Regulation of GluA1 α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor function by protein kinase C at serine-818 and threonine-840

Molecular Pharmacology

Volumn 85, Issue 4, 2014, Pages 618-629

  Jenkins, Meagan A ^a   Wells, Gordon ^a   Bachman, Julia ^b   Snyder, James P ^a   Jenkins, Andrew ^a   Huganir, Richard L ^b   Oswald, Robert E ^c   Traynelis, Stephen F ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^c Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID RECEPTOR; AMPA RECEPTOR; PROTEIN KINASE C; SERINE; SERINE 818; THREONINE; THREONINE 840; UNCLASSIFIED DRUG;

AGONIST; ANIMAL TISSUE; ARTICLE; CONDUCTANCE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; GENE MUTATION; HIPPOCAMPUS; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; PYRAMIDAL NERVE CELL; REGULATORY MECHANISM;

ANIMALS; FEMALE; HEK293 CELLS; HIPPOCAMPUS; HUMANS; MALE; MICE; MODELS, MOLECULAR; MUTATION; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEIN CONFORMATION; PROTEIN KINASE C; RATS; RECEPTORS, AMPA; SERINE; THREONINE;

EID: 84896840708     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.091488     Document Type: Article

References (52)

1. Banke TG, Bowie D, Lee H, Huganir RL, Schousboe A, and Traynelis SF (2000) Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J Neurosci 20:89-102. (Pubitemid 30220495)
2. Barria A, Derkach V, and Soderling T (1997a) Identification of the Ca2+/calmodulindependent protein kinase II regulatory phosphorylation site in the a-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate-type glutamate receptor. J Biol Chem 272:32727-32730. (Pubitemid 28023601)
3. Barria A, Muller D, Derkach V, Griffith LC, and Soderling TR (1997b) Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276:2042-2045. (Pubitemid 27443609)
4. Benke TA, Lüthi A, Isaac JT, and Collingridge GL (1998) Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393:793-797. (Pubitemid 28299491)
5. Bliss TV and Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39. (Pubitemid 23020772)
6. Boehm J, Ehrlich I, Hsieh H, and Malinow R (2006a) Two mutations preventing PDZ-protein interactions of GluR1 have opposite effects on synaptic plasticity. Learn Mem 13:562-565. (Pubitemid 44498405)
7. Boehm J, Kang MG, Johnson RC, Esteban J, Huganir RL, and Malinow R (2006b) Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 51:213-225. (Pubitemid 44041865)
8. Copits BA and Swanson GT (2013) Kainate receptor post-translational modifications differentially regulate association with 4.1N to control activity-dependent receptor endocytosis. J Biol Chem 288:8952-8965.
9. Cull-Candy SG, Howe JR, and Ogden DC (1988) Noise and single channels activated by excitatory amino acids in rat cerebellar granule neurones. J Physiol 400:189-222.
10. Delaglio F, Grzesiek S, Vuister GW, Zhu G, Pfeifer J, and Bax A (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6:277-293.
11. Delgado JY, Coba M, Anderson CN, Thompson KR, Gray EE, Heusner CL, Martin KC, Grant SG, and O'Dell TJ (2007) NMDA receptor activation dephosphorylates AMPA receptor glutamate receptor 1 subunits at threonine 840. J Neurosci 27:13210-13221. (Pubitemid 350220483)
12. Derkach V, Barria A, and Soderling TR (1999) Ca2+/calmodulin-kinase II enhances channel conductance of a-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci USA 96:3269-3274. (Pubitemid 29148880)
13. Derkach VA (2003) Silence analysis of AMPA receptor mutated at the CaM-kinase II phosphorylation site. Biophys J 84:1701-1708. (Pubitemid 36322933)
14. Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, and Malinow R (2003) PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci 6:136-143. (Pubitemid 36182782)
15. Hu GY, Hvalby O, Walaas SI, Albert KA, Skjeflo P, Andersen P, and Greengard P (1987) Protein kinase C injection into hippocampal pyramidal cells elicits features of long term potentiation. Nature 328:426-429. (Pubitemid 17097773)
16. Jenkins MA and Traynelis SF (2012) PKC phosphorylates GluA1-Ser831 to enhance AMPA receptor conductance. Channels (Austin) 6:60-64.
17. Jin R, Banke TG, Mayer ML, Traynelis SF, and Gouaux E (2003) Structural basis for partial agonist action at ionotropic glutamate receptors. Nat Neurosci 6:803-810. (Pubitemid 36929700)
18. Kelley LA and Sternberg MJ (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363-371.
19. Kessels HW and Malinow R (2009) Synaptic AMPA receptor plasticity and behavior. Neuron 61:340-350.
20. Kristensen AS, Jenkins MA, Banke TG, Schousboe A, Makino Y, Johnson RC, Huganir R, and Traynelis SF (2011) Mechanism of Ca2+/calmodulin-dependent kinase II regulation of AMPA receptor gating. Nat Neurosci 14:727-735.
21. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, and Thornton JM (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8:477-486. (Pubitemid 126706801)
22. Lee HK, Takamiya K, He K, Song L, and Huganir RL (2010) Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus. J Neurophysiol 103:479-489.
