainate glutamate receptors regulate the deficit in brain reward function associated with nicotine withdrawal in rats. J. Pharmacol. Exp. Ther. 306, 1068-1076.
26. Kenny, P. J., and Markou, A. (2004). The ups and downs of addiction: role of metabotropic glutamate receptors. Trends Pharmacol. Sci. 25, 265-272.
27. Keywood, C., Wakefield, M., and Tack, J. (2009). A proof of concept study evaluating the effect of ADX10059, a metabotropic glutamate receptor-5 negative allosteric modulator, on acid exposure and symptoms in gastro-esophageal reflux disease. Gut 58, 1192-1199.
28. Kinney, G. G., O'Brien, J. A., Lemaire, W., Burno, M., Bickel, D. J., Clements, M. K., Chen, T. B., Wisnoski, D. D., Lindsley, C. W., Tiller, P. R., Smith, S., Jacobson, M. A., Sur, C., Duggan, M. E., Pettibone, D. J., Conn, P. J., and Williams, D. L. Jr. (2005). A novel selective positive allosteric modulator of metabotropic glutamate receptor subtype 5 has in vivo activity and antipsychotic-like effects in rat behavioral models. J. Pharmacol. Exp. Ther. 313, 199-206.
29. Kornetsky, C., and Bain, G. (1992). Brain-stimulation reward: a model for the study of the rewarding effects of abused drugs. NIDA Res. Monogr. 124, 73-93.
30. Kornetsky, C., and Esposito, R. U. (1979). Euphorigenic drugs: effects on the reward pathways of the brain. Fed. Proc. 38, 2473-2476.
31. Krystal, J. H., Mathew, S. J., D'Souza, D. C., Garakani, A., Gunduz-Bruce, H., and Charney, D. S. (2010). Potential psychiatric applications of metabotropic glutamate receptor agonists and antagonists. CNS Drugs 24, 669-693.
32. Lea, P. M., and Faden, A. I. (2006). Metabotropic glutamate receptor subtype 5 antagonists MPEP and MTEP. CNS Drug Rev. 12, 149-166.
33. Lindsley, C. W., Wisnoski, D. D., Leister, W. H., O'Brien, J. A., Lemaire, W., Williams, D. L. Jr., Burno, M., Sur, C., Kinney, G. G., Pettibone, D. J., Tiller, P. R., Smith, S., Duggan, M. E., Hartman, G. D., Conn, P. J., and Huff, J. R. (2004). Discovery of positive allosteric modulators for the metabotropic glutamate receptor subtype 5 from a series of N-(1,3-diphenyl-1H-pyrazol-5-yl)benzamides that potentiate receptor function in vivo. J. Med. Chem. 47, 5825-5828.
34. Liu, F., Grauer, S., Kelley, C., Navarra, R., Graf, R., Zhang, G., Atkinson, P. J., Wantuch, C., Popiolek, M., Day, M., Khawaja, X., Smith, D., Olsen, M., Kouranova, E., Gilbert, A., Lai, M., Pausch, M. H., Pruthi, F., Pulicicchio, C., Brandon, N. J., Comery, T. A., Beyer, C. E., Logue, S., Rosenzweig-Lipson,S.,and Marquis, K. L. (2008). ADX47273: a novel metabotropic glutamate receptor 5 selective positive allosteric modulator with preclinical antipsychoticlike and pro-cognitive activities. J. Pharmacol. Exp. Ther. 327, 827-839.
35. Markou, A., and Koob, G. F. (1992). Construct validity of a selfstimulation threshold paradigm: effects of reward and performance manipulations. Physiol. Behav. 51, 111-119.
36. Montana, M. C., Cavallone, L. F., Stubbert, K. K., Stefanescu, A. D., Kharasch, E. D., and Gereau, R. W. (2009). The metabotropic glutamate receptor subtype 5 antagonist fenobam is analgesic and has improved in vivo selectivity as compared to the prototypical antagonist 2-methyl-6-(phenylethynyl)-pyridine. J. Pharmacol. Exp. Ther. 330, 834-843.
