The CaMKII/NMDAR complex as a molecular memory

Molecular Brain

Volumn 6, Issue 1, 2013, Pages

  Sanhueza, Magdalena ^a   Lisman, John ^b  

^a UNIVERSITY OF CHILE   (Chile)

^b BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID BINDING PROTEIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; DELTA CATENIN; DENSIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE CELL ADHESION MOLECULE; UNCLASSIFIED DRUG;

CARBOXY TERMINAL SEQUENCE; HIPPOCAMPUS; LONG TERM POTENTIATION; MEMORY; NEUROTRANSMISSION; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; HUMANS; LONG-TERM POTENTIATION; MEMORY; PROTEIN KINASE C; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION;

EID: 84873604107     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-6-10     Document Type: Review

References (83)

1. Mechanisms of CaMKII action in long-term potentiation. Lisman J, Yasuda R, Raghavachari S, Nat Rev Neurosci 2012 13 3 169 182 22334212
2. Calmodulin as a direct detector of Ca2+ signals. Faas G, et al. Nat Neurosci 2011 14 3 301 304 10.1038/nn.2746 21258328
3. Modulation of AMPA receptor unitary conductance by synaptic activity. Benke TA, et al. Nature 1998 393 6687 793 797 10.1038/31709 9655394 (Pubitemid 28299491)
4. Mechanism of Ca2+/calmodulin-dependent kinase II regulation of AMPA receptor gating. Kristensen AS, et al. Nat Neurosci 2011 14 6 727 35 10.1038/nn.2804 21516102
5. Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs. Tomita S, et al. Neuron 2005 45 2 269 77 10.1016/j.neuron.2005.01.009 15664178 (Pubitemid 40128120)
6. CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Opazo P, et al. Neuron 2010 67 2 239 252 10.1016/j.neuron.2010.06.007 20670832
7. Identification of a phosphorylation site for calcium/calmodulindependent protein kinase II in the NR2B subunit of the N-methyl-D-aspartate receptor. Omkumar RV, et al. J Biol Chem 1996 271 49 31670 31678 10.1074/jbc.271.49.31670 8940188 (Pubitemid 26408631)
8. Autophosphorylation-dependent targeting of calcium/ calmodulin-dependent protein kinase II by the NR2B subunit of the N-methyl- D-aspartate receptor. Strack S, Colbran RJ, J Biol Chem 1998 273 33 20689 20692 10.1074/jbc.273.33. 20689 9694809 (Pubitemid 28385342)
9. Calcium/calmodulin-dependent protein kinase II is associated with NR2A/B subunits of NMDA receptor in postsynaptic densities. Gardoni F, et al. J Neurochem 1998 71 4 1733 1741 9751209 (Pubitemid 28443048)
10. Calcium/calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor. Leonard AS, et al. Proc Natl Acad Sci USA 1999 96 6 3239 3244 10.1073/pnas.96.6.3239 10077668 (Pubitemid 29148875)
11. Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B. Bayer KU, et al. J Neurosci 2006 26 4 1164 1174 10.1523/JNEUROSCI.3116-05.2006 16436603 (Pubitemid 43237049)
12. LTP in hippocampal neurons is associated with a CaMKII-mediated increase in GluA1 surface expression. Appleby VJ, et al. J Neurochem 2011 116 4 530 543 10.1111/j.1471-4159.2010.07133.x 21143596
13. Persistent accumulation of calcium/calmodulin-dependent protein kinase II in dendritic spines after induction of NMDA receptor-dependent chemical long-term potentiation. Otmakhov N, et al. The Journal of neuroscience: the official journal of the Society for Neuroscience 2004 24 42 9324 31 10.1523/JNEUROSCI.2350-04.2004 (Pubitemid 39426169)
14. Optical induction of plasticity at single synapses reveals input-specific accumulation of alphaCaMKII. Zhang YP, Holbro N, Oertner TG, Proc Natl Acad Sci USA 2008 105 33 12039 44 10.1073/pnas.0802940105 18697934
