Study of novel selective mGlu2 agonist in the temporo-ammonic input to CA1 neurons reveals reduced mGlu2 receptor expression in a wistar substrain with an anxiety-like phenotype

Journal of Neuroscience

Volumn 31, Issue 18, 2011, Pages 6721-6731

  Ceolin, Laura ^a   Kantamneni, Sriharsha ^a   Barker, Gareth R I ^a   Hanna, Lydia ^a   Murray, Laura ^a   Warburton, E Clea ^a   Robinson, Emma S J ^a   Monn, James A ^b   Fitzjohn, Stephen M ^a,b   Collingridge, Graham L ^a,c   Bortolotto, Zuner A ^a   Lodge, David ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b ELI LILLY AND COMPANY   (United States)

^c Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2,3 DICARBOXYCYCLOPROPYL)GLYCINE; 2 AMINO 4 METHYLBICYCLO[3.1.0]HEXANE 2,6 DICARBOXYLIC ACID; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 3; METABOTROPIC RECEPTOR AGONIST; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ENTORHINAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPAL CA1 REGION; MALE; MAZE TEST; MOUSE; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RAT STRAIN; SENSITIVITY ANALYSIS; STRAIN DIFFERENCE; STRATUM LACUNOSUM MOLECULARE; TEMPORO AMMONIC PATHWAY; WISTAR RAT;

ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; CA1 REGION, HIPPOCAMPAL; CYCLOPROPANES; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCINE; MALE; MICE; MICE, KNOCKOUT; NEURONS; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; SYNAPTIC TRANSMISSION;

EID: 79955752583     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0418-11.2011     Document Type: Article

References (58)

