Synaptic memory requires CaMKII
Open accessAbstract
Long-term potentiation (LTP) is arguably the most compelling cellular model for learning and memory. While the mechanisms underlying the induction of LTP (‘learning’) are well understood, the maintenance of LTP (‘memory’) has remained contentious over the last 20 years. Here, we find that Ca 2+ -calmodulin-dependent kinase II (CaMKII) contributes to synaptic transmission and is required LTP maintenance. Acute inhibition of CaMKII erases LTP and transient inhibition of CaMKII enhances subsequent LTP. These findings strongly support the role of CaMKII as a molecular storage device.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The slow time course of inhibition is not due to slow access of the inhibitors to the site of action, since paAIP2 acts within seconds and has the same slow time course.
“The slow time course is not due to slow access of the inhibitors to the site of action, since paAIP2, a photoactivatable peptide inhibitor (203) that acts within seconds of light exposure, has the same slow time course (361).”
From Synaptic memory and CaMKII (2023) · cites this paper as [361]
In Results (Blocking CaMKII inhibits synaptic transmission; page not specified), blue light rapidly exposes paAIP2, yet inhibition develops slowly, with kinetics similar to myr-CN27 and myr-AIP. The authors say this *suggests* slow access is not the cause; the citing sentence states that conclusion as fact. The copy describes rapid activation but does not specify that paAIP2 acts within seconds. (LLM, conf=0.85)
Experimental — accuracy not yet measuredTransiently inhibiting CaMKII and reducing baseline transmission results in a larger magnitude of LTP.
“Thus, if one were to transiently inhibit CaMKII and reduce baseline transmission, the magnitude of LTP should be larger. Again, experiments confirm this prediction (361).”
From Synaptic memory and CaMKII (2023) · cites this paper as [361]
Chelating postsynaptic Ca2+ has no effect on CaMKII constitutive activity.
“Chelating postsynaptic Ca2+ has no effect on this CaMKII constitutive activity (361).”
From Synaptic memory and CaMKII (2023) · cites this paper as [361]
After transient inhibition of CaMKII with the photoactivatable inhibitor paAIP2, there is no recovery of synaptic responses.
“After the transient inhibition of CaMKII with the photoactivatable inhibitor (paAIP2) (203), there is no recovery (361).”
From Synaptic memory and CaMKII (2023) · cites this paper as [361]
Deleting NMDARs in individual neurons or replacing GluN1 with a pore-dead mutant in utero, thus preventing NMDAR-dependent LTP, prevents generation of constitutive CaMKII activity.
“Deleting NMDARs in individual neurons or replacing GluN1 with a pore-dead mutant in utero, thus preventing NMDAR-dependent LTP, should prevent generation of constitutive CaMKII activity. This indeed is the case (361).”
From Synaptic memory and CaMKII (2023) · cites this paper as [361]
The higher concentrations of inhibitor that do reverse LTP could result from the displacement of GluN2B bound to CaMKII.
“The higher concentrations of inhibitor that do reverse LTP (154, 361) could result from the displacement of GluN2B bound to CaMKII.”
