Role of Glutamate Autoreceptors at Hippocampal Mossy Fiber Synapses

Neuron

Volumn 60, Issue 6, 2008, Pages 1082-1094

  Kwon, Hyung Bae ^a   Castillo, Pablo E ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

CELLBIO; MOLNEURO

Indexed keywords

AUTORECEPTOR; GLUTAMATE RECEPTOR; KAINIC ACID RECEPTOR; METABOTROPIC RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; AUTORECEPTORS; BIOPHYSICS; CALCIUM; CYCLOPROPANES; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLYCINE; HIPPOCAMPUS; KAINIC ACID; MICE; MICE, KNOCKOUT; MOSSY FIBERS, HIPPOCAMPAL; NEURONS; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; RECEPTORS, GLUTAMATE; SODIUM CHANNEL BLOCKERS; SYNAPSES; TETRODOTOXIN;

EID: 57649185003     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2008.10.045     Document Type: Article

References (64)

1. Alle H., and Geiger J.R. Combined analog and action potential coding in hippocampal mossy fibers. Science 311 (2006) 1290-1293
2. Bergles D.E., and Jahr C.E. Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J. Neurosci. 18 (1998) 7709-7716
3. Bortolotto Z.A., Clarke V.R., Delany C.M., Parry M.C., Smolders I., Vignes M., Ho K.H., Miu P., Brinton B.T., Fantaske R., et al. Kainate receptors are involved in synaptic plasticity. Nature 402 (1999) 297-301
4. Bortolotto Z.A., Lauri S., Isaac J.T., and Collingridge G.L. Kainate receptors and the induction of mossy fibre long-term potentiation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 (2003) 657-666
5. Breustedt J., and Schmitz D. Assessing the role of GLUK5 and GLUK6 at hippocampal mossy fiber synapses. J. Neurosci. 24 (2004) 10093-10098
6. Bureau I., Bischoff S., Heinemann S.F., and Mulle C. Kainate receptor-mediated responses in the CA1 field of wild-type and GluR6-deficient mice. J. Neurosci. 19 (1999) 653-663
7. Carter A.G., Vogt K.E., Foster K.A., and Regehr W.G. Assessing the role of calcium-induced calcium release in short-term presynaptic plasticity at excitatory central synapses. J. Neurosci. 22 (2002) 21-28
8. Castillo P.E., Malenka R.C., and Nicoll R.A. Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388 (1997) 182-186
9. Castillo P.E., Schoch S., Schmitz F., Sudhof T.C., and Malenka R.C. RIM1α is required for presynaptic long-term potentiation. Nature 415 (2002) 327-330
10. Claiborne B.J., Xiang Z., and Brown T.H. Hippocampal circuitry complicates analysis of long-term potentiation in mossy fiber synapses. Hippocampus 3 (1993) 115-121
11. Contractor A., Swanson G.T., Sailer A., O'Gorman S., and Heinemann S.F. Identification of the kainate receptor subunits underlying modulation of excitatory synaptic transmission in the CA3 region of the hippocampus. J. Neurosci. 20 (2000) 8269-8278
12. Contractor A., Swanson G., and Heinemann S.F. Kainate receptors are involved in short- and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 29 (2001) 209-216
13. -/- mice. J. Neurosci. 23 (2003) 422-429
14. Cossart R., Esclapez M., Hirsch J.C., Bernard C., and Ben-Ari Y. GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat. Neurosci. 1 (1998) 470-478
15. Cotman C.W., Flatman J.A., Ganong A.H., and Perkins M.N. Effects of excitatory amino acid antagonists on evoked and spontaneous excitatory potentials in guinea-pig hippocampus. J. Physiol. 378 (1986) 403-415
16. Darstein M., Petralia R.S., Swanson G.T., Wenthold R.J., and Heinemann S.F. Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J. Neurosci. 23 (2003) 8013-8019
17. Engelman H.S., and MacDermott A.B. Presynaptic ionotropic receptors and control of transmitter release. Nat. Rev. Neurosci. 5 (2004) 135-145
18. Frerking M., Malenka R.C., and Nicoll R.A. Synaptic activation of kainate receptors on hippocampal interneurons. Nat. Neurosci. 1 (1998) 479-486
