In vivo modulation of extracellular hippocampal glutamate and GABA levels and limbic seizures by group I and II metabotropic glutamate receptor ligands

Journal of Neurochemistry

Volumn 88, Issue 5, 2004, Pages 1068-1077

  Smolders, Ilse ^a   Lindekens, Hilde ^a   Clinckers, Ralph ^a   Meurs, Alfred ^b   O'Neill, Michael J ^c   Lodge, David ^c   Ebinger, Guy ^b   Michotte, Yvette ^a  

^a PHARMACEUTICAL INSTITUTE   (Belgium)

^b UNIVERSITY HOSPITAL BRUSSELS   (Belgium)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

Epilepsy; GABA; Glutamate; Hippocampus; Metabotropic glutamate receptors; Microdialysis

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; 3,5 DIHYDROXYPHENYLGLYCINE; 4 AMINOBUTYRIC ACID; 4 CARBOXY 2 METHYLPHENYLGLYCINE; GLUTAMIC ACID; LIGAND; METABOTROPIC RECEPTOR; PILOCARPINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTICONVULSANT ACTIVITY; ARTICLE; COMPLEX PARTIAL SEIZURE; CONTROLLED STUDY; DIALYSATE LEVEL; DRUG RECEPTOR BINDING; HIPPOCAMPUS; MICRODIALYSIS; NONHUMAN; PRIORITY JOURNAL; RAT;

AMINO ACIDS; ANIMALS; ANTICONVULSANTS; BENZOATES; BICYCLO COMPOUNDS, HETEROCYCLIC; CYCLOPROPANES; DISEASE MODELS, ANIMAL; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXTRACELLULAR FLUID; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GLYCINE; HIPPOCAMPUS; LIGANDS; LIMBIC SYSTEM; MALE; MICRODIALYSIS; PILOCARPINE; PYRIDINES; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; SEIZURES;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 1442274950     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.02251.x     Document Type: Article

References (47)