From Synaptic memory and CaMKII (2023) · cites this paper as [361]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Bienenstock, E., Cooper, L., & Munro, P. (1982) · The Journal of Neuroscience · doi:10.1523/jneurosci.02-01-00032.1982 · Cited by 2,896 · see citing works
AMPA Receptor Trafficking and Synaptic Plasticity
Malinow, R., & Malenka, R. C. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142758 · Cited by 2,588 · see citing works
Mechanisms of CaMKII action in long-term potentiation
Lisman, J., Yasuda, R., & Raghavachari, S. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3192 · Cited by 1,134 · see citing works
Involvement of a calcineurin/ inhibitor-1 phosphatase cascade in hippocampal long-term depression
Mulkey, R. M., Endo, S., Shenolikar, S., & Malenka, R. C. (1994) · Nature · doi:10.1038/369486a0 · Cited by 1,083 · see citing works
Long-term depression in the CNS
Collingridge, G. L., Peineau, S., Howland, J. G., & Wang, Y. T. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2867 · Cited by 926 · see citing works
Interaction with the NMDA receptor locks CaMKII in an active conformation
Bayer, K.-U., De Koninck, P., Leonard, A. S., Hell, J. W., & Schulman, H. (2001) · Nature · doi:10.1038/35081080 · Cited by 732 · see citing works
Estimating Intracellular Calcium Concentrations and Buffering without Wavelength Ratioing
Maravall, M., Mainen, Z. F., Sabatini, B. L., & Svoboda, K. (2000) · Biophysical Journal · doi:10.1016/s0006-3495(00)76809-3 · Cited by 416 · see citing works
The BCM theory of synapse modification at 30: interaction of theory with experiment
Cooper, L. N., & Bear, M. F. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3353 · Cited by 395 · see citing works
Pettit, D. L., Perlman, S., & Malinow, R. (1994) · Science · doi:10.1126/science.7997883 · Cited by 329 · see citing works
Synaptic Signaling in Learning and Memory
Kennedy, M. B. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016824 · Cited by 270 · see citing works
Poncer, J. C., Esteban, J. A., & Malinow, R. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-11-04406.2002 · Cited by 177 · see citing works
Buard, I., Coultrap, S. J., Freund, R. K., Lee, Y.-S., Dell'Acqua, M. L., Silva, A. J., & Bayer, K. U. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1469-10.2010 · Cited by 160 · see citing works
Is Persistent Activity of Calcium/Calmodulin-Dependent Kinase Required for the Maintenance of LTP?
Chen, H.-X., Otmakhov, N., Strack, S., Colbran, R. J., & Lisman, J. E. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.85.4.1368 · Cited by 126 · see citing works
DAPK1 Mediates LTD by Making CaMKII/GluN2B Binding LTP Specific
Goodell, D. J., Zaegel, V., Coultrap, S. J., Hell, J. W., & Bayer, K. U. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.05.068 · Cited by 88 · see citing works
CA1 Long-Term Potentiation Is Diminished but Present in Hippocampal Slices from α-CaMKII Mutant Mice
Hinds, H. L., Tonegawa, S., & Malinow, R. (1998) · Learning & Memory · doi:10.1101/lm.5.4.344 · Cited by 86 · see citing works
Ishida, A., Shigeri, Y., Tatsu, Y., Uegaki, K., Kameshita, I., Okuno, S., Kitani, T., Yumoto, N., & Fujisawa, H. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00405-0 · Cited by 64 · see citing works
Flagged first, then by citations
Research works printed but not linked: 78
- Achterberg KG Buitendijk GHS Kool MJ Goorden SMI Post L Slump DE Silva AJ van Woerden GM Kushner SA Elgersma Y 2014 Temporal and region-specific requirements of αCaMKII in spatial and contextual learning The Journal of Neuroscience 34 11180 11187 10.1523/JNEUROSCI.0640-14.2014 25143599 PMC4340969 · DOI · Paper page
