Group III and subtype 4 metabotropic glutamate receptor agonists: Discovery and pathophysiological applications in Parkinson's disease

Neuropharmacology

Volumn 66, Issue , 2013, Pages 53-64

  Amalric, M ^a   Lopez, S ^a   Goudet, C ^b,c   Fisone, G ^d   Battaglia, G ^e   Nicoletti, F ^e,f   Pin, J P ^b,c   Acher, F C ^g  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b UNIV MONTPELLIER   (France)

^c INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^d KAROLINSKA INSTITUTE   (Sweden)

^e IRCCS NEUROMED   (Italy)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

^g UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

6 Hydroxydopamine (6 OHDA); Agonist; Allosteric and orthosteric modulation; Basal ganglia; Group III mGlu receptors; Metabotropic glutamate receptors; Neurodegeneration; Parkinson's disease

Indexed keywords

1 AMINO 2 (PHOSPHONOMETHYL)CYCLOPROPANECARBOXYLIC ACID; 1 AMINOCYCLOPENTANE 1,3,4 TRICARBOXYLIC ACID; 2 (3,5 DICHLOROPHENYLCARBAMOYL)CYCLOHEXANECARBOXYLIC ACID; 2 AMINO 4 PHOSPHONOBUTYRIC ACID; 3,4 DICARBOXYPHENYLGLYCINE; 5 METHYL N (4 METHYLPYRIMIDIN 2 YL) 4 (1H PYRAZOL 4 YL)THIAZOL 2 AMINE; [(3 AMINO 3 CARBOXY)PROPYL][(4 HYDROXY 5 METHOXY 3 NITROPHENYL)HYDROXYMETHYL]PHOSPHINIC ACID; [(3 AMINO 3 CARBOXY)PROPYL][4 (CARBOXYMETHOXY)HYDROXYMETHYL]PHOSPHINIC ACID; [(3 AMINO 3 CARBOXY)PROPYL][[4 (CARBOXYMETHOXY)PHENYL]METHYL]PHOSPHINIC ACID; ADX 88178; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; AMINO ACID RECEPTOR AFFECTING AGENT; AMINO ACID RECEPTOR STIMULATING AGENT; AMN 082; ANTIPARKINSON AGENT; CENTRAL NERVOUS SYSTEM AGENTS; GLUTAMATE RECEPTOR AGONIST; LEVODOPA; LSP 1 2111; LSP 3 2156; LSP 4 2022; LUAF 21934; METABOTROPIC RECEPTOR 4; METABOTROPIC RECEPTOR 6; METABOTROPIC RECEPTOR 7; METABOTROPIC RECEPTOR 8; METABOTROPIC RECEPTOR AGONIST; N (3 CHLOROPHENYL)PICOLINAMIDE; N (3,4 DICHLOROPHENYL)CYCLOHEXANE 1,2 DICARBOXAMIDE; N [3 CHLORO 4 (BICYCLO[2.2.1]HEPT 5 ENE 1,3 DIOXO 1H ISOINDOL 1 YL)]PHENYL; N [3 CHLORO 4 [(BICYCLO[2.2.1]HEPT 5 ENE 1,3 DIOXO 1H ISOINDOL 1 YL)]PHENYL]PICOLINAMIDE; N PHENYL 7 (HYDROXYIMINO)CYCLOPROPA[B]CHROMEN 1A CARBOXAMIDE; PHOSPHOSERINE; POMAGLUMETAD METHIONIL; UNCLASSIFIED DRUG; UNINDEXED DRUG; VU 0400195; VU 364770;

AKINESIA; ALLOSTERISM; BASAL GANGLION; CATALEPSY; DOSE RESPONSE; DRUG DETERMINATION; DRUG EFFICACY; DRUG POTENCY; DRUG PROTEIN BINDING; DYSKINESIA; GABAERGIC TRANSMISSION; HUMAN; HYPERALGESIA; INFLAMMATORY PAIN; LOW DRUG DOSE; NEUROMODULATION; NEUROPATHIC PAIN; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; REVIEW; SCHIZOPHRENIA; STRUCTURE ACTIVITY RELATION;

ANIMALS; BASAL GANGLIA; DISEASE MODELS, ANIMAL; DYSKINESIA, DRUG-INDUCED; EXCITATORY AMINO ACID AGONISTS; MODELS, NEUROLOGICAL; NEUROPROTECTIVE AGENTS; PARKINSON DISEASE; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 84872156818     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2012.05.026     Document Type: Review

References (154)

1. D. Aarsland, S. Påhlhagen, C.G. Ballard, U. Ehrt, and P. Svenningsson Depression in Parkinson disease-epidemiology, mechanisms and management Nat. Rev. Neurol. 8 2012 35 47
2. F.C. Acher, and H.O. Bertrand Amino acid recognition by Venus flytrap domains is encoded in an 8-residue motif Biopolymers 80 2005 357 366
3. F. Acher, F. Tellier, I. Brabet, L. Fagni, R. Azerad, and J.-P. Pin Synthesis and pharmacological characterization of aminocyclopentane tricarboxylic acids (ACPT): new tools to discriminate between metabotropic glutamate receptor subtypes J. Med. Chem. 40 1997 3119 3129
4. R.L. Albin, A.B. Young, and J.B. Penney The functional anatomy of basal ganglia disorders Trends Neurosci. 12 1989 366 375
5. M. Amalric, C. Baunez, and A. Nieoullon Does the blockade of excitatory amino acid transmission in the basal ganglia simply reverse reaction time deficits induced by dopamine inactivation? Behav. Pharmacol. 6 1995 508 519
6. L. Amori, G. Costantino, M. Marinozzi, R. Pellicciari, F. Gasparini, P.J. Flor, R. Kuhn, and I. Vranesic Synthesis, molecular modeling and preliminary biological evaluation of 1-Amino-3-phosphono-3-cyclopentene-1-carboxylic acid and 1-Amino-3-phosphono-2-cyclopentene-1-carboxylic acid, two novel agonists of metabotropic glutamate receptors of group III Bioorg. Med. Chem. Lett. 10 2000 1447 1450
7. L. Amori, M. Serpi, M. Marinozzi, G. Costantino, M. Diaz, M.B. Hermit, C. Thomsen, and R. Pellicciari Synthesis and preliminary biological evaluation of (2S,1′R,2′S)- and (2S,1′S,2′R)-2-(2′- phosphonocyclopropyl)glycines, two novel conformationally constrained l-AP4 analogues Bioorg. Med. Chem. Lett. 16 2006 196 199
8. P. Andine, N. Widermark, R. Axelsson, G. Nyberg, U. Olofsson, E. Martensson, and M. Sandberg Characterization of MK-801-induced behavior as a putative rat model of psychosis J. Pharmacol. Exp. Ther. 290 1999 1393 1408