1. Arvanov V. L., Holmes K. H., Keele N. B. and Shinnick-Gallagher P. (1995) The functional role of metabotropic glutamate receptors in epileptiform activity induced by 4-aminopyridine in the rat amygdala slice. Brain Res. 669, 140-144.
2. Attwell P. J., Singh Kent N., Jane D. E., Croucher M. J. and Bradford H. F. (1998) Anticonvulsant and glutamate release-inhibiting properties of the highly potent metabotropic glutamate receptor agonist (2S,2′R., 3′R.)-2-(2′,3′-dicarboxycyclopropyl) glycine (DCG-IV). Brain Res. 805, 138-143.
3. Baker D. A., Xi Z. X., Shen H., Swanson C. J. and Kalivas P. W. (2002) The origin and neuronal function of in vivo non-synaptic glutamate. J. Neurosci. 22, 9134-9141.
4. Battaglia G., Monn J. A. and Schoepp D. D. (1997) In vivo inhibition of veratridine-evoked release of striatal excitatory amino acids by the group II metabotropic glutamate receptor agonist LY354740 in rats. Neurosci. Lett. 229, 161-164.
5. Battaglia G., Bruno V., Pisani A., Centonze D., Catania M. V., Calabresi P. and Nicoletti F. (2001) Selective blockade of type-1 metabotropic glutamate receptors induces neuroprotection by enhancing GABAergic transmission. Mol. Cell Neurosci. 17, 1071-1083.
6. Bond A., Ragumoorthy N., Monn J. A., Hicks C. A., Ward M. A., Lodge D. and O'Neill M. J. (1999) LY379268, a potent and selective group II metabotropic glutamate receptor agonist, is neuroprotective in gerbil global, but not focal, cerebral ischaemia. Neurosci. Lett. 273, 191-194.
7. Bordi F. and Ugolini A. (1999) Group I metabotropic glutamate receptors: implications for brain diseases. Prog. Neurobiol. 59, 55-79.
8. Bruno V., Battaglia G., Copani A., D'Onofrio M., Di Iorio P., De Blasi A., Melchiorri D., Flor P. J. and Nicoletti F. (2001) Metabotropic glutamate receptor subtypes as targets for neuroprotective drugs. J. Cereb. Blood Flow Metab. 21, 1013-1033.
9. Burke J. P. and Hablitz J. J. (1995) Modulation of epileptiform activity by metabotropic glutamate receptors in immature rat neocortex. J. Neurophysiol. 73, 205-217.
10. Cartmell J. and Schoepp D. D. (2000) Regulation of neurotransmitter release by metabotropic glutamate receptors. J. Neurochem. 75, 889-907.
11. Chapman A. G. (2000) Glutamate and epilepsy. J. Nutr. 130, 1043S-1045S.
12. Chapman A. G., Yip P. K., Yap J. S., Quinn L. P., Tang E., Harris J. R. and Meldrum B. S. (1999) Anticonvulsant actions of LY 367385 (+)-2-methyl-4-carboxyphenylglycine) and AIDA (RS)-1-amino-indan-1,5-dicarboxylic acid). Eur. J. Pharmacol. 368, 17-24.
13. Chapman A. G., Nanan K., Williams M. and Meldrum B. S. (2000) Anticonvulsant activity of two metabotropic glutamate group I antagonists selective for the mGlu5 receptor: 2-methyl-6-(phenylethynyl)-pyridine (MPEP), and (E)-6-methyl-2-styryl-pyridine (SIB 1893). Neuropharmacology 39, 1567-1574.
14. Conn P. J. and Pin J. P. (1997) Pharmacology and functions of metabotropic glutamate receptors. Annu. Rev. Pharmacol. Toxicol. 37, 205-237.
15. Cozzi A., Attucci S., Peruginelli F., Marinozzi M., Luneia R., Pellicciari R. and Moroni F. (1997) Type 2 metabotropic glutamate (mGlu) receptors tonically inhibit transmitter release in rat caudate nucleus: in vivo studies with (2S, 1′S,2′S,3′R.)-2-(2′-carboxy-3′ -phenylcyclopropyl) glycine, a new potent and selective antagonist. Eur. J. Neurosci. 9, 1350-1355.
16. Dietrich D., Kral T., Clusmann H., Friedl M. and Schramm J. (2002) Presynaptic group II metabotropic glutamate receptors reduce stimulated and spontaneous transmitter release in human dentate gyrus. Neuropharmacology 42, 297-305.
17. Folbergrova J., Haugvicova R. and Mares P. (2001) Attenuation of seizures induced by homocysteic acid in immature rats by metabotropic glutamate group II and group III receptor agonists. Brain Res. 908, 120-129.
18. Gasparini F., Lingenhohl K., Stoehr N. et al. (1999) 2-Methyl-6-(phenylethynyl)-pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist. Neuropharmacology 38, 1493-1503.
19. Gereau R. W. and Conn P. J. (1995) Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J. Neurosci. 15, 6879-6889.
20. Greenslade R. G., Woodhouse S., O'Neill M. J., Bond A., Ward M. A. and Mitchell S. N. (1999) Is there a role for GABA in the neuroprotective effects of LY379268, a group II mGluR agonist, in global cerebral ischemia? Proceedings of the 8th International Conference on in vivo Methods, June 19-23, 1999, New York, NY.
21. Hardison J. L., Okazaki M. M. and Nadler J. V. (2000) Modest increase in extracellu]ar potassium unmasks effect of recurrent mossy fiber growth. J. Neurophysiol. 84, 2380-2389.
22. Herrero I., Miras-Portugal M. T. and Sanchez-Prieto J. (1998) Functional switch from facilitation to inhibition in the control of glutamate release by metabotropic glutamate receptors. J. Biol. Chem. 273, 1951-1958.
23. Ireland D. R. and Abraham W. C. (2002) Group I mGluRs increase excitability of hippocampal CA1 pyramidal neurons by a PLC-independent mechanism. J. Neurophysiol. 88, 107-116.