- Allen JK Brock DJ Kondow-McConaghy HM Pellois JP 2018 Efficient Delivery of Macromolecules into Human Cells by Improving the Endosomal Escape Activity of Cell-Penetrating Peptides: Lessons Learned from dfTAT and its Analogs Biomolecules 8 E50 10.3390/biom8030050 29997347 PMC6165022 · DOI
- Amin JB Salussolia CL Chan K Regan MC Dai J Zhou HX Furukawa H Bowen ME Wollmuth LP 2017 Divergent roles of a peripheral transmembrane segment in AMPA and NMDA receptors The Journal of General Physiology 149 661 680 10.1085/jgp.201711762 28507080 PMC5460951 · DOI
- Barcomb K Hell JW Benke TA Bayer KU 2016 The CaMKII/GluN2B Protein Interaction Maintains Synaptic Strength The Journal of Biological Chemistry 291 16082 16089 10.1074/jbc.M116.734822 27246855 PMC4965558 · DOI
- Bayer KU LeBel E McDonald GL O’Leary H Schulman H De Koninck P 2006 Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B The Journal of Neuroscience 26 1164 1174 10.1523/JNEUROSCI.3116-05.2006 16436603 PMC2890238 · DOI
- Bayer KU Schulman H 2019 CaM Kinase: Still Inspiring at 40 Neuron 103 380 394 10.1016/j.neuron.2019.05.033 31394063 PMC6688632 · DOI
- Benfenati F Valtorta F Rubenstein JL Gorelick FS Greengard P Czernik AJ 1992 Synaptic vesicle-associated Ca2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I Nature 359 417 420 10.1038/359417a0 1328883 · DOI
- Bhattacharyya M Stratton MM Going CC McSpadden ED Huang Y Susa AC Elleman A Cao YM Pappireddi N Burkhardt P Gee CL Barros T Schulman H Williams ER Kuriyan J 2016 Molecular mechanism of activation-triggered subunit exchange in Ca2+/calmodulin-dependent protein kinase II eLife 5 e13405 10.7554/eLife.13405 26949248 PMC4859805 · DOI · Paper page
- Bhattacharyya M Karandur D Kuriyan J 2020 Structural Insights into the Regulation of Ca 2+ /Calmodulin-Dependent Protein Kinase II (CaMKII) Cold Spring Harbor Perspectives in Biology 12 a035147 10.1101/cshperspect.a035147 31653643 PMC7263085 · DOI · Paper page
- Bird TD Plum F 1968 Recovery from barbiturate overdose coma with a prolonged isoelectric electroencephalogram Neurology 18 456 460 10.1212/wnl.18.5.456 5691172 · DOI · Paper page
- Cajal SR 1911 Histologie Du Systeme Nerveux de l’Homme et Des Vertebres Translated New York Oxford University Press 10.5962/bhl.title.48637 · DOI
- Chang BH Mukherji S Soderling TR 1998 Characterization of a calmodulin kinase II inhibitor protein in brain PNAS 95 10890 10895 10.1073/pnas.95.18.10890 9724800 PMC27991 · DOI · Paper page
- Chang BH Mukherji S Soderling TR 2001 Calcium/calmodulin-dependent protein kinase II inhibitor protein: localization of isoforms in rat brain Neuroscience 102 767 777 10.1016/S0306-4522(00)00520-0 11182241 · DOI · Paper page
- Cheriyan J Kumar P Mayadevi M Surolia A Omkumar RV Linden R 2011 Calcium/Calmodulin Dependent Protein Kinase II Bound to NMDA Receptor 2B Subunit Exhibits Increased ATP Affinity and Attenuated Dephosphorylation PLOS ONE 6 e16495 10.1371/journal.pone.0016495 21423658 PMC3057968 · DOI
- Choquet D 2018 Linking Nanoscale Dynamics of AMPA Receptor Organization to Plasticity of Excitatory Synapses and Learning The Journal of Neuroscience 38 9318 9329 10.1523/JNEUROSCI.2119-18.2018 30381423 PMC6705996 · DOI · Paper page
- Collingridge GL Isaac JT Wang YT 2004 Receptor trafficking and synaptic plasticity Nature Reviews. Neuroscience 5 952 962 10.1038/nrn1556 15550950 · DOI · Paper page
- Coultrap SJ Bayer KU 2012 CaMKII regulation in information processing and storage Trends in Neurosciences 35 607 618 10.1016/j.tins.2012.05.003 22717267 PMC3461103 · DOI
