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Abstract:

Gene expression is a necessary step for memory re-stabilization after retrieval, a process known as reconsolidation. Histone acetylation is a fundamental mechanism involved in epigenetic regulation of gene expression and has been implicated in memory consolidation. However, few studies are available in reconsolidation, all of them in vertebrate models. Additionally, the recruitment of histone acetylation as a function of different memory strengths has not been systematically analyzed before. Here we studied the role of histone acetylation in reconsolidation using a well-characterized memory model in invertebrate, the context-signal memory in the crab Chasmagnathus. Firstly, we found an increase in histone H3 acetylation 1. h after memory reactivation returning to basal levels at 3. h. Strikingly, this increment was only detected during reconsolidation of a long-term memory induced by a strong training of 30 trials, but not for a short-term memory formed by a weak training of five trials or for a long-term memory induced by a standard training of 15 trials. Furthermore, we showed that a weak memory which was enhanced during consolidation by histone deacetylases inhibition, also recruited histone H3 acetylation in reconsolidation as the strong training does. Accordingly, we found the first evidence that the administration of a histone acetyl transferase inhibitor during memory reconsolidation impairs long-term memory re-stabilization. Finally, we found that strong training memory, at variance with the standard training memory, was resistant to extinction, indicating that such strong training induced in fact a stronger memory. In conclusion, the results presented here support that the participation of histone acetylation during reconsolidation is an evolutionary conserved feature and constitutes a specific molecular characteristic of strong memories. © 2012 IBRO.

Registro:

Documento: Artículo
Título:Reconsolidation involves histone acetylation depending on the strength of the memory
Autor:Federman, N.; Fustiñana, M.S.; Romano, A.
Filiación:Laboratorio de Neurobiologia de la Memoria, Departamento de Fisiologia, Biologia Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, IFIByNE, CONICET, Ciudad Universitaria, Pab. II, 2do piso (1428EHA), Buenos Aires, Argentina
Palabras clave:HAT inhibitor; HDAC inhibitor; Histone acetylation; Long-term memory; Reconsolidation; butyric acid; histone deacetylase; histone H3; animal experiment; animal tissue; article; brain tissue; Chasmagnathus granulatus; context signal memory; controlled study; crab; enzyme inhibition; histone acetylation; long term memory; male; memory; memory consolidation; memory reconsolidation; nonhuman; priority journal; reinforcement; short term memory; Acetylation; Animals; Brachyura; Histones; Male; Memory
Año:2012
Volumen:219
Página de inicio:145
Página de fin:156
DOI: http://dx.doi.org/10.1016/j.neuroscience.2012.05.057
Título revista:Neuroscience
Título revista abreviado:Neuroscience
ISSN:03064522
CODEN:NRSCD
CAS:butyric acid, 107-92-6, 156-54-7, 461-55-2; histone deacetylase, 9076-57-7; Histones
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_03064522_v219_n_p145_Federman

Referencias:

