MAP Kinase Translocates into the Nucleus of the Presynaptic Cell and Is Required for Long-Term Facilitation in Aplysia
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Long-term facilitation of the sensory to motor synapse in Aplysia requires gene expression. While some transcription factors involved in long-term facilitation are phosphorylated by PKA, others lack PKA sites but contain MAP Kinase (MAPK) phosphorylation sites. We now show that MAPK translocates into the nucleus of the presynaptic but not the postsynaptic cell during 5-HT-induced long-term facilitation. The presynaptic nuclear translocation of MAPK is also triggered by elevations in intracellular cAMP. Injection of anti-MAPK antibodies or of MAPK Kinase inhibitors into the presynaptic cell blocks long-term facilitation, without affecting basal synaptic transmission or short-term facilitation. Thus, MAPK appears to be specifically recruited and necessary for the long-term form of facilitation. This mechanism for long-term plasticity may be quite general: cAMP also activated MAPK in mouse hippocampal neurons, suggesting that MAPK may play a role in hippocampal long-term potentiation.
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The PKA and ERK cascades are necessary to induce long-term synaptic facilitation (LTF) in Aplysia.
“Two biochemical cascades required for LTF are those that mediate activation of protein kinase A (PKA)12–15 and the MAP kinase isoform termed extracellular signal-regulated kinase (ERK)16–18.”
From Computational design of enhanced learning protocols (2012) · cites this paper as [16]
Cites
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · see citing works
Marshall, C. J. (1995) · Cell · doi:10.1016/0092-8674(95)90401-8 · Cited by 4,557 · see citing works
Alessi, D. R., Cuenda, A., Cohen, P., Dudley, D. T., & Saltiel, A. R. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.46.27489 · Cited by 3,396 · see citing works
A synthetic inhibitor of the mitogen-activated protein kinase cascade.
Dudley, D. T., Pang, L., Decker, S. J., Bridges, A. J., & Saltiel, A. R. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.17.7686 · Cited by 2,679 · see citing works
Synaptic tagging and long-term potentiation
Frey, U., & Morris, R. G. M. (1997) · Nature · doi:10.1038/385533a0 · Cited by 1,736 · see citing works
Protein synthesis and memory: A review.
Davis, H. P., & Squire, L. R. (1984) · Psychological Bulletin · doi:10.1037/0033-2909.96.3.518 · Cited by 1,505 · see citing works
Coupling of the RAS-MAPK Pathway to Gene Activation by RSK2, a Growth Factor-Regulated CREB Kinase
Xing, J. W., Ginty, D. D., & Greenberg, M. E. (1996) · Science · doi:10.1126/science.273.5277.959 · Cited by 1,246 · see citing works
Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons
Frey, U., Huang, Y.-Y., & Kandel, E. R. (1993) · Science · doi:10.1126/science.8389057 · Cited by 1,218 · see citing works
Self-citationAbel, T., Nguyen, P. V., Barad, M., Deuel, T. A. S., Kandel, E. R., & Bourtchouladze, R. (1997) · Cell · doi:10.1016/s0092-8674(00)81904-2 · Cited by 1,217 · see citing works
Self-citationcAMP Activates MAP Kinase and Elk-1 through a B-Raf- and Rap1-Dependent Pathway
Vossler, M. R., Yao, H. W., York, R. D., Pan, M., Rim, C. S., & Stork, P. A. (1997) · Cell · doi:10.1016/s0092-8674(00)80184-1 · Cited by 1,044 · see citing works
The long and the short of long–term memory—a molecular framework
Goelet, P., Castellucci, V. F., Schacher, S., & Kandel, E. R. (1986) · Nature · doi:10.1038/322419a0 · Cited by 1,041 · see citing works
Self-citationInhibition by cAMP of Ras-Dependent Activation of Raf
Cook, S. J., & McCormick, F. P. (1993) · Science · doi:10.1126/science.7694367 · Cited by 942 · see citing works
Requirement of a Critical Period of Transcription for Induction of a Late Phase of LTP
Nguyen, P. V., Abel, T., & Kandel, E. R. (1994) · Science · doi:10.1126/science.8066450 · Cited by 888 · see citing works
Self-citationTraverse, S., Gómez, N., Paterson, H., Marshall, C. J., & Cohen, P. (1992) · Biochemical Journal · doi:10.1042/bj2880351 · Cited by 874 · see citing works
Montarolo, P. G., Goelet, P., Castellucci, V. F., Morgan, J., Kandel, E. R., & Schacher, S. (1986) · Science · doi:10.1126/science.3775383 · Cited by 769 · see citing works
Self-citationDash, P. K., Hochner, B., & Kandel, E. R. (1990) · Nature · doi:10.1038/345718a0 · Cited by 747 · see citing works