9. F. Ango, L. Prezeau, T. Muller, J.C. Tu, B. Xiao, P.F. Worley, J.P. Pin, J. Bockaert, and L. Fagni Agonist-independent activation of metabotropic glutamate receptors by the intracellular protein Homer Nature 411 2001 962 965
10. T. Araki, T. Kumagai, M. Matsubara, T. Ido, Y. Imai, and Y. Itoyama Protective effect of riluzole on MPTP-induced depletion of dopamine and its metabolite content in mice Metab. Brain Dis. 15 2000 193 201
11. S. Attucci, V. Carla, G. Mannaioni, and F. Moroni Activation of type 5 metabotropic glutamate receptors enhances NMDA responses in mice cortical wedges Br. J. Pharmacol. 132 2001 799 806
12. P.J. Austin, M.J. Betts, M. Broadstock, M.J. O'Neill, S.N. Mitchell, and S. Duty Symptomatic and neuroprotective effects following activation of nigral group III metabotropic glutamate receptors in rodent models of Parkinson's disease Br. J. Pharmacol. 160 2010 1741 1753
13. H. Awad, G.W. Hubert, Y. Smith, A.I. Levey, and P.J. Conn Activation of metabotropic glutamate receptor 5 has direct excitatory effects and potentiates NMDA receptor currents in neurons of the subthalamic nucleus J. Neurosci. 20 2000 7871 7879
14. G. Battaglia, C.L. Busceti, G. Molinaro, F. Biagioni, A. Traficante, F. Nicoletti, and V. Bruno Pharmacological activation of mGlu4 metabotropic glutamate receptors reduces nigrostriatal degeneration in mice treated with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine J. Neurosci. 26 2006 7222 7229
15. K.E. Bennouar, M.A. Uberti, C. Melon, M.D. Bacolod, H.N. Jimenez, M. Cajina, L. Kerkerian-Le Goff, D. Doller, and P. Gubellini Synergy between l-DOPA and a novel positive allosteric modulator of metabotropic glutamate receptor 4: implications for Parkinson's disease treatment and dyskinesia Neuropharmacology 66 2013 158 169
16. H.O. Bertrand, A.S. Bessis, J.P. Pin, and F.C. Acher Common and selective molecular determinants involved in metabotopic glutamate receptor agonist activity J. Med. Chem. 45 2002 3171 3183
17. A.-S. Bessis, P. Rondard, F. Gaven, I. Brabet, N. Triballeau, L. Prézeau, F. Acher, and J.-P. Pin Closure of the Venus Flytrap module of mGlu8 receptor and the activation process: insights from mutations converting antagonists into agonists Proc. Natl. Acad. Sci. U. S. A. 99 2002 11097 11102
18. A.-S. Bessis, G. Vadesne, E. Bourrat, G. Bertho, J.-P. Pin, and F. Acher 3-Carboxy-4-phosphonocyclopentane amino acids: new metabotropic glutamate receptor ligands Amino Acids 24 2003 303 310
19. M.J. Betts, M.J. O'Neill, and S. Duty Allosteric modulation of the group III mGlu receptor 4 provides functional neuroprotection in the 6-OHDA rat model of Parkinson's disease Br. J. Pharmacol. 2012 (Epub ahead of print)
20. C. Beurrier, S. Lopez, D. Revy, C. Selvam, C. Goudet, M. Lherondel, P. Gubellini, L. Kerkerian-LeGoff, F. Acher, J.P. Pin, and M. Amalric Electrophysiological and behavioral evidence that modulation of metabotropic glutamate receptor 4 with a new agonist reverses experimental parkinsonism FASEB J. 23 2009 3619 3628
21. F. Blandini, and J.T. Greenamyre Prospects of glutamate antagonists in the therapy of Parkinson's disease Fundam. Clin. Pharmacol. 12 1998 4 12
22. F. Blandini, G. Nappi, C. Tassorelli, and E. Martignoni Functional changes of the basal ganglia circuitry in Parkinson's disease Prog. Neurobiol. 62 2000 63 88
23. S.R. Bradley, D.G. Standaert, K.J. Rhodes, H.D. Rees, C.M. Testa, A.I. Levey, and P.J. Conn Immunohistochemical localization of subtype 4a metabotropic glutamate receptors in the rat and mouse basal ganglia J. Comp. Neurol. 407 1999 33 46
24. M. Broadstock, P. Austin, M. Betts, and S. Duty Antiparkinsonian potential of targeting group III metabotropic glutamate receptor subtypes in the rodent substantia nigra pars reticulata Br. J. Pharmacol. 165 2012 1034 1045
25. M. Carlsson, and A. Carlsson Interactions between glutamatergic and monoaminergic systems within the basal ganglia-implications for schizophrenia and Parkinson's disease Trends Neurosci. 13 1990 272 276
26. F.Y. Carroll, A. Stolle, P.M. Beart, A. Voerste, I. Brabet, F. Mauler, C. Joly, H. Antonicek, J. Bockaert, T. Muller, J.P. Pin, and L. Prezeau BAY36-7620: a potent non-competitive mGlu1 receptor antagonist with inverse agonist activity Mol. Pharmacol. 59 2001 965 973
27. S. Célanire, and B. Campo Recent advances in the drug discovery of metabotropic glutamate receptor 4 (mGluR4) activators for the treatment of CNS and non-CNS disorders Expert Opin. Drug Discov. 7 2012 261 280
28. T.N. Chase, F. Bibbiani, and J.D. Oh Striatal glutamatergic mechanisms and extrapyramidal movement disorders Neurotox. Res. 5 2003 139 146
29. K.R. Chaudhuri, D.G. Healy, and A.H. Schapira Non-motor symptoms of Parkinson's disease: diagnosis and management Lancet Neurol. 5 2006 235 245
