Mechanism of Ca2+/calmodulin-dependent kinase II regulation of AMPA receptor gating

Nature Neuroscience

Volumn 14, Issue 6, 2011, Pages 727-735

  Kristensen, Anders S ^a,b   Jenkins, Meagan A ^a   Banke, Tue G ^a   Schousboe, Arne ^b   Makino, Yuichi ^c   Johnson, Richard C ^c   Huganir, Richard ^c   Traynelis, Stephen 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

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; SERINE; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CELL MEMBRANE CONDUCTANCE; CHANNEL GATING; CONTROLLED STUDY; FEMALE; HIPPOCAMPUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; C57BL MOUSE; CYTOLOGY; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; METABOLISM; NERVE CELL; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; GENE EXPRESSION REGULATION; GENE KNOCK-IN TECHNIQUES; HIPPOCAMPUS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; NEURONS; PHOSPHORYLATION; RECEPTORS, AMPA; SERINE; SIGNAL TRANSDUCTION;

EID: 79960795718     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.2804     Document Type: Article

References (50)

1. Traynelis, S.F. et al. Glutamate receptor ion channels: structure, regulation, and function. Pharmacol. Rev. 62, 405-496 (2010).
2. Malinow, R. & Malenka, R.C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126 (2002). (Pubitemid 34748013)
3. Sobolevsky, A.I., Rosconi, M.P. & Gouaux, E. X-ray structure, symmetry and mechanism of an AMPA-subtype glutamate receptor. Nature 462, 745-756 (2009).
4. Derkach, V., Barria, A. & Soderling, T.R. Ca2+/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 (1999). (Pubitemid 29148880)
5. Barria, A., Derkach, V. & Soderling, T. Identification of the Ca2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in the α-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate-type glutamate receptor. J. Biol. Chem. 272, 32727-32730 (1997). (Pubitemid 28023601)
6. Shepherd, J.D. & Huganir, R.L. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol. 23, 613-643 (2007).
7. Tomita, S. et al. Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature 435, 1052-1058 (2005). (Pubitemid 40910507)
8. Banke, T.G. et al. Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J. Neurosci. 20, 89-102 (2000). (Pubitemid 30220495)
9. Holmes, W.R. & Grover, L.M. Quantifying the magnitude of changes in synaptic level parameters with long-term potentiation. J. Neurophysiol. 96, 1478-1491 (2006). (Pubitemid 44371537)
10. Benke, T.A., Lüthi, A., Isaac, J.T. & Collingridge, G.L. Modulation of AMPA receptor unitary conductance by synaptic activity. Nature 393, 793-797 (1998). (Pubitemid 28299491)
11. Malenka, R.C., Kauer, J.A., Zucker, R.S. & Nicoll, R.A. Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science 242, 81-84 (1988).
12. Lee, H.K. et al. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112, 631-643 (2003).
13. Lee, H.K., Barbarosie, M., Kameyama, K., Bear, M.F. & Huganir, R.L. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature 405, 955-959 (2000). (Pubitemid 30435052)
14. Silva, A.J., Stevens, C.F., Tonegawa, S. & Wang, Y. Deficient hippocampal long-term potentiation in α-calcium-calmodulin kinase II mutant mice. Science 257, 201-206 (1992).
15. Lamsa, K., Irvine, E.E., Giese, K.P. & Kullmann, D.M. NMDA receptor-dependent long-term potentiation in mouse hippocampal interneurons shows a unique dependence on Ca2+/calmodulin-dependent kinases. J. Physiol. (Lond.) 584, 885-894 (2007). (Pubitemid 350031929)
16. Lee, H.K., Takamiya, K., He, K., Song, L. & Huganir, R.L. 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 (2010).
17. Barria, A., Muller, D., Derkach, V., Griffith, L.C. & Soderling, T.R. Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276, 2042-2045 (1997). (Pubitemid 27443609)
18. Mammen, A.L., Kameyama, K., Roche, K.W. & Huganir, R.L. Phosphorylation of the α-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. J. Biol. Chem. 272, 32528-32533 (1997). (Pubitemid 28011939)
19. Hayashi, Y. et al. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262-2267 (2000). (Pubitemid 30177031)
20. Lüthi, A. et al. Bi-directional modulation of AMPA receptor unitary conductance by synaptic activity. BMC Neurosci. 5, 44 (2004).
21. Poncer, J.C., Esteban, J.A. & Malinow, R. Multiple mechanisms for the potentiation of AMPA receptor-mediated transmission by α-Ca2+/calmodulin- dependent protein kinase II. J. Neurosci. 22, 4406-4411 (2002). (Pubitemid 37465657)
22. Palmer, M.J., Isaac, J.T. & Collingridge, G.L. Multiple, developmentally regulated expression mechanisms of long-term potentiation at CA1 synapses. J. Neurosci. 24, 4903-4911 (2004). (Pubitemid 38697822)
