Translocation of CaMKII to dendritic microtubules supports the plasticity of local synapses

Lemieux, Mado; Labrecque, Simon; Tardif, Christian; Labrie-Dion, Étienne; Lebel, Estelle; Koninck, Paul De

doi:10.1083/jcb.201202058

Cited by 71 publications

(58 citation statements)

References 68 publications

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“…Hanson et al (1994) predicted that repetitive calcium pulses would lead to the recruitment of limited calmodulin to the holoenzyme, which would further stimulate autophosphorylation while De Koninck et al (1998) showed that the enzyme can decode the frequency of Ca 2+ spikes into distinct amounts of kinase activity. Hence, a calcium increase compartmentalized in an activated spine would lead to CaMKII activation specifically in that subcellular region (Lee et al 2009;Lemieux et al 2012). On the other hand, calcium increases happening through voltage-dependent calcium channels or endoplasmic reticulum release might convey a specific signal supporting the plasticity of neighboring synapses (Greer and Greenberg 2008;Wheeler et al 2008;Rose et al 2009).…”

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confidence: 99%

Long-term potentiation can be induced in the CA1 region of hippocampus in the absence of αCaMKII T286-autophosphorylation

2014

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a-calcium/calmodulin-dependent protein kinase (aCaMKII) T286-autophosphorylation provides a short-term molecular memory that was thought to be required for LTP and for learning and memory. However, it has been shown that learning can occur in aCaMKII-T286A mutant mice after a massed training protocol. This raises the question of whether there might be a form of LTP in these mice that can occur without T286 autophosphorylation. In this study, we confirmed that in CA1 pyramidal cells, LTP induced in acute hippocampal slices, after a recovery period in an interface chamber, is strictly dependent on postsynaptic aCaMKII autophosphorylation. However, we demonstrated that aCaMKII-autophosphorylation-independent plasticity can occur in the hippocampus but at the expense of synaptic specificity. This nonspecific LTP was observed in mutant and wild-type mice after a recovery period in a submersion chamber and was independent of NMDA receptors. Moreover, when slices prepared from mutant mice were preincubated during 2 h with rapamycin, high-frequency trains induced a synapse-specific LTP which was added to the nonspecific LTP. This specific LTP was related to an increase in the duration and the amplitude of NMDA receptor-mediated response induced by rapamycin.The formation of memories is believed to be achieved through strengthening of synaptic communication between two simultaneously active neurons, a phenomenon called long-term potentiation (LTP). For several years, numerous studies have sought to better understand the molecular mechanisms of synaptic plasticity and LTP, and in particular the role of calcium-calmodulin-dependent protein kinase II (CaMKII), one of the most important postsynaptic components in glutamatergic synapses. Indeed, CaMKII is both necessary and sufficient for LTP induction. The application of CaMKII inhibitors, such as KN-62 or KN-93, or genetic disruption of the CaMKII gene can block LTP (Malinow et al. 1989;Otmakhov et al. 1997;Hinds et al. 1998;Yamagata et al. 2009). Conversely, the injection or viral expression of a constitutively active form of CaMKII leads to the improvement of spatial memory (Poulsen et al. 2007), in enhancement of AMPAR-mediated synaptic transmission and occludes further induction of LTP (McGladeMcCulloh et al. 1993;Pettit et al. 1994;Lledo et al. 1995). This enhancement in AMPAR conductance has been proposed to occur through an increase in synaptic trafficking of GluA1 subunits, as well as phosphorylation of GluA1 at Ser831 (Shi et al. 1999;Hayashi et al. 2000;Broutman and Baudry 2001;Esteban et al. 2003;Oh et al. 2006). Besides its role in synaptic transmission, CaMKII is also involved in the structural plasticity of spines, and more specifically in activity-dependent spine growth following NMDAR activation (Okamoto et al. 2009;Pi et al. 2010). Moreover, it seems that CaMKII-dependent processes involved in hippocampal LTP in CA1 synapses are quite general since the kinase also affects in vivo plasticity in different brain regions (Wu and Cline 1998;Zou and Cline 1999). ...