30. L. Chen, Z. Liu, Z. Tian, Y. Wang, and S. Li Prevention of neurotoxin damage of 6-OHDA to dopaminergic nigral neuron by subthalamic nucleus lesions Stereotact. Funct. Neurosurg. 75 2000 66 75
31. Y. Chen, Y. Nong, C. Goudet, K. Hemstapat, T. de Paulis, J.P. Pin, and P.J. Conn Interaction of novel positive allosteric modulators of metabotropic glutamate receptor 5 with the negative allosteric antagonist site is required for potentiation of receptor responses Mol. Pharmacol. 71 2007 1389 1398
32. Y. Chen, C. Goudet, J.P. Pin, and P.J. Conn N-{4-Chloro-2-[(1,3-dioxo-1, 3-dihydro-2H-isoindol-2-yl)methyl]phenyl}-2-hydroxybenzamide (CPPHA) acts through a novel site as a positive allosteric modulator of group 1 metabotropic glutamate receptors Mol. Pharmacol. 73 2008 909 918
33. P.J. Conn, and J.P. Pin Pharmacology and functions of metabotropic glutamate receptors Annu. Rev. Pharmacol. Toxicol. 37 1997 205 237
34. P.J. Conn, G. Battaglia, M.J. Marino, and F. Nicoletti Metabotropic glutamate receptors in the basal ganglia motor circuit Nat. Rev. Neurosci. 6 2005 787 798
35. C. Corti, L. Aldegheri, P. Somogyi, and F. Ferraguti Distribution and synaptic localisation of the metabotropic glutamate receptor 4 (mGluR4) in the rodent CNS Neuroscience 110 2002 403 420
36. T.J. Counihan, G.B. Landwehrmeyer, D.G. Standaert, C.M. Kosinski, C.R. Scherzer, L.P. Daggett, G. Velicelebi, A.B. Young, and J.B. Penney Jr. Expression of N-methyl-D-Aspartate receptor subunit mRNA in the human brain: mesencephalic dopaminergic neurons J. Comp. Neurol. 390 1998 91 101
37. D. Cuomo, G. Martella, E. Barabino, P. Platania, D. Vita, G. Madeo, C. Selvam, C. Goudet, N. Oueslati, J.-P. Pin, F. Acher, A. Pisani, C. Beurrier, C. Melon, L. Kerkerian-Le Goff, and P. Gubellini Metabotropic glutamate receptor subtype 4 selectively modulates both glutamate and GABA transmission in the striatum: implications for Parkinson's disease treatment J. Neurochem. 109 2009 1096 1105
38. S. Darmopil, A.B. Martin, I.R. De Diego, S. Ares, and R. Moratalla Genetic inactivation of dopamine D1 but not D2 receptors inhibits l-DOPA-induced dyskinesia and histone activation Biol. Psychiatry 66 2009 603 613
39. M.R. DeLong Primate models of movement disorders of basal ganglia origin Trends Neurosci. 13 1990 281 285
40. L. Di, and E.H. Kerns Profiling drug-like properties in discovery research Curr. Opin. Chem. Biol. 7 2003 402 408
41. S. Duty Therapeutic potential of targeting group III metabotropic glutamate receptors in the treatment of Parkinson's disease Br. J. Pharmacol. 161 2010 271 287
42. S.P. East, S. Bamford, M.G. Dietz, C. Eickmeier, A. Flegg, B. Ferger, M.J. Gemkow, R. Heilker, B. Hengerer, A. Kotey, P. Loke, G. Schanzle, H.D. Schubert, J. Scott, M. Whittaker, M. Williams, P. Zawadzki, and K. Gerlach An orally bioavailable positive allosteric modulator of the mGlu4 receptor with efficacy in an animal model of motor dysfunction Bioorg. Med. Chem. Lett. 20 2010 4901 4905
43. D.W. Engers, P.R. Gentry, R. Williams, J.D. Bolinger, C.D. Weaver, U.N. Menon, P.J. Conn, C.W. Lindsley, C.M. Niswender, and C.R. Hopkins Synthesis and SAR of novel, 4-(phenylsulfamoyl)phenylacetamide mGlu4 positive allosteric modulators (PAMs) identified by functional high-throughput screening (HTS) Bioorg. Med. Chem. Lett. 20 2010 5175 5178
44. G. Fabbrini, J.M. Brotchie, F. Grandas, M. Nomoto, and C.G. Goetz Levodopa-induced dyskinesias Mov. Disord. 22 2007 1379 1389
45. M.J. Fell, D.L. McKinzie, J.A. Monn, and K.A. Svensson Group II metabotropic glutamate receptor agonists and positive allosteric modulators as novel treatments for schizophrenia Neuropharmacology 62 2012 1473 1483
46. M. Feyder, A. Bonito-Oliva, and G. Fisone l-DOPA-induced dyskinesia and abnormal signaling in striatal medium spiny neurons: focus on dopamine D1 receptor-mediated transmission Front. Behav. Neurosci. 5 2011 71
47. A. Galvan, M. Kuwajima, and Y. Smith Glutamate and GABA receptors and transporters in the basal ganglia: what does their subsynaptic localization reveal about their function? Neuroscience 143 2006 351 375
48. M.P. Gleeson, A. Hersey, D. Montanari, and J. Overington Probing the links between in vitro potency, ADMET and physicochemical parameters Nat. Rev. Drug Discov. 10 2011 197 208
49. C.G. Goetz, W. Poewe, O. Rascol, and C. Sampaio Evidence-based medical review update: pharmacological and surgical treatments of Parkinson's disease: 2001 to 2004 Mov. Disord. 20 2005 523 539
50. C. Goudet, V. Binet, L. Prezeau, and J.-P. Pin Allosteric modulators of class-C G-Protein coupled receptors open new possibilities for therapeutic application Drug Discov. Today Ther. Strat. 1 2004 125 133
51. C. Goudet, F. Gaven, J. Kniazeff, C. Vol, J. Liu, M. Cohen-Gonsaud, F. Acher, L. Prézeau, and J.P. Pin Heptahelical domain of metabotropic glutamate receptor 5 behaves like rhodopsin-like receptors Proc. Natl. Acad. Sci. U. S. A. 101 2004 378 383
