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Abstract:

Calcium/calmodulin-dependent protein kinase II (CaMKII) is a key protein kinase in neural plasticity and memory, as have been shown in several studies since the first evidence in long-term potentiation (LTP) 30 years ago. However, most of the studies were focused mainly in one of the four isoforms of this protein kinase, the CaMKIIα. Here we review the characteristics and the role of each of the four isoforms in learning, memory and neural plasticity, considering the well known local role of α and β isoforms in dendritic terminals as well as recent findings about the γ isoform as calcium signals transducers from synapse to nucleus and δ isoform as a kinase required for a more persistent memory trace. © 2018 Zalcman, Federman and Romano.

Registro:

Documento: Artículo
Título:CaMKII isoforms in learning and memory: Localization and function
Autor:Zalcman, G.; Federman, N.; Romano, A.
Filiación:Instituto de Fisiología, Biología Molecular y Neurociencias, Universidad de Buenos Aires – Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:CaMKII; CaMKIIα; CaMKIIβ; CaMKIIγ; CaMKIIδ; Learning; Memory; calcium calmodulin dependent protein kinase II; calcium calmodulin dependent protein kinase II alpha; calcium calmodulin dependent protein kinase II beta; calcium calmodulin dependent protein kinase II delta; calcium calmodulin dependent protein kinase II gamma; isoprotein; n methyl dextro aspartic acid receptor; unclassified drug; autophosphorylation; brain injury; calcium signaling; cell migration; gene expression; glutamatergic synapse; human; learning; learning disorder; long term potentiation; memory; nerve cell plasticity; nerve growth; neurite outgrowth; neurotransmitter release; nonhuman; protein expression; protein phosphorylation; protein processing; regulatory mechanism; reperfusion injury; Review; signal transduction; spatial memory
Año:2018
Volumen:11
DOI: http://dx.doi.org/10.3389/fnmol.2018.00445
Título revista:Frontiers in Molecular Neuroscience
Título revista abreviado:Front. Mol. Neurosci.
ISSN:16625099
CAS:calcium calmodulin dependent protein kinase II, 141467-21-2
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_16625099_v11_n_p_Zalcman

Referencias:

  • Ahmed, R., Zha, X., Green, S.H., Dailey, M.E., Synaptic activity and F-actin coordinately regulate CaMKIIalpha localization to dendritic postsynaptic sites in developing hippocampal slices (2006) Mol. Cell. Neurosci, 31, pp. 37-51. , 16214364
  • Alberini, C.M., Transcription factors in long-term memory and synaptic plasticity (2009) Physiol. Rev, 89, pp. 121-145. , 19126756
  • Awad, S., Al-Haffar, K.M.A., Marashly, Q., Quijada, P., Kunhi, M., Al-Yacoub, N., Control of histone H3 phosphorylation by CaMKIIδ in response to haemodynamic cardiac stress (2015) J. Pathol, 235, pp. 606-618. , 25421395
  • Bachstetter, A.D., Webster, S.J., Tu, T., Goulding, D.S., Haiech, J., Watterson, D.M., Generation and behavior characterization of CaMKIIβ knockout mice (2014) PLoS One, 9 (e105191). , 25127391
  • Bai, L., Morozov, A.V., Gene regulation by nucleosome positioning (2010) Trends Genet, 26, pp. 476-483. , 20832136
  • Bangaru, M.L.Y., Meng, J., Kaiser, D.J., Yu, H., Fischer, G., Hogan, Q.H., Differential expression of CaMKII isoforms and overall kinase activity in rat dorsal root ganglia after injury (2015) Neuroscience, 300, pp. 116-127. , 25982557
  • Bayer, K.U., Löhler, J., Schulman, H., Harbers, K., Developmental expression of the CaM kinase II isoforms: ubiquitous gamma- and delta-CaM kinase II are the early isoforms and most abundant in the developing nervous system (1999) Brain Res. Mol. Brain Res, 70, pp. 147-154. , 10381553