15. Spatiotemporal Regulation of Signaling in and out of Dendritic Spines: CaMKII and Ras. Lee SJ, Yasuda R, The open neuroscience journal 2009 3 117 127 10.2174/1874082000903020117 20463853
16. Interaction with the NMDA receptor locks CaMKII in an active conformation. Bayer KU, et al. Nature 2001 411 6839 801 5 10.1038/35081080 11459059 (Pubitemid 32588103)
17. Quantitative estimates of the cytoplasmic, PSD, and NMDAR-bound pools of CaMKII in dendritic spines. Feng B, Raghavachari S, Lisman J, Brain Res 2011 1419 46 52 21925648
18. Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Tanaka J-I, et al. Science 2008 319 5870 1683 1687 10.1126/science.1152864 18309046 (Pubitemid 351432509)
19. Long-term potentiation is associated with an increased activity of Ca2+/calmodulin-dependent protein kinase II. Fukunaga K, et al. J Biol Chem 1993 268 11 7863 7 8385124 (Pubitemid 23120362)
20. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Barria A, Malinow R, Neuron 2005 48 2 289 301 10.1016/j.neuron.2005.08.034 16242409 (Pubitemid 41476362)
21. Mechanism and regulation of calcium/calmodulin-dependent protein kinase II targeting to the NR2B subunit of the N-methyl-D-aspartate receptor. Strack S, McNeill RB, Colbran RJ, J Biol Chem 2000 275 31 23798 806 10.1074/jbc. M001471200 10764765 (Pubitemid 30624665)
22. CaMKII binding to GluN2B is critical during memory consolidation. Halt A, et al. EMBO J 2012 31 5 1203 1216 10.1038/emboj.2011.482 22234183
23. Interactions between the NR2B receptor and CaMKII modulate synaptic plasticity and spatial learning. Zhou Y, et al. J Neurosci 2007 27 50 13843 13853 10.1523/JNEUROSCI.4486-07.2007 18077696 (Pubitemid 350278268)
24. CaMKII control of spine size and synaptic strength: role of phosphorylation states and nonenzymatic action. Pi HJ, et al. Proc Natl Acad Sci USA 2010 107 32 14437 42 10.1073/pnas.1009268107 20660727
25. Dual mechanism of a natural CaMKII inhibitor. Vest RS, et al. Mol Biol Cell 2007 18 12 5024 33 10.1091/mbc.E07-02-0185 17942605 (Pubitemid 350246702)
26. Characterization of a calmodulin kinase II inhibitor protein in brain. Chang BH, Mukherji S, Soderling TR, Proc Natl Acad Sci USA 1998 95 18 10890 5 10.1073/pnas.95.18.10890 9724800 (Pubitemid 28413164)
27. Role of the CaMKII/NMDA receptor complex in the maintenance of synaptic strength. Sanhueza M, et al. J Neurosci 2011 31 25 9170 9178 10.1523/JNEUROSCI.1250-11.2011 21697368
28. Dosemeci A, et al. The effect of CaMKII inhibitor tatCN21 on the re-distribution of CaMKII and SynGAP in hippocampal neurons under excitatory conditions. SFN Program#/Poster#: 43.15/C53. In Society for Neuroscience New Orleans 2012
29. Postsynaptic inhibitors of calcium/calmodulin-dependent protein kinase type II block induction but not maintenance of pairing-induced long-term potentiation. Otmakhov N, Griffith LC, Lisman JE, J Neurosci 1997 17 14 5357 5365 9204920 (Pubitemid 27300303)
30. Is persistent activity of calcium/calmodulin-dependent kinase required for the maintenance of LTP? Chen HX, et al. J Neurophysiol 2001 85 4 1368 1376 11287461
31. A structural mechanism for maintaining the 'on-state' of the CaMKII memory switch in the post-synaptic density. Mullasseril P, et al. J Neurochem 2007 103 1 357 64 17877639 (Pubitemid 47404211)
32. Involvement of the CA3-CA1 synapse in the acquisition of associative learning in behaving mice. Gruart A, Munoz MD, Delgado-Garcia JM, The Journal of neuroscience: the official journal of the Society for Neuroscience 2006 26 4 1077 87 10.1523/JNEUROSCI.2834-05.2006 (Pubitemid 43237039)
