Artículo

Zalcman, G.; Federman, N.; Fiszbein, A.; de la Fuente, V.; Ameneiro, L.; Schor, I.; Romano, A. "Sustained CaMKII Delta Gene Expression Is Specifically Required for Long-Lasting Memories in Mice" (2019) Molecular Neurobiology. 56(2):1437-1450
Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Although important information is available on the molecular mechanisms of long-term memory formation, little is known about the processes underlying memory persistence in the brain. Here, we report that persistent gene expression of CaMKIIδ isoform participates in object recognition long-lasting memory storage in mice hippocampus. We found that CaMKIIδ mRNA expression was sustained up to one week after training and paralleled memory retention. Antisense DNA infusion in the hippocampus during consolidation or even after consolidation impairs 7-day- but not 1-day-long memory, supporting a role of CaMKIIδ in memory persistence. CaMKIIδ gene expression was accompanied by long-lasting nucleosome occupancy changes at its promoter. This epigenetic mechanism is described for the first time in a memory process and offers a novel mechanism for persistent gene expression in neurons. CaMKIIδ protein is mainly present in nucleus and presynaptic terminals, suggesting a role in these subcellular compartments for memory persistence. All these results point to a key function of the sustained gene expression of this overlooked CaMKII isoform in long-lasting memories. © 2018, Springer Science+Business Media, LLC, part of Springer Nature.

Registro:

Documento: Artículo
Título:Sustained CaMKII Delta Gene Expression Is Specifically Required for Long-Lasting Memories in Mice
Autor:Zalcman, G.; Federman, N.; Fiszbein, A.; de la Fuente, V.; Ameneiro, L.; Schor, I.; Romano, A.
Filiación:Laboratorio de Neurobiología de la Memoria, Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto de Fisiología, Biología Molecular y Neurociencias (IFIByNE), UBA-CONICET, Ciudad Universitaria, Buenos Aires, 1428EHA, Argentina
Laboratorio de Circuitos Neuronales, Instituto de Investigación en Biomedicina de Buenos Aires (IBioBA)—CONICET—Partner Institute of the Max Planck Society, Godoy Cruz 2390, Buenos Aires, C1425FQD, Argentina
Palabras clave:CaMKII; Hippocampus; Long-term memory; Neuroepigenetics; Nucleosome occupancy
Año:2019
Volumen:56
Número:2
Página de inicio:1437
Página de fin:1450
DOI: http://dx.doi.org/10.1007/s12035-018-1144-3
Título revista:Molecular Neurobiology
Título revista abreviado:Mol. Neurobiol.
ISSN:08937648
CODEN:MONBE
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_08937648_v56_n2_p1437_Zalcman

Referencias:

  • Zovkic, I.B., Guzman-Karlsson, M.C., Sweatt, J.D., Epigenetic regulation of memory formation and maintenance (2013) Learn Mem, 20 (2), pp. 61-74. , COI: 1:CAS:528:DC%2BC3sXmsVCmsLs%3D, PID: 23322554
  • Miller, C.A., Gavin, C.F., White, J.A., Parrish, R.R., Honasoge, A., Yancey, C.R., Rivera, I.M., Sweatt, J.D., Cortical DNA methylation maintains remote memory (2010) Nat Neurosci, 13 (6), pp. 664-666. , COI: 1:CAS:528:DC%2BC3cXmsVWmsrs%3D, PID: 20495557
