CaMKII: a molecular substrate for synaptic plasticity and memory.

Learning and memory is widely believed to result from changes in connectivity within neuronal circuits due to synaptic plasticity. Work over the past two decades has shown that Ca(2+) influx during LTP induction triggers the activation of CaMKII in dendritic spines. CaMKII activation results in autophosphorylation of the kinase rendering it constitutively active long after the Ca(2+) dissipates within the spine. This "molecular switch"(1) mechanism is essential for LTP and learning and memory. Here, we discuss this key regulatory mechanism and the diversity of downstream targets that can be modulated by CaMKII to exert dynamic control of synaptic structure and function.

[1]  H. Schulman,et al.  Inhibitory autophosphorylation of multifunctional Ca2+/calmodulin-dependent protein kinase analyzed by site-directed mutagenesis. , 1992, The Journal of biological chemistry.

[2]  Yan Hua Huang,et al.  Regulation of the NMDA Receptor Complex and Trafficking by Activity-Dependent Phosphorylation of the NR2B Subunit PDZ Ligand , 2004, The Journal of Neuroscience.

[3]  D. Surmeier,et al.  Kalirin-7 Controls Activity-Dependent Structural and Functional Plasticity of Dendritic Spines , 2007, Neuron.

[4]  J. Rostas,et al.  Phosphorylation of CaMKII at Thr253 occurs in vivo and enhances binding to isolated postsynaptic densities , 2006, Journal of neurochemistry.

[5]  J. H. Connor,et al.  Molecular memory by reversible translocation of calcium/calmodulin-dependent protein kinase II , 2000, Nature Neuroscience.

[6]  Michael J Higley,et al.  Calcium Signaling in Dendritic Spines , 2022 .

[7]  Yasushi Shigeri,et al.  Cytoplasmic Polyadenylation Element Binding Protein-Dependent Protein Synthesis Is Regulated by Calcium/Calmodulin-Dependent Protein Kinase II , 2004, The Journal of Neuroscience.

[8]  R. Nicoll,et al.  Activated CaMKII couples GluN2B and casein kinase 2 to control synaptic NMDA receptors. , 2013, Cell reports.

[9]  Y. Goda,et al.  Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy , 2008, Nature Reviews Neuroscience.

[10]  Dominique Muller,et al.  Increased Phosphorylation of Ca/Calmodulin-dependent Protein Kinase II and Its Endogenous Substrates in the Induction of Long Term Potentiation (*) , 1995, The Journal of Biological Chemistry.

[11]  K. Fukunaga,et al.  Ca2+– and Calmodulin‐Dependent Phosphorylation of Microtubule‐Associated Protein 2 and t Factor, and Inhibition of Microtubule Assembly , 1983, Journal of neurochemistry.

[12]  D. Choquet,et al.  A three-step model for the synaptic recruitment of AMPA receptors , 2011, Molecular and Cellular Neuroscience.

[13]  Roberto Malinow,et al.  Multiple Mechanisms for the Potentiation of AMPA Receptor-Mediated Transmission by α-Ca2+/Calmodulin-Dependent Protein Kinase II , 2002, The Journal of Neuroscience.

[14]  R. V. Omkumar,et al.  Regulation of Ca2+/calmodulin-dependent protein kinase II catalysis by N-methyl-D-aspartate receptor subunit 2B. , 2009, The Biochemical journal.

[15]  J. Isaac,et al.  Casein Kinase 2 Regulates the NR2 Subunit Composition of Synaptic NMDA Receptors , 2010, Neuron.

[16]  M. Waxham,et al.  Three-dimensional Reconstructions of Calcium/Calmodulin-dependent (CaM) Kinase IIα and Truncated CaM Kinase IIα Reveal a Unique Organization for Its Structural Core and Functional Domains* , 2000, The Journal of Biological Chemistry.

[17]  J. Lisman,et al.  A Model of Synaptic Memory A CaMKII/PP1 Switch that Potentiates Transmission by Organizing an AMPA Receptor Anchoring Assembly , 2001, Neuron.

