Activation of mGluR5 modulates GABAA receptor function in retinal amacrine cells

Journal of Neurophysiology

Volumn 88, Issue 4, 2002, Pages 1766-1776

  Hoffpauir, Brian K ^a   Gleason, Evanna L ^a  

^a LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

(1,2,5,6 TETRAHYDROPYRIDINE 4 YL)METHYLPHOSPHINIC ACID; 12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; 2 CHLORO 5 HYDROXYPHENYLGLYCINE; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID C RECEPTOR BLOCKING AGENT; BICUCULLINE; CALCIUM ION; CHLORIDE ION; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GLUTAMATE RECEPTOR; GLYCEROL 2 ACETATE 1 OLEATE; METABOTROPIC RECEPTOR; PHORBOL 13 ACETATE 12 MYRISTATE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL CULTURE; CHICK EMBRYO; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA CELL; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP;

EID: 0036799241     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2002.88.4.1766     Document Type: Article

References (69)

1. Aramori I and Nakanishi S. Signal transduction and pharmacological characteristics of a metabotropic glutamate receptor, mGluR1, in transfected CHO cells. Neuron 8: 757-765, 1992.
2. Awatramani GB and Slaughter MM. Intensity-dependent, rapid activation of presynaptic metabotropic glutamate receptors at a central synapse. J Neurosci 21: 741-749, 2001.
3. Bateson AN. Lasham A, and Darlison MG. gamma-Aminobutyric acid A receptor heterogeneity is increased by alternative splicing of a novel beta-subunit gene transcript. J Neurochem 56: 1437-1440, 1991.
4. A receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J Biol Chem 275: 38856-38862, 2000.
5. Brandon NJ, Uren JM, Kittler JT, Wang H, Olsen R, Parker PJ, and Moss SJ. Subunit-specific association of protein kinase C and the receptor for activated C kinase with GABA type A receptors. J Neurosci 19: 9228-9234, 1999.
6. Cai W and Pourcho RG. Localization of metabotropic glutamate receptors mGluR1alpha and mGluR2/3 in the cat retina. J Comp Neurol 407: 427437, 1999.
7. Caramelo OL, Santos PF, Carvalho AP, and Duarte CB. Metabotropic glutamate receptors modulate [(3)H] acetylcholine release from cultured amacrine-like neurons. J Neurosci Res 58: 505-514, 1999.
8. b receptors regulate chick retinal calcium waves. J Neurosci 21: 897-910, 2001.
9. Choe ES and Wang JQ. Group I metabotropic glutamate receptor activation increases phosphorylation of cAMP response element-binding protein, Elk-1, and extracellular signal-regulated kinases in rat dorsal striatum. Brain Res Mol Brain Res 94: 75-84, 2001.
10. Conn PJ and Pin JP. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol 37: 205-237, 1997.
11. Connolly CN, Kittler JT, Thomas P, Uren JM, Brandon NJ, Smart TG, and Moss SJ. Cell surface stability of gamma-aminobutyric acid type A receptors. Dependence on protein kinase C activity and subunit composition. J Biol Chem 274: 36565-36572, 1999.
12. 2+ channel Cavl.2. Science 293: 98-101, 2001.
13. Dixon DB and Copenhagen DR. Metabotropic glutamate receptor-mediated suppression of an inward rectifier current is linked via a cGMP cascade. J Neurosci 17: 8945- 8954, 1997.
14. Doherty AJ, Palmer MJ, Henley JM, Collingridge GL, and Jane DE. (RS)-2-chloro-5-hydroxyphenylglycine (CHPG) activates mGlu5, but no mglu1, receptors expressed in CHO cells and potentiates NMDA responses in the hippocampus. Neuropharmacology 36: 265-267, 1997.
15. Dowling JE and Boycott BB. Neural connections of the retina: fine structure of the inner plexiform layer. Cold Spring Harb Symp Quant Biol 30: 393-402, 1965.
16. Dubin MW. The inner plexiform layer of the vertebrate retina: a quantitative and comparative electron microscopic analysis. J Comp Neurol 140: 479-505, 1970.
17. Filippova N, Sedelnikova A, Zong Y, Fortinberry H, and Weiss DS. Regulation of recombinant gamma-aminobutyric acid (GABA)(A) and GABA(C) receptors by protein kinase C. Mol Pharmacol 57: 847-856, 2000.
18. Forster IC, Harvey RJ, Darlison MG, and Benson JA. Functional pharmacology of GABA(A) receptors containing the chicken brain gamma 4 subunit. Eur J Pharmacol 419: 1-7, 2001.
19. Frerking M, Borges S, and Wilson M. Variation in GABA mini amplitude is the consequence of variation in transmitter concentration. Neuron 15: 885-895, 1995.
20. Gereau RW and Conn PJ. Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J Neurosci 15: 6879-6889, 1995.