52. C. Goudet, E. Chapuy, A. Alloui, F. Acher, J.-P. Pin, and A. Eschalier Group III metabotropic glutamate receptors inhibit hyperalgesia in animal models of inflammation and neuropathic pain Pain 137 2008 112 124
53. C. Goudet, B. Vilar, T. Courtiol, T. Deltheil, T. Bessiron, I. Brabet, N. Oueslati, D. Rigault, H.O. Bertrand, H. McLean, H. Daniel, M. Amalric, F. Acher, and J.P. Pin A novel selective metabotropic glutamate receptor 4 agonist reveals new possibilities for developing subtype selective ligands with therapeutic potential FASEB J. 26 2012 1682 1693
54. B. Greco, S. Lopez, H. van der Putten, P.J. Flor, and M. Amalric Metabotropic glutamate 7 receptor subtype modulates motor symptoms in rodent models of Parkinson's disease J. Pharmacol. Exp. Ther. 332 2010 1064 1071
55. J.T. Greenamyre, and C.F. O'Brien N-methyl-D-Aspartate antagonists in the treatment of Parkinson's disease Arch. Neurol. 48 1991 977 981
56. J.T. Greenamyre Glutamatergic influences on the basal ganglia Clin. Neuropharmacol. 24 2001 65 70
57. P. Gubellini, B. Picconi, M. Bari, N. Battista, P. Calabresi, D. Centonze, G. Bernardi, A. Finazzi-Agro, and M. Maccarrone Experimental parkinsonism alters endocannabinoid degradation: implications for striatal glutamatergic transmission J. Neurosci. 22 2002 6900 6907
58. P. Gubellini, A. Pisani, D. Centonze, G. Bernardi, and P. Calabresi Metabotropic glutamate receptors and striatal synaptic plasticity: implications for neurological diseases Prog. Neurobiol. 74 2004 271 300
59. A. Gupta, V.L. Dawson, and T.M. Dawson What causes cell death in Parkinson's disease? Ann. Neurol. 64 Suppl. 2 2008 S3 15
60. H. Harris, and D.C. Rubinsztein Control of autophagy as a therapy for neurodegenerative disease Nat. Rev. Neurol. 8 2011 108 117
61. E.C. Hirsch, and S. Hunot Neuroinflammation in Parkinson's disease: a target for neuroprotection? Lancet Neurol. 8 2009 382 397
62. E.C. Hirsch, C. Perier, G. Orieux, C. Francois, J. Feger, J. Yelnik, M. Vila, R. Levy, E.S. Tolosa, C. Marin, M. Trinidad Herrero, J.A. Obeso, and Y. Agid Metabolic effects of nigrostriatal denervation in basal ganglia Trends Neurosci. 23 2000 S78 S85
63. J.J. Hoozemans, E.S. van Haastert, D.A. Nijholt, A.J. Rozemuller, and W. Scheper Activation of the unfolded protein response is an early event in Alzheimer's and Parkinson's disease Neurodegener. Dis. 10 2012 212 215
64. L. Iacovelli, L. Capobianco, M. Iula, V. Di Giorgi Gerevini, A. Picascia, J. Blahos, D. Melchiorri, F. Nicoletti, and A. De Blasi Regulation of mGlu4 metabotropic glutamate receptor signaling by type-2 G-protein coupled receptor kinase (GRK2) Mol. Pharmacol. 65 2004 1103 1110
65. P. Jenner, and C.W. Olanow The pathogenesis of cell death in Parkinson's disease Neurology 66 2006 S24 S36
66. P. Jenner Molecular mechanisms of l-DOPA-induced dyskinesia Nat. Rev. Neurosci. 9 2008 665 677
67. P.A. Johansen, L.A. Chase, A.D. Sinor, J.F. Koerner, R.L. Johnson, and M.B. Robinson Type 4a metabotropic glutamate receptor: identification of new potent agonists and differentiation from the L-(+)-2-Amino-4-phosphonobutanoic acid-sensitive receptor in the lateral perforant pathway in rats Mol. Pharmacol. 46 1995 140 149
68. C.K. Jones, D.W. Engers, A.D. Thompson, J.R. Field, A.L. Blobaum, S.R. Lindsley, Y. Zhou, R.D. Gogliotti, S. Jadhav, R. Zamorano, J. Bogenpohl, Y. Smith, R. Morrison, J.S. Daniels, C.D. Weaver, P.J. Conn, C.W. Lindsley, C.M. Niswender, and C.R. Hopkins Discovery, synthesis, and structure-Activity relationship development of a series of N-4-(2,5-dioxopyrrolidin-1-yl) phenylpicolinamides (VU0400195, ML182): characterization of a novel positive allosteric modulator of the metabotropic glutamate receptor 4 (mGlu(4)) with oral efficacy in an antiparkinsonian animal model J. Med. Chem. 54 2011 7639 7647
69. C.K. Jones, M. Bubser, A.D. Thompson, J.W. Dickerson, N. Turle-Lorenzo, M. Amalric, A.L. Blobaum, T.M. Bridges, R.D. Morrison, S. Jadhav, D.W. Engers, K. Italiano, J. Bode, J.S. Daniels, C.W. Lindsley, C.R. Hopkins, P.J. Conn, and C.M. Niswender The mGlu4 positive allosteric modulator VU0364770 produces efficacy alone and in combination with l-DOPA or an adenosine A2A antagonist in preclinical rodent models of Parkinson's disease J. Pharmacol. Exp. Ther. 340 2012 404 421
70. E.H. Kerns, and L. Di Pharmaceutical profiling in drug discovery Drug Discov. Today 8 2003 316 323
71. K. Klak, A. Palucha, P. Branski, M. Sowa, and A. Pilc Combined administration of PHCCC, a positive allosteric modulator of mGlu4 receptors and ACPT-I, mGlu III receptor agonist evokes antidepressant-like effects in rats Amino Acids 32 2007 169 172
72. J. Kniazeff, L. Prezeau, P. Rondard, J.-P. Pin, and C. Goudet Dimers and beyond: functional puzzles of class C GPCRs Pharmacol. Ther. 130 2011 9 25