[18]  Steven S. Vogel,et al.  Structural rearrangement of CaMKIIα catalytic domains encodes activation , 2009, Proceedings of the National Academy of Sciences.

[19]  Y. Goda,et al.  The actin cytoskeleton: integrating form and function at the synapse. , 2005, Annual review of neuroscience.

[20]  J E Lisman,et al.  Is persistent activity of calcium/calmodulin-dependent kinase required for the maintenance of LTP? , 2001, Journal of neurophysiology.

[21]  Paul De Koninck,et al.  Interaction with the NMDA receptor locks CaMKII in an active conformation , 2001, Nature.

[22]  Yasunori Hayashi,et al.  The roles of CaMKII and F-actin in the structural plasticity of dendritic spines: a potential molecular identity of a synaptic tag? , 2009, Physiology.

[23]  R. Colbran,et al.  Multivalent Interactions of Calcium/Calmodulin-dependent Protein Kinase II with the Postsynaptic Density Proteins NR2B, Densin-180, and α-Actinin-2* , 2005, Journal of Biological Chemistry.

[24]  S Mukherji,et al.  Mutational analysis of secondary structure in the autoinhibitory and autophosphorylation domains of calmodulin kinase II. , 1994, The Journal of biological chemistry.

[25]  S. Shenolikar,et al.  Long-Term Potentiation Induced by θ Frequency Stimulation Is Regulated by a Protein Phosphatase-1-Operated Gate , 2000, The Journal of Neuroscience.

[26]  Andreas Lüthi,et al.  Modulation of AMPA receptor unitary conductance by synaptic activity , 1998, Nature.

[27]  J. Grotta,et al.  Calcium/Calmodulin‐Dependent Protein Kinase II Activity in Focal Ischemia With Reperfusion in Rats , 1994, Stroke.

[28]  S. Carr,et al.  Cell Cycle Regulation of Myosin-V by Calcium/Calmodulin-Dependent Protein Kinase II , 2001, Science.

[29]  D. Lovinger,et al.  Translocation of Autophosphorylated Calcium/Calmodulin-dependent Protein Kinase II to the Postsynaptic Density* , 1997, The Journal of Biological Chemistry.

[30]  R. Colbran,et al.  Differential Modulation of Ca2+/Calmodulin-dependent Protein Kinase II Activity by Regulated Interactions with N-Methyl-D-aspartate Receptor NR2B Subunits and α-Actinin* , 2005, Journal of Biological Chemistry.

[31]  R. Huganir,et al.  Characterization of Multiple Phosphorylation Sites on the AMPA Receptor GluR1 Subunit , 1996, Neuron.

[32]  D. Tabb,et al.  Identification and Validation of Novel Spinophilin-associated Proteins in Rodent Striatum Using an Enhanced ex Vivo Shotgun Proteomics Approach* , 2010, Molecular & Cellular Proteomics.

[33]  R. Colbran,et al.  Autophosphorylation-dependent Targeting of Calcium/ Calmodulin-dependent Protein Kinase II by the NR2B Subunit of theN-Methyl- d-aspartate Receptor* , 1998, The Journal of Biological Chemistry.

[34]  John Kuriyan,et al.  Intersubunit capture of regulatory segments is a component of cooperative CaMKII activation , 2010, Nature Structural &Molecular Biology.

[35]  H. Schulman,et al.  Calmodulin Trapping by Calcium-Calmodulin-Dependent Protein Kinase , 1992, Science.

[36]  M. Kennedy,et al.  A Synaptic Ras-GTPase Activating Protein (p135 SynGAP) Inhibited by CaM Kinase II , 1998, Neuron.

[37]  Alcino J. Silva,et al.  Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. , 1992, Science.

[38]  Suzanne Paradis,et al.  The Rac1-GEF Tiam1 Couples the NMDA Receptor to the Activity-Dependent Development of Dendritic Arbors and Spines , 2005, Neuron.

[39]  Stephen G. Miller,et al.  Sequences of autophosphorylation sites in neuronal type II CaM kinase that control Ca2+-independent activity , 1988, Neuron.

