Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase

Journal of Neuroscience

Volumn 20, Issue 1, 2000, Pages 89-102

  Banke, T G ^a,b   Bowie, D ^a   Lee, H K ^c   Huganir, R L ^c   Schousboe, A ^b   Traynelis, S F ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMPA receptors; Calcineurin; GluR1; Glutamate; LTD; Open probability; PKA

Indexed keywords

AMPA RECEPTOR; CALCINEURIN; CALMODULIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUTAMATE RECEPTOR; RECEPTOR SUBUNIT;

AMINO ACID SUBSTITUTION; ARTICLE; CONTROLLED STUDY; GENE MUTATION; HUMAN; HUMAN CELL; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

EID: 0034001787     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-01-00089.2000     Document Type: Article

References (84)

1. Asztely F, Gustafsson B (1996) Ionotropic glutamate receptors. Their possible role in the expression of hippocampal synaptic plasticity. Mol Neurobiol 12:1-11.
2. Banke T, Traynelis SF (1998) Control of GluR1 activation by cAMP-dependent protein kinase. Soc Neurosci Abtr 24:1272.
3. 2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in the α-amino-3-hydroxy-5-methyl-4-isoxazole-propionate-type glutamate receptor. J Biol Chem 272:32727-32730.
4. Benke TA, Luthi A, Isaac JTR, Collingridge GL (1998) Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393:793-797.
5. Blackstone C, Murphy TH, Moss SJ, Baraban JM, Huganir RL (1994) Cyclic AMP and synaptic activity-dependent phosphorylation of AMPA-preferring glutamate receptors. J Neurosci 14:7585-7593.
6. Bolshakov VY, Siegelbaum SA (1994) Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science 264:1148-1152.
7. Boulter J, Hollmann M, O'Shea-Greenfield A, Hartley M, Deneris E, Maron C, Heinemann S (1990) Molecular cloning and functional expression of glutamate receptor subunit genes. Science 249:1033-1037.
8. Bowie D, Lange GD, Mayer ML (1998) Activity-dependent modulation of glutamate receptors by polyamines. J Neurosci 18:8175-8185.
9. Carroll RC, Lissin DV, von Zastrow M, Nicoll RA, Malenka RC (1999) Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat Neurosci 2:454-460.
10. Chavez-Noriega LE, Stevens CF (1992) Modulation of synaptic efficacy in field CA1 of the rat hippocampus by forskolin. Brain Res 574:85-92.
11. Chen C, Okayama H (1987) High efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752.
12. Coghlan VM, Perrino BA, Howard M, Langeberg LK, Hicks JB, Gallatin WM, Scott JD (1995) Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science 267:108-111.
13. + channel Kir 2.3 to PSD-95 is regulated by protein kinase A phosphorylation. Neuron 17:759-767.
14. Colquhoun D, Hawkes AG (1977) Relaxation and fluctuations of membrane currents that flow through drug-operated channels. Proc R Soc Lond B Biol Sci 199:231-262.
15. Colquhoun D, Sigworth FJ (1995) Fitting and statistical analysis of single channel records. In Single-channel recording (Sakman B, Neher E, eds), pp 483-588. New York: Plenum.
16. Colquhoun D, Jonas P, Sakmann B (1992) Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices. J Physiol (Lond) 458:261-287.
17. Cull-Candy SG, Usowicz MM (1987) Multiple conductance channels activated by excitatory amino acids in cerebellar neurons. Nature 325:525-528.
18. Cull-Candy SG, Howe JR, Ogden DC (1988) Noise and single channels activated by excitatory amino acids in large cerebellar neurons of the rat. J Physiol (Lond) 400:189-222.
19. 2+ /calmodulin-kinase II enhances channel conductance of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci USA 96:3269-3274.
20. Dingledine R, Borges K, Bowie D, Traynelis SF (1999) The glutamate receptor ion channels. Pharmacol Rev 51:7-61.
21. Fraser IDC, Scott JD (1999) Modulation of ion channels: a current view of AKAPS. Neuron 23:423-426.
22. Gomperts SN, Rao A, Craig AM, Malenka RC, Nicoll RA (1998) Postsynaptically silent synapses in single neuron cultures. Neuron 21:1443-1451.
23. Greengard P, Jen J, Nairn AC, Stevens CF (1991) Enhancement of the glutamate response by cAMP-dependent protein kinase in hippocampal neurons. Science 253:1135-1138.
24. Hausser M, Roth A (1997) Dendritic and somatic glutamate receptor channels in rat cerebellar Purkinje cells. J Physiol (Lond) 501:77-95.
25. Heckmann M, Bufler J, Franke C, Dudel J (1996) Kinetics of homomeric GluR6 glutamate receptor channels. Biophys J 71:1743-1750.
26. Heinemann SH, Conti F (1942) Nonstationary noise analysis and application to patch clamp recordings. Methods Enzymol 207:131-148.