1. Anderson WW, Collingridge GL (2007) Capabilities of the WinLTP data acquisition program extending beyond basic LTP experimental functions. J Neurosci Methods 162:346-356.
2. Bond A, Monn JA, Lodge D (1997) A novel orally active group 2 metabo-tropic glutamate receptor agonist: LY354740. Neuroreport 8:1463-1466.
3. Bond A, O'Neill MJ, Hicks CA, Monn JA, Lodge D (1998) Neuroprotective effects of a systemically active group II metabotropic glutamate receptor agonist LY354740 in a gerbil model of global ischaemia. Neuroreport 9:1191-1193.
4. Bruno V, Battaglia G, Copani A, D'Onofrio M, Di Iorio P, De Blasi A, Mel-chiorri D, Flor PJ, Nicoletti F (2001) Metabotropic glutamate receptor subtypes as targets for neuroprotective drugs. J Cereb Blood Flow Metab 21:1013-1033.
5. Capogna M (2004) Distinct properties of presynaptic group II and III metabotropic glutamate receptor-mediated inhibition of perforant pathway-CA1 EPSCs. Eur J Neurosci 19:2847-2858.
6. Cartmell J, Schoepp DD (2000) Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 75:889-907.
7. Cartmell J, Monn JA, Schoepp DD (2000a) The mGlu(2/3) receptor agonist LY379268 selectively blocks amphetamine ambulations and rearing. Eur J Pharmacol 400:221-224.
8. Cartmell J, Monn JA, Schoepp DD (2000b) Attenuation of specific PCP-evoked behaviors by the potent mGlu2/3 receptor agonist, LY379268 and comparison with the atypical antipsychotic, clozapine. Psychopharma-cology (Berl) 148:423-429.
9. Catania MV, De Socarraz H, Penney JB, Young AB (1994) Metabotropic glutamate receptor heterogeneity in rat brain. Mol Pharmacol 45:626-636.
10. Ceolin L, Bortolotto ZA, Collingridge GL, Lodge D (2008) Differentiation of perforant path inputs into CA1 by an mGluR2 agonist, LY395756. Neuropharmacology 55:591.
11. Chiechio S, Zammataro M, Morales ME, Busceti CL, Drago F, Gereau RW 4th, Copani A, Nicoletti F (2009) Epigenetic modulation of mGlu2 receptors by histone deacetylase inhibitors in the treatment of inflammatory pain. Mol Pharmacol 75:1014-1020.
12. Colbert CM, Levy WB (1992) Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by gluta-mate receptors. J Neurophysiol 68:1-8.
13. Corti C, Crepaldi L, Mion S, Roth AL, Xuereb JH, Ferraguti F (2007a) Altered dimerization of metabotropic glutamate receptor 3 in schizophrenia. Biol Psychiatry 62:747-755.
14. Corti C, Battaglia G, Molinaro G, Riozzi B, Pittaluga A, Corsi M, Mugnaini M, Nicoletti F, Bruno V (2007b) The use of knock-out mice unravels distinct roles for mGlu2 and mGlu3 metabotropic glutamate receptors in mechanisms of neurodegeneration/neuroprotection. J Neurosci 27:8297-8308.
15. Cryan JF, Holmes A (2005) The ascent of mouse: advances in modelling human depression and anxiety. Nat Rev Drug Discov 4:775-790.
16. Dominguez C, Prieto L, Valli MJ, Massey SM, Bures M, Wright RA, Johnson BG, Andis SL, Kingston A, Schoepp DD, Monn JA (2005) Methyl substitution of 2-aminobicyclo[3.1.0]hexane 2,6-dicarboxylate (LY354740) determines functional activity atmetabotropic glutamate receptors: identification of a subtype selective mGlu2 receptor agonist. J Med Chem 48:3605-3612.
17. Dunayevich E, Erickson J, Levine L, Landbloom R, Schoepp DD, Tollefson GD (2008) Efficacy and tolerability of an mGlu2/3 agonist in the treatment of generalized anxiety disorder. Neuropsychopharmacology 33:1603-1610.
18. Empson RM, Heinemann U (1995) The perforant path projection to hip-pocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice. J Physiol 484:707-720.
19. Fell MJ, Svensson KA, Johnson BG, Schoepp DD (2008) Evidence for the role of metabotropic glutamate (mGlu)2 not mGlu3 receptors in the preclinical antipsychotic pharmacology of the mGlu2/3 receptor agonist (-)-(1R,4S,5S,6S)-4-amino-2-sulfonylbicyclo[3.1.0]hexane-4,6-dicarboxylic acid (LY404039). J Pharmacol Exp Ther 326:209-217.
20. File SE (2001) Factors controlling measures of anxiety and responses to novelty in the mouse. Behav Brain Res 125:151-157.
