Medial perforant path inhibition mediated by mGluR7 is reduced after status epilepticus

Journal of Neurophysiology

Volumn 92, Issue 3, 2004, Pages 1549-1557

  Bough, Kristopher J ^a   Mott, David D ^a   Dingledine, Raymond J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METABOTROPIC RECEPTOR 7; PILOCARPINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; EPILEPTIC STATE; EPILEPTOGENESIS; HIPPOCAMPUS; KNOCKOUT MOUSE; MOUSE; NEUROTRANSMISSION; NONHUMAN; PERFORANT NERVE TRACT; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPSE; WILD TYPE;

ANIMALS; EXCITATORY AMINO ACID AGONISTS; MALE; MICE; MICE, KNOCKOUT; NEURAL INHIBITION; PERFORANT PATHWAY; RECEPTORS, METABOTROPIC GLUTAMATE; STATUS EPILEPTICUS; SYNAPTIC TRANSMISSION;

EID: 4143052597     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00315.2004     Document Type: Article

References (53)

1. Abdul-Ghani AS, Attwell PJ, Singh Kent N, Bradford HF, Croucher MJ, and Jane DE. Anti-epileptogenic and anticonvulsant activity of L-2-amino-4- phosphonobutyrate, a presynaptic glutamate receptor agonist. Brain Res 755: 202-212, 1997.
2. Allen JW, Ivanova SA, Fan L, Espey MG, Basile AS, and Faden AI. Group II metabotropic glutamate receptor activation attenuates traumatic neuronal injury and improves neurological recovery after traumatic brain injury. J Pharmacol Exp Ther 290: 112-120, 1999.
3. Anwyl R. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev 29: 83-120, 1999.
4. Aronica EM, Gorter JA, Paupard MC, Grooms SY, Bennett MV, and Zukin RS. Status epilepticus-induced alterations in metabotropic glutamate receptor expression in young and adult rats. J Neurosci 17: 8588-8595, 1997.
5. Aronica EM, van Vliet EA, Mayboroda OA, Troost D, da Silva FH, and Gorter JA. Upregulation of metabotropic glutamate receptor subtype mGluR3 and mGluR5 in reactive astrocytes in a rat model of mesial temporal lobe epilepsy. Eur J Neurosci 12: 2333-2344, 2000.
6. Attwell PJ, Singh Kent N, Jane DE, Croucher MJ, and Bradford HF. 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, 1998.
7. Behr J, Lyson KJ, and Mody I. Enhanced propagation of epileptiform activity through the kindled dentate gyrus. J Neurophysiol 79: 1726-1732, 1998.
8. Bender RA, Soleymani SV, Brewster AL, Nguyen ST, Beck H, Mathern GW, and Baram TZ. Enhanced expression of a specific hyperpolarization-activated cyclic nucleotide-gated cation channel (HCN) in surviving dentate gyrus granule cells of human and experimental epileptic hippocampus. J Neurosci 23: 6826-6836, 2003.
9. Blumcke I, Suter B, Behle K, Kuhn R, Schramm J, Elger CE, and Wiestler OD. Loss of hilar mossy cells in Ammon's horn sclerosis. Epilepsia 41(Suppl 6): S174-S180, 2000.
10. Borges K, Gearing M, McDermott DL, Smith AB, Almonte AG, Wainer BH and Dingledine R. Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp Neurol 182: 21-34, 2003.
11. Bradley SR, Levey AI, Hersch SM, and Conn PJ. Immunocytochemical localization of group III metabotropic glutamate receptors in the hippocampus with subtype-specific antibodies. J Neurosci 16: 2044-2056, 1996.
12. Buckmaster PS and Jongen-Relo AL. Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J Neurosci 19: 9519-9529, 1999.
13. Burke JP and Hablitz JJ. Metabotropic glutamate receptor activation decreases epileptiform activity in rat neocortex. Neurosci Lett 174: 29-33, 1994.
14. Conn PJ and Pin JP. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37: 205-237, 1997.
15. Dietrich D, Kral T, Clusmann H, Friedl M, and Schramm J. Reduced function of L-AP4-sensitive metabotropic glutamate receptors in human epileptic sclerotic hippocampus. Eur J Neurosci 11: 1109-1113, 1999.