[40]  M. di Luca,et al.  Hippocampal Synaptic Plasticity Involves Competition between Ca2+/Calmodulin-Dependent Protein Kinase II and Postsynaptic Density 95 for Binding to the NR2A Subunit of the NMDA Receptor , 2001, The Journal of Neuroscience.

[41]  Hongbo Yu,et al.  Experience-dependent regulation of CaMKII activity within single visual cortex synapses in vivo , 2011, Proceedings of the National Academy of Sciences.

[42]  T. Soderling,et al.  Calcium/calmodulin-independent autophosphorylation sites of calcium/calmodulin-dependent protein kinase II. Studies on the effect of phosphorylation of threonine 305/306 and serine 314 on calmodulin binding using synthetic peptides. , 1990, The Journal of biological chemistry.

[43]  M. Bear,et al.  Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity , 2000, Nature.

[44]  C. Hansel,et al.  βCaMKII controls the direction of plasticity at parallel fiber–Purkinje cell synapses , 2009, Nature Neuroscience.

[45]  T. Reese,et al.  Inhibition of Endogenous Phosphatase in a Postsynaptic Density Fraction Allows Extensive Phosphorylation of the Major Postsynaptic Density Protein , 1993, Journal of neurochemistry.

[46]  Leslie C Griffith,et al.  A structural mechanism for maintaining the ‘on‐state’ of the CaMKII memory switch in the post‐synaptic density , 2007, Journal of neurochemistry.

[47]  I. Efimov,et al.  Diabetes increases mortality after myocardial infarction by oxidizing CaMKII. , 2013, The Journal of clinical investigation.

[48]  A. Miyawaki,et al.  Visualization of Synaptic Ca2+ /Calmodulin-Dependent Protein Kinase II Activity in Living Neurons , 2005, The Journal of Neuroscience.

[49]  T. Soderling,et al.  Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. , 1997, Science.

[50]  S. Shenolikar,et al.  Gating of CaMKII by cAMP-regulated protein phosphatase activity during LTP. , 1998, Science.

[51]  Alcino J. Silva,et al.  Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. , 1998, Science.

[52]  M. Kennedy,et al.  Distinct forebrain and cerebellar isozymes of type II Ca2+/calmodulin-dependent protein kinase associate differently with the postsynaptic density fraction. , 1985, The Journal of biological chemistry.

[53]  Mark J. Thomas,et al.  Behavioral and Structural Responses to Chronic Cocaine Require a Feedforward Loop Involving ΔFosB and Calcium/Calmodulin-Dependent Protein Kinase II in the Nucleus Accumbens Shell , 2013, The Journal of Neuroscience.

[54]  M K Smith,et al.  Calcium/calmodulin-dependent protein kinase II. , 1989, The Biochemical journal.

[55]  T. Soderling,et al.  Identification of the Ca2+/Calmodulin-dependent Protein Kinase II Regulatory Phosphorylation Site in the α-Amino-3-hydroxyl-5-methyl4-isoxazole-propionate-type Glutamate Receptor* , 1997, The Journal of Biological Chemistry.

[56]  Paul De Koninck,et al.  Transition from Reversible to Persistent Binding of CaMKII to Postsynaptic Sites and NR2B , 2006, The Journal of Neuroscience.

[57]  A. Nairn,et al.  Multisite phosphorylation of microtubule-associated protein 2 (MAP-2) in rat brain: Peptide mapping distinguishes between cyclic AMP-, calcium/calmodulin-, and calcium/phospholipid-regulated phosphorylation mechanisms , 2008, Journal of Molecular Neuroscience.

[58]  M K Bennett,et al.  Purification and characterization of a calmodulin-dependent protein kinase that is highly concentrated in brain. , 1983, The Journal of biological chemistry.

[59]  B. Barylko,et al.  Regulation of the Proteasome by Neuronal Activity and Calcium/Calmodulin-dependent Protein Kinase II* , 2009, The Journal of Biological Chemistry.

[60]  D. Johnston,et al.  Calcium–Calmodulin-Dependent Kinase II Modulates Kv4.2 Channel Expression and Upregulates Neuronal A-Type Potassium Currents , 2004, The Journal of Neuroscience.