Self-citationToward a molecular definition of long-term memory storage
Bailey, C. H., Bartsch, D., & Kandel, E. R. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.24.13445 · Cited by 691 · see citing works
Self-citationPHAS-I as a Link Between Mitogen-Activated Protein Kinase and Translation Initiation
Lin, T.-A., Kong, X., Haystead, T., Pause, A., Belsham, G. J., Sonenberg, N., & Lawrence, J. C. (1994) · Science · doi:10.1126/science.7939721 · Cited by 671 · see citing works
Mediation of Hippocampal Mossy Fiber Long-Term Potentiation by Cyclic AMP
Weisskopf, M. G., Castillo, P. E., Zalutsky, R. A., & Nicoll, R. A. (1994) · Science · doi:10.1126/science.7916482 · Cited by 618 · see citing works
Ferrell, J. E. (1996) · Trends in Biochemical Sciences · doi:10.1016/s0968-0004(96)20026-x · Cited by 591 · see citing works
Activation of p42 Mitogen-activated Protein Kinase in Hippocampal Long Term Potentiation
English, J. D., & Sweatt, J. D. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.40.24329 · Cited by 579 · see citing works
Nakajima, T., Kinoshita, S. M., Sasagawa, T., Sasaki, K., Naruto, M., Kishimoto, T., & Akira, S. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.6.2207 · Cited by 578 · see citing works
Bartsch, D., Ghirardi, M., Skehel, P. A., Karl, K. A., Herder, S. P., Chen, M., Bailey, C. H., & Kandel, E. R. (1995) · Cell · doi:10.1016/0092-8674(95)90213-9 · Cited by 572 · see citing works
Self-citationSpatially Resolved Dynamics of cAMP and Protein Kinase A Subunits in Aplysia Sensory Neurons
Bacskai, B. J., Hochner, B., Mahaut‐Smith, M. P., Adams, S., Kaang, B., Kandel, E. R., & Tsien, R. Y. (1993) · Science · doi:10.1126/science.7682336 · Cited by 546 · see citing works
Self-citationC/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia
Alberini, C. M., Ghirardl, M., Metz, R., & Kandel, E. R. (1994) · Cell · doi:10.1016/0092-8674(94)90386-7 · Cited by 523 · see citing works
Self-citationHuang, Y.-Y., Li, X.-C., & Kandel, E. R. (1994) · Cell · doi:10.1016/0092-8674(94)90401-4 · Cited by 490 · see citing works
Self-citationFaure, M., Voyno-Yasenetskaya, T., & Bourne, H. R. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37127-2 · Cited by 476 · see citing works
Huang, Y.-Y., & Kandel, E. R. (1994) · Learning & Memory · doi:10.1101/lm.1.1.74 · Cited by 476 · see citing works
Self-citationDiversity in function and regulation of MAP kinase pathways
BLUMER, K. J., & Johnson, G. L. (1994) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(94)90147-3 · Cited by 465 · see citing works
Stimulation of Protein Tyrosine Phosphorylation by NMDA Receptor Activation
Bading, H., & Greenberg, M. E. (1991) · Science · doi:10.1126/science.1715095 · Cited by 463 · see citing works
Identification of substrate recognition determinants for human ERK1 and ERK2 protein kinases.
Gonzalez, F. A., Raden, D. L., & Davis, R. J. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)54548-8 · Cited by 454 · see citing works
Cool, D. R., Normant, E., Shen, F.-S., Chen, H., Pannell, L. K., Zhang, Y., & Loh, Y. P. (1997) · Cell · doi:10.1016/s0092-8674(00)81860-7 · Cited by 449 · see citing works
Graves, L. M., Bornfeldt, K., Raines, E. W., Potts, B. C. M., Macdonald, S. G., Ross, R., & Krebs, E. G. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.21.10300 · Cited by 447 · see citing works
Morphological Basis of Long-Term Habituation and Sensitization in Aplysia
Bailey, C. H., & Chen, M. (1983) · Science · doi:10.1126/science.6828885 · Cited by 420 · see citing works
Clark‐Lewis, I., Sanghera, J. S., & Pelech, S. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)98601-1 · Cited by 406 · see citing works
Modulation of an NCAM-Related Adhesion Molecule with Long-Term Synaptic Plasticity in Aplysia
Mayford, M. R., Barzilai, A., Keller, F., Schacher, S., & Kandel, E. R. (1992) · Science · doi:10.1126/science.1585176 · Cited by 371 · see citing works
Self-citationSchuster, C., Davis, G. W., Fetter, R. D., & Goodman, C. S. (1996) · Neuron · doi:10.1016/s0896-6273(00)80198-1 · Cited by 371 · see citing works
Increasing cAMP attenuates activation of mitogen-activated protein kinase.
Sevetson, B. R., Kong, X., & Lawrence, J. C. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.21.10305 · Cited by 366 · see citing works
Cyclic AMP activates the mitogen-activated protein kinase cascade in PC12 cells.