- Coultrap SJ Freund RK O’Leary H Sanderson JL Roche KW Dell’Acqua ML Bayer KU 2014 Autonomous CaMKII mediates both LTP and LTD using a mechanism for differential substrate site selection Cell Reports 6 431 437 10.1016/j.celrep.2014.01.005 24485660 PMC3930569 · DOI · Paper page
- Davies SN Martin D Millar JD Aram JA Church J Lodge D 1988 Differences in results from in vivo and in vitro studies on the use-dependency of N-methylaspartate antagonism by MK-801 and other phencyclidine receptor ligands European Journal of Pharmacology 145 141 151 10.1016/0014-2999(88)90225-7 2832187 · DOI
- Dore K Aow J Malinow R 2016 The Emergence of NMDA Receptor Metabotropic Function: Insights from Imaging Frontiers in Synaptic Neuroscience 8 20 10.3389/fnsyn.2016.00020 27516738 PMC4963461 · DOI
- D’Esposito M Postle BR 2015 The cognitive neuroscience of working memory Annual Review of Psychology 66 115 142 10.1146/annurev-psych-010814-015031 25251486 PMC4374359 · DOI · Paper page
- Feng TP 1995 The involvement of PKC and multifunctional CaM kinase II of the postsynaptic neuron in induction and maintenance of long-term potentiation Progress in Brain Research 105 55 63 10.1016/s0079-6123(08)63283-5 7568897 · DOI · Paper page
- Fusi S Drew PJ Abbott LF 2005 Cascade models of synaptically stored memories Neuron 45 599 611 10.1016/j.neuron.2005.02.001 15721245 · DOI · Paper page
- Giese KP Fedorov NB Filipkowski RK Silva AJ 1998 Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning Science 279 870 873 10.1126/science.279.5352.870 9452388 · DOI · Paper page
- Goold CP Nicoll RA 2010 Single-cell optogenetic excitation drives homeostatic synaptic depression Neuron 68 512 528 10.1016/j.neuron.2010.09.020 21040851 PMC3111089 · DOI · Paper page
- Gouet C Aburto B Vergara C Sanhueza M 2012 On the mechanism of synaptic depression induced by CaMKIIN, an endogenous inhibitor of CaMKII PLOS ONE 7 e49293 10.1371/journal.pone.0049293 23145145 PMC3493544 · DOI
- Granger AJ Shi Y Lu W Cerpas M Nicoll RA 2013 LTP requires a reserve pool of glutamate receptors independent of subunit type Nature 493 495 500 10.1038/nature11775 23235828 PMC3998843 · DOI · Paper page
- Hell JW 2014 CaMKII: claiming center stage in postsynaptic function and organization Neuron 81 249 265 10.1016/j.neuron.2013.12.024 24462093 PMC4570830 · DOI
- Hinds HL Goussakov I Nakazawa K Tonegawa S Bolshakov VY 2003 Essential function of alpha-calcium/calmodulin-dependent protein kinase II in neurotransmitter release at a glutamatergic central synapse PNAS 100 4275 4280 10.1073/pnas.0530202100 12629219 PMC153083 · DOI
- Huganir RL Nicoll RA 2013 AMPARs and synaptic plasticity: the last 25 years Neuron 80 704 717 10.1016/j.neuron.2013.10.025 24183021 PMC4195488 · DOI · Paper page
- Inagaki HK Fontolan L Romani S Svoboda K 2019 Discrete attractor dynamics underlies persistent activity in the frontal cortex Nature 566 212 217 10.1038/s41586-019-0919-7 30728503 · DOI · Paper page
- Incontro S Díaz-Alonso J Iafrati J Vieira M Asensio CS Sohal VS Roche KW Bender KJ Nicoll RA 2018 The CaMKII/NMDA receptor complex controls hippocampal synaptic transmission by kinase-dependent and independent mechanisms Nature Communications 9 2069 10.1038/s41467-018-04439-7 29802289 PMC5970233 · DOI · Paper page
- LeCher JC Nowak SJ McMurry JL 2017 Breaking in and busting out: cell-penetrating peptides and the endosomal escape problem Biomolecular Concepts 8 131 141 10.1515/bmc-2017-0023 28841567 PMC5640260 · DOI
- Lee S-JR Escobedo-Lozoya Y Szatmari EM Yasuda R 2009 Activation of CaMKII in single dendritic spines during long-term potentiation Nature 458 299 304 10.1038/nature07842 19295602 PMC2719773 · DOI · Paper page
