Heteromeric kainate receptors formed by the coassembly of GluR5, GluR6, and GluR7

Journal of Neuroscience

Volumn 19, Issue 19, 1999, Pages 8281-8291

  Cui, Changhai ^a   Mayer, Mark L ^a,b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

ATPA; Coassembly; Glutamate receptors; Heteromeric glutamate receptors; Iodowillardiine; Kainate receptors; Polyamines

Indexed keywords

AMPA RECEPTOR AGONIST; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR AGONIST; KAINIC ACID RECEPTOR; RECEPTOR SUBTYPE; RECOMBINANT PROTEIN;

ARTICLE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; MULTIGENE FAMILY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION;

EID: 0033216120     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-19-08281.1999     Document Type: Article

References (53)

1. Bahn S, Volk B, Wisden W (1994) Kainate receptor gene expression in the developing brain. J Neurosci 14:5525-5547.
2. Bähring R, Bowie D, Benveniste M, Mayer ML (1997) Permeation and block of rat GluR6 glutamate receptor channels by internal and external polyamines. J Physiol (Lond) 502:575-589.
3. Belcher SM, Howe JR (1997) Characterization of RNA editing of the glutamate-receptor subunits GluR5 and GluR6 in granule cells during cerebellar development. Brain Res Mol Brain Res 52:130-138.
4. Bettler B, Boulter J, Hermans-Borgmeyer I, O'Shea-Greenfield A, Deneris ES, Moll C, Borgmeyer U, Hollmann M, Heinemann S (1990) Cloning of a novel glutamate receptor subunit, GluR5: expression in the nervous system during development. Neuron 5:583-595.
5. Bischoff S, Barhanin J, Bettler B, Mulle C, Heinemann S (1997) Spatial distribution of kainate receptor subunit mRNA in the mouse basal ganglia and ventral mesencephalon. J Comp Neurol 379:541-562.
6. Bowie D, Mayer ML (1995) Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 15:453-462.
7. Brose N, Huntley GW, Stern-Bach Y, Sharma G, Morrison JH, Heinemann SF (1994) Differential assembly of coexpressed glutamate receptor subunits in neurons of rat cerebral cortex. J Biol Chem 269:16780-16784.
8. Bureau I, Bischoff S, Heinemann SF, Mulle C (1999) Kainate receptor-mediated responses in the CA1 field of wild-type and GluR6-deficient mice. J Neurosci 19:653-663.
9. Castillo PE, Malenka RC, Nicoll RA (1997) Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 388:182-186.
10. Chen C, Okayama H (1987) High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752.
11. Clarke VR, Ballyk BA, Hoo KH, Mandelzys A, Pellizzari A, Bath CP, Thomas J, Sharpe EF, Davies CH, Ornstein PL, Schoepp DD, Kamboj RK, Collingridge GL, Lodge D, Bleakman D (1997) A GluR5 kainate receptor that regulates inhibitory synaptic transmission in the hippocampus. Nature 389:599-603.
12. DeVries SH, Schwartz EA (1999) Kainate receptors mediate synaptic transmission between cones and "OFF" bipolar cells in a mammalian retina. Nature 397:157-160.
13. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-45.
14. Everts I, Petroski R, Kizelsztein P, Teichberg VI, Heinemann SF, Hollmann M (1999) Lectin-induced inhibition of desensitization of the kainate receptor GluR6 depends on the activation state and can be mediated by a single native or ectopic N-linked carbohydrate side chain. J Neurosci 19:916-927.
15. Frerking M, Malenka RC, Nicoll RA (1998) Synaptic activation of kainate receptors on hippocampal interneurons [see comments]. Nat Neurosci 1:479-486.
16. Heckmann M, Bufler J, Franke C, Dudel J (1996) Kinetics of homomeric GluR6 glutamate receptor channels. Biophys J 71:1743-1750.
17. 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.
18. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
19. Huettner JE (1990) Glutamate receptor channels in rat dorsal root ganglion neurons: activation by kainate and quisqualate, and blockade of desensitization by concanavalin A. Neuron 5:255-266.
20. Keinänen K, Wisden W, Sommer B, Werner P, Herb A, Verdoorn TA, Sakmann B, Seeburg PH (1990) A family of AMPA-selective glutamate receptors. Science 249:556-560.
21. 2+ permeability in both TM1 and TM2 of high-affinity kainate receptor channels: diversity by RNA editing. Neuron 10:491-500.
22. Lauridsen J, Honore T, Krogsgaard-Larsen P (1985) Ibotenic acid analogues. Synthesis, molecular flexibility, and in vitro activity of agonists and antagonists at central glutamic acid receptors. J Med Chem 28:668-672.
23. Li H, Rogawski MA (1998) GluR5 kainate receptor-mediated synaptic transmission in rat basolateral amygdala in vitro. Neuropharmacology 37:1279-1286.
24. Li P, Wilding TJ, Kim SJ, Calejesan AA, Huettner JE, Zhuo M (1999) Kainate-receptor-mediated sensory synaptic transmission in mammalian spinal cord. Nature 397:161-164.
25. Lomeli H, Wisden W, Köhler M, Keinänen K, Sommer B, Seeburg PH (1992) High-affinity kainate and domoate receptors in rat brain. FEBS Lett 307:139-143.
