Autonomous CaMKII mediates both LTP and LTD using a mechanism for differential substrate site selection

Cell Reports

Volumn 6, Issue 3, 2014, Pages 431-437

  Coultrap, Steven J ^a   Freund, Ronald K ^a   O'Leary, Heather ^a,b   Sanderson, Jennifer L ^a   Roche, Katherine W ^c   Dell'Acqua, Mark L ^a   Bayer, K Ulrich ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b Children's Hospital Colorado   (United States)

^c NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; HIPPOCAMPUS; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MICE; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHOSPHOSERINE; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SUBSTRATE SPECIFICITY;

AMPA RECEPTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; GLUTAMINE; SERINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; BINDING SITE; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOLECULAR MECHANICS; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

EID: 84893866641     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.01.005     Document Type: Article

References (44)

1. 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 1997, 276:2042-2045.
2. Bayer K.U., De Koninck P., Leonard A.S., Hell J.W., Schulman H. Interaction with the NMDA receptor locks CaMKII in an active conformation. Nature 2001, 411:801-805.
3. Bayer K.U., De Koninck P., Schulman H. Alternative splicing modulates the frequency-dependent response of CaMKII to Ca(2+) oscillations. EMBO J. 2002, 21:3590-3597.
4. Bayer K.U., LeBel E., McDonald G.L., O'Leary H., Schulman H., De Koninck P. Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B. J.Neurosci. 2006, 26:1164-1174.
5. Benke T.A., Lüthi A., Isaac J.T., Collingridge G.L. Modulation ofAMPA receptor unitary conductance by synaptic activity. Nature 1998, 393:793-797.
6. Buard I., Coultrap S.J., Freund R.K., Lee Y.S., Dell'Acqua M.L., Silva A.J., Bayer K.U. CaMKII "autonomy" is required for initiating but not for maintaining neuronal long-term information storage. J.Neurosci. 2010, 30:8214-8220.
7. Chao L.H., Stratton M.M., Lee I.H., Rosenberg O.S., Levitz J., Mandell D.J., Kortemme T., Groves J.T., Schulman H., Kuriyan J. A mechanism for tunable autoinhibition in the structure of a human Ca2+/calmodulin- dependent kinase II holoenzyme. Cell 2011, 146:732-745.
8. Colbran R.J., Brown A.M. Calcium/calmodulin-dependent protein kinase II and synaptic plasticity. Curr. Opin. Neurobiol. 2004, 14:318-327.
9. Collingridge G.L., Peineau S., Howland J.G., Wang Y.T. Long-term depression in the CNS. Nat. Rev. Neurosci. 2010, 11:459-473.
10. Coultrap S.J., Bayer K.U. CaMKII regulation in information processing and storage. Trends Neurosci. 2012, 35:607-618.
11. Coultrap S.J., Buard I., Kulbe J.R., Dell'Acqua M.L., Bayer K.U. CaMKII autonomy is substrate-dependent and further stimulated by Ca2+/calmodulin. J.Biol. Chem. 2010, 285:17930-17937.
12. Coultrap S.J., Barcomb K., Bayer K.U. A significant but rather mild contribution of T286 autophosphorylation to Ca2+/CaM-stimulated CaMKII activity. PLoS ONE 2012, 7:e37176.
13. De Koninck P., Schulman H. Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 1998, 279:227-230.
14. 2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate type glutamate receptors. Proc. Natl. Acad. Sci. USA 1999, 96:3269-3274.
15. Dudek S.M., Bear M.F. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc. Natl. Acad. Sci. USA 1992, 89:4363-4367.
16. Dudek S.M., Bear M.F. Bidirectional long-term modification of synaptic effectiveness in the adult and immature hippocampus. J.Neurosci. 1993, 13:2910-2918.
17. Elgersma Y., Fedorov N.B., Ikonen S., Choi E.S., Elgersma M., Carvalho O.M., Giese K.P., Silva A.J. Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity, and learning. Neuron 2002, 36:493-505.
18. Giese K.P., Fedorov N.B., Filipkowski R.K., Silva A.J. Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science 1998, 279:870-873.
19. Hayashi Y., Shi S.H., Esteban J.A., Piccini A., Poncer J.C., Malinow R. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 2000, 287:2262-2267.
