Activation of group III metabotropic glutamate receptors by endogenous glutamate protects against glutamate-mediated excitotoxicity in the hippocampus in vivo

Journal of Neuroscience Research

Volumn 90, Issue 5, 2012, Pages 1055-1066

  Vera, Gabriela ^a   Tapia, Ricardo ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

4 aminopyridine; Epilepsy; Glutamate transport; Metabotropic glutamate receptors; Neurodegeneration

Indexed keywords

4 AMINOPYRIDINE; DICARBOXYLIC ACID; DIZOCILPINE; GLUTAMATE RECEPTOR; METABOTROPIC RECEPTOR 3; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PYRROLIDINE DERIVATIVE;

AMINO ACID ANALYSIS; AMINO ACID TRANSPORT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DISEASE SEVERITY; ELECTROENCEPHALOGRAM; EPILEPTIC STATE; EXCITOTOXICITY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HISTOLOGY; HYPERSALIVATION; IN VIVO STUDY; LOCOMOTION; MALE; MICRODIALYSIS; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SEIZURE; TONIC CLONIC SEIZURE;

4-AMINOPYRIDINE; AMINO ACIDS; ANIMALS; CARBOXYLIC ACIDS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROCHEMISTRY; ELECTROENCEPHALOGRAPHY; EPILEPSY; EXCITATORY AMINO ACID ANTAGONISTS; EXTRACELLULAR FLUID; GLUTAMIC ACID; HIPPOCAMPUS; MALE; MICRODIALYSIS; PHOSPHOSERINE; POTASSIUM CHANNEL BLOCKERS; PYRIDINES; RATS; RATS, WISTAR; RECEPTORS, METABOTROPIC GLUTAMATE; TIME FACTORS;

EID: 84858009151     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23006     Document Type: Article

References (53)

