Abstract:
Reconsolidation has been defined as the process of memory stabilization after retrieval involving, among others, gene expression regulation and post-translational modifications. Many of these mechanisms are shared with memory consolidation. Here, we studied hippocampal ERK participation on memory reconsolidation of an inhibitory avoidance task in CF-1 mice. We found a retrieval-induced cytosolic ERK2 activation in the hippocampus (HIP) 15. min after memory reactivation, and an inhibition at 45. min. PD098059, a MEK1/2 (MAPK/ERK kinase) inhibitor, administered in the HIP immediately after retrieval impaired memory in a dose-dependent fashion. However, infusions of the highest dose of PD098059 performed 40. min after retrieval enhanced memory in mice trained with a weaker footshock. These results suggest for the first time that ERK2 is involved in memory reconsolidation in a biphasic fashion. Furthermore, the inhibition of ERK could either impair or enhance mice performance depending on ERK state of activation. © 2015 IBRO.
Registro:
Documento: |
Artículo
|
Título: | Memory reconsolidation of an inhibitory avoidance task in mice involves cytosolic ERK2 bidirectional modulation |
Autor: | Krawczyk, M.C.; Blake, M.G.; Baratti, C.M.; Romano, A.; Boccia, M.M.; Feld, M. |
Filiación: | Laboratorio de Neurofarmacología de los Procesos de Memoria, Cátedra de Farmacología, Fac. Farmacia y Bioquímica, UBA, Argentina Laboratorio de Neurobiología de la Memoria, Dto. Fisiología, Biología Molecular y Celular, Fac. Cs. Exactas y Naturales, UBA/IFIByNE, CONICET, Argentina
|
Palabras clave: | ERK; Inhibitory avoidance; MAPK; Memory reconsolidation; Mice; PD098059; 2 (2 amino 3 methoxyphenyl)chromone; mitogen activated protein kinase 1; mitogen activated protein kinase 3; mitogen activated protein kinase 1; animal behavior; animal experiment; animal tissue; Article; avoidance behavior; controlled study; enzyme activation; enzyme inhibition; footshock; hippocampus; inhibition kinetics; male; memory consolidation; mental task; mouse; neuromodulation; nonhuman; priority journal; task performance; animal; avoidance behavior; memory; metabolism; phosphorylation; physiology; protein processing; signal transduction; Animals; Avoidance Learning; Hippocampus; Male; MAP Kinase Signaling System; Memory; Mice; Mitogen-Activated Protein Kinase 1; Phosphorylation; Protein Processing, Post-Translational |
Año: | 2015
|
Volumen: | 294
|
Página de inicio: | 227
|
Página de fin: | 237
|
DOI: |
http://dx.doi.org/10.1016/j.neuroscience.2015.03.019 |
Título revista: | Neuroscience
|
Título revista abreviado: | Neuroscience
|
ISSN: | 03064522
|
CODEN: | NRSCD
|
CAS: | 2 (2 amino 3 methoxyphenyl)chromone, 167869-21-8; mitogen activated protein kinase 1, 137632-08-7; mitogen activated protein kinase 3, 137632-07-6; Mitogen-Activated Protein Kinase 1
|
Registro: | https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03064522_v294_n_p227_Krawczyk |
Referencias:
- Adams, J.P., Anderson, A.E., Varga, A.W., Dineley, K.T., Cook, R.G., Pfaffinger, P.J., The A-type potassium channel Kv4.2 is a substrate for the mitogen-activated protein kinase ERK (2000) J Neurochem, 75, pp. 2277-2287
- Alberini, C.M., Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes? (2005) Trends Neurosci, 28, pp. 51-56
- Alberini, C.M., Transcription factors in long-term memory and synaptic plasticity (2009) Physiol Rev, 89, pp. 121-145
