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Abstract:

NF-κB is an evolutionarily conserved family of transcription factors (TFs) critically involved in basic cellular mechanisms of the immune response, inflammation, development and apoptosis. In spite of the fact that it is expressed in the central nervous system, particularly in areas involved in memory processing, and is activated by signals such as glutamate and Ca 2+, its role in neural plasticity and memory has only recently become apparent. A surprising feature of this molecule is its presence within the synapse. An increasing number of reports have called attention to the role of this TF in processes that require long-term regulation of the synaptic function underlying memory and neural plasticity. Here we review the evidence regarding a dual role for NF-κB, as both a signalling molecule after its activation at the synapse and a transcriptional regulator upon reaching the nucleus. The specific role of this signal, as well as the general transcriptional mechanism, in the process of memory formation is discussed. Converging lines of evidence summarized here point to a pivotal role for the NF-κB transcription factor as a direct signalling mechanism in the regulation of gene expression involved in long-term memory. © The Authors (2006).

Registro:

Documento: Artículo
Título:Evolutionarily-conserved role of the NF-κB transcription factor in neural plasticity and memory
Autor:Romano, A.; Freudenthal, R.; Merlo, E.; Routtenberg, A.
Filiación:Laboratorio de Neurobiología de la Memoria, Departamento de Fisiología, Biología Molecular Y Celular, Pab. II, (1428) Buenos Aires, Argentina
Cresap Neuroscience Laboratory, North-western University, Evanston, IL, United States
Palabras clave:Gene expression; Long-term memory; Synaptic plasticity; immunoglobulin enhancer binding protein; transcription factor; cell nucleus; gene expression regulation; genetic transcription; invertebrate; knockout mouse; long term memory; mammal; nerve cell plasticity; nonhuman; priority journal; protein function; review; signal transduction; synapse; Animals; Biological Evolution; Evolution; Gene Expression; Humans; Memory; Models, Biological; Neuronal Plasticity; NF-kappa B
Año:2006
Volumen:24
Número:6
Página de inicio:1507
Página de fin:1516
DOI: http://dx.doi.org/10.1111/j.1460-9568.2006.05022.x
Título revista:European Journal of Neuroscience
Título revista abreviado:Eur. J. Neurosci.
ISSN:0953816X
CODEN:EJONE
CAS:NF-kappa B
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_0953816X_v24_n6_p1507_Romano

Referencias:

  • Abel, T., Martin, K.C., Bartsch, D., Kandel, E.R., Memory suppressor genes: Inhibitory constraints on the storage of long-term memory (1998) Science, 279, pp. 338-341
  • Albensi, B.C., Mattson, M.P., Evidence for the involvement of TNF and NF-kappaB in hippocampal synaptic plasticity (2000) Synapse, 35, pp. 151-159
  • Alcamo, E., Mizgerd, J.P., Horwitz, B.H., Bronson, R., Beg, A.A., Scott, M., Doerschuk, C.M., Baltimore, D., Targeted mutation of TNF receptor I rescues the RelA-deficient mouse and reveals a critical role for NF-κB in leukocyte recruitment (2001) J. Immunol., 167, pp. 1592-1600
  • Bailey, C.H., Bartsch, D., Kandel, E.R., Toward a molecular definition of long-term memory storage (1996) Proc. Natl Acad. Sci. USA, 93, pp. 13445-13452
