Structure and pharmacological properties of a molluscan glutamate-gated cation channel and its likely role in feeding behavior

Journal of Neuroscience

Volumn 16, Issue 9, 1996, Pages 2869-2880

  Stühmer, Thorsten ^a   Amar, Muriel ^a,b   Harvey, Robert J ^a   Bermudez, Isabel ^b   Van Minnen, Jan ^c   Darlison, Mark G ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

4 cluster motorneurons; buccal ganglion; complementary DNA cloning; feeding behavior; in situ hybridization; ion channel; ionotropic glutamate receptor; kainate receptor; mollusc (Lymnaea stagnalis); Xenopus oocyte expression

Indexed keywords

1 (4 CHLOROBENZOYL) 2,3 PIPERAZINEDICARBOXYLIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; 6,7 DINITRO 2,3 QUINOXALINEDIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMINO ACID; CATION; CATION CHANNEL; COMPLEMENTARY DNA; GLUTAMATE RECEPTOR; GLUTAMIC ACID; IBOTENIC ACID; KAINIC ACID; POTASSIUM ION; RECEPTOR SUBUNIT; RNA; SODIUM ION;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; FEEDING BEHAVIOR; IN SITU HYBRIDIZATION; MOTONEURON; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; VOLTAGE CLAMP; XENOPUS LAEVIS;

EID: 0029940701     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-09-02869.1996     Document Type: Article

References (65)