Frödin, M., Peraldi, P., & Obberghen‐Schilling, E. V. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37589-0 · Cited by 326 · see citing works
González, F. M., Seth, A., Raden, D. L., Bowman, D., Fay, F., & Davis, R. J. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.122.5.1089 · Cited by 320 · see citing works
Bailey, C. H., Chen, M., Keller, F., & Kandel, E. R. (1992) · Science · doi:10.1126/science.1585177 · Cited by 314 · see citing works
Self-citationQuantal analysis and synaptic anatomy--integrating two views of hippocampal plasticity.
Lisman, J., & Harris, K. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90122-3 · Cited by 271 · see citing works
Dissection of memory formation: from behavioral pharmacology to molecular genetics
DeZazzo, J., & Tully, T. (1995) · Trends in Neurosciences · doi:10.1016/0166-2236(95)93905-d · Cited by 270 · see citing works
Buchs, P., & Müller, D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.15.8040 · Cited by 267 · see citing works
cAMP Evokes Long-Term Facilitation in Aplysia Sensory Neurons That Requires New Protein Synthesis
Schacher, S., Castellucci, V. F., & Kandel, E. R. (1988) · Science · doi:10.1126/science.2454509 · Cited by 264 · see citing works
Self-citationThe Signal-Dependent Coactivator CBP Is a Nuclear Target for pp90RSK
Nakajima, T., Fukamizu, A., Takahashi, J. B., Gage, F. H., Fisher, T., Blenis, J., & Montminy, M. (1996) · Cell · doi:10.1016/s0092-8674(00)80119-1 · Cited by 254 · see citing works
Castellucci, V. F., Blumenfeld, H., Goelet, P., & Kandel, E. R. (1989) · Journal of Neurobiology · doi:10.1002/neu.480200102 · Cited by 232 · see citing works
Self-citationDavis, G. W., Schuster, C., & Goodman, C. S. (1996) · Neuron · doi:10.1016/s0896-6273(00)80199-3 · Cited by 230 · see citing works
Target-Dependent Structural Changes Accompanying Long-Term Synaptic Facilitation in Aplysia Neurons
Glanzman, D. L., Kandel, E. R., & Schacher, S. (1990) · Science · doi:10.1126/science.2389145 · Cited by 224 · see citing works
Self-citationMolecular Enhancement of Memory Formation
Carew, T. J. (1996) · Neuron · doi:10.1016/s0896-6273(00)80016-1 · Cited by 202 · see citing works
Role of Transforming Growth Factor-β in Long-Term Synaptic Facilitation in Aplysia
Zhang, F., Endo, S., Cleary, L. J., Eskin, A., & Byrne, J. H. (1997) · Science · doi:10.1126/science.275.5304.1318 · Cited by 186 · see citing works
Spatial and temporal changes in signal transduction pathways during LTP
Thomas, K. L., Laroche, S., Errington, M. L., Bliss, T. V. P., & Hunt, S. P. (1994) · Neuron · doi:10.1016/0896-6273(94)90040-x · Cited by 182 · see citing works
Bailey, C. H., Kaang, B., Chen, M., Martin, K. C., Lim, C., Casadio, A., & Kandel, E. R. (1997) · Neuron · doi:10.1016/s0896-6273(00)80331-1 · Cited by 180 · see citing works
Self-citationEdwards, F. A. (1995) · Physiological Reviews · doi:10.1152/physrev.1995.75.4.759 · Cited by 179 · see citing works
Rayport, S., & Schacher, S. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-03-00759.1986 · Cited by 177 · see citing works
Fiore, R. S., Bayer, V. E., Pelech, S., Posada, J. A., Cooper, J. A., & Baraban, J. M. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90516-i · Cited by 158 · see citing works
Vaillancourt, R. R., Gardner, A. M., & Johnson, G. L. (1994) · Molecular and Cellular Biology · doi:10.1128/mcb.14.10.6522 · Cited by 157 · see citing works
Brondello, J., McKenzie, F. R., Sun, H., Tonks, N. K., & Pouysségur, J. (1995) · PubMed · Cited by 154 · see citing works
Synapse restructuring associated with the maintenance phase of hippocampal long-term potentiation
Geinisman, Y., deToledo‐Morrell, L., Morrell, F., Persina, I. S., & Beatty, M. A. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960506)368:3 · Cited by 140 · see citing works
Bailey, C. H., & Chen, M. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.23.9356 · Cited by 121 · see citing works