1. Ayala GX, Tapia R. 2003. Expression of heat shock protein 70 induced by 4-aminopyridine through glutamate-mediated excitotoxic stress in rat hippocampus in vivo. Neuropharmacology 45: 649-660.
2. Ayala GX, Tapia R. 2005. Late N-methyl-D-aspartate receptor blockade rescues hippocampal neurons from excitotoxic stress and death after 4-aminopyridine-induced epilepsy. Eur J Neurosci 22: 3067-3076.
3. Bradley SR, Levey AI, Hersch SM. Conn PJ. 1996. Immunocytochemical localization of group III metabotropic glutamate receptors in the hippocampus with subtype-specific antibodies. J Neurosci 16: 2044-2056.
4. 4. Neuropharmacology 34: 239-241.
5. Bushell TJ, Jane DE, Tse H-W, Watkins JC, Garthwaite J, Collingridge GL. 1996. Pharmacological antagonism of the actions of group II and III mGluR agonists in the lateral perforant path of rat hippocampal slices. Brit J Pharmacol 117: 1457-1462.
6. Cartmell J, Schoepp DD. 2000. Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 75: 889-907.
7. Corona JC, Tapia R. 2004. AMPA receptor activation, but no accumulation of endogenous extracellular glutamate, induces paralysis and motor neuron death in spinal cord in vivo. J Neurochem 89: 988-997.
8. Franks NP. 2008. General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 9: 370-386.
9. Gereau RWIV, Conn PJ. 1995. Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J Neurosci 15: 6879-6889.
10. Gereau RWIV, Conn PJ, Robert W. 1995. Roles of specific metabotropic glutamate receptor subtypes in regulation of hippocampal CA1 pyramidal cell excitability. J Neurophysiol 74: 122-129.
11. Guiramand J, Martin A, de Jesus M-C, Cohen-Solal C, Vignes M, Récasens M. 2005. Gliotoxicity in hippocampal cultures is induced by transportable, but not by nontransportable, glutamate uptake inhibitors. J Neurosci Res 81: 199-207.
12. Lievens J-C, Bernal F, Forni C, Mahy N, Kerkerian-Le Goff L. 2000. Characterization of striatal lesions produced by glutamate uptake alteration: cell death, reactive gliosis, and changes in GLT1 and GADD45 mRNA expression. Glia 29: 222-232.
13. Macek TA, Winde DG, Gereau RWIV, 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.
14. MacInnes N, Duty S. 2008. Group III metabotropic receptors act as hetero-receptors modulating evoked GABA release in the globus pallidus in vivo. Eur J Pharmacol 580: 95-99.
15. Martin D, Plagenhoef M, Abraham J, Dennison R, Aronstam R. 1995. Volatile anesthetic and glutamate activation of N-methyl-D-aspartate receptors. Biochem Pharmacol 49: 809-817.
16. Massieu L, Tapia R. 1997. Glutamate uptake impairment and neuronal damage in young and ages rats in vivo. J Neurochem 69: 1151-1160.
17. Massieu L, Morales-Villagrán A, Tapia R. 1995. Accumulation of extracellular glutamate by inhibition of its uptake is not sufficient for inducing neuronal damage: an in vivo microdialysis study. J Neurochem 64: 2262-2271.
18. Massieu L, del Río P, Montiel T. 2001. Neurotoxicity of glutamate uptake inhibition in vivo: correlation with succinate dehydrogenase activity and prevention by energy substrates. Neuroscience 106: 669-677.
19. Matsui T, Kita H. 2003. Activation of group III metabotropic glutamate receptors presynaptically reduces both GABAergic and glutamatergic transmission in the rat globus pallidus. Neuroscience 122: 727-737.
20. Mitchell SJ, Silver RA. 2000. Glutamate spillover suppresses inhibition by activating presynaptic mGluRs. Nature 404: 498-502.
21. Montiel T, Camacho A, Estrada-Sánchez AM, Massieu L. 2005. Differential effects of the substrate inhibitor L-trans-pyrrolidine-2, 4-dicarboxylate (PDC) and the non-substrate inhibitor DL-threo-β-benzyloxyaspartate (DL-TBOA) of glutamate transporters on neuronal damage and extracellular amino acid levels in rat brain in vivo. Neuroscience 133: 667-678.
22. Morales-Villagrán A, Ureña-Guerrero ME, Tapia R. 1996. Protection by NMDA receptor antagonist against seizures induced by intracerebral administration of 4-aminopyridine. Eur J Pharmacol 305: 87-93.
23. Obrenovitch TP, Urenjak J, Zilkha E. 1996. Evidence disputing the link between seizure activity and high extracellular glutamate. J Neurochem 66: 2446-2454.
24. Ohishi H, Nomura S, Ding Y, Shigemoto R, Wada E, Kinoshita A, Li J, Neki A, Nakanishi S, Mizuno N. 1995. Presynaptic localization of metabotropic glutamate receptor, mGluR7, in the primary afferent neurons: an immunohistochemical study in the rat. Neurosci Lett 202: 85-88.
25. Oliet SHR, Piet R, Poulain DA. 2001. Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292: 923-925.
26. Panatier A, Poulain DA, Oliet SHR. 2004. Regulation of transmitter release by high-affinity group III mGluRs in the supraoptic nucleus of the rat hypothalamus. Neuropharmacology 47: 333-341.
