Expression and function of kainate receptors in the rat olfactory bulb

Synapse

Volumn 61, Issue 5, 2007, Pages 320-334

  Davila, Nestor G ^a   Houpt, Thomas A ^a   Trombley, Paul Q ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Confocal microscopy; Electrophysiology; Glutamate; In situ hybridization; RT PCR

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SYNAPSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTERNEURON; MEMBRANE DEPOLARIZATION; NEUROTRANSMISSION; NEWBORN; NONHUMAN; OLFACTORY BULB; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR DENSITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CELLS, CULTURED; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MEMBRANE POTENTIALS; MICROSCOPY, CONFOCAL; NEURONS; OLFACTORY BULB; OLFACTORY PATHWAYS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33947131713     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20376     Document Type: Article

References (79)

1. Agrawal SG, Evans RH. 1986. The primary afferent depolarizing action of kainate in the rat. Br J Pharmacol 87:345-355.
2. Ali AB. 2003. Involvement of post-synaptic kainate receptors during synaptic transmission between unitary connections in rat neocortex. Eur J Neurosci 17:2344-2350.
3. Aroniadou-Anderjaska V, Ennis M, Shipley MT. 1999. Current-source density analysis in the rat olfactory bulb: Laminar distribution of kainate/AMPA- and NMDA-receptor-mediated currents. J Neurophysiol 81:15-28.
4. Bailey A, Kelland EE, Thomas A, Biggs J, Crawford D, Kitchen I, Toms NJ. 2001. Regional mapping of low-affinity kainate receptors in mouse brain using [(3)H](2S,4R)-4-methylglutamate autoradiography. Eur J Pharmacol 431:305-310.
5. Bailey MS, Shipley MT. 1993. Astrocyte subtypes in the rat olfactory bulb: Morphological heterogeneity and differential laminar distribution. J Comp Neurol 328:501-526.
6. Berkowicz DA, Trombley PQ, Shepherd GM. 1994. Evidence for glutamate as the olfactory receptor cell neurotransmitter. J Neurophysiol 71:2557-2561.
7. Bowie D, Garcia EP, Marshall J, Traynelis SF, Lange GD. 2003. Allosteric regulation and spatial distribution of kainate receptors bound to ancillary proteins. J Physiol 547 (Part 2):373-385.
8. Carlson GC, Slawecki ML, Lancaster E, Keller A. 1997. Distribution and activation of intracellular Ca2+ stores in cultured olfactory bulb neurons. J Neurophysiol 78:2176-2185.
9. Carlson GC, Shipley MT, Keller A. 2000. Long-lasting depolarizations in mitral cells of the rat olfactory bulb. J Neurosci 20:2011-2021.
10. Castillo PE, Malenka RC, Nicoll RA. 1997. Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388:182-186.
11. Chittajallu R, Vignes M, Dev KK, Barnes JM, Collingridge GL, Henley JM. 1996. Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 379:78-81.
12. Chiu K, Greer CA. 1996. Immunocytochemical analyses of astrocyte development in the olfactory bulb. Brain Res Dev Brain Res 95:28-37.
13. Christie JM, Westbrook GL. 2006. Lateral excitation within the olfactory bulb. J Neurosci 26:2269-2277.
14. Christie JM, Bark C, Hormuzdi SG, Helbig I, Monyer H, Westbrook GL. 2005. Connexin36 mediates spike synchrony in olfactory bulb glomeruli. Neuron 46:761-772.
15. Clarke VR, Collingridge GL. 2002. Characterisation of the effects of ATPA, a GLU(K5) receptor selective agonist, on excitatory synaptic transmission in area CA1 of rat hippocampal slices. Neuropharmacology 42:889-902.
16. Collingridge GL, Kehl SJ, McLennan H. 1983. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 334:33-46.
17. Constanti A, Connor JD, Galvan M, Nistri A. 1980. Intracellularly- recorded effects of glutamate and aspartate on neurones in the guinea-pig olfactory cortex slice. Brain Res 195:403-420.
18. Contractor A, Swanson GT, Sailer A, O'Gorman S, Heinemann SF. 2000. Identification of the kainate receptor subunits underlying modulation of excitatory synaptic transmission in the CA3 region of the hippocampus. J Neurosci 20:8269-8278.