24. Kingston A. E., Ornstein P. L., Wright R. A., Johnson B. G., Mayne N. G., Bumett J. P., Belagaje R., Wu S. and Schoepp D. D. (1998) LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37, 1-12.
25. Klodzinska A., Bijak M., Chojnacka-Wojcik E., Kroczka B., Swiader M., Czuczwar S. J. and Pilc A. (2000) Roles of group II metabotropic glutamate receptors in modulation of seizure activity. Naunyn Schmiedebergs Arch. Pharmacol. 361, 283-288.
26. Merlin L. R., Taylor G. W. and Wong R. K. (1995) Role of metabotropic glutamate receptor subtypes in the patterning of epileptiform activities in vitro. J. Neurophysiol. 74, 896-900.
27. Moldrich R. X., Beart P. M., Jane D. E., Chapman A. G. and Meldrum B. S. (2001a) Anticonvulsant activity of 3,4-dicarboxyphenylglycines in DBA/2 mice. Neuropharmacology 40, 732-735.
28. Moldrich R. X., Jeffrey M., Talebi A., Beart P. M., Chapman A. G. and Meldrum B. S. (2001b) Anti-epileptic activity of group II metabotropic glutamate receptor agonists (-)-2-oxa-4-aminobicyclo[3.1.0]hexane-4,6-dicarboxylate (LY379268) and (-)-2-thia-4-aminobicyclo[3.1.0]hexane-4,6-dicarboxylate (LY389795). Neuropharmacology 41, 8-18.
29. Moldrich R. X., Talebi A., Beart P. M., Chapman A. G. and Meldrum B. S. (2001c) The mGlu (2/3) agonist 2R,4R-4-aminopyrrolidine-2, 4-dicarboxylate, is anti- and proconvulsant in DBA/2 mice. Neurosci. Lett. 299, 125-129.
30. Monn J. A., Valli M. J., Massey S. M. et al. (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, 1027-10140.
31. Moroni F., Cozzi A., Lombardi G., Sourtcheva S., Leonardi P., Carfi M. and Pellicciari R. (1998) Presynaptic mGlu1 type receptors potentiate transmitter output in the rat cortex. Eur. J. Pharmacol. 347, 189-195.
32. Murray T. K., Messenger M. J., Ward M. A., Woodhouse S., Osborne D. J., Duty S. and O'Neill M. J. (2002) Evaluation of the mGluR2/3 agonist LY379268 in rodent models of Parkinson's disease. Pharmacol. Biochem. Behav. 73, 455-466.
33. Nicoletti F., Bruno V., Catania M. V., Battaglia G., Copani A., Barbagallo G., Cena V., Sanchez-Prieto J., Spano P. F. and Pizzi M. (1999) Group-I metabotropic glutamate receptors: hypotheses to explain their dual role in neurotoxicity and neuroprotection. Neuropharmacology 38, 1477-1484.
34. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press Inc, San Diego.
35. Pellegrini-Giampietro D. E., Peruginelli F., Meli E., Cozzi A., Albani-Torregrossa S., Pellicciari R. and Moroni F. (1999) Protection with metabotropic glutamate 1 receptor antagonists in models of ischemic neuronal death: time-course and mechanisms. Neuropharmacology 38, 1607-1619.
36. Pin J. P., De Colle C., Bessis A. S. and Acher F. (1999) New perspectives for the development of selective metabotropic glutamate receptor ligands. Eur. J. Pharmacol. 375, 277-294.
37. Racine R. J. (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32, 281-294.
38. Sacaan A. I. and Schoepp D. D. (1992) Activation of hippocampal metabotropic excitatory amino acid receptors leads to seizures and neuronal damage. Neurosci. Lett. 139, 77-82.
39. Schoepp D. D. (2001) Unveiling the functions of presynaptic metabotropic glutamate receptors in the central nervous system. J. Pharmacol. Exp. Ther. 299, 12-20.
40. Schoepp D. D., Jane D. E. and Monn J. A. (1999) Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38, 1431-1476.
41. Smolders I., Sarre S., Michotte Y. and Ebinger G. (1995) The analysis of excitatory, inhibitory and other amino acids in rat brain microdialysates using microbore liquid chromatography. J. Neurosci. Meth 57, 47-53.
42. Smolders I., Khan G. M., Lindekens H., Prikken S., Marvin C. A., Manil J., Ebinger G. and Michotte Y. (1997a) Effectiveness of vigabatrin against focally evoked pilocarpine-induced seizures and concomitant changes in extracellular hippocampal and cerebellar glutamate, γ-aminobutyric acid and dopamine levels, a microdialysis-electrocorticography study in freely moving rats. J. Pharmacol. Exp. Ther. 283, 1239-1248.
43. Smolders I., Khan G. M., Manil J., Ebinger G. and Michotte Y. (1997b) NMDA receptor-mediated pilocarpine-induced seizures: characterization in freely moving rats by microdialysis. Br. J. Pharmacol. 121, 1171-1179.
44. Smolders I., Bortolotto Z. A., Clarke V. R. et al. (2002) Antagonists of GLU (K5)-containing kainate receptors prevent pilocarpihe-induced limbic seizures. Nat. Neurosci. 5, 796-804.
45. Tizzano J. P., Griffey K. I. and Schoepp D. D. (1995) Induction or protection of limbic seizures in mice by mGluR subtype selective agonists. Neuropharmacology 34, 1063-1067.
46. Wisniewski K. and Carr H. (2002) (S)-3,5-DHPG: a review. CNS Drug Rev. 8, 101-116.
47. Xi Z. X., Baker D. A., Shan H., Carson D. S. and Kalivas P. W. (2002) Group II metabotropic glutamate receptors modulate extracellular glutamate in the nucleus accumbens. J. Pharmacol. Exp. Ther. 300, 162-171.