- Bailey, C.H., Kaang, B.K., Chen, M., Martin, K.C., Lim, C.S., Casadio, A., Mutation in the phosphorylation sites of MAP kinase blocks learning-related internalization of apCAM in Aplysia sensory neurons (1997) Neuron, 18, pp. 913-924
- Baratti, C.M., Boccia, M.M., Blake, M.G., Pharmacological effects and behavioral interventions on memory consolidation and reconsolidation (2009) Braz J Med Biol Res, 42, pp. 148-154
- Besnard, A., Caboche, J., Laroche, S., Recall and reconsolidation of contextual fear memory: differential control by ERK and Zif268 expression dosage (2013) PloS One, 8, p. e72006
- Besnard, A., Laroche, S., Caboche, J., Comparative dynamics of MAPK/ERK signalling components and immediate early genes in the hippocampus and amygdala following contextual fear conditioning and retrieval (2014) Brain Struct Funct, 219, pp. 415-430
- Blake, M.G., Boccia, M.M., Baratti, C.M., Behavioral differences on memory retrieval between two variants of step-through inhibitory avoidance task in mice (2008) Neurosci Lett, 444, pp. 102-105
- Blake, M.G., Boccia, M.M., Krawczyk, M.C., Delorenzi, A., Baratti, C.M., Choline reverses scopolamine-induced memory impairment by improving memory reconsolidation (2012) Neurobiol Learn Mem, 98, pp. 112-121
- Blake, M.G., Krawczyk, M.C., Baratti, C.M., Boccia, M.M., Neuropharmacology of memory consolidation and reconsolidation: insights on central cholinergic mechanisms (2014) J Physiol Paris
- Boccia, M., Freudenthal, R., Blake, M., de la Fuente, V., Acosta, G., Baratti, C., Activation of hippocampal nuclear factor-kappa B by retrieval is required for memory reconsolidation (2007) J Neurosci, 27, pp. 13436-13445
- 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
- Boccia, M.M., Blake, M.G., Acosta, G.B., Baratti, C.M., Post-retrieval effects of icv infusions of hemicholinium in mice are dependent on the age of the original memory (2006) Learn Mem, 13, pp. 376-381
- Boccia, M.M., Blake, M.G., Krawczyk, M.C., Baratti, C.M., Hippocampal α7 nicotinic receptors modulate memory reconsolidation of an inhibitory avoidance task in mice (2010) Neuroscience, 171, pp. 531-543
- Boccia, M.M., Blake, M.G., Krawczyk, M.C., Baratti, C.M., Sildenafil, a selective phosphodiesterase type 5 inhibitor, enhances memory reconsolidation of an inhibitory avoidance task in mice (2011) Behav Brain Res, 220, pp. 319-324
- Boggio, E.M., Putignano, E., Sassoè-Pognetto, M., Pizzorusso, T., Giustetto, M., Visual stimulation activates ERK in synaptic and somatic compartments of rat cortical neurons with parallel kinetics (2007) PloS One, 2, p. e604
- Casar, B., Pinto, A., Crespo, P., Essential role of ERK dimers in the activation of cytoplasmic but not nuclear substrates by ERK-scaffold complexes (2008) Mol Cell, 31, pp. 708-721
- Cestari, V., Costanzi, M., Castellano, C., Rossi-Arnaud, C., A role for ERK2 in reconsolidation of fear memories in mice (2006) Neurobiol Learn Mem, 86, pp. 133-143
- Davis, H.P., Squire, L.R., Protein synthesis and memory: a review (1984) Psychol Bull, 96, pp. 518-559
- Dawson, R.G., McGaugh, J.L., Electroconvulsive shock effects on a reactivated memory trace: further examination (1969) Science, 166, pp. 525-527
- Denny, C.A., Kheirbek, M.A., Alba, E.L., Tanaka, K.F., Brachman, R.A., Laughman, K.B., Hippocampal memory traces are differentially modulated by experience, time, and adult neurogenesis (2014) Neuron, 83, pp. 189-201