21. Fricker AC, Mok MH, de la Flor R, Shah AJ, Woolley M, Dawson LA, Kew JN (2009) Effects of N-acetylaspartylglutamate (NAAG) at group II mGluRs and NMDAR. Neuropharmacology 56:1060-1067.
22. Galici R, Echemendia NG, Rodriguez AL, Conn PJ (2005) A selective allosteric potentiator of metabotropic glutamate (mGlu) 2 receptors has effects similar to an orthosteric mGlu2/3 receptor agonist in mouse models predictive of antipsychotic activity. J Pharmacol Exp Ther 315:1181-1187.
23. Giocomo LM, Hasselmo ME (2006) Difference in time course of modulation of synaptic transmission by group II versus group III metabotropic glutamate receptors in region CA1 of the hippocampus. Hippocampus 16:1004-1016.
24. Grillon C, Cordova J, Levine LR, Morgan CA 3rd (2003) Anxiolytic effects of a novel group II metabotropic glutamate receptor agonist (LY354740) in the fear-potentiated startle paradigm in humans. Psychopharmacology (Berl) 168:446-454.
25. Harrison PJ, Lyon L, Sartorius LJ, Burnet PW, Lane TA (2008) The group II metabotropic glutamate receptor 3 (mGluR3, mGlu3, GRM3): expression, function and involvement in schizophrenia. J Psychopharmacol 22:308-322.
26. Hayashi Y, Momiyama A, Takahashi T, Ohishi H, Ogawa-Meguro R, Shige-moto R, Mizuno N, Nakanishi S (1993) Role of a metabotropic glutamate receptor in synaptic modulation in the accessory olfactory bulb. Nature 366:687-690.
27. Helton DR, Tizzano JP, Monn JA, Schoepp DD, Kallman MJ (1998) Anxiolytic and side-effect profile of LY354740: a potent, highly selective, orally active agonist for group II metabotropic glutamate receptors. J Pharmacol Exp Ther 284:651-660.
28. Johnson MP, Baez M, Jagdmann GE Jr, Britton TC, Large TH, Callagaro DO, Tizzano JP, Monn JA, Schoepp DD (2003) Discovery of allosteric potentiators for the metabotropic glutamate 2 receptor: synthesis and subtype selectivity of N-(4-(2-methoxyphenoxy)phenyl)-N-(2,2,2- trifluoroethyl-sulfonyl)pyrid-3-ylmethylamine. J Med Chem 46:3189-3192.
29. Jones CK, Eberle EL, Peters SC, Monn JA, Shannon HE (2005) Analgesic effects of the selective group II (mGlu2/3) metabotropic glutamate receptor agonists LY379268 and LY389795 in persistent and inflammatory pain models after acute and repeated dosing. Neuropharmacology 49 [Suppl 1]:206-218.
30. Kew JN, Ducarre JM, Pflimlin MC, Mutel V, Kemp JA (2001) Activity-dependent presynaptic autoinhibition by group II metabotropic glutamate receptors at the perforant path inputs to the dentate gyrus and CA1. Neuropharmacology 40:20-27.
31. Kew JN, Pflimlin MC, Kemp JA, Mutel V (2002) Differential regulation of synaptic transmission by mGlu2 and mGlu3 at the perforant path inputs to the dentate gyrus and CA1 revealed in mGlu2-/- mice. Neuropharmacology 43:215-221.
32. Kilbride J, Huang LQ, Rowan MJ, Anwyl R (1998) Presynaptic inhibitory action of the group II metabotropic glutamate receptor agonists, LY354740 and DCG-IV. Eur J Pharmacol 356:149-157.
33. Kingston AE, Ornstein PL, Wright RA, Johnson BG, Mayne NG, Burnett JP, Belagaje R, Wu S, Schoepp DD (1998) LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37:1-12.
34. Landgraf R, Wigger A (2003) Born to be anxious: neuroendocrine and genetic correlates of trait anxiety in HAB rats. Stress 6:111-119.
35. Linden AM, Shannon H, Baez M, Yu JL, Koester A, Schoepp DD (2005) Anxiolytic-like activity of the mGLU2/3 receptor agonist LY354740 in the elevated plus maze test is disrupted in metabotropic glutamate receptor 2 and 3 knock-out mice. Psychopharmacology (Berl) 179:284-291.
36. Macek TA, Winder DG, Gereau RW 4th, Ladd CO, Conn PJ (1996) Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J Neurophysiol 76:3798-3806.
37. McBride WJ, Li TK (1998) Animal models of alcoholism: neurobiology of high alcohol-drinking behavior in rodents. Crit Rev Neurobiol 12:339-369.
38. McNaughton BL (1980) Evidence for two physiologically distinct perforant pathways to the fascia dentata. Brain Res 199:1-19.
39. Moghaddam B, Adams BW (1998) Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats. Science 281:1349-1352.