[61]  H. Schulman,et al.  Functional Implications of the Subunit Composition of Neuronal CaM Kinase II* , 1999, The Journal of Biological Chemistry.

[62]  Nils Z. Borgesius,et al.  βCaMKII Plays a Nonenzymatic Role in Hippocampal Synaptic Plasticity and Learning by Targeting αCaMKII to Synapses , 2011, The Journal of Neuroscience.

[63]  M. Kennedy,et al.  Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[64]  T. Soderling,et al.  Autophosphorylation of Ca2+/calmodulin-dependent protein kinase II. Effects on total and Ca2+-independent activities and kinetic parameters. , 1987, The Journal of biological chemistry.

[65]  E. Kandel,et al.  Chromatin Acetylation, Memory, and LTP Are Impaired in CBP+/− Mice A Model for the Cognitive Deficit in Rubinstein-Taybi Syndrome and Its Amelioration , 2004, Neuron.

[66]  Mark E. Anderson,et al.  The multifunctional Ca2+/calmodulin-dependent kinase II regulates vascular smooth muscle migration through matrix metalloproteinase 9. , 2012, American journal of physiology. Heart and circulatory physiology.

[67]  C. Hoogenraad,et al.  The postsynaptic architecture of excitatory synapses: a more quantitative view. , 2007, Annual review of biochemistry.

[68]  Quan-guang Zhang,et al.  Autophosphorylated calcium/calmodulin-dependent protein kinase IIα (CaMKIIα) reversibly targets to and phosphorylates N-methyl-d-aspartate receptor subunit 2B (NR2B) in cerebral ischemia and reperfusion in hippocampus of rats , 2003, Brain Research.

[69]  C. McMurray,et al.  Calmodulin Kinase II Attenuation of Gene Transcription by Preventing cAMP Response Element-binding Protein (CREB) Dimerization and Binding of the CREB-binding Protein* , 2001, The Journal of Biological Chemistry.

[70]  R. Yasuda,et al.  AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK–dependent manner during long-term potentiation , 2010, Proceedings of the National Academy of Sciences.

[71]  D. Clapham,et al.  SynGAP-MUPP1-CaMKII Synaptic Complexes Regulate p38 MAP Kinase Activity and NMDA Receptor- Dependent Synaptic AMPA Receptor Potentiation , 2004, Neuron.

[72]  J. M. Bradshaw,et al.  Chemical Quenched Flow Kinetic Studies Indicate an Intraholoenzyme Autophosphorylation Mechanism for Ca2+/Calmodulin-dependent Protein Kinase II* , 2002, The Journal of Biological Chemistry.

[73]  S. Raghavachari,et al.  Quantitative estimates of the cytoplasmic, PSD, and NMDAR-bound pools of CaMKII in dendritic spines , 2011, Brain Research.

[74]  R. Nicoll,et al.  Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Mark E. Anderson,et al.  Oxidation of CaMKII determines the cardiotoxic effects of aldosterone , 2011, Nature Medicine.

[76]  R. Tsien,et al.  Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. , 1989, Science.

[77]  Isabelle M. Mansuy,et al.  Protein phosphatase 1 is a molecular constraint on learning and memory , 2002, Nature.

[78]  Chris I. De Zeeuw,et al.  αCaMKII Is Essential for Cerebellar LTD and Motor Learning , 2006, Neuron.

[79]  M. Kennedy,et al.  SynGAP Regulates Steady-State and Activity-Dependent Phosphorylation of Cofilin , 2008, The Journal of Neuroscience.

[80]  P. De Koninck,et al.  Interaction Between αCaMKII and GluN2B Controls ERK-Dependent Plasticity , 2012, The Journal of Neuroscience.

[81]  J. Sweatt,et al.  ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning. , 2006, Learning & memory.

[82]  Niels Voigt,et al.  Oxidized CaMKII causes cardiac sinus node dysfunction in mice. , 2011, The Journal of clinical investigation.

[83]  T. Hirano,et al.  Gating of long‐term depression by Ca2+/calmodulin‐dependent protein kinase II through enhanced cGMP signalling in cerebellar Purkinje cells , 2013, The Journal of physiology.