19. Henze D.A., Urban N.N., and Barrionuevo G. The multifarious hippocampal mossy fiber pathway: a review. Neuroscience 98 (2000) 407-427
20. Henze D.A., Wittner L., and Buzsaki G. Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat. Neurosci. 5 (2002) 790-795
21. Jung M.W., and McNaughton B.L. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3 (1993) 165-182
22. Kamiya H., and Ozawa S. Dual mechanism for presynaptic modulation by axonal metabotropic glutamate receptor at the mouse mossy fibre-CA3 synapse. J. Physiol. 518 (1999) 497-506
23. Kamiya H., and Ozawa S. Kainate receptor-mediated presynaptic inhibition at the mouse hippocampal mossy fibre synapse. J. Physiol. 523 (2000) 653-665
24. Kamiya H., Shinozaki H., and Yamamoto C. Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. J. Physiol. 493 (1996) 447-455
25. 2+ influx at the hippocampal mossy fiber synapses. J. Neurosci. 22 (2002) 9237-9243
26. Kingston A.E., Ornstein P.L., Wright R.A., Johnson B.G., Mayne N.G., Burnett J.P., Belagaje R., Wu S., and Schoepp D.D. LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors. Neuropharmacology 37 (1998) 1-12
27. Kobayashi K., Manabe T., and Takahashi T. Presynaptic long-term depression at the hippocampal mossy fiber-CA3 synapse. Science 273 (1996) 648-650
28. Langdon R.B., Johnson J.W., and Barrionuevo G. Asynchrony of mossy fibre inputs and excitatory postsynaptic currents in rat hippocampus. J. Physiol. 472 (1993) 157-176
29. Lauri S.E., Bortolotto Z.A., Bleakman D., Ornstein P.L., Lodge D., Isaac J.T., and Collingridge G.L. A critical role of a facilitatory presynaptic kainate receptor in mossy fiber LTP. Neuron 32 (2001) 697-709
30. 2+ stores in kainate receptor-dependent synaptic facilitation and LTP at mossy fiber synapses in the hippocampus. Neuron 39 (2003) 327-341
31. Lawrence J.J., and McBain C.J. Interneuron diversity series: containing the detonation-feedforward inhibition in the CA3 hippocampus. Trends Neurosci. 26 (2003) 631-640
32. Lerma J. Roles and rules of kainate receptors in synaptic transmission. Nat. Rev. Neurosci. 4 (2003) 481-495
33. Lester R.A., Quarum M.L., Parker J.D., Weber E., and Jahr C.E. Interaction of 6-cyano-7-nitroquinoxaline-2,3-dione with the N-methyl-D-aspartate receptor-associated glycine binding site. Mol. Pharmacol. 35 (1989) 565-570
34. Manzoni O.J., Castillo P.E., and Nicoll R.A. Pharmacology of metabotropic glutamate receptors at the mossy fiber synapses of the guinea pig hippocampus. Neuropharmacology 34 (1995) 965-971
35. Melyan Z., Wheal H.V., and Lancaster B. Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34 (2002) 107-114
36. Miller R.J. Presynaptic receptors. Annu. Rev. Pharmacol. Toxicol. 38 (1998) 201-227
37. Min M.Y., Rusakov D.A., and Kullmann D.M. Activation of AMPA, kainate, and metabotropic receptors at hippocampal mossy fiber synapses: role of glutamate diffusion. Neuron 21 (1998) 561-570
38. More J.C., Nistico R., Dolman N.P., Clarke V.R., Alt A.J., Ogden A.M., Buelens F.P., Troop H.M., Kelland E.E., Pilato F., et al. Characterisation of UBP296: a novel, potent and selective kainate receptor antagonist. Neuropharmacology 47 (2004) 46-64
39. Mori M., Abegg M.H., Gahwiler B.H., and Gerber U. A frequency-dependent switch from inhibition to excitation in a hippocampal unitary circuit. Nature 431 (2004) 453-456
40. Mulle C., Sailer A., Perez-Otano I., Dickinson-Anson H., Castillo P.E., Bureau I., Maron C., Gage F.H., Mann J.R., Bettler B., and Heinemann S.F. Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392 (1998) 601-605
41. Nicoll R.A., and Schmitz D. Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci. 6 (2005) 863-876