26. Mulle C, Sailer A, Perez-Otano I, Dickinson-Anson H, Castillo PE, Bureau I, Maron C, Gage FH, Mann JR, Bettler B, Heinemann SF (1998) Altered synaptic physiology and reduced susceptibility to kainate-induced seizures in GluR6-deficient mice. Nature 392:601-605.
27. Panchenko VA, Glasser CR, Partin KM, Mayer ML (1999) Amino acid substitutions in the pore of rat glutamate receptors at sites influencing block by polyamines. J Physiol (Lond), in press.
28. Partin KM, Patneau DK, Winters CA, Mayer ML, Buonanno A (1993) Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11:1069-1082.
29. Paternain AV, Rodriguez-Moreno A, Villarroel A, Lerma J (1998) Activation and desensitization properties of native and recombinant kainate receptors. Neuropharmacology 37:1249-1259.
30. Pemberton KE, Belcher SM, Ripellino JA, Howe JR (1998) High-affinity kainate-type ion channels in rat cerebellar granule cells. J Physiol (Lond) 510:401-420.
31. Puchalski RB, Louis JC, Brose N, Traynelis SF, Egebjerg J, Kukekov V, Wenthold RJ, Rogers SW, Lin F, Moran T, Morrison JH, Heinemann SF (1994) Selective RNA editing and subunit assembly of native glutamate receptors. Neuron 13:131-147.
32. Ripellino JA, Neve RL, Howe JR (1998) Expression and heteromeric interactions of non-NMDA glutamate receptor subunits in the developing and adult cerebellum. Neuroscience 82:485-497.
33. Rodriguez-Moreno A, Herreras O, Lerma J (1997) Kainate receptors presynaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19:893-901.
34. Rosenmund C, Stern-Bach Y, Stevens CF (1998) The tetrameric structure of a glutamate receptor channel. Science 280:1596-1599.
35. Ruano D, Lambolez B, Rossier J, Paternain AV, Lerma J (1995) Kainate receptor subunits expressed in single cultured hippocampal neurons: molecular and functional variants by RNA editing. Neuron 14:1009-1017.
36. Sahara Y, Noro N, Iida Y, Soma K, Nakamura Y (1997) Glutamate receptor subunits GluR5 and KA-2 are coexpressed in rat trigeminal ganglion neurons. J Neurosci 17:6611-620.
37. Schiffer HH, Swanson GT, Heinemann SF (1997) Rat GluR7 and a carboxy-terminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate. Neuron 19:1141-1146.
38. Sommer B, Burnashev N, Verdoorn TA, Keinänen K, Sakmann B, Seeburg PH (1992) A glutamate receptor channel with high affinity for domoate and kainate. EMBO J 11:1651-1656.
39. Swanson GT, Heinemann SF (1998) Heterogeneity of homomeric GluR5 kainate receptor desensitization expressed in HEK293 cells. J Physiol (Lond) 513:639-646.
40. Swanson GT, Feldmeyer D, Kaneda M, Cull-Candy SG (1996) Effect of RNA editing and subunit coassembly on single-channel properties of recombinant kainate receptors. J Physiol (Lond) 492:129-142.
41. Swanson GT, Gereau RW, Green T, Heinemann SF (1997) Identification of amino acid residues that control functional behavior in GluR5 and GluR6 kainate receptors. Neuron 19:913-926.
42. Swanson GT, Green T, Heinemann SF (1998) Kainate receptors exhibit differential sensitivities to (S)-5-iodowillardiine. Mol Pharmacol 53:942-949.
43. Traynelis SF, Wahl P (1997) Control of rat GluR6 glutamate receptor open probability by protein kinase A and calcineurin. J Physiol (Lond) 503:513-531.
44. Vignes M, Collingridge GL (1997) The synaptic activation of kainate receptors. Nature 388:179-182.
45. Vignes M, Bleakman D, Lodge D, Collingridge GL (1997) The synaptic activation of the GluR5 subtype of kainate receptor in area CA3 of the rat hippocampus. Neuropharmacology 36:1477-1481.
46. Vignes M, Clarke VR, Parry MJ, Bleakman D, Lodge D, Ornstein PL, Collingridge GL (1998) The GluR5 subtype of kainate receptor regulates excitatory synaptic transmission in areas CA1 and CA3 of the rat hippocampus. Neuropharmacology 37:1269-1277.
47. Vyklicky L, Benveniste M, Mayer ML (1990) Modulation of N-methyl-D-aspartic acid receptor desensitization by glycine in mouse cultured hippocampal neurones. J Physiol (Lond) 428:313-331.
48. Washburn MS, Numberger M, Zhang S, Dingledine R (1997) Differential dependence on GluR2 expression of three characteristic features of AMPA receptors. J Neurosci 17:9393-9406.
49. Wenthold RJ, Trumpy VA, Zhui WS, Petralia RS (1994) Biochemical and assembly properties of GluR6 and KA2, two members of the kainate receptor family determined with subunit-specific antibodies. J Biol Chem 269:1332-1339.
50. Werner P, Voigt M, Keinänen K, Wisden W, Seeburg PH (1991) Cloning of a putative high-affinity kainate receptor expressed predominantly in hippocampal CA3 cells. Nature 351:742-744.
51. Wilding TJ, Huettner JE (1997) Activation and desensitization of hippocampal kainate receptors. J Neurosci 17:2713-2721.
52. Wisden W, Seeburg PH (1993) A complex mosaic of high-affinity kainate receptors in rat brain. J Neurosci 13:3582-3598.
53. Wong LA, Mayer ML, Jane DE, Watkins JC (1994) Willardiines differentiate agonist binding sites for kainate-versus AMPA-preferring glutamate receptors in DRG and hippocampal neurons. J Neurosci 14:3881-3897.