Long-Term Facilitation in Aplysia Involves Increase in Transmitter Release
Dale, N., Schacher, S., & Kandel, E. R. (1988) · Science · doi:10.1126/science.2892269 · Cited by 116 · see citing works
Self-citationProtein Serine/Threonine Kinases of the MAPK Cascade
Graves, J. D., Campbell, J. S., & Krebs, E. G. (1995) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1995.tb26684.x · Cited by 86 · see citing works
Faure, M., & Bourne, H. R. (1995) · Molecular Biology of the Cell · doi:10.1091/mbc.6.8.1025 · Cited by 68 · see citing works
Sossin, W. S. (1996) · Trends in Neurosciences · doi:10.1016/0166-2236(96)20016-5 · Cited by 63 · see citing works
Gause, K. C., Homma, M. K., Licciardi, K. A., Seger, R., Ahn, N. G., Peterson, M. J., Krebs, E. G., & Meier, K. E. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)85398-x · Cited by 59 · see citing works
Yao, H. W., Labudda, K., Rim, C. S., Capodieci, P., Loda, M. F., & Stork, P. A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.35.20748 · Cited by 54 · see citing works
Qian, Z., Gilbert, M. E., & Kandel, E. R. (1994) · Learning & Memory · doi:10.1101/lm.1.3.180 · Cited by 30 · see citing works
Self-citation
Flagged first, then by citations
1 of the 68 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The molecular biology of memory storage: a dialogue between genes and synapses
Kandel, E. R. (2001) · Science · doi:10.1126/science.1067020 · Cited by 3,917 · see citing works
Self-citationBerridge, M. J. (1998) · Neuron · doi:10.1016/s0896-6273(00)80510-3 · Cited by 2,189 · see citing works
Long-Term Potentiation and Memory
Lynch, M. A. (2004) · Physiological Reviews · doi:10.1152/physrev.00014.2003 · Cited by 2,001 · see citing works
Cognitive Neuroscience and the Study of Memory
Milner, B. A., Squire, L. R., & Kandel, E. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80987-3 · Cited by 1,300 · see citing works
Self-citationAddiction, Dopamine, and the Molecular Mechanisms of Memory
Berke, J. D., & Hyman, S. E. (2000) · Neuron · doi:10.1016/s0896-6273(00)81056-9 · Cited by 1,167 · see citing works
The Molecular and Systems Biology of Memory
Kandel, E. R., Dudai, Y., & Mayford, M. R. (2014) · Cell · doi:10.1016/j.cell.2014.03.001 · Cited by 1,134 · see citing works
Self-citationSweatt, J. D. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00054.x · Cited by 1,131 · see citing works
The MAPK cascade is required for mammalian associative learning
Atkins, C. M., Selcher, J. C., Petraitis, J. J., Trzaskos, J. M., & Sweatt, J. D. (1998) · Nature Neuroscience · doi:10.1038/2836 · Cited by 1,083 · see citing works
Mitogen-activated protein kinases in synaptic plasticity and memory
Sweatt, J. D. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.04.001 · Cited by 990 · see citing works
Transcription Factors in Long-Term Memory and Synaptic Plasticity
Alberini, C. M. (2009) · Physiological Reviews · doi:10.1152/physrev.00017.2008 · Cited by 991 · see citing works
The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB
Kandel, E. R. (2012) · Molecular Brain · doi:10.1186/1756-6606-5-14 · Cited by 904 · see citing works
Self-citationImpey, S., Obrietan, K. H., Wong, S. T., Poser, S., Yano, S., Wayman, G. A., Deloulme, J., Chan, G. C. ‐., & Storm, D. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80602-9 · Cited by 889 · see citing works
Cobb, M. H. (1999) · Progress in Biophysics and Molecular Biology · doi:10.1016/s0079-6107(98)00056-x · Cited by 869 · see citing works
Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity
Ji, R., Baba, H., Brenner, G. J., & Woolf, C. J. (1999) · Nature Neuroscience · doi:10.1038/16040 · Cited by 782 · see citing works
Martin, K. C., Casadio, A., Zhu, H.-X., Yaping, E., Rose, J. C., Chen, M. C., Bailey, C. H., & Kandel, E. R. (1997) · Cell · doi:10.1016/s0092-8674(00)80484-5 · Cited by 752 · see citing works
Self-citationThe Restless Engram: Consolidations Never End