23. Smith, T.C. & Howe, J.R. Concentration-dependent substate behavior of native AMPA receptors. Nat. Neurosci. 3, 992-997 (2000).
24. Poon, K., Nowak, L.M. & Oswald, R.E. Characterizing single-channel behavior of GluA3 receptors. Biophys. J. 99, 1437-1446 (2010).
25. Rosenmund, C., Stern-Bach, Y. & Stevens, C.F. The tetrameric structure of a glutamate receptor channel. Science 280, 1596-1599 (1998). (Pubitemid 28277703)
26. Jin, R., Banke, T.G., Mayer, M.L., Traynelis, S.F. & Gouaux, E. Structural basis for partial agonist action at ionotropic glutamate receptors. Nat. Neurosci. 6, 803-810 (2003). (Pubitemid 36929700)
27. Prieto, M.L. & Wollmuth, L.P. Gating modes in AMPA receptors. J. Neurosci. 30, 4449-4459 (2010).
28. Wenthold, R.J., Petralia, R.S., Blahos, J. II & Niedzielski, A.S. Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci. 16, 1982-1989 (1996). (Pubitemid 26144011)
29. Traynelis, S.F. & Jaramillo, F. Getting the most out of noise in the central nervous system. Trends Neurosci. 21, 137-145 (1998). (Pubitemid 28157181)
30. Derkach, V.A. Silence analysis of AMPA receptor mutated at the CaM-kinase II phosphorylation site. Biophys. J. 84, 1701-1708 (2003). (Pubitemid 36322933)
31. Swanson, G.T., Kamboj, S.K. & Cull-Candy, S.G. Single-channel properties of recombinant AMPA receptors depend on RNA editing, splice variation, and subunit composition. J. Neurosci. 17, 58-69 (1997). (Pubitemid 27008850)
32. Tomita, S., Stein, V., Stocker, T.J., Nicoll, R.A. & Bredt, D.S. Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Neuron 45, 269-277 (2005). (Pubitemid 40128120)
33. Oh, M.C. & Derkach, V.A. Dominant role of the GluR2 subunit in regulation of AMPA receptors by CaMKII. Nat. Neurosci. 8, 853-854 (2005).
34. Stern-Bach, Y., Russo, S., Neuman, M. & Rosenmund, C. A point mutation in the glutamate binding site blocks desensitization of AMPA receptors. Neuron 21, 907-918 (1998). (Pubitemid 28498797)
35. Deng, F., Price, M.G., Davis, C.F., Mori, M. & Burgess, D.L. Stargazin and other transmembrane AMPA receptor regulating proteins interact with synaptic scaffolding protein MAGI-2 in brain. J. Neurosci. 26, 7875-7884 (2006). (Pubitemid 44315157)
36. Soto, D., Coombs, I.D., Kelly, L., Farrant, M. & Cull-Candy, S.G. Stargazin attenuates intracellular polyamine block of calcium-permeable AMPA receptors. Nat. Neurosci. 10, 1260-1267 (2007). (Pubitemid 47480295)
37. Milstein, A.D. & Nicoll, R.A. TARP modulation of synaptic AMPA receptor trafficking and gating depends on multiple intracellular domains. Proc. Natl. Acad. Sci. USA 106, 11348-11351 (2009).
38. Milstein, A.D., Zhou, W., Karimzadegan, S., Bredt, D.S. & Nicoll, R.A. TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron 55, 905-918 (2007). (Pubitemid 47391192)
39. Nicoll, R.A., Tomita, S. & Bredt, D.S. Auxiliary subunits assist AMPA-type glutamate receptors. Science 311, 1253-1256 (2006). (Pubitemid 43334707)
40. Hogner, A. et al. Structural basis for AMPA receptor activation and ligand selectivity: crystal structures of five agonist complexes with the GluR2 ligand-binding core. J. Mol. Biol. 322, 93-109 (2002). (Pubitemid 36138726)
41. Frandsen, A. et al. Tyr702 is an important determinant of agonist binding and domain closure of the ligand-binding core of GluR2. Mol. Pharmacol. 67, 703-713 (2005). (Pubitemid 40372239)
42. Traynelis, S.F. & Wahl, P. Control of rat GluR6 glutamate receptor open probability by protein kinase A and calcineurin. J. Physiol. (Lond.) 503, 513-531 (1997). (Pubitemid 27496665)
43. Roche, K.W., O'Brien, R.J., Mammen, A.L., Bernhardt, J. & Huganir, R.L. Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16, 1179-1188 (1996). (Pubitemid 26227239)
44. Boehm, J. et al. Synaptic incorporation of AMPA receptors during LTP is controlled by a PKC phosphorylation site on GluR1. Neuron 51, 213-225 (2006). (Pubitemid 44041865)
45. Lin, D.T. et al. Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation. Nat. Neurosci. 12, 879-887 (2009).
46. Tavalin, S.J. 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 (2008).
47. Lisman, J. & Raghavachari, S. A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci. STKE 2006, re11 (2006).
48. Lee, H.K. et al. Identification and characterization of a novel phosphorylation site on the GluR1 subunit of AMPA receptors. Mol. Cell. Neurosci. 36, 86-94 (2007).
49. Delgado, J.Y. et al. NMDA receptor activation dephosphorylates AMPA receptor glutamate receptor 1 subunits at threonine 840. J. Neurosci. 27, 13210-13221 (2007). (Pubitemid 350220483)
50. Serulle, Y. et al. A GluR1-cGKII interaction regulates AMPA receptor trafficking. Neuron 56, 670-688 (2007). (Pubitemid 350102028)