  • Bennett, M.K., Erondu, N.E., Kennedy, M.B., Purification and characterization of a calmodulin-dependent protein kinase that is highly concentrated in brain (1983) J. Biol. Chem, 258, pp. 12735-12744
  • Berger, S.M., Bartsch, D., The role of L-type voltage-gated calcium channels Cav1.2 and Cav1.3 in normal and pathological brain function (2014) Cell Tissue Res, 357, pp. 463-476. , 24996399
  • Blichenberg, A., Rehbein, M., Müller, R., Garner, C.C., Richter, D., Kindler, S., Identification of a cis-acting dendritic targeting element in the mRNA encoding the alpha subunit of Ca2+/calmodulin-dependent protein kinase II (2001) Eur. J. Neurosci, 13, pp. 1881-1888. , 11403681
  • Borgesius, N.Z., van Woerden, G.M., Buitendijk, G.H.S., Keijzer, N., Jaarsma, D., Hoogenraad, C.C., βCaMKII plays a nonenzymatic role in hippocampal synaptic plasticity and learning by targeting αCaMKII to synapses (2011) J. Neurosci, 31, pp. 10141-10148
  • Brocke, L., Chiang, L.W., Wagner, P.D., Schulman, H., Functional implications of the subunit composition of neuronal CaM kinase II (1999) J. Biol. Chem, 274, pp. 22713-22722. , 10428854
  • Brocke, L., Srinivasan, M., Schulman, H., Developmental and regional expression of multifunctional Ca2+/calmodulin-dependent protein kinase isoforms in rat brain (1995) J. Neurosci, 15, pp. 6797-6808. , 7472438
  • Buard, I., Coultrap, S.J., Freund, R.K., Lee, Y.-S., Dell’Acqua, M.L., Silva, A.J., CaMKII “autonomy” is required for initiating but not for maintaining neuronal long-term information storage (2010) J. Neurosci, 30, pp. 8214-8220
  • Cammarota, M., Bernabeu, R., Levi De Stein, M., Izquierdo, I., Medina, J.H., Learning-specific, time-dependent increases in hippocampal Ca2+/calmodulin-dependent protein kinase II activity and AMPA GluR1 subunit immunoreactivity (1998) Eur. J. Neurosci, 10, pp. 2669-2676. , 9767396
  • Cammarota, M., Bevilaqua, L.R.M., Viola, H., Kerr, D.S., Reichmann, B., Teixeira, V., Participation of CaMKII in Neuronal Plasticity and Memory Formation (2002) Cell. Mol. Neurobiol, 22, pp. 259-267
  • Chang, J.-Y., Parra-Bueno, P., Laviv, T., Szatmari, E.M., Lee, S.J.R., Yasuda, R., CaMKII autophosphorylation is necessary for optimal integration of ca2+ signals during LTP induction, but not maintenance (2017) Neuron, 94, pp. 800-808. , 28521133.e4
  • Cho, M.H., Cao, X., Wang, D., Tsien, J.Z., Dentate gyrus-specific manipulation of β-Ca2+/calmodulin-dependent kinase II disrupts memory consolidation (2007) Proc. Natl. Acad. Sci. U.S.A, 104, pp. 16317-16322. , 17913888
  • Cohen, S.M., Suutari, B., He, X., Wang, Y., Sanchez, S., Tirko, N.N., Calmodulin shuttling mediates cytonuclear signaling to trigger experience-dependent transcription and memory (2018) Nat. Commun, 9 (2451). , 29934532
  • Cook, S.G., Bourke, A.M., O’Leary, H., Zaegel, V., Lasda, E., Mize-Berge, J., Analysis of the CaMKIIα and β splice-variant distribution among brain regions reveals isoform-specific differences in holoenzyme formation (2018) Sci. Rep, 8 (5448). , 29615706
  • Coultrap, S.J., Bayer, K.U., CaMKII regulation in information processing and storage (2012) Trends Neurosci, 35, pp. 607-618. , 22717267
  • D’Amours, G., Bureau, G., Boily, M.-J., Cyr, M., Differential gene expression profiling in the mouse brain during motor skill learning: focus on the striatum structure (2011) Behav. Brain Res, 221, pp. 108-117. , 21376085
  • de la Fuente, V., Federman, N., Zalcman, G., Salles, A., Freudenthal, R., Romano, A., NF-κB transcription factor role in consolidation and reconsolidation of persistent memories (2015) Front. Mol. Neurosci, 8 (50)