[84]  Karl Peter Giese,et al.  Inhibitory Autophosphorylation of CaMKII Controls PSD Association, Plasticity, and Learning , 2002, Neuron.

[85]  T Yamauchi,et al.  Structural features of Ca2+/calmodulin-dependent protein kinase II revealed by electron microscopy , 1991, The Journal of cell biology.

[86]  A. Ikai,et al.  Role of threonine-286 as autophosphorylation site for appearance of Ca2(+)-independent activity of calmodulin-dependent protein kinase II alpha subunit. , 1991, Journal of Biochemistry (Tokyo).

[87]  D. Choquet,et al.  CaMKII Triggers the Diffusional Trapping of Surface AMPARs through Phosphorylation of Stargazin , 2010, Neuron.

[88]  K. Shen,et al.  Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation. , 1999, Science.

[89]  Nils Brose,et al.  CaMKII binding to GluN2B is critical during memory consolidation , 2012, The EMBO journal.

[90]  R. Nicoll,et al.  Bidirectional Synaptic Plasticity Regulated by Phosphorylation of Stargazin-like TARPs , 2005, Neuron.

[91]  R. Malinow,et al.  Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. , 2000, Science.

[92]  J. Hell,et al.  Calcium/calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[93]  J. Hell,et al.  Activity-Dependent Growth of New Dendritic Spines Is Regulated by the Proteasome , 2012, Neuron.

[94]  M. Sheng,et al.  Autophosphorylated CaMKIIα Acts as a Scaffold to Recruit Proteasomes to Dendritic Spines , 2010, Cell.

[95]  Magdalena G. Wutte,et al.  Calcium/Calmodulin-Dependent Protein Kinase II Mediates Group I Metabotropic Glutamate Receptor-Dependent Protein Synthesis and Long-Term Depression in Rat Hippocampus , 2011, The Journal of Neuroscience.

[96]  M. Luca,et al.  CaMKII-dependent Phosphorylation Regulates SAP97/NR2A Interaction* , 2003, Journal of Biological Chemistry.

[97]  R. Colbran,et al.  Differential association of postsynaptic signaling protein complexes in striatum and hippocampus , 2013, Journal of neurochemistry.

[98]  J. Lisman A mechanism for memory storage insensitive to molecular turnover: a bistable autophosphorylating kinase. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[99]  R. V. Omkumar,et al.  Calcium/Calmodulin Dependent Protein Kinase II Bound to NMDA Receptor 2B Subunit Exhibits Increased ATP Affinity and Attenuated Dephosphorylation , 2011, PloS one.

[100]  Paul De Koninck,et al.  CaMKII control of spine size and synaptic strength: Role of phosphorylation states and nonenzymatic action , 2010, Proceedings of the National Academy of Sciences.

[101]  Eric C. Griffith,et al.  Brain-Specific Phosphorylation of MeCP2 Regulates Activity-Dependent Bdnf Transcription, Dendritic Growth, and Spine Maturation , 2006, Neuron.

[102]  R. Huganir,et al.  Mechanism of Ca2+/calmodulin-dependent kinase II regulation of AMPA receptor gating , 2011, Nature Neuroscience.

[103]  Alcino J. Silva,et al.  Interactions between the NR2B Receptor and CaMKII Modulate Synaptic Plasticity and Spatial Learning , 2007, The Journal of Neuroscience.

[104]  R. Malinow,et al.  NMDA Receptor Subunit Composition Controls Synaptic Plasticity by Regulating Binding to CaMKII , 2005, Neuron.

[105]  V. Derkach Zooming in on AMPA receptor regulation by CaMKII , 2011, Nature Neuroscience.

[106]  Tobias Meyer,et al.  CaMKIIβ Functions As an F-Actin Targeting Module that Localizes CaMKIIα/β Heterooligomers to Dendritic Spines , 1998, Neuron.

[107]  Guangyi Zhang,et al.  Autophosphorylated calcium/calmodulin-dependent protein kinase II α induced by cerebral ischemia immediately targets and phosphorylates N-methyl-d-aspartate receptor subunit 2B (NR2B) in hippocampus of rats , 2002, Neuroscience Letters.