27. Hestrin S (1992) Activation and desensitization of glutamate-activated channels mediating fast excitatory synaptic currents in the visual cortex. Neuron 9:991-999.
28. Hollmann M, Heinemann SF (1994) Cloned glutamate receptors. Annu Rev Neurosci 17:31-108.
29. Huggenvik JI, Collard MW, Stofko RE, Seasholtz AF, Uhler MD (1991) Regulation of the human enkephalin promoter by two isoforms of the catalytic subunit of cyclic adenosine 3′5′-monophosphate-dependent protein kinase. Mol Endocrinol 5:921-930.
30. Irizarry SN, Pemberton KE, Howe JR (1998) Agonist-specific differences in the unitary properties of homomeric GluR1 receptors. Soc Neurosci Abstr 24:847.
31. Jahr CE, Stevens CF (1987) Glutamate activates multiple single channel conductances in hippocampal neurons. Nature 325:522-525.
32. Jonas P, Sakmann B (1992) Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells of rat hippocampal slices. J Physiol (Lond) 455:143-171.
33. Jonas P, Major G, Sakmann B (1993) Quantal components of unitary EPSCs at the mossy-fibre synapse on CA3 pyramidal cells of rat hippocampus. J Physiol (Lond) 472:615-663.
34. Kameyama K, Lee H-K, Bear M F, Huganir RL (1998) Involvement of a postsynaptic protein kinase A substrate in the expression of homosynaptic long-term depression. Neuron 21:1163-1175.
35. Kandler K, Katz LC, Kauer JA (1998) Focal photolysis of caged glutamate produces long-term depression of hippocampal glutamate receptors. Nat Neurosci 1:119-123.
36. Keller BU, Hollmann M, Heinemann S, Konnerth A (1992) Calcium influx through subunits GluR1/GluR3 of kainate/AMPA receptor channels is regulated by cAMP dependent protein kinase. EMBO J 11:891-896.
37. Kim YH, Huganir RL (1999) Organization and regulation of proteins at synapses. Curr Opin Cell Biol 2:248-254.
38. Knapp AG, Schmidt KF, Dowling JE (1990) Dopamine modulates the kinetics of ion channels gated by excitatory amino acids in retinal horizontal cells. Proc Natl Acad Sci USA 87:767-771.
39. Kullmann DM, Asztely F (1998) Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends Neurosci 21:8-14.
40. Kullmann DM, Siegelbaum SA (1995) The site of expression of NMDA receptor-dependent LTP: new fuel for an old fire. Neuron 15:997-1002.
41. Lee H-K, Kameyama K, Huganir RL, Bear MF (1998) NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 21:1151-1162.
42. Leranth C, Szeidemann Z, Hsu M, Buzsaki G (1996) AMPA receptors in the rat and primate hippocampus: a possible absence of GluR2/3 subunits in most interneurons. Neuroscience 70:631-652.
43. Levenes C, Daniel H, Crepel F (1998) Long-term depression of synaptic transmission in the cerebellum: cellular and molecular mechanisms revisited. Prog Neurobiol 55:79-91.
44. Linden DJ (1994) Long-term synaptic depression in the mammalian brain. Neuron 12:457-472.
45. Malenka RC, Nicoll RA (1999) Long-term potentiation - a decade of progress? Science 285:1870-1874.
46. Mammen AL, Kameyama K, Roche KW, Huganir RL (1997) Phosphorylation of the α-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. J Biol Chem 272:32528-32533.
47. Maren S, Baudry M (1995) Properties and mechanisms of long-term synaptic plasticity in the mammalian brain: relationships to learning and memory. Neurobiol Learn Mem 63:1-18.
48. Marshall J, Molloy R, Moss GW, Howe JR, Hughes TE (1995) The jellyfish green fluorescent protein: a new tool for studying ion channel expression and function. Neuron 14:211-215.
49. Matsuda S, Mikawa S, Hirai H (1999) Phosphorylation of serine-880 in GluR2 by protein kinase C prevents its C terminus from binding with glutamate receptor-interacting protein. J Neurochem 73:1765-1768.
50. Monyer H, Seeburg PH, Wisden W (1991) Glutamate-operated channels: developmentally early and mature forms arise by alternative splicing. Neuron 6:799-810.
51. Mosbacher J, Schoepfer R, Monyer H, Burnashev N, Seeburg PH, Ruppersberg JP (1994) A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266:1059-1062.
52. Mulkey RM, Endo S, Shenolikar S, Malenka RC (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369:486-488.
53. Neher E, Stevens CF (1977) Conductance fluctuations and ionic pores in membranes. Annu Rev Biophys Bioeng 6:345-381.
54. Partin KM, Fleck MW, Mayer ML (1996) AMPA receptor flip/flop mutants affecting deactivation, desensitization, and modulation by cyclothiazide, antiracetam, and thiocyanate. J Neurosci 16:6634-6647.
55. Pearson RB, Kemp BE (1991) Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol 200A:62-81.