  • Federman, N., de la Fuente, V., Zalcman, G., Corbi, N., Onori, A., Passananti, C., Romano, A., Nuclear factor κB-dependent histone acetylation is specifically involved in persistent forms of memory (2013) J Neurosci, 33 (17), pp. 7603-7614. , COI: 1:CAS:528:DC%2BC3sXhtl2js7rE, PID: 23616565
  • Kwapis, J.L., Helmstetter, F.J., Does PKM(zeta) maintain memory? (2014) Brain Res Bull, 105, pp. 36-45. , COI: 1:CAS:528:DC%2BC3sXhs1SrtLjO, PID: 24076105
  • Tsokas, P., Hsieh, C., Yao, Y., Lesburguères, E., Wallace, E.J.C., Tcherepanov, A., Jothianandan, D., Hartley, B.R., Compensation for PKMζ in long-term potentiation and spatial long-term memory in mutant mice (2016) Elife, 5
  • Bangaru, M.L.Y., Meng, J., Kaiser, D.J., Yu, H., Fischer, G., Hogan, Q.H., Hudmon, A., Differential expression of CaMKII isoforms and overall kinase activity in rat dorsal root ganglia after injury (2015) Neuroscience, 300, pp. 116-127. , COI: 1:CAS:528:DC%2BC2MXos1elt7c%3D, PID: 25982557
  • Lisman, J., Schulman, H., Cline, H., The molecular basis of CaMKII function in synaptic and behavioural memory (2002) Nat Rev Neurosci, 3 (3), pp. 175-190. , COI: 1:CAS:528:DC%2BD38Xit1GrtLk%3D, PID: 11994750
  • Lucchesi, W., Mizuno, K., Giese, K.P., Novel insights into CaMKII function and regulation during memory formation (2011) Brain Res Bull, 85 (1-2), pp. 2-8. , COI: 1:CAS:528:DC%2BC3MXkvVKgtLc%3D, PID: 21070840
  • Irvine, E.E., von Hertzen, L.S.J., Plattner, F., Giese, K.P., alphaCaMKII autophosphorylation: a fast track to memory (2006) Trends Neurosci, 29 (8), pp. 459-465. , COI: 1:CAS:528:DC%2BD28Xns1Slurk%3D, PID: 16806507
  • Bachstetter, A.D., Webster, S.J., Tu, T., Goulding, D.S., Haiech, J., Watterson, D.M., van Eldik, L.J., Generation and behavior characterization of CaMKIIβ knockout mice (2014) PLoS One, 9 (8)
  • Sirri, A., Bianchi, V., Pelizzola, M., Mayhaus, M., Ricciardi-Castagnoli, P., Toniolo, D., D'Adamo, P., Temporal gene expression profile of the hippocampus following trace fear conditioning (2010) Brain Res, 1308, pp. 14-23. , COI: 1:CAS:528:DC%2BD1MXhsFanu7rO, PID: 19857472
  • Jarome, T.J., Thomas, J.S., Lubin, F.D., The epigenetic basis of memory formation and storage (2014) Prog Mol Biol Transl Sci, 128, pp. 1-27. , COI: 1:CAS:528:DC%2BC28XhsVOisLfJ, PID: 25410539
  • Zovkic, I.B., Paulukaitis, B.S., Day, J.J., Etikala, D.M., Sweatt, J.D., Histone H2A.Z subunit exchange controls consolidation of recent and remote memory (2014) Nature, 515 (7528), pp. 582-586. , COI: 1:CAS:528:DC%2BC2cXhvVemtrzO, PID: 4768489
  • Maze, I., Wenderski, W., Noh, K.M., Bagot, R.C., Tzavaras, N., Purushothaman, I., Elsässer, S.J., Allis, C.D., Critical role of histone turnover in neuronal transcription and plasticity (2015) Neuron, 87 (1), pp. 77-94. , COI: 1:CAS:528:DC%2BC2MXht1Wksr3M, PID: 4491146
  • Vogel-Ciernia, A., Matheos, D.P., Barrett, R.M., Kramár, E.A., Azzawi, S., Chen, Y., Magnan, C.N., Wood, M.A., The neuron-specific chromatin regulatory subunit BAF53b is necessary for synaptic plasticity and memory (2013) Nat Neurosci, 16 (5), pp. 552-561. , COI: 1:CAS:528:DC%2BC3sXksVOgtr4%3D, PID: 23525042