  • de Ligt, J., Willemsen, M.H., van Bon, B.W.M., Kleefstra, T., Yntema, H.G., Kroes, T., Diagnostic exome sequencing in persons with severe intellectual disability (2012) N. Engl. J. Med, 367, pp. 1921-1929. , 23033978
  • de Quervain, D.J.F., Papassotiropoulos, A., Identification of a genetic cluster influencing memory performance and hippocampal activity in humans (2006) Proc. Natl. Acad. Sci. U.S.A, 103, pp. 4270-4274. , 16537520
  • Donai, H., Nakamura, M., Sogawa, Y., Wang, J.K., Urushihara, M., Yamauchi, T., Involvement of Ca2+/calmodulin-dependent protein kinase II in neurite outgrowth induced by cAMP treatment and serum deprivation in a central nervous system cell line, CAD derived from rat brain (2000) Neurosci. Lett, 293, pp. 111-114. , 11027846
  • Easley, C.A., Faison, M.O., Kirsch, T.L., Lee, J.A., Seward, M.E., Tombes, R.M., Laminin activates CaMK-II to stabilize nascent embryonic axons (2006) Brain Res, 1092, pp. 59-68. , 16690036
  • Elgersma, Y., Fedorov, N.B., Ikonen, S., Choi, E.S., Elgersma, M., Carvalho, O.M., Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity, and learning (2002) Neuron, 36, pp. 493-505. , 12408851
  • Elgersma, Y., Sweatt, J.D., Giese, K.P., Mouse genetic approaches to investigating calcium/calmodulin-dependent protein kinase II function in plasticity and cognition (2004) J. Neurosci, 24, pp. 8410-8415. , 15456813
  • Erondu, N.E., Kennedy, M.B., Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain (1985) J. Neurosci, 5, pp. 3270-3277
  • Faison, M.O., Perozzi, E.F., Caran, N., Stewart, J.K., Tombes, R.M., Axonal localization of delta Ca2+/calmodulin-dependent protein kinase II in developing P19 neurons (2002) Int. J. Dev. Neurosci, 20, pp. 585-592. , 12526889
  • Federman, N., de la Fuente, V., Zalcman, G., Corbi, N., Onori, A., Passananti, C., Nuclear factor κB-dependent histone acetylation is specifically involved in persistent forms of memory (2013) J. Neurosci, 33, pp. 7603-7614
  • Federman, N., Zalcman, G., de la Fuente, V., Fustiñana, M.S., Romano, A., Epigenetic mechanisms and memory strength: a comparative study (2014) J. Physiol. Paris, 108, pp. 278-285. , 24978317
  • 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 (e83903). , 24349558
  • Frankland, P.W., Bontempi, B., Talton, L.E., Kaczmarek, L., Silva, A.J., The involvement of the anterior cingulate cortex in remote contextual fear memory (2004) Science, 304, pp. 881-883. , 15131309
  • Frankland, P.W., O’Brien, C., Ohno, M., Kirkwood, A., Silva, A.J., Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory (2001) Nature, 411, pp. 309-313. , 11357133
  • Gaertner, T.R., Kolodziej, S.J., Wang, D., Kobayashi, R., Koomen, J.M., Stoops, J.K., Comparative analyses of the three-dimensional structures and enzymatic properties of α, β, γ, and δ isoforms of Ca2+-calmodulin-dependent protein kinase II (2004) J. Biol. Chem, 279, pp. 12484-12494. , 14722083
  • Gangopadhyay, S.S., Barber, A.L., Gallant, C., Grabarek, Z., Smith, J.L., Morgan, K.G., Differential functional properties of calmodulin-dependent protein kinase IIgamma variants isolated from smooth muscle (2003) Biochem. J, 372, pp. 347-357. , 12603201
  • Giese, K.P., Fedorov, N.B., Filipkowski, R.K., Silva, A.J., Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning (1998) Science, 279, pp. 870-873
  • Giese, K.P., Mizuno, K., The roles of protein kinases in learning and memory (2013) Learn. Mem. Cold Spring Harb. N, 20, pp. 540-552. , 24042850