Dudai, Y. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150500 · Cited by 644 · see citing works
Schafe, G. E., Atkins, C. M., Swank, M. W., Bauer, E. P., Sweatt, J. D., & LeDoux, J. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-21-08177.2000 · Cited by 674 · see citing works
Davis, S., Vanhoutte, P., Pagès, C., Caboche, J., & Laroche, S. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-12-04563.2000 · Cited by 621 · see citing works
Impey, S., Obrietan, K. H., & Storm, D. R. (1999) · Neuron · doi:10.1016/s0896-6273(00)80747-3 · Cited by 613 · see citing works
Brunet, A., Roux, D., Lenormand, P., Dowd, S., Keyse, S. M., & Pouysségur, J. (1999) · The EMBO Journal · doi:10.1093/emboj/18.3.664 · Cited by 595 · see citing works
Molecular Psychology: Roles for the ERK MAP Kinase Cascade in Memory
Adams, J. P., & Sweatt, J. D. (2002) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.42.082701.145401 · Cited by 588 · see citing works
Extracellular-signal-regulated kinase signalling in neurons
Grewal, S., York, R. D., & Stork, P. A. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00010-0 · Cited by 555 · see citing works
Involvement of the Extracellular Signal-Regulated Kinase Cascade for Cocaine-Rewarding Properties
Valjent, E., Corvol, J., Pagès, C., Besson, M., Maldonado, R. J., & Caboche, J. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-23-08701.2000 · Cited by 548 · see citing works
Roberson, E. D., English, J. D., Adams, J. P., Selcher, J. C., Kondratick, C. M., & Sweatt, J. D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-11-04337.1999 · Cited by 542 · see citing works
Blum, S., Moore, A. N., Adams, F., & Dash, P. K. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-09-03535.1999 · Cited by 522 · see citing works
The Central Dogma Decentralized: New Perspectives on RNA Function and Local Translation in Neurons
Holt, C. E., & Schuman, E. M. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.036 · Cited by 525 · see citing works
Depolarization and cAMP Elevation Rapidly Recruit TrkB to the Plasma Membrane of CNS Neurons
Meyer-Franke, A., Wilkinson, G. A., Kruttgen, A., Hu, M., Munro, E., Hanson, M. G., Reichardt, L. F., & Barres, B. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80586-3 · Cited by 516 · see citing works
Memory consolidation of Pavlovian fear conditioning: a cellular and molecular perspective
Schafe, G. E., Nader, K., Blair, H. T., & LeDoux, J. E. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01969-x · Cited by 510 · see citing works
Casadio, A., Martin, K. C., Giustetto, M., Zhu, H., Chen, M., Bartsch, D., Bailey, C. H., & Kandel, E. R. (1999) · Cell · doi:10.1016/s0092-8674(00)81653-0 · Cited by 503 · see citing works
Self-citationGuan, Z., Giustetto, M., Lomvardas, S., Kim, J.-H., Miniaci, M. C., Schwartz, J. H., Thanos, D., & Kandel, E. R. (2002) · Cell · doi:10.1016/s0092-8674(02)01074-7 · Cited by 497 · see citing works
Self-citationMolecular mechanisms underlying emotional learning and memory in the lateral amygdala
Rodrigues, S. M., Schafe, G. E., & LeDoux, J. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.014 · Cited by 491 · see citing works
Wong, S. T., Athos, J., Figueroa, X. A., Pineda, V. V., Schaefer, M. L., Chavkin, C. C., Muglia, L. J., & Storm, D. R. (1999) · Neuron · doi:10.1016/s0896-6273(01)80036-2 · Cited by 486 · see citing works
Wu, G., Deisseroth, K. A., & Tsien, R. W. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.051634198 · Cited by 477 · see citing works
Molecular Substrates for Retrieval and Reconsolidation of Cocaine-Associated Contextual Memory
Miller, C. A., & Marshall, J. F. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.006 · Cited by 467 · see citing works
Pittenger, C., Huang, Y. Y., Paletzki, R. F., Bourtchouladze, R., Scanlin, H., Vronskaya, S., & Kandel, E. R. (2002) · Neuron · doi:10.1016/s0896-6273(02)00684-0 · Cited by 464 · see citing works
Self-citationMathematical modeling of gene networks.