42. Pelkey K.A., Lavezzari G., Racca C., Roche K.W., and McBain C.J. mGluR7 is a metaplastic switch controlling bidirectional plasticity of feedforward inhibition. Neuron 46 (2005) 89-102
43. Pelkey K.A., Topolnik L., Lacaille J.C., and McBain C.J. Compartmentalized Ca(2+) channel regulation at divergent mossy-fiber release sites underlies target cell-dependent plasticity. Neuron 52 (2006) 497-510
44. Perrais D., Pinheiro P.S., Jane D.E., and Mulle C. Antagonism of recombinant and native GluK3-containing kainate receptors. Neuropharmacology (2008) in press
45. Pinheiro P.S., and Mulle C. Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat. Rev. Neurosci. 9 (2008) 423-436
46. Pinheiro P.S., Perrais D., Coussen F., Barhanin J., Bettler B., Mann J.R., Malva J.O., Heinemann S.F., and Mulle C. GluR7 is an essential subunit of presynaptic kainate autoreceptors at hippocampal mossy fiber synapses. Proc. Natl. Acad. Sci. USA 104 (2007) 12181-12186
47. Regehr W.G., Delaney K.R., and Tank D.W. The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J. Neurosci. 14 (1994) 523-537
48. Rodriguez-Moreno A., and Sihra T.S. Presynaptic kainate receptor facilitation of glutamate release involves protein kinase A in the rat hippocampus. J. Physiol. 557 (2004) 733-745
49. Salin P.A., Scanziani M., Malenka R.C., and Nicoll R.A. Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc. Natl. Acad. Sci. USA 93 (1996) 13304-13309
50. Scanziani M., Salin P.A., Vogt K.E., Malenka R.C., and Nicoll R.A. Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385 (1997) 630-634
51. Schmitz D., Frerking M., and Nicoll R.A. Synaptic activation of presynaptic kainate receptors on hippocampal mossy fiber synapses. Neuron 27 (2000) 327-338
52. Schmitz D., Mellor J., and Nicoll R.A. Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291 (2001) 1972-1976
53. Schmitz D., Mellor J., Breustedt J., and Nicoll R.A. Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation. Nat. Neurosci. 6 (2003) 1058-1063
54. Shigemoto R., Kinoshita A., Wada E., Nomura S., Ohishi H., Takada M., Flor P.J., Neki A., Abe T., Nakanishi S., and Mizuno N. Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J. Neurosci. 17 (1997) 7503-7522
55. Tong G., Shepherd D., and Jahr C.E. Synaptic desensitization of NMDA receptors by calcineurin. Science 267 (1995) 1510-1512
56. Toth K., Suares G., Lawrence J.J., Philips-Tansey E., and McBain C.J. Differential mechanisms of transmission at three types of mossy fiber synapse. J. Neurosci. 20 (2000) 8279-8289
57. Vignes M., and Collingridge G.L. The synaptic activation of kainate receptors. Nature 388 (1997) 179-182
58. Vogt K.E., and Nicoll R.A. Glutamate and γ-aminobutyric acid mediate a heterosynaptic depression at mossy fiber synapses in the hippocampus. Proc. Natl. Acad. Sci. USA 96 (1999) 1118-1122
59. Weisskopf M.G., and Nicoll R.A. Presynaptic changes during mossy fibre LTP revealed by NMDA receptor-mediated synaptic responses. Nature 376 (1995) 256-259
60. Wigstrom H., and Gustafsson B. Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 301 (1983) 603-604
61. Wisden W., and Seeburg P.H. A complex mosaic of high-affinity kainate receptors in rat brain. J. Neurosci. 13 (1993) 3582-3598
62. Wittner L., Henze D.A., Zaborszky L., and Buzsaki G. Three-dimensional reconstruction of the axon arbor of a CA3 pyramidal cell recorded and filled in vivo. Brain Struct. Funct. 212 (2007) 75-83
63. Yamamoto C., Sawada S., and Takada S. Suppressing action of 2-amino-4-phosphonobutyric acid on mossy fiber-induced excitation in the guinea pig hippocampus. Exp. Brain Res. 51 (1983) 128-134
64. Zucker R.S., and Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64 (2002) 355-405