23. Lee HK, Takamiya K, Kameyama K, He K, Yu S, Rossetti L, Wilen D, and Huganir RL (2007) Identification and characterization of a novel phosphorylation site on the GluR1 subunit of AMPA receptors. Mol Cell Neurosci 36:86-94. (Pubitemid 47379556)
24. Lee HK, Takamiya K, Han JS, Man H, Kim CH, Rumbaugh G, Yu S, Ding L, He C, and Petralia RS et al. (2003) Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112:631-643. (Pubitemid 36331776)
25. Lee S, Song B, Kim J, Park K, Hong I, An B, Song S, Lee J, Park S, and Kim J et al. (2013) GluA1 phosphorylation at serine 831 in the lateral amygdala is required for fear renewal. Nat Neurosci 16:1436-1444.
26. Lin DT and Huganir RL (2007) PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptorinduced internalization. J Neurosci 27:13903-13908. (Pubitemid 350278247)
27. Lin DT, Makino Y, Sharma K, Hayashi T, Neve R, Takamiya K, and Huganir RL (2009) Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation. Nat Neurosci 12:879-887.
28. Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, and Nicoll RA (2009) Subunit composition of synaptic AMPA receptors revealed by a singlecell genetic approach. Neuron 62:254-268.
29. Lüthi A, Wikström MA, Palmer MJ, Matthews P, Benke TA, Isaac JT, and Collingridge GL (2004) Bi-directional modulation of AMPA receptor unitary conductance by synaptic activity. BMC Neurosci 5:44.
30. Makino Y, Johnson RC, Yu Y, Takamiya K, and Huganir RL (2011) Enhanced synaptic plasticity in mice with phosphomimetic mutation of the GluA1 AMPA receptor. Proc Natl Acad Sci USA 108:8450-8455.
31. Malinow R (1994) LTP: desperately seeking resolution. Science 266:1195-1196. (Pubitemid 24371269)
32. Malinow R and Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103-126. (Pubitemid 34748013)
33. Mammen AL, Kameyama K, Roche KW, and Huganir RL (1997) Phosphorylation of the a-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. J Biol Chem 272:32528-32533. (Pubitemid 28011939)
34. Ouyang Y, Rosenstein A, Kreiman G, Schuman EM, and Kennedy MB (1999) Tetanic stimulation leads to increased accumulation of Ca (21)/calmodulin- dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J Neurosci 19:7823-7833. (Pubitemid 30225781)
35. Poncer JC, Esteban JA, and Malinow R (2002) Multiple mechanisms for the potentiation of AMPA receptor-mediated transmission by a-Ca2+/calmodulin- dependent protein kinase II. J Neurosci 22:4406-4411. (Pubitemid 37465657)
36. Poon K, Ahmed AH, Nowak LM, and Oswald RE (2011) Mechanisms of modal activation of GluA3 receptors. Mol Pharmacol 80:49-59.
37. Prieto ML and Wollmuth LP (2010) Gating modes in AMPA receptors. J Neurosci 30:4449-4459.
38. Ramakers GM, Gerendasy DD, and De Graan PN (1999) Substrate phosphorylation in the protein kinase Cgamma knockout mouse. J Biol Chem 274:1873-1874.
39. Roche KW, O'Brien RJ, Mammen AL, Bernhardt J, and Huganir RL (1996) Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16:1179-1188. (Pubitemid 26227239)
40. Rosenmund C, Stern-Bach Y, and Stevens CF (1998) The tetrameric structure of a glutamate receptor channel. Science 280:1596-1599. (Pubitemid 28277703)
41. Rucker SP and Shaka AJ (1989) Broadband homonuclear cross polarization in 2D N. M. R. using DIPSI-2. Mol Phys 68:509-517 DOI: 10.1080/00268978900102331.
42. Schwieters CD, Kuszewski JJ, and MariusClore G (2006) Using Xplor-NIH for NMR molecular structure determination. Prog Nucl Magn Reson Spectrosc 48:47-62.
43. Silva AJ, Stevens CF, Tonegawa S, and Wang Y (1992) Deficient hippocampal longterm potentiation in a-calcium-calmodulin kinase II mutant mice. Science 257:201-206.
44. Sobolevsky AI, Rosconi MP, and Gouaux E (2009) X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462:745-756.
45. Sommer B, Keinänen K, Verdoorn TA, Wisden W, Burnashev N, Herb A, Köhler M, Takagi T, Sakmann B, and Seeburg PH (1990) Flip and flop: a cell-specific functional switch in glutamate-operated channels of the CNS. Science 249:1580-1585.
46. Song I and Huganir RL (2002) Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci 25:578-588. (Pubitemid 35254182)
47. Stern-Bach Y, Russo S, Neuman M, and Rosenmund C (1998) A point mutation in the glutamate binding site blocks desensitization of AMPA receptors. Neuron 21:907-918. (Pubitemid 28498797)
48. Tavalin SJ (2008) AKAP79 selectively enhances protein kinase C regulation of GluR1 at a Ca2+-calmodulin-dependent protein kinase II/protein kinase C site. J Biol Chem 283:11445-11452.
49. Thomas GM, Lin DT, Nuriya M, and Huganir RL (2008) Rapid and bi-directional regulation of AMPA receptor phosphorylation and trafficking by JNK. EMBO J 27:361-372. (Pubitemid 351161658)
50. 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)
51. Traynelis SF and Jaramillo F (1998) Getting the most out of noise in the central nervous system. Trends Neurosci 21:137-145. (Pubitemid 28157181)
52. Wenthold RJ, Petralia RS, Blahos J II, and Niedzielski AS (1996) Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J Neurosci 16:1982-1989. (Pubitemid 26144011)