19. Contractor A, Sailer AW, Darstein M, Maron C, Xu J, Swanson GT, Heinemann SF. 2003. Loss of kainate receptor-mediated heterosynaptic facilitation of mossy-fiber synapses in KA2-/- mice. J Neurosci 23:422-429.
20. Cossart R, Esclapez M, Hirsch JC, Bernard C, Ben-Ari Y. 1998. GluR5 kainate receptor activation in interneurons increases tonic inhibition of pyramidal cells. Nat Neurosci 1:470-478.
21. Cossart R, Epsztein J, Tyzio R, Becq H, Hirsch J, Ben-Ari Y, Crepel V. 2002. Quantal release of glutamate generates pure kainate and mixed AMPA/kainate EPSCs in hippocampal neurons. Neuron 35:147-159.
22. Cui C, Mayer ML. 1999. Heteromeric kainate receptors formed by the coassembly of GluR5, GluR6, and GluR7. J Neurosci 19:8281-8291.
23. Dai WM, Christensen KV, Egebjerg J, Ebert B, Lambert JD. 2002. Correlation of the expression of kainate receptor subtypes to responses evoked in cultured cortical and spinal cord neurones. Brain Res 926:94-107.
24. Davila NG, Blakemore LJ, Trombley PQ. 2003. Dopamine modulates synaptic transmission between rat olfactory bulb neurons in culture. J Neurophysiol 90:395-404.
25. Delaney AJ, Jahr CE. 2002. Kainate receptors differentially regulate release at two parallel fiber synapses. Neuron 36:475-482.
26. Edwards JG, Michel WC. 2003. Pharmacological characterization of ionotropic glutamate receptors in the zebrafish olfactory bulb. Neuroscience 122:1037-1047.
27. Ennis M, Zimmer LA, Shipley MT. 1996. Olfactory nerve stimulation activates rat mitral cells via NMDA and non-NMDA receptors in vitro. Neuroreport 7:989-992.
28. Ennis M, Linster C, Aroniadou-Anderjaska V, Ciombor K, Shipley MT. 1998. Glutamate and synaptic plasticity at mammalian primary olfactory synapses. Ann N Y Acad Sci 855:457-466.
29. Gallyas F, Ball SM, Molnar E. 2003. Assembly and cell surface expression of KA-2 subunit-containing kainate receptors. J Neurochem 86:1414-1427.
30. Garcia EP, Mehta S, Blair LA, Wells DG, Shang J, Fukushima T, Fallon JR, Garner CC, Marshall J. 1998. SAP90 binds and clusters kainate receptors causing incomplete desensitization. Neuron 21:727-739.
31. Halasz N, Shepherd GM. 1983. Neurochemistry of the vertebrate olfactory bulb. Neuroscience 10:579-619.
32. Herb A, Burnashev N, Werner P, Sakmann B, Wisden W, Seeburg PH, 1992. The KA-2 subunit of excitatory amino acid receptors shows widespread expression in brain and forms ion channels with distantly related subunits. Neuron 8:775-785.
33. Hirbec H, Francis JC, Lauri SE, Braithwaite SP, Coussen F, Mulle C, Dev KK, Coutinho V, Meyer G, Isaac JT, Collingridge GL, Henley JM, Couthino V. 2003. Rapid and differential regulation of AMPA and kainate receptors at hippocampal mossy fibre synapses by PICK1 and GRIP. Neuron 37:625-638.
34. Hwang SJ, Pagliardini S, Rustioni A, Valtschanoff JG. 2001. Presynaptic kainate receptors in primary afferents to the superficial laminae of the rat spinal cord. J Comp Neurol 436:275-289.
35. Jiang L, Xu J, Nedergaard M, Kang J. 2001. A kainate receptor increases the efficacy of GABAergic synapses. Neuron 30:503-513.
36. Kamiya H, Ozawa S. 2000. Kainate receptor-mediated presynaptic inhibition at the mouse hippocampal mossy fibre synapse. J Physiol 523 (Part 3):653-665.
37. Kasowski HJ, Kim H, Greer CA. 1999. Compartmental organization of the olfactory bulb glomerulus. J Comp Neurol 407:261-274.
