Activation of group I metabotropic glutamate receptors potentiates heteromeric kainate receptors

Molecular Pharmacology

Volumn 83, Issue 1, 2013, Pages 106-121

  Rojas, Asheebo ^a   Wetherington, Jonathon ^a   Shaw, Renee ^a   Serrano, Geidy ^a   Swanger, Sharon ^a   Dingledine, Raymond ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 AMINOPHENYL) 4 METHYL 7,8 METHYLENEDIOXY 5H 2,3 BENZODIAZEPINE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 2,5 PYRROLIDINEDIONE; 2 AMINO 4 PHOSPHONOBUTYRIC ACID; 2 AMINO 5 PHOSPHONOVALERIC ACID; 3 [8 [(DIMETHYLAMINO)METHYL] 6,7,8,9 TETRAHYDROPYRIDO[1,2 A]INDOL 10 YL] 4 (1 METHYL 1H INDOL 3 YL) 1H PYRROLE 2,5 DIONE; 4 METHYLGLUTAMIC ACID; 6 CYANO 7 NITRO 2,3 QUINOXALINEDIONE; 6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMN 082; BICUCULLINE; CALCIUM ION; DIZOCILPINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; ETHYLENEDIAMINE DERIVATIVE; GENISTEIN; KAINIC ACID RECEPTOR; LAVENDUSTIN A; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 2; METABOTROPIC RECEPTOR 4; METABOTROPIC RECEPTOR 5; N,N' BIS(DIPHENYLMETHYL) 1,2 ETHANEDIAMINE; OKADAIC ACID; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOLIPASE C; PROTEIN KINASE C; SERINE; STAUROSPORINE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BRAIN CORTEX; CALCIUM MOBILIZATION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; EMBRYO; FEMALE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SITE DIRECTED MUTAGENESIS; XENOPUS LAEVIS;

ANIMALS; BRAIN; CALCIUM; CELLS, CULTURED; CEREBRAL CORTEX; ENZYME ACTIVATION; FEMALE; HIPPOCAMPUS; MALE; OOCYTES; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, KAINIC ACID; RECEPTORS, METABOTROPIC GLUTAMATE; TYPE C PHOSPHOLIPASES; XENOPUS LAEVIS;

EID: 84871604041     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.081802     Document Type: Article

References (56)

1. Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M, and Fukami Y (1987) Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 262:5592-5595.
2. Alt A, Weiss B, Ogden AM, Knauss JL, Oler J, Ho K, Large TH, and Bleakman D (2004) Pharmacological characterization of glutamatergic agonists and antagonists at recombinant human homomeric and heteromeric kainate receptors in vitro. Neuropharmacology 46:793-806. (Pubitemid 38368912)
3. Aniksztejn L, Otani S, and Ben-Ari Y (1992) Quisqualate Metabotropic Receptors Modulate NMDA Currents and Facilitate Induction of Long-Term Potentiation Through Protein Kinase C. Eur J Neurosci 4:500-505.
4. Anwyl R (1994) Synaptic plasticity. A molecular switch for memory. Curr Biol 4:854-856.
5. Anwyl R (1999) Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev 29:83-120.
6. Bahn S, Volk B, and Wisden W (1994) Kainate receptor gene expression in the developing rat brain. J Neurosci 14:5525-5547. (Pubitemid 24279070)
7. Berthele A, Laurie DJ, Platzer S, Zieglgänsberger W, Tölle TR, and Sommer B (1998) Differential expression of rat and human type I metabotropic glutamate receptor splice variant messenger RNAs. Neuroscience 85:733-749. (Pubitemid 28223636)
8. Besheer J and Hodge CW (2005) Pharmacological and anatomical evidence for an interaction between mGluR5- and GABA(A) alpha1-containing receptors in the discriminative stimulus effects of ethanol. Neuropsychopharmacology 30:747-757. (Pubitemid 40397081)
9. Bettler B and Mulle C (1995) Review: neurotransmitter receptors. II. AMPA and kainate receptors. Neuropharmacology 34:123-139.
10. Bortolotto ZA, Clarke VR, and Delany CM et al. (1999a) Kainate receptors are involved in synaptic plasticity. Nature 402:297-301. (Pubitemid 129516266)
11. Bortolotto ZA, Fitzjohn SM, and Collingridge GL (1999b) Roles of metabotropic glutamate receptors in LTP and LTD in the hippocampus. Curr Opin Neurobiol 9:299-304. (Pubitemid 29267600)
12. Bureau I, Bischoff S, Heinemann SF, and Mulle C (1999) Kainate receptor-mediated responses in the CA1 field of wild-type and GluR6-deficient mice. J Neurosci 19:653-663. (Pubitemid 29036017)
13. Chamberlain SE, González-González IM, Wilkinson KA, Konopacki FA, Kantamneni S, Henley JM, and Mellor JR (2012) SUMOylation and phosphorylation of GluK2 regulate kainate receptor trafficking and synaptic plasticity. Nat Neurosci 15:845-852.
14. Chen C and Leonard JP (1996) Protein tyrosine kinase-mediated potentiation of currents from cloned NMDA receptors. J Neurochem 67:194-200.
15. Chittajallu R, Vignes M, Dev KK, Barnes JM, Collingridge GL, and Henley JM (1996) Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 379:78-81. (Pubitemid 26008139)
16. Cho K, Francis JC, Hirbec H, Dev K, Brown MW, Henley JM, and Bashir ZI (2003) Regulation of kainate receptors by protein kinase C and metabotropic glutamate receptors. J Physiol 548:723-730. (Pubitemid 36592768)
17. Clarke VR, Ballyk BA, and Hoo KH et al. (1997) A hippocampal GluR5 kainate receptor regulating inhibitory synaptic transmission. Nature 389:599-603. (Pubitemid 27446176)
18. Darstein M, Petralia RS, Swanson GT, Wenthold RJ, and Heinemann SF (2003) Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J Neurosci 23:8013-8019. (Pubitemid 37082453)
19. Dascal N (1997) Signalling via the G protein-activated K1 channels. Cell Signal 9:551-573.
20. DeWire SM, Ahn S, Lefkowitz RJ, and Shenoy SK (2007) Beta-arrestins and cell signaling. Annu Rev Physiol 69:483-510.
21. Donevan SD, Beg A, Gunther JM, and Twyman RE (1998) The methylglutamate, SYM 2081, is a potent and highly selective agonist at kainate receptors. J Pharmacol Exp Ther 285:539-545. (Pubitemid 28237430)
22. Egebjerg J and Heinemann SF (1993) Ca21 permeability of unedited and edited versions of the kainate selective glutamate receptor GluR6. Proc Natl Acad Sci USA 90:755-759. (Pubitemid 23028944)
23. Ferraguti F, Conquet F, Corti C, Grandes P, Kuhn R, and Knopfel T (1998) Immunohistochemical localization of the mGluR1beta metabotropic glutamate receptor in the adult rodent forebrain: evidence for a differential distribution of mGluR1 splice variants. J Comp Neurol 400:391-407. (Pubitemid 28447098)
24. Geissler JF, Traxler P, Regenass U, Murray BJ, Roesel JL, Meyer T, McGlynn E, Storni A, and Lydon NB (1990) Thiazolidine-diones. Biochemical and biological activity of a novel class of tyrosine protein kinase inhibitors. J Biol Chem 265:22255-22261. (Pubitemid 120014293)
25. Harvey J and Collingridge GL (1993) Signal transduction pathways involved in the acute potentiation of NMDA responses by 1S,3R-ACPD in rat hippocampal slices. Br J Pharmacol 109:1085-1090. (Pubitemid 23216776)
26. Hirbec H, Francis JC, and Lauri SE et al. (2003) Rapid and differential regulation of AMPA and kainate receptors at hippocampal mossy fibre synapses by PICK1 and GRIP. Neuron 37:625-638. (Pubitemid 36262984)
27. Huettner JE (2003) Kainate receptors and synaptic transmission. Prog Neurobiol 70:387-407.
28. Isaac JT, Mellor J, Hurtado D, and Roche KW (2004) Kainate receptor trafficking: physiological roles and molecular mechanisms. Pharmacol Ther 104:163-172. (Pubitemid 39531925)