73. J. Konieczny, J. Wardas, K. Kuter, A. Pilc, and K. Ossowska The influence of group III metabotropic glutamate receptor stimulation by (1S,3R,4S)-1-Aminocyclo-pentane-1,3,4-tricarboxylic acid on the parkinsonian-like akinesia and striatal proenkephalin and prodynorphin mRNA expression in rats Neuroscience 145 2007 611 620
74. S. Konitsiotis, P.J. Blanchet, L. Verhagen, E. Lamers, and T.N. Chase AMPA receptor blockade improves levodopa-induced dyskinesia in MPTP monkeys Neurology 54 2000 1589 1595
75. C.M. Kosinski, S. Risso Bradley, P.J. Conn, A.I. Levey, G.B. Landwehrmeyer, J.B. Penney Jr.; A.B. Young, and D.G. Standaert Localization of metabotropic glutamate receptor 7 mRNA and mGluR7a protein in the rat basal ganglia J. Comp. Neurol. 415 1999 266 284
76. N. Kunishima, Y. Shimada, Y. Tsuji, T. Sato, M. Yamamoto, T. Kumasaka, S. Nakanishi, H. Jingami, and K. Morikawa Structural basis of glutamate recognition by a dimeric metabotropic glutamate receptor Nature 407 2000 971 977
77. A. Kupsch, P.A. Loschmann, H. Sauer, G. Arnold, P. Renner, D. Pufal, M. Burg, H. Wachtel, G. ten Bruggencate, and W.H. Oertel Do NMDA receptor antagonists protect against MPTP-toxicity? Biochemical and immunocytochemical analyses in black mice Brain Res. 592 1992 74 83
78. M. Lebel, L. Chagniel, G. Bureau, and M. Cyr Striatal inhibition of PKA prevents levodopa-induced behavioural and molecular changes in the hemiparkinsonian rat Neurobiol. Dis. 38 2010 59 67
79. J. Lin, D.C. Sahakian, S.M. de Morais, J.J. Xu, R.J. Polzer, and S.M. Winter The role of absorption, distribution, metabolism, excretion and toxicity in drug discovery Curr. Top. Med. Chem. 3 2003 1125 1154
80. C.A. Lipinski, F. Lombardo, B.W. Dominy, and P.J. Feeney Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings Adv. Drug Deliv. Rev. 46 2001 3 26
81. S. Litschig, F. Gasparini, D. Rueegg, N. Stoehr, P.J. Flor, I. Vranesic, L. Prézeau, J.-P. Pin, C. Thomsen, and R. Kuhn CPCCOEt, a noncompetitive metabotropic glutamate receptor1 antagonist, inhibits receptor signaling without affecting glutamate binding Mol. Pharm. 55 1999 453 461
82. S. Lopez, N. Turle-Lorenzo, F. Acher, E. De Leonibus, A. Mele, and M. Amalric Targeting group III metabotropic glutamate receptors produces complex behavioral effects in rodent models of Parkinson's disease J. Neurosci. 27 2007 6701 6711
83. S. Lopez, N. Turle-Lorenzo, T.H. Johnston, J.M. Brotchie, S. Schann, P. Neuville, and M. Amalric Functional interaction between adenosine A2A and group III metabotropic glutamate receptors to reduce parkinsonian symptoms in rats Neuropharmacology 55 2008 483 490
84. S. Lopez, A. Bonito-Oliva, S. Pallottino, F. Acher, and G. Fisone Activation of metabotropic glutamate 4 receptors decreases l-DOPA-induced dyskinesia in a mouse model of Parkinson's disease J. Parkinsons Dis. 1 2011 339 346
85. S. Lopez, L. Jouve, T.L. N, L. Kerkerian-LeGoff, P. Salin, and M. Amalric Antiparkinsonian action of a selective group III mGlu receptor agonist is associated with reversal of subthalamonigral overactivity Neurobiol. Dis. 46 2012 69 77
86. N. Macinnes, and S. Duty Group III metabotropic glutamate receptors act as hetero-receptors modulating evoked GABA release in the globus pallidus in vivo Eur. J. Pharmacol. 580 2008 95 99
87. N. MacInnes, M.J. Messenger, and S. Duty Activation of group III metabotropic glutamate receptors in selected regions of the basal ganglia alleviates akinesia in the reserpine-treated rat Br. J. Pharmacol. 141 2004 15 22
88. M. Maj, V. Bruno, Z. Dragic, R. Yamamoto, G. Battaglia, W. Inderbitzin, N. Stoehr, T. Stein, F. Gasparini, I. Vranesic, R. Kuhn, F. Nicoletti, and P.J. Flor (-)-PHCCC, a positive allosteric modulator of mGluR4: characterization, mechanism of action, and neuroprotection Neuropharmacology 45 2003 895 906
89. P. Malherbe, N. Kratochwil, F. Knoflach, M.T. Zenner, J.N. Kew, C. Kratzeisen, H.P. Maerki, G. Adam, and V. Mutel Mutational analysis and molecular modeling of the allosteric binding site of a novel, selective, noncompetitive antagonist of the metabotropic glutamate 1 receptor J. Biol. Chem. 278 2003 8340 8347
90. M.J. Marino, D.L.J. Williams, J.A. O'Brien, O. Valenti, T.P. McDonald, M.K. Clements, R. Wang, A.G. DiLella, J.F. Hess, G.G. Kinney, and P.J. Conn Allosteric modulation of group III metabotropic glutamate receptor 4: a potential approach to Parkinson's disease treatment Proc. Natl. Acad. Sci. U. S. A. 100 2003 13668 13673
91. J.M. Mathiesen, and M.T. Ramirez The metabotropic glutamate receptor 4 is internalized and desensitized upon protein kinase C activation Br. J. Pharmacol. 148 2006 279 290
92. M.J. Messenger, L.G. Dawson, and S. Duty Changes in metabotropic glutamate receptor 1-8 gene expression in the rodent basal ganglia motor loop following lesion of the nigrostriatal tract Neuropharmacology 43 2002 261 271