20. Helmchen F. Raising the speed limit-fast Ca(2+) handling in dendritic spines. Trends Neurosci. 2002, 25:438-441. discussion 441.
21. Hinds H.L., Tonegawa S., Malinow R. CA1 long-term potentiation is diminished but present in hippocampal slices from alpha-CaMKII mutant mice. Learn. Mem. 1998, 5:344-354.
22. Ismailov I., Kalikulov D., Inoue T., Friedlander M.J. The kinetic profile of intracellular calcium predicts long-term potentiation and long-term depression. J.Neurosci. 2004, 24:9847-9861.
23. Kristensen A.S., Jenkins M.A., Banke T.G., Schousboe A., Makino Y., Johnson R.C., Huganir R., Traynelis S.F. Mechanism of Ca2+/calmodulin-dependent kinase II regulation of AMPA receptor gating. Nat. Neurosci. 2011, 14:727-735.
24. Lee H.K., Kameyama K., Huganir R.L., Bear M.F. NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 1998, 21:1151-1162.
25. Lisman J., Yasuda R., Raghavachari S. Mechanisms of CaMKII action in long-term potentiation. Nat. Rev. Neurosci. 2012, 13:169-182.
26. Lu W., Isozaki K., Roche K.W., Nicoll R.A. Synaptic targeting of AMPA receptors is regulated by a CaMKII site in the first intracellular loop of GluA1. Proc. Natl. Acad. Sci. USA 2010, 107:22266-22271.
27. Malenka R.C., Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 2004, 44:5-21.
28. Martin S.J., Grimwood P.D., Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 2000, 23:649-711.
29. Massey P.V., Johnson B.E., Moult P.R., Auberson Y.P., Brown M.W., Molnar E., Collingridge G.L., Bashir Z.I. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J.Neurosci. 2004, 24:7821-7828.
30. Miller S.G., Kennedy M.B. Regulation of brain type II Ca2+/calmodulin-dependent protein kinase by autophosphorylation: a Ca2+-triggered molecular switch. Cell 1986, 44:861-870.
31. Mockett B.G., Guévremont D., Wutte M., Hulme S.R., Williams J.M., Abraham W.C. Calcium/calmodulin-dependent protein kinase II mediates group I metabotropic glutamate receptor-dependent protein synthesis and long-term depression in rat hippocampus. J.Neurosci. 2011, 31:7380-7391.
32. Mulkey R.M., Malenka R.C. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 1992, 9:967-975.
33. Opazo P., Labrecque S., Tigaret C.M., Frouin A., Wiseman P.W., De Koninck P., Choquet D. CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 2010, 67:239-252.
34. 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 1996, 16:1179-1188.
35. Sanderson J.L., Gorski J.A., Gibson E.S., Lam P., Freund R.K., Chick W.S., Dell'Acqua M.L. AKAP150-anchored calcineurin regulates synaptic plasticity by limiting synaptic incorporation of Ca2+-permeable AMPA receptors. J.Neurosci. 2012, 32:15036-15052.
36. Schnabel R., Palmer M.J., Kilpatrick I.C., Collingridge G.L. A CaMKII inhibitor, KN-62, facilitates DHPG-induced LTD in the CA1 region of the hippocampus. Neuropharmacology 1999, 38:605-608.
37. Silva A.J., Stevens C.F., Tonegawa S., Wang Y. Deficient hippocampal long-term potentiation in α-calcium-calmodulin kinase II mutant mice. Science 1992, 257:201-206.
38. Stanton P.K., Gage A.T. Distinct synaptic loci of Ca2+/calmodulin-dependent protein kinase II necessary for long-term potentiation and depression. J.Neurophysiol. 1996, 76:2097-2101.
39. Stevens C.F., Tonegawa S., Wang Y. The role of calcium-calmodulin kinase II in three forms of synaptic plasticity. Curr. Biol. 1994, 4:687-693.
40. Vest R.S., Davies K.D., O'Leary H., Port J.D., Bayer K.U. Dual mechanism of a natural CaMKII inhibitor. Mol. Biol. Cell 2007, 18:5024-5033.
41. Wikström M.A., Matthews P., Roberts D., Collingridge G.L., Bortolotto Z.A. Parallel kinase cascades are involved in the induction of LTP at hippocampal CA1 synapses. Neuropharmacology 2003, 45:828-836.
42. Xia Z., Storm D.R. The role of calmodulin as a signal integrator for synaptic plasticity. Nat. Rev. Neurosci. 2005, 6:267-276.
43. Yasuda H., Barth A.L., Stellwagen D., Malenka R.C. A developmental switch in the signaling cascades for LTP induction. Nat. Neurosci. 2003, 6:15-16.
44. Zucker R.S. Calcium- and activity-dependent synaptic plasticity. Curr. Opin. Neurobiol. 1999, 9:305-313.