16. Dietrich D, Kral T, Clusmann H, Friedl M, and Schramm J. Presynaptic group II metabotropic glutamate receptors reduce stimulated and spontaneous transmitter release in human dentate gyrus. Neuropharmacology 42: 297-305, 2002.
17. Doherty J and Dingledine R. Reduced excitatory drive onto interneurons in the dentate gyrus after status epilepticus. J Neurosci 21: 2048-2057, 2001.
18. Duvoisin RM, Zhang C, and Ramonell K. A novel metabotropic glutamate receptor expressed in the retina and olfactory bulb. J Neurosci 15: 3075-3083, 1995.
19. Folbergrova J, Haugvicova R, and Mares P. 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, 2001.
20. Folbergrova J, Haugvicova R, and Mares P. Seizures induced by homocysteic acid in immature rats are prevented by group III metabotropic glutamate receptoragonist (R,S)-4-phosphonophenylglycine. Exp Neurol 180: 46-54, 2003.
21. Gasparini F, Bruno V, Battaglia G, Lukic S, Leonhardt T, Inderbitzin W, Laurie D, Sommer B, Varney MA, Hess SD, Johnson EC, Kuhn R, Urwyler S, Sauer D, Portet C, Schmutz M, Nicoletti F, and Flor PJ. (R,S)-4-phosphonophenylglycine, a potent and selective group III metabotropic glutamate receptor agonist, is anticonvulsive and neuroprotective in vivo. J Pharmacol Exp Ther 289: 1678-1687, 1999.
22. Gereau RWt and Conn PJ. Roles of specific metabotropic glutamate receptor subtypes in regulation of hippocampal CA1 pyramidal cell excitability. J Neurophysiol 74: 122-129, 1995.
23. Gutierrez R. Activity-dependent expression of simultaneous glutamatergic and GABAergic neurotransmission from the mossy fibers in vitro. J Neurophysiol 87: 2562-2570, 2002.
24. Kew JN, Ducarre JM, Pflimlin MC, Mutel V, and Kemp JA. 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, 2001.
25. Kew JN, Pflimlin MC, Kemp JA, and Mutel V. 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, 2002.
26. Klapstein GJ, Meldrum BS, and Mody I. Decreased sensitivity to Group III mGluR agonists in the lateral perforant path following kindling. Neuropharmacology 38: 927-933, 1999.
27. Kobayashi M, Wen X, and Buckmaster PS. Reduced inhibition and increased output of layer II neurons in the medial entorhinal cortex in a model of temporal lobe epilepsy. J Neurosci 23: 8471-8479, 2003.
28. Kral T, Erdmann E, Sochivko D, Clusmann H, Schramm J, and Dietrich D. Down-regulation of mGluR8 in pilocarpine epileptic rats. Synapse 47: 278-284, 2003.
29. Laezza F, Doherty JJ, and Dingledine R. Long-term depression in hippocampal interneurons: joint requirement for pre- and postsynaptic events. Science 285: 1411-1414, 1999.
30. Linden AM, Johnson BG, Peters SC, Shannon HE, Tian M, Wang Y, Yu JL, Koster A, Baez M, and Schoepp DD. Increased anxiety-related behavior in mice deficient for metabotropic glutamate 8 (mGlu8) receptor. Neuropharmacology 43: 251-259, 2002.
31. Lovinger DM and McCool BA. Metabotropic glutamate receptor-mediated presynaptic depression at corticostriatal synapses involves mGLuR2 or 3. J Neurophysiol 73: 1076-1083, 1995.
32. Macek TA, Winder DG, Gereau RWt, Ladd CO, and Conn PJ. Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J Neurophysiol 76: 3798-3806, 1996.
33. McNaughton BL. Evidence for two physiologically distinct perforant pathways to the fascia dentata. Brain Res 199: 1-19, 1980.
34. Moldrich RX, Chapman AG, De Sarro G, and Meldrum BS. Glutamate metabotropic receptors as targets for drug therapy in epilepsy. Eur J Pharmacol 476: 3-16, 2003.
35. Neugebauer V, Zinebi F, Russell R, Gallagher JP, and Shinnick-Gallagher P. Cocaine and kindling alter the sensitivity of group II and III metabotropic glutamate receptors in the central amygdala. J Neurophysiol 84: 759-770, 2000.