  • Agranoff, B.W., Davis, R.E., Casola, L., Lim, R., Actinomycin D blocks formation of memory of shock avoidance in goldfish (1967) Science, 158 (808), pp. 1600-1601
  • 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., The role of protein synthesis during the labile phases of memory: revisiting the skepticism (2008) Neurobiol Learn Mem, 89, pp. 234-246
  • Annau, Z., Kamin, L.J., The conditioned emotional response as a function of intensity of the US (1961) J Comp Physiol Psychol, 54, pp. 428-432
  • Bredy, T.W., Wu, H., Crego, C., Zellhoefer, J., Sun, Y.E., Barad, M., Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear (2007) Learn Mem, 14 (4), pp. 268-276
  • Bredy, T.W., Barad, M., The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear (2008) Learn Mem, 15, pp. 39-45
  • Bustos, S.G., Giachero, M., Maldonado, H., Molina, V.A., Previous stress attenuates the susceptibility to Midazolam's disruptive effect on fear memory reconsolidation: influence of pre-reactivation d-cycloserine administration (2010) Neuropsychopharmacology, 35, pp. 1097-1108
  • Carbo Tano, M., Molina, V.A., Maldonado, H., Pedreira, M.E., Memory consolidation and reconsolidation in an invertebrate model: the role of the GABAergic system (2009) Neuroscience, 158, pp. 387-401
  • Dudai, Y., The neurobiology of consolidations, or, how stable is the engram? (2004) Annu Rev Psychol, 55, pp. 51-86
  • Dudai, Y., Reconsolidation: the advantage of being refocused (2006) Curr Opin Neurobiol, 16, pp. 174-178
  • Federman, N., Fustiñana, M.S., Romano, A., Histone acetylation is recruited in consolidation as a molecular feature of stronger memories (2009) Learn Mem, 16, pp. 600-606
  • Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M., Tsai, L., Recovery of learning and memory is associated with chromatin remodelling (2007) Nature, 447, pp. 178-182
  • Forcato, C., Rodríguez, M.L., Pedreira, M.E., Repeated labilization-reconsolidation processes strengthen declarative memory in humans (2011) PLoS One, 6 (8), pp. e23305. , Epub 2011 August 5
  • 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
  • Frenkel, L., Maldonado, H., Delorenzi, A., Retrieval improvement is induced by water shortage through angiotensin II (2005) Neurobiol Learn Mem, 83, pp. 173-177
  • Freudenthal, R., Romano, A., Participation of Rel/NF-kappaB transcription factors in long-term memory in the crab Chasmagnathus (2000) Behav Brain Res, 855, pp. 274-281
  • Gleeson, R.A., Paul, L.Z., The determination of hemolymph volume in the blue crab, Callinectes sapidus, utilizing 14C-thiocyanate (1977) Comp Biochem Physiol A Physiol, 56, pp. 411-413
  • Goelet, P., Castelucci, 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
  • Hepp, Y., Perez-Cuesta, L.M., Maldonado, H., Pedreira, M.E., Extinction memory in the crab Chasmagnathus: recovery protocols and effects of multi-trial extinction training (2009) Anim Cogn, 13, pp. 391-403
  • 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
  • Hoeger, U., Florey, E., Catecholamine degradation in the hemolymph of the Chinese crab, Eriocheir sinensis (1989) Comp Biochem Physiol C Comp Pharmacol, 92, pp. 323-327
  • Inda, M.C., Muravieva, E.V., Alberini, C.M., Memory retrieval and the passage of time: from reconsolidation and strengthening to extinction (2011) J Neurosci, 31 (5), pp. 1635-1643
  • Lee, J.L.C., Reconsolidation: maintaining memory relevance (2009) Trends Neurosci, 32, pp. 413-420
  • Levenson, J.M., O'Riordan, K.J., Brown, K.D., Trinh, M.A., Molfese, D.L., Sweatt, J.D., Regulation of histone acetylation during memory formation in the hippocampus (2004) J Biol Chem, 279, pp. 40545-40559
  • Levenson, J.M., Sweatt, J.D., Epigenetic mechanisms in memory formation (2005) Nat Rev Neurosci, 6, pp. 108-118
  • Lozada, M., Romano, A., Maldonado, H., Long-term habituation to a danger stimulus in the crab Chasmagnathus granulatus (1990) Physiol Behav, 47, pp. 35-41
  • Lubin, F.D., Sweatt, J.D., The IkappaB kinase regulates chromatin structure during reconsolidation of conditioned fear memories (2007) Neuron, 55, pp. 942-957
  • Maddox, S.A., Schafe, G.E., Epigenetic alterations in the lateral amygdala are required for reconsolidation of a Pavlovian fear memory (2011) Learn Mem, 18 (9), pp. 579-593
  • Malvaez, M., Sanchis-Segura, C., Vo, D., Lattal, K.M., Wood, M.A., Modulation of chromatin modification facilitates extinction of cocaine-induced conditioned place preference (2010) Biol Psychiatry, 67 (1), pp. 36-43
  • Mamiya, N., Fukushima, H., Suzuki, A., Matsuyama, Z., Homma, S., Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory (2009) J Neurosci, 29, pp. 402-413
  • Marek, R., Coelho, C.M., Sullivan, R.K., Baker-Andresen, D., Li, X., Ratnu, V., Dudley, K.J., Bredy, T.W., Paradoxical enhancement of fear extinction memory and synaptic plasticity by inhibition of the histone acetyltransferase p300 (2011) J Neurosci, 31 (20), pp. 7486-7491
  • 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
  • Merlo, E., Romano, A., Memory extinction entails the inhibition of the transcription factor NF-kappaB (2008) PLoS One, 3, pp. e3687