  • Gray, C.B.B., Heller Brown, J., CaMKIIdelta subtypes: localization and function (2014) Front. Pharmacol, 5 (15)
  • Gray, C.B.B., Suetomi, T., Xiang, S., Mishra, S., Blackwood, E.A., Glembotski, C.C., CaMKIIδ subtypes differentially regulate infarct formation following ex vivo myocardial ischemia/reperfusion through NF-κB and TNF-α (2017) J. Mol. Cell. Cardiol, 103, pp. 48-55. , 28077321
  • Griffith, L.C., Lu, C.S., Sun, X.X., CaMKII, an enzyme on the move: regulation of temporospatial localization (2003) Mol. Interv, 3, pp. 386-403. , 14993460
  • Hanson, P.I., Kapiloff, M.S., Lou, L.L., Rosenfeld, M.G., Schulman, H., Expression of a multifunctional Ca2+/calmodulin-dependent protein kinase and mutational analysis of its autoregulation (1989) Neuron, 3, pp. 59-70
  • Hanson, P.I., Meyer, T., Stryer, L., Schulman, H., Dual role of calmodulin in autophosphorylation of multifunctional CaM kinase may underlie decoding of calcium signals (1994) Neuron, 12, pp. 943-956. , 8185953
  • Heist, E.K., Srinivasan, M., Schulman, H., Phosphorylation at the nuclear localization signal of Ca2+/calmodulin-dependent protein kinase II blocks its nuclear targeting (1998) J. Biol. Chem, 273, pp. 19763-19771. , 9677407
  • Hell, J.W., CaMKII: claiming center stage in postsynaptic function and organization (2014) Neuron, 81, pp. 249-265. , 24462093
  • Hoffman, L., Farley, M.M., Waxham, M.N., Calcium-calmodulin-dependent protein kinase II isoforms differentially impact the dynamics and structure of the actin cytoskeleton (2013) Biochemistry, 52, pp. 1198-1207. , 23343535
  • Hotulainen, P., Hoogenraad, C.C., Actin in dendritic spines: connecting dynamics to function (2010) J. Cell Biol, 189, pp. 619-629. , 20457765
  • Hsieh, C., Tsokas, P., Serrano, P., Hernandez, I., Tian, D., Cottrell, J.E., Persistent increased PKMζ in long-term and remote spatial memory (2016) Neurobiol. Learn. Mem, 138, pp. 135-144. , 27417578
  • Hudmon, A., Schulman, H., Neuronal CA2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function (2002) Annu. Rev. Biochem, 71, pp. 473-510. , 12045104
  • Hudson, G.M., Watson, P.J., Fairall, L., Jamieson, A.G., Schwabe, J.W.R., Insights into the Recruitment of Class IIa Histone Deacetylases (HDACs) to the SMRT/NCoR transcriptional repression complex (2015) J. Biol. Chem, 290, pp. 18237-18244. , 26055705
  • Igaz, L.M., Bekinschtein, P., Izquierdo, I., Medina, J.H., One-trial aversive learning induces late changes in hippocampal CaMKIIalpha, Homer 1a, Syntaxin 1a and ERK2 protein levels (2004) Brain Res. Mol. Brain Res, 132, pp. 1-12. , 15548423
  • Irvine, E.E., Vernon, J., Giese, K.P., αCaMKII autophosphorylation contributes to rapid learning but is not necessary for memory (2005) Nat. Neurosci, 8, pp. 411-412. , 15778710
  • Irvine, E.E., von Hertzen, L.S.J., Plattner, F., Giese, K.P., alphaCaMKII autophosphorylation: a fast track to memory (2006) Trends Neurosci, 29, pp. 459-465. , 16806507
  • Johnson, L.D., Willoughby, C.A., Burke, S.H., Paik, D.S., Jenkins, K.J., Tombes, R.M., delta Ca(2+)/Calmodulin-dependent protein kinase II isozyme-specific induction of neurite outgrowth in P19 embryonal carcinoma cells (2000) J. Neurochem, 75, pp. 2380-2391. , 11080189
  • Jourdain, P., Fukunaga, K., Muller, D., Calcium/calmodulin-dependent protein kinase II contributes to activity-dependent filopodia growth and spine formation (2003) J. Neurosci, 23, pp. 10645-10649. , 14627649
  • Jovanovic, J.N., Sihra, T.S., Nairn, A.C., Hemmings, H.C., Greengard, P., Czernik, A.J., Opposing changes in phosphorylation of specific sites in synapsin I during Ca2+-dependent glutamate release in isolated nerve terminals (2001) J. Neurosci, 21, pp. 7944-7953. , 11588168