- Dineley, K.T., Westerman, M., Bui, D., Bell, K., Ashe, K.H., Sweatt, J.D., Beta-amyloid activates the mitogen-activated protein kinase cascade via hippocampal alpha7 nicotinic acetylcholine receptors: in vitro and in vivo mechanisms related to Alzheimer's disease (2001) J Neurosci, 21, pp. 4125-4133
- Dudai, Y., Eisenberg, M., Rites of passage of the engram: reconsolidation and the lingering consolidation hypothesis (2004) Neuron, 44, pp. 93-100
- Duvarci, S., Nader, K., LeDoux, J.E., Activation of extracellular signal-regulated kinase-mitogen-activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning (2005) Eur J Neurosci, 21, pp. 283-289
- Earnest, S., Khokhlatchev, A., Albanesi, J.P., Barylko, B., Phosphorylation of dynamin by ERK2 inhibits the dynamin-microtubule interaction (1996) FEBS Lett, 396, pp. 62-66
- English, J.D., Sweatt, J.D., A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation (1997) J Biol Chem, 272, pp. 19103-19106
- Exton-McGuinness, M.T.J., Lee, J.L.C., Reichelt, A.C., Updating memories-the role of prediction errors in memory reconsolidation (2014) Behav Brain Res, 278 C, pp. 375-384
- Feld, M., Dimant, B., Delorenzi, A., Coso, O., Romano, A., Phosphorylation of extra-nuclear ERK/MAPK is required for long-term memory consolidation in the crab Chasmagnathus (2005) Behav Brain Res, 158, pp. 251-261
- Feld, M., Krawczyk, M.C., Sol Fustiñana, M., Blake, M.G., Baratti, C.M., Romano, A., Decrease of ERK/MAPK overactivation in prefrontal cortex reverses early memory deficit in a mouse model of Alzheimer's disease (2014) J Alzheimers Dis, 40, pp. 69-82
- Flexner, J.B., Flexner, L.B., Stellar, E., Memory in mice as affected by intracerebral puromycin (1963) Science, 141, pp. 57-59
- Forcato, C., Fernandez, R.S., Pedreira, M.E., Strengthening a consolidated memory: the key role of the reconsolidation process (2014) J Physiol Paris, 108, pp. 323-333
- Franklin, K.B.J., Paxinos, G., (1997) The mouse brain in stereotaxic coordinates, , Academic Press, San Diego
- Freudenthal, R., Locatelli, F., Hermitte, G., Maldonado, H., Lafourcade, C., Delorenzi, A., Kappa-B like DNA-binding activity is enhanced after spaced training that induces long-term memory in the crab Chasmagnathus (1998) Neurosci Lett, 242, pp. 143-146
- Fukushima, H., Zhang, Y., Archbold, G., Ishikawa, R., Nader, K., Kida, S., Enhancement of fear memory by retrieval through reconsolidation (2014) eLife, 3, p. e02736
- Gold, P.E., The use of avoidance training in studies of modulation of memory storage (1986) Behav Neural Biol, 46, pp. 87-98
- Gong, R., Tang, S.-J., Mitogen-activated protein kinase signaling is essential for activity-dependent dendritic protein synthesis (2006) Neuroreport, 17, pp. 1575-1578
- Ivanov, A., Pellegrino, C., Rama, S., Dumalska, I., Salyha, Y., Ben-Ari, Y., Opposing role of synaptic and extrasynaptic NMDA receptors in regulation of the extracellular signal-regulated kinases (ERK) activity in cultured rat hippocampal neurons (2006) J Physiol, 572, pp. 789-798
- Kandel, E.R., Schwartz, J.H., Molecular biology of learning: modulation of transmitter release (1982) Science, 218, pp. 433-443
- Kelleher, R.J., Govindarajan, A., Jung, H.-Y., Kang, H., Tonegawa, S., Translational control by MAPK signaling in long-term synaptic plasticity and memory (2004) Cell, 116, pp. 467-479
- Kelly, A., Laroche, S., Davis, S., Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory (2003) J Neurosci, 23, pp. 5354-5360