33. Learning induces long-term potentiation in the hippocampus. Whitlock JR, et al. Science 2006 313 5790 1093 7 10.1126/science.1128134 16931756 (Pubitemid 44300229)
34. Direct measurement of quantal changes underlying long-term potentiation in CA1 hippocampus. Liao D, Jones A, Malinow R, Neuron 1992 9 6 1089 1097 10.1016/0896-6273(92)90068-O 1334418 (Pubitemid 23007180)
35. Heterogeneity of synaptic plasticity at unitary CA3-CA1 and CA3-CA3 connections in rat hippocampal slice cultures. Debanne D, Gahwiler BH, Thompson SM, The Journal of neuroscience: the official journal of the Society for Neuroscience 1999 19 24 10664 71 (Pubitemid 30235713)
36. On the Mechanism of Synaptic Depression Induced by CaMKIIN, an Endogenous Inhibitor of CaMKII. Gouet C, et al. PLoS One 2012 7 11 49293 10.1371/journal.pone.0049293 23145145
37. Ontogeny of postsynaptic density proteins at glutamatergic synapses. Petralia RS, et al. Mol Cell Neurosci 2005 29 3 436 52 10.1016/j.mcn.2005.03.013 15894489 (Pubitemid 40799216)
38. Structure and composition of the postsynaptic density during development. Swulius MT, et al. J Comp Neurol 2010 518 20 4243 60 10.1002/cne.22451 20878786
39. Synaptic remodeling, synaptic growth and the storage of long-term memory in Aplysia. Bailey CH, Kandel ER, Prog Brain Res 2008 169 179 198 18394474 (Pubitemid 351451903)
40. Coordination of size and number of excitatory and inhibitory synapses results in a balanced structural plasticity along mature hippocampal CA1 dendrites during LTP. Bourne JN, Harris KM, Hippocampus 2011 21 4 354 73 10.1002/hipo.20768 20101601
41. Synaptic tagging and long-term potentiation. Frey U, Morris RG, Nature 1997 385 6616 533 536 10.1038/385533a0 9020359 (Pubitemid 27074671)
42. CaMKII activation is a novel effector of alcohol's neurotoxicity in neural crest stem/progenitor cells. Garic A, et al. J Neurochem 2011 118 4 646 57 10.1111/j.1471-4159.2011.07273.x 21496022
43. Synaptic tagging and capture: differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation. Redondo RL, et al. The Journal of neuroscience: the official journal of the Society for Neuroscience 2010 30 14 4981 9 10.1523/JNEUROSCI. 3140-09.2010
44. Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Bozdagi O, et al. Neuron 2000 28 1 245 59 10.1016/S0896-6273(00)00100-8 11086998
45. Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin. Bozdagi O, et al. The Journal of neuroscience: the official journal of the Society for Neuroscience 2010 30 30 9984 9 10.1523/JNEUROSCI.1223-10.2010
46. A role for the cadherin family of cell adhesion molecules in hippocampal long-term potentiation. Tang L, Hung CP, Schuman EM, Neuron 1998 20 6 1165 75 10.1016/S0896-6273(00)80497-3 9655504 (Pubitemid 28293133)
47. N-cadherin mediates plasticity-induced long-term spine stabilization. Mendez P, et al. J Cell Biol 2010 189 3 589 600 10.1083/jcb.201003007 20440002
48. Densin-180 forms a ternary complex with the (alpha)-subunit of Ca2+/calmodulin-dependent protein kinase II and (alpha)-actinin. Walikonis RS, et al. The Journal of neuroscience: the official journal of the Society for Neuroscience 2001 21 2 423 33 (Pubitemid 32107433)
49. Multivalent Interactions of Calcium/Calmodulin-dependent Protein Kinase II with the Postsynaptic Density Proteins NR2B, Densin-180, and α-Actinin-2. Robison AJ, et al. J Biol Chem 2005 280 42 35329 35336 10.1074/jbc.M502191200 16120608 (Pubitemid 41532721)