21. Gillette MA and Dacheux RF. Protein kinase modulation of GABAA currents in rabbit retinal rod bipolar cells. J Neurophysiol 76: 3070-3086, 1996.
22. Gleason E, Borges S, and Wilson M. Synaptic transmission between pairs of retinal amacrine cells in culture. J Neurosci 13: 2359-2370, 1993.
23. 2+ influx and efflux. Neuron 13: 1109-1117, 1994.
24. Gleason E, Mobbs P, Nuccitelli R, and Wilson M. Development of functional calcium channels in cultured avian photoreceptors. Vis Neurosci 8: 315-327, 1992.
25. Greferath U, Grunert U, Fritschy JM, Stephenson A, Mohler H, and Wässle H. GABAA receptor subunits have differential distributions in the rat retina: in situ hybridization and immunohistochemistry. J Comp Neurol 353: 553-571, 1995.
26. Hartveit E. Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. J Neurophysiol 81: 2923-2936, 1999.
27. Harvey RJ, Kim HC, and Darlison MG. Molecular cloning reveals the existence of a fourth gamma subunit of the vertebrate brain GABAA receptor. FEBS Lett 331: 211-216, 1993.
28. Harvey RJ, Kim HC, and Darlison MG. Expression patterns of the GABAA receptor alpha1-, beta2-, gamma2-, and gamma4-subunit genes in chick retina. Neurosci Res Commun 15: 95-102, 1994.
29. Horn R and Marty A. Muscarinic activation of ionic currents measured by a new whole-cell recording method. J Gen Physiol 92: 145-159, 1988.
30. Joly C, Gomeza J, Brabet I, Curry K, Bockaert J, and Pin JP. Molecular, functional, and pharmacological characterization of the metabotropic glutamate receptor type 5 splice variants: comparison with mGluR1. J Neurosci 15: 3970-3981, 1995.
31. Kellenberger S, Malherbe P, and Sigel E. Function of the alpha 1 beta 2 gamma 2S gamma-aminobutyric acid type A receptor is modulated by protein kinase C via multiple phosphorylation sites. J Biol Chem 267: 25660-25663, 1992.
32. Kolb H. Amacrine cells of the mammalian retina: neurocircuitry and functional roles. Eye 11: 904-923, 1997
33. Korpi ER, Kuner T, Seeburg PH, and Luddens H. Selective antagonist for the cerebellar granule cell-specific gamma-aminobutyric acid type A receptor. Mol Pharmacol 47: 283-289, 1995.
34. Koulen P, Kuhn R, Wässle H, and Brandstatter JH. Group I metabotropic glutamate receptors mGluR1alpha and mGluR5a: localization in both synaptic layers of the rat retina. J Neurosci 17: 2200-2211, 1997.
35. Koulen P, Kuhn R, Wässle H, and Brandstatter JH. Modulation of the intracellular calcium concentration in photoreceptor terminals by a presynaptic metabotropic glutamate receptor. Proc Natl Acad Sci USA 96: 9909-9914, 1999.
36. Kreimborg KM, Lester ML, Medler KF, and Gleason EL. Group I metabotropic glutamate receptors are expressed in the chicken retina and by cultured retinal amacrine cells. J Neurochem 77: 452-465, 2001.
37. Krishek BJ, Xie X, Blackstone C, Huganir RL, Moss SJ, and Smart TG. Regulation of GABAA receptor function by protein kinase C phosphorylation. Neuron 12: 1081-1095, 1994.
38. Leidenheimer NJ, McQuilkin SJ, Hahner LD, Whiting P, and Harris RA. Activation of protein kinase C selectively inhibits the gamma-aminobutyric acidA receptor: role of desensitization. Mol Pharmacol 41: 1116-1123. 1992.
39. Lin YF, Angelotti TP, Dudek EM, Browning MD, and MacDonald RL. Enhancement of recombinant alpha 1 beta 1 gamma 2L gamma-aminobutyric acidA receptor whole-cell currents by protein kinase C is mediated through phosphorylation of both beta 1 and gamma 2L subunits. Mol Pharmacol 50: 185-195, 1996.
40. Lin YF, Browning MD, Dudek EM, and MacDonald RL. Protein kinase C enhances recombinant bovine alpha 1 beta 1 gamma 2L GABAA receptor whole-cell currents expressed in L929 fibroblasts. Neuron 13: 1421-1431, 1994.
41. Linn CL and Gafka AC. Activation of metabotropic glutamate receptors modulates the voltage-gated sustained calcium current in a teleost horizontal cell. J Neurophysiol 81: 425-434, 1999.
42. Liu SC, Parent L, Harvey RJ, Darlison MG, and Barnes EM Jr. Chicken GABA(A) receptor beta4 subunits form robust homomeric GABA- gated channels in Xenopus oocytes. Eur J Pharmacol 354: 253-259, 1998.
43. Llano I, Gonzalez J, Caputo C, Lai FA, Blayney LM, Tan YP, and Marty A. Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat Neurosci 3: 1256-1265, 2000.
44. MacNeil MA, Heussy JK, Dacheux RF, Raviola E, and Masland RH. The shapes and numbers of amacrine cells: matching of photofilled with Golgistained cells in the rabbit retina and comparison with other mammalian species. J Comp Neurol 413: 305-326, 1999.