  • Kamata, A., Takeuchi, Y., Fukunaga, K., Identification of the isoforms of Ca2+/calmodulin-dependent protein kinase II and expression of brain-derived neurotrophic factor mRNAs in the substantia nigra (2006) J. Neurochem, 96, pp. 195-203. , 16277604
  • Kim, S., Kaang, B.-K., Epigenetic regulation and chromatin remodeling in learning and memory (2017) Exp. Mol. Med, 49 (e281). , 28082740
  • Lamprecht, R., The actin cytoskeleton in memory formation (2014) Prog. Neurobiol, 117, pp. 1-19. , 24530292
  • Lee, S.J.R., Escobedo-Lozoya, Y., Szatmari, E.M., Yasuda, R., Activation of CaMKII in single dendritic spines during long-term potentiation (2009) Nature, 458, pp. 299-304. , 19295602
  • Li, Q., Rothkegel, M., Xiao, Z.C., Abraham, W.C., Korte, M., Sajikumar, S., Making synapses strong: metaplasticity prolongs associativity of long-term memory by switching synaptic tag mechanisms (2012) Cereb. Cortex, 24, pp. 353-363. , 23048020
  • Lin, Y.-C., Redmond, L., CaMKIIβ binding to stable F-actin in vivo regulates F-actin filament stability (2008) Proc. Natl. Acad. Sci. U.S.A, 105, pp. 15791-15796. , 18840684
  • Lisman, J., Schulman, H., Cline, H., The molecular basis of CaMKII function in synaptic and behavioural memory (2002) Nat. Rev. Neurosci, 3, pp. 175-190. , 11994750
  • Lisman, J., Yasuda, R., Raghavachari, S., Mechanisms of CaMKII action in long-term potentiation (2012) Nat. Rev. Neurosci, 13, pp. 169-182. , 22334212
  • Liu, X., Jones, E.G., Alpha isoform of calcium-calmodulin dependent protein kinase II (CAM II kinase-alpha) restricted to excitatory synapses in the CA1 region of rat hippocampus (1997) Neuroreport, 8, pp. 1475-1479. , 9172157
  • Liu, X.B., Jones, E.G., Localization of alpha type II calcium calmodulin-dependent protein kinase at glutamatergic but not gamma-aminobutyric acid (GABAergic) synapses in thalamus and cerebral cortex (1996) Proc. Natl. Acad. Sci. U.S.A, 93, pp. 7332-7336. , 8692993
  • Liu, X.-B., Murray, K.D., Neuronal excitability and calcium/calmodulin-dependent protein kinase type II: location, location, location (2012) Epilepsia, pp. 45-52. , 22612808, 53(Sul. 1
  • Lu, F.-M., Hawkins, R.D., Presynaptic and postsynaptic Ca2+ and CamKII contribute to long-term potentiation at synapses between individual CA3 neurons (2006) Proc. Natl. Acad. Sci. U.S.A, 103, pp. 4264-4269. , 16537519
  • Lucchesi, W., Mizuno, K., Giese, K.P., Novel insights into CaMKII function and regulation during memory formation (2011) Brain Res. Bull, 85, pp. 2-8. , 21070840
  • Ma, H., Groth, R.D., Cohen, S.M., Emery, J.F., Li, B.-X., Hoedt, E., γCaMKII shuttles Ca2+/CaM to the nucleus to trigger CREB phosphorylation and gene expression (2014) Cell, 159, pp. 281-294. , 25303525
  • Malik, Z.A., Stein, I.S., Navedo, M.F., Hell, J.W., Mission CaMKIIγ: shuttle calmodulin from membrane to nucleus (2014) Cell, 159, pp. 235-237. , 25303520
  • Mayer, P., Möhlig, M., Idlibe, D., Pfeiffer, A., Novel and uncommon isoforms of the calcium sensing enzyme calcium/calmodulin dependent protein kinase II in heart tissue (1995) Basic Res. Cardiol, 90, pp. 372-379. , 8585858
  • Mayer, P., Möhlig, M., Schatz, H., Pfeiffer, A., New isoforms of multifunctional calcium/calmodulin-dependent protein kinase II (1993) FEBS Lett, 333, pp. 315-318
  • Mayford, M., Baranes, D., Podsypanina, K., Kandel, E.R., The 3′-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites (1996) Proc. Natl. Acad. Sci. U.S.A, 93, pp. 13250-13255
  • 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, pp. 507-519. , 12408852