50. Densin-180 interacts with delta-catenin/neural plakophilin-related armadillo repeat protein at synapses. Izawa I, et al. J Biol Chem 2002 277 7 5345 50 10.1074/jbc.M110052200 11729199 (Pubitemid 34968580)
51. Cadherin-catenin adhesion complexes at the synapse. Brigidi GS, Bamji SX, Curr Opin Neurobiol 2011 21 2 208 14 10.1016/j.conb.2010.12.004 21255999
52. Quantal analysis and synaptic anatomy-integrating two views of hippocampal plasticity. Lisman JE, Harris KM, Trends Neurosci 1993 16 4 141 7 10.1016/0166-2236(93)90122-3 7682347 (Pubitemid 23085470)
53. The pre/post LTP debate. Lisman J, Neuron 2009 63 3 281 284 10.1016/j.neuron.2009.07.020 19679068
54. A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Lisman J, Raghavachari S, Science's signal transduction knowledge environment 2006 2006 356 e11 re11 23437439
55. Synaptic anchorage of AMPA receptors by cadherins through neural plakophilin-related arm protein-AMPA receptor-binding protein complexes. Silverman JB, et al. J Neurosci 2007 27 32 8505 8516 10.1523/JNEUROSCI.1395-07. 2007 17687028 (Pubitemid 47254250)
56. Differential Palmitoylation Directs the AMPA Receptor-Binding Protein ABP to Spines or to Intracellular Clusters. DeSouza S, et al. J Neurosci 2002 22 9 3493 3503 11978826
57. Regulation of AMPA receptor trafficking by δ-catenin. Ochiishi T, et al. Mol Cell Neurosci 2008 39 4 499 507 10.1016/j.mcn.2008.06.002 18602475
58. Deletion of the neuron-specific protein delta-catenin leads to severe cognitive and synaptic dysfunction. Israely I, et al. Current biology: CB 2004 14 18 1657 63 10.1016/j.cub.2004.08.065 15380068 (Pubitemid 39239363)
59. Extracellular interactions between GluR2 and N-cadherin in spine regulation. Saglietti L, et al. Neuron 2007 54 3 461 77 10.1016/j.neuron.2007. 04.012 17481398 (Pubitemid 46659810)
60. GluA2 (GluR2) regulates metabotropic glutamate receptor-dependent long-term depression through N-cadherin-dependent and cofilin-mediated actin reorganization. Zhou Z, et al. The Journal of neuroscience: the official journal of the Society for Neuroscience 2011 31 3 819 33 10.1523/JNEUROSCI.3869-10.2011
61. Differential control of presynaptic efficacy by postsynaptic N-cadherin and [beta]-catenin. Vitureira N, et al. Nat Neurosci 2012 15 1 81 89
62. Presynaptic and postsynaptic Ca(2+) and CamKII contribute to long-term potentiation at synapses between individual CA3 neurons. Lu FM, Hawkins RD, Proc Natl Acad Sci USA 2006 103 11 4264 9 10.1073/pnas.0508162103 16537519
63. Differential control of presynaptic CaMKII activation and translocation to active zones. Shakiryanova D, et al. The Journal of neuroscience: the official journal of the Society for Neuroscience 2011 31 25 9093 100 10.1523/JNEUROSCI.0550-11.2011
64. Substrate-selective and calcium-independent activation of CaMKII by alpha-actinin. Jalan-Sakrikar N, et al. J Biol Chem 2012 287 19 15275 83 10.1074/jbc.M112.351817 22427672
65. Association of calcium/calmodulin-dependent kinase II with developmentally regulated splice variants of the postsynaptic density protein densin-180. Strack S, et al. J Biol Chem 2000 275 33 25061 4 10.1074/jbc.C000319200 10827168
66. Deletion of densin-180 results in abnormal behaviors associated with mental illness and reduces mGluR5 and DISC1 in the postsynaptic density fraction. Carlisle HJ, et al. The Journal of neuroscience: the official journal of the Society for Neuroscience 2011 31 45 16194 207 10.1523/JNEUROSCI.5877-10. 2011