  • Vogel-Ciernia, A., Wood, M.A., Neuron-specific chromatin remodeling: a missing link in epigenetic mechanisms underlying synaptic plasticity, memory and intellectual disability disorders (2014) Neuropharmacology, 80, pp. 18-27. , COI: 1:CAS:528:DC%2BC3sXhs12ltLrP, PID: 24140580
  • Hemstedt, T.J., Lattal, K.M., Wood, M.A., Reconsolidation and extinction: using epigenetic signatures to challenge conventional wisdom (2017) Neurobiol Learn Mem, 142, pp. 55-65. , PID: 5457345
  • López, A.J., Wood, M.A., Role of nucleosome remodeling in neurodevelopmental and intellectual disability disorders (2015) Front Behav Neurosci, 9, p. 100. , PID: 25954173
  • Bai, L., Morozov, A.V., Gene regulation by nucleosome positioning (2010) Trends Genet, 26 (11), pp. 476-483. , COI: 1:CAS:528:DC%2BC3cXht12qurjN, PID: 20832136
  • McGaugh, J.L., Memory—a century of consolidation (2000) Science, 287 (5451), pp. 248-251. , COI: 1:CAS:528:DC%2BD3cXlvVSnsQ%3D%3D
  • Neidl, R., Schneider, A., Bousiges, O., Majchrzak, M., Barbelivien, A., de Vasconcelos, A.P., Dorgans, K., Boutillier, A.L., Late-life environmental enrichment induces acetylation events and nuclear factor κB-dependent regulations in the hippocampus of aged rats showing improved plasticity and learning (2016) J Neurosci, 36 (15), pp. 4351-4361. , COI: 1:CAS:528:DC%2BC28XhtlentrfO, PID: 27076430
  • Ponts, N., Harris, E.Y., Lonardi, S., Le Roch, K.G., Nucleosome occupancy at transcription start sites in the human malaria parasite: a hard-wired evolution of virulence? (2011) Infect Genet Evol, 11 (4), pp. 716-724. , COI: 1:CAS:528:DC%2BC3MXmslGrtL8%3D, PID: 20708104
  • Tirosh, I., Barkai, N., Two strategies for gene regulation by promoter nucleosomes (2008) Genome Res, 18 (7), pp. 1084-1091. , COI: 1:CAS:528:DC%2BD1cXotlKmsbc%3D, PID: 18448704
  • Kessels, H.W., Malinow, R., Synaptic AMPA receptor plasticity and behavior (2009) Neuron, 61 (3), pp. 340-350. , COI: 1:CAS:528:DC%2BD1MXltFSntLw%3D, PID: 19217372
  • Morris, R.G.M., NMDA receptors and memory encoding (2013) Neuropharmacology, 74, pp. 32-40. , COI: 1:CAS:528:DC%2BC3sXnslakurs%3D, PID: 23628345
  • Shen, K., Teruel, M.N., Subramanian, K., Meyer, T., CaMKIIbeta functions as an F-actin targeting module that localizes CaMKIIalpha/beta heterooligomers to dendritic spines (1998) Neuron, 21 (3), pp. 593-606. , COI: 1:CAS:528:DyaK1cXms1eht7s%3D
  • Miller, S., Yasuda, M., Coats, J.K., Jones, Y., Martone, M.E., Mayford, M., Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation (2002) Neuron, 36 (3), pp. 507-519. , COI: 1:CAS:528:DC%2BD38XosV2htLY%3D, PID: 12408852
  • Mishra, S., Gray, C.B.B., Miyamoto, S., Bers, D.M., Brown, J.H., Location matters: clarifying the concept of nuclear and cytosolic CaMKII subtypes (2011) Circ Res, 109 (12), pp. 1354-1362. , COI: 1:CAS:528:DC%2BC3MXhsF2jsrrI, PID: 21998325
  • Ma, H., Li, B., Tsien, R.W., Distinct roles of multiple isoforms of CaMKII in signaling to the nucleus (2015) Biochim Biophys Acta, 1853 (9), pp. 1953-1957. , COI: 1:CAS:528:DC%2BC2MXivFKisb8%3D, PID: 25700840