56. Raman IM, Trussell LO (1992) The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus. Neuron 9:173-186.
57. Raman IM, Trussell LO (1995) Concentration-jump analysis of voltage dependent conductances activated by glutamate and kainate in neurons of the avian cochlear nucleus. Biophys J 69:1868-1879.
58. Rison RA, Stanton PK (1995) Long-term potentiation and N-methyl-D-aspartate receptors: foundations of memory and neurologic disease? Neurosci Biobehav Rev 19:533-552.
59. Roberson ED, Sweatt JD (1996) Transient activation of cyclic AMP-dependent protein kinase during hippocampal long-term potentiation. J Biol Chem 271:30436-30441.
60. Roche KW, O'Brien RJ, Mammen AL, Bernhardt J, Huganir RL (1996) Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16:1179-1188.
61. Rosenmund C, Carr DW, Bergeson SE, Nilaver G, Scott JD, Westbrook GL (1994) Anchoring of protein kinase A is required for modulation of AMPA/kainate receptors on hippocampal neurons. Nature 368:853-856.
62. Rosenmund C, Stern-Bach Y, Stevens CF (1998) The tetrameric structure of a glutamate receptor channel. Science 280:1596-1599.
63. Sigworth FJ (1980) The variance of sodium current fluctuations at the node of Ranvier. J Physiol (Lond) 307:97-129.
64. Silberberg SD, Magleby KL (1993) Preventing errors when estimating single channel properties from the analysis of current fluctuations. Biophys J 65:1570-1584.
65. Sommer B, Keinanen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, Kohler M, Takagi T, Sakmann B, Seeburg PH (1990) Flip and flop: a cell-specific functional switch ion glutamate-operated channels of the CNS. Science 249:1580-1585.
66. Spruston N, Jonas P, Sakmann B (1995) Dendritic glutamate receptor channels in rat hippocampal CA3 and CA1 pyramidal neurons. J Physiol (Lond) 482:325-352.
67. Stern-Bach Y, Bettler B, Hartley M, Sheppard PO, O'Hara PJ, Heinemann SF (1994) Agonist selectivity of glutamate receptors is specified by two domains structurally related to bacterial amino acid-binding proteins. Neuron 13:1345-1357.
68. Stevens CF, Wang Y (1994) Changes in reliability of synaptic function as a mechanism for plasticity. Nature 371:704-707.
69. Swanson GT, Feldmeyer D, Kaneda M, Cull-Candy SG (1996) Effect of RNA editing and subunit co-assembly on single-channel properties of recombinant kainate receptors. J Physiol (Lond) 492:129-142.
70. Swanson GT, Kamboj SK, Cull-Candy SG (1997) Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J Neurosci 17:58-69.
71. Traynelis SF, Jaramillo F (1998) Making the most out of noise in the central nervous system. Trends Neurosci 21:137-145.
72. Traynelis SF, Wahl P (1997) Control of GluR6 receptor open probability by protein kinase A and calcineurin. J Physiol (Lond) 503:513-531.
73. Trussell LO, Fischbach GD (1989) Glutamate receptor desensitization and its role in synaptic transmission. Neuron 3:209-218.
74. Tzounopoulos T, Janz R, Sudhof TC, Nicoll RA, Malenka RC (1998) A role for cAMP in long-term depression at hippocampal mossy fiber synapses. Neuron 21:837-845.
75. Wahl P, Anker C, Traynelis SF, Egebjerg J, Rasmussen JS, Krogsgaard-Larsen P, Madsen U (1998) Antagonist properties of a phosphono isoxazole amino acid at GluR1-4 (R,S)-2-amino-3-(3-hydroxy-5-methyl-4-isoxazolyl)propionic acid receptor subtypes. Mol Pharmacol 53:590-596.
76. 2+ signaling mechanisms in hippocampal CA1 neurons. J Neurosci 17:4600-4611.
77. Wang J-H, Stelzer A (1994) Inhibition of phosphatase 2B prevents expression of hippocampal long-term potentiation. NeuroReport 5:2377-2380.
78. Wang LY, Salter MW, MacDonald JF (1991) Regulation of kainate receptors by cAMP-dependent protein kinase and phosphatases. Science 253:1132-1135.
79. 1 receptor mRNA down-regulation in vascular smooth muscle cells. Mol Pharmacol 54:514-524.
80. Washburn MS, Numberger M, Zhang S, Dingledine R (1997) Differential dependence of GluR2 expression of three characteristic features of AMPA receptors. J Neurosci 17:9393-9406.
81. Wyllie DJA, Traynelis SF, Cull-Candy SG (1993) Evidence for more than one type of non-NMDA receptor in outside-out patches from rat cerebellar granule cells. J Physiol (Lond) 463:193-226.
82. Yan Z, Hsieh-Wilson L, Feng J, Tomizawa K, Allen PB, Fienberg AA, Nairn AC, Greengard P (1999) Protein phosphatase 1 modulation of neostriatal AMPA channels: regulation by DARP-32 and spinophilin. Nat Neurosci 2:13-17.
83. Yan-You H, Kandel ER (1998) Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21:169-178.
84. Zar JH (1999) Biostatistical analysis. Upper Saddle River, NJ: Prentice Hall.