[108]  R. Tsien,et al.  α- and βCaMKII Inverse Regulation by Neuronal Activity and Opposing Effects on Synaptic Strength , 2002, Neuron.

[109]  Andy Hudmon,et al.  Neuronal CA2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function. , 2002, Annual review of biochemistry.

[110]  Jay T. Groves,et al.  A Mechanism for Tunable Autoinhibition in the Structure of a Human Ca2+/Calmodulin- Dependent Kinase II Holoenzyme , 2011, Cell.

[111]  K. Mackie,et al.  CaMKII is a novel regulator of diacylglycerol lipase-α and striatal endocannabinoid signaling , 2013, Nature Neuroscience.

[112]  R. Colbran,et al.  Substrate-selective and Calcium-independent Activation of CaMKII by α-Actinin* , 2012, The Journal of Biological Chemistry.

[113]  Tobias Meyer,et al.  Selective Regulation of Neurite Extension and Synapse Formation by the β but not the α Isoform of CaMKII , 2003, Neuron.

[114]  Seok-Jin R. Lee,et al.  Activation of CaMKII in single dendritic spines during long-term potentiation , 2009, Nature.

[115]  M. Passafaro,et al.  Motor protein–dependent transport of AMPA receptors into spines during long-term potentiation , 2008, Nature Neuroscience.

[116]  R. Colbran,et al.  Inactivation of Ca2+/calmodulin-dependent protein kinase II by basal autophosphorylation. , 1993, The Journal of biological chemistry.

[117]  C. Hoogenraad,et al.  Relative and Absolute Quantification of Postsynaptic Density Proteome Isolated from Rat Forebrain and Cerebellum*S , 2006, Molecular & Cellular Proteomics.

[118]  M E Greenberg,et al.  Stimulation of protein tyrosine phosphorylation by NMDA receptor activation , 1991, Science.

[119]  J. Exton,et al.  Phospholipase C‐γ, protein kinase C and Ca2+/calmodulin‐dependent protein kinase II are involved in platelet‐derived growth factor‐induced phosphorylation of Tiam1 , 1998, FEBS letters.

[120]  J. Hell,et al.  Regulation of Calcium/Calmodulin-dependent Protein Kinase II Docking toN-Methyl-d-aspartate Receptors by Calcium/Calmodulin and α-Actinin* , 2002, The Journal of Biological Chemistry.

[121]  K. Svoboda,et al.  The Life Cycle of Ca2+ Ions in Dendritic Spines , 2002, Neuron.

[122]  John Lisman,et al.  Role of the CaMKII/NMDA Receptor Complex in the Maintenance of Synaptic Strength , 2011, The Journal of Neuroscience.

[123]  Alastair M. Hosie,et al.  Identification of the Sites for CaMK-II-dependent Phosphorylation of GABAA Receptors* , 2007, Journal of Biological Chemistry.

[124]  Mark F. Bear,et al.  Internalization of ionotropic glutamate receptors in response to mGluR activation , 2001, Nature Neuroscience.

[125]  Alcino J. Silva,et al.  Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. , 1992, Science.

[126]  Roberto Malinow,et al.  Subunit-Specific Rules Governing AMPA Receptor Trafficking to Synapses in Hippocampal Pyramidal Neurons , 2001, Cell.

[127]  Wen Hwa Lee,et al.  Structure of the CaMKIIδ/Calmodulin Complex Reveals the Molecular Mechanism of CaMKII Kinase Activation , 2010, PLoS biology.

[128]  R. Colbran,et al.  Characterization of a Central Ca2+/Calmodulin-dependent Protein Kinase IIα/β Binding Domain in Densin That Selectively Modulates Glutamate Receptor Subunit Phosphorylation* , 2011, The Journal of Biological Chemistry.

[129]  Justin Toupin,et al.  Electrical stimulation protocols for hippocampal synaptic plasticity and neuronal hyper-excitability: Are they effective or relevant? , 2007, Experimental Neurology.