  • Shema, R., Haramati, S., Ron, S., Hazvi, S., Chen, A., Sacktor, T.C., Dudai, Y., Enhancement of consolidated long-term memory by overexpression of protein kinase Mζ in the neocortex (2011) Science, 331 (6021), pp. 1207-1210. , COI: 1:CAS:528:DC%2BC3MXislOku7s%3D, PID: 21385716
  • Hsieh, C., Persistent increased PKMζ in long-term and remote spatial memory (2016) Neurobiol Learn Mem
  • Xiao, H.-S., Huang, Q.H., Zhang, F.X., Bao, L., Lu, Y.J., Guo, C., Yang, L., Zhang, X., Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain (2002) Proc Natl Acad Sci U S A, 99 (12), pp. 8360-8365. , COI: 1:CAS:528:DC%2BD38XkvVGgu7Y%3D, PID: 12060780
  • Katche, C., Bekinschtein, P., Slipczuk, L., Goldin, A., Izquierdo, I.A., Cammarota, M., Medina, J.H., Delayed wave of c-Fos expression in the dorsal hippocampus involved specifically in persistence of long-term memory storage (2010) Proc Natl Acad Sci U S A, 107 (1), pp. 349-354. , COI: 1:CAS:528:DC%2BC3cXnsFCrtg%3D%3D, PID: 20018662
  • Yaida, Y., Nowak, T.S., Distribution of phosphodiester and phosphorothioate oligonucleotides in rat brain after intraventricular and intrahippocampal administration determined by in situ hybridization (1995) Regul Pept, 59 (2), pp. 193-199. , COI: 1:CAS:528:DyaK2MXos1ajtrw%3D, PID: 8584754
  • Shema, R., Sacktor, T.C., Dudai, Y., Rapid erasure of long-term memory associations in the cortex by an inhibitor of PKM zeta (2007) Science, 317 (5840), pp. 951-953. , COI: 1:CAS:528:DC%2BD2sXptVaju7c%3D, PID: 17702943
  • Quivy, V., Van Lint, C., Regulation at multiple levels of NF-κB-mediated transactivation by protein acetylation (2004) Biochem Pharmacol, 68 (6), pp. 1221-1229. , COI: 1:CAS:528:DC%2BD2cXmslOnsL4%3D, PID: 15313420
  • Kim, S., Kaang, B.-K., Epigenetic regulation and chromatin remodeling in learning and memory (2017) Exp Mol Med, 49 (1). , PID: 28082740
  • Lone, I.N., Shukla, M.S., Charles Richard, J.L., Peshev, Z.Y., Dimitrov, S., Angelov, D., Binding of NF-κB to nucleosomes: effect of translational positioning, nucleosome remodeling and linker histone H1 (2013) PLoS Genet, 9 (9). , COI: 1:CAS:528:DC%2BC3sXhsFKitbrI, PID: 24086160
  • Cohen, S.J., Stackman, R.W., Assessing rodent hippocampal involvement in the novel object recognition task. A review (2015) Behav Brain Res, 285, pp. 105-117. , PID: 25169255
  • Takeuchi, Y., Yamamoto, H., Matsumoto, K., Kimura, T., Katsuragi, S., Miyakawa, T., Miyamoto, E., Nuclear localization of the delta subunit of Ca 2+ /calmodulin-dependent protein kinase II in rat cerebellar granule cells (1999) J Neurochem, 72 (2), pp. 815-825. , COI: 1:CAS:528:DyaK1MXmt1yltQ%3D%3D, PID: 9930758
  • Awad, S., al-Haffar, K.M.A., Marashly, Q., Quijada, P., Kunhi, M., al-Yacoub, N., Wade, F.S., Poizat, C., Control of histone H3 phosphorylation by CaMKIIδ in response to haemodynamic cardiac stress (2015) J Pathol, 235 (4), pp. 606-618. , COI: 1:CAS:528:DC%2BC2MXitlKqtLs%3D, PID: 25421395