  • Moncada, D., Ballarini, F., Martinez, M.C., Frey, J.U., Viola, H., Identification of transmitter systems and learning tag molecules involved in behavioral tagging during memory formation (2011) Proc. Natl. Acad. Sci. U.S.A, 108, pp. 12931-12936. , 21768371
  • Mori, Y., Imaizumi, K., Katayama, T., Yoneda, T., Tohyama, M., Two cis-acting elements in the 3′ untranslated region of alpha-CaMKII regulate its dendritic targeting (2000) Nat. Neurosci, 3, pp. 1079-1084. , 11036263
  • Morris, R.G.M., NMDA receptors and memory encoding (2013) Neuropharmacology, 74, pp. 32-40. , 23628345
  • Murakoshi, H., Shin, M.E., Parra-Bueno, P., Szatmari, E.M., Shibata, A.C.E., Yasuda, R., Kinetics of Endogenous CaMKII required for synaptic plasticity revealed by optogenetic kinase inhibitor (2017) Neuron, 94 (690). , 28472663
  • Néant-Fery, M., Pérès, E., Nasrallah, C., Kessner, M., Gribaudo, S., Greer, C., A role for dendritic translation of CaMKIIα mRNA in olfactory plasticity (2012) PLoS One, 7 (e40133). , 22768241
  • Ninan, I., Arancio, O., Presynaptic CaMKII is necessary for synaptic plasticity in cultured hippocampal neurons (2004) Neuron, 42, pp. 129-141. , 15066270
  • Ojuka, E.O., Goyaram, V., Smith, J.A.H., The role of CaMKII in regulating GLUT4 expression in skeletal muscle (2012) Am. J. Physiol. Endocrinol. Metab, 303, pp. E322-E331. , 22496345
  • Okamoto, K.-I., Narayanan, R., Lee, S.H., Murata, K., Hayashi, Y., The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure (2007) Proc. Natl. Acad. Sci. U.S.A, 104, pp. 6418-6423. , 17404223
  • Okuno, H., Akashi, K., Ishii, Y., Yagishita-Kyo, N., Suzuki, K., Nonaka, M., Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ (2012) Cell, 149, pp. 886-898. , 22579289
  • O’Leary, H., Lasda, E., Bayer, K.U., CaMKIIβ association with the actin cytoskeleton is regulated by alternative splicing (2006) Mol. Biol. Cell, 17, pp. 4656-4665. , 16928958
  • Redondo, R.L., Okuno, H., Spooner, P.A., Frenguelli, B.G., Bito, H., Morris, R.G.M., Synaptic tagging and capture: differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation (2010) J. Neurosci, 30, pp. 4981-4989. , 20371818
  • Reul, J.M.H.M., Making memories of stressful events: a journey along epigenetic, gene transcription, and signaling pathways (2014) Front. Psychiatry, 5 (5). , 24478733
  • Romano, A., NF-kB transcription factor: a model for the study of transcription regulation in memory consolidation, reconsolidation and extinction (2012) Transcription Factors CREB and NF-κB: Involvement in Synaptic Plasticity and Memory Formation, pp. 97-112. , Albensi B.C., (ed), Sharjah, Bentham Science Publishers
  • Rossetti, T., Banerjee, S., Kim, C., Leubner, M., Lamar, C., Gupta, P., Memory erasure experiments indicate a critical role of CaMKII in memory storage (2017) Neuron, 96, pp. 207-216. , 28957669.e2
  • Sajikumar, S., Navakkode, S., Frey, J.U., Identification of compartment- and process-specific molecules required for “synaptic tagging” during long-term potentiation and long-term depression in hippocampal CA1 (2007) J. Neurosci, 27, pp. 5068-5080. , 17494693
  • Sanabria, H., Swulius, M.T., Kolodziej, S.J., Liu, J., Waxham, M.N., {beta}CaMKII regulates actin assembly and structure (2009) J. Biol. Chem, 284, pp. 9770-9780. , 19208632
  • 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, pp. 821-834. , 23141539
  • Sanhueza, M., Lisman, J., The CaMKII/NMDAR complex as a molecular memory (2013) Mol. Brain, 6 (10). , 23410178
  • Schulman, H., Heist, K., Srinivasan, M., Decoding Ca2+ signals to the nucleus by multifunctional CaM kinase (1995) Prog. Brain Res, 105, pp. 95-104. , 7568901