38. Kerchner GA, Wilding TJ, Li P, Zhuo M, Huettner JE. 2001. Presynaptic kainate receptors regulate spinal sensory transmission. J Neurosci 21:59-66.
39. Kerchner GA, Wilding TJ, Huettner JE, Zhuo M. 2002. Kainate receptor subunits underlying presynaptic regulation of transmitter release in the dorsal horn. J Neurosci 22:8010-8017.
40. Kidd FL, Isaac JT. 1999. Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature 400:569-573.
41. Kidd FL, Isaac JT. 2001. Kinetics and activation of postsynaptic kainate receptors at thalamocortical synapses: Role of glutamate clearance. J Neurophysiol 86:1139-1148.
42. Kieval JZ, Hubert GW, Charara A, Pare JF, Smith Y. 2001. Subcellular and subsynaptic localization of presynaptic and postsynaptic kainate receptor subunits in the monkey striatum. J Neurosci 21:8746-8757.
43. Lauri SE, Bortolotto ZA, Bleakman D, Ornstein PL, Lodge D, Isaac JT, Collingridge GL. 2001a. A critical role of a facilitatory presynaptic kainate receptor in mossy fiber LTP. Neuron 32:697-709.
44. Lauri SE, Delany C, Clarke VR, Bortolotto ZA, Ornstein PL, J TRI, Collingridge GL. 2001b. Synaptic activation of a presynaptic kainate receptor facilitates AMPA receptor-mediated synaptic transmission at hippocampal mossy fibre synapses. Neuropharmacology 41:907-915.
45. Lerma J, Paternain AV, Naranjo JR, Mellstrom B. 1993. Functional kainate-selective glutamate receptors in cultured hippocampal neurons. Proc Natl Acad Sci USA 90:11688-11692.
46. Lerma J, Paternain AV, Rodriguez-Moreno A, Lopez-Garcia JC. 2001. Molecular physiology of kainate receptors. Physiol Rev 81: 971-998.
47. Li H, Chen A, Xing G, Wei ML, Rogawski MA. 2001. Kainate receptor-mediated heterosynaptic facilitation in the amygdala. Nat Neurosci 4:612-620.
48. Lowe G. 2003. Flash photolysis reveals a diversity of ionotropic glutamate receptors on the mitral cell somatodendritic membrane. J Neurophysiol 90:1737-1746.
49. Mehta S, Wu H, Garner CC, Marshall J. 2001. Molecular mechanisms regulating the differential association of kainate receptor subunits with SAP90/PSD-95 and SAP97. J Biol Chem 276: 16092-16099.
50. Melyan Z, Wheal HV, Lancaster B. 2002. Metabotropic-mediated kainate receptor regulation of IsAHP and excitability in pyramidal cells. Neuron 34:107-114.
51. Miller LP, Johnson AE, Gelhard RE, Insel TR. 1990. The ontogeny of excitatory amino acid receptors in the rat forebrain-II. Kainic acid receptors. Neuroscience 35:45-51.
52. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn M, Edmondson J, Axel R. 1996. Visualizing an olfactory sensory map. Cell 87:675-686.
53. Monaghan DT, Cotman CW. 1982. The distribution of [3H]kainic acid binding sites in rat CNS as determined by autoradiography. Brain Res 252:91-100.
54. Monaghan DT, Holets VR, Toy DW, Cotman CW. 1983. Anatomical distributions of four pharmacologically distinct 3H-L-glutamate binding sites. Nature 306:176-179.
55. Monaghan DT, Yao D, Cotman CW. 1985. L-[3H]Glutamate binds to kainate-, NMDA- and AMPA-sensitive binding sites: An autoradiographic analysis. Brain Res 340:378-383.
56. Montague AA, Greer CA. 1999. Differential distribution of ionotropic glutamate receptor subunits in the rat olfactory bulb. J Comp Neurol 405:233-246.
57. Nadi NS, Hirsch JD, Margolis FL. 1980. Laminar distribution of putative neurotransmitter amino acids and ligand binding sites in the dog olfactory bulb. J Neurochem 34:138-146.