93. M. Mezler, H. Geneste, L. Gault, and G.J. Marek LY-2140023, a prodrug of the group II metabotropic glutamate receptor agonist LY-404039 for the potential treatment of schizophrenia Curr. Opin. Investig. Drugs 11 2010 833 845
94. P.P. Michel, and Y. Agid The glutamate antagonist, MK-801, does not prevent dopaminergic cell death induced by the 1-methyl-4-phenylpyridinium ion (MPP+) in rat dissociated mesencephalic cultures Brain Res. 597 1992 233 240
95. R.X. Moldrich, P.M. Beart, D.E. Jane, A.G. Chapman, and B.S. Meldrum Anticonvulsant activity of 3,4-dicarboxyphenylglycines in DBA/2 mice Neuropharmacology 40 2001 732 735
96. J.A. Monn, M.J. Valli, B.G. Johnson, C.R. Salhoff, R.A. Wright, T. Howe, A. Bond, D. Lodge, L.A. Spangle, J.W. Paschal, J.B. Campbell, K. Griffey, J.P. Tizzano, and D.D. Schoepp Synthesis of the four Isomers of 4-Aminopyrrolidine-2, 4-dicarboxylate: Identification of a potent, highly selective, and systemically-Active agonist for metabotropic glutamate receptors negatively coupled to adenylate cyclase J. Med. Chem. 39 1996 2990 3000
97. J.A. Monn, M.J. Valli, S.M. Massey, R.A. Wright, C.R. Salhoff, B.G. Johnson, T. Howe, C.A. Alt, G.A. Rhodes, R.L. Robey, K.R. Griffey, J.P. Tizzano, M.J. Kallman, D.R. Helton, and D.D. Schoepp 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 1997 528 537
98. J.L. Montastruc, O. Rascol, J.M. Senard, and A. Rascol A pilot study of N-methyl-D-Aspartate (NMDA) antagonist in Parkinson's disease J. Neurol. Neurosurg. Psychiatry 55 1992 630 631
99. T. Muto, D. Tsuchiya, K. Morikawa, and H. Jingami Structures of the extracellular regions of the group II/III metabotropic glutamate receptors Proc. Natl. Acad. Sci. U. S. A. 104 2007 3759 3764
100. I. Nafia, D.B. Re, F. Masmejean, C. Melon, P. Kachidian, L. Kerkerian-Le Goff, A. Nieoullon, and L. Had-Aissouni Preferential vulnerability of mesencephalic dopamine neurons to glutamate transporter dysfunction J. Neurochem. 105 2008 484 496
101. C.M. Niswender, and P.J. Conn Metabotropic glutamate receptors: physiology, pharmacology, and disease Annu. Rev. Pharmacol. Toxicol. 50 2010 295 322
102. C.M. Niswender, C.K. Jones, and P.J. Conn New therapeutic frontiers for metabotropic glutamate receptors Curr. Top. Med. Chem. 5 2005 847 857
103. C.M. Niswender, K.A. Johnson, C.D. Weaver, C.K. Jones, Z. Xiang, Q. Luo, A.L. Rodriguez, J.E. Marlo, T. de Paulis, A.D. Thompson, E.L. Days, T. Nalywajko, C.A. Austin, M.B. Williams, J.E. Ayala, R. Williams, C.W. Lindsley, and P.J. Conn Discovery, characterization, and antiparkinsonian effect of novel positive allosteric modulators of metabotropic glutamate receptor 4 Mol. Pharmacol. 74 2008 1345 1358
104. M.J. Noetzel, J.M. Rook, P.N. Vinson, H. Cho, E. Days, Y. Zhou, A.L. Rodriguez, H. Lavreysen, S.R. Stauffer, C.M. Niswender, Z. Xiang, J.S. Daniels, C.K. Jones, C.W. Lindsley, C.D. Weaver, and P.J. Conn Functional impact of allosteric agonist activity of selective positive allosteric modulators of mGlu5 in regulating CNS function Mol. Pharmacol. 81 2012 120 133
105. J.A. Obeso, C.W. Olanow, and J.G. Nutt Levodopa motor complications in Parkinson's disease Trends Neurosci. 23 2000 S2 S7
106. J.A. Obeso, M.C. Rodriguez-Oroz, M. Rodriguez, J.L. Lanciego, J. Artieda, N. Gonzalo, and C.W. Olanow Pathophysiology of the basal ganglia in Parkinson's disease Trends Neurosci. 23 2000 S8 19
107. J.A. Obeso, M.C. Rodriguez-Oroz, J.L. Lanciego, and M. Rodriguez Diaz How does Parkinson's disease begin? The role of compensatory mechanisms Trends Neurosci. 27 2004 125 127 Author reply 127-128
108. K. Ossowska, M. Pietraszek, J. Wardas, and S. Wolfarth Potential antipsychotic and extrapyramidal effects of (R, S)-3,4-dicarboxyphenylglycine [(R, S)-3,4-DCPG], a mixed AMPA antagonist/mGluR8 agonist Pol J. Pharmacol. 56 2004 295 304
109. A. Pagano, D. Ruegg, S. Litschig, N. Stoehr, C. Stierlin, M. Heinrich, P. Floersheim, L. Prezeau, F. Carroll, J.-P. Pin, A. Cambria, I. Vranesic, P.J. Flor, F. Gasparini, and R. Kuhn The non-competitive antagonists 2-methyl-6-(phenylethynyl)pyridine and 7-hydroxyiminocyclopropan[b]chromen-1a- carboxylic acid ethyl ester interact with overlapping binding pockets in the transmembrane region of group I metabotropic glutamate receptors J. Biol. Chem. 275 2000 33750 33758
110. A. Palucha, E. Tatarczynska, P. Branski, B. Szewczyk, J.M. Wieronska, K. Klak, E. Chojnacka-Wojcik, G. Nowak, and A. Pilc Group III mGlu receptor agonists produce anxiolytic- and antidepressant-like effects after central administration in rats Neuropharmacology 46 2004 151 159
111. A. Palucha-Poniewiera, A. Klodzinska, K. Stachowicz, K. Tokarski, G. Hess, S. Schann, M. Frauli, P. Neuville, and A. Pilc Peripheral administration of group III mGlu receptor agonist ACPT-I exerts potential antipsychotic effects in rodents Neuropharmacology 55 2008 517 524