  • McGaugh, J.L., Time-dependent processes in memory storage (1966) Science, 153, pp. 1351-1358
  • Merlo, E., Freudenthal, R., Maldonado, H., Romano, A., Activation of the transcription factor NF-kappaB by retrieval is required for long-term memory reconsolidation (2005) Learn Mem, 12, pp. 23-29
  • 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
  • Nader, K., Memory traces unbound (2003) Trends Neurosci, 26, pp. 65-72
  • Norton, V.G., Imai, B.S., Yau, P., Bradbury, E.M., Histone acetylation reduces nucleosome core particle linking number change (1989) Cell, 108 (3), pp. 449-457
  • Oliveira, A.M., Wood, M.A., McDonough, C.B., Abel, T., Transgenic mice expressing an inhibitory truncated form of p300 exhibit long-term memory deficits (2007) Learn Mem, 14 (9), pp. 564-572
  • Oliveira, A.M., Estévez, M.A., Hawk, J.D., Grimes, S., Brindle, P.K., Abel, T., Subregion-specific p300 conditional knock-out mice exhibit long-term memory impairments (2011) Learn Mem, 18 (3), pp. 161-169
  • Pedreira, M.E., Dimant, B., Tomsic, D., Quesada-Allue, L.A., Maldonado, H., Cycloheximide inhibits context memory and long-term habituation in the crab Chasmagnathus (1995) Pharmacol Biochem Behav, 52, pp. 385-395
  • 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., 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. 34-45
  • Pedreira, M.E., Maldonado, H., Protein synthesis subserves reconsolidation or extinction depending on reminder duration (2003) Neuron, 38, pp. 863-869
  • Pereyra, P., Gonzalez 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
  • Pérez-Cuesta, L.M., Maldonado, H., Memory reconsolidation and extinction in the crab: mutual exclusion or coexistence? (2009) Learn Mem, 16, pp. 714-721
  • Romano, A., Lozada, M., Maldonado, H., Effect of naloxone pretreatment on habituation in the crab Chasmagnathus granulatus (1990) Behav Neural Biol, 53, pp. 113-122
  • Romano, A., Delorenzi, A., Pedreira, M.E., Tomsic, D., Maldonado, H., Acute administration of a permeant analog of cAMP and a phosphodiesterase inhibitor improve long-term habituation in the crab Chasmagnathus (1996) Behav Brain Res, 75, pp. 119-125
  • Sara, S.J., Retrieval and reconsolidation: toward a neurobiology of remembering (2000) Learn Mem, 7, pp. 73-84
  • Sterner, D.E., Berger, S.L., Acetylation of histones and transcription-related factors (2000) Microbiol Mol Biol Rev, 64, pp. 435-459
  • Stefanko, D.P., Barrett, R.M., Ly, A.R., Reolon, G.K., Wood, M.A., Modulation of long-term memory for object recognition via HDAC inhibition (2009) Proc Natl Acad Sci USA, 106, pp. 9447-9452
  • Suárez, L.D., Smal, L., Delorenzi, A., Updating contextual information during consolidation as result of a new memory trace (2010) Neurobiol Learn Mem, 93, pp. 561-571
  • 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
  • Tully, T., Quinn, W.G., Classical conditioning and retention in normal and mutant Drosophila melanogaster (1985) J Comp Physiol A, 157 (2), pp. 263-277
  • Vecsey, C.G., Hawk, J.D., Lattal, K.M., Stein, J.M., Fabian, S.A., Attner, M.A., Cabrera, S.M., Wood, M.A., Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation (2007) J Neurosci, 27, pp. 6128-6140
  • Vettese-Dadey, M., Grant, P.A., Hebbes, T.R., Crane-Robinson, C., Allis, C.D., Workman, J.L., Acetylation of histone H4 plays a primary role in enhancing transcription factor binding to nucleosomal DNA in vitro (1996) EMBO J, 15 (10), pp. 2508-2518
  • von Hertzen, L.S.J., Giese, K.P., Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation (2005) J Neurosci, 25, pp. 1935-1942
  • Wood, M.A., Hawk, J.D., Abel, T., Combinatorial chromatin modifications and memory storage: a code for memory? (2006) Learn Mem, 13, pp. 241-244
  • Yeh, S., Lin, C., Gean, P., 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
  • Yang, J., Yu, J., Jia, X., Zhu, W., Zhao, L., Li, S., Xu, C., Lu, L., Inhibition of nuclear factor-κB impairs reconsolidation of morphine reward memory in rats (2011) Behav Brain Res, 216, pp. 592-596

Citas:

---------- APA ----------
Federman, N., Fustiñana, M.S. & Romano, A. (2012) . Reconsolidation involves histone acetylation depending on the strength of the memory. Neuroscience, 219, 145-156.
http://dx.doi.org/10.1016/j.neuroscience.2012.05.057
---------- CHICAGO ----------
Federman, N., Fustiñana, M.S., Romano, A. "Reconsolidation involves histone acetylation depending on the strength of the memory" . Neuroscience 219 (2012) : 145-156.
http://dx.doi.org/10.1016/j.neuroscience.2012.05.057
---------- MLA ----------
Federman, N., Fustiñana, M.S., Romano, A. "Reconsolidation involves histone acetylation depending on the strength of the memory" . Neuroscience, vol. 219, 2012, pp. 145-156.
http://dx.doi.org/10.1016/j.neuroscience.2012.05.057
---------- VANCOUVER ----------
Federman, N., Fustiñana, M.S., Romano, A. Reconsolidation involves histone acetylation depending on the strength of the memory. Neuroscience. 2012;219:145-156.
http://dx.doi.org/10.1016/j.neuroscience.2012.05.057