58. Paarmann I, Frermann D, Keller BU, Hollmann M. 2000. Expression of 15 glutamate receptor subunits and various splice variants in tissue slices and single neurons of brainstem nuclei and potential functional implications. J Neurochem 74:1335-1345.
59. Paternain AV, Herrera MT, Nieto MA, Lerma J. 2000. GluR5 and GluR6 kainate receptor subunits coexist in hippocampal neurons and coassemble to form functional receptors. J Neurosci 20:196-205.
60. Petralia RS, Wang YX, Wenthold RJ. 1994. Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies. J Comp Neurol 349:85-110.
61. Ren Z, Riley NJ, Garcia EP, Sanders JM, Swanson GT, Marshall J. 2003. Multiple trafficking signals regulate kainate receptor KA2 subunit surface expression. J Neurosci 23:6608-6616.
62. Robinson JH, Deadwyler SA. 1981. Kainic acid produces depolarization of CA3 pyramidal cells in the vitro hippocampal slice. Brain Res 221:117-127.
63. Rodriguez-Moreno A, Lopez-Garcia JC, Lerma J. 2000. Two populations of kainate receptors with separate signaling mechanisms in hippocampal interneurons. Proc Natl Acad Sci USA 97:1293-1298.
64. Rozas JL, Paternain AV, Lerma J. 2003. Noncanonical signaling by ionotropic kainate receptors. Neuron 39:543-553.
65. Salin PA, Lledo PM, Vincent JD, Charpak S. 2001. Dendritic glutamate autoreceptors modulate signal processing in rat mitral cells. J Neurophysiol 85:1275-1282.
66. Sassoe-Pognetto M, Utvik JK, Camoletto P, Watanabe M, Stephenson FA, Bredt DS, Ottersen OP. 2003. Organization of postsynaptic density proteins and glutamate receptors in axodendritic and dendrodendritic synapses of the rat olfactory bulb. J Comp Neurol 463:237-248.
67. Schmitz D, Mellor J, Nicoll RA. 2001. Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291:1972-1976.
68. Schmitz D, Mellor J, Breustedt J, Nicoll RA. 2003. Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation. Nat Neurosci 6:1058-1063.
69. Schoppa NE, Westbrook GL. 2002. AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli. Nat Neurosci 5:1194-1202.
70. Stone LM, Browning MD, Finger TE. 1994. Differential distribution of the synapsins in the rat olfactory bulb. J Neurosci 14:301-309.
71. Thukral V, Chikaraishi D, Hunter DD, Wang JK. 1997. Expression of non-N-methyl-D-aspartate glutamate receptor subunits in the olfactory epithelium. Neuroscience 79:411-424.
72. Trombley PQ, Blakemore LJ. 1999. Mammalian olfactory bulb neurons. In:Haynes LW, editor. The neuron in tissue culture. West Sussex, UK: Wiley. p 585-592.
73. Trombley PQ, Westbrook GL. 1990. Excitatory synaptic transmission in cultures of rat olfactory bulb. J Neurophysiol 64:598-606.
74. Unnerstall JR, Wamsley JK, 1983. Autoradiographic localization of high-affinity [3H]kainic acid binding sites in the rat forebrain. Eur J Pharmacol 86:361-371.
75. Urban NN, Sakmann B. 2002. Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. J Physiol 542 (Part 2):355-367.
76. van den Pol A, Hermans-Borgmeyer I, Hofer M, Ghosh P, Heinemann S. 1994. Ionotropic glutamate-receptor gene expression in hypothalamus: Localization of AMPA, kainate, and NMDA receptor RNA with in situ hybridization. J Comp Neurol 343:428-444.
77. Vignes M, Collingridge GL. 1997. The synaptic activation of kainate receptors. Nature 388:179-182.
78. Westbrook GL, Lothman EW. 1983. Cellular and synaptic basis of kainic acid-induced hippocampal epileptiform activity. Brain Res 273:97-109.
79. Zhou LM, Gu ZQ, Costa AM, Yamada KA, Mansson PE, Giordano T, Skolnick P, Jones KA. 1997. (2S,4R)-4-methylglutamic acid (SYM 2081): A selective, high-affinity ligand for kainate receptors. J Pharmacol Exp Ther 280:422-427.