112. M.-L. Parmentier, L. Prézeau, J. Bockaert, and J.-P. Pin A model for the functioning of family 3 GPCRs Trends Pharmacol. Sci. 23 2002 268 274
113. S.T. Patil, L. Zhang, F. Martenyi, S.L. Lowe, K.A. Jackson, B.V. Andreev, A.S. Avedisova, L.M. Bardenstein, I.Y. Gurovich, M.A. Morozova, S.N. Mosolov, N.G. Neznanov, A.M. Reznik, A.B. Smulevich, V.A. Tochilov, B.G. Johnson, J.A. Monn, and D.D. Schoepp Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized Phase 2 clinical trial Nat. Med. 13 2007 1102 1107
114. B. Piallat, A. Benazzouz, and A.L. Benabid Subthalamic nucleus lesion in rats prevents dopaminergic nigral neuron degeneration after striatal 6-OHDA injection: behavioural and immunohistochemical studies Eur. J. Neurosci. 8 1996 1408 1414
115. J.P. Pin, and R. Duvoisin The metabotropic glutamate receptors: structure and functions Neuropharmacology 34 1995 1 26
116. A. Pisani, P. Calabresi, D. Centonze, and G. Bernardi Activation of group III metabotropic glutamate receptors depresses glutamatergic transmission at corticostriatal synapse Neuropharmacology 36 1997 845 851
117. A. Pisani, P. Gubellini, P. Bonsi, F. Conquet, B. Picconi, D. Centonze, G. Bernardi, and P. Calabresi Metabotropic glutamate receptor 5 mediates the potentiation of N-methyl-D-Aspartate responses in medium spiny striatal neurons Neuroscience 106 2001 579 587
118. S. Przedborski, and V. Jackson-Lewis Mechanisms of MPTP toxicity Mov. Disord. 13 Suppl. 1 1998 35 38
119. C. Rangel-Barajas, I. Silva, L.M. Lopez-Santiago, J. Aceves, D. Erlij, and B. Floran l-DOPA-induced dyskinesia in hemiparkinsonian rats is associated with up-regulation of adenylyl cyclase type V/VI and increased GABA release in the substantia nigra reticulata Neurobiol. Dis. 41 2011 51 61
120. P. Rondard, J. Liu, S. Huang, F. Malhaire, C. Vol, A. Pinault, G. Labesse, and J.-P. Pin Coupling of agonist binding to effector domain activation in metabotropic glutamate-like receptors J. Biol. Chem. 281 2006 24653 24661
121. P. Rondard, C. Goudet, J. Kniazeff, J.-P. Pin, and L. Prezeau The complexity of their activation mechanism opens new possibilities for the modulation of mGlu and GABAB class C G protein-coupled receptors Neuropharmacology 60 2011 82 92
122. S.T. Rouse, M.J. Marino, S.R. Bradley, H. Awad, M. Wittmann, and P.J. Conn Distribution and roles of metabotropic glutamate receptors in the basal ganglia motor circuit: implications for treatment of Parkinson's disease and related disorders Pharmacol. Ther. 88 2000 427 435
123. X. Rovira, D. Roche, J. Serra, J. Kniazeff, J.-P. Pin, and J. Giraldo Modeling the binding and function of metabotropic glutamate receptors J. Pharmacol. Exp. Ther. 325 2008 443 456
124. E. Santini, E. Valjent, A. Usiello, M. Carta, A. Borgkvist, J.A. Girault, D. Herve, P. Greengard, and G. Fisone Critical involvement of cAMP/DARPP-32 and extracellular signal-regulated protein kinase signaling in l-DOPA-induced dyskinesia J. Neurosci. 27 2007 6995 7005
125. E. Santini, M. Heiman, P. Greengard, E. Valjent, and G. Fisone Inhibition of mTOR signaling in Parkinson's disease prevents l-DOPA-induced dyskinesia Sci. Signal. 2 2009 ra36
126. H. Schaffhauser, B.A. Rowe, S. Morales, L.E. Chavez-Noriega, R. Yin, C. Jachec, S.P. Rao, G. Bain, A.B. Pinkerton, J.M. Vernier, L.J. Bristow, M.A. Varney, and L.P. Daggett Pharmacological characterization and identification of amino acids involved in the positive modulation of metabotropic glutamate receptor subtype 2 Mol. Pharmacol. 64 2003 798 810
127. A. Schrag, and N. Quinn Dyskinesias and motor fluctuations in Parkinson's disease. A community-based study Brain 123 Pt 11 2000 2297 2305
128. C. Selvam, N. Oueslati, I. Lemasson, I. Brabet, D. Rigault, T. Courtiol, S. Cesarini, N. Triballeau, H.-O. Bertrand, C. Goudet, J.-P. Pin, and F.C. Acher A virtual screening hit reveals new possibilities for developing group III metabotropic glutamate receptor agonists J. Med. Chem. 53 2010 2797 2813
129. G. Servant, C. Tachdjian, X. Li, and D.S. Karanewsky The sweet taste of true synergy: positive allosteric modulation of the human sweet taste receptor Trends Pharmacol. Sci. 32 2011 631 636
130. P. Sibille, S. Lopez, I. Brabet, O. Valenti, N. Oueslati, F. Gaven, C. Goudet, H.-O. Bertrand, J. Neyton, M.J. Marino, M. Amalric, J.-P. Pin, and F.C. Acher Synthesis and biological evaluation of 1-Amino-2- phosphonomethylcyclopropane carboxylic acids, new group III metabotropic glutamate receptor agonists J. Med. Chem. 50 2007 3585 3595
131. Y. Smith, T. Wichmann, S.A. Factor, and M.R. DeLong Parkinson's disease therapeutics: new developments and challenges since the introduction of levodopa Neuropsychopharmacology 37 2012 213 246
132. P.K. Sonsalla, W.J. Nicklas, and R.E. Heikkila Role for excitatory amino acids in methamphetamine-induced nigrostriatal dopaminergic toxicity Science 243 1989 398 400