- Leonard AS Lim IA Hemsworth DE Horne MC Hell JW 1999 Calcium/calmodulin-dependent protein kinase II is associated with the N-methyl-D-aspartate receptor PNAS 96 3239 3244 10.1073/pnas.96.6.3239 10077668 PMC15926 · DOI · Paper page
- Lisman JE Goldring MA 1988 Feasibility of long-term storage of graded information by the Ca2+/calmodulin-dependent protein kinase molecules of the postsynaptic density PNAS 85 5320 5324 10.1073/pnas.85.14.5320 3393540 PMC281742 · DOI · Paper page
- Lisman JE Zhabotinsky AM 2001 A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly Neuron 31 191 201 10.1016/s0896-6273(01)00364-6 11502252 · DOI
- Lisman J Schulman H Cline H 2002 The molecular basis of CaMKII function in synaptic and behavioural memory Nature Reviews. Neuroscience 3 175 190 10.1038/nrn753 11994750 · DOI · Paper page
- Lisman J Raghavachari S 2015 Biochemical principles underlying the stable maintenance of LTP by the CaMKII/NMDAR complex Brain Research 1621 51 61 10.1016/j.brainres.2014.12.010 25511992 PMC4466085 · DOI
- Lisman J 2017 Criteria for identifying the molecular basis of the engram (CaMKII, PKMzeta) Molecular Brain 10 55 10.1186/s13041-017-0337-4 29187215 PMC5707903 · DOI
- Lledo PM Hjelmstad GO Mukherji S Soderling TR Malenka RC Nicoll RA 1995 Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism PNAS 92 11175 11179 10.1073/pnas.92.24.11175 7479960 PMC40594 · DOI · Paper page
- Malenka RC Kauer JA Perkel DJ Mauk MD Kelly PT Nicoll RA Waxham MN 1989 An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation Nature 340 554 557 10.1038/340554a0 2549423 · DOI · Paper page
- Malenka RC Bear MF 2004 LTP and LTD: an embarrassment of riches Neuron 44 5 21 10.1016/j.neuron.2004.09.012 15450156 · DOI · Paper page
- Malinow R Schulman H Tsien RW 1989 Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP Science 245 862 866 10.1126/science.2549638 2549638 · DOI · Paper page
- Miller SG Kennedy MB 1986 Regulation of brain type II Ca2+/calmodulin-dependent protein kinase by autophosphorylation: a Ca2+-triggered molecular switch Cell 44 861 870 10.1016/0092-8674(86)90008-5 3006921 · DOI · Paper page
- Morrison A Diesmann M Gerstner W 2008 Phenomenological models of synaptic plasticity based on spike timing Biological Cybernetics 98 459 478 10.1007/s00422-008-0233-1 18491160 PMC2799003 · DOI · Paper page
- Mulkey RM Herron CE Malenka RC 1993 An essential role for protein phosphatases in hippocampal long-term depression Science 261 1051 1055 10.1126/science.8394601 8394601 · DOI · Paper page
- Mullasseril P Dosemeci A Lisman JE Griffith LC 2007 A structural mechanism for maintaining the “on-state” of the CaMKII memory switch in the post-synaptic density Journal of Neurochemistry 103 357 364 10.1111/j.1471-4159.2007.04744.x 17877639 PMC2665908 · DOI
- Murakoshi H Shin ME Parra-Bueno P Szatmari EM Shibata ACE Yasuda R 2017 Kinetics of Endogenous CaMKII Required for Synaptic Plasticity Revealed by Optogenetic Kinase Inhibitor Neuron 94 690 10.1016/j.neuron.2017.04.027 28472663 · DOI · Paper page
- Nelson AR Borland L Allbritton NL Sims CE 2007 Myristoyl-based transport of peptides into living cells Biochemistry 46 14771 14781 10.1021/bi701295k 18044965 PMC2408932 · DOI
- Nicoll RA 2017 A Brief History of Long-Term Potentiation Neuron 93 281 290 10.1016/j.neuron.2016.12.015 28103477 · DOI · Paper page
- Otmakhov N Griffith LC Lisman JE 1997 Postsynaptic Inhibitors of Calcium/Calmodulin-Dependent Protein Kinase Type II Block Induction But Not Maintenance of Pairing-Induced Long-Term Potentiation The Journal of Neuroscience 17 5357 5365 10.1523/JNEUROSCI.17-14-05357.1997 9204920 PMC6793827 · DOI · Paper page
- Özden C Santos N Agnello E Gaubitz C Lapinskas E 2020 CaMKII Binds Both Substrates and Effectors at the Active Site bioRxiv 10.1101/20201025354241 PMC9336311 35830796 · DOI