Smolen, P., Baxter, D., & Byrne, J. (2000) · Neuron · doi:10.1016/s0896-6273(00)81194-0 · Cited by 466 · see citing works
Nitric Oxide Signaling Contributes to Late-Phase LTP and CREB Phosphorylation in the Hippocampus
Lü, Y.-F., Kandel, E. R., & Hawkins, R. D. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-23-10250.1999 · Cited by 409 · see citing works
Self-citationRajasethupathy, P., Fiumara, F., Sheridan, R., Betel, D., Puthanveettil, S. V., Russo, J. J., Sander, C., Tuschl, T., & Kandel, E. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.029 · Cited by 406 · see citing works
Self-citationSchafe, G. E., Nadel, N. V., Sullivan, G. M., Harris, A. Z., & LeDoux, J. E. (1999) · Learning & Memory · doi:10.1101/lm.6.2.97 · Cited by 407 · see citing works
Structural Components of Synaptic Plasticity and Memory ConsolidationPreprint
Bailey, C. H., Kandel, E. R., & Harris, K. M. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021758 · Cited by 393 · see citing works
Self-citationSpaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology
Wu, G., Deisseroth, K. A., & Tsien, R. W. (2001) · Nature Neuroscience · doi:10.1038/83976 · Cited by 389 · see citing works
Is Heterosynaptic modulation essential for stabilizing hebbian plasiticity and memory
Bailey, C. H., Giustetto, M., Huang, Y.-Y., Hawkins, R. D., & Kandel, E. R. (2000) · Nature Reviews Neuroscience · doi:10.1038/35036191 · Cited by 382 · see citing works
Self-citationBartsch, D., Casadio, A., Karl, K. A., Serodio, P., & Kandel, E. R. (1998) · Cell · doi:10.1016/s0092-8674(00)81752-3 · Cited by 373 · see citing works
Self-citationHoffman, D. A., & Johnston, D. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-10-03521.1998 · Cited by 373 · see citing works
Dalby, K. N., MORRICE, N. A., Caudwell, F. B., Avruch, J., & Cohen, P. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.3.1496 · Cited by 373 · see citing works
The Regulation of Transcription in Memory Consolidation
Alberini, C. M., & Kandel, E. R. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021741 · Cited by 362 · see citing works
Self-citationThe molecular and cellular biology of enhanced cognition
Lee, Y.-S., & Silva, A. J. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2572 · Cited by 361 · see citing works
Targeting the CREB pathway for memory enhancers
Tully, T., Bourtchouladze, R., Scott, R., & Tallman, J. F. (2003) · Nature Reviews Drug Discovery · doi:10.1038/nrd1061 · Cited by 355 · see citing works
MAPK activation in nociceptive neurons and pain hypersensitivity
Obata, K., & Noguchi, K. (2004) · Life Sciences · doi:10.1016/j.lfs.2004.01.007 · Cited by 358 · see citing works
A Complex Program of Striatal Gene Expression Induced by Dopaminergic Stimulation
Berke, J. D., Paletzki, R. F., Aronson, G. J., Hyman, S. E., & Gerfen, C. R. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-14-05301.1998 · Cited by 355 · see citing works
Dai, Y., Iwata, K., Fukuoka, T., Kondo, E., Tokunaga, A., Yamanaka, H., Tachibana, T., Liu, Y., & Noguchi, K. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-17-07737.2002 · Cited by 354 · see citing works
Manji, H. K., Moore, G. J., & Chen, G. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(00)00979-3 · Cited by 352 · see citing works
Winder, D. G., Mansuy, I. M., Osman, M., Moallem, T. M., & Kandel, E. R. (1998) · Cell · doi:10.1016/s0092-8674(00)80896-x · Cited by 351 · see citing works
Self-citationSignaling from synapse to nucleus: the logic behind the mechanisms
Deisseroth, K. A., Mermelstein, P. G., Xia, H., & Tsien, R. W. (2003) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(03)00076-x · Cited by 350 · see citing works
A Necessity for MAP Kinase Activation in Mammalian Spatial Learning
Selcher, J. C., Atkins, C. M., Trzaskos, J. M., Paylor, R., & Sweatt, J. D. (1999) · Learning & Memory · doi:10.1101/lm.6.5.478 · Cited by 341 · see citing works
Modeling transcriptional control in gene networks—methods, recent results, and future directions
Smolen, P., Baxter, D., & Byrne, J. (2000) · Bulletin of Mathematical Biology · doi:10.1006/bulm.1999.0155 · Cited by 386 · see citing works
Winder, D. G., Martin, K. C., Muzzio, I. A., Rohrer, D. K., Chruscinski, A. J., Kobilka, B. K., & Kandel, E. R. (1999) · Neuron · doi:10.1016/s0896-6273(00)81124-1 · Cited by 321 · see citing works
Self-citationMemory Suppressor Genes: Inhibitory Constraints on the Storage of Long-Term Memory
Abel, T. G., Martin, K. C., Bartsch, D., & Kandel, E. R. (1998) · Science · doi:10.1126/science.279.5349.338 · Cited by 316 · see citing works
Self-citationYuan, L., Adams, J. P., Swank, M. W., Sweatt, J. D., & Johnston, D. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-12-04860.2002 · Cited by 314 · see citing works
Cammarota, M., Bevilaqua, L. R., Ardenghi, P. G., Paratcha, G., de Stein, M. L., Izquierdo, I., & Medina, J. H. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(99)00329-0 · Cited by 310 · see citing works