133. P.K. Sonsalla, G.D. Zeevalk, L. Manzino, A. Giovanni, and W.J. Nicklas MK-801 fails to protect against the dopaminergic neuropathology produced by systemic 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine in mice or intranigral 1-methyl-4-phenylpyridinium in rats J. Neurochem. 58 1992 1979 1982
134. M.S. Starr, B.S. Starr, and S. Kaur Stimulation of basal and l-DOPA-induced motor activity by glutamate antagonists in animal models of Parkinson's disease Neurosci. Biobehav. Rev. 21 1997 437 446
135. S.J. Sukoff Rizzo, S.K. Leonard, A. Gilbert, P. Dollings, D.L. Smith, M.Y. Zhang, L. Di, B.J. Platt, S. Neal, J.M. Dwyer, C.N. Bender, J. Zhang, T. Lock, D. Kowal, A. Kramer, A. Randall, C. Huselton, K. Vishwanathan, S.Y. Tse, J. Butera, R.H. Ring, S. Rosenzweig-Lipson, Z.A. Hughes, and J. Dunlop The metabotropic glutamate receptor 7 allosteric modulator AMN082: a monoaminergic
136. Y. Tanabe, A. Nomura, M. Masu, R. Shigemoto, N. Mizuno, and S. Nakanishi Signal transduction, pharmacologic properties, and expression patterns of two rat metabotropic glutamate receptors, mGluR3 and mGluR4 J. Neurosci. 13 1993 1372 1378
137. M.G. Tansey, and M.S. Goldberg Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention Neurobiol. Dis. 37 2010 510 518
138. N.K. Thomas, R.A. Wright, P.A. Howson, A.E. Kingston, D.D. Schoepp, and D.E. Jane (S)-3,4-DCPG, a potent and selective mGlu8a receptor agonist, activates metabotropic glutamate receptors on primary afferent terminals in the neonatal rat spinal cord Neuropharmacology 40 2001 311 318
139. N. Triballeau, F. Acher, I. Brabet, J.-P. Pin, and H.-O. Bertrand Virtual screening workflow development guided by the ROC curve approach. Application to high-throughput docking on metabotropic glutamate receptor subtype 4 J. Med. Chem. 48 2005 2534 2547
140. 3+ Proc. Natl. Acad. Sci. U. S. A. 99 2002 2660 2665
141. L. Turski, K. Bressler, K.J. Rettig, P.A. Loschmann, and H. Wachtel Protection of substantia nigra from MPP+ neurotoxicity by N-methyl-d-Aspartate antagonists Nature 349 1991 414 418
142. S. Urwyler Allosteric modulation of family C G-protein-coupled receptors: from molecular insights to therapeutic perspectives Pharmacol. Rev. 63 2011 59 126
143. O. Valenti, M.J. Marino, M. Wittmann, E. Lis, A.G. DiLella, G.G. Kinney, and P.J. Conn Group III metabotropic glutamate receptor-mediated modulation of the striatopallidal synapse J. Neurosci. 23 2003 7218 7226
144. O. Valenti, G. Mannaioni, G.R. Seabrook, P.J. Conn, and M.J. Marino Group III metabotropic glutamate-receptor-mediated modulation of excitatory transmission in rodent substantia nigra pars compacta dopamine neurons J. Pharmacol. Exp. Ther. 313 2005 1296 1304
145. K. Vekrellis, M. Xilouri, E. Emmanouilidou, H.J. Rideout, and L. Stefanis Pathological roles of alpha-synuclein in neurological disorders Lancet Neurol. 10 2011 1015 1025
146. A.C. Vernon, S. Palmer, K.P. Datla, V. Zbarsky, M.J. Croucher, and D.T. Dexter Neuroprotective effects of metabotropic glutamate receptor ligands in a 6-hydroxydopamine rodent model of Parkinson's disease Eur. J. Neurosci. 22 2005 1799 1806
147. A.C. Vernon, V. Zbarsky, K.P. Datla, D.T. Dexter, and M.J. Croucher Selective activation of group III metabotropic glutamate receptors by L-(+)-2-Amino-4-phosphonobutryic acid protects the nigrostriatal system against 6-hydroxydopamine toxicity in vivo J. Pharmacol. Exp. Ther. 320 2007 397 409
148. Y.Q. Wang, H.J. Hu, R. Cao, and L.W. Chen Differential co-localization of neurokinin-3 receptor and NMDA/AMPA receptor subunits in neurons of the substantia nigra of C57/BL mice Brain Res. 1053 2005 207 212
149. G. Wasner, and G. Deuschl Pains in Parkinson disease-many syndromes under one umbrella Nat. Rev. Neurol. 2012 (Epub ahead of print)
150. J.E. Westin, L. Vercammen, E.M. Strome, C. Konradi, and M.A. Cenci Spatiotemporal pattern of striatal ERK1/2 phosphorylation in a rat model of L-DOPA-induced dyskinesia and the role of dopamine D1 receptors Biol. Psychiatry 62 2007 800 810
151. M. Wittmann, M.J. Marino, S.R. Bradley, and P.J. Conn Activation of group III mGluRs inhibits GABAergic and glutamatergic transmission in the substantia nigra pars reticulata J. Neurophysiol. 85 2001 1960 1968
152. M. Wittmann, M.J. Marino, and P.J. Conn Dopamine modulates the function of group II and group III metabotropic glutamate receptors in the substantia nigra pars reticulata J. Pharmacol. Exp. Ther. 302 2002 433 441
153. F. Zhang, B. Klebansky, R.M. Fine, H. Xu, A. Pronin, H. Liu, C. Tachdjian, and X. Li Molecular mechanism for the umami taste synergism Proc. Natl. Acad. Sci. U. S. A. 105 2008 20930 20934
154. F. Zhang, B. Klebansky, R.M. Fine, H. Liu, H. Xu, G. Servant, M. Zoller, C. Tachdjian, and X. Li Molecular mechanism of the sweet taste enhancers Proc. Natl. Acad. Sci. U. S. A. 107 2010 4752 4757