37. Montana, M. C., Conrardy, B. A., Cavallone, L. F., Kolber, B. J., Rao, L. K., Greco, S. C., and Gereau, R. W. T. (2011). Metabotropic glutamate receptor 5 antagonism with fenobam: examination of analgesic tolerance and side effect profile in mice. Anesthesiology 115, 1239-1250.
38. Nic Dhonnchadha, B. A., and Kantak, K. M. (2011). Cognitive enhancers for facilitating drug cue extinction: insights from animal models. Pharmacol. Biochem. Behav. 99, 229-244.
39. Niswender, C. M., and Conn, P. J. (2010). Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu.Rev.Pharmacol. Toxicol. 50, 295-322.
40. O'Leary, D. M., Movsesyan, V., Vicini, S., and Faden, A. I. (2000). Selective mGluR5 antagonists MPEP and SIB-1893 decrease NMDA or glutamatemediated neuronal toxicity through actions that reflect NMDA receptor antagonism. Br. J. Pharmacol. 131, 1429-1437.
41. Olive, M. F. (2009). Metabotropic glutamate receptor ligands as potential therapeutics for drug addiction. Curr. Drug Abuse Rev. 2, 83-98.
42. Osborne, M. P. H., and Olive, M. F. (2008). A role for mGluR5 receptors in intravenous methamphetamine self-administration. Ann. N. Y. Acad. Sci. 1139, 206-211.
43. Palmatier, M. I., Liu, X., Donny, E. C., Caggiula, A. R., and Sved, A. F. (2008). Metabotropic glutamate 5 receptor (mGluR5) antagonists decrease nicotine seeking, but do not affect the reinforcement enhancing effects of nicotine. Neuropsychopharmacology 33, 2139-2147.
44. Paxinos, G., and Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates. San Diego: Academic Press.
45. Pecknold, J. C., Mcclure, D. J., and Appeltauer, L. (1980). Fenobam in anxious outpatients. Curr. Ther. Res. 27, 119-123.
46. Pecknold, J. C., Mcclure, D. J., Appeltauer, L., Wrzesinski, L., and Allan, T. (1982). Treatment of anxiety using fenobam (a nonbenzodiazepine) in a double-blind standard (diazepam) placebo-controlled study. J. Clin. Psychopharmacol. 2, 129-133.
47. Porter, R. H., Jaeschke, G., Spooren, W., Ballard, T., Buettelmann, B., Kolczewski, S., Peters, J. U., Prinssen, E., Wichmann, J., Vieira, E., Muehlemann, A., Gatti, S., Mutel, V., and Malherbe, P. (2005). Fenobam: a clinically validated non-benzodiazepine anxiolytic is a potent, selective and noncompetitive mGlu5 receptor antagonist with inverse agonist activity. J. Pharmacol. Exp. Ther. 315, 711-721.
48. Sidhpura, N., Weiss, F., and Martin Fardon, R. (2010). Effects of the mGlu2/3 agonist LY379268 and the mGlu5 antagonist MTEP on ethanol seeking and reinforcement are differentially altered in rats with a history of ethanol dependence. Biol. Psychiatry 67, 804-811.
49. Spooren, W. P., Gasparini, F., Salt, T. E., and Kuhn, R. (2001). Novel allosteric antagonists shed light on mglu5 receptors and CNS disorders. Trends Pharmacol. Sci. 22, 331-337.
50. Zerbib, F., Bruley, D. V. S., Roman, S., Tutuian, R., Galmiche, J. P., Mion, F., Tack, J., Malfertheiner, P., and Keywood, C. (2011). Randomised clinical trial: effects of monotherapy with ADX10059, a mGluR5 inhibitor, on symptoms and reflux events in patients with gastro-oesophageal reflux disease. Aliment. Pharmacol. Ther. 33, 911-921.