67. Persistent Reversal of Enhanced Amphetamine Intake by Transient CaMKII Inhibition. Loweth JA, et al. The Journal of neuroscience: the official journal of the Society for Neuroscience 2013 33 4 1411 6 10.1523/JNEUROSCI.4386-13.2013
68. Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. Shen K, Meyer T, Science 1999 284 5411 162 6 10.1126/science.284.5411.162 10102820 (Pubitemid 29282073)
69. Kinase-dead knock-in mouse reveals an essential role of kinase activity of Ca2+/calmodulin-dependent protein kinase IIalpha in dendritic spine enlargement, long-term potentiation, and learning. Yamagata Y, et al. J Neurosci 2009 29 23 7607 7618 10.1523/JNEUROSCI.0707-09.2009 19515929
70. Nucleotides and phosphorylation bi-directionally modulate Ca2+/calmodulin-dependent protein kinase II (CaMKII) binding to the N-methyl-D-aspartate (NMDA) receptor subunit GluN2B. O'Leary H, et al. J Biol Chem 2011 286 36 31272 81 10.1074/jbc.M111.233668 21768120
71. Inducible protein knockout reveals temporal requirement of CaMKII reactivation for memory consolidation in the brain. Wang H, et al. Proc Natl Acad Sci USA 2003 100 7 4287 92 10.1073/pnas.0636870100 12646704 (Pubitemid 36418195)
72. Modulation of CaV2.1 channels by Ca2+/calmodulin-dependent protein kinase II bound to the C-terminal domain. Jiang X, et al. Proc Natl Acad Sci USA 2008 105 1 341 346 10.1073/pnas.0710213105 18162541
73. Phosphorylated CaMKII post-synaptic binding to NR2B subunits in the anterior cingulate cortex mediates visceral pain in visceral hypersensitive rats. Li Y, et al. J Neurochem 2012 121 4 662 671 10.1111/j.1471-4159.2012. 07717.x 22380661
74. Memory maintenance by PKMzeta-an evolutionary perspective. Sacktor T, Mol Brain 2012 5 1 31 31 10.1186/1756-6606-5-31 22986281
75. Persistent phosphorylation by protein kinase Mzeta maintains late-phase long-term potentiation. Serrano P, Yao Y, Sacktor T, J Neurosci 2005 25 8 1979 1984 10.1523/JNEUROSCI.5132-04.2005 15728837 (Pubitemid 40289402)
76. Storage of spatial information by the maintenance mechanism of LTP. Pastalkova E, et al. Science 2006 313 5790 1141 4 10.1126/science.1128657 16931766 (Pubitemid 44300243)
77. Cellular pharmacology of protein kinase Mζ (PKMζ) contrasts with its in vitro profile: implications for PKMζ as a mediator of memory. Wu-Zhang A, et al. J Biol Chem 2012 287 16 12879 12885 10.1074/jbc.M112.357244 22378786
78. Memory erasure by very high concentrations of ZIP may not be due to PKM-zeta. Lisman J, Hippocampus 2012 22 3 648 649 10.1002/hipo.20980 21956821
79. Matching biochemical and functional efficacies confirm ZIP as a potent competitive inhibitor of PKMζ in neurons. Yao Y, et al. Neuropharmacology 2013 64 37 44 22846225
80. PKM-zeta is not required for hippocampal synaptic plasticity, learning and memory. Volk LJ, et al. Nature 2013 493 7432 420 3 10.1038/nature11802 23283174
81. Tsokas P, et al Conditional knockout of the PKC/PKMζ gene in the adult mouse hippocampus prevents L-LTP. in 2012 Society for Neuroscience Meeting: New Orleans SfN: LA 2012
82. Distribution of Postsynaptic Density (PSD)-95 and Ca2+/Calmodulin- Dependent Protein Kinase II at the PSD. Petersen JD, et al. J Neurosci 2003 23 35 11270 11278 14657186 (Pubitemid 37548963)
83. Activity-dependent growth of new dendritic spines is regulated by the proteasome. Hamilton AM, et al. Neuron 2012 74 6 1023 30 10.1016/j.neuron.2012. 04.031 22726833