1. Bertrand D, Ballivet M, Gomez M, Bertrand S, Phannavong B, Gundelfinger ED (1994) Physiological properties of neuronal nicotinic receptors reconstituted from the vertebrate β2 subunit and Drosophila α subunits. Eur J Neurosci 6:869-875.
2. 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.
3. Bettler B, Egebjerg J, Sharma G, Pecht G, Hermans-Borgmeyer I, Moll C, Stevens CF, Heinemann S (1992) Cloning of a putative glutamate receptor: a low affinity kainate-binding subunit. Neuron 8:257-265.
4. Bolshakov VY, Gapon SA, Magazanik LG (1991) Different types of glutamate receptors in isolated and identified neurones of the mollusc Planorbarius corneus. J Physiol (Lond) 439:15-35.
5. Ciabarra AM, Sullivan JM, Gahn LG, Pecht G, Heinemann S, Sevarino KA (1995) Cloning and characterization of χ-1: a developmentally regulated member of a novel class of the ionotropic glutamate receptor family. J Neurosci 15:6498-6508.
6. Dale N, Kandel ER (1993) L-Glutamate may be the fast excitatory transmitter of Aplysia sensory neurons. Proc Natl Acad Sci USA 90:7163-7167.
7. Darlison MG, Stühmer T, Harvey RJ, Dautzenberg FM, Kim H-C, Zimmermann C, Amar M, Bermudez I, van Minnen J (1994) Molecular characterisation and functional expression of molluscan ion-channel receptors that can be activated by either γ-aminobutyric acid or L-glutamate. Neth J Zool 44:473-485.
8. Dascal N (1987) The use of Xenopus oocytes for the study of ion channels. CRC Crit Rev Biochem 22:317-387.
9. 2+ permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci USA 90:755-759.
10. Egebjerg J, Bettler B, Hermans-Borgmeyer I, Heinemann S (1991) Cloning of a cDNA for a glutamate receptor subunit activated by kainate but not AMPA. Nature 351:745-748.
11. Foster AC, Fagg GE (1984) Acidic amino acid binding sites in mammalian neuronal membranes: their characteristics and relationship to synaptic receptors. Brain Res Rev 7:103-164.
12. Frohman MA, Martin GR (1989) Rapid amplification of cDNA ends using nested primers. Technique 1:165-170.
13. Goldschmeding JT, Bruins HJ, Everts WM (1977) Topography of buccal and cerebral neurones involved in feeding in the freshwater snail Lymnaea stagnalis. Proc K Ned Acad Wet 80:83-96.
14. Gregor P, Mano I, Maoz I, McKeown M, Teichberg VI (1989) Molecular structure of the chick cerebellar kainate-binding subunit of a putative glutamate receptor. Nature 342:689-692.
15. A receptor subunit which can form a chimeric receptor with a vertebrate α subunit. EMBO J 10:3239-3245.
16. A receptor α1-, β2-. γ2- and γ4-subunit genes in chick retina. Neurosci Res Commun 15:95-102.
17. Harvey RJ, Schmitt B, Hermans-Borgmeyer I, Gundelfinger ED, Betz H, Darlison MG (1994b) Sequence of a Drosophila ligand-gated ion-channel polypeptide with an unusual amino-terminal extracellular domain. J Neurochem 62:2480-2483.
18. 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.
19. Hollmann M, Heinemann S (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
20. Hollmann M, O'Shea-Greenfield A, Rogers SW, Heinemann S (1989) Cloning by functional expression of a member of the glutamate receptor family. Nature 342:643-648.
21. Hollmann M, Maron C, Heinemann S (1994) N-glycosylation site tagging suggests a three transmembrane domain topology for the glutamate receptor GluR1. Neuron 13:1331-1343.
22. Hutton ML, Harvey RJ, Barnard EA, Darlison MG (1991) Cloning of a cDNA that encodes an invertebrate glutamate receptor subunit. FEBS Lett 292:111-114.
23. Ikeda K, Nagasawa M, Mori H, Araki K, Sakimura K, Watanabe M, Inoue Y, Mishina M (1992) Cloning and expression of the ∈4 subunit of the NMDA receptor channel. FEBS Lett 313:34-38.
24. Ikemoto Y, Akaike N (1988) The glutamate-induced chloride current in Aplysia neurones lacks pharmacological properties seen for excitatory responses to glutamate. Eur J Pharmacol 150:313-318.
25. Jan LY, Jan YN (1976) L-Glutamate as an excitatory transmitter at the Drosophila larval neuromuscular junction. J Physiol (Lond) 262:215-236.
26. Katz PS, Levitan IB (1993) Quisqualate and ACPD are agonists for a glutamate-activated current in identified Aplysia neurons. J Neurophysiol 69:143-150.
27. Kehoe J (1978) Transformation by concanavalin A of the response of molluscan neurones to L-glutamate. Nature 274.866-869.
28. 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.
29. Kemenes G, Daykin K, Elliott CJH (1991) Photoinactivation of neurones axonally filled with the fluorescent dye 5(6)-carboxyfluorescein in the pond snail, Lymnaea stagnalis. J Neurosci Methods 39:207-216.
30. Kemp BE, Pearson RB (1990) Protein kinase recognition sequence motifs. Trends Biochem Sci 15:342-346.
31. Kimura N, Kurosawa N, Kondo K, Tsukada Y (1993) Molecular cloning of the kainate-binding protein and calmodulin genes which are induced by an imprinting stimulus in ducklings. Mol Brain Res 17:351-355.
32. 2+ permeability in both TM1 and TM2 of high affinity kainate receptor channels: diversity by RNA editing. Neuron 10:491-500.
33. Kutsuwada T, Kashiwabuchi N, Mori H, Sakimura K, Kushiya E, Araki K, Meguro H, Masaki H, Kumanishi T, Arakawa M, Mishina M (1992) Molecular diversity of the NMDA receptor channel. Nature 358:36-41.
34. + channel determined by construction of multimeric cDNAs. Neuron 9:861-871.
35. 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.