  • Schworer, C.M., Rothblum, L.I., Thekkumkara, T.J., Singer, H.A., Identification of novel isoforms of the delta subunit of Ca2+/calmodulin-dependent protein kinase II. Differential expression in rat brain and aorta (1993) J. Biol. Chem, 268, pp. 14443-14449. , 8390994
  • Shema, R., Haramati, S., Ron, S., Hazvi, S., Chen, A., Sacktor, T.C., Enhancement of consolidated long-term memory by overexpression of protein kinase Mζ in the neocortex (2011) Science, 331, pp. 1207-1210. , 21385716
  • Shen, K., Meyer, T., Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation (1999) Science, 284, pp. 162-166. , 10102820
  • 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, pp. 593-606. , 9768845
  • Shioda, N., Sawai, M., Ishizuka, Y., Shirao, T., Fukunaga, K., Nuclear translocation of Calcium/Calmodulin-dependent Protein Kinase IIδ3 Promoted by Protein Phosphatase-1 Enhances Brain-derived Neurotrophic Factor Expression in Dopaminergic Neurons (2015) J. Biol. Chem, 290, pp. 21663-21675. , 26163515
  • Silva, A.J., Paylor, R., Wehner, J.M., Tonegawa, S., Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice (1992) Science, 257, pp. 206-211. , a
  • Silva, A.J., Rosahl, T.W., Chapman, P.F., Marowitz, Z., Friedman, E., Frankland, P.W., Impaired learning in mice with abnormal short-lived plasticity (1996) Curr. Biol, 6, pp. 1509-1518. , 8939606
  • Silva, A.J., Stevens, C.F., Tonegawa, S., Wang, Y., Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice (1992) Science, 257, pp. 201-206. , b, 1378648
  • Srinivasan, M., Edman, C.F., Schulman, H., Alternative splicing introduces a nuclear localization signal that targets multifunctional CaM kinase to the nucleus (1994) J. Cell Biol, 126, pp. 839-852
  • Szabó, E.C., Manguinhas, R., Fonseca, R., The interplay between neuronal activity and actin dynamics mimic the setting of an LTD synaptic tag (2016) Sci. Rep, 6 (33685). , 27650071
  • Takeuchi, Y., Yamamoto, H., Matsumoto, K., Kimura, T., Katsuragi, S., Miyakawa, T., Nuclear localization of the delta subunit of Ca2+/calmodulin-dependent protein kinase II in rat cerebellar granule cells (1999) J. Neurochem, 72, pp. 815-825. , 9930758
  • Tan, S.-E., Liang, K.-C., Spatial learning alters hippocampal calcium/calmodulin-dependent protein kinase II activity in rats (1996) Brain Res, 711, pp. 234-240. , 8680867
  • Tobimatsu, T., Fujisawa, H., Tissue-specific expression of four types of rat calmodulin-dependent protein kinase II mRNAs (1989) J. Biol. Chem, 264, pp. 17907-17912. , 2553697
  • Tombes, R.M., Faison, M.O., Turbeville, J.M., Organization and evolution of multifunctional Ca(2+)/CaM-dependent protein kinase genes (2003) Gene, 322, pp. 17-31. , 14644494
  • van Woerden, G.M., Hoebeek, F.E., Gao, Z., Nagaraja, R.Y., Hoogenraad, C.C., Kushner, S.A., betaCaMKII controls the direction of plasticity at parallel fiber-Purkinje cell synapses (2009) Nat. Neurosci, 12, pp. 823-825. , 19503086
  • Wang, H., Shimizu, E., Tang, Y.-P., Cho, M., Kyin, M., Zuo, W., Inducible protein knockout reveals temporal requirement of CaMKII reactivation for memory consolidation in the brain (2003) Proc. Natl. Acad. Sci. U.S.A, 100, pp. 4287-4292. , 12646704
  • Wang, Q., Yin, P., Yu, B., Zhao, Z., Richter-Levin, G., Yu, L., Down-regulation of dorsal striatal αCaMKII causes striatum-related cognitive and synaptic disorders (2017) Exp. Neurol, 298, pp. 112-121. , 28890075
  • Wang, Z.-W., Regulation of synaptic transmission by presynaptic CaMKII and BK channels (2008) Mol. Neurobiol, 38, pp. 153-166. , 18759010