- Patel SG Sayers EJ He L Narayan R Williams TL Mills EM Allemann RK Luk LYP Jones AT Tsai YH 2019 Cell-penetrating peptide sequence and modification dependent uptake and subcellular distribution of green florescent protein in different cell lines Scientific Reports 9 6298 10.1038/s41598-019-42456-8 31000738 PMC6472342 · DOI
- Pellicena P Schulman H 2014 CaMKII inhibitors: from research tools to therapeutic agents Frontiers in Pharmacology 5 21 10.3389/fphar.2014.00021 24600394 PMC3929941 · DOI
- Petersen JD Chen X Vinade L Dosemeci A Lisman JE Reese TS 2003 Distribution of Postsynaptic Density (PSD)-95 and Ca 2+ /Calmodulin-Dependent Protein Kinase II at the PSD The Journal of Neuroscience 23 11270 11278 10.1523/JNEUROSCI.23-35-11270.2003 14657186 PMC6741048 · DOI
- Pi HJ Otmakhov N Lemelin D De Koninck P Lisman J 2010 Autonomous CaMKII can promote either long-term potentiation or long-term depression, depending on the state of T305/T306 phosphorylation The Journal of Neuroscience 30 8704 8709 10.1523/JNEUROSCI.0133-10.2010 20592192 PMC2903435 · DOI · Paper page
- Rossetti T Banerjee S Kim C Leubner M Lamar C Gupta P Lee B Neve R Lisman J 2017 Memory Erasure Experiments Indicate a Critical Role of CaMKII in Memory Storage Neuron 96 207 216 10.1016/j.neuron.2017.09.010 28957669 PMC5634137 · DOI · Paper page
- Sanhueza M McIntyre CC Lisman JE 2007 Reversal of synaptic memory by Ca2+/calmodulin-dependent protein kinase II inhibitor The Journal of Neuroscience 27 5190 5199 10.1523/JNEUROSCI.5049-06.2007 17494705 PMC6672374 · DOI
- Sanhueza M Fernandez-Villalobos G Stein IS Kasumova G Zhang P Bayer KU Otmakhov N Hell JW Lisman J 2011 Role of the CaMKII/NMDA receptor complex in the maintenance of synaptic strength The Journal of Neuroscience 31 9170 9178 10.1523/JNEUROSCI.1250-11.2011 21697368 PMC3138556 · DOI · Paper page
- Sanhueza M Lisman J 2013 The CaMKII/NMDAR complex as a molecular memory Molecular Brain 6 10 10.1186/1756-6606-6-10 23410178 PMC3582596 · DOI · Paper page
- Scanziani M Malenka RC Nicoll RA 1996 Role of intercellular interactions in heterosynaptic long-term depression Nature 380 446 450 10.1038/380446a0 8602244 · DOI · Paper page
- Schnell E Sizemore M Karimzadegan S Chen L Bredt DS Nicoll RA 2002 Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number PNAS 99 13902 13907 10.1073/pnas.172511199 12359873 PMC129795 · DOI · Paper page
- Schulman H 1984 Phosphorylation of microtubule-associated proteins by a Ca2+/calmodulin-dependent protein kinase The Journal of Cell Biology 99 11 19 10.1083/jcb.99.1.11 6736124 PMC2275617 · DOI
- Silva AJ Stevens CF Tonegawa S Wang Y 1992 Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice Science 257 201 206 10.1126/science.1378648 1378648 · DOI · Paper page
- Stein IS Park DK Claiborne N Zito K 2021 Non-ionotropic NMDA receptor signaling gates bidirectional structural plasticity of dendritic spines Cell Reports 34 108664 10.1016/j.celrep.2020.108664 33503425 PMC7952241 · DOI
- Stevens CF Tonegawa S Wang Y 1994 The role of calcium-calmodulin kinase II in three forms of synaptic plasticity Current Biology 4 687 693 10.1016/s0960-9822(00)00153-6 7953554 · DOI
- Stoppini L Buchs PA Muller D 1991 A simple method for organotypic cultures of nervous tissue Journal of Neuroscience Methods 37 173 182 10.1016/0165-0270(91)90128-m 1715499 · DOI
- Strack S Choi S Lovinger DM Colbran RJ 1997 Translocation of autophosphorylated calcium/calmodulin-dependent protein kinase II to the postsynaptic density The Journal of Biological Chemistry 272 13467 13470 10.1074/jbc.272.21.13467 9153188 · DOI