36. Lomeli H, Sprengel R, Laune DJ, Köhr G, Herb A, Seeburg PH, Wisden W (1993) The rat delta-1 and delta-2 subunits extend the excitatory amino acid receptor family. FEBS Lett 315:318-322.
37. Mat Jais AM, Kerkut GA, Walker RJ (1984) The ionic mechanisms associated with the excitatory response of kainate, L-glutamate, quisqualate, ibotenate, AMPA and methyltetrahydrofolate on leech Retzius cells. Comp Biochem Physiol [C] 77:115-126.
38. Mathers DA, Usherwood PNR (1976) Concanavalin A blocks desensitisation of glutamate receptors on insect muscle fibres. Nature 259:409-411.
39. Mayer ML, Vyklicky L Jr (1989) Concanavalin A selectively reduces desensitization of mammalian neuronal quisqualate receptors. Proc Natl Acad Sci USA 86:1411-1415.
40. Meguro H, Mori H, Araki K, Kushiya E, Kutsuwada T, Yamazaki M, Kumanishi T, Arakawa M, Sakimura K, Mishina M (1992) Functional characterization of a heteromeric NMDA receptor channel expressed from cloned cDNAs. Nature 357:70-74.
41. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, Seeburg PH (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256:1217-1221.
42. Morita T, Sakimura K, Kushiya E, Yamazaki M, Meguro H, Araki K, Abe T, Mori KJ, Mishina M (1992) Cloning and functional expression of a cDNA encoding the mouse β2 subunit of the kainate-selective glutamate receptor channel Mol Brain Res 14:143-146.
43. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakanishi S (1991) Molecular cloning and characterization of the rat NMDA receptor. Nature 354:31-37.
44. Nakanishi N, Shneider NA, Axel R (1990) A family of glutamate receptor genes: evidence for the formation of heteromultimeric receptors with distinct channel properties. Neuron 5:569-581.
45. Quinlan EM, Murphy AD (1991) Glutamate as a putative neurotransmitter in the buccal central pattern generator of Helisoma trivolvis. J Neurophysiol 66:1264-1271.
46. Quinlan EM, Gregory K, Murphy AD (1995) An identified glutamatergic interneuron patterns feeding motor activity via both excitation and inhibition. J Neurophysiol 73:945-956.
47. Roberts CJ, Nielsen E, Krogsgaard-Larsen P, Walker RJ (1982) The actions of ibotenate, homoibotenate analogues and AMPA on central neurons of Hirudo, Limulus and Helix. Comp Biochem Physiol [C] 73:439-444.
48. Rose RM, Benjamin PR (1979) The relationship of the central motor pattern to the feeding cycle of Lymnaea stagnalis. J Exp Biol 80:137-163.
49. Sakimura K, Bujo H, Kushiya E, Araki K, Yamazaki M, Yamazaki M, Meguro H, Warashina A, Numa S, Mishina M (1990) Functional expression from cloned cDNAs of glutamate receptor species responsive to kainate and quisqualate. FEBS Lett 272:73-80.
50. Sakimura K, Morita T, Kushiya E, Mishina M (1992) Primary structure and expression of the γ2 subunit of the glutamate receptor channel selective for kainate. Neuron 8:267-274.
51. Schuster CM, Ultsch A, Schloss P, Cox JA, Schmitt B, Betz H (1991) Molecular cloning of an invertebrate glutamate receptor subunit expressed in Drosophila muscle. Science 254:112-114.
52. Sommer B, Kohler M, Sprengel R, Seeburg PH (1991) RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67:11-19.
53. 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.
54. Sucher NJ, Akbarian S, Chi CL, Ledere CL, Awobuluyi M, Deitcher DL, Wu MK, Yuan JP, Jones EG, Lipton SA (1995) Developmental and regional expression of a novel NMDA receptor-like subunit (NMDAR-L) in the rodent brain. J Neurosci 15:6509-6520.
55. Ultsch A, Schuster CM, Laube B, Schloss P, Schmitt B, Betz H (1992) Glutamate receptors of Drosophila melanogaster. Cloning of a kainate-selective subunit expressed in the central nervous system. Proc Natl Acad Sci USA 89:10484-10488.
56. Ultsch A, Schuster CM, Laube B, Betz H, Schmitt B (1993) Glutamate receptors of Drosophila melanogaster. Primary structure of a putative NMDA receptor protein expressed in the head of the adult fly. FEBS Lett 324:171-177.
57. Vernino S, Amador M, Luetje CW, Patrick J, Dani JA (1992) Calcium modulation and high calcium permeability of neuronal nicotinic acetylcholine receptors. Neuron 8:127-134.
58. von Heijne G (1986) A new method for predicting signal sequence cleavage sites. Nucleic Acids Res 14:4683-4690.
59. Wada K, Dechesne CJ, Shimasaki S, King RG, Kusano K, Buonanno A, Hampson DR, Banner C, Wenthold RJ, Nakatani Y (1989) Sequence and expression of a frog brain complementary DNA encoding a kainate-binding protein. Nature 342:684-689.
60. 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.
61. Wisden W, Morris BJ, Hunt SP (1991) In situ hybridization with synthetic DNA probes. In: Molecular neurobiology - a practical approach, Vol 2. (Chad J, Wheal H, eds), pp 205-225. Oxford: IRL Press.
62. Wo ZG, Oswald RE (1994) Transmembrane topology of two kainate receptor subunits revealed by N-glycosylation. Proc Natl Acad Sci USA 91:7154-7158.
63. Woodgett JR, Gould KL, Hunter T (1986) Substrate specificity of protein kinase C. Use of synthetic peptides corresponding to physiological sites as probes for substrate recognition requirements. Eur J Biochem 161:177-184.
64. Yamazaki M, Araki K, Shibata A, Mishina M (1992) Molecular cloning of a cDNA encoding a novel member of the mouse glutamate receptor channel family. Biochem Biophys Res Commun 183:886-892.
65. Yarowslcy PJ, Carpenter DO (1976) Aspartate: distinct receptors on Aplysia neurons. Science 192:807-809.