  • Wu, X., McMurray, C.T., Calmodulin Kinase II Attenuation of Gene Transcription by Preventing cAMP Response Element-binding Protein (CREB) Dimerization and Binding of the CREB-binding Protein (2001) J. Biol. Chem, 276, pp. 1735-1741. , 11013247
  • Xiao, H.-S., Huang, Q.-H., Zhang, F.-X., Bao, L., Lu, Y.-J., Guo, C., 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, pp. 8360-8365. , 12060780
  • Yamagata, Y., Kobayashi, S., Umeda, T., Inoue, A., Sakagami, H., Fukaya, M., Kinase-dead knock-in mouse reveals an essential role of kinase activity of Ca2+/calmodulin-dependent protein kinase IIα in dendritic spine enlargement, long-term potentiation, and learning (2009) J. Neurosci, 29, pp. 7607-7618
  • Yamasaki, N., Maekawa, M., Kobayashi, K., Kajii, Y., Maeda, J., Soma, M., Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders (2008) Mol. Brain, 1 (6). , 18803808
  • Yasuda, M., Mayford, M.R., CaMKII activation in the entorhinal cortex disrupts previously encoded spatial memory (2006) Neuron, 50, pp. 309-318. , 16630840
  • Yin, P., Xu, H., Wang, Q., Wang, J., Yin, L., Xu, M., Overexpression of βCaMKII impairs behavioral flexibility and NMDAR-dependent long-term depression in the dentate gyrus (2017) Neuropharmacology, 116, pp. 270-287. , 27993520
  • Zalcman, G., Federman, N., Fiszbein, A., de la Fuente, V., Ameneiro, L., Schor, I., Sustained CaMKII delta gene expression is specifically required for long-lasting memories in mice (2018) Mol. Neurobiol, , 29948945, [Epub ahead of print]
  • Zhang, M., Shan, H., Gu, Z., Wang, D., Wang, T., Wang, Z., Increased expression of calcium/calmodulin-dependent protein kinase type II subunit delta after rat traumatic brain injury (2012) J. Mol. Neurosci, 46, pp. 631-643. , 22048920
  • Zhang, T., Brown, J.H., Role of Ca2+/calmodulin-dependent protein kinase II in cardiac hypertrophy and heart failure (2004) Cardiovasc. Res, 63, pp. 476-486. , 15276473
  • Zhang, T., Johnson, E.N., Gu, Y., Morissette, M.R., Sah, V.P., Gigena, M.S., The cardiac-specific nuclear delta(B) isoform of Ca2+/calmodulin-dependent protein kinase II induces hypertrophy and dilated cardiomyopathy associated with increased protein phosphatase 2A activity (2002) J. Biol. Chem, 277, pp. 1261-1267. , 11694533
  • Zhang, T., Kohlhaas, M., Backs, J., Mishra, S., Phillips, W., Dybkova, N., CaMKIIdelta isoforms differentially affect calcium handling but similarly regulate HDAC/MEF2 transcriptional responses (2007) J. Biol. Chem, 282, pp. 35078-35087. , 17923476
  • Zhang, T., Maier, L.S., Dalton, N.D., Miyamoto, S., Ross, J., Bers, D.M., The deltaC isoform of CaMKII is activated in cardiac hypertrophy and induces dilated cardiomyopathy and heart failure (2003) Circ. Res, 92, pp. 912-919. , 12676814

Citas:

---------- APA ----------
Zalcman, G., Federman, N. & Romano, A. (2018) . CaMKII isoforms in learning and memory: Localization and function. Frontiers in Molecular Neuroscience, 11.
http://dx.doi.org/10.3389/fnmol.2018.00445
---------- CHICAGO ----------
Zalcman, G., Federman, N., Romano, A. "CaMKII isoforms in learning and memory: Localization and function" . Frontiers in Molecular Neuroscience 11 (2018).
http://dx.doi.org/10.3389/fnmol.2018.00445
---------- MLA ----------
Zalcman, G., Federman, N., Romano, A. "CaMKII isoforms in learning and memory: Localization and function" . Frontiers in Molecular Neuroscience, vol. 11, 2018.
http://dx.doi.org/10.3389/fnmol.2018.00445
---------- VANCOUVER ----------
Zalcman, G., Federman, N., Romano, A. CaMKII isoforms in learning and memory: Localization and function. Front. Mol. Neurosci. 2018;11.
http://dx.doi.org/10.3389/fnmol.2018.00445