27. Paxinos G, Watson C. 1982. The rat brain in stereotaxic coordinates. Sydney: Academic Press.
28. Peña F, Tapia R. 1999. Relationships among seizures, extracellular amino acid changes, and neurodegeneration induced by 4-aminopyridine in rat hippocampus: a microdialysis and electroencephalographic study. J Neurochem 72: 2006-2014.
29. Peña F, Tapia R. 2000. Seizures and neurodegeneration induced by 4-aminopyridine in rat hippocampus in vivo: role of glutamate- and GABA-mediated neurotransmission and of ion channels. Neuroscience 101: 547-561.
30. Peña F, Bargas J, Tapia R. 2002. Paired pulse facilitation is turned into paired pulse depression in hippocampal slices after epilepsy induced by 4-aminopyridine in vivo. Neuropharmacology 42: 807-812.
31. Piet R, Bonhomme R, Theodosis DT, Poulain DA, Oliet SHR. 2003. Modulation of GABAergic transmission by endogenous glutamate in the rat supraoptic nucleus. Eur J Neurosci 17: 1777-1785.
32. Piet R, Vargova L, Sykova E, Poulain DA, Oliet SHR. 2004. Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc Nat Acad Sci U S A 101: 2151-2155.
33. Pinheiro PS, Mulle C. 2008. Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat Rev Neurosci 9: 423-436.
34. Ramírez-Munguía N, Vera G, Tapia R. 2003. Epilepsy, neurodegeneration and extracellular glutamate in the hippocampus of awake and anesthetized rats treated with okadaic acid. Neurochem Res 20: 1517-1524.
35. Ré DB, Boucraut J, Samuel D, Birman S, Kerkerian-Le Goff L, Had-Aissouni H. 2003. Glutamate transport alteration triggers differentiation-state selective oxidative death of cultured astrocytes: a mechanism different from excitotoxicity depending on intracellular GSH contents. J Neurochem 85: 1159-1170.
36. Rudolph U, Antkowiak B. 2004. Molecular and neuronal substrates for general anesthetics. Nat Rev Neurosci 5: 709-720.
37. 4 and MCCG, in the rat thalamus in vivo. Neuroscience 65: 5-13.
38. Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA. 1997. Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385: 630-634.
39. Schoepp DD. 2001. Unveiling the functions of the presynaptic metabotropic glutamate receptors in the central nervous system. J Pharmacol Exp Ther 299: 12-20.
40. Sekiyama N, Hayashi Y, Nakanishi S, Jane DE, Tse H-W, Brise EF, Watkins JC. 1996. Structure-activity relationships of new agonists and antagonists of different metabotropic glutamate receptor subtypes. Br J Pharmacol 117: 1493-1503.
41. Selkirk JV, Naeve GS, Foster AC. 2003. Blockade of excitatory amino acid transporters in the rat hippocampus results in enhanced activation of group I and group III metabotropic glutamate receptors. Neuropharmacology 45: 885-894.
42. Semyanov A, Kullmann DM. 2000. Modulation of GABAergic signaling among interneurons by metabotropic glutamate receptors. Neuron 25: 663-672.
43. Shigemoto R, Kulik A, Roberts JDB, Ohishi H, Nusser Z, Kaneko T, Somogyi P. 1996. Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381: 523-525.
44. 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.
45. Thomas NK, Jane DE, Tse H-W, Watkins JC. 1996. α-Methyl derivatives of serine-O-phosphate as novel, selective competitive metabotropic glutamate receptor antagonists. Neuropharmacology 35: 637-642.
46. Tovar-y-Romo LB, Tapia R. 2006. Cerebral neurons of transgenic ALS mice are vulnerable to glutamate release stimulation but not to increased extracellular glutamate due to transport blockade. Exp Neurol 199: 281-290.
47. Tovar-y-Romo LB, Santa-Cruz LD, Zepeda A, Tapia R. 2009. Chronic elevation of extracellular glutamate due to transport blockade is innocuous for spinal motoneurons in vivo. Neurochem Int 54: 186-191.
48. Tzingounis AV, Wadiche JI. 2007. Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 8: 935-947.
49. Valenti O, Marino MJ, Wittmann M, Lis E, DiLella AG, Kinney GG, Conn PJ. 2003. Group III metabotropic glutamate receptor-mediated modulation of the striatopallidal synapse. J Neurosci 23: 7218-7226.
50. Vázquez E, Sánchez-Prieto J. 1997. Presynaptic modulation of glutamate release targets different calcium channels in rat cerebrocortical nerve terminals. Eur J Neurosci 9: 2009-2018.
51. Velasco I, Tapia R, Massieu L. 1996. Inhibition of glutamate uptake induces progressive accumulation of extracellular glutamate and neuronal damage in rat cortical cultures. J Neurosci Res 44: 551-561.
52. Vernon AC, Palmer S, Datla KP, Zbarsky V, Croucher MJ, Dexter DT. 2005. Neuroprotective effects of metabotropic glutamate receptor ligands in a 6-hydroxydopamine rodent model of Parkinson's disease. Eur J Neurosci 22: 1799-1806.
53. Wakasugi M, Hirota K, Roth S, Ito Y. 1999. The effects of general anesthetics on excitatory and inhibitory synaptic transmission in area CA1 of the hippocampus in vitro. Anesth Analg 88: 676-680.