  • Balschun, D., Wolfer, D.P., Gass, P., Mantamadiotis, T., Welzl, H., Schutz, G., Frey, J.U., Lipp, H.P., Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory? (2003) J. Neurosci., 23, pp. 6304-6314
  • Barger, S.W., Moerman, A.M., Mao, X., Molecular mechanisms of cytokine-induced neuroprotection: NFkappaB and neuroplasticity (2005) Curr. Pharm. Des., 11, pp. 985-998
  • Beg, A.A., Sha, W.C., Bronson, R.T., Ghosh, S., Baltimore, D., Embryonic lethality and liver degeneration in mice lacking the RelA component of NF-κB (1995) Nature, 376, pp. 167-170
  • Boccia, M.M., Acosta, G.B., Blake, M.G., Baratti, C.M., Memory consolidation and reconsolidation of an inhibitory avoidance response in mice: Effects of i.c.v. injections of hemicholinium-3 (2004) Neuroscience, 124, pp. 735-741
  • Brink, J.J., Davis, R.E., Agranoff, B.W., Effects of puromycin, acetoxycycloheximide and actinomycin D on protein synthesis in goldfish brain (1966) J. Neurochem., 13, pp. 889-896
  • Cavallaro, S., D'Agata, V., Manickam, P., Dufour, F., Alkon, D.L., Memory-specific temporal profiles of gene expression in the hippocampus (2002) Proc. Natl Acad. Sci. USA, 99, pp. 16279-16284
  • Cavallaro, S., Schreurs, B.G., Zhao, W., D'Agata, V., Alkon, D.L., Gene expression profiles during long-term memory consolidation (2001) Eur. J. Neurosci., 13, pp. 1809-1815
  • Choi, J., Krushel, L.A., Crossin, K.L., NF-kappaB activation by NCAM and cytokines in astrocytes is regulated by multiple protein kinases and redox modulation (2001) Glia, 33, pp. 45-56
  • Cui, Z., Wang, H., Tan, Y., Zaia, K.A., Zhang, S., Tsien, J.Z., Inducible and reversible NR1 knockout reveals crucial role of the NMDA receptor in preserving remote memories in the brain (2004) Neuron, 41, pp. 781-793
  • Davis, H.P., Squire, L.R., Protein synthesis and memory: A review (1984) Psychol. Bull., 96, pp. 518-559
  • Debiec, J., Ledoux, J.E., Nader, K., Cellular and systems reconsolidation in the hippocampus (2002) Neuron, 36, pp. 527-538
  • Deisseroth, K., Heist, E.K., Tsien, R.W., Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons (1998) Nature, 392, pp. 198-202
  • Deisseroth, K., Mermelstein, P.G., Xia, H., Tsien, R.W., Signaling from synapse to nucleus: The logic behind the mechanisms (2003) Curr. Opin. Neurobiol., 13, pp. 354-365
  • Delorenzi, A., Dimant, B., Frenkel, L., Nahmod, V.E., Nassel, D.R., Maldonado, H., High environmental salinity induces memory enhancement and increases levels of brain angiotensin-like peptides in the crab Chasmagnathus granulatus (2000) J. Exp. Biol., 203, pp. 3369-3379
  • Delorenzi, A., Pedreira, E.M., Romano, A., García, S., Pirola, C., Nahmod, V., Maldonado, H., Angiotensin II enhances long-term memory in the crab Chasmagnathus (1996) Brain Res. Bull., 47, pp. 211-219
  • Dudai, Y., Molecular bases of long-term memories: A question of persistence (2002) Curr. Opin. Neurobiol., 12, pp. 211-216
  • Feld, M., Dimant, B., Delorenzi, A., Coso, O., Romano, A., Extranuclear activation of ERK/MAPK is required for long-term memory consolidation in the crab Chasmagnathus (2005) Behav. Brain Res., 150, pp. 251-261
  • Flexner, L.B., Loss of memory in mice as related to regional inhibition of cerebral protein synthesis (1966) Tex. Report Biol. Med., 24, pp. 3-19