36. Nomura A, Shigemoto R, Nakamura Y, Okamoto N, Mizuno N, and Nakanishi S. Developmentally regulated postsynaptic localization of a metabotropic glutamate receptor in rat rod bipolar cells. Cell 77: 361-369, 1994.
37. Sansig G, Bushell TJ, Clarke VR, Rozov A, Burnashev N, Portet C, Gasparini F, Schmutz M, Klebs K, Shigemoto R, Flor PJ, Kuhn R, Knoepfel T, Schroeder M, Hampson DR, Collett VJ, Zhang C, Duvoisin RM, Collingridge GL, and van Der Putten H. Increased seizure susceptibility in mice lacking metabotropic glutamate receptor 7. J Neurosci 21: 8734-8745, 2001.
38. Schwartzkroin PA. Mechanisms of brain plasticity: from normal brain function to pathology. Int Rev Neurobiol 45: 1-15, 2001.
39. Semyanov A and Kullmann DM. Modulation of GABAergic signaling among interneurons by metabotropic glutamate receptors. Neuron 25: 663-672, 2000.
40. Sheng M and Kim MJ. Postsynaptic signaling and plasticity mechanisms. Science 298: 776-780, 2002.
41. Shibley H and Smith BN. Pilocarpine-induced status epilepticus results in mossy fiber sprouting and spontaneous seizures in C57BL/6 and CD-1 mice. Epilepsy Res 49: 109-120, 2002.
42. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S, and Mizuno N. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17: 7503-7522, 1997.
43. Shigemoto R, Kulik A, Roberts JD, Ohishi H, Nusser Z, Kaneko T, and Somogyi P. Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381: 523-525, 1996.
44. Snead OC III, Banerjee PK, Burnham M, and Hampson D. Modulation of absence seizures by the GABA(A) receptor: a critical rolefor metabotropic glutamate receptor 4 (mGluR4). J Neurosci 20: 6218-6224, 2000.
45. Stringer JL, Williamson JM, and Lothman EW. Induction of paroxysmal discharges in the dentate gyrus: frequency dependence and relationship to afterdischarge production. J Neurophysiol 62: 126-135, 1989.
46. Tang FR, Lee WL, Yang J, Sim MK, and Ling EA. Metabotropic glutamate receptor 8 in the rat hippocampus after pilocarpine induced status epilepticus. Neurosci Lett 300: 137-140, 2001.
47. Thomas NK, Wright RA, Howson PA, Kingston AE, Schoepp DD, and Jane DE. (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: 311-318, 2001.
48. Williams PA, Wuarin JP, Dou P, Ferraro DJ and Dudek FE. Reassessment of the effects of cycloheximide on mossy fiber sprouting and epileptogenesis in the pilocarpine model of temporal lobe epilepsy. J Neurophysiol 88: 2075-2087, 2002.
49. Witter MP, Naber PA, van Haeften T, Machielsen WC, Rombouts SA, Barkhof F, Scheltens P, and Lopes da Silva FH. Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10: 398-410, 2000.
50. Wong RK, Bianchi R, Taylor GW, and Merlin LR. Role of metabotropic glutamate receptors in epilepsy. Adv Neurol 79: 685-698, 1999.
51. Wu S, Wright RA, Rockey PK, Burgett SG, Arnold JS, Rosteck PR Jr, Johnson BG, Schoepp DD, and Belagaje RM. Group III human metabotropic glutamate receptors 4, 7 and 8: molecular cloning, functional expression, and comparison of pharmacological properties in RGT cells. Brain Res Mol Brain Res 53: 88-97, 1998.
52. Yip PK, Meldrum BS, and Rattray M. Elevated levels of group-III metabotropic glutamate receptors in the inferior colliculus of genetically epilepsyprone rats following intracollicular administration of L-serine-O-phosphate. J Neurochem 78: 13-23, 2001.
53. Zhai J, Tian MT, Wang Y, Yu JL, Koster A, Baez M, and Nisenbaum ES. Modulation of lateral perforant path excitatory responses by metabotropic glutamate 8 (mGlu8) receptors. Neuropharmacology 43: 223-230, 2002.