Dynamic Regulation of RGS2 Suggests a Novel Mechanism in G-Protein Signaling and Neuronal Plasticity
Ingi, T., Krumins, A. M., Chidiac, P., Brothers, G. M., Chung, S., Snow, B. E., Barnes, C. A., Lanahan, A. A., Siderovski, D. P., Ross, E. M., et al. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07178.1998 · Cited by 298 · see citing works
Neural recognition molecules and synaptic plasticity
Schachner, M. (1997) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(97)80115-9 · Cited by 284 · see citing works
Patterson, S. L., Pittenger, C., Morozov, A., Martin, K. C., Scanlin, H., Drake, C., & Kandel, E. R. (2001) · Neuron · doi:10.1016/s0896-6273(01)00443-3 · Cited by 334 · see citing works
Self-citationThe Molecular Biology of Memory Storage: A Dialog Between Genes and Synapses
Kandel, E. R. (2004) · Bioscience Reports · doi:10.1007/s10540-005-2742-7 · Cited by 280 · see citing works
Self-citationNOBEL LECTURE: The Molecular Biology of Memory Storage: A Dialog Between Genes and Synapses
Kandel, E. R. (2001) · Bioscience Reports · doi:10.1023/a:1014775008533 · Cited by 280 · see citing works
Self-citationBerman, D. E., Hazvi, S., Rosenblum, K., Seger, R., & Dudai, Y. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-23-10037.1998 · Cited by 280 · see citing works
The Persistence of Long-Term Memory
Bailey, C. H., Kandel, E. R., & Si, K. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.017 · Cited by 277 · see citing works
Self-citationHuang, Y.-Y., Martin, K. C., & Kandel, E. R. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-17-06317.2000 · Cited by 269 · see citing works
Self-citationPositive and negative regulatory mechanisms that mediate long-term memory storage
Abel, T. G., & Kandel, E. R. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00050-7 · Cited by 267 · see citing works
Self-citationWaltereit, R., Dammermann, B., Wulff, P., Scafidi, J., Staubli, U. V., Kauselmann, G., Bundman, M. C., & Kuhl, D. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05484.2001 · Cited by 259 · see citing works
Structural basis for selective inhibition of Src family kinases by PP1
Liu, Y., Bishop, A. C., Witucki, L. A., Kraybill, B. C., Shimizu, E., Tsien, J. Z., Ubersax, J. A., Blethrow, J. D., Morgan, D. O., & Shokat, K. M. (1999) · Chemistry & Biology · doi:10.1016/s1074-5521(99)80118-5 · Cited by 252 · see citing works
Tancredi, V., D’Antuono, M., Café, C., Giovedı̀, S., Buè, M. C., D’Arcangelo, G., Onofri, F., & Benfenati, F. (2000) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2000.0750634.x · Cited by 249 · see citing works
Crosio, C., Heitz, E., Allis, C. D., Borrelli, E., & Sassone‐Corsi, P. (2003) · Journal of Cell Science · doi:10.1242/jcs.00804 · Cited by 242 · see citing works
York, R. D., Molliver, D. C., Grewal, S., Stenberg, P. E., McCleskey, E. W., & Stork, P. A. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.21.8069-8083.2000 · Cited by 242 · see citing works
Morozov, A., Muzzio, I. A., Bourtchouladze, R., Van-Strien, N., Lapidus, K. A. B., Yin, D., Winder, D. G., Adams, J. P., Sweatt, J. D., & Kandel, E. R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00404-5 · Cited by 237 · see citing works
Self-citationMolecular Mechanisms of Memory Storage inAplysia
Hawkins, R. D., Kandel, E. R., & Bailey, C. H. (2006) · Biological Bulletin · doi:10.2307/4134556 · Cited by 231 · see citing works
Self-citationA Role for Prefrontal Cortex in Memory Storage for Trace Fear Conditioning
Runyan, J. D., Moore, A. N., & Dash, P. K. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.4880-03.2004 · Cited by 224 · see citing works
Murray, B., Alessandrini, A., Cole, A. J., Yee, A. G., & Furshpan, E. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11975 · Cited by 224 · see citing works
Tong, L., Balazs, R., Thornton, P. L., & Cotman, C. W. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5463-03.2004 · Cited by 221 · see citing works
Lu, K., Walker, D. L., & Davis, M. E. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-16-j0005.2001 · Cited by 222 · see citing works
Dual MAP kinase pathways mediate opposing forms of long-term plasticity at CA3–CA1 synapses
Bolshakov, V. Y., Carboni, L., Cobb, M. H., Siegelbaum, S. A., & Belardetti, F. (2000) · Nature Neuroscience · doi:10.1038/80624 · Cited by 220 · see citing works
Common molecular mechanisms in explicit and implicit memory
Barco, Á., Bailey, C. H., & Kandel, E. R. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.03870.x · Cited by 217 · see citing works
Self-citationMolecular Mechanisms of the Memory Trace
Asok, A., Leroy, F., Rayman, J. B., & Kandel, E. R. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.10.005 · Cited by 213 · see citing works
Self-citationMice Lacking the ERK1 Isoform of MAP Kinase Are Unimpaired in Emotional LearningPreprint