[130]  K. Fukunaga,et al.  Dephosphorylation of autophosphorylated Ca2+/calmodulin-dependent protein kinase II by protein phosphatase 2C. , 1993, The Journal of biological chemistry.

[131]  Stefan Strack,et al.  Mechanism and Regulation of Calcium/Calmodulin-dependent Protein Kinase II Targeting to the NR2B Subunit of the N-Methyl-d-aspartate Receptor* , 2000, The Journal of Biological Chemistry.

[132]  Yasunori Hayashi,et al.  The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure , 2007, Proceedings of the National Academy of Sciences.

[133]  P. Greengard,et al.  A calcium/calmodulin-dependent protein kinase from mammalian brain that phosphorylates Synapsin I: partial purification and characterization , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[134]  R. Huganir,et al.  Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus. , 2010, Journal of neurophysiology.

[135]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

[136]  T. Soderling,et al.  Bidirectional Regulation of Cytoplasmic Polyadenylation Element-Binding Protein Phosphorylation by Ca2+/Calmodulin-Dependent Protein Kinase II and Protein Phosphatase 1 during Hippocampal Long-Term Potentiation , 2005, The Journal of Neuroscience.

[137]  Paul Matthews,et al.  Bi-directional modulation of AMPA receptor unitary conductance by synaptic activity , 2004, BMC Neuroscience.

[138]  R. Colbran,et al.  Targeting of calcium/calmodulin-dependent protein kinase II. , 2004, The Biochemical journal.

[139]  S. Moss,et al.  Differential phosphorylation of intracellular domains of gamma-aminobutyric acid type A receptor subunits by calcium/calmodulin type 2-dependent protein kinase and cGMP-dependent protein kinase. , 1994, The Journal of biological chemistry.

[140]  Mary B. Kennedy,et al.  The postsynaptic density at glutamatergic synapses , 1997, Trends in Neurosciences.

[141]  R. Malinow,et al.  Ras and Rap Control AMPA Receptor Trafficking during Synaptic Plasticity , 2002, Cell.

[142]  J. López-Barneo,et al.  High External Potassium Induces an Increase in the Phosphorylation of the Cytoskeletal Protein MAP2 in Rat Hippocampal Slices , 1993, The European journal of neuroscience.

[143]  E. Gratton,et al.  Genetically encoded probe for fluorescence lifetime imaging of CaMKII activity. , 2008, Biochemical and biophysical research communications.

[144]  T. Furihata,et al.  Characterization of a Novel synGAP Isoform, synGAP-β* , 2001, The Journal of Biological Chemistry.

[145]  Mark E. Anderson,et al.  A Dynamic Pathway for Calcium-Independent Activation of CaMKII by Methionine Oxidation , 2008, Cell.

[146]  E. M. Espreafico,et al.  Brain Myosin-V, a Calmodulin-carrying Myosin, Binds to Calmodulin-dependent Protein Kinase II and Activates Its Kinase Activity* , 1999, The Journal of Biological Chemistry.

[147]  R. Colbran,et al.  Loss of Thr286 phosphorylation disrupts synaptic CaMKIIα targeting, NMDAR activity and behavior in pre-adolescent mice , 2011, Molecular and Cellular Neuroscience.

[148]  K. Svoboda,et al.  Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. , 1999, Science.

[149]  Leslie C. Griffith Calcium/Calmodulin-Dependent Protein Kinase II: An Unforgettable Kinase , 2004, The Journal of Neuroscience.

[150]  P. Kelly,et al.  Identification of protein phosphatase 1 in synaptic junctions: dephosphorylation of endogenous calmodulin-dependent kinase II and synapse-enriched phosphoproteins , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[151]  D. Muller,et al.  Long-term potentiation is associated with an increased activity of Ca2+/calmodulin-dependent protein kinase II. , 1993, The Journal of biological chemistry.

[152]  Paul De Koninck,et al.  Autonomous CaMKII Can Promote either Long-Term Potentiation or Long-Term Depression, Depending on the State of T305/T306 Phosphorylation , 2010, The Journal of Neuroscience.