  • Little, G.H., Bai, Y., Williams, T., Poizat, C., Nuclear calcium/calmodulin-dependent protein kinase IIdelta preferentially transmits signals to histone deacetylase 4 in cardiac cells (2007) J Biol Chem, 282 (10), pp. 7219-7231. , COI: 1:CAS:528:DC%2BD2sXitlSrsbw%3D, PID: 17179159
  • Zhang, T., Kohlhaas, M., Backs, J., Mishra, S., Phillips, W., Dybkova, N., Chang, S., Brown, J.H., CaMKIIdelta isoforms differentially affect calcium handling but similarly regulate HDAC/MEF2 transcriptional responses (2007) J Biol Chem, 282 (48), pp. 35078-35087. , COI: 1:CAS:528:DC%2BD2sXhtlCrt7nN, PID: 17923476
  • Sando, R., Gounko, N., Pieraut, S., Liao, L., Yates, J., Maximov, A., HDAC4 governs a transcriptional program essential for synaptic plasticity and memory (2012) Cell, 151 (4), pp. 821-834. , COI: 1:CAS:528:DC%2BC38Xhs1KjsbzI, PID: 23141539
  • Wang, W.-H., Intracellular trafficking of histone deacetylase 4 regulates long-term memory formation (2011) Anat Rec, 294 (6), pp. 1025-1034. , COI: 1:CAS:528:DC%2BC3MXosVOrt78%3D
  • Fitzsimons, H.L., Schwartz, S., Given, F.M., Scott, M.J., The histone deacetylase HDAC4 regulates long-term memory in Drosophila (2013) PLoS One, 8 (12). , PID: 24349558
  • Ninan, I., Arancio, O., Presynaptic CaMKII is necessary for synaptic plasticity in cultured hippocampal neurons (2004) Neuron, 42 (1), pp. 129-141. , COI: 1:CAS:528:DC%2BD2cXjs1ygtLc%3D, PID: 15066270
  • Lu, F.-M., Hawkins, R.D., Presynaptic and postsynaptic Ca 2+ and CamKII contribute to long-term potentiation at synapses between individual CA3 neurons (2006) Proc Natl Acad Sci U S A, 103 (11), pp. 4264-4269. , COI: 1:CAS:528:DC%2BD28XivFWhsrY%3D, PID: 16537519
  • Paxinos, G., Franklin, K.B.J., (2004) The Mouse Brain in Stereotaxic Coordinates, , Gulf Professional Publishing
  • Kirk, R.E., (2012) Experimental design: procedures for the behavioral sciences, , 4, SAGE Publications, Inc, Thousand Oaks

Citas:

---------- APA ----------
Zalcman, G., Federman, N., Fiszbein, A., de la Fuente, V., Ameneiro, L., Schor, I. & Romano, A. (2019) . Sustained CaMKII Delta Gene Expression Is Specifically Required for Long-Lasting Memories in Mice. Molecular Neurobiology, 56(2), 1437-1450.
http://dx.doi.org/10.1007/s12035-018-1144-3
---------- CHICAGO ----------
Zalcman, G., Federman, N., Fiszbein, A., de la Fuente, V., Ameneiro, L., Schor, I., et al. "Sustained CaMKII Delta Gene Expression Is Specifically Required for Long-Lasting Memories in Mice" . Molecular Neurobiology 56, no. 2 (2019) : 1437-1450.
http://dx.doi.org/10.1007/s12035-018-1144-3
---------- MLA ----------
Zalcman, G., Federman, N., Fiszbein, A., de la Fuente, V., Ameneiro, L., Schor, I., et al. "Sustained CaMKII Delta Gene Expression Is Specifically Required for Long-Lasting Memories in Mice" . Molecular Neurobiology, vol. 56, no. 2, 2019, pp. 1437-1450.
http://dx.doi.org/10.1007/s12035-018-1144-3
---------- VANCOUVER ----------
Zalcman, G., Federman, N., Fiszbein, A., de la Fuente, V., Ameneiro, L., Schor, I., et al. Sustained CaMKII Delta Gene Expression Is Specifically Required for Long-Lasting Memories in Mice. Mol. Neurobiol. 2019;56(2):1437-1450.
http://dx.doi.org/10.1007/s12035-018-1144-3