- Strack S Barban MA Wadzinski BE Colbran RJ 2002 Differential Inactivation of Postsynaptic Density-Associated and Soluble Ca2+/Calmodulin-Dependent Protein Kinase II by Protein Phosphatases 1 and 2A Journal of Neurochemistry 68 2119 2128 10.1046/j.1471-4159.1997.68052119.x 9109540 · DOI · Paper page
- Stratton M Lee IH Bhattacharyya M Christensen SM Chao LH Schulman H Groves JT Kuriyan J 2014 Activation-triggered subunit exchange between CaMKII holoenzymes facilitates the spread of kinase activity eLife 3 e01610 10.7554/eLife.01610 24473075 PMC3901001 · DOI · Paper page
- Toyoizumi T Kaneko M Stryker MP Miller KD 2014 Modeling the dynamic interaction of Hebbian and homeostatic plasticity Neuron 84 497 510 10.1016/j.neuron.2014.09.036 25374364 PMC4223656 · DOI · Paper page
- Trinidad JC Thalhammer A Specht CG Schoepfer R Burlingame AL 2005 Phosphorylation state of postsynaptic density proteins Journal of Neurochemistry 92 1306 1316 10.1111/j.1471-4159.2004.02943.x 15748150 · DOI
- Turrigiano GG 2008 The self-tuning neuron: synaptic scaling of excitatory synapses Cell 135 422 435 10.1016/j.cell.2008.10.008 18984155 PMC2834419 · DOI · Paper page
- Vest RS Davies KD O’Leary H Port JD Bayer KU 2007 Dual mechanism of a natural CaMKII inhibitor Molecular Biology of the Cell 18 5024 5033 10.1091/mbc.e07-02-0185 17942605 PMC2096578 · DOI
- Wang JH Kelly PT 1996 The balance between postsynaptic Ca(2+)-dependent protein kinase and phosphatase activities controlling synaptic strength Learning & Memory 3 170 181 10.1101/lm.3.2-3.170 10456087 · DOI
- Wang XJ 2001 Synaptic reverberation underlying mnemonic persistent activity Trends in Neurosciences 24 455 463 10.1016/s0166-2236(00)01868-3 11476885 · DOI · Paper page
- Wong JM Gray JA 2018 Long-Term Depression Is Independent of GluN2 Subunit Composition The Journal of Neuroscience 38 4462 4470 10.1523/JNEUROSCI.0394-18.2018 29593052 PMC5943974 · DOI
Cited by
Sorted by citations
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
“An inhibition of synaptic transmission with identical properties including magnitude, selectivity, and time course was found with myr-AIP (361).”
BackgroundSelf-citationSynaptic memory survives molecular turnover
Lee, J., Chen, X., & Nicoll, R. A. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2211572119 · Cited by 27 · see citing works
Self-citationLTP expression mediated by autonomous activity of GluN2B-bound CaMKII
Rumian, N. L., Barker, C. M., Larsen, M. E., Tullis, J. E., Freund, R. K., Taslimi, A., Coultrap, S. J., Tucker, C. L., Dell’Acqua, M. L., & Bayer, K. U. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114866 · Cited by 20 · see citing works
- Authors
- Tao, W., Lee, J., Chen, X., Díaz-Alonso, J., Zhou, J., Pleasure, S., & Nicoll, R. A.
- Affiliations
- Fujian Medical University (CN)
- University of California, San Francisco (US)
- Corresponding author
- Nicoll, Roger A
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2021-12-15
- Volume
- 10
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC8798046
- OpenAlex
- W4200085151
- Cited by
- 72
- References
- 16
- Citations by year
- 2026: 11 · 2025: 13 · 2024: 18 · 2023: 21 · 2022: 9
- FWCI
- 5.51
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (MH070957)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Keywords
- CaMKII, long-term potentiation, synaptic memory, LTP maintenance, synaptic transmission, memory storage, learning and memory, calcium/calmodulin-dependent protein kinase
- MeSH terms
- Animals, Synaptic Transmission, Long-Term Potentiation, Mice, Calcium-Calmodulin-Dependent Protein Kinase Type 2
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review