Selcher, J. C., Nekrasova, T., Paylor, R. E., Landreth, G. E., & Sweatt, J. D. (2001) · Learning & Memory · doi:10.1101/lm.37001 · Cited by 211 · see citing works
Guan, Z., Peng, X., & Fang, J. (2004) · Brain Research · doi:10.1016/j.brainres.2004.05.032 · Cited by 208 · see citing works
Functional identification of sensory mechanisms required for developmental song learning
London, S. E., & Clayton, D. F. (2008) · Nature Neuroscience · doi:10.1038/nn.2103 · Cited by 208 · see citing works
Lenormand, P., Brondello, J., Brunet, A., & Pouysségur, J. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.3.625 · Cited by 207 · see citing works
Associative Learning in Invertebrates
Hawkins, R. D., & Byrne, J. H. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021709 · Cited by 199 · see citing works
Nociceptor Sensitization by Extracellular Signal-Regulated Kinases
Aley, K. O., Martin, A., McMahon, T. J., Mok, J., Levine, J. D., & Messing, R. O. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-17-06933.2001 · Cited by 198 · see citing works
Cavanaugh, J. E., Ham, J., Hetman, M., Poser, S., Yan, C., & Xia, Z. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-02-00434.2001 · Cited by 196 · see citing works
Chronic activation of ERK and neurodegenerative diseases
Colucci‐D'Amato, L., Perrone‐Capano, C., & di Porzio, U. (2003) · BioEssays · doi:10.1002/bies.10355 · Cited by 195 · see citing works
Arendt, T. (2003) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2003.09.007 · Cited by 188 · see citing works
Kushner, S. A., Elgersma, Y., Murphy, G. G., Jaarsma, D., van Woerden, G. M., Hojjati, M. R., Cui, Y., LeBoutillier, J. C., Marrone, D. F., Choi, E. S., et al. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2836-05.2005 · Cited by 188 · see citing works
Is the Ras-MAPK signalling pathway necessary for long-term memory formation?
Orban, P. C., Chapman, P. F., & Brambilla, R. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01306-x · Cited by 186 · see citing works
Smolen, P., Baxter, D. A., & Byrne, J. H. (1998) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1998.274.2.c531 · Cited by 185 · see citing works
ERKI/II Regulation by the Muscarinic Acetylcholine Receptors in Neurons
Rosenblum, K., Futter, M., Jones, M. W., Hulme, E. C., & Bliss, T. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-03-00977.2000 · Cited by 180 · see citing works
Bailey, C. H., Kaang, B., Chen, M., Martin, K. C., Lim, C., Casadio, A., & Kandel, E. R. (1997) · Neuron · doi:10.1016/s0896-6273(00)80331-1 · Cited by 180 · see citing works
Self-citationERK/MAPK regulates the Kv4.2 potassium channel by direct phosphorylation of the pore-forming subunit
Schrader, L. A., Birnbaum, S. G., Nadin, B. M., Ren, Y., Bui, D., Anderson, A. E., & Sweatt, J. D. (2005) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00358.2005 · Cited by 176 · see citing works
In search of general mechanisms for long-lasting plasticity: Aplysia and the hippocampus
Pittenger, C., & Kandel, E. R. (2003) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1247 · Cited by 174 · see citing works
Self-citationDrosophila Perlecan modulates FGF and Hedgehog signals to activate neural stem cell division
Park, Y., Rangel, C., Reynolds, M., Caldwell, M. C., Johns, M., Nayak, M. S., Welsh, C. J., McDermott, S., & Datta, S. (2003) · Developmental Biology · doi:10.1016/s0012-1606(02)00019-2 · Cited by 172 · see citing works
- Authors
- Martin, K. C., Michael, D., Rose, J. C., Barad, M., Casadio, A., Zhu, H., & Kandel, E. R.
- Affiliations
- Howard Hughes Medical Institute (US)
- Columbia University Irving Medical Center (US)
- Corresponding author
- Kandel, Eric R
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 1997-06
- Volume
- 18
- Issue
- 6
- Pages
- 899-912
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2066592391
- Cited by
- 545
- References
- 68
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 8 · 2023: 5 · 2022: 9 · 2021: 9 · 2020: 9 · 2019: 11 · 2018: 13 · 2017: 14 · 2016: 13 · 2015: 14 · 2014: 16 · 2013: 16 · 2012: 14
- FWCI
- 16.93
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Neuron (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- 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
- mitogen-activated protein kinase, nuclear translocation, long-term facilitation, Aplysia, serotonin, cyclic AMP, synaptic plasticity, gene expression, hippocampal long-term potentiation
- MeSH terms
- Cyclic AMP, Amino Acid Sequence, Animals, Aplysia, Cell Compartmentation, Cell Nucleus, Cells, Cultured, Enzyme Inhibitors, Flavonoids, Colforsin, Hippocampus, Molecular Sequence Data, Synaptic Transmission, Neuronal Plasticity, Neurons, Afferent, Peptides, Protein-Tyrosine Kinases, Serotonin, Synapses, Protein Serine-Threonine Kinases, Presynaptic Terminals, Long-Term Potentiation, Calcium-Calmodulin-Dependent Protein Kinases, Mitogen-Activated Protein Kinase Kinases, MAP Kinase Kinase 1
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