29. Jiang J, Ganesh T, and Du Y et al. (2010) Neuroprotection by selective allosteric potentiators of the EP2 prostaglandin receptor. Proc Natl Acad Sci USA 107:2307-2312.
30. Kawajiri S and Dingledine R (1993) Multiple structural determinants of voltage-dependent magnesium block in recombinant NMDA receptors. Neuropharmacology 32:1203-1211. (Pubitemid 23322116)
31. Kelso SR, Nelson TE, and Leonard JP (1992) Protein kinase C-mediated enhancement of NMDA currents by metabotropic glutamate receptors in Xenopus oocytes. J Physiol 449:705-718.
32. Kleckner NW and Dingledine R (1988) Requirement for glycine in activation of NMDA-receptors expressed in Xenopus oocytes. Science 241:835-837.
33. Köhr G and Seeburg PH (1996) Subtype-specific regulation of recombinant NMDA receptor-channels by protein tyrosine kinases of the src family. J Physiol 492:445-452. (Pubitemid 26137754)
34. Konopacki FA, Jaafari N, Rocca DL, Wilkinson KA, Chamberlain S, Rubin P, Kantamneni S, Mellor JR, and Henley JM (2011) Agonist-induced PKC phosphorylation regulates GluK2 SUMOylation and kainate receptor endocytosis. Proc Natl Acad Sci USA 108:19772-19777.
35. Kornreich BG, Niu L, Roberson MS, and Oswald RE (2007) Identification of C-terminal domain residues involved in protein kinase A-mediated potentiation of kainate receptor subtype 6. Neuroscience 146:1158-1168. (Pubitemid 46694125)
36. Lerma J (2003) Roles and rules of kainate receptors in synaptic transmission. Nat Rev Neurosci 4:481-495.
37. Lerma J, Paternain AV, Rodríguez-Moreno A, and López-García JC (2001) Molecular physiology of kainate receptors. Physiol Rev 81:971-998. (Pubitemid 32611226)
38. Manders EMM, Verbeek FJ, and Aten JA (1993) Measurement of Colocalization of Objects in Dual-Color Confocal Images. Journal of Microscopy 169:375-382. (Pubitemid 23119681)
39. Mott DD, Benveniste M, and Dingledine RJ (2008) pH-dependent inhibition of kainate receptors by zinc. J Neurosci 28:1659-1671. (Pubitemid 351287031)
40. Mott DD, Rojas A, Fisher JL, Dingledine RJ, and Benveniste M (2010) Subunit-specific desensitization of heteromeric kainate receptors. J Physiol 588:683-700.
41. Nasu-Nishimura Y, Jaffe H, Isaac JT, and Roche KW (2010) Differential regulation of kainate receptor trafficking by phosphorylation of distinct sites on GluR6. J Biol Chem 285:2847-2856.
42. Paternain AV, Herrera MT, Nieto MA, and Lerma J (2000) GluR5 and GluR6 kainate receptor subunits coexist in hippocampal neurons and coassemble to form functional receptors. J Neurosci 20:196-205. (Pubitemid 30220507)
43. Raymond LA, Blackstone CD, and Huganir RL (1993) Phosphorylation and modulation of recombinant GluR6 glutamate receptors by cAMP-dependent protein kinase. Nature 361:637-641. (Pubitemid 23062396)
44. Raymond LA, Tingley WG, Blackstone CD, Roche KW, and Huganir RL (1994) Glutamate receptor modulation by protein phosphorylation. J Physiol Paris 88:181-192. (Pubitemid 24307056)
45. Rivera R, Rozas JL, and Lerma J (2007) PKC-dependent autoregulation of membrane kainate receptors. EMBO J 26:4359-4367. (Pubitemid 47587666)
46. Rodríguez-Moreno A, Herreras O, and Lerma J (1997) Kainate receptors pre-synaptically downregulate GABAergic inhibition in the rat hippocampus. Neuron 19 :893-901. (Pubitemid 27471393)
47. Ruiz A, Sachidhanandam S, Utvik JK, Coussen F, and Mulle C (2005) Distinct subunits in heteromeric kainate receptors mediate ionotropic and metabotropic function at hippocampal mossy fiber synapses. J Neurosci 25:11710-11718. (Pubitemid 43098463)
48. Schiffer HH, Swanson GT, and Heinemann SF (1997) Rat GluR7 and a carboxyterminal splice variant, GluR7b, are functional kainate receptor subunits with a low sensitivity to glutamate. Neuron 19:1141-1146. (Pubitemid 27512373)
49. Selak S, Paternain AV, Aller MI, Picó E, Rivera R, and Lerma J (2009) A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 63:357-371.
50. Simonyi A, Ngomba RT, Storto M, Catania MV, Miller LA, Youngs B, DiGiorgi-Gerevini V, Nicoletti F, and Sun GY (2005) Expression of groups I and II metabotropic glutamate receptors in the rat brain during aging. Brain Res 1043:95-106. (Pubitemid 40603376)
51. Sommer B, Burnashev N, Verdoorn TA, Keinänen K, Sakmann B, and Seeburg PH (1992) A glutamate receptor channel with high affinity for domoate and kainate. EMBO J 11:1651-1656.
52. Traynelis SF and Wahl P (1997) Control of rat GluR6 glutamate receptor open probability by protein kinase A and calcineurin. J Physiol 503:513-531. (Pubitemid 27496665)
53. Traynelis SF, Wollmuth LP, McBain CJ, Menniti FS, Vance KM, Ogden KK, Hansen KB, Yuan H, Myers SJ, and Dingledine R (2010) Glutamate receptor ion channels: structure, regulation, and function. Pharmacol Rev 62:405-496.
54. Wang LY, Taverna FA, Huang XP, MacDonald JF, and Hampson DR (1993) Phosphorylation and modulation of a kainate receptor (GluR6) by cAMP-dependent protein kinase. Science 259 :1173-1175. (Pubitemid 23085357)
55. Wang YT and Salter MW (1994) Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 369:233-235. (Pubitemid 24154800)
56. Wenthold RJ, Trumpy VA, Zhu WS, and 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. (Pubitemid 24032527)