45. MacNeil MA and Masland RH. Extreme diversity among amacrine cells: implications for function. Neuron 20: 971-982, 1998.
46. Mao L and Wang JQ. Activation of metabotropic glutamate receptor mediates upregulation of transcription factor mRNA expression in rat striatum induced by acute administration of amphetamine. Brain Res 924: 167-175, 2002.
47. Marc RE and Liu W. Fundamental GABAergic amacrine cell circuitries in the retina: nested feedback, concatenated inhibition, and axosomatic synapses. J Comp Neurol 425: 560-582, 2000.
48. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, Hug H, Marme D, and Schachtele C. Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J Biol Chem 268: 9194-9197, 1993.
49. Masu M, Iwakabe H, Tagawa Y, Miyoshi T, Yamashita M, Fukuda Y, Sasaki H, Hiroi K, Nakamura Y, Shigemoto R. Specific deficit of the ON response in visual transmission by targeted disruption of the mGluR6 gene. Cell 80: 757-765, 1995.
50. Moss SJ and Smart TG. Modulation of amino acid-gated ion channels by protein phosphorylation. Int Rev Neurobiol 39: 1-52, 1996.
51. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R, Mizuno N, and Nakanishi S. Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate, J Biol Chem 268: 11868-11873, 1993.
52. Poisbeau P, Cheney MC, Browning MD, and Mody I. Modulation of synaptic GABAA receptor function by PKA and PKC in adult hippocampal neurons. J Neurosci 19: 674-683, 1999.
53. Poncer JC, McKinney RA, Gahwiler BH, and Thompson SM. Differential control of GABA release at synapses from distinct interneurons in rat hippocampus. J Physiol (Lond) 528: 123-130, 2000.
54. Poncer JC, Shinozaki H, and Miles R. Dual modulation of synaptic inhibition by distinct metabotropic glutamate receptors in the rat hippocampus. J Physiol (Lond) 485: 121-134, 1995.
55. Raciozzino D, Woodward RM, Murata Y, Eusebi F, Overman LE, and Miledi R. Design and in vitro pharmacology of a selective gamma-aminobutyric acid C receptor antagonist. Mol Pharmacol 50: 1024-1030. 1996.
56. Schrader LA and Tasker JG. Presynaptic modulation by metabotropic glutamate receptors of excitatory and inhibitory synaptic inputs to hypothalamic magnocellular neurons. J Neurophysiol 77: 527-536, 1997.
57. Semyanov A and Kullmann DM. Modulation of GABAergic signaling among interneurons by metabotropic glutamate receptors. Neuron 25: 663-672, 2000.
58. Shen W and Slaughter MM. Metabotropic and ionotropic glutamate receptors regulate calcium channel currents in salamander retinal ganglion cells. J Physiol (Lond) 510: 815-828, 1998.
59. Sigel E, Baur R, and Malherbe P. Activation of protein kinase C results in down-modulation of different recombinant GABAA-channels. FEBS Lett 291: 150-152, 1991.
60. Stefani A, Pisani A, Mercuri NB, Bernardi G, and Calabresi P. Activation of metabotropic glutamate receptors inhibits calcium currents and GABA-mediated synaptic potentials in striatal neurons. J Neurosci 14: 6734-6743, 1994.
61. Swope SL, Moss SI, Raymond LA, and Huganir RL. Regulation of ligandgated ion channels by protein phosphorylation. Adv Second Messenger Phosphoprotein Res 33: 49-78, 1999.
62. Tapia JC, Espinoza F, and Aguayo LG. Differential intracellular regulation of cortical GABA(A) and spinal glycine receptors in cultured neurons. Brain Res 769: 203-210, 1997.
63. Thompson SA, Arden SA, Marshall G, Wingrove PB, Whiting PJ, and Wafford KA. Residues in transmembrane domains I and II determine gamma-aminobutyric acid type AA receptor subtype-selective antagonism by furosemide. Mol Phamacol 55: 993-999, 1999.
64. Tian N and Slaughter MM. Pharmacology of the GABAB receptor in amphibian retina. Brain Res 660: 267-274, 1994.
65. Vardi N and Morigiwa K. ON cone bipolar cells in rat express the metabotropic receptor mGluR6. Vis Neurosci 14: 789-794, 1997.
66. Vardi N, Morigiwa K, Wang TL, Shi YJ, and Sterling P. Neurochemistry of the mammalian cone 'synaptic complex'. Vision Res 38: 1359-1369, 1998.
67. Wafford KA, Thompson SA, Thomas D, Sikela J, Wilcox AS, and Whiting PJ. Functional characterization of human gamma-aminobutyric acidA receptors containing the alpha 4 subunit. Mol Pharmacol 50: 670-678, 1996.
68. Wall MJ. Cis-4-amino-crotonic acid activates alpha6 subunit-containing GABA(A) but not GABA(C) receptors in granule cells of adult rat cerebellar slices. Neitrosci Lett 316: 37-40, 2001.
69. Wässle H, Koulen P, Brandstatter JH, Fletcher EL, and Becker CM. Glycine and GABA receptors in the mammalian retina. Vision Res 38: 1411-1430, 1998.