- Korzus, E., Rosenfeld, M.G., Mayford, M., CBP histone acetyltransferase activity is a critical component of memory consolidation (2004) Neuron, 42, pp. 961-972
- Krapivinsky, G., Krapivinsky, L., Manasian, Y., Ivanov, A., Tyzio, R., Pellegrino, C., The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1 (2003) Neuron, 40, pp. 775-784
- Lattal, K.M., Abel, T., Different requirements for protein synthesis in acquisition and extinction of spatial preferences and context-evoked fear (2001) J Neurosci, 21, pp. 5773-5780
- Leal, G., Comprido, D., Duarte, C.B., BDNF-induced local protein synthesis and synaptic plasticity (2014) Neuropharmacology, 76, pp. 639-656
- Maldonado, N.M., Espejo, P.J., Martijena, I.D., Molina, V.A., Activation of ERK2 in basolateral amygdala underlies the promoting influence of stress on fear memory and anxiety: influence of midazolam pretreatment (2014) Eur Neuropsychopharmacol, 24, pp. 262-270
- Martijena, I.D., Molina, V.A., The influence of stress on fear memory processes (2012) Braz J Med Biol Res, 45, pp. 308-313
- Martin, K.C., Michael, D., Rose, J.C., Barad, M., Casadio, A., Zhu, H., Kandel, E.R., MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia (1997) Neuron, 18, pp. 899-912
- Mazzucchelli, C., Knockout of ERK1 MAP kinase enhances synaptic plasticity in the striatum and facilitates striatal-mediated learning and memory (2002) Neuron, 34, pp. 807-820
- McGaugh, J.L., Time-dependent processes in memory storage (1966) Science, 153, pp. 1351-1358
- McGaugh, J.L., Memory-a century of consolidation (2000) Science, 287, pp. 248-251
- McGaugh, J.L., Izquierdo, I., The contribution of pharmacology to research on the mechanisms of memory formation (2000) Trends Pharmacol Sci, 21, pp. 208-210
- Milekic, M.H., Alberini, C.M., Temporally graded requirement for protein synthesis following memory reactivation (2002) Neuron, 36, pp. 521-525
- Milekic, M.H., Pollonini, G., Alberini, C.M., Temporal requirement of C/EBPbeta in the amygdala following reactivation but not acquisition of inhibitory avoidance (2007) Learn Mem, 14, pp. 504-511
- Miller, C.A., Marshall, J.F., Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory (2005) Neuron, 47, pp. 873-884
- Misanin, J.R., Miller, R.R., Lewis, D.J., Retrograde amnesia produced by electroconvulsive shock after reactivation of a consolidated memory trace (1968) Science, 160, pp. 554-555
- Nader, K., Schafe, G.E., Le Doux, J.E., Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval (2000) Nature, 406, pp. 722-726
- Pedreira, M.E., Maldonado, H., Protein synthesis subserves reconsolidation or extinction depending on reminder duration (2003) Neuron, 38, pp. 863-869
- Pedreira, M.E., Pérez-Cuesta, L.M., Maldonado, H., Mismatch between what is expected and what actually occurs triggers memory reconsolidation or extinction (2004) Learn Mem, 11, pp. 579-585
- Power, A.E., Berlau, D.J., McGaugh, J.L., Steward, O., Anisomycin infused into the hippocampus fails to block "reconsolidation" but impairs extinction: the role of re-exposure duration (2006) Learn Mem, 13, pp. 27-34
- Przybyslawski, J., Roullet, P., Sara, S.J., Attenuation of emotional and nonemotional memories after their reactivation: role of beta adrenergic receptors (1999) J Neurosci, 19, pp. 6623-6628
- Samuels, I.S., Karlo, J.C., Faruzzi, A.N., Pickering, K., Herrup, K., Sweatt, J.D., Deletion of ERK2 mitogen-activated protein kinase identifies its key roles in cortical neurogenesis and cognitive function (2008) J Neurosci, 28, pp. 6983-6995