  • Frenkel, L., Freudenthal, R., Romano, A., Nahmod, V.E., Maldonado, H., Delorenzi, A., Angiotensin II and transcription factor Rel/NF-kappaB link environmental water shortage with memory improvement (2002) Neuroscience, 115, pp. 1079-1087
  • Frenkel, L., Maldonado, H., Delorenzi, A., Memory strengthening by a real-life episode during reconsolidation: An outcome of water deprivation via brain angiotensin II (2005) Eur. J. Neurosci., 22, pp. 1757-1766
  • Freudenthal, R., Boccia, M.M., Acosta, G.B., Blake, M.G., Merlo, E., Baratti, C.M., Romano, A., NF-kappaB transcription factor is required for inhibitory avoidance long-term memory in mice (2005) Eur. J. Neurosci., 21, pp. 2845-2852
  • Freudenthal, R., Locatelli, F., Hermitte, G., Maldonado, H., Delorenzi, A., Lafourcade, C., Romano, A., Kappa-B like DNA-binding activity is enhanced after a spaced training that induces long-term memory in the crab Chasmagnathus (1998) Neurosci. Lett., 242, pp. 143-146
  • Freudenthal, R., Romano, A., Participation of NF-kB transcription factors in long-term memory in the crab Chasmagnathus (2000) Brain Res., 855, pp. 274-281
  • Freudenthal, R., Romano, A., Routtenberg, A., Activation of the transcription factor NF-κB after in vivo perforant path LTP in the mouse hippocampus (2004) Hippocampus, 14, pp. 677-683
  • Frey, U., Morris, R.G., Synaptic tagging: Implications for late maintenance of hippocampal long-term potentiation (1998) Trend Neurosci., 21, pp. 181-188
  • Gerlai, R., Gene-targeting studies of mammalian behavior: Is it the mutation or the background genotype? (1996) Trends Neurosci., 19, pp. 177-181
  • Ghosh, S., Karin, M., Missing pieces in the NF-kappaB puzzle (2002) Cell, 109 (SUPPL.), pp. S81-S96
  • Goelet, P., Castellucci, V.F., Schacher, S., Kandel, E.R., The long and the short of long-term memory - A molecular framework (1986) Nature, 322, pp. 419-422
  • Guerrini, L., Blasi, F., Denis-Donini, S., Synaptic activation of NF-kappa B by glutamate in cerebellar granule neurons in vitro (1995) Proc. Natl Acad. Sci. USA, 92, pp. 9077-9081
  • Gutierrez, H., Hale, V.A., Dolcet, X., Davies, A., NF-κB signalling regulates the growth of neural processes in the developing PNS and CNS (2005) Development, 132, pp. 1713-1726
  • Hermitte, G., Pedreira, M.E., Tomsic, D., Maldonado, H., Context shift and protein synthesis inhibition disrupt long-term habituation after spaced, but not massed, training in the crab Chasmagnathus (1999) Neurobiol. Learn. Mem., 71, pp. 34-49
  • Hohmann, H.P., Remy, R., Aigner, L., Brockhaust, M., Van Loon, A.P., Protein kinases negatively affect nuclear factor-kappa B activation by tumor necrosis factor-alpha at two different stages in promyelocytic HL60 cells (1992) J. Biol. Chem., 267, pp. 2065-2072
  • Hoult, J.R., Pharmacological and biochemical actions of sulphasalazine (1986) Drugs, 32, pp. 18-26
  • Huguet, C., Crepieux, P., Laudet, V., Rel/NF-kappa B transcription factors and I kappa B inhibitors: Evolution from a unique common ancestor (1997) Oncogene, 15, pp. 2965-2974
  • Kaang, B.K., Kandel, E.R., Grant, S.G., Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons (1993) Neuron, 10, pp. 427-435
  • Kaltschmidt, C., Kaltschmidt, B., Bauerle, P.A., Brain synapses contain inducible forms of the transcription factor NF-kappa B (1993) Mech. Dev., 43, pp. 135-147
  • Kaltschmidt, B., Ndiaye, D., Korte, M., Pothion, S., Arbibe, L., Prullage, M., Pfeiffer, J., Memet, S., NF-kappaB regulates spatial memory formation and synaptic plasticity through protein kinase A/CREB signaling (2006) Mol Cell Biol., 26, pp. 2936-2946
  • Kaltschmidt, B., Widera, D., Kaltschmidt, C., Signaling via NF-kappaB in the nervous system (2005) Biochim. Biophys. Acta, 1745, pp. 287-299
  • Kandel, E.R., The molecular biology of memory storage: A dialogue between genes and synapses (2001) Science, 29, pp. 1030-1038
  • Kassed, C.A., Herkenham, M., NF-kappaB p50-decient mice show reduced anxiety-like behaviors in tests of exploratory drive and anxiety (2004) Behav. Brain Res., 154, pp. 577-584
  • Kassed, C.A., Willing, A.E., Garbuzova-Davis, S., Sanberg, P.R., Pennypacker, K.R., Lack of NF-kappaB p50 exacerbates degeneration of hippocampal neurons after chemical exposure and impairs learning (2002) Exp. Neurol., 176, pp. 277-288
  • Kinney, W., Routtenberg, A., Brief exposure to a novel environment enhances binding of hippocampal transcription factors to their DNA recognition elements (1993) Brain Res. Mol. Brain Res., 20, pp. 147-152
  • Korner, M., Rattner, A., Mauxion, F., Sen, R., Citri, Y., A brain-specific transcription activator (1989) Neuron, 3, pp. 563-572
  • Krushel, L.A., Cunningham, B.A., Edelman, G.M., Crossin, K.L., NF-kappaB activity is induced by neural cell adhesion molecule binding to neurons and astrocytes (1999) J. Biol. Chem., 274, pp. 2432-2439
  • Lee, J.L.C., Everitt, B.J., Thomas, K.L., Independent cellular processes for hippocampal memory consolidation and reconsolidation (2004) Science, 304, pp. 839-843
  • Levenson, J.M., Choi, S., Lee, S.Y., Cao, Y.A., Ahn, H.J., Worley, K.C., Pizzi, M., Sweatt, J.D., A bioinformatics analysis of memory consolidation reveals involvement of the transcription factor c-rel (2004) J. Neurosci., 24, pp. 3933-3943
  • Locatelli, F., Maldonado, H., Romano, A., Two critical periods for cAMP-dependent protein kinase activity during long-term memory consolidation in the crab Chasmagnathus (2002) Neurobiol. Learn. Mem., 77, pp. 234-249
  • Locatelli, F., Romano, A., Differential role of cAMP-dependent protein kinase isoforms during long-term memory consolidation in the crab Chasmagnathus (2005) Neurobiol. Learn. Mem., 83, pp. 232-242
  • Lozada, M., Romano, A., Maldonado, H., Long-term habituation in the crab Chasmagnathus granulatus (1990) Phisiol. Behav., 47, pp. 35-41
  • Mactutus, C.F., Riccio, D.C., Ferek, J.M., Retrograde amnesia for old (reactivated) memory: Some anomalous characteristics (1979) Science, 204, pp. 1319-1320
  • Marini, A.M., Jiang, X., Wu, X., Tian, F., Zhu, D., Okagaki, P., Lipsky, R.H., Role of brain-derived neurotrophic factor and NF-kappaB in neuronal plasticity and survival: From genes to phenotype (2004) Restor. Neurol. Neurosci., 22, pp. 121-130
  • Mattson, M.P., Camandola, S., NF-kappaB in neuronal plasticity and neurodegenerative disorders (2001) J. Clin. Invest., 107, pp. 247-254
  • Mattson, M.P., Meffert, M.K., Roles for NF-kappaB in nerve cell survival, plasticity, and disease (2006) Cell Death. Differ., 13, pp. 852-860
  • Meberg, P.J., Kinney, W.R., Valcourt, E.G., Routtenberg, A., Gene expression of the transcription factor NF-B in hippocampus: Regulation by synaptic activity (1996) Mol. Brain Res., 38, pp. 179-190
  • Meffert, M.K., Baltimore, D., Physiological functions for brain NF-kappaB (2005) Trends Neurosci., 28, pp. 37-43
  • Meffert, M.K., Chang, J.M., Wiltgen, B.J., Fanselow, M.S., Baltimore, D., NF-κB function in synaptic signaling and behavior (2003) Nature Neurosci., 6, pp. 1072-1078
  • Mellstrom, B., Torres, B., Link, W.A., Naranjo, J.R., The BDNF gene: Exemplifying complexity in Ca2+-dependent gene expression (2004) Crit. Rev. Neurobiol., 16, pp. 43-49
  • Merlo, E., Freudenthal, R., Maldonado, H., Romano, A., Activation of the transcription factor NF-κB by retrieval is required for long-term memory reconsolidation (2005) Learn. Mem., 12, pp. 23-29
  • Merlo, E., Freudenthal, R., Romano, A., The IkappaB kinase inhibitor sulfasalazine impairs long-term memory in the crab Chasmagnathus (2002) Neuroscience, 112, pp. 161-172
  • Misanin, J.R., Miller, R.R., Lewis, D.J., Retrograde amnesia produced by electroconvulsive shock following reactivation of a consolidated memory trace (1968) Science, 16, pp. 554-555
  • Morgan, J.M., Routtenberg, A., Angiotensin injected into the neostriatum after learning disrupts retention performance (1977) Science, 196, pp. 87-89
  • Myers, K.M., Davis, M., Behavioral and neural analysis of extinction (2002) Neuron, 36, pp. 567-584
  • Nader, K., Schafe, G.E., Ledoux, J.E., Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval (2000) Nature, 406, pp. 722-726
  • O'Neill, L.A.J., Kaltschmidt, C., NFκ-B: A crucial transcription factor for glial and neuronal cell function (1997) Trends Neurosci., 20, pp. 252-258
  • Pedreira, M.E., Dimant, B., Maldonado, H., Inhibitors of protein and RNA synthesis block context memory and long-term habituation in the crab Chasmagnathus (1996) Pharmacol. Biochem. Behav., 54, pp. 611-617
  • Pedreira, M.E., Dimant, B., Tomsic, D., Quesada-Allue, L.A., Maldonado, H., Cycloheximide inhibits long-term habituation and context memory in the crab Chasmagnathus (1995) Pharmacol. Biochem. Behav., 52, pp. 385-395
  • Pedreira, M.E., Maldonado, H., Protein synthesis subserves reconsolidation or extinction depending on reminder duration (2003) Neuron, 38, pp. 863-869
  • Pedreira, M.E., Perez-Cuesta, L.M., Maldonado, H., Reactivation and reconsolidation of long-term memory in the crab Chasmagnathus: Protein synthesis requirement and mediation by NMDA-type glutamatergic receptors (2002) J. Neurosci., 22, pp. 8305-8311
  • Pedreira, M.E., Romano, A., Tomsic, D., Lozada, M., Maldonado, H., Massed and spaced training build up different components of long-term habituation in the crab Chasmagnathus (1998) Anim. Learn. Behav., 26, pp. 34-38
  • Pereyra, P., Gonzale, Z., Portino, E., Maldonado, H., Long-lasting and context-specific freezing preference is acquired after spaced repeated presentations of a danger stimulus in the crab Chasmagnathus (2000) Neurobiol. Learn. Mem., 74, pp. 119-134
  • Routtenberg, A., Anatomical localization of phosphoprotein and glycoprotein substrates of memory (1979) Prog. Neurobiol., 12, pp. 85-113
  • Routtenberg, A., Reverse piedpiperase: Is the knockout mouse leading neuroscientists to a watery end? (1996) Trends Neurosci., 19, pp. 471-472
  • Routtenberg, A., Rekart, J.L., Post-translational protein modification for long-lasting memory (2005) Trends Neurosci., 28, pp. 12-19
  • Saccani, S., Pantano, S., Natoli, G., Two waves of nuclear factor kappaB recruitment to target promoters (2001) J. Exp. Med., 193, pp. 1351-1359
  • Salinska, E., Bourne, R.C., Rose, S.P.R., Reminder effects: The molecular cascade following a reminder in young chicks does not recapitulate that following training on a passive avoidance task (2004) Eur. J. Neurosci., 19, pp. 3042-3047
  • Sara, S.J., Retrieval and reconsolidation: Toward a neurobiology of remembering (2000) Learn. Mem., 7, pp. 73-84
  • Thompson, K.R., Otis, K.O., Chen, D.Y., Zhao, Y., O'Dell, T.J., Martin, K.C., Synapse to nucleus signaling during long-term synaptic plasticity; a role for the classical active nuclear import pathway (2004) Neuron, 44, pp. 997-1009
  • Tomsic, D., Pedreira, E.M., Romano, A., Maldonado, H., Context-US association as a determinant of long-term habituation in the crab Chasmagnathus (1998) Anim Learn. Behav., 26, pp. 196-209
  • Wahl, C., Liptay, S., Adler, G., Schmid, R., Sulfasalazine: A potent and specific inhibitor of Nuclear Factor Kappa B (1998) J. Clin. Invest., 101, pp. 1163-1174
  • Weber, C.K., Liptay, S., Wirth, T., Adler, G., Schmid, R.M., Suppression of NF-kappaB activity by sulfasalazine is mediated by direct inhibition of IkappaB kinases alpha and beta (2000) Gastroenterology, 119, pp. 1209-1218
  • Wellmann, H., Kaltschmidt, B., Kaltschmidt, C., Retrograde transport of transcription factor NF-kappaB in living neurons (2001) J. Biol. Chem., 276, pp. 11821-11829
  • Yeh, S.H., Lin, C.H., Gean, P.W., Acetylation of nuclear factor-kappaB in rat amygdala improves long-term but not short-term retention of fear memory (2004) Mol. Pharmacol., 65, pp. 1286-1292
  • Yeh, S.H., Lin, C.H., Lee, C.F., Gean, P.W., A requirement of nuclear factor-kappaB activation in fear-potentiated startle (2002) J. Biol. Chem., 277, pp. 46720-46729
  • Yin, J.C., Tully, T., CREB and the formation of long-term memory (1996) Curr. Opin. Neurobiol., 6, pp. 264-268
  • Zhong, H., Voll, R.E., Ghosh, S., Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300 (1998) Mol. Cell., 1, pp. 661-671

Citas:

---------- APA ----------
Romano, A., Freudenthal, R., Merlo, E. & Routtenberg, A. (2006) . Evolutionarily-conserved role of the NF-κB transcription factor in neural plasticity and memory. European Journal of Neuroscience, 24(6), 1507-1516.
http://dx.doi.org/10.1111/j.1460-9568.2006.05022.x
---------- CHICAGO ----------
Romano, A., Freudenthal, R., Merlo, E., Routtenberg, A. "Evolutionarily-conserved role of the NF-κB transcription factor in neural plasticity and memory" . European Journal of Neuroscience 24, no. 6 (2006) : 1507-1516.
http://dx.doi.org/10.1111/j.1460-9568.2006.05022.x
---------- MLA ----------
Romano, A., Freudenthal, R., Merlo, E., Routtenberg, A. "Evolutionarily-conserved role of the NF-κB transcription factor in neural plasticity and memory" . European Journal of Neuroscience, vol. 24, no. 6, 2006, pp. 1507-1516.
http://dx.doi.org/10.1111/j.1460-9568.2006.05022.x
---------- VANCOUVER ----------
Romano, A., Freudenthal, R., Merlo, E., Routtenberg, A. Evolutionarily-conserved role of the NF-κB transcription factor in neural plasticity and memory. Eur. J. Neurosci. 2006;24(6):1507-1516.
http://dx.doi.org/10.1111/j.1460-9568.2006.05022.x