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Long-term potentiation can be induced in the CA1 region of hippocampus in the absence of αCaMKII T286-autophosphorylation

2014

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“…This association and phosphorylation has even been proposed to be a means of directly encoding information on microtubules [33]. The only study of the functional consequences of the CaMKIIα/microtubule interaction [21] offered strong evidence that an interaction between CaMKIIα and dendritic microtubules increases the surface expression of AMPA receptors and spine remodelling. This study also showed that this translocation of CaMKIIα requires stable microtubules [21].…”

Section: Discussionmentioning

confidence: 99%

“…The only study of the functional consequences of the CaMKIIα/microtubule interaction [21] offered strong evidence that an interaction between CaMKIIα and dendritic microtubules increases the surface expression of AMPA receptors and spine remodelling. This study also showed that this translocation of CaMKIIα requires stable microtubules [21]. Although the intermediate mechanism is speculative, their result supports the model wherein activated CaMKIIα translocates to microtubules to ultimately potentiate synaptic strength.…”

Section: Discussionmentioning

confidence: 99%

“…A recent study showed that during KCl depolarization, CaMKIIα undergoes a rapid and sustained translocation to microtubules [21]. Since the microtubule translocation and self-aggregation of CaMKIIα can both be caused by depolarization, but are mutually exclusive behaviours, we sought to compare the time-course and localization of GFP-CaMKIIα during neuronal depolarization.…”

Section: Depletion Of P600 Interrupts the Cytoskeletal Localization Omentioning

confidence: 99%

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p600 stabilizes microtubules to prevent the aggregation of CaMKIIα during photoconductive stimulation

Belzil¹,

Ramos²,

Sanada³

et al. 2014

Cellular and Molecular Biology Letters

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“…Whereas this question requires further investigation, it is interesting to note that CaMKIIa is a major player in the synaptic development and plasticity of both excitatory and inhibitory synapses. Indeed, CaMKIIa plays an essential role in decoding Ca 2+ signals in excitatory neurons and modulates the synaptic remodeling and plasticity of these cells [40][41][42][43]. CaMKIIa is also involved in the remodeling and plasticity of inhibitory synapses via trafficking of different GABA A receptor subunits as well as gephyrin, the main scaffolding protein of inhibitory synapses [44][45][46][47].…”

Section: Discussionmentioning

confidence: 99%

CaMKIIα Expression Defines Two Functionally Distinct Populations of Granule Cells Involved in Different Types of Odor Behavior

Malvaut¹,

Gribaudo

Hardy³

et al. 2017

Current Biology

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International audienceGranule cells (GCs) in the olfactory bulb (OB) play an important role in odor information processing. Although they have been classified into various neurochemical subtypes, the functional roles of these subtypes remain unknown. We used in vivo two-photon Ca2+ imaging combined with cell-type-specific identification of GCs in the mouse OB to examine whether functionally distinct GC subtypes exist in the bulbar network. We showed that half of GCs express Ca2+/calmodulin-dependent protein kinase IIα (CaMKIIα+) and that these neurons are preferentially activated by olfactory stimulation. The higher activity of CaMKIIα+ neurons is due to the weaker inhibitory input that they receive compared to their CaMKIIα-immunonegative (CaMKIIα−) counterparts. In line with these functional data, immunohistochemical analyses showed that 75%–90% of GCs expressing the immediate early gene cFos are CaMKIIα+ in naive animals and in mice that have been exposed to a novel odor and go/no-go operant conditioning, or that have been subjected to long-term associative memory and spontaneous habituation/dishabituation odor discrimination tasks. On the other hand, a perceptual learning task resulted in increased activation of CaMKIIα− cells

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Translocation of CaMKII to dendritic microtubules supports the plasticity of local synapses

Abstract: Synaptic plasticity correlates with the local dendritic translocation of CaMKII in a Ca2+- and microtubule-dependent manner.

Cited by 71 publications

References 68 publications

Long-term potentiation can be induced in the CA1 region of hippocampus in the absence of αCaMKII T286-autophosphorylation

Long-term potentiation can be induced in the CA1 region of hippocampus in the absence of αCaMKII T286-autophosphorylation

p600 stabilizes microtubules to prevent the aggregation of CaMKIIα during photoconductive stimulation

CaMKIIα Expression Defines Two Functionally Distinct Populations of Granule Cells Involved in Different Types of Odor Behavior

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