- Sara, S.J., Retrieval and reconsolidation: toward a neurobiology of remembering (2000) Learn Mem, 7, pp. 73-84
- Satoh, Y., Endo, S., Nakata, T., Kobayashi, Y., Yamada, K., Ikeda, T., ERK2 contributes to the control of social behaviors in mice (2011) J Neurosci, 31, pp. 11953-11967
- Selkoe, D.J., Alzheimer's disease: genes, proteins, and therapy (2001) Physiol Rev, 81, pp. 741-766
- Siegel, S., (1956) Nonparametric statistics for the behavioral sciences, , McGraw-Hill
- Squire, L.R., Slater, P.C., Chace, P.M., Reactivation of recent or remote memory before electroconvulsive therapy does not produce retrograde amnesia (1976) Behav Biol, 18, pp. 335-343
- Suzuki, A., Josselyn, S.A., Frankland, P.W., Masushige, S., Silva, A.J., Kida, S., Memory reconsolidation and extinction have distinct temporal and biochemical signatures (2004) J Neurosci, 24, pp. 4787-4795
- Sweatt, J.D., Mitogen-activated protein kinases in synaptic plasticity and memory (2004) Curr Opin Neurobiol, 14, pp. 311-317
- Taubenfeld, S.M., Milekic, M.H., Monti, B., Alberini, C.M., The consolidation of new but not reactivated memory requires hippocampal C/EBPbeta (2001) Nat Neurosci, 4, pp. 813-818
- Vianna, M.R., Szapiro, G., McGaugh, J.L., Medina, J.H., Izquierdo, I., Retrieval of memory for fear-motivated training initiates extinction requiring protein synthesis in the rat hippocampus (2001) Proc Natl Acad Sci U S A, 98, pp. 12251-12254
- Wang, J., Chen, Y.B., Zhu, X.N., Chen, R.Z., Activation of p42/44 mitogen-activated protein kinase pathway in long-term potentiation induced by nicotine in hippocampal CA1 region in rats (2001) Acta Pharmacol Sin, 22, pp. 685-690
- Yuan, L.-L., Adams, J.P., Swank, M., Sweatt, J.D., Johnston, D., Protein kinase modulation of dendritic K+ channels in hippocampus involves a mitogen-activated protein kinase pathway (2002) J Neurosci, 22, pp. 4860-4868
- Zhai, S., Ark, E.D., Parra-Bueno, P., Yasuda, R., Long-distance integration of nuclear ERK signaling triggered by activation of a few dendritic spines (2013) Science, 342, pp. 1107-1111
Citas:
---------- APA ----------
Krawczyk, M.C., Blake, M.G., Baratti, C.M., Romano, A., Boccia, M.M. & Feld, M.
(2015)
. Memory reconsolidation of an inhibitory avoidance task in mice involves cytosolic ERK2 bidirectional modulation. Neuroscience, 294, 227-237.
http://dx.doi.org/10.1016/j.neuroscience.2015.03.019---------- CHICAGO ----------
Krawczyk, M.C., Blake, M.G., Baratti, C.M., Romano, A., Boccia, M.M., Feld, M.
"Memory reconsolidation of an inhibitory avoidance task in mice involves cytosolic ERK2 bidirectional modulation"
. Neuroscience 294
(2015) : 227-237.
http://dx.doi.org/10.1016/j.neuroscience.2015.03.019---------- MLA ----------
Krawczyk, M.C., Blake, M.G., Baratti, C.M., Romano, A., Boccia, M.M., Feld, M.
"Memory reconsolidation of an inhibitory avoidance task in mice involves cytosolic ERK2 bidirectional modulation"
. Neuroscience, vol. 294, 2015, pp. 227-237.
http://dx.doi.org/10.1016/j.neuroscience.2015.03.019---------- VANCOUVER ----------
Krawczyk, M.C., Blake, M.G., Baratti, C.M., Romano, A., Boccia, M.M., Feld, M. Memory reconsolidation of an inhibitory avoidance task in mice involves cytosolic ERK2 bidirectional modulation. Neuroscience. 2015;294:227-237.
http://dx.doi.org/10.1016/j.neuroscience.2015.03.019