40. Monn JA, Valli MJ, Massey SM, Wright RA, Salhoff CR, Johnson BG, Howe T, Alt CA, Rhodes GA, Robey RL, Griffey KR, Tizzano JP, Kallman MJ, Helton DR, Schoepp DD (1997) Design, synthesis, and pharmacological characterization of (+)-2-aminobicyclo[3.1.0]hexane-2,6-dicarboxylic acid (LY354740): a potent, selective, and orally active group 2 metabotropic glutamate receptor agonist possessing anticonvulsant and anxiolytic properties. J Med Chem 40:528-537.
41. Monn JA, Valli MJ, Massey SM, Hansen MM, Kress TJ, Wepsiec JP, Harkness AR, Grutsch JL Jr, Wright RA, Johnson BG, Andis SL, Kingston A, Tomlinson R, Lewis R, Griffey KR, Tizzano JP, Schoepp DD (1999) Synthesis, pharmacological characterization, and molecular modeling of heterobicyclic amino acids related to (+)-2-aminobicyclo[3.1.0] hexane-2,6-dicarboxylic acid (LY354740): identification of two new potent, selective, and systemically active agonists for group II metabotropic glutamate receptors. J Med Chem 42:1027-1040.
42. Niswender CM, Conn PJ (2010) Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol 50:295-322.
43. Overstreet DH (2002) Behavioral characteristics of rat lines selected for differential hypothermic responses to cholinergic or serotonergic agonists. Behav Genet 32:335-348.
44. Patil ST, Zhang L, Martenyi F, Lowe SL, Jackson KA, Andreev BV, Avedisova AS, Bardenstein LM, Gurovich IY, Morozova MA, Mosolov SN, Neznanov NG, Reznik AM, Smulevich AB, Tochilov VA, Johnson BG, Monn JA, Schoepp DD (2007) Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized Phase 2 clinical trial. Nat Med 13:1102-1107.
45. Petralia RS, Wang YX, Niedzielski AS, Wenthold RJ (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience 71:949-976.
46. Price CJ, Karayannis T, Pal BZ, Capogna M (2005) Group II and III mGluRs-mediated presynaptic inhibition of EPSCs recorded from hip-pocampal interneurons of CA1 stratum lacunosum moleculare. Neuropharmacology 49 [SUPPL 1]:45-56.
47. Sagvolden T (2000) Behavioral validation of the spontaneously hypertensive rat (SHR) as an animal model of attention-deficit/hyperactivity disorder (AD/HD). Neurosci Biobehav Rev 24:31-39.
48. Schoepp DD, Jane DE, Monn JA (1999) Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38:1431-1476.
49. Schoepp DD, Wright RA, Levine LR, Gaydos B, Potter WZ (2003) LY354740, an mGlu2/3 receptor agonist as a novel approach to treat anxiety/stress. Stress 6:189-197.
50. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S, Mizuno N (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17:7503-7522.
51. Simmons RM, Webster AA, Kalra AB, Iyengar S (2002) Group II mGluR receptor agonists are effective in persistent and neuropathic pain models in rats. Pharmacol Biochem Behav 73:419-427.
52. Smolders I, Lindekens H, Clinckers R, Meurs A, O'Neill MJ, Lodge D, Ebinger G, Michotte Y (2004) In vivo modulation of extracellular hippocampal glutamate and GABA levels and limbic seizures by group I and II metabo-tropic glutamate receptor ligands. J Neurochem 88:1068-1077.
53. Steward O, Scoville SA (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169:347-370.
54. Tamaru Y, Nomura S, Mizuno N, Shigemoto R (2001) Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: differential location relative to pre- and postsynaptic sites. Neuroscience 106:481-503.
55. Walker DL, Rattiner LM, Davis M (2002) Group II metabotropic glutamate receptors within the amygdala regulate fear as assessed with potentiated startle in rats. Behav Neurosci 116:1075-1083.
56. Witter MP, Amaral DG (2004) Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. In: The rat nervous system, Ed 3 (Paxinos G, ed), pp 637-703. San Diego: Elsevier Academic.
57. Woolley ML, Pemberton DJ, Bate S, Corti C, Jones DN (2008) The mGlu2 but not the mGlu3 receptor mediates the actions of the mGluR2/3 agonist, LY379268,in mouse models predictive of antipsychotic activity. Psy-chopharmacology (Berl) 196:431-440.
58. Wroblewska B, Wroblewski JT, Pshenichkin S, Surin A, Sullivan SE, Neale JH (1997) N-acetylaspartylglutamate selectively activates mGluR